Human Niche Construction

ISSN 0962-8436 volume 366 number 1566 pages 783–934 In this Issue Human niche construction Papers of a Theme issue ...

Author: Jeremy R. Kendal | Jamshid J. Tehrani | John Odling-Smee (Editors)

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ISSN 0962-8436

volume 366

number 1566

pages 783–934

In this Issue

Human niche construction Papers of a Theme issue compiled and edited by Jeremy R. Kendal, Jamshid J. Tehrani and John Odling-Smee

The world’s first science journal

27 March 2011

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Human niche construction Papers of a Theme issue compiled and edited by Jeremy R. Kendal, Jamshid J. Tehrani and John Odling-Smee

Contents

Preface 784

The entangled (and constructed) human bank E. Jablonka

Introduction Human niche construction in interdisciplinary focus J. Kendal, J. J. Tehrani and J. Odling-Smee

785

Articles Adaptation and niche construction in human prehistory: a case study from the southern Scandinavian Late Glacial F. Riede

793

From hominins to humans: how sapiens became behaviourally modern K. Sterelny

809

Runaway cultural niche construction L. Rendell, L. Fogarty and K. N. Laland

823

General patterns of niche construction and the management of ‘wild’ plant and animal resources by small-scale pre-industrial societies B. D. Smith

836

Foraging and farming as niche construction: stable and unstable adaptations P. Rowley-Conwy and R. Layton

849

Evolution of lactase persistence: an example of human niche construction P. Gerbault, A. Liebert, Y. Itan, A. Powell, M. Currat, J. Burger, D. M. Swallow and M. G. Thomas

863

Gene –culture coevolution and the nature of human sociality H. Gintis

878

Evolution of culture-dependent discriminate sociality: a gene – culture coevolutionary model Y. Ihara

889

The influence of social niche on cultural niche construction: modelling changes in belief about marriage form in Taiwan M. Lipatov, M. J. Brown and M. W. Feldman

901

Property and wealth inequality as cultural niche construction S. Shennan

918

Niche construction on Bali: the gods of the countryside J. S. Lansing and K. M. Fox

927

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Downloaded from rstb.royalsocietypublishing.org on January 9, 2012

Phil. Trans. R. Soc. B (2011) 366, 784 doi:10.1098/rstb.2010.0364

Preface

The entangled (and constructed) human bank All living organisms are active agents, altering through their activities the living conditions in which they and their descendants develop, act and are selected. The reciprocal feedback between organisms’ activities and their selective environment is known as niche construction, and a large body of observations and many models point to its ubiquity and evolutionary significance. Humans are probably the most creative niche constructors on the planet. Their constructions modify the abiotic environment that they inhabit and influence the evolution of the organisms with which they interact as well as their own evolution, including the evolution of traits that we identify as the hallmarks of humanness, such as language. The human niche has ecological, social and epistemic aspects, which make up what we call human culture. Human cultural evolution, the historical change in human culture, involves changes in the intergenerational transfer of ecological legacies, in the reconstruction of developmental conditions, in the transmission of behavioural and symbolic information and in the selective stabilization of practices and preferences. Human cultural evolution is therefore a special and extreme case of niche construction. It is different from other types of niche construction not just in scope but also because it involves deliberate and planned actions that are based on communally shared, virtual (imagined) realities that are stabilized by learning, pedagogy and social conventions. Because human niche construction is often future-oriented, and because it is stabilized by reasoning and by conventional beliefs, the potential range of constructed human niches is enormous. The actual diversification and sophistication of humanconstructed environments is a testimony to the special properties of human niche construction. As the papers in this issue show, there are several overlapping reasons for the usefulness of the niche construction approach to human history and evolution. Firstly, it does justice to the complexity inherent in the misleadingly simple term ‘human environment’, with its interacting ecological, social and symbolic components. Secondly, it stresses the active role of humans in the construction of their world and their own evolution, highlighting the intricate relations between different aspects of human

existence, for example between social practices and belief systems, which can change on different time scales, can influence and transform one another and can lead to the complex patterns of cultural change that have been documented by sociologists and anthropologists, but have not been captured by conventional evolutionary approaches. Thirdly, ongoing, systematic, niche construction can lead to genetic changes in the niche-constructing species (e.g. human) or the niche-constructed species (e.g. domesticates such as the dog or wheat). Such coevolution of genes and culture that affects the niche-constructing cultural capacities themselves can lead to an increase in the evolvability of culture, something that may explain human-specific cognitive and affective traits. Fourthly, the niche-construction approach provides a unifying theoretical framework for scientists from disciplines as different as ecology, population genetics, archaeology, anthropology, sociology and economics, and thus encourages collaboration among them. For example, ecologists and palaeontologists can document changes in landscapes and species distribution, and correlate them with the changes in human practices documented by archaeologists or anthropologists. Similarly, genetic data contributed by population geneticists can be put together with data gathered by archaeologists and ecologists. Comparative methods and formal models based on assumptions that incorporate niche construction can be used to analyse and evaluate different hypotheses about the reciprocal interactions between human activities and the selective environments. The authors who contribute to this issue show the productiveness and power of the niche-construction approach, and demonstrate how this framework can generate a real dialogue between the different disciplines studying the culture and evolution of our species.

Eva Jablonka*

October 2010

The Cohn Institute for the History and Philosophy of Science and Ideas, Tel-Aviv University, Tel Aviv 69978, Israel *[email protected]

One contribution of 13 to a Theme Issue ‘Human niche construction’.

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This journal is q 2011 The Royal Society

Phil. Trans. R. Soc. B (2011) 366, 785–792 doi:10.1098/rstb.2010.0306

Introduction

Human niche construction in interdisciplinary focus Jeremy Kendal1,*, Jamshid J. Tehrani1 and John Odling-Smee2 1

Centre for the Coevolution of Biology and Culture, Department of Anthropology, University of Durham, South Road, Durham DH1 3LE, UK 2 School of Anthropology, University of Oxford, 51/53 Banbury Road, Oxford OX2 6PE, UK

Niche construction is an endogenous causal process in evolution, reciprocal to the causal process of natural selection. It works by adding ecological inheritance, comprising the inheritance of natural selection pressures previously modified by niche construction, to genetic inheritance in evolution. Human niche construction modifies selection pressures in environments in ways that affect both human evolution, and the evolution of other species. Human ecological inheritance is exceptionally potent because it includes the social transmission and inheritance of cultural knowledge, and material culture. Human genetic inheritance in combination with human cultural inheritance thus provides a basis for gene – culture coevolution, and multivariate dynamics in cultural evolution. Niche construction theory potentially integrates the biological and social aspects of the human sciences. We elaborate on these processes, and provide brief introductions to each of the papers published in this theme issue. Keywords: niche construction; gene – culture coevolution; cultural evolution; human evolution

1. INTRODUCTION Niche-construction theory (NCT) originated as a branch of evolutionary biology that emphasizes the capacity of organisms to modify their environment and thereby influence their own and other species’ evolution [1]. The defining characteristic of niche construction is not the modification of environments per se, but rather organism-induced changes in selection pressures in environments [1]. The effects of niche construction have been documented across a wide range of species including animals manufacturing nests, burrows and webs, and plants modifying nutrient cycles. The papers presented in this special issue explore the phenomenon in Homo sapiens, for whom endogenous causes of evolutionary dynamics are impossible to ignore. NCT differs from standard evolutionary theory (SET) in recognizing that the evolution of organisms is co-directed by both natural selection and niche construction. While genetic variation is subject to natural selection through differential survival and reproductive success, the selective environments themselves are partly determined by modifications made by nicheconstructing organisms. Hence NCT recognizes natural selection and niche construction as reciprocal causal processes in evolution, and treats the adaptations of organisms as products of both processes [2].

Evolution entails networks of causation and feedback in which previously selected organisms drive environmental changes, and organism-modified environments subsequently select for changes in organisms. NCT provides both a philosophical shift in the way we view and understand evolutionary processes as well as a testable scientific theory. While the effects of niche construction on the evolutionary process have often been neglected in the past, it is also important to note that many aspects of NCT are already incorporated in standard theories of evolutionary biology, ecology, developmental biology and the human sciences. However, rather than aiming just to relabel or reclassify established theories such as gene– culture coevolution or ecosystem engineering, NCT is put to better use when formulating new hypotheses, or building a more general evolutionary framework within which other theories can be subsumed. NCT provides mechanisms by which currently disconnected bodies of theory, such as evolutionary and developmental biology (‘evo-devo’) [1,3,4], or human cultural evolution and structuration theory ([5], see below) can be united [6]. Here, we review the fundamental principles of contemporary NCT, initially in the context of biological evolution, before showing how the theory incorporates cultural evolutionary processes, and how it provides a framework for consilience between the natural and the social sciences [7]. Where appropriate, we give short summaries of each of the contributing papers in this theme issue.

* Author for correspondence ([email protected]). One contribution of 13 to a Theme Issue ‘Human niche construction’.

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Introduction. Human niche construction

2. FUNDAMENTAL PRINCIPLES OF NICHE CONSTRUCTION An early advocate of the niche construction perspective, Lewontin [8], neatly summarized the differences between standard evolutionary theory and NCT in two pairs of coupled differential equations. His first pair (equations 2.1a,b) summarizes SET: dO ¼ f ðO; EÞ dt

ð2:1aÞ

and dE ¼ gðEÞ: dt

ð2:1bÞ

In equation (2.1a), evolutionary change in organisms, dO/dt, depends on both organisms’ states, O, and environmental states, E. In equation (2.1b), environmental change, dE/dt, depends exclusively on environmental states. In general, organisms are not treated as the cause of any evolutionarily significant changes in their environments, with the exception of cases such as frequency dependent selection, habitat selection, maternal inheritance and coevolution. Instead adaptive evolutionary change is assumed to be governed exclusively by a single ‘causal arrow’, natural selection. However, SET underestimates the significance of the fact that, to stay alive, organisms must be active as well as reactive relative to their environments. Organisms must gain resources from their external environments by genetically informed, or in animals, possibly brain informed, fuel consuming, nonrandom work [3]. They must perturb specific components of their environments, often at locations chosen by the organisms themselves, and they must excrete detritus to their environments throughout their lives [1]. Organisms are, therefore, compelled to modify some natural selection pressures in their environments by the accumulating consequences of their activities. Lewontin captured this point by his second pair (equations 2.2a,b) of equations that, in effect, summarize NCT: dO ¼ f ðO; EÞ dt

ð2:2aÞ

and dE ¼ gðO; EÞ: dt

ð2:2bÞ

In equation (2.2a) change in organisms, dO/dt, is again assumed to depend on both organisms’ states and environmental states, but in equation (2.2b) environmental change, dE/dt, is now assumed to depend on both environment states, and the niche-constructing activities of organisms. Therefore, equation (2.2b) introduces the second ‘causal arrow’ in evolution that Odling-Smee [9] called niche construction. The philosopher Godfrey-Smith [10] highlighted the same distinction between SET and NCT by describing SET as an ‘externalist’ theory of evolution. SET is externalist because it seeks to explain the internal properties of organisms, their adaptations, exclusively in terms of properties of their external Phil. Trans. R. Soc. B (2011)

environments, natural selection pressures. SET is also fully consistent with the traditional view expounded by Mayr [11], who regarded natural selection as the ultimate cause of phenotypic characters [12]. It is a view that devalues so-called proximate causes, including developmental processes such as learning, and human cultural processes in evolutionary biology [13,14]. In SET, niche-construction effects caused by developmental or proximate processes can be regarded as the expression of phenotypic plasticity [15], or sometimes as extended phenotypes [16], but ultimately they still have to be explained by prior natural selection [17]. For many purposes, SET is sufficient, but it is insufficient when genetic selective environments are modified as a function of phenotypic variation derived from so-called proximate processes such as learning. For example, human cultural variation, depending largely on differential social transmission of information through social learning, may result in cultural nicheconstructing practices that modify the natural selection of some human genes. As the selected genes may also influence human cultural practices, the assignment of ‘causation’ becomes complex. NCT replaces SET’s dichotomous proximate and ultimate distinction with ‘reciprocal causation’. Adaptations of organisms depend on natural selection that is modified by niche construction, and niche construction that is selected by natural selection [1,2]. In this light, niche construction is a mechanism of endogenous causation, reciprocal to natural selection in the evolutionary process. NCT asserts that, as a consequence of ancestral niche construction, offspring inherit not only genes, but an ecological inheritance, in the form of modified local selective environments relative to genetic fitness. Overall, each offspring actually inherits an initial organism – environment relationship, or ‘niche’, from its ancestors such that: NðtÞ ¼ hðO; EÞ;

ð2:3Þ

where N(t) represents the niche of a population of organisms O at time t in an environment E. The dynamics of N(t) are driven by the interaction of both population-modifying natural selection pressures in E, and by the environment-modifying niche-constructing activities of populations, O [3]. In effect, this innovation replaces an ‘externalist’ theory by an ‘interactionist’ theory of evolution [10]. A niche is a neutral explanatory reference device. It can capture reciprocal causation in evolution without imposing any bias either in favour of natural selection and against niche construction, or vice versa [3]. Conceptually, it permits differential natural selection to be treated no longer as a function of external environments, but, where appropriate, as a function of organism – environment interactions. In humans, much niche construction is influenced by socially transmitted behaviour This observation provoked Laland et al. [18] to propose a triple inheritance evolutionary framework, delineating genetic, cultural and ecological inheritance systems. Either genetically or culturally influenced behaviours can modify an environmental resource that subsequently

Introduction. Human niche construction contributes to a human ecological inheritance across generations. In Laland et al.’s models the inherited environmental resource was originally assumed to be a material or energetic resource previously modified by cultural niche construction. The inherited resource might then affect either a human cultural process without having any effect on human genetics, or it could affect the natural selection of human genes including, sometimes, the natural selection of genes that subsequently influenced the expression of human cultural processes [18 – 20]. Riede [21] in this issue argues that this triple inheritance system (genes, culture and ecology) can provide an effective framework to study archaeological data, and he reviews a variety of cases where archaeology provides signatures of human niche construction activity within this system. A problem with using the archaeological record is that it can be difficult to distinguish causal relationships between nicheconstructing traditions and traditions selected as consequences. To overcome this, Riede advocates the use of phylogenetic comparative methods used to study correlated evolution in biology. He demonstrates the potential of this approach in a case study investigating the causal relationships between traditions for reindeer economies and dog use in Late Palaeolithic populations of southern Scandinavia, using a cultural phylogeny derived from artefact traditions. Recently, Odling-Smee [3,22] suggested that Laland et al.’s triple inheritance system is unnecessarily complicated and constraining. Instead, the original cultural and ecological inheritance systems can be collapsed into a single ecological inheritance system consisting of informatic as well as physical material and energy resources (figure 1). This simplification is consistent with the idea that an individual can inherit both a social and a physical niche that can include culturally transmitted knowledge and behaviours, as well as material culture, providing both culturally modified sources of information and culturally modified physical resources, in an individual’s developmental environment [23,24]. Semantic information in an individual’s inherited niche might take the form of a behaviour, demonstrated by peers or elders, acquired through social learning, such as subsistence practices or social norms. Inherited physical resources could refer to aspects of material culture, for example, nutritional resources or tools, created through hunter – gathering activity or farming. Many inherited niches obviously consist of both informatic and physical resources: for instance, farmed livestock and crops are not just nutritional resources, but also a source of public information concerning subsistence practices. While the proposed two-track human inheritance system is consistent with Laland et al.’s [18] original triple inheritance model, it is founded on general principles that should apply to all organisms. Informally, evolution based on the transmission of adaptive semantic information or ‘know how’ requires energy and material resources to pay for its physical acquisition, storage (whether it be in RNA, DNA or neurons etc.), use and transmission. Thus, there is a natural delineation between the ecological inheritance Phil. Trans. R. Soc. B (2011)

J. Kendal et al. 787

natural selection time

niche construction

ecological inheritance

semantic information* and physical resources**

genetic inheritance

natural selection

niche construction Figure 1. A schematic diagram of NCT. *Includes cultural knowledge; ** includes material culture.

of informatic and energetic/physical resources. The delineation assumes a working definition of semantic information to be ‘anything that reduces uncertainty about selective environments, relative to the fitness interests of organisms’ [3, p. 184]. In addition, the inherited ecological niche can include epigenetic informatic and physical resources that lie internal to the organism, such as the epigenetic inheritance of DNA methylation patterns or the cytoplasmic inheritance of nutritional resources [14,25]. These ‘evo-devo’ considerations at the cellular level are beyond the scope of this theme issue. Systematic changes in developmental environments can also result in systematic changes to the phenotypic expression of developing organisms [26]. For example, the construction of a developmental niche may modify the shape of the relevant norm of reaction by reducing the range of developmental environments to which juveniles are exposed [2,6]. Animal burrows and nests typically buffer variation in environmental variables such as temperature and humidity, while human habitation and clothing provide similar roles. Constructed human social environments may also affect behavioural development. For instance, activities such as play and teaching can provide scaffolding for learning [27]. Sterelney [28] in this issue argues that the construction of developmental niche has been critical for the evolution of behavioural modernity in humans. In particular, he asserts that in the context of demographic expansion in the Upper Palaeolithic, the construction of structured learning environments, which result in apprentice learning, allows high fidelity cultural transmission of skill sets across generations, resulting in the behaviourally modern cultures.

3. EVOLUTIONARY CONSEQUENCES OF NICHE CONSTRUCTION There has been considerable use of mathematical models to examine the evolutionary consequences of niche construction. These studies are often based on

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a two-locus population genetic framework, where a genetic (or cultural) trait at one locus affects the selective environment for recipient genetic (or cultural) traits at the second locus [1,18,29 – 34]. The research has revealed interesting evolutionary dynamics such as momentum effects (populations continuing to evolve in the same direction after selection has stopped or reversed), time lags and inertia in response to selection, and sudden catastrophic responses to selection [6,19,29,30,35,36]. The findings have also been consistent with quantitative genetic analysis of indirect genetic effects and maternal inheritance [37– 40]. Cultural niche construction can affect either genetic or cultural evolutionary dynamics (or both), depending in part on the relative intensity of selection. Theory suggests that human gene–culture coevolution will typically occur if a genetic selective environment remains stable across sufficient generations for natural selection to act on human genetic variation [1]. Human evolution may be unique insofar as our cultural capacities and adaptive cultural niche-constructing activities reinforce and amplify each other [1,19,41,42]. Thus, the capacities for social, technical or cultural intelligence, such as language and cooperation, have apparently coevolved with the cumulative cultural evolution of technologies and social conventions that these capacities afford [43–45]. In the current issue Rendell et al. [46] use a cellular automaton model to explore local and global spatial effects of cultural niche construction on gene – culture coevolutionary dynamics. Similar to runaway sexual selection, they explore coevolution through ‘hitchhiking’ between cultural transmission of a behaviour (equivalent to the mate preference) that modifies the local selective environment of a genetic trait (equivalent to the preferred trait), even when there is an inherent cost associated with either the cultural trait or the genetic trait. They also examine the unique spatial influence on the evolution, through secondary hitchhiking, of a genetic trait that affects the capacity for cultural niche construction, but bears an inherent cost. The findings show the potential importance of cultural niche construction influencing, for example, genetic evolution of disease resistance and hominid brain size. Gene – culture coevolutionary dynamics are likely to have been particularly important in recent human evolution by influencing processes such as global dispersal and migration, language evolution, behavioural modernity and sociality, the advent of agriculture, and the evolution of human and domesticate diseases [20,47,48]. This is consistent with evidence for recent and rapid genetic selection, affecting characteristics including skin pigmentation, body shape, dentition, brain function, metabolic efficiency and disease resistance [20,47]. The impact of cultural niche construction and gene – culture coevolutionary dynamics on both human technological and social evolution are considered in the current theme issue. One of the most powerful examples of such changes is in humans’ exploitation and modification of natural resources. In this issue, Smith [49] draws on a wealth of fascinating examples, largely from North America, to develop a classification of niche-constructing Phil. Trans. R. Soc. B (2011)

activities, used by small-scale human societies, to produce food and raw material resources from wild flora and fauna. He highlights how the scheme distinguishes particular characteristics of wild taxa that make them likely targets for niche construction, as well as the proactive impact that humans have had on their own subsequent resource selection as a function of yields. Rowley-Conwy & Layton [50] in this issue contrast the stability of constructed niches by hunter – gatherers with constructed niches during the advent of agriculture. Considering a wide variety of plant manipulation and hunting activity, they show how hunter – gatherers can proactively alter both the ecological stability and evolutionary dynamics of the affected species. The authors examine the role of niche construction in the development and geographical expansion of both cereal and livestock agriculture, and highlight the feedback effects of population expansion on niche instability. Gerbault et al. [51] in this issue review the current understanding of perhaps the most well-cited case of gene – culture coevolution, that of lactase persistence and dairy farming. Their paper takes an interdisciplinary approach, considering new genetic data, archaeological evidence and simulation modelling to explore how this coevolutionary process took place. Focusing on the European Neolithic transition, including the spread of animal domestication and uptake of dairy farming, Gerbault et al. synthesize these data to give a contemporary explanation for the observed distribution of lactase persistence, highlighting the role of both demography and niche construction. The role of gene – culture coevolution on the evolution of human sociality is explored in this issue by Gintis [52]. This paper provides a formal argument that culture is not a by-product of genetic evolution, but rather that culturally constituted aspects of the social environment have driven the genetic evolution of predispositions for cognitive features such as prosocial emotions and moral cognition. The paper draws on both theoretical and experimental literature to support the case for the impact of gene– culture coevolution on, for instance, the internalization of norms, altruism and character virtues. The theme of human sociality is continued in this issue by Ihara [53], who develops a mathematical model to examine how culture-dependent discriminate sociality could have evolved by gene–culture coevolution. Using the scenario of a Hawk–Dove game to elicit resource competition, Ihara shows how a culturally transmitted trait can alter the selective environment to favour the genetic evolution of culture-dependent discriminators that exercise either in-group favouritism or prestige bias as a function of the cultural trait distribution. Ramifications for the evolution of discriminate sociality include the intriguing possibility that the evolution of this capacity in Homo sapiens, but not Neanderthals, contributed to their contrasting fates during the Middle to Upper Palaeolithic transition. Ihara notes that his model is also consistent with a cultural practice influencing the cultural, rather than genetic, evolution of discriminate sociality. In general, it is probably more common for cultural niche construction to result in a cultural, rather than a genetic

Introduction. Human niche construction response. Feasibly, trans-generational cultural niche construction can modify environments in ways that favour ever-more culture, causing cultural niche construction to become ever-more powerful [1,18,23,43,54]. This process may have led to the accumulation of complex social norms and complex cultural knowledge in behaviourally modern humans. Fast cultural responses to a culturally modified niche can also render genetic responses unnecessary [19]. For example, human-induced pollution may provoke new technology to remove environmental contaminants, thus counteracting the change in the genetic selective environments for species across relevant ecosystems. Here, the initial detrimental activity could be due to ‘inceptive’ niche construction, while the cultural response is likely to depend on ‘counteractive’ niche construction. Similarly, drug treatments to prevent diseases may relax genetic selection for disease resistance or susceptibility. For instance, Boni & Feldman [55] develop a mathematical model to examine how antibiotic use, favouring selection of resistant bacterial strains, can result in cultural selection for the avoidance of antibiotic use. This example is also notable as a case of interspecific niche construction, as the cultural and genetic evolution of antibiotic use and bacterial strains, respectively, modify the selective environments of one another. NCT may be particularly relevant to the dynamics of cultural traits because the theory can incorporate the effects of cultural backgrounds, or environments, as components of constructed niches, affecting selection between cultural variants [56]. This point is illustrated by theoretical studies of fertility control and the demographic transition. Ihara & Feldman [31] examined the effects of a preference for a high or low level of education on the evolution of small family size. They assumed that the average level of education can affect the degree to which traits are transmitted obliquely rather than vertically, for example, from teachers rather than from parents, to pupils. They found that a preference for small family size can evolve if individuals with few offspring are more likely to transmit their fertility preference to the offspring generation than are individuals with a high number of offspring. This study revealed the classic niche-construction characteristic of a time-lag between the increase of the average level of education and a subsequent decline in fertility: a pattern that is consistent with, and may partially explain, a typical demographic transition. In a related study, Borenstein et al. [34] developed a metapopulation cultural nicheconstruction model where the frequency of a trait, such as the preference for a high level of education, affects the construction of a social interaction network, through which other cultural traits may percolate. They found that local between-population cultural niche construction could account for the spread of reduced fertility preference across countries occurring at ever-lower levels of development [57]. Lipatov et al. [58] in this issue distinguish between a social niche, referring to the structure of expected social roles, and a cultural niche, referring to a set of socially transmitted symbolic or meaningful ideas. Drawing on rich ethnographic data relating to a shift Phil. Trans. R. Soc. B (2011)


from uxorilocal to virilocal marriage practices in early twentieth century Tawain, they develop a mathematical model to explore the interaction between social structure and cultural ideas. Lipatov et al. show how a disjuncture between practice and belief can be affected by changes in the economy, specifically the proportion of the population wealthy enough to pay the observed brideprice in the virilocal system. Shennan [59] in this issue chooses to focus on the inheritance of material wealth, such as property, as a constructed niche or resource afforded by private property rights that develop with agriculturalist and pastoralist societies. Shennan explores the influence of this niche on variation and stratification of reproductive strategies, and in addition, uses McNamara & Houston’s [60] model for non-genetic inheritance of phenotypic quality to bring insight to the importance of inter-generational transfers of land wealth on long-term reproductive success.

4. INTEGRATING HUMAN, BIOLOGICAL AND SOCIAL SCIENCES Human and social scientists have been reticent to make use of evolutionary theory in the past for several reasons. One is that human scientists are predominantly interested in human behaviour and culture, rather than genes, and as a consequence they have little use for a standard theory of evolution that is exclusively driven by natural selection acting on genetic variation. A second reason is that an adaptationist account of behaviour derived from SET, for example in evolutionary psychology, is regarded somewhere between oversimplification and misrepresentation [61]. NCT addresses both these issues by accounting for the proactive role of human development and cultural processes in human evolution through the modification and ecological inheritance of selective environments. The inherited selective environment can pertain to any form of ecologically inherited semantic information, including culturally inherited information, as well as physical environments. This enables human scientists to explore human phenotypic variation from the perspective of genetic, ontogenetic and cultural processes operating at distinct, but richly interconnected levels [62], as exemplified in many of the papers in the current issue. Another source of reticence is the perception among social scientists that evolutionary theory cannot account for cultural diversity, but only for panhuman traits. It is, therefore, unable to offer social scientists any insights into the phenomena that primarily interest them. However, NCT provides a framework for the quantitative examination of cultural diversity through modification of cultural and social selective environments to affect local cultural histories and promote additional cultural diversity, where it is unnecessary to consider genetic fitness consequences [63]. Furthermore, it is now well established that a quantitative evolutionary model can be of great utility to study cultural diversity [56,64 – 66]. There are also some parallels between the evolutionary framework offered by NCT and some recent

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developments in social theory that have tried to transcend the classic dichotomy between structure (the rules and institutions of societies) and agency (the intentions, motivations and performances of individuals). So-called ‘structuration theory’ [5] is based on a similar premise to niche construction in that it emphasizes that social structures are both the context and the consequences of individual actions. Cultural meanings, moral orders and the distribution of economic and political power constrain agency and inform its goals, but they also depend on it for their reproduction. Humans’ ability to assess the effectiveness of their behaviours (‘reflexive monitoring’) allows them to manipulate and occasionally even to transform structure, which can have intended and unintended consequences for their and others’ future behaviour. The importance of evaluative and purposeful agency has clear implications for our understanding of human niche construction, as Lansing & Fox [67] discuss in their contribution to this issue. They describe how the engineered landscape of Balinese rice terraces is governed principally by local farming associations responding to the ecologically inherited conflicting interests of water availability and pest control. The development of rice cults has played a crucial role in coordinating farmers’ behaviours, but has also generated a wide range of new cultural representations and paradigms, including the agricultural calendar, cosmological system and religious consciousness.

5. CONCLUSION We can gain a richer understanding of evolutionary processes by accounting explicitly for phenotypic modification of selective environments that can result in the ecological inheritance of semantic and physical resources (figure 1). Thus, niche construction provides an endogenous causal role in evolution that is reciprocal to that of selection. In recent human evolution, the most potent human contributions to human ecological inheritance have probably occurred through cultural inheritance. If so, that requires the investigation of human evolution in the context of a theory of gene – culture coevolution that explicitly includes cultural niche construction. One potential advantage of combining NCT with gene–culture coevolutionary theory is that it should make gene–culture coevolutionary models more empirically tractable by including NCT’s mechanisms of niche construction and ecological inheritance, both of which are open to investigation [1]. Niche construction provides a powerful framework for bringing together different perspectives on the role of culture as a selective force in human evolution that have developed in recent decades [68]. When framed in terms of SET, these approaches often seem to be in conflict with one another—for example, over the question of the extent to which culture is ‘adaptive’ [69]. In NCT, these differences largely disappear. Rather than focusing on the adaptiveness of cultural behaviours relative to an external environment, NCT recognizes that culture is a crucial part of our ‘ecological inheritance’. Thus, over the last Phil. Trans. R. Soc. B (2011)

100 000 years or so, humans have become increasingly reliant on physical and semantic resources that have been shaped by the cultural activities of preceding generations—from domesticated animals and tool-making to writing, the built environment and even religious cosmologies. Such inventions have in various ways both depended on and then subsequently shaped the evolution of genetic and other cultural traits. Niche construction provides a unique paradigm for studying these relationships that explicitly recognizes the reciprocal influences of cultural evolution, cultural evolvability and gene – cultural evolution on one another. Empirical investigations will not be easy, however. The eco-evolutionary feedbacks generated by cultural niche construction are typically complicated, and they are likely to demand multi-disciplinary approaches [70]. At present, different disciplines, ranging from population geneticists, ecologists and molecular biologists to anthropologists, archaeologists and economists, contribute different datasets and different theoretical interpretations to different arcs of these feedback cycles. In future, a better understanding of human evolution may only be achieved by closer between-discipline cooperation, and the mutual sharing and integration of different bodies of theory from different disciplines [20]. This promises to be an illuminating, though challenging, enterprise. The papers represented in this issue constitute an encouraging start.

This theme issue is borne out of an interdisciplinary meeting on human niche construction hosted by the Institute of Advanced Study and the Department of Anthropology at Durham University, in association with AHRC Centre for the Evolution of Cultural Diversity. We thank them for their financial and academic support, which was fundamental to the development of this theme issue. We also thank Kevin Laland for his helpful comments on an early draft. Finally, we thank all the contributors to this theme issue for their enthusiasm, hard work and cooperation. J.K. and J.T. are funded by RCUK Academic Fellowships.

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Research

Adaptation and niche construction in human prehistory: a case study from the southern Scandinavian Late Glacial Felix Riede*,† AHRC Centre for the Evolution of Cultural Diversity, Institute of Archaeology, University College London, 31 – 34 Gordon Square, London WC1H 0PY, UK The niche construction model postulates that human bio-social evolution is composed of three inheritance domains, genetic, cultural and ecological, linked by feedback selection. This paper argues that many kinds of archaeological data can serve as proxies for human niche construction processes, and presents a method for investigating specific niche construction hypotheses. To illustrate this method, the repeated emergence of specialized reindeer (Rangifer tarandus) hunting/herding economies during the Late Palaeolithic (ca 14.7–11.5 kyr BP) in southern Scandinavia is analysed from a niche construction/triple-inheritance perspective. This economic relationship resulted in the eventual domestication of Rangifer. The hypothesis of whether domestication was achieved as early as the Late Palaeolithic, and whether this required the use of domesticated dogs (Canis familiaris) as hunting, herding or transport aids, is tested via a comparative analysis using material culture-based phylogenies and ecological datasets in relation to demographic/genetic proxies. Only weak evidence for sustained niche construction behaviours by prehistoric hunter–gatherer in southern Scandinavia is found, but this study nonetheless provides interesting insights into the likely processes of dog and reindeer domestication, and into processes of adaptation in Late Glacial foragers. Keywords: niche construction; southern Scandinavia; Late Palaeolithic; comparative method; Canis familiaris; Rangifer

1. NICHE CONSTRUCTION AND ARCHAEOLOGY Niche construction (NC) has been defined as the evolutionary process whereby organisms modify their own and other organisms’ environments in such a way that selection pressures on the current and subsequent generations are altered significantly [1]. From this point of view, adaptation can be the result of two processes: (i) environment . selection . adapted organism, or (ii) organism . NC . modified environment. The end-result of both pathways is a fit between organism and environment (adaptation), but, importantly, the process differs. This distinction was flagged-up by Lewontin [2,3] some time ago, but it is only recently that its wider implications with regards to the evolutionary trajectories in a range of species are being explored in quantitative detail (e.g. [4–9]). Odling-Smee et al. [10] have compiled a long list of potential nicheconstructing behaviours found across most taxonomic

groups. They have also noted that humans in particular are adept niche constructers, and that many human genes may be the result of recent, culturally modified selection pressures [11]. Yet, despite considerable efforts to model human biological and cultural evolution in relation to NC (e.g. [12–23]), there are only relatively few quantitative studies of human NC [14,24]. One of the reasons for this lack may be that few disciplines have access to information on the sustained and long-term modification of ecologically relevant environmental parameters and their subsequent selective repercussions. However, ‘archaeology provides unique quantitative information on population-level distributions of cultural attributes over long periods of time. This information concerns not only socially transmitted cultural traditions but also the ongoing process of niche construction’ [25, p. 177]. I argue here that the tools of the comparative method, together with archaeological data, can be used to investigate hypotheses about specific prehistoric NC processes. The NC model recognizes three domains of inheritance (cf. [26])—genetic, ecological and cultural—and archaeology can provide proxy information on all three domains. Archaeological data on craft traditions can be used to track cultural inheritance, thereby plotting the historical relationships among past communities of teachers and learners. Patterns of social information transmission among traditional societies tend to be

*[email protected] † Present address: Department of Prehistoric Archaeology, Institute for Anthropology, Archaeology and Linguistics, Moesga˚rd, 8270 Højbjerg, Denmark and Interdisciplinary Evolutionary Studies Group, Aarhus University, Denmark. Electronic supplementary material is available at http://dx.doi.org/ 10.1098/rstb.2010.0266 or via http://rstb.royalsocietypublishing.org. One contribution of 13 to a Theme Issue ‘Human niche construction’.

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conservative, operating largely within family groups [27,28], often with considerable pedagogical involvement by adults [29]. This conservatism is reflected in the many well-known typological sequences, indicating high degrees of cultural inheritance stability over many generations. Phylogenetic methods are increasingly being used to describe and analyse these patterns of material culture diversity (e.g. [30– 32]). The key advantage of cultural phylogenetics over traditional typological methods is that a given phylogenetic tree represents an explicit and quantitative hypothesis of how given archaeological ‘taxa’ [33] are related historically. Cultural phylogenetics thus opens the door to formal studies of adaptation using the tools of the so-called comparative method [34,35]. In addition, much archaeological data pertains directly to human modifications of the biotic and abiotic environments, both locally and transiently as well as at larger geographical and temporal scales [36,37]. Culture, it has long been argued, constitutes the human niche [38,39], and environmental archaeologists have made human niche modification and its consequences their primary concern [40]. This includes the domestication of animals and plants [41], as well as ‘domesticated landscapes’ [42, p. 323], and even ‘transported landscapes’ [43, p. 217]: landscape modifications and built environments brought about by collective human efforts as well as entire economies/ecologies taken from one place to another during dispersals. The ecological transmission of physical resources in the form of modified environments, domesticated plants and animals is particularly relevant to an archaeological application of NC theory, because traditional human economies, subsistence practices and land-use strategies can be described well with reference to ecological inheritance (e.g. [44– 46]). Sterelny [47, pp. 151 – 152] underlines that ‘to the extent that information does flow collectively, niche construction is our best model of the generation-by-generation accumulation of skill, technology and information’ in human societies. This collective information transmission is echoed in Oswalt’s [48] distinction between weapons/instruments on the one hand, and facilities on the other. In this view, material culture that reflects personal transmission of information and use, such as projectile points, basketry or pottery (weapons/ instruments), provides information on cultural inheritance in the strict sense. Material culture that reflects a collective transmission of information and use, such as tents and housing structures, fishing platforms, fortifications as well as field systems (facilities), can conceptually and analytically be framed as part of the ecological inheritance passed from generation to generation [49]. Alternatively, such features could be viewed as part of the human extended phenotype [50,51], but their selective relevance is via modified environments, particularly in subsequent generations born into a niche that already is modified in a given way [18,52]. Furthermore, facilities often have a uselife longer than a single human generation, and are continuously or periodically modified and changed. These evident ecological modifications cannot be readily related to the genotypes of those who played Phil. Trans. R. Soc. B (2011)

no part in putting them in place. Instead, they reference the collectively held stock of ecological knowledge and its implementation: a modified environment that constitutes the ontogenetic niche for subsequent generations. Finally, the adaptive or maladaptive effects of human NC processes should be reflected in genetic inheritance patterns of the niche-constructing populations as well as the animals and plants whose niches are affected. The increasing availability of ancient and population genetic data facilitates inferences about, and direct insights into, past demographic processes [53]. Gene frequency patterns in both modern and ancient DNA can, for instance, be used to demonstrate the evident success of early farmers and their NC behaviours involving a range of domesticated animals and plants (e.g. [54– 56]). However, genetic change is merely the endpoint of what is best thought of as a continuum of processes [57 – 59]. Archaeologists have access to datasets that reflect the (conscious or unconscious) manipulation of the behaviour or distribution of candidate domesticates long before genetic changes take place and become widely established in the target population [59]. In addition, demographic success of the nicheconstructing population itself is also reflected in a range of archaeological proxies, such as range expansion, increases in the number and/or size of sites or the number of 14C dates in a given period [60,61]. In the following section, I will provide some examples of human NC that leave archaeologically visible traces. I will contrast the NC behaviours of farmers and foragers, arguing that the domestication of plants and animals [41] as well as the lasting modification or ‘domestication’ of landscapes [42,62] sets the benchmark for effective NC. I will then go on to explore in more detail a case study of prehistoric forager NC involving domesticated dogs (Canis familiaris) and reindeer (Rangifer tarandus) hunting/herding strategies in the Late Glacial of southern Scandinavia (approx. 14.7– 11.5 kyr BP), where I use comparative methods to investigate the feedback relations between these two NC behaviours.

2. ARCHAEOLOGICAL SIGNATURES OF HUMAN NICHE CONSTRUCTION A first example, the human occupation of Greenland between about AD 950 and 1500 serves to contrast the NC behaviours of farmers and foragers. Greenland was first settled by hunter – gatherer groups from North America and Siberia in several waves beginning sometime after approximately 4.5 kyr BP [63]. Around AD 950, the southern tip of Greenland was also settled by Viking (Norse) farmers from Iceland. The expanding Greenland Norse brought with them their agricultural niche package fine-tuned to Norwegian conditions, including animals and crops. They rapidly transformed local landscapes to suit their traditional niche requirements [64,65]. During milder climatic episodes—the first few hundred years of occupation—they fared sufficiently well. When the climate in the Northern Hemisphere turned colder as well as stormier during the Medieval Cold Period,

Human niche construction in prehistory traditional crops and herding techniques began to fail [66]. Anthropogenic landscape changes such as deforestation aggravated the conditions [67,68]. The deteriorating niche quality, coupled with unfavourable climate change, isolation and an insistence on maintaining a social and economic/ecological adaptation ill-suited to High Arctic environments, culminated in the local extinction of the Greenland Norse [69]. Meanwhile, Inuit groups of the Thule culture thrived [63]. The impact of these groups on the landscape was subtler and took the form of various facilities (e.g. drive lines, hunting stands and marked pathways: [70– 72]) placed strategically in the landscape in order to facilitate travel and the management of reindeer movements. The fate of the Greenland Norse serves to highlight that initially successful NC can have negative adaptive consequences in the longer term [73]. Generally, however, dispersing farming populations provide good examples of extensive NC involving both landscape modifications and the domestication of plants and animals. Their genetic and linguistic legacies can be traced worldwide [74,75]. The first dispersal of farming populations to Europe in particular has been studied intensively and much data on the changing plant and animal ecologies of these pioneering groups are available [76 – 79]. Shennan ([25], pp. 180 – 181; my emphasis) further adds that the dispersal of agricultural populations into Europe ‘is a classic example of natural selection acting on people through an inherited cultural tradition, which gave a selective advantage to those who adopted it and passed it on to their children. In fact, the process involved not simply the inheritance of a tradition but also the transmission of a new niche, because the actual descendants of the cereal crops and animals that had originally been domesticated were being carried along as part of the dispersal’. The evolutionary success of farmers under this model is largely due to the powerful positive NC that is part and parcel of most agricultural societies [55]. Equally, however, environmental archaeological data also indicate the collapse of such early agricultural societies in some regions because farming practices destroyed the environment [80]. Continuous settlement then required further NC (e.g. slope terracing) to counteract these negative effects (e.g. [81]). Turning again to foragers, a recent ethnographic study by Bliege Bird et al. ([82]; see also [83]) provides detailed insights into the kind of landscape modifications that prehistoric hunter–gatherers may also have practised, and their adaptive outcomes. They show that episodic and systematic landscape burning by Australian Aboriginals increases hunting success measured in caloric yield per unit land. The effects of this burning on the species composition of that habitat is also documented. They demonstrate how this behaviour is underwritten and maintained via a stock of knowledge transmitted from generation to generation along with the physical niche component, the territory. Indeed, it has been argued that this behaviour has considerable time-depth in Australia [84–86]. Using detailed analyses of pollen profiles, fungal spores and charcoal traces in the vicinity of prehistoric Phil. Trans. R. Soc. B (2011)

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settlement sites, it has likewise been argued that Mesolithic and Late Palaeolithic hunter – gatherers in Europe and elsewhere had similar burning practices (e.g. [87 – 92]), and that these had important adaptive benefits by increasing access to animals [93] and plants [94]. Increasingly, the notion of pre-Neolithic agriculture is being considered [95], and fire undoubtedly played an important role in the formation of the human niche in the long term [45,96]. It is such landscape manipulations that provide the context for the most evident process of prehistoric NC, the domestication of plants and animals [41,42]. The primary domesticate found among hunter – gatherers is the dog (C. familiaris). Numerous theories for why humans first began to domesticate dogs have been put forward [97,98], with many workers stressing the adaptive benefits of using dogs as hunting companions (e.g. [99,100]). The considerable extent to which doguse enhances hunting success has recently been quantified within a behavioural ecological framework [101]. Keeping dogs also involves additional tools and trappings (tethers, leashes, pens, etc.) that together make up the constructed niche to which they are so well adapted physically, physiologically and cognitively [102 – 105]. From approximately 14 kyr BP onwards, the archaeological record is speckled with dog burials, signalling the symbiotic relationship and the important social as well as ecological role played by this first domesticate [98,106]. The effects of this long association between humans and dogs are evidenced by the significantly altered genetic composition, cognition, distribution and ecology of domesticated dogs, especially when compared with their now nearly extinct ancestor Canis lupus. The most recent suggestions regarding the geographical origin and timing of dog domestication based on genetic data alone point to present-day southern China and argue that all extant dog breeds originated there less than approximately 16.3 kyr BP [107]. This stands in direct opposition to reports of domesticated dogs in Upper Palaeolithic contexts in Europe dating to 31.7 kyr BP [108,109] and would require an extremely rapid diffusion of this resource even if only the nextoldest European specimens were considered [99]. If, as argued above, domestication is considered as a process—and the domestication of Canis should be no exception in this respect [110]—then these seemingly opposing positions can be reconciled. Behavioural, morphological and genetic markers of domestication are not linked in a lock-step fashion [59]. The presence of C. familiaris in a range of Late Glacial archaeological sites in northern Europe [99,106,111] indicates that, at the very least, these hunter–gatherer groups were beginning to engage in symbiotic relations with wolves. Possibly, these early breeds never became fully (i.e. genetically) domesticated. Alternatively, breeds brought to Europe by dispersing farming populations later replaced these earlier lineages [112]. Either way, important questions about the process of dog domestication remain open, and southern Scandinavia constitutes a useful testing ground for investigating the emergence of this important NC behaviour. Paralleling the first finds of C. familiaris, Palaeolithic foragers also began to engage in intense specialized

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economic/ecological relations with reindeer. Abundant reindeer bones that comprise practically 100 per cent of all faunal remains at some Late Glacial sites in southern Scandinavia (reviewed in the next section) document the repeated emergence of such specialized economies [113]. In fact, it has been suggested that the economic specialization seen in these earliest Late Glacial pioneers indicates a move towards reindeer herd management and domestication [114–117]. Specialized reindeer herding economies are widespread in high-latitude Eurasia today, and these practices have resulted in the partial domestication of this species [118]. While the intentional breeding of reindeer is a comparatively recent phenomenon, herd management is argued to go back a very long time indeed [119–121]. Faunal remains from key archaeological sites of this period do not support the notion of comprehensive herd control [122], but domesticated and wild reindeer herds are difficult to distinguish morphologically and demographically as even managed herds roam freely much of the time. Recent genetic studies indicate multiple independent domestication events in extant Rangifer populations in northern Europe [123], and standard zooarchaeological techniques may therefore not be able to readily detect incipient or small-scale reindeer herd management. Reindeer hunting and reindeer herding have much in common from an ecological perspective [124]. Istomin and Dwyer [125, p. 613] describe the relationship between humans and Rangifer as a kind of ‘dynamic mutual adaptation’, where humans impact the behaviour and biology of wild and domesticated reindeer, while they in turn influence their human counterparts. In addition, Ingold [126] and Ventsel [127] stress the continuity between techniques and technologies of Rangifer hunting and herding. These technologies—drive lines and pathways, for instance—are signatures of forager NC involving reindeer, and are found in Scandinavia from at least the Early Holocene [128,129]. Ingold also notes that reindeer economies provide excellent opportunities for canine companions, and Mu¨ller-Wille et al. [121] point out that northern European reindeer economies not only are associated with but also require the use of dogs. In the following, I therefore explore the specific hypothesis that intense reindeer specializations akin to herd management evolved already during the Late Glacial in southern Scandinavia. I ask whether the domestication or introduction of C. familiaris facilitated the repeated emergence of this kind of economy, which in terms of its use of dogs and in its relationship with reindeer reflects the NC behaviours of these hunter–gatherer groups. Odling-Smee et al. [10, p. 344] have suggested that such ‘signatures of past human cultural niche construction’ can be investigated using the tools of the comparative method, a powerful and well-described suite of methods for the analysis of adaptation and causal correlations in biology [35]. The comparative method requires phylogenies in order to control for the historical relatedness and attendant statistical nonindependence of the units under study, known as ‘Galton’s Problem’. What such comparative analyses allow is to establish whether two given NC trait evolve in a correlated manner, where one trait, the niche-constructing trait, drives change in another trait, the Phil. Trans. R. Soc. B (2011)

recipient trait whose fitness depends on the effects of previous NC [18]. Such correlated evolution over time establishes the feedback relations between niche modifications that are at the heart of the NC model. Material culture phylogenies are here constructed using Bayesian phylogenetic methods and lithic projectile point data, which reflect patterns of teaching and learning in Late Palaeolithic southern Scandinavia [130,131]. Such data, in non-phylogenetic formats, have traditionally provided the backbone for the culture-history in this region [132]. Information on the presence/absence of domesticated dogs and on reindeer specialization is plotted onto these phylogenies, and the resulting pattern is queried for correlations among the selected traits. In formal terms, this paper addresses the following hypotheses: (H0) Dog-use and successful specialized reindeer economies evolve independently. (H1) Dog-use and successful specialized reindeer economies evolve in concert. If support for H1 can be found, it can be addressed which of the traits is the primary niche-constructing and which the recipient trait: (H1a) Dog-use facilitate the evolution of specialized reindeer economies (dog-use ¼ nicheconstructing trait, reindeer specialization ¼ recipient trait). (H1b) The adoption of specialized reindeer economies necessitate dogs (reindeer specialization ¼ nicheconstructing trait, dog-use ¼ recipient trait). I first briefly review southern Scandinavian Late Palaeolithic culture-history, the evidence for specialized reindeer economies and the use of domesticated dogs in this period. Then, a methodology is presented that examines the correlation between reindeer specialization and dog-use across Bayesian material culture phylogenies reflecting the major culturehistorical trends of this period. The likelihood ratio (LR) test and Bayes factors (BFs) are used to assess whether these two traits are correlated. These analyses indicate that specialized reindeer hunting without dogs was probably an unstable strategy tenable only under favourable climatic conditions during the Late Glacial, and that domesticated dogs were a necessary component of successful specialized reindeer economies, as suggested by Mu¨ller-Wille et al. [121]. They also support the idea that domesticated dogs during this period were a costly resource that, while conferring important adaptive advantages in hunting, also required significant maintenance and training costs [133]. The periodic absence of dogs during the Late Glacial colonization of northern Europe—known also from the later human colonization of High Arctic Greenland [134]—indicates that despite the evident adaptive benefits of dog-use, they may have dropped out of the cultural repertoire on occasion. In addition to the relationship between the two NC traits under study, archaeological proxies as well as recent population genetic data indicate that a demographically viable, continuous human presence in Scandinavia was only


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Table 1. The demographic and culture-historical framework for the Late Glacial resettlement of northern Europe, modified from Gamble et al. [137]. The event stratigraphy follows Bjo¨rck et al. [138] and Lowe et al. [139]. GS, Greenland Stadial; GI, Greenland Interstadial.

event stratigraphy

GRIP ice core years of onset (BP)

Holocene

11 500

GI-1a

12 650

GI-1b

12 900

GI-1c GI-1d

13 150 13 900

GI-1e GS-2a GS-2b GS-2c

14 500 16 900 19 500 21 200 21 800

GS-1

GS-2

GI-2

chronozones

Younger Dryas 5. contraction Late Allerød Laacher See eruption Intra-Allerød 4. stasis and population Cold Phase decline Early Allerød Older Dryas 3. colonization, abandonment and re-colonization Bølling 2. initial expansions into central Europe Last Glacial Maximum

possible during the later part of the Late Glacial when dogs were firmly established in the ecologically inherited repertoire of these forager groups.

3. THE SOUTHERN SCANDINAVIAN LATE PALAEOLITHIC At the height of the Last Ice Age, southern Scandinavia was almost fully covered by ice and devoid of people. The reappearance of hunter–gatherer groups just before 14.7 kyr BP was part of the general human reexpansion from their glacial refugia. Gamble and colleagues [135–137] have provided a framework for this process incorporating insights from environmental science, population genetics and archaeology (table 1). Although southern Scandinavia became part of the human world from about 14.7 kyr BP, it remained demographically marginal until the beginning of the Holocene climatic amelioration. Population densities were low [140] and probably fluctuated in accord with environmental changes [141,142]. Traditionally, four cultures or techno-complexes are recognized in the region, arranged in chronological succession: the Hamburgian (divided into an earlier Classic, and a later Havelte phase), the FedermesserGruppen (FMG), the Bromme and Ahrensburgian cultures, each with a characteristic stone tool repertoire (figure 1). Numerous hypotheses regarding the process of re-colonization have been proposed. Eriksen [143, p. 169], for instance, suggests that this sequence represents ‘a continuous and largely endogenous cultural development’, while Petersen [144] argues for a discontinuous human presence. Other recent studies have also suggested that these techno-complexes may represent discrete expansion – retraction pulses [145,146], and much recent work has focused on better understanding the underlying processes of culture change. Riede [147,148] has suggested that the origin of the Bromme should be seen in relation to the eruption of the Laacher See volcano around Phil. Trans. R. Soc. B (2011)

population events

1. refugium

techno-complexes

Ahrensburgian Bromme culture Federmesser-Gruppen (FMG) Hamburgian (Havelte and Classic phases) Southern Scandinavia not settled Southern Scandinavia not settled

13 kyr BP and the subsequent isolation experienced by peripheral groups belonging to the FMG techno-complex. Follow-up studies have explored different forcing mechanisms responsible for the relocation of animal and human populations away from areas affected by the volcanic ash fall-out [149,150]. Economically, however, neither the FMG nor the Bromme are characterized by specialized reindeer hunting. In contrast, both the preceding Hamburgian techno-complex and the later Ahrensburgian cultures are seen as specialized reindeer hunters, based on faunal evidence from a range of sites [151 –153]. Late Palaeolithic hunter – gatherers may also have controlled or domesticated reindeer, as discussed above, and they may have manipulated the landscape by building cairns, flag lines, hunting stands etc. in order to steer the movements of herds for their own advantage [151,154], and to facilitate travel in an otherwise relatively featureless landscape [155]. In sum, ‘northern Europe is an extraordinary laboratory for the investigation of human colonization and adaptation’ [156, p. 185]. Adaptation and range expansion are possible outcomes of NC [157]. Specialized reindeer economies emerged in the Hamburgian and Ahrensburgian, but these two cultures are separated in time by nearly 1 kyr. It is essential to take account of the historical relatedness or otherwise of these groups when discussing whether their reindeer specializations were, in fact, adaptive and whether they relate to other NC behaviours such as dog-use.

4. MATERIAL AND METHODS As in many other regions, characteristic projectile points have provided the backbone for culture-historical reconstruction in southern Scandinavian prehistory [132]. Because of their historical sensitivity, projectile points have also been analysed, with increasing frequency, using phylogenetic methods [158]. Cultural

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Human niche construction in prehistory (a)

(b)

3 2

2

3

4

5

1

4 1

1 cm (c)

1 cm

(d) 1

2

3 1

2

3

1 cm

4

1 cm

Figure 1. The formal tools of the four Late Palaeolithic techno-complexes. (a) Hamburgian: 1, shouldered point (Classic phase); 2, shouldered point (Havelte phase); 3, combination tool; 4, double-ended burin; 5, blade-scraper with lateral retouch. (b) Federmesser-Gruppen: 1, arch-backed point; 2, burin on retouch; 3, tanged scraper; 4, thumbnail scraper. (c) Bromme: 1, large tanged point; 2, dihedral burin; 3, end-scraper. (d) Ahrensburgian: 1, tanged point; 2, early microlithic (Zonhoven) point; 3, burin; 4, scraper. Filled dots mark the percussion end; arrows indicate burin blows. After Eriksen [132].

XVII

IV

trait list:

II

XXI

XXII

I X XV

XIV V

XIII

VI XII

IX

I II III IV V VI VII VIII IX X XI XII XIII XIV XV XVI XVII XVIII XIX XX XXI XXII XXIII

maximum length maximum width maximum thickness body/tang ratio percussion bulb presence/absence tang orientation tang retouch direction, right tang retouch direction, left tang retouch length, right tang retouch length, left hafting notch presence/absence tang symmetry tang alignment shoulder angle, right shoulder angle, left tip angle tip retouch intensity, right tip retouch intensity, left tip retouch direction, right tip retouch direction, left tip retouch length, right tip retouch length, left tip alignment

Figure 2. Measured characters. Characters used in phylogeny building are listed in table 2, and the data matrix is provided as electronic supplementary material, table S1. Photo by the author with permission from the National Museum of Denmark, Copenhagen.

phylogenetics has advantages over traditional typological approaches in that a given phylogeny constitutes a quantitative hypothesis of the historical relatedness among the chosen units of analysis [159]. Such hypotheses can then be evaluated statistically and in relation to external datasets, such as stratigraphic, geographical or radiocarbon dating information. While a phylogenetic quantification of material culture relations alone can reveal important new insights in its own right, phylogenies can also be used in Phil. Trans. R. Soc. B (2011)

additional comparative analyses. Here, a method is presented that uses these tools to detect Late Palaeolithic hunter – gatherer NC.

(a) Construction of archaeological taxonomic units The method of taxon construction largely follows that described by O’Brien et al. [160,161] and Darwent & O’Brien [162], although an initial analysis also used


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Table 2. Attribute and attribute states used in phylogeny building. character

character state

character

character state

I maximum length (mm)

0. 45 1. 45–68 2. . 68 0. ,19 1. 19

VII tang retouch direction

III maximum thickness (mm)

0. ,5 1. 5

IX tip retouch

IV volumea

0. ,39 1. 39–58 2. 59–166 3. .166 0. unilateral retouch 1. no tang 2. ,2.0 3. 2.0 0. faint bulb 1. pronounced bulb 2. distinct bulb with scarring

X combined tang/body ratioc

0. opposing 1. none 2. same side 0. .2.5 1. 1.5– 2.5 2. 1.0– 1.4 0. none 1. unilateral 2. bilateral 0. ,23 1. 23–42 2. .42

II maximum width (mm)

V tang/body ratiob

VI percussion bulb morphology

VIII tang symmetry

XI retouch extent ratiod

0. 4 –18 1. 19–40 2. .40

XII tang retouch symmetry

0. 1.4 1. no tang 2. .1.4

a

Volume ¼ length width thickness. Tang/body ratio ¼ length/shortest tang retouch. c Length/tang/body. d Total retouch extent/(length width). b

(b) Phylogeny construction Bayesian Markov chain Monte Carlo (MCMC) methods are used to retrieve a sample of trees from the most likely regions of the universe of possible topologies [165]. The model of evolution used is a simple multistate model (KSTATES), where the rates of character state change are presumed to be equal, and only minimal assumptions about mode, tempo and direction of character change are introduced. The trees were rooted using the taxon associated with the oldest radiocarbon date. A total of 10 000 k iterations were run and the tree universe sampled at every 40 kth iteration to minimize autocorrelation among the trees in the final sample. The Markov chain quickly converged on the most likely tree configurations, and after a few thousand iterations, only minor fluctuations in the likelihood score of each tree are observed (figure 3). Figure 4 shows the consensus tree of the resulting tree sample Phil. Trans. R. Soc. B (2011)

–80 –100 –120 log Lh

–140 –160 –180 –200 –220

0 00 20

00 16

00

0 00

0 00 00 12

00 80

00 00 40

00

–240

0

phylogenetic networks [163,164] to explore potential instances of blending and reticulation [159]. A total of 607 specimens were measured for a variety of characters (figure 2), which were divided into discrete character states using exploratory statistics and lithic analytical principles as guidelines [131]. Twelve of these attributes were used to construct the phylogenies presented here, and these reflect the size and shape of the projectiles as well as manufacturing methods (table 2). Each taxon comprises at least five specimens identical in their attribute compositions, thus reflecting recurrently taught and learned flint-knapping behaviour [29,131]. This approach yielded 16 taxa, of which the taxon associated with the oldest 14C date was chosen as outgroup.

iterations Figure 3. The Markov chains trajectory through the likelihood landscape during the first 200 k iterations.

(n ¼ 251). This tree differs little from those produced using other maximum-likelihood (ML) and parsimony-based approaches (F. Riede 2007, unpublished PhD thesis), and the major techno-complexes recognized by traditional typological analysis are represented in the phylogeny, albeit not all as monophyletic clades [157]. The branch lengths reflect both the chronological sequence of diversification and the degree to which these groups experienced isolation (especially the Bromme clade). Even rates of cultural change cannot, however, be assumed. At times, craftsmen deliberately introduce variation into the manufacturing process [171], which can rapidly increase branch length. Note that the consensus tree is not used in further analyses. Instead, the uncertainties associated with the tree-building procedure are

800

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Human niche construction in prehistory outgroup

(0/1) (0/1)

Classic Hamburgian (0/1) 49

(0/1) 51

100

(0/0)

FMG clade 78

(0/0) 90

26

Ahrensburgian clade

(0/1) 67

(0/1)

Havelte clade (1/1)

33

(1/1) 75

(1/1)

41

(0/0) (0/0)

96

(0/0)

34

Bromme clade

(0/0)

29 83

(0/0)

0.1

Figure 4. The consensus tree based on a sample of 251 Bayesian trees produced using the MCMC methods implemented in BAYESPHYLOGENIES [165]. Branch support values below 50 are shown in grey and reflect the inherent difficulty of accurately distinguishing the tools of some cultures from this period. The presence/absence scores for specialized dog-use/reindeer hunting are presented alongside each taxon. Information on the presence of dogs, taken from [99,106,111,166 –169], is assigned to the taxa at the level of the respective cultural groupings. BAYESPHYLOGENIES is available from www.evolution.reading.ac.uk. See Walker [170] for a comprehensive bibliography of prehistoric Canis remains.

8.0

incorporated into subsequent analyses by querying the entire sample of 251 trees.

7.0 6.0

(d) Transition rate analysis The transition rate probabilities provided as part of the output by BAYESTRAITS (table 3) give clues as to the order of correlated change, and such correlations Phil. Trans. R. Soc. B (2011)

5.0 %

(c) Examining correlated trait change Each taxon is associated with the two traits (dog-use/reindeer specialization) under investigation, scored as presence (1)/absence (0), at the level of their associated techno-complex. The ML and Bayesian algorithms implemented in BAYESTRAITS [172,173] were used to approximate trait correlations. The posterior log-likelihoods for an ML model (iterations ¼ 1000 k; rate deviation ¼ 80; multiple tries ¼ 25; sample period ¼ 20) in which the two traits evolve independently are differently distributed than those in which the two traits are assumed to evolve in concert (figure 5). The LR test, described by Pagel [172] and calculated by 2*[log-Lh(D) 2 logLh(I)], can be used to statistically evaluate trait correlations in each tree sample. This test indicates that the mean of these likelihood (Lh) distributions is not statistically significant (p . 0.21, x 2, d.f. ¼ 4). In the more appropriate Bayesian framework, the so-called Bayes factor can be used to assess relative support for one over the other model (see [173] for a detailed description). This analysis (parameter settings as above; burn-in ¼ 50 k) returns a log BF (¼2*[log(harmonic mean(D)) 2 log(harmonic mean(I))]) of 0.7, i.e. positive if very weak evidence in favour of the dependent model [174].

4.0 3.0 2.0 1.0 0 –20

–18

–16 –14 –12 log-Lh(I) and log-Lh(D)

–10

–8

Figure 5. The distribution (in %) of log-likelihood values in the independent (log-Lh(I )) (grey bars) and dependent models (log-Lh(D) (black bars).

establish which trait is the active niche-constructing trait and which the recipient trait (figure 6). In the ML-dependent model, the distributions of transition rates for each trait combination across the 251 trees show some patterning (electronic supplementary material, figure S1). The transition rates for the evolution of non-dog-using economic generalists to non-dog-using reindeer specialists are the lowest and contrast with those for the transition from dog-using generalists to dog-using specialists (q12 = q34), indicating that it was unlikely for reindeer specialization to emerge in the absence of dogs. In addition, dog-use appears to have facilitated economic flexibility as expressed in the more frequent transitions between generalist and specialized economies in the presence


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Table 3. Mean ML transition rates for the independent and dependent models. independent model dog-use 0 1 reindeer specialization 0 1

0 — q10: 6.22 0 — q10: 3.08

1 q01: 13.11 — 1 q01: 2.75 —

dependent model dog-use/reindeer specialization 0/0 0/1 1/0 1/1

0/0 – q21: 0.43 q31: 1.66 —

0/1 q12: 0.07 — — q42: 19.92

q12: 0.07 q21: 0.43

q31: 1.66

q34: 28.96

q43: 20.49

q42: 19.92

1,0 (dog-user/ economic generalist)

0/1 (not dog-user/ economic specialist) q24: 11.13

q13: 0.03

0/0 (not dog-user/ economic generalist)

1/1 (dog-user/ economic specialist)

Figure 6. This flow diagram shows the mean transition rates in the dependent (ML) model. The thickness of the arrows corresponds to the transition likelihoods from one trait combination to another. BAYESTRAITS is available from www.evolution.reading.ac.uk.

of dogs (q43, q43), while itself being a labile trait with a relatively high likelihood of becoming lost (q42, q31). 5. DISCUSSION AND CONCLUSION The foregoing analysis has found limited positive support for H1, a correlated evolution of the use of domesticated dogs as hunting/herding/transport aids and the repeated emergence of specialized reindeer economies. Both traits can be understood as a constructed niche dimension and interpreted within the NC framework. However, this support is not statistically significant. Why is the evidence for a correlated evolution of dog-use and specialized reindeer hunting not stronger, given the dependency of reindeer economies upon dogs observed today? The results of this study support the notion that prehistoric forager NC was in fact limited and intermittent, with little impact on target animals or landscapes. In this view, the fragmentary record of domesticated dogs in the northern European Late Glacial may not be the result of poor preservation, but rather of the fact that dog domestication/use was not a core part of the cultural repertoire at the time, much like in prehistoric Greenland [134]. It is possible, for instance, that early tamed or domesticated dogs did not provide significant advantages in food procurement [133]. If so, the costs of keeping these pets would regularly outweigh their benefits, particularly perhaps during Phil. Trans. R. Soc. B (2011)

1/0 q13: 0.03 — — q43: 20.49

1/1 — q24: 11.13 q34: 28.96 —

times of food crisis. It is also worth noting that the increasingly close association of humans and dogs may already at this point have resulted in the zoonotic emergence of a range of infectious diseases [175], which can be seen as a negative NC effect. In addition, and in contrast to some recent suggestions, this study finds no support for the notion of reindeer herd management during the earliest phases (Hamburgian) of human presence in southern Scandinavia during the Late Glacial. The adoption of a specialized reindeer economy possibly involving a degree of herd management or incipient domestication by Ahrensburgian groups was contingent on the adoption of domesticated dogs. Further distinguishing between successful and unsuccessful reindeer economies may aid in interpreting these results. Both Petersen [144] and Riede [155,176] have argued that the Hamburgian occupation of southern Scandinavia was ultimately unsuccessful. Both mitochondrial and non-recombining Y-chromosome data in Scandinavia indicate that a demographically viable colonization of the region is linked to the Ahrensburgian [177–179], implying that earlier colonization attempts had been unsuccessful. The Ahrensburgian is accordingly associated with a range expansion as well as an increase in the number and size of settlements (e.g. [180,181]). The emergence of specialized reindeer economies together with dog-use in the Ahrensburgian can thus be seen as an example of positive cultural NC that enabled an efficient adaptation to the harsh GS-1 conditions. In contrast, the appearance of Hamburgian hunters seems strongly correlated with a pronounced abundance of Rangifer during the initial stages of faunal succession, first in the southern part of Scandinavia, and then increasingly northwards [176,182]. The disappearance of the Hamburgian techno-complex, in this view, represents a concrete example of negative NC, i.e. the failure of an adaptive system: ‘even the most adaptable of creatures will experience limits to its tolerance space, outside of which it is unable to behave adaptively’ ([183], p. 98). In the absence of dogs, and coupled with the climatic downturn at GI-1d most probably associated with a pronounced drop in reindeer populations across the region, Hamburgian foragers were no longer able to uphold the cultural buffer mechanisms protecting their niche space from larger scale, independent changes in the environment. Figure 7 summarizes the NC processes investigated in this study.

F. Riede

Human niche construction in prehistory cultural processes

cultural response: Ahb: reindeer specialization

cultural niche construction: Ahb: dog domestication Hmb: reindeer specialization

modified environments

no cultural response in Hmb

gene pool

culturally transformed natural selection: Ahb: +expansion/radiation Hmb: –contraction/extinction

cultural niche construction modifies environments

802

route 1

route 2

Figure 7. The correlated evolution of dog domestication and use and specialized reindeer economies during the southern Scandinavia Late Glacial provides evidence of what Odling-Smee et al. [10] call ‘route 1’ and ‘route 2’ NC processes. The domestication of dogs in or their introduction to southern Scandinavia during the Ahrensburgian (Ahb) led to the emergence of specialized reindeer economies, possibly involving herd management and early forms of reindeer domestication. In this case, an initial niche-constructing behaviour (dog domestication/use) drove further behavioural changes (specialized reindeer hunting/herding; route 1). The cumulative genetic effects of this NC are seen in the range expansion of Ahrensburgian groups and the genetic signature of this expansion in living northern European populations (route 2, positive). In contrast, the adoption of specialized reindeer economies without domesticated dogs during the earliest phase of colonization (Hamburgian: Hmb), while initially advantageous, ultimately led to the demise of these pioneering populations (route 2, negative). Modified from Odling-Smee et al. [10].

With regards to the methods used here, it should be noted that the search for correlations in analyses with few taxa is difficult [172]. Also, posterior branch support values for some clades used in this study are quite low. Larger, more robust phylogenies will increase our confidence in subsequent trait correlation analyses, yet ‘even partial phylogenetic information provides a better model of the variance in the data than completely ignoring phylogeny and assuming independence’ [34, p. 717]. A particular advantage of the time-depth provided by archaeological data is that it offers the opportunity to integrate stratigraphic and phylogenetic information, and to give directionality to both independent and dependent comparative models. Assigning particular trait states to known or reconstructed nodes would constrain comparative models, facilitating hypothesis testing. Finally, if the disappearance of the Hamburgian techno-complex at the GI-1d (Older Dryas) cold spell does represent a cultural ‘extinction’, then the inclusion of such ‘extinct’ taxa in the correlation analysis might distort the results of any comparative analyses [184,185]. Future work could profitably tackle these methodological issues, paralleling similar efforts in evolutionary biology [184], and by making use of some of the freely available software packages discussed by Freckleton [186]. Yet, despite the caveat of statistical non-significance, a comparative analysis of early dog domestication/use in northern Europe and the repeated emergence of specialized reindeer economies has highlighted several interesting features of this process, and a series of additional hypotheses are generated: Did the Late Glacial dogs that dispersed into northern Europe with their human partners belong to the currently dominant Phil. Trans. R. Soc. B (2011)

lineages? If yes, current interpretations about the timing and geography of the earliest dog domestication may have to be revised. If not, then repeated but incomplete domestication events have to be considered. Ancient DNA analysis of selected Late Glacial dog remains could be used to establish the relationship between prehistoric and present dog breeds. If extinct breeds can be found, these could be used to track the expansion of human groups in Europe and to investigate the interactions between indigenous populations and later immigrants [187,188]. Likewise, the genetic analysis of Late Glacial reindeer from different periods could aid in exploring their relation to each other, and to extant wild and domestic herds. In addition, targeted archaeological fieldwork might unearth technologies more directly associated with the keeping of dogs or the herding of reindeer. This paper has built on previous efforts to identify and track prehistoric hunter – gatherer NC signatures [189 – 191] by exploring a quantitative method that searches for evolutionary correlations of ecologically inherited traits across material culture phylogenies. This methodology—potentially applicable across a wide range of archaeological datasets that act as proxies for past human NC—allows a discrimination of niche-constructing and recipient traits. Given the inherent difficulties in investigating human NC experimentally, archaeological data may provide useful quantitative data on such long-term processes and their evolutionary consequences. The present analysis has not found statistically significant support for sustained NC practices by Late Glacial hunter– gatherers in southern Scandinavia, and future analysis of prehistoric NC should perhaps focus on the more

Human niche construction in prehistory extensive environmental modifications and domestication efforts of past farming populations. In line with the arguments presented here, palaeontologists [192,193] as well as those concerned with the formation of soils [194,195] and landforms [196 – 199] have suggested that organisms play a demonstrable role in shaping the physical and adaptive landscapes in which they live, at scales ranging from the geological to the microscopic, from the long term to the transient. Supplementing these disciplines, prehistoric archaeology provides information on specifically human NC at specifically prehistoric timescales. Research for this paper was conducted while working as British Academy Postdoctoral Fellow (PDF/2007/462) at the AHRC Center for the Evolution of Cultural Diversity (UCL). The support of Stephen Shennan and all colleagues at the CECD is gratefully acknowledged. I also thank the two anonymous reviewers for their comments and Jamie Tehrani and Jeremy Kendall for a stimulating workshop.

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Review

From hominins to humans: how sapiens became behaviourally modern Kim Sterelny* Philosophy Program and Tempo and Mode, Australian National University and Philosophy Program, Victoria University of Wellington, Wellington, New Zealand This paper contributes to a debate in the palaeoarchaeological community about the major time-lag between the origin of anatomically modern humans and the appearance of typically human cultural behaviour. Why did humans take so long—at least 100 000 years—to become ‘behaviourally modern’? The transition is often explained as a change in the intrinsic cognitive competence of modern humans: often in terms of a new capacity for symbolic thought, or the final perfection of language. These cognitive breakthrough models are not satisfactory, for they fail to explain the uneven palaeoanthropological record of human competence. Many supposed signature capacities appear (and then disappear) before the supposed cognitive breakthrough; many of the signature capacities disappear again after the breakthrough. So, instead of seeing behavioural modernity as a simple reflection of a new kind of mind, this paper presents a niche construction conceptual model of behavioural modernity. Humans became behaviourally modern when they could reliably transmit accumulated informational capital to the next generation, and transmit it with sufficient precision for innovations to be preserved and accumulated. In turn, the reliable accumulation of culture depends on the construction of learning environments, not just intrinsic cognitive machinery. I argue that the model is (i) evolutionarily plausible: the elements of the model can be assembled incrementally, without implausible selective scenarios; (ii) the model coheres with the broad palaeoarchaeological record; (iii) the model is anthropologically and ethnographically plausible; and (iv) the model is testable, though only in coarse, preliminary ways. Keywords: niche construction; behavioural modernity; hominins

1. DEVELOPMENTAL NICHE CONSTRUCTION The theory of niche construction begins with the insight that agents individually and collectively shape their environment. Selection results in the adaptation of agents to their environments. But agents also adapt their environments to their own phenotypes. Termites flourish in the environments they experience in part because they experience environments they have built themselves [1,2]. Much work in niche construction focuses on the effects organisms have on their selective environment. But termite mounds and beaver complexes do not just modify the effects of the physical, social and biological world on adults. They also structure the environment in which the next generation develops. In modifying their own environment, many organisms also engineer the developmental environment of their offspring. As the effects of genes are often sensitive to their context [3], these effects on developmental environment influence the next generation’s phenotypes. Thus, termites develop in a world built by and for termites, and so their developmental environment has been stabilized. Compared with their presocial ancestors, termite genes are

expressed in a narrowed range of developmental environments, and hence the phenotypic effects of those genes are more predictable (see [4,5] on the importance of these environment – gene expression effects). Developmental niche construction is of profound evolutionary significance. Indeed, there is a case for the idea that complex multi-celled animal life depends on intergenerationally engineered developmental environments. It is a truism of evolutionary theory that cumulative evolution depends on high fidelity inheritance, and high fidelity inheritance depends on sending developmental signals across the generation with high fidelity [6]. But complex multi-cellularity increases the demands on these mechanisms. Multicelled organisms have evolved many times [7], but only in a few cases have these lineages generated impressive disparity and diversity. The evolution of complex multicellularity requires the evolution of a developmental cycle, and that in turn requires a major advance in mechanisms of inheritance. Protist genes never have to build the critical inner cellular structures of protists. The cell divides, but crucial intercellular structures do not have to be constructed from scratch in the descendant cells. Reproduction can largely be reduced to growth and fission. In contrast, organs and tissues do not exist in miniature in fertilized ova.

* [email protected] One contribution of 13 to a Theme Issue ‘Human niche construction’.

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Thus, one major transition in complex multicellularity is a transition from (largely) preformationist to epigenetic development. Complex multi-celled organisms exist only because there are developmental cycles in which key structures of adult organisms are rebuilt from scratch in the new generation. So, the problem of cross-generation fidelity is more pressing for macrobes than for microbes. It is likely that increased parental control of developmental environments was crucial to the Metazoan radiation. For genes to have stable phenotypic effects, they must be inserted into a structured and predictable developmental environment. Even if replication is of high fidelity, it is of no use to just make a new set of genes: the parental generation must build an environment in which those genes are used in the right way. The more complex the developmental pathways, the more the genereading environment is as important as signal quantity and fidelity. The egg is such a structured system; it is arguable that its invention is the major breakthrough that allowed the flow of genes across the generations to orchestrate development in a fine-grained and reliable way [8]. It is adapted both to function in an environment and to provide an initial set of triggers for gene expression. Whatever the fate of this specific suggestion, macrobe evolution depends on the evolution of increased developmental control. The evolution of complex form, then, depends both on high fidelity genetic inheritance and on the stability of the genotype – phenotype map. This stability depends, in part, on control by the adult organism of the environment of gene expression. But while genetic inheritance is the most fundamental system of inheritance, it is not the only one [9]. Intergenerational social learning is another, and while the overall importance of learning as a mechanism of inheritance is a matter of much debate, it is widely agreed to have been important in human evolution [10 – 12]. The core argument of this paper is, first, to show that the fidelity of social learning depends both on the intrinsic accuracy of cognitive learning mechanisms and on the control of the developmental environment and, second, to relate this idea to the gradually emerging but profound changes in human material culture; changes that emerged between 100 000 (or a little earlier) and 50 000 years BP. I begin with the interactionist perspective on social learning. Human cultural life depends on our capacity to accumulate and transmit cognitive capital. Individually and collectively, humans act effectively in their economic, social and technological worlds largely because their lifeways are supported by information they inherit from the previous generation. Such transfer depends, in part, on specific cognitive adaptations for social learning (for example: language, imitation). But it also depends on adapted learning environments, on developmental niche construction. Humans accumulate cognitive capital through interaction between intrinsic, genetically canalized features of human minds and adaptively organized developmental environments. Thus, identifying the role of niche construction in human evolution is not an alternative to the dual-inheritance models that Stephen Shennan and others have been recently developing [13]. Rather, identifying the ways humans Phil. Trans. R. Soc. B (2011)

organize the developmental environment of the next generation helps explain the fidelity and bandwidth (the volume) of cultural inheritance, the features that make it central to human evolution. Apprentice learning offers a helpful conceptual model of the synergy between organized learning environment and individual cognitive adaptation. Apprentice learning is a very powerful mode of social learning, making possible the reliable re-acquisition of complex and difficult skills. It is learning by doing. But it is learning by doing in an environment seeded with informational resources. These include raw materials processed, partly processed, unprocessed. In addition, full and partial templates of the final product are available to guide action. Moreover, there are many opportunities to learn by observing highly skilled practitioners. Often advice is available from both experts and peers, for learning is often social and collaborative. Apprentice learning depends on individual cognitive adaptations for social learning but it depends as well on adaptively structured learning environments. I will argue that this mode of social learning has deep roots in sapiens history. The apprentice learning model has four important virtues. First: it identifies a form of learning that can be assembled incrementally. The reliable transmission of skill can begin as a side-effect of adult activity, without adult teaching or adaptations for social learning in the young. Once established, it then brings with it selection for cognitive and social changes that increase the reliability or reduce the cost of learning. But rudimentary and reliable skill transmission does not presuppose such adaptations [14]. Second, apprentice learning is known to support high fidelity, high bandwidth knowledge flow. Until recently, much technical competence in the industrial society depended on apprentice learning. Third, the model fits ethnographic data quite well. Formal educational institutions and explicit teaching are not prominent parts of traditional society. But many forager societies organize and enhance children’s participation in economic activity, and this supports the transmission of traditional craft skills [15,16]. Finally, the model can be tested against the archaeological record, though only in a preliminary, suggestive, way. One test depends on applying the model to a famous problem in palaeoanthropology: the origins of ‘behavioural modernity’. That problem arises out of an apparent disjunction between the origin of our species and the archaeological record of our cultures. From about 50 kyr BP, the archaeological record seems to show human cultures that resemble foraging cultures known from historical records [17 – 20]. Those ancient members of our species often had a diverse, complex and regionally well-differentiated technology. They were ecologically flexible, exploiting a wide range of resources, responding appropriately to seasonal fluctuations, and able to penetrate quite demanding habitats. They were capable of crossing significant stretches of ocean in boats or rafts. Their lives were rich in the use of physical symbols. They stylized some of their technology. They made jewellery, and almost certainly used ochre to decorate their bodies and goods. They buried their dead.


Review. From hominins to humans There is as yet no clear evidence of music, but that may well reflect limits on preservation rather than limits on these ancient cultures. In short, they were ‘behaviourally modern’. Modernity does not, however, coincide with the first appearance of our species (or any other). Anatomically modern humans—our species—seem to have appeared in Southern Africa at some stage during the period 200 – 150 kyr BP [18,21]. But those first humans do not seem to have been behaviourally modern. Their technology seems to have been less diverse; their ecology less flexible; their cultural lives less mediated by physical symbols. It was once thought that this ensemble of contrasts between behaviourally modern and early sapiens arose abruptly in hominin history, 50– 60 kyr BP. This saltationist model is still sometimes defended, but there seems to be good evidence that the modern cultural ensemble arose gradually in Africa, and that its abrupt appearance in the European record is the signature of migration (and perhaps indigenous response) rather than rapid biocultural evolution [20,22– 24]. Even so, there seems to be a contrast between the more recent sapiens cultures and those of the first two-thirds of the history of the species, and this has led to a vigorous debate in palaeoanthropology about the identification of behavioural modernity, its significance and how its origin is to be explained. I will first review this debate, and then show that niche construction theory enables us to develop a satisfying solution to the puzzle that is supposedly at its heart.

2. BEHAVIOURAL MODERNITY It can be reasonably doubted whether there is a qualitative difference between the earliest sapiens cultures and those that established in Africa, Europe, the Middle East, Asia and the Sahul 50 000 years ago or so. Perhaps the supposed cultural difference is a result of our imperfect record of the cultural and cognitive life of the earliest sapiens. Moreover, Peter Hiscock and Sue O’Connor point out that rare technologies are less well preserved when we look deeper into the past. The record is not just imperfect, it is biased, showing us less of the most ancient cultures [25,26]. Moreover, we would expect a smaller and geographically restricted set of populations to have a less varied material technology than larger and more widespread populations, even if their fundamental cognitive capacities and social organization are the same. Even so, in archaeology and palaeoanthropology, the prevailing orthodoxy holds that there is a qualitative difference, and I shall accept that consensus in this paper. The nature of that qualitative difference, though, is a matter of great dispute, and this section and the next identify the change to be explained. On one view, behavioural modernity is a cluster of cognitive capacities that are both critical in themselves to contemporary human culture and which leave a detectable signature in the historical record. Perhaps, the most influential paper in this genre is Sally McBrearty and Andrew Brooks’ The Revolution That Wasn’t [24]. As the authors see it, these cognitive competences are: behavioural and technological Phil. Trans. R. Soc. B (2011)

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innovativeness; abstract thinking (the capacity to think about the elsewhere and the elsewhen); the ability to plan as an individual and to coordinate with others; and the ability to make and use physical symbols. And they suggest potential archaeological signatures of all of these capacities. The most obvious are technological signatures of innovation. Innovation is signalled by any or all of: new stone technologies (blades, microblades, backing); the increasing use of new materials like bone and antler; a larger toolkit (e.g. projectiles); and an increased control of fire. Likewise, they argue that planning and coordination can be detected in the historical record, for example, in the expansion of the human range into challenging environments. Moreover, the capacity to hunt large and dangerous animals without excessive risk is the evidence of planning, cooperation and coordination, and not just of technological ability. Symbolic behaviour, too, they argue, leaves a detectable signature. The most obvious is self-adornment with beads and ornaments, but it is also evident in the use of pigment, in decorated objects, in burying the dead and in the imposition of style on utilitarian objects. Of course, these crucial human capacities are not instantly recognizable in the human record: they are recognizable only when they have been magnified by history and culture. An innovation will only be recognizable once it has established and spread. We do not see origins in the record, but the cultural effects of innovations as their effects accumulate. We do not see the first instance of an innovation; we see it once it has become a routine feature of the community toolkit. But over time and place, these elements of the ‘modernity suite’ will leave traces. The physical traces of behaviourally modern humans will be different from those left by their more technologically and ecologically constrained ancestors. One crucial problem with the project of reading ancient minds from ancient behaviours is that technology and resource use reflect the local economic landscape as well as cognitive capacity. The techniques used and the resources exploited depend on agents’ abilities but also on relative costs and benefits. These relativities depend on environment and demography. Haim Ofek, for example, suggests that fire keeping was probably the first technical specialization, and points out that such specialization is only possible once market size—a function of demography—reaches a threshold [27]. So if we do not see the systematic exploitation of hard-to-process foods (birds, fish, grain), this might just show that those humans had no need to impose those burdens on themselves, not that they were incapable of carrying them. The ‘broad spectrum revolution’—the extension of the human ecological base to birds, fish, grain—may well be a response to the exhaustion of more valuable resources as populations expanded, signalling new needs, not new capacities [28]. For this reason, it is sometimes thought that symbolic behaviour leaves a more reliable trace in the record than do the capacities for innovation and flexibility. In contrast to these technical competences, symbol use is not a response to immediate environmental demands. Moreover, symbolic behaviour seems to be distinctive


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of a specifically human form of social life. People do not just belong to groups. They recognize themselves as a member of a group; and often treat that fact as a central feature of their lives. Individuals identify with their communities, and identity with their distinctive norms and customs. When agents use symbols that are insignias of their group, or of their place in that group, we know that agents are aware of and identify with their groups. Thus, physical symbols have been identified as the benchmark of behavioural modernity (hence the very recent excitement generated by Joaõ Zilhaõ’s claim to have discovered indisputably indigenous Neanderthal shell jewellery [29]). Symbol use is a sign of a cultural revolution; a transition from coexistence with others to identifying oneself with others. Moreover (the idea goes), the archaeological record suggests that this is a recent development, and so distinctive of recent sapiens populations (and possibly those of our large-brained sister species). Thus, McBrearty and Stringer clearly thinks of symbols as forging a new form of social life when they write: ‘The ability to manipulate symbols is considered an essential part of modern human cognition and behaviour, although definite traces of symbols in the archaeological record are difficult to recognize and are often obscured by the ravages of time. All humans today express their social status and group identity through visual clues such as clothing, jewellery, cosmetics and hairstyle. Shell beads, and haematite used as pigment, show that this behaviour dates to 80 000 years ago in coastal North and South Africa’ [30, p. 793]

Thus, archaeologists have come to focus on material symbols as the distinctive signature of the modern mind, both because symbol use is important in itself and because it is more reliably detected than other elements of the modern cognitive suite. I am sceptical. Insignias of identity and role are not archaeologically transparent. Consider, for example, recent arguments that insignia symbols have quite a deep African history, long pre-dating the Upper Palaeolithic [31 – 34]. The most systematic early examples of possible ‘symbolic behaviour’ are burial of the dead and the use of ochre. But while there is evidence of fairly systematic burial of the dead [24], the significance of this practice is not clear. It is one thing not to treat as refuse the corpse of your father, sister, daughter. It is another to construct a magical narrative about their ongoing significance. In the absence of grave goods, there is no evidence of magical narrative. In short, while burial of the dead is evidence of emotional attachment, it is not evidence of anything else. Ochre, too, is ambiguous in its significance. Ochre may have purely utilitarian purposes: as a preservative, insect repellent or ingredient of glue. But suppose, in some cases, such mundane uses can be excluded. It does not follow that the use of ochre is symbolic, either in the sense of displaced reference, or in the sense of social marking. It could, for example, be used in signal enhancement: making a face, a shield, a person more visible, startling or threatening. Imagine, for example spooking animals by suddenly emerging from cover in a game drive. Signal Phil. Trans. R. Soc. B (2011)

enhancement would make such a tactic much more effective. Kuhn & Striner [35] make a somewhat similar suggestion in the context of interpersonal interactions. Camouflage is another possibility: for example, using ochre to break up contours. This suggestion seems especially relevant given recent reports of Neanderthal use of dark ochres. Moreover, there is good reason to think that the fabrication and use of physical symbols, like other material technologies, is sensitive to demography, economics and social organization. In itself, it is not a direct reflection of social cognition. In an important discussion, Kuhn and Stiner compare ochre and shellbased beads as signalling systems. Ochre significantly precedes the use of shells as beads in the archaeological record; ochre use may be as early as 280 kyr BP [29]. As we have seen, ochre has uses other than human-to-human signalling. So perhaps its use was established before humans regularly altered their bodies and garments to send social signals, and was then exapted as an existing technology to send signals. That may explain why shell-beads, which have no use except as signals, arrive later in the record. However, Kuhn & Stiner show that ochre and shell-based beads have different properties as signals. They suggest that shell-based systems are well-suited for withingroup signals. Shells can be standardized and compositionally organized. Their pattern and placement can itself be a signal, and one that can be duplicated or systematically varied. Having (say) three rows of shells rather than two around one’s neck can be a discrete, regular and repeated signal. As a consequence, shellbead systems have the capacity to encode precise information about rank, role, age, status, gender or even individual identity, just as ornithologists use the sequence of colour bands on a bird’s leg to identify individual birds. But while being potentially precise and rich, such signals have low amplitude: the precise pattern is difficult to see at any distance. Moreover, if the comparison with symbols of rank or identity is apt, the system is both somewhat complex and arbitrary. The significance of a particular array will be obvious only to insiders. In contrast, ochre has a high amplitude. A shield, a face or a garment coloured in a distinctive way is visible and recognizable at a distance. In contrast to shell-bead signals, ochre-based signals would be well-designed to signal group membership or identity to another group. While such signals are arbitrary, they are neither part of a complex system, nor are they displaced in space and time from their referents. They are like national flags, and as with flags, their role could be learned simply and quickly by individuals in other groups. If these considerations are persuasive, the appearance of ochre, beads and the like in the archaeological record is an effect of demographic change. Signals and symbols are not just information: symbols of rank sometimes serve to assert and reinforce hierarchy, not just signal an agent’s place in a hierarchy. But to the extent that material symbols are information-sending systems, in simple social environments they have no function. There are no strangers to inform. This demographic suggestion is supported by the fact that physical symbol making


Review. From hominins to humans emerges at different times in differing sapiens groups [19]. According to the population-structure hypothesis, the appearance of physical symbols of group membership in the archaeological record does not mark the first appearance of people thinking of themselves as members of groups. Rather, it is the invention of advertising. Members of a group only needed to badge their identity—to wear insignias—once their social world became dense. After that threshold, they regularly met others who did not know them as individuals located in a specific network. That transition selected for physically advertising group membership [36– 38]. Beads and similar low amplitude, shortrange signals appear later, as groups become more internally complex, more differentiated and perhaps more hierarchical. Physical symbols, then, are just one fallible indicator of cultural richness. There is no palaeoanthropological golden spike, no material trace left when and only when agents live in social worlds that fall within the modern range. Thus, McBrearty’s approach, treating modernity as a syndrome of capacities, is preferable to one that focuses on material symbols. However, the syndrome is a proxy for a more fundamental cognitive and social phenomenon, or so I shall argue in the next section.

3. A SAPIENT PARADOX? ‘if the genetic basis of the new species (i.e. of Homo sapiens) is different from that of earlier hominids, and of decisive significance, why is that new inherent genetic capacity not more rapidly visible in its effects, in what is seen in the archaeological record? That rather puzzling question may be termed the sapient paradox. It has significant consequences. They become even more obvious if the transition to Homo sapiens is set earlier and relocated to Africa’ [34, p. 72]

It is one thing to identify socio-cultural differences between the first sapiens and those living 150 kyr later. It is another to think that this difference poses a profound explanatory puzzle. Colin Renfrew thinks the puzzle is so profound that it amounts to a paradox: the paradox of explaining why it took 100 000 years for humans to behave like humans. This is a paradox only if it is conjoined with a ‘simple-reflection model’ of the relations between cultures, minds and genes: a model in which cultures reflect the intrinsic capacities of human minds, and these in turn reflect our evolved genetic endowment. Obviously, no-one thinks that the intrinsic structures of the mind determine fine-grained features of culture: they define a range of variation. The particular funeral practices of a group will reflect its idiosyncratic history. But having funeral practices of some kind (rather than, say, letting mum rot where she drops) is part of what it is to be in a human culture. We do not treat the remains of our fellows as debris, and that reflects the intrinsic structure of the human mind. This simple reflection model is explicit in Mark Hauser’s recent opinion piece exploring potential parallels between Chomsky’s theoretical linguistics and theoretical morphology [39]. As Hauser [40] sees it, both research Phil. Trans. R. Soc. B (2011)

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programmes aim to identify innate constraints on individual developmental mechanisms. These in turn define a space of possible variation. Theoretical linguistics characterizes a space of possible human languages. That space is larger than the actual variation but it excludes many readily describable, apparently possible, languages. Likewise, theoretical morphology characterizes (for example) a space of possible skeletons. That space includes many skeletons never found in nature. But it also excludes many that can readily be imagined. Hauser suggests a similar but broader programme for cognitive science: that of characterizing a space of possible human societies—a ‘culturespace’, a space of social organizations compatible with the innate structure of the human mind [39, p. 195]. The simple reflection model is never explicit in palaeoanthropology, but it is often implicit in much palaeoanthropological theorizing. For example, there is an important strand of work on Neanderthal extinction which presupposes that Neanderthal displacement by sapiens must have been owing to some important sociocultural difference between Neanderthal and sapiens groups, and that this sociocultural difference, in turn, was due to an intrinsic cognitive difference between sapiens and Neanderthal minds. For example, Steven Mithen and others have argued that the Neanderthals lacked full human language [21,41–43]. Indeed, the simple reflection model is implicit in the claim that the sapiens paradox is, indeed, a paradox. If ancient sapiens and recent sapiens were genetically similar (as their morphological similarity suggests), and if genetic similarity implies cognitive similarity, which in turn implies cultural similarity, the cultural contrast between our recent and our more ancient ancestors is indeed surprising. Something has to give. One response, guided by the reflection model, is to try to identify a small but important genetic-cognitive difference between behaviourally modern humans and their early sapiens ancestors (perhaps, a difference in cognitive fluidity or language [20,22,44]). However, it is also possible to reject the reflection model: the complexity and organization of human culture is not sharply constrained by innate features of the human mind. Humans act on their material environment. But they also act on their informational environment, and this informational engineering often has important consequences for cognition and culture. In acting on their informational environment, humans sometimes enhance individual cognitive capacity. The invention of numerals, and of systems of numerical notation, enabled humans to think about quantity in ways that were previously impossible [45 – 47]. Material symbols enhance memory, as do various other external prompts [48]. Many important cognitive capacities are like literacy: they exist only in environments in which they are supported. So, individual cognitive capacities often depend on cultural resources that amplify learning capacities. Moreover, informational labour can be divided: in cooperative environments, agents serve as memory and expertise stores for one another, and so individual capacity— innate or acquired—does not sharply constrain cultural complexity. Perhaps the most powerful example is that of the natural sciences themselves. Individuals organized


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and connected in the right way, and only in that way, are a self-improving, accelerating engine of discovery. Science has been made possible in part by making individual scientists smarter (by providing them with cognitive tools), and in part by organizing their collective effort, at and across time, in the right ways. The social amplification of individual capacity is important to adult capacity. But children profit immensely from adult organization of their learning environment. Behavioural modernity is a real and important phenomenon. But it was not a new and especially bright light being turned on in human minds by a sudden but subtle genetic shift in sapiens genomes. Rather, it represents the cumulation of a long trend in hominin evolution. The capacity to retain, and ultimately to amplify, the cognitive resources inherited from the preceding generation became increasingly important. Behaviourally modern humans control, and depend on controlling, impressive amounts of information about their local environment, local natural history and material technology. As Peter Richerson, Robert Boyd and their students have pointed out, life as a forager depends on the control of rich, detailed information, especially in the unforgiving environments in which behaviourally modern humans have flourished [12,49]. The information resources on which these lifeways depend were built gradually and passed on reliably. Ecological and technological adaptability depends on a culture’s capacity to retain an informational bedrock about locally appropriate technology, local resources and dangers; to improve on that base (especially, but not only if conditions change); and to preserve those improvements for the succeeding generation. That ability, in turn, depends both on individual cognitive capacities for teaching and for social learning, and also on an adapted learning environment. As the apprentice model suggests, high fidelity, high bandwidth social learning depends on both individual adaptations and adapted environments. Individual cognitive capacity has coevolved with learning environments. That coevolution has deep roots; its origins long-predate our species. Behavioural modernity, I shall argue, represents a threshold in the bandwidth and fidelity of the cross-generation flow of expertise. At that threshold, human groups can both reliably preserve large information stores, and can recognize and retain incremental improvements in those information stores. The new flexibility of sapiens groups comes from this enhanced capacity to innovate. These changes in the social organization of learning may well have interacted with genetic change. It has become increasingly clear that there has been significant, selected, change in the human gene pool in the life of our species, though the specific phenotypic effects of these gene changes are as yet rarely known [50– 52]. So, gene change may have played some role in the establishment of behavioural modernity. But if so, it was through gradual coevolutionary interaction, and not a sudden genetic trigger just prior to the African Diaspora. On this view, behavioural modernity itself is the collective capacity to retain and upgrade rich systems of information and technique. The specific component signatures of modernity (symbol use, composite tool Phil. Trans. R. Soc. B (2011)

making, ecological breadth and the like) are just fallible indicators of this basic cognitive-cum-cultural capacity. None have special significance in themselves.

4. ACCUMULATING COGNITIVE CAPITAL I suggested above that behavioural modernity is a threshold effect; we see the signal of modernity when a stabilized system of interaction makes the accumulation of cognitive capital reliable. For there is an important distinction between the conditions that allow information to be preserved reliably, and those that allow it to be expanded reliably. This distinction allows us to make sense of the hominin record. That record seems to show three phases: a long phase of mere preservation, a not yet stable shift to expansion and a final phase in which innovations and additions to the communal stock of information are much more reliably transmitted to the next generation; of course, each phase fades into the next rather than terminating crisply. Thus, hominin history began with a very long phase of technological conservatism. Technology did change, but very slowly. Simple chopping tools and flakes emerge approximately 2.6 Ma in Africa and make a first appearance in Europe some time later. Eventually, at about 1.6 Ma, this technology is supplemented with the classic Acheulian handaxe (and perhaps also with worked bone tools [53]). These handaxes are bi-facially flaked, and often have a somewhat standardized ‘tear drop’ shape. Middle Stone Age points begin to appear about 280 kyr BP, and this change may signal the arrival of hafted rather than hand-held tools. These points require not just attachment to a shaft; the points themselves require a two-step manufacturing process. From about 200 000 years ago, technological and ecological traditions become less conservative. There are innovations in this period that anticipate later technological revolutions, but these innovations often seem to fade out. The accumulation of innovation is not yet stable. The final phase, of course, is the signature period of behavioural modernity: innovation, regional variation and expansion into all but the most forbidding habitats and inaccessible regions. One striking element of this pattern is that the pace of innovation is initially very slow. But a second is that (especially over the last 300 000 years or so), change in technological competence is not unidirectional. Technological and ecological innovations appear (and establish over sufficient space and time to leave a trace), but then disappear again. In their reviews, Conard and co-workers emphasize these early appearances of technologies that become signatures of later periods [17,26]. Thus, for example, microliths are regular-shaped, point-like artefacts that are often taken to be a signature technology of behavioural modernity, both because they can be made in regionally distinctive, but still regular, ways and because they are thought to have been mounted on spears or arrows. Hence, they show the capacity to make multi-part artefacts. Yet, Hiscock and O’Connor point out that microliths are found in significant numbers early in one region of the African Middle Stone Age (perhaps 300 – 250 kyr BP) and again late in the


Review. From hominins to humans Middle Stone Age (as part of the Howieson’s Port industry; perhaps 70 kyr BP). So microliths are found before the establishment of paradigm, behaviourally modern cultures but patchily in space and time. So, perhaps sometime between 300 and 200 kyr BP, hominin culture became cumulative in two senses. The volume of culturally mediated learning increases: a larger range of hominin action owes its character to intergenerational social learning. Thus, the range of materials expands (including ochre, bone, antler, ivory). There was an increase in the variety of tools used, in part because technology took on new functions. It was used to make material symbols, to make other artefacts (awls and needles were used to make clothes), in shelter construction and the organization of domestic space [54], and in making clothing [55]. Hominins expanded the range of resources they exploited [56]. Moreover, at some point in hominin evolution, children came to learn the norms and customs of their community, not just the local techniques for making a living. Human behaviour became more diverse and less stereotyped, in ways that were guided by information flows from the preceding generation. The bandwidth of cultural learning expands. But culture transmission gradually becomes cumulative in a second sense as well, permitting the stepwise improvement of specific technologies. For example, fire almost certainly was domesticated in stages, beginning with the maintenance and exploitation of natural fire; probably followed by the development of techniques for making fire portable. These important breakthroughs were followed by ignition technologies and improvements in the control and use of established fire, in hearths and the like [27,57]. Stepwise improvement requires high-fidelity transmission. In the hominin record, the expansion of bandwidth seems to be roughly correlated with increasing fidelity (assuming that more complex technologies depend on higher fidelity), and behaviourally modern cultures depend on both high fidelity and expanded bandwidth. Behavioural modernity probably depends both on an increase in the rate of innovation, as individual humans come to deliberately intervene on the world in ways guided by their increasing understanding, and by improved preservation and amplification of successful innovation (see [58] for a nuanced discussion of the interplay between deliberate innovation and population level processes of preservation). So we need an explanation of both aspects of cultural accumulation. Cross-generational information flow does not in itself require specific adaptations for cultural learning. In their Animal Traditions, Avital & Jablonka [14] show that traditions can begin with a lucky accident, with an innovation that is profitable enough to result in adults changing their behaviour to take advantage of their luck. In those species in which the young stay with their parent(s), this lifeway reorganization will have a side effect: the young will come to explore an environment much richer in opportunities to repeat the accident. The improbable in the first generation becomes likely in the second. Traditions in using Oldowan technology might well establish in this way. If making sharp flakes and cores gave the early users of that technology access to (say) carcasses and marrow, Phil. Trans. R. Soc. B (2011)

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the juveniles accompanying those adults would have many chances to acquire stone-working skills through undirected exploration and play. There is archaeological evidence that making and using Oldowan tools was a frequent, regular activity rather than an occasional one. For some sites, cores show signs of heavy, repeated use [59, p. 2]. Crucial information can flow reliably from one generation to the next, even without distinctive adaptations for social learning. Almost certainly, though, early hominins inherited cognitive capacities from their last common ancestor with the chimpanzee clade, capacities that primed them for the uptake of simple stone technologies. Studies of the living great ape species indicate that the earliest hominins were equipped with some of the motortechnical capacities that make stone tool making possible and that they were persistent and effective trial and error learners. Moreover, these studies also suggest that these early hominins had some capacity for cross-generation social learning, through some mix of emulation, coarse-grained imitation and stimulus enhancement [59 – 61]. So, while there can be information transmission across the generations without adaptation for social learning, almost certainly juvenile hominins noticed adults making and using tools, and responded adaptively to that experience. So the earliest hominins were able to retain a core of technological and foraging skills. But the conditions that allow accumulation are much more onerous than those that merely allow preservation of a few key skills, and early hominin technologies probably did not depend on high-fidelity social learning. Consider, for example, the signature technology of the erectus-grade hominins, the Acheulian handaxe. Acheulian tool-making probably did not depend on the cross-generational transmission of high-fidelity information about the tool itself. As McNabb and co-workers note in their detailed case study of one specific site, there is little evidence of standardization of group norms governing hand axe design. There is plenty of variability in both shape and degree of symmetry. Indeed, many handaxes show little symmetry [62]. The overall record is complex, for some sites seem to show more constrained variation [63]. Moreover, there is some evidence of local clustering in handaxe shape, giving rise to regional patterns in variation. But even on sophisticated multi-dimensional analysis, these local groupings are not strongly marked: there is roughly a 70 per cent chance of assigning a handaxe to its source of origin, but 60 different variables needed to be measured to assign artefacts to regions with that accuracy [64]. Social learning affects process as well as product, so highfidelity social learning may have been important to the transmission of manufacturing techniques, for it was necessary to know how to produce large blanks from source material, which could then be shaped into a large cutting tool. But there is no reason to suppose that high-fidelity social learning controlled the shape of the tool itself. The most plausible picture is that the general idea of a large cutting tool plus some techniques for tool-making were transmitted socially, with the help of some capacities for social learning and an organized learning environment [62].


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Thus, cultural transmission has had an increasing footprint in the hominin record, a trend culminating in behaviourally modern cultures. I suggest that this trend is due to three interacting factors. One, uncontroversially, is the evolution of minds increasingly well-adapted for culturally learning and, ultimately, teaching (see, for example, [65] for a summary of human communicative adaptations). But while these adaptations are probably necessary for the stability of behaviourally modern cultures, they are not sufficient. As Tehrani & Riede [66] remark, the manual skills required for many traditional craft skills are extraordinarily intricate, and they would be very difficult to master by, for example, imitation learning, even by agents well adapted for such learning. Yet, often such skills are transmitted so reliably that characteristic products reappear recognizably for many generations. Apel [67], for example, details intricately made Neolithic stone daggers from Scandinavia made to a design that was transmitted for at least 24 generations. Tehrani & Riede are right to doubt that such intricate patterns could be transmitted by unsupported imitation, arguing that such cases show the historical depth of active pedagogy. I agree, but teaching often has its effects through structuring the learning environment rather than by direct instruction. So behaviourally modern culture depends on the construction of adapted learning environments; the young come to explore and act in a world that supports and directs learning. This, I shall argue, culminates in something like apprentice learning. A third factor is the changing demography of hominin populations; as we shall see, small population sizes make it harder to maintain and expand informational resources. Moreover, there is likely to be positive feedback between local population size and the volume of cultural learning: innovation increases carrying capacity, allowing growth, which supports specialization and buffers crucial skills against accidental loss [68]. Apprentice learning is a good model of the ways learning environments are organized to make possible the transmission of a high volume of information with high fidelity. These learning environments can evolve gradually, beginning with juvenile interest in parental activities, and parental tolerance of their inquisitive exploration. From that platform, there can evolve both increasingly sophisticated individual adaptations for social learning, and increasing adult support of learning. This form of learning is sufficiently powerful to explain the observed phenomena—the maintenance of complex, demanding skills in populations without literacy or formal educational institutions. A skilled cabinet maker (for example) has absorbed an enormous amount of information and skill from his/her teachers. An apprentice obviously brings to the learning environment a complex set of individual cognitive adaptations: physical skills, theory of mind, joint attention, conditional reasoning, observation learning. Most apprentices acquiring complex skills benefit from explicit advice and instruction (though there seems to be enormous cultural variation in the extent of explicit teaching), and a good deal of information comes from the observation of expertise in action. Often, those learning share information too, about both failure Phil. Trans. R. Soc. B (2011)

and success. But most learning is hybrid: apprentices mostly learn through socially structured trial-anderror learning. They are surrounded by tools, by partial and complete products and the occasional failure, and by raw materials in various stages of processing. They learn on the job, but they are assigned jobs by those who understand how much or little they can do. So their trial-and-error learning often involves structured trials. Skilled craftsmen assign tasks that they judge to be within, or close to, their current capacity. Those tasks build foundations for more complex skills. The overall result is that apprentice learning systems combine high fidelity with large bandwidth. Moreover, the apprentice learning model is ethnographically and archaeologically plausible. In foraging societies, extensive explicit instruction does not seem to play a prominent role in the acquisition of hunting skills. But children are provided with informational resources. For example, they are provided with miniature hunting weapons [69]; they are sometimes taught how to make the tracks they must follow (see [70, pp. 166 – 176] for series of photos of aboriginals making pseudo-tracks). They learn games that rehearse key physical skills. They accompany adults on hunts, and these are sometimes reorganized to make this possible [16]. And while there may not be much explicit instruction, they are exposed to an enormous amount of hunting lore [71,72]. They have access to the expertise of those with the relevant skills; they have the time and opportunity to practice, and that practice is guided. Indeed, there are some cultures in which hunting skill is passed on though something like explicit apprenticeship [73]. In these cases high-fidelity, high-bandwidth social learning depends both on an organized and adapted learning environment and on specific cognitive adaptations. Likewise, there is significant anthropological documentation of the acquisition of craft skills in apprentice-style situations. Apprentice transmission of weaving traditions are documented from a range of cultures, though these are often family-based, mother – daughter lineages [66, pp. 321 – 322]. Lave [74] discusses two examples in some detail: apprentice tailors in Liberia and the study of Islamic law in nineteenth century Cairo. These examples are important because they document the flexibility of apprentice learning and teaching: it supports the acquisition of much more than manual skill. Liberian apprentice tailors learn about the social and economic organization of a tailor’s life, not just how to make trousers. Islamic law is not a manual skill, but it is not just a textual skill either. The student learns about the social and institutional organization of Islamic courts, not just about the texts, from being immersed in those institutions. It is obviously more difficult to reconstruct the social organization of teaching and learning in extinct cultures. Tehrani & Riede [66] suggest that a detailed analysis of the life history of artefacts can identify artefact traditions: continuity in form over time that is not owing to the constraints imposed by raw materials and function. Likewise, Bamforth & Finlay [75] develop criteria for identifying highly skilled stone work, and also less-skilled work that is likely to be the result of


Review. From hominins to humans novice practice. In favourable cases, these methods will expose high-fidelity, high-volume social learning in former social worlds. They document the importance of social learning. But by themselves they do not reveal the social organization or cognitive preconditions of such learning. However, there are occasional archaeological symptoms of an apprentice-like organization of craftsmanship. For there are artefacts that appear to have been produced collaboratively, with an expert guiding or helping the less expert. Inexpertly made stone tools sometimes show signs of expert repair or improvement. More systematically, Patricia Crown [76] has demonstrated collaboration between the expert and inexpert in pottery making, both ethnographically and archaeologically, with expert potters often controlling the most difficult parts of the construction process, leaving the less expert (often children) to complete the routine parts. For example, experts lay down the basic design that children then paint in. Moreover, the size and organization of the local community is also extremely important to its capacity to retain and to accumulate information. As Haim Ofek [27] has noted, a larger market size allows more specialization and more division of labour, both of which impact positively on a group’s informational resources. A small group will not be able to afford a specialist firekeeper or bow maker; a medium-sized or large group, perhaps, can. They will have enough customers to support specialization. Specialists typically have higher skill levels, and hence set a higher bar for the next generation. Moreover, a more diverse group with a varied skill set is more likely to innovate than a small, more homogeneous group. Those who specialize in a craft are the most likely to find an improvement in it, and innovation through cross-fertilization is more likely as the overall skill base becomes more diverse and extensive. Specialists may also be more accurate in filtering unsuccessful innovation, and as Enquist & Ghirlanda [77] show, filtering is essential if culture is to become cumulative. Second, redundancy plays a critical role in buffering the group’s informational resources. Larger groups store information in more heads than smaller ones. Information can easily drift out of a small group, through unlucky accidents to those with rare skills (see [78], though in response see [79,80]). In addition, redundancy may play a second role in compensating for low-fidelity cultural learning. Modern humans are clearly individually adapted for social learning [81– 83]. But Richerson and colleagues doubt that these adaptations suffice for high fidelity, and argue that the social environment compensates for low fidelity through redundancy. Naive agents have many opportunities to acquire specific skills and critical information, and they develop models to show that redundancy—for example, a naive agent using many models rather than a single model—can compensate for low fidelity one-on-one learning. Thus, so long as there is sufficient redundancy, with members of a population connected in the right ways, a population can preserve its informational resources in transmission to the next generation through low-fidelity channels [12,84– 86]. Phil. Trans. R. Soc. B (2011)

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However, while demographic factors are important in the establishment of behaviourally modern cultures, demographic expansion alone does not explain the acceleration of innovation. Redundancy allows low-fidelity transmission to preserve informational resources, allowing already established and widespread skills to be copied via multiple trials to the next generation. But such mechanisms will not allow small, incremental improvements to existing techniques to be preserved, copied to the next generation and spread to be the foundation for further improvement. This claim is somewhat controversial. Henrich has developed redundancy-based models with accumulation despite low fidelity [78], models which have recently been extended [87]. But the conception of skill on which Henrich’s model depends is not psychologically plausible. He models the information structure underlying a capacity or skill as a continuous quality. The product of a skill may often be a quantity of some kind: hunting success; the robustness of a pot; the power of a bow. Indeed, we often use those products to measure a skill: in an archery competition, for example, we use a product of the skill—the number of arrows on target— as its measure. But the systems of information and capacity on which those products depend are not continuous quantities. To see this, consider the challenges involved in learning such a skill. The skills of an artisan are hard to master, but that is not because there must be some measurement error while trying to match a quantity. Rather, it is because the informational basis of skill is only partially manifest in any particular act. A specific, somewhat stereotyped motor skill might be modelled, to a first approximation, as a quantity. But a skilled artisan can respond effectively to a range of different circumstances, demands and materials. That is part of skill. A kayak-maker does not manifest all his skills in making any one kayak. An expert flint knapper responds appropriately to variation in raw materials and in functional demands. Stone tool making is not stereotyped in the way, say, a tennis serve (Henrich’s example) might well be. These models make a convincing case for the importance of demography. Moreover, Powell, Shennan and Thomas’s extension of Henrich’s work shows that the models are robust, and that the parameter values that predict accumulation map quite plausibly onto estimates of human populations just prior to the establishment of behavioural modernity. But these extensions retain the oversimplified picture of the relationship between a capacity and its underlying informational basis. So while they show that demography plays a crucial role in the establishment of behavioural modernity, so too does high-fidelity learning. In general, low-fidelity learning plus redundancy is not enough for accumulation. In summary, then, the cultural learning characteristic of the Upper Palaeolithic transition and later periods of human culture—social transmission with both a large bandwidth and sufficient accuracy for a ratchet of improvement— requires individual cognitive adaptations for cultural learning, highly structured learning environments and population structures that both buffer existing resources effectively and which support enough specialization to generate a supply of innovation.


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There were no medieval craft guilds in the Upper Palaeolithic, though the adze-making traditions of Neolithic New Guinea are strikingly convergent on that social practice [88]. But if the model developed in this paper is correct, information-rich, expertisedependent, forager lifestyles depended on a similar combination of an organized learning environment and specific adaptations for social learning. The pulse of cultural and technological innovation that is most dramatically visible in the archaeological record in the Upper Palaeolithic revolution is a signal of such a social world: a social world which makes possible high-fidelity, high-bandwidth transmission across the generations. Individuals in these social worlds were equipped for social learning. But they depended on an adapted environment, as well, and on populations which spread risk and supported specialist expertise. The persistence of these lifeways depended on highly skilled agents sharing their expertise and on the reliable replication of the learning environment in which crucial expertise was acquired. This combination, and only this combination, allowed cognitive capital to be accumulated and behaviourally modern cultures to emerge.

5. TESTING THE MODEL No-one doubts that the evolution of enhanced social learning was one of the most distinctive features of hominin evolution, and that it was one important factor driving the increasing phenotypic difference between the hominin and the chimpanzee clade. This paper has tried to identify that evolutionary trend more precisely, especially its culmination in behaviourally modern culture. Further, it develops a model of the evolutionary preconditions of behavioural modernity. Individual cognitive adaptations for learning and teaching were doubtless important, but not in themselves sufficient. An adapted learning environment—best understood as apprentice transmission—and a favourable demographic profile were also necessary. But it is one thing to advance a plausible model, another to test it. So how can the model be turned into a testable hypothesis about the origins and establishment of behavioural modernity? Archaeology, ethnography and experimental psychology can be combined to test the model, though only in preliminary ways. The most obvious test is archaeological: comparing the predictions of the niche construction model of behavioural modernity with alternatives. One alternative is Peter Hiscock and Sue O’Connor’s suggestion that the supposed ‘sapiens paradox’ is a pseudo-problem created by preservation biases. They suspect that there was no qualitative difference between first sapiens cultures and those of 50 kyr BP. Smaller groups use fewer artefacts, and so their immediate archaeological footprint is smaller, even in those places were they were found, and they were found in fewer places. Moreover, the older the site, the more likely it is to be degraded. Even so, if there is no qualitative difference in cultural complexity between the first sapiens peoples and those of the later Pleistocene, the apparent gap should steadily close in the face of increasing sampling, and by Phil. Trans. R. Soc. B (2011)

correcting for sampling biases in comparing records. A (approximate) steady-state model can also be tested against the record of more recent cultures (like those of Ancient Australia) where preservation problems may be less formidable. On the niche construction view, there is a genuine difference between stabilized high-fidelity, high-volume cultures, their ancestors and some successors. So the apparent difference should persist in the face of increased sampling effort and bias correction. The most prominent alternative to the niche construction model is Richard Klein’s genetic-pulse hypothesis. In contrast to Klein’s picture, the niche construction model does not predict a unidirectional increase in the capacity to mobilize informational resources, even after the fundamental genetic capacities essential to that mobilization have evolved. For the developmental environment is critical, and subject to multiple routes of disturbance. Nor do we find a unidirectional pattern. So, for example, it has recently been argued that behavioural modernity appears to arrive gradually, with its elements not tightly coupled, in multiple locations, and perhaps incipiently in Neanderthals as well as sapiens [17,19,24,26]. Richard Klein continues to resist the idea that there are convincing early examples of modern-like behaviour. Moreover, he argues that population pressure models are the only alternative to his genetic breakthrough hypothesis, and notes that they face serious challenges: (i) population pressure models owe us an account of how the need for innovation generates the capacity to innovate; (ii) population pressure models need to explain why hominin populations expanded prior to the acquisition of new skills and capacities; (iii) in the crucial period in Africa (100–50 kyr BP), there is no independent evidence of an increased human population or increased ecological footprint [20,89]. While these are serious problems for population pressure models, the apprentice learning model does not depend on population pressure to explain the onset of behavioural modernity. The crucial factor is the size of, and interactions within, the local group, not the ecological footprint of the metapopulation on the landscape’s resources. Suppose that Klein is right to discount ancient signals of apparently modern behaviour, Hiscock & O’Connor point out that the apparent disappearance, then return, of signs of modernity in the record after 50 kyr BP is an equally serious challenge to the genetic switch model of behavioural modernity. A one-factor genetic-switch model cannot explain the variability in the signs of modernity that postdate the switch. If additional demographic, cultural or genetic factors are added to the genetic switch model to track variability, the genetic switch itself becomes redundant. In short, the genetic switch model seems to predict a qualitative change in cultural complexity somewhere around 60 000 – 50 000 kyr BP, followed by a new, higher equilibrium. Arguably, the data do not support the sudden upward shift. But perhaps they do not support the idea that there was a higher equilibrium, either. For this reason the Australian archaeological record is an informative lens through which to view the interaction of individual cognition with collective capacity.


Review. From hominins to humans The initial expansion of humans into the Sahul about 45 000 years BP could not have been accidental. These humans had the capacity to plan and cooperate. Moreover, they had technology complex enough to cross significant stretches of ocean [90]. However, before the Last Glacial Maximum, 20 kyr or so ago, the archaeological record resembles that of Middle Stone Age Africa. So for the first 25 000 years of their occupation, the first Australians seem to have had a limited technological toolkit; exploited a narrow resource band; and showed limited signs of symbolic culture. Eventually, the standard symptoms of behavioural modernity do appear. But as in the African case, the archaeological signatures of behavioural modernity do not appear together in space and time. Ochre use and burial of the dead is relatively early, as is the use of freshwater shellfish (perhaps 40 kyr BP). There are beads from about 35 kyr BP. But the first signs of marine shellfish exploitation and bone tools, and cave art with recognizable motifs are all much younger. Moreover, the lithic toolkit stays quite simple until the Holocene (see [91, p. 211, fig. 9]). Only over the last 20 000 years, do we consistently see the usual archaeological signatures of behavioural modernity: broad-range foraging; environmental management; technological innovation; and obvious symbolic culture [36,92,93], though it is possible that this too is a sampling effect [25]. Allen & O’Connell [90] interpret this record as showing that people can be behaviourally modern without showing that they are behaviourally modern. To arrive at all, they must have been technologically and ecologically flexible, but as a consequence of environmental and demographic factors, modernity left no trace for upwards of 25 kyr. O’Connell & Allen do not consider the idea that Australians ceased to be modern after they arrived; nor do Habgood & Franklin. Neglecting this possibility makes sense if we think modernity is coded and canalized in individual genomes, if it is an attribute individuals have largely independently of their cultural environment. But it makes no sense if behavioural modernity is partially dependent on the organization of social life—a social life that would have changed fundamentally as small numbers of people dispersed into an enormous landscape. The communal resources available to very small groups dispersed over enormous and inhospitable distances would be very different to those available to communities based on the fertile islands and shallow seas of southeast Asia. Quite likely, informational resources were buffered less well, and group size was too small to support much specialization, depressing innovation. On the niche construction model but not genetic switch models, behavioural modernity can be lost as well as gained, and losses should be detectable in the record. In short, we have three different predictions. The Hiscock – O’Connor suggestion (it is no more than that) predicts an approximate steady state, discounted by preservation biases and the effects of group size. There is no qualitative upward trend in cultural complexity before the Holocene. The niche construction model does predict such a trend, but it is potentially fragile, so interruption and reversal is possible. Phil. Trans. R. Soc. B (2011)

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The gene-switch model predicts a sharp upward shift, once the gene has spread through the population, followed by a stable, higher equilibrium. In principle, ethnographic data can test the model. The model predicts that crucial skills are acquired by socially supported trial-and-error learning: adults with expertise are actively involved in juvenile learning. However, the form of that involvement will vary by culture and by skill, for the core skills of small-scale societies were very varied. They included: stone technology; fire and fire management; woodworking; the use of skins and other materials for clothes and covering; making shelters; folk medicine; tracking and hunting skills; natural history expertise; and (eventually) weaving and pottery. These skills vary in their transparency to reverse engineering; their transparency to observational learning techniques; the ease with which stepwise improvement is possible; the precision needed in production (their error tolerance); the cost of raw materials and hence the cost of experimentation; and the risks of failed trials. So we would expect the mix of explicit instruction, supervised experiment and support by the provision of tools, raw materials and exemplars to vary from case to case. But we do not expect to find ethnographic evidence that core skills are acquired by independent trial-and-error learning. Nor de we expect to find them acquired by instruction alone. Moreover, the model predicts differences between skills that are transmitted vertically, within families, and those that are transmitted communally, with many-tomany transmission. Communal transmission buffers skill acquisition by spreading risk, and perhaps allows a higher rate of accumulation, if the most skilled members of the community serve as models for the next generation. In practice, ethnographic data is at best suggestive. There are a few admirable case studies [15,88]. But there is simply not enough systematic, broadly based data. For example, Katharine McDonald’s admirable survey of forager skill acquisition has almost no information about making hunting equipment, for almost all hunting was done with store-bought equipment. Hunting with dogs and guns changes the skill base needed for hunting too, so it is far from clear that we can project information about near-contemporary foraging people back into the past. There is some prospect of supplementing ethnographic and archaeological data by experiment. It is still early days for experimental work on fidelity, bandwidth and accumulation in social learning (for a review, see [94]). But there is already suggestive work on the diffusion of technique in humans and great apes. While the results are far from conclusive, they suggest that both emulation and imitation play important roles in social learning and that, at least in some simple cases, imitation may not be necessary for accumulating improvement [59,61]. For example, Christine Caldwell and Ailsa Millen, in experiments using paper plane construction as the target skill, found that reverse-engineering the product was sufficient to learn and sometimes improve designs. Improvement was possible when naive subjects were allowed to examine finished planes, even when they never saw them being made [95]. As they note,


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paper planes are a simple technology, with the design often being obvious from the product, so this result may not generalize to many other cases. The ideal experiments, then, would combine ethnographic and archaeological data identifying those techniques that seem to persist stably, perhaps using the criteria discussed in Tehrani & Riede [66], with an experimental programme. That programme would probe the learning environments necessary and sufficient for those techniques’ acquisition. The niche construction model predicts, of course, that without rich and extensive scaffolding, core skills are not transmittable. Unfortunately, very serious logistical problems prevent implementation of this ideal. Informal report suggests that, for example, advanced stone tool working skills take many years of intensive practice to acquire [67]. That is just as the model predicts, but it follows that direct experimental study of complex skill transmission is not tractable. The hope is to decompose complex skills into relatively independent constituents, whose acquisition can be studied in experiments of reasonable duration. In brief, the model is partially testable against both archaeological and ethnographic evidence, but not in very rigorous ways. Greater rigour is possible, if ethnography and archaeology can be used to identify target skills, and if those target skills can then be decomposed into component capacities whose transmission conditions can be studied experimentally.

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Research

Runaway cultural niche construction Luke Rendell*, Laurel Fogarty and Kevin N. Laland School of Biology, University of St Andrews, Bute Building, Westburn Lane, St Andrews, Fife KY16 9TS, UK Cultural niche construction is a uniquely potent source of selection on human populations, and a major cause of recent human evolution. Previous theoretical analyses have not, however, explored the local effects of cultural niche construction. Here, we use spatially explicit coevolutionary models to investigate how cultural processes could drive selection on human genes by modifying local resources. We show that cultural learning, expressed in local niche construction, can trigger a process with dynamics that resemble runaway sexual selection. Under a broad range of conditions, cultural niche-constructing practices generate selection for gene-based traits and hitchhike to fixation through the build up of statistical associations between practice and trait. This process can occur even when the cultural practice is costly, or is subject to counteracting transmission biases, or the genetic trait is selected against. Under some conditions a secondary hitchhiking occurs, through which genetic variants that enhance the capability for cultural learning are also favoured by similar dynamics. We suggest that runaway cultural niche construction could have played an important role in human evolution, helping to explain why humans are simultaneously the species with the largest relative brain size, the most potent capacity for niche construction and the greatest reliance on culture. Keywords: niche construction; cultural transmission; gene – culture coevolution; human evolution; spatially explicit models

1. INTRODUCTION In recent years, there has been increasing recognition of the significance of niche construction, the capacity of organisms to modify natural selection in their environment and thereby act as co-directors of their own, and other species’, evolution [1,2]. Examples of niche construction include animals manufacturing nests, burrows and webs, and plants modifying nutrient cycles. The defining characteristic of niche construction is not a modification of the environment per se, but rather an organism-induced change in the selective environment; hence the term includes migration, dispersal and habitat selection, where organisms relocate in space and experience new conditions, as well as traits that have a negative effect on the constructor’s fitness, such as habitat degradation [2]. Genetic and ecological models have demonstrated that niche construction can affect evolutionary outcomes, even without culture [2 – 6]. For instance, niche construction can fix genes that would otherwise be deleterious [3,4], allow the persistence of organisms in inhospitable environmental conditions that would otherwise lead to their extinction [6], and be favoured even when costly because of the benefits that will accrue to distant descendants [7]. However, mathematical models reveal that niche construction due to

cultural processes can be even more potent than gene-based niche construction, and demonstrate that cultural niche construction can modify selection on human genes with resulting effects on evolutionary outcomes [2,8– 11]. Indeed, human niche construction is informed by a uniquely potent and cumulative cultural knowledge base [2,12]. It is highly probable that human cultural niche construction has co-directed human evolution [8,10, 13–15]. In the last 100 kyr, humans have spread from East Africa around the globe, experienced an ice age, begun to exploit agriculture, witnessed rapid increases in densities, domesticated hundreds of species of plants and animals, and, by keeping animals, experienced a new proximity to animal pathogens [15]. Each of these events represents a major transformation in human selection pressures, and all (except the ice age) have been self-imposed. Humans have modified selection, for instance, by dispersing into new environments with different climatic regimes, devising agricultural practices or domesticating livestock. Niche-construction theory leads to the expectation that gene–culture coevolution has been a general feature of human evolution [15]. This perspective is reinforced by analyses of data from the human genome, which have revealed numerous genes that have experienced recent positive selection, many of which exhibit functions that imply they are responses to human cultural practices [15–21]. For instance, several lines of evidence demonstrate that dairy farming created the selective environment that favoured the spread of alleles for adult lactose tolerance


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[22–26]. Similarly, Perry et al. [27] found that copy number of the salivary amylase gene (AMY1) is positively correlated with salivary amylase protein level and that individuals from populations with high-starch diets have, on average, more AMY1 copies than those with traditionally low-starch diets. Higher AMY1 copy numbers and protein levels are thought to improve the digestion of starchy foods, consumed at elevated levels by agricultural populations, and may buffer against the fitness-reducing effects of intestinal disease. The transition to novel food sources with the advent of agriculture would appear to have been a major source of selection on human genes, and several genes related to the metabolism of protein, carbohydrates, lipids and phosphates show signals of recent selection [16,17,21,28]. In turn, agriculture and the domestication of animals is known to have facilitated the spread of crowd diseases and zoonoses, generating selection for human genes that confer resistance to these diseases in regions where they are prevalent [16–18,20,29,30]. Cultural niche construction could also have selected for enhanced cognitive capabilities, and many of the alleles subject to recent selection are known to be expressed in the brain [15–17]. Estimates for the number of human genes subject to recent rapid evolution range from a few hundred to two thousand; Williamson et al. [21] conclude that as much as 10 per cent of the human genome may be affected by linkage to targets of positive selection. While, in the vast majority of cases, it is not known what phenotype was the target of the inferred selection, nor which environmental conditions favoured such phenotypes, human cultural practices remain primary candidates, and geneticists are increasingly considering culture as a source of selection on humans [31,32]. One of the best-researched cases is the haemoglobin S allele (HbS), famous as a textbook case of heterozygote advantage, since it provides protection against malaria in the heterozygote form. Durham [22] studied populations of Kwa-speaking agriculturalists from West Africa, who cut clearings in forests to grow crops, often yams. The removal of trees had the effect of inadvertently increasing the amount of standing water when it rained, which provided better breeding grounds for malaria-carrying mosquitoes, which intensified selection on HbS. The fact that adjacent populations whose agricultural practices are different do not show the same increase in allele frequency supports the conclusion that cultural practices can drive genetic evolution. Moreover, this example illustrates how it may be necessary for models to take account of the frequency of resources modified through human niche construction (in this case, the amount of standing water) if they are to capture coevolutionary dynamics accurately. Human agricultural practices are tied to specific spatial locations, and the selective feedback on human genes resulting from such practices, whether related to diet, disease resistance or morphology, is likely to covary in space with the incidence of the practice. Accordingly, there is a need for spatially explicit models with which to better understand how some human cultural processes have interacted Phil. Trans. R. Soc. B (2011)

with human genes during recent human evolution, while simultaneously tracking the frequency of relevant resources [26]. While there has been extensive modelling of human gene –culture coevolution [15,33 – 39], thus far spatial effects have been comparatively neglected. However, the introduction of spatial structure and stochasticity in finite populations is known to affect evolutionary outcomes when compared with non-spatial models [40 – 42]. Moreover, spatially explicit models of gene-based niche construction have revealed that niche-constructing traits can drive themselves to fixation by creating statistical associations with the recipient traits they favour [5]. Niche-constructing alleles expressed in the modification of local resources transform environmental conditions to favour some genotypes, and provided mating and dispersal is local, the niche-constructing alleles can hitchhike across a landscape to fixation. Here, we develop spatially explicit gene – culture coevolutionary models to explore the interaction between local cultural niche construction and genetic evolution. Our aim was to explore whether interactions between cultural traits and alleles mediated by niche construction can create the conditions under which runaway selection can lead to evolutionary outcomes that can overcome external natural selection. We therefore investigate whether, and under what circumstances, cultural niche-constructing practices can ‘run away’ with genetic variation, and to what extent this dynamic is affected by (i) cultural transmission biases operating against the nicheconstructing trait, (ii) the cost of cultural niche construction, modelled as a viability deficit to the cultural practice, and (iii) a viability cost to the genotype favoured by cultural niche construction. We also consider (iv) whether genetic variation enhancing the capability for cultural niche construction can be favoured by this runaway dynamic. Our analysis concentrates on three questions: 1. Can a culturally transmitted niche-constructing practice become universal, even when costly, through statistical association with a genetic trait it favours? 2. Can cultural niche construction generate selection for costly genetic traits that confer improved ability to cope with, or exploit the products of, said niche construction (e.g. genes expressed in disease resistance, or an expensive digestive protein)? 3. Can cultural niche construction favour the secondary hitchhiking of costly capabilities at other loci which confer more powerful niche-constructing abilities on the bearer (e.g. bigger brains)?

2. METHODS Our model marries the spatially explicit individualbased methods of Silver & Di Paolo [5] with the gene – culture coevolutionary analysis of Laland et al. [8]. The model therefore draws on simpler, wellunderstood systems to provide a foundation for exploring these complex coevolutionary processes.


Runaway cultural niche construction We consider a finite population of diploid individuals. We focus initially on a single diallelic resourcedependent locus, A, with alleles A and a, and a single two-state cultural niche-constructing practice, E, with variants E and e, but add a further genetic locus, B, for later analyses. Following Silver & Di Paolo [5], individuals are arranged in an n n square lattice with wrap-around (toroidal) boundaries. Each lattice point (i, j) is occupied by a single individual with phenogenotype fAij,Eijg and has an associated, local environmental resource frequency fRijg. Each individual has eight nearest neighbours (its Moore neighbourhood). Alleles make a contribution to fitness that is in part a function of the local resource frequency. Resource frequencies are subject to change as a result of (i) the niche-constructing activities of individuals in the population and (ii) independent processes of depletion and renewal. An individual’s capacity for niche construction depends on the cultural practice deployed, with E individuals exhibiting niche construction, and e individuals exhibiting no niche construction. As in Laland et al. [8], if pt21(E) is the frequency of the trait E in the population at time t21, the amount of the resource, R, at time t is given by Rt ¼ l1 Rt1 þ l2 pt1 ðEÞ þ l3 :


Table 1. Phenogenotype fitness functions to explore the evolution of costly cultural niche construction (a is the selection coefficient operating on the cultural practice E).

AA Aa aa

E

e

w11 ¼ a þ 1R pffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi w21 ¼ a þ 1 Rð1 RÞ w31 ¼ a þ 1(1 2 R)

w12 ¼ 1 þ 1R pffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi w22 ¼ 1 þ 1 Rð1 RÞ w32 ¼ 1 þ 1(1 2 R)

Table 2. Phenogenotype fitness functions to explore the evolution of a costly capability to exploit cultural niche construction. Here, Rt ¼ l1Rt21 þ l2u þ l3, and u is the frequency of AE. genotype

fitness

AA Aa aa

w11 ¼ h þ 1R pffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi w21 ¼ 1 þ 1 Rð1 RÞ w31 ¼ 1 þ 1(1 2 R)

the three genotypes are based on Laland et al. [8] as follows: fAA ¼ h1 þ 1R; pffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi fAa ¼ 1 þ 1 Rð1 RÞ;

ð2:1Þ

Here, l1 is the coefficient of independent depletion; l2 is the coefficient of positive niche construction, corresponding to niche-constructing activity that increases R (we consider only positive niche construction here); and l3 is a coefficient of independent renewal. Following Silver & Di Paolo [5], a scalar version of this equation is applied at each lattice point. At any particular lattice point, p(E) takes one of the values f0, 1g corresponding to the two possible cultural states, respectively fe, Eg. Local resource frequency is thus a function of independent processes of depletion and renewal, and of the cumulative effect of local niche-construction activity over preceding generations. Following Laland et al. [8], we assume that 0 , l1, l2, l3, l1 þ l2 þ l3 1, so that the local resource frequency, Rij, can take any real value between 0, corresponding to a complete absence of the resource, and 1, corresponding to resource ‘saturation’. Unless otherwise specified, these parameters were set to l1 ¼ 0.7, l2 ¼ 0.2 and l3 ¼ 0.1 in the simulations we report here. These values mean that we assume a resource that depletes in the absence of niche construction to an equilibrium of l3/(1 2 l1) ¼ 1/3. For example, in the case of the aforementioned Kwa, the amount of standing water is a function of independent renewal (i.e. rainfall), independent depletion (e.g. evaporation, runoff, absorption) and niche-constructing activities over multiple generations (e.g. planting crops, which reduces absorption and thereby increases standing water). All variables and coefficients are dimensionless. We allocate fitnesses to combinations of genotype and cultural practice, henceforth ‘phenogenotypes’, as specified in tables 1 – 3, which are tailored to addressing questions 1 – 3 above. Genotype fitnesses depend both on resource frequency and on selection from an external source. In all models, the baseline fitness of

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and

ð2:2Þ

faa ¼ h2 þ 1ð1 RÞ;

where R ¼ Rij, the resource frequency at the individual’s lattice point. The first terms in each of these fitness relations correspond to fixed fitness components, representing the effect of external selection operating at A. The second terms refer to the resource frequency-dependent components of selection, and it is these that are affected by niche construction. The coefficient of proportionality 1 determines the strength (relative to external selection), and direction of resource frequency-dependent selection, with positive 1 indicating that increased environmental resource levels will favour the A allele. We set 1 ¼ 0.3 in all the simulations we report here. A summary of all parameters used is given in table 4. Individuals mate with a randomly chosen neighbour (Moore neighbourhood), and offspring inherit their parents’ genotypes in Mendelian proportions. Here we consider both vertical and oblique transmission of cultural traits. Vertical transmission occurs according to the parameters specified in table 5. Offspring (viability) fitness is determined with reference to the resource level at one (randomly selected) parent’s location, under the assumption that newborn offspring develop in the same location as one of their parents. The probability of an offspring surviving is proportional to its fitness related to the minimum and maximum values of equation (2.2) given the selection coefficients in a given simulation and the limits of R (0,1). Offspring surviving to the dispersal stage are placed in a cell chosen at random from the eight cells in the neighbourhood of the parent with which the newborn develops, plus that parent’s own cell, replacing the original occupant. These individuals are then considered adult and capable of reproduction.


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Table 3. Can niche construction favour the hitchhiking of costly capabilities at other loci? Here, Rt ¼ l1Rt21 þ l2(z1(1 þ w) þ z2(1 þ w/2) þ z3) þ l3, where z1 –z3 are the frequencies of BBE, BbE and bbE individuals, respectively.

AA (h ¼ 0.999) Aa (1) aa (1)

BB (b1)

Bb ((b1 þ b2)/2)

bb (b2 ¼ 1)

w11 ¼ b1 þ 1R pffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi w21 ¼ b1 þ 1 Rð1 RÞ w31 ¼ b1 þ 1(1 2 R)

w12 ¼ ((b1 þ b2)/2) þ 1Rpffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi w22 ¼ ððb1 þ b2 Þ=2Þ þ 1 Rð1 RÞ w32 ¼ ((b1 þ b2)/2) þ 1(1 2 R)

w13 ¼ 1 þ 1R pffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi w23 ¼ 1 þ 1 Rð1 RÞ w33 ¼ 1 þ 1(1 2 R)

Table 4. Summary of terms. term

explanation

E,e A,a B,b R l1 l2 l3 p(E) g 1

alternative niche-constructing cultural practices alleles at A locus alleles at B locus resource frequency independent resource depletion positive niche construction independent resource renewal frequency of E cultural practice negative niche construction strength and direction of resource frequency dependence selection coefficient acting on cultural practice probability e e mating has E offspring probability e E mating has E offspring probability E e mating has E offspring probability E E mating has E offspring AA fitness aa fitness BB fitness bb fitness degree to which B potentiates niche construction probability of oblique transmission

a c0 c1 c2 c3 h1 h2 b1 b2 w f

In this way fitter offspring may spread out to colonize neighbouring cells, while an effective carrying capacity equal to the total population size is maintained. Following Silver & Di Paolo [5], a generation is defined as n 2 consecutive random matings, so that there will be significant overlap between one generation and the next. We considered questions 1 – 3 in turn, in each case running a series of simulations to explore the behaviour of the system, using the parameters and fitness equations described in tables 1 – 3, respectively. For each set of parameter values we varied the starting frequencies of A and E independently from 0.1 to 0.9 in 0.1 increments, giving 81 different starting conditions, and ran 10 simulations at each one. Spatial models ran in a 60 60 toroidal grid, and non-spatial models had the same population size of 3600 individuals. Alleles were distributed randomly and independently of each other at the start of each simulation, such that genotype frequencies at the start of the simulation averaged Hardy – Weinberg proportions, and cultural traits were randomly distributed across individuals irrespective of genotype. Lattice points were assigned uniform randomly distributed starting resource values (R) between 0 and 1. For each analysis, we also ran non-spatial controls in which the ‘neighbourhoods’ for mating and dispersal comprised the entire lattice so that individuals and resource locations were Phil. Trans. R. Soc. B (2011)

Table 5. Probabilities of vertical cultural transmission of E and e given parental traits. parental traits

probability of E offspring

probability of e offspring

EE Ee eE ee

c3 c2 c1 c0

1 2 c3 1 2 c2 1 2 c1 1 2 c0

picked at random from the general population. All simulations ran until A (question 1), E (question 2) or A and E (question 3) became either fixed or extinct, or simulations reached 1000 generations. 1. Can a cultural niche-constructing practice drive itself to fixation, even when costly, through statistical association with a genetic trait it favours? We consider a costly niche-constructing practice E (selection coefficient a , 1), which increases the amount of resource R in the environment and generates selection favouring allele A. Phenogenotype fitnesses are specified in table 1. Here we explore how a transmission bias for and against the cultural practice E (i.e. variation in c ¼ c1 ¼ c2 ¼ f0.45, 0.5, 0.55g, c0 ¼ 0, c3 ¼ 1) and selection against E (a) affect the dynamics. 2. Can cultural niche construction generate selection for costly genetic traits? We consider a costly genetic trait AA (selection coefficient h 1), which is favoured by the niche-constructing practice E (selection coefficient a ¼ 1). Here, the increase in resource due to niche construction depends on the frequency of both A and E. The modified version of equation (2.1) used to update the resource level and the relevant phenogenotype fitness functions are specified in table 2. We explore how a transmission bias for and against the cultural practice E(c) and selection against the AA genotype (h) affect the dynamics. 3. Can cultural niche construction favour the secondary hitchhiking of costly capabilities at other loci, expressed in more potent niche construction? For this question we introduce a second genetic locus, B, with alleles B and b, where allele B enhances the rate at which niche constructors produce resource R. Homozygous BB individuals have selection coefficient b1, those with bb have coefficient b2, and heterozygotes (Bb) have (b1þ b2)/2. In individuals with the cultural trait E (selection coefficient a ¼ 1), BB enhances niche construction by proportion 1 þ f, and Bb by proportion 1 þ f/2 (although the condition 0 R 1 was still applied). The modified version of equation (2.1) used to update the resource level and the relevant


Runaway cultural niche construction (a)


selection against E

selection against A

transmission bias in favour of E

niche construction by E individuals mainly AAE individuals

mainly heterozygotes mainly aae individuals transmission bias against E (b)

A locus genotypes

cultural trait (E)

resource level

1.0 0.8 0.6 0.4 0.2

(AA = white, Aa = grey, aa = black)

(E = white, e = black)

0

Figure 1. (a) Schematic of evolutionary forces acting on spatial clusters of individuals carrying linked cultural niche-construction traits and alleles favoured by niche construction. (b) Snapshot illustrating spatial clustering associations between A, E and R during a simulation run of the evolution of a costly capability to take advantage of cultural niche construction (selection against A allele, h ¼ 0.95, no cultural transmission bias).

phenogenotype fitness functions are specified in table 3. We explore how a transmission bias for and against the cultural practice E(c) and selection against the B allele (b1 , 1, b2 ¼ 1) affect the evolutionary dynamics. 3. RESULTS (a) Can a cultural niche-constructing practice drive itself to fixation, even when costly? Across a broad range of conditions, cultural nicheconstructing practices can generate selection for specific gene-based traits and hitchhike to elevated frequencies through the build up of statistical associations between practice and trait (figures 1 – 3). This is most apparent where there is little or no fitness cost to the cultural practice (figure 2, a 1), but is observed to a lesser degree even in the face of strong selection against E (e.g. a 5% disadvantage). These dynamics occur because, initially by chance, clusters of niche constructors appear in specific regions of space, generating a local concentration of the resource R, which in turn generates selection that favours allele A. In the spatial model, individuals mate and reproduce locally. Under these circumstances, allele A becomes statistically associated with the niche-constructing practice E, while allele a becomes associated with e. This means that the Phil. Trans. R. Soc. B (2011)

selection on A generated by niche construction inadvertently favours E through hitchhiking. Provided the clusters of niche constructors reach a critical threshold size they will typically increase until the trait is fixed. This assortative mating does not occur in the non-spatial model, preventing E from being disproportionately favoured by selection on A. The cluster size effect represents a balance of several processes (figure 1). The dynamics are similar to those observed in Silver & Di Paolo’s [5] genetic niche construction spatial model, but here there is the additional complication of cultural transmission biases. To understand the process, it is helpful to envisage two concentric circles, the smallest encompassing the cluster. Because the niche construction leads to non-random associations between the alleles and cultural traits, inside the inner circle are mainly AAE individuals, while outside the outer circle are mainly aae individuals. Separating the two is a boundary layer dominated by heterozygotes. Newly born AAE individuals disperse into the boundary layer from the inner circle, while newly born aae individuals enter the boundary layer from the outer region. Because the outer circle is larger than the inner circle, other matters being equal, this dispersal will tend to act to reduce cluster size. The magnitude of this force diminishes with cluster size, since the relative size of


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final frequency of E

0.8 0.6 0.4 0.2

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1.00

c = 0.5

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0.2

0


final frequency of A



1.0

0.8 0.6

c = 0.55 0.4 0.2 0 0.90

0.95 a (selection coefficient on E)

1.00

Figure 2. Evolution of costly cultural niche construction. Plots show frequency of allele A favoured by higher resource levels and cultural niche-constructing trait E at the end of simulations run with varying levels of selection against, and cultural transmission bias with respect to, E (a and c parameters, respectively). Values are means over all starting conditions with respect to the initial frequencies of A and E and error bars show +1 s.e. Open circles show results from simulations with local mating and dispersal, filled circles are from those with global interactions.

the two circles approaches 1 as the cluster increases. Opposing this process is the niche construction of those boundary layer individuals exhibiting the E cultural practice. This niche construction generates conditions that favour the A allele, which is disproportionately found in E individuals. Natural selection and cultural transmission also play a role, by affecting phenogenotype fitness (figure 1). Provided the balance of these processes favours E over e within the boundary layer, then the clusters will increase in size. We found that cultural niche construction could overcome moderate and sometimes even strong counter selection, and evolve to high frequency, especially when there was no transmission bias or where a transmission bias favoured the practice (c . 0.5) (figure 2). The similarity in outcome for both the A allele and the E cultural practice shows that strong associations are built up between them under most conditions. Generally, in spatially structured populations A and E both reached higher frequencies on average than in fully mixed scenarios, except when counter-acting natural or cultural selection was very strong. This difference was driven largely by spatial structure, enabling both trait and practice to become established and increase from lower initial frequencies (figure 3). When initial frequencies are very high or very low there are also differences between spatial and Phil. Trans. R. Soc. B (2011)

non-spatial model outcomes. These result from the possibility in spatial models that local gene frequencies can diverge significantly from population-level frequencies. This can have a buffering effect that acts to preserve low-frequency alleles in pockets of local abundance in situations where a lack of spatial structure would lead to extirpation of the allele. The exception to this trend occurred when a cultural transmission bias (i.e. c , 0.5) or extremely strong selection (i.e. a ¼ 0.9) acted against the E trait. In this case, the outcomes in mixed and structured populations were very similar. While here we concentrate on the findings of a vertical cultural transmission model, we have also analysed a model with oblique transmission, in which individuals learn from their immediate neighbours. We found that the effects described above break down when oblique transmission is very potent (i.e. the probability of learning from a non-parent is greater than 0.8), but that the effects persist with moderate or low levels of oblique transmission.

(b) Can cultural niche construction generate selection for costly gene-based traits? Here our results were very clear. Under almost all conditions a cultural niche-construction trait could drive a genetic trait to fixation, in spite of a significant viability


Runaway cultural niche construction final frequency of A

initial E frequency

(a)

initial E frequency

(b)



0.9 1.0

0.5

0.9 0.1

0.8 0.7

0.9 0.6 0.5

0.5

0.4 0.1 0.3

initial E frequency

(c)

0.2

0.9

0.1 0.5

0

0.1 0.1 0.5 0.9 non-spatial model

0.1

0.5 0.9 0.1 0.5 0.9 spatial model non-spatial model initial A frequency

0.1

0.5 0.9 spatial model

Figure 3. Effect of starting conditions on the evolution of costly cultural niche construction. Plots show end frequencies of A and E against their starting frequencies. Cell values are means over all levels of selection against E (a ¼{0.9, 0.95, 0.99, 0.999, 1}). (a) c ¼ 0.45; (b) c ¼ 0.5; (c) c ¼ 0.55.

deficit to the trait. The only exception occurred when a cultural transmission bias against the niche-constructing practice and a very strong viability deficit to the trait were both acting together. The aforementioned dynamics, resulting from the association of genetic trait and cultural practice, is sufficiently strong to overcome strong counter selection (e.g. more than 5% disadvantage). Even more striking is the observation that a modest cultural transmission bias favouring the practice can generate selection that takes extremely low fitness traits (e.g. more than 10% disadvantage) to fixation. That this is not dependent on spatially mediated hitchhiking is illustrated by the observation of the same process operating in non-spatial populations, and is consistent with earlier analyses of the impact of cultural niche construction [8]. The niche construction allows allele A to reach high frequencies when counter-selection was moderate to weak, and persist at non-negligible frequencies even in the face of potent counter-selection (figure 4). Only a moderate cultural transmission bias (i.e. c . 0.5) is required to strongly favour the niche-constructing practice so that both allele and cultural practice nearly always evolve to fixation even when initially quite rare (figure 5). Again, spatial structure facilitates the spread of these traits to higher frequencies than in mixed populations. We note in presenting these results that the values we chose for l1, l2, l3, and 1 mean that the fitness functions defined in equation (2.2) produce an asymmetry with respect to that portion of fitness Phil. Trans. R. Soc. B (2011)

that relates to the level of R that favours the A allele (in the long-term presence of E, R ! 1, so the second term of the fitness function for AA evaluates to 1 while for aa in the long-term presence of e this evaluates to 21/3). Not surprisingly, altering the dynamics of the niche-constructing ecology via these parameters can alter the model outcomes such that the coevolution of A and E no longer occurs. We concentrated here on areas of the parameter space where these effects could occur, but the reader should bear in mind that there will be areas where it does not. In terms of starting frequencies, the switch between those resulting in extinction of the trait and those resulting in fixation occurred over much smaller change in starting conditions than the previous analysis. Under some conditions, particularly when cultural transmission biases favour E, a change in the starting frequencies of either allele by 0.1 can shift the outcome from a high probability of extinction to a near-certainty of fixation, suggesting that factors such as drift, bottlenecks or founder effects could play a significant role in shifting populations from one state to another. (c) Can cultural niche construction favour the secondary hitchhiking of costly capabilities at other loci, expressed in more potent niche construction? Here a similar analysis produced more ambiguous results, with B only hitchhiking to higher frequency under much more restricted conditions. Across the


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0.8 0.6 0.4 0.2

0.8 0.6

0.2

1.0

1.0


0

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1.00

c = 0.5

0.4

0

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c = 0.45

0.4

0





1.0

0.8 0.6

c = 0.55

0.4 0.2 0 0.90

0.95 h (selection coefficient on AA)

1.00

Figure 4. Evolution of a costly capability to take advantage of cultural niche construction. Plots show frequency of allele A favoured by higher resource levels and cultural niche-constructing trait E at the end of simulations run with varying levels of selection against the homozygote AA (h ¼ f0.9, 0.95, 0.99, 0.999, 1g), and cultural transmission bias with respect to E (c). Values are means over all starting conditions with respect to the initial frequencies of A and E and error bars show +1 s.e. Open circles show results from simulations with local mating and dispersal, filled circles are from those with global interactions.

bulk of conditions under which E hitchhikes, B does not. While A and E both reach high frequencies, and exhibited a similarity of outcome that showed they were highly associated, there was no indication that B had formed any association with either A or E. To the contrary, its outcomes were independent of the practice and the alleles at the other locus, and appeared largely to be affected only by selection at B, even for large values of f (e.g. f ¼ 10), and no matter the strength of cultural transmission bias, c. These results occur in spite of the fact that, even with f ¼ 1, the effect of B on resource levels is dramatic. However, there is a restricted region of parameter space in which the secondary hitchhiking reliably occurs. It requires, perhaps counter-intuitively, a low coefficient of positive niche construction, l2. Figure 6 shows that B’s hitchhiking lags behind the rapid and strong interaction between A and E; this is the characteristic pattern. There exists a window of low levels of positive niche construction, l2, under which secondary hitchhiking is apparent (figure 7), with values of l2 too high or too low failing to lead to increased frequencies of B. When l2 is too high then the niche construction of individuals with bb genotype and the E practice is already potent, and the resource R reaches saturation before enough time Phil. Trans. R. Soc. B (2011)

has passed for an association of alleles A and B to build up. Once A and E become fixed, the opportunity for B to hitchhike on them is lost. Conversely, when l2 is too low then the niche construction of E individuals with the bb genotype is too weak, so A and E simply never become established, and B cannot hitchhike. Only when niche construction is within the window illustrated in figure 7 are A’s and E’s spread to fixation sufficiently reliable and slow to allow linkages to build up between these and B. Once the association is established, typically in a confined spatial region, then the AABBE combination begins to expand. This effect was only observed in spatial models, and never in non-spatial ones. Spatial structure is absolutely essential for B’s spread because the requisite mutual reinforcement of the A, E and B traits cannot happen if their effects are diluted and dispersed across a population.

4. DISCUSSION We have used spatially explicit gene –culture coevolutionary models to investigate how cultural processes could drive bouts of selection on human genes through modifying local resource distributions. The principle point to emerge from our analysis is that under a


Runaway cultural niche construction final frequency of A



initial E frequency

(a)

initial E frequency

(b)

0.9 1.0

0.5 0.9

0.1

0.8 0.7

0.9 0.6

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initial E frequency

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0.1

0.5 0.9 0.1 0.5 0.9 spatial model non-spatial model initial A frequency

0.1

0.5 0.9 spatial model

Figure 5. Effect of starting conditions on the evolution of a costly capability to take advantage of cultural niche construction. Plots show end frequencies of A and E against their starting frequencies. Cell values are means over all levels of selection against A (h). (a) c ¼ 0.45; (b) c ¼ 0.5; (c) c ¼ 0.55.

allele or trait frequency

1.0 0.8 0.6 0.4 0.2

0

100

200

300 400 generations

500

600

Figure 6. Time series of a single simulation run with l2 ¼ 0.06, showing lagged hitchhiking of B allele even when selection acts against BB (b1 ¼ 0.99). Note that after A and E fix (typically at this point the resource, R, will also be saturated), B can no longer hitchhike and begins to show drift-like dynamics. Other parameters were cultural transmission bias, c ¼ 0.5, selection on AA, h ¼ 0.999, and selection on bb, b2 ¼ 1. Black line, A; red line, B; blue line, E.

broad range of conditions cultural niche-constructing practices can generate selection for specific genebased traits and hitchhike to fixation through the Phil. Trans. R. Soc. B (2011)

build up of statistical associations between practice and trait. This is most apparent where the fitness cost of the cultural practice is low but is observed to a lesser degree even in the face of very strong counter-selection. Cultural niche construction could overcome moderate and even strong counter selection and evolve to high frequency, especially when there was no transmission bias or where a transmission bias favoured the practice. These dynamics are most pronounced in the spatially explicit models because niche construction and spatial structure lead the genetic trait and cultural practice to become statistically associated. This means that the selection on genes generated by niche construction inadvertently favours the cultural nicheconstructing practice itself through hitchhiking. Provided the clusters of niche constructors reach a critical threshold size they will typically increase until the trait is fixed. The dynamics are similar to those observed in Silver & Di Paolo’s [5] genetic niche construction spatial model, but further complicated by cultural transmission biases. They are robust to moderate levels of oblique cultural transmission (here, learning from neighbours), although high levels of oblique transmission unsurprisingly make it harder to build up gene – culture correlations. In essence, the dynamical process we describe closely resembles that of runaway sexual selection.


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final frequency of B

(a) 0.9

(b)

0.6

0.3

0

final frequency of B

(c) 0.9

(d)

0.6

0.3

0

0.05

0.10 l2

0.15

0.20

0

0.05

0.10 l2

0.15

0.20

Figure 7. Effect of l2, the coefficient of positive niche construction, and f, the strength of B’s effect on niche construction, on the evolution of costly genes that potentiate niche construction. Plots show frequency of allele B at the end of simulation runs, with each point representing the mean (+1 s.e.) of 10 runs. Symbols are shaded according to the proportion of the 10 runs in which A and E both fixed (white ¼ no runs fixed, black ¼ all runs fixed). All other parameters were fixed—cultural transmission bias, c ¼ 0.5, selection on AA, h ¼ 0.999, selection on BB, b1 ¼ 0.99, selection on bb, b2 ¼ 1. Initial frequencies of E, A and B were set at 0.25, 0.5 and 0.25, respectively. Note the high levels of B at intermediate values of l2 for spatial models only. Triangles, spatial model; circles, non-spatial model; dashed lines, B starting frequency. (a) f ¼ 1; (b) f ¼ 2; (c) f ¼ 5; (d) w ¼ 10.

Geneticist Fisher [43] proposed a positive feedback mechanism that could potentially explain the evolution of costly traits in animals that do not increase survival. Such traits were thought to be favoured because they increase the individual’s attractiveness to the opposite sex. Subsequent analysis has established that if the preference reaches a sufficiently high frequency it can overcome a viability deficit to the trait and generate selection that will increase trait frequency. Since individuals with the trait mate assortatively with individuals with the preference, over time these characters become statistically associated, such that the selection on the trait leads to the preference hitchhiking to higher frequency [44,45]. The process is described as ‘runaway’ because over time it would facilitate the elaboration of both trait and preference. Here the cultural niche-construction practice (E) is analogous to the mating preference which, provided it is of sufficiently high frequency, could generate a selective environment that favours the otherwise costly allele A. We find strong support for the hypothesis that cultural niche construction can generate selection for costly gene-based traits. The cultural niche-construction trait almost always drove the low viability genetic trait to fixation, with the only exception being where both natural selection and a transmission bias opposed the process. Population structure Phil. Trans. R. Soc. B (2011)

strengthens this effect because it promotes assortative mating leading to non-random associations between trait and practice. While here the process stops once the trait reaches fixation, the resulting uplift in the frequency of E is sufficient to significantly increase the chances of E becoming fixed. Niche-constructing cultural traits have effectively driven themselves to fixation. Note, our focus on a single diallelic locus is purely for mathematical convenience, and is designed to provide insight into the probable selection on any relevant genetic variation. In reality, human biological traits are likely to be influenced by multiple genes, and the runaway cultural niche-construction process we describe would potentially favour, and hitchhike on, any genetic variation that thrived in the resource rich environment. Moreover, genetic variation that enhances the cultural niche-constructing capability can also be caught up in this dynamic, opening up the possibility that both cultural practice and trait may experience repeated waves of selection, as is characteristic of runaway sexual selection. This process can help explain the evolution of certain costly biological traits in the human lineage, such as large brains, complex cognition or expensive digestive enzyme production. We note that alleles expressed in the nervous system, brain function and brain development are an overrepresented category among classes of genes known to be


Runaway cultural niche construction subject to recent selection [16,17]. Molecular geneticists have not only identified numerous brain-expressed genes in the human genome (or, indeed, no longer in the human genome) that have been subject to recent selection, they have estimated the time depth of these changes, and they have mapped them onto geneexpression networks using molecular tools such as co-expression analysis [32]. Cultural niche construction is a prime candidate for the source of this selection [15], and the processes revealed by our analysis are potentially important candidate mechanisms. Such considerations are further strengthened by our description of the conditions favouring secondary hitchhiking at other loci, whereby costly alleles are favoured simply because they amplify the nicheconstructing effects of the cultural trait E. Two points stand out in these findings—firstly, that this secondary hitchhiking can only occur when the niche-constructing effect on resource dynamics is comparatively weak, and secondly that this can only occur in spatially structured populations. The first limitation arises from the time lag between the initial favouring of the AAE complex and the subsequent hitchhiking of the B allele on its rising frequency. If, either because niche construction is too weak to favour allele A, or because niche construction is so effective that AAE fixes too rapidly and the resource R saturates, B cannot hitchhike. However, within this window of opportunity, weak but nonetheless effective niche-constructing capabilities generate selection for more potent niche-constructing capabilities, in a self-reinforcing dynamic. We note that this restriction to the range of circumstances under which secondary hitchhiking occurs results directly from the assumption of our model that there is a fixed upper bound to R. One might argue that for many aspects of human niche construction this assumption might be relaxed. For example, agricultural revolutions have repeatedly produced massive increases in yields per unit area. If R was an unbounded resource, then it is possible to envisage how a prolonged upward dynamic of primary hitchhiking resulting from niche construction could produce broader conditions favourable to the secondary hitchhiking of enhanced niche-constructing capabilities. Nonetheless, most resources cannot rise without limit, so at some point an upper bound will be reached, and the opportunities for the evolution of more potent niche construction will diminish. The second limitation, that secondary hitchhiking can only occur in spatially structured populations, is especially interesting because it appears to reflect so well the kind of agriculture- or technology-driven gene – culture coevolution discussed in the introduction. This spatial structure acts in two ways. Firstly, it generates a local concentration of the AAE complex, and secondly, it creates an advancing boundary zone of heterozygotes (figure 1), which is especially fertile ground for secondary hitchhiking. It is possible to envisage such zones occurring as waves of agricultural or technological innovation, through which cultural niche-constructing traits favour locally advantageous genotypes and in the process relentlessly drive their own advance, and perhaps even their own potency. Phil. Trans. R. Soc. B (2011)


In the non-spatial case, the dispersal of niche-constructing individuals across the shared resources of a population dilutes local resource concentrations, and means that statistical associations between the A and B alleles cannot build up. Our findings suggest that runaway cultural niche construction could have played an important role in human evolution, both through driving specific gene– culture coevolutionary episodes, and through facilitating the evolution of an enhanced niche-constructing capability in the human lineage through secondary hitchhiking [15]. Note that the models we have presented here considered only moderate biases in cultural transmission (0.45 c 0.55), but such biases can be considerably stronger [33], and this may well increase the potency of cultural niche construction further. The B locus in our model can potentially serve to represent any genetic locus expressed in a costly biological trait that impacts the niche-constructing capability. Our consideration of this secondary hitchhiking was largely motivated by the possibility that the average effect of allele B might confer a larger brain or enhanced cognitive capability. The latter includes an improved cultural capability, for instance, a capacity for motor imitation, teaching or language. Accordingly, our analysis may help to explain the observations that humans are simultaneously the species with the largest relative brain size, the most potent capacity for niche construction, and the greatest reliance on culture. Furthermore, it has not escaped our attention that in spatially structured contexts such as those we address, the benefits of local niche construction could potentially accrue both to the constructor’s own offspring and those of its neighbours. The potential for niche-construction theory to generate insights into the evolution of cooperation is an exciting area for future research [7,46,47]. It is apparent that cultural niche construction can lead to non-trivial alterations in evolutionary processes, especially in the case of spatially structured populations. We consider it highly probable that human cultural processes have driven evolutionary episodes in the human lineage, and our analysis may help understand current features of the human genome. This research was supported in part by BBSRC (BB/C005 430/ 1) and EU (CULTAPTATION (043 434), EVOCULTURE (232 823)) grants to KNL and a BBSRC studentship to LF. We are grateful to John Odling-Smee for helpful comments on earlier drafts of this manuscript. We also thank Jeremy Kendal and two anonymous reviewers for many improving comments.

REFERENCES 1 Lewontin, R. C. 1983 Gene, organism and environment. In Evolution from molecules to men (ed. D. S. Bendall), pp. 273 –285. Cambridge, UK: Cambridge University Press. 2 Odling-Smee, F. J., Laland, K. N. & Feldman, M. W. 2003 Niche construction: the neglected process in evolution. Princeton, NJ: Princeton University Press. 3 Laland, K. N., Odling-Smee, F. J. & Feldman, M. W. 1996 The evolutionary consequences of niche construction: a theoretical investigation using two-locus theory. J. Evol. Biol. 9, 293 –316. (doi:10.1046/j.1420-9101. 1996.9030293.x)


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22 Durham, W. H. 1991 Coevolution: genes, culture, and human diversity. Stanford, CA: Stanford University Press. 23 Holden, C. & Mace, R. 1997 Phylogenetic analysis of the evolution of lactose digestion in adults. Hum. Biol. 69, 605 –628. 24 Burger, J., Kirchner, M., Bramanti, B., Haak, W. & Thomas, M. G. 2007 Absence of the lactase-persistence-associated allele in early neolithic Europeans. Proc. Natl Acad. Sci. USA 104, 3736–3741. (doi:10. 1073/pnas.0607187104) 25 Tishkoff, S. A. et al. 2007 Convergent adaptation of human lactase persistence in Africa and Europe. Nat. Genet. 39, 31–40. (doi:10.1038/Ng1946) 26 Gerbault, P., Liebert, A., Itan, Y., Powell, A., Currat, M., Burger, J., Swallow, D. M. & Thomas, M. G. 2011 Evolution of lactase persistence: an example of human niche construction. Phil. Trans. R. Soc. B 366, 863 –877. (doi:10.1098/rstb.2010.0268) 27 Perry, G. H. et al. 2007 Diet and the evolution of human amylase gene copy number variation. Nat. Genet. 39, 1256–1260. (doi:10.1038/Ng2123) 28 Richards, M. P., Schulting, R. J. & Hedges, R. E. M. 2003 Sharp shift in diet at onset of Neolithic. Nature 425, 366. (doi:10.1038/425366a) 29 Saunders, M. A., Hammer, M. F. & Nachman, M. W. 2002 Nucleotide variability at g6pd and the signature of malarial selection in humans. Genetics 162, 1849– 1861. 30 Thompson, E. E., Kuttab-Boulos, H., Witonsky, D., Yang, L., Roe, B. A. & Di Rienzo, A. 2004 Cyp3a variation and the evolution of salt-sensitivity variants. Am. J. Hum. Genet. 75, 1059–1069. (doi:10.1086/ 426406) 31 Hawks, J., Wang, E. T., Cochran, G. M., Harpending, H. C. & Moyzis, R. K. 2007 Recent acceleration of human adaptive evolution. Proc. Natl Acad. Sci. USA 104, 20 753 –20 758. (doi:10.1073/pnas. 0707650104) 32 Varki, A., Geschwind, D. H. & Eichler, E. E. 2008 Explaining human uniqueness: genome interactions with environment, behaviour and culture. Nat. Rev. Genet. 9, 749–763. (doi:10.1038/Nrg2428) 33 Cavalli-Sforza, L. L. & Feldman, M. W. 1981 Cultural transmission and evolution: a quantitative approach. Princeton, NJ: Princeton University Press. 34 Boyd, R. & Richerson, P. J. 1985 Culture and the evolutionary process. Chicago, IL: Chicago University Press. 35 Kumm, J., Laland, K. N. & Feldman, M. W. 1994 Gene –culture coevolution and sex-ratios — the effects of infanticide, sex-selective abortion, sex selection, and sex-biased parental investment on the evolution of sexratios. Theoret. Popul. Biol. 46, 249 –278. (doi:10.1006/ tpbi.1994.1027) 36 Aoki, K. & Feldman, M. W. 1991 Recessive hereditary deafness, assortative mating, and persistence of a sign language. Theoret. Popul. Biol. 39, 358 –372. (doi:10. 1016/0040-5809(91)90029-F) 37 Aoki, K. & Feldman, M. W. 1997 A gene –culture coevolutionary model for brother-sister mating. Proc. Natl Acad. Sci. USA 94, 13 046 –13 050. (doi:10.1073/pnas. 94.24.13046) 38 Mesoudi, A. & Laland, K. N. 2007 Culturally transmitted paternity beliefs and the evolution of human mating behaviour. Proc. R. Soc. B 274, 1273 –1278. (doi:10.1098/rspb.2006.0396) 39 Enquist, M., Eriksson, K. & Ghirlanda, S. 2007 Critical social learning: a solution to Rogers’ paradox of nonadaptive culture. Am. Anthropol. 109, 727–734. (doi:10.1525/aa.2007.109.4.727)


Runaway cultural niche construction 40 Durrett, R. & Levin, S. 1994 The importance of being discrete (and spatial). Theoret. Popul. Biol. 46, 363– 394. (doi:10.1006/tpbi.1994.1032) 41 Durrett, R. & Levin, S. A. 1994 Stochastic spatial models—a users guide to ecological applications. Phil. Trans. R. Soc. Lond. B 343, 329 –350. (doi:10.1098/ rstb.1994.0028) 42 Krakauer, D. C. & Pagel, M. 1995 Spatial structure and the evolution of honest cost-free signaling. Proc. R. Soc. Lond. B 260, 365 –372. (doi:10.1098/rspb. 1995.0106) 43 Fisher, R. A. 1930 The genetical theory of natural selection. Oxford, UK: Clarendon Press.



44 Lande, R. 1981 Models of speciation by sexual selection on polygenic traits. Proc. Natl Acad. Sci. USA 78, 3721 – 3725. (doi:10.1073/pnas.78.6.3721) 45 Kirkpatrick, M. 1982 Sexual selection and the evolution of female choice. Evolution 36, 1 –12. (doi:10.2307/ 2407961) 46 Lehmann, L. 2007 The evolution of trans-generational altruism: kin selection meets niche construction. J. Evol. Biol. 20, 181–189. (doi:10.1111/j.1420-9101. 2006.01202.x) 47 Ihara, Y. 2011 Evolution of culture-dependent discriminate sociality: a gene–culture coevolutionary model. Phil. Trans. R. Soc. B 366, 889–900. (doi:10.1098/rstb.2010.0247)


Research

General patterns of niche construction and the management of ‘wild’ plant and animal resources by small-scale pre-industrial societies Bruce D. Smith* Program in Human Ecology and Archaeobiology, Department of Anthropology, National Museum of Natural History, Smithsonian Institution, Washington, DC 20560, USA Niche construction efforts by small-scale human societies that involve ‘wild’ species of plants and animals are organized into a set of six general categories based on the shared characteristics of the target species and similar patterns of human management and manipulation: (i) general modification of vegetation communities, (ii) broadcast sowing of wild annuals, (iii) transplantation of perennial fruit-bearing species, (iv) in-place encouragement of economically important perennials, (v) transplantation and in-place encouragement of perennial root crops, and (vi) landscape modification to increase prey abundance in specific locations. Case study examples, mostly drawn from North America, are presented for each of the six general categories of human niche construction. These empirically documented categories of ecosystem engineering form the basis for a predictive model that outlines potential general principles and commonalities in how small-scale human societies worldwide have modified and manipulated their ‘natural’ landscapes throughout the Holocene. Keywords: human niche construction; resource management; indigenous knowledge small-scale societies; ecosystem engineering; predictive modelling

1. INTRODUCTION

Clearly separated in space and time, these multiple independent domestication events occurred, it has been argued, within a broader behavioural context of niche construction [16]. As world climates and environments stabilized by about 12 000–10 000 years ago, human societies worldwide were actively auditioning many wild species of plants and animals, and intervening in their life cycles in a variety of different ways that would reshape local biotic communities and ecosystems. Some of these human management efforts led to the domestication of plants and animals, and genetic and archaeological research in recent years has substantially expanded our understanding of the temporal and spatial context of initial domestication of an increasing number of species worldwide [21]. While human manipulation and management of some species resulted in genetic and morphological changes associated with their domestication, other human niche construction efforts have targeted a broad spectrum of species that would remain ‘wild’ in terms of an absence of obvious genetic and morphological modification. Nakao [2] coined the term ‘hansaibai’ (han and saibai, i.e. half and cultivation) to refer to such species that are neither domesticated nor wild [22,23]. Although they lack both the morphological markers and the higher profile accorded domesticates, these numerous manipulated species have been, throughout the Holocene, the subject of sustained human attention and energy, and have represented

What is certain is that the forest dwellers . . . were not passive in their environment but actively altered it. Groube [1, p. 289]

Humans have a long history of niche construction—of modifying their environments in a wide range of different ways, large and small, through behaviour patterns that are both deliberate and inadvertent [1 – 20]. Although the consequences of human niche construction are not always anticipated, one of the primary goals of environmental engineering by human societies has been to increase their share of the annual productivity of the ecosystems they occupy by increasing both the abundance and reliability of the plant and animal resources they rely on for food and raw materials. Using fire and simple technology in the modification of vegetation communities, our distant ancestors were shaping environments more to their liking in ways that we can see in the archaeological record back perhaps as far as 40 000 years ago [1,8]. Human manipulation of ecosystems intensified at the end of the Pleistocene, when societies in different regions of the world began to independently domesticate a broad spectrum of plant and animal species. *[email protected] One contribution of 13 to a Theme Issue ‘Human niche construction’.

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Patterns of human niche construction important long-term resources for pre-industrial human subsistence economies worldwide. Along with obtaining a much more accurate and complete picture of where and when different species of plants and animals were domesticated worldwide, research has also substantially expanded our understanding of many of the basic underlying rules that define and shape the various developmental contexts and pathways that have led to domestication—the general characteristics that make particular plants and animals attractive targets for domestication—why some taxa are independently domesticated multiple times in different world regions, while others are not, and the basic general strategies used by human societies to create and sustain relationships of domestication [21]. In comparison, relatively little attention has been focused on looking for underlying principles or general patterns of niche construction exhibited by small-scale human societies worldwide during the Holocene in their utilization of wild or non-domesticated plants and animals. Are there certain sets of characteristics, and certain taxa of wild plants and animals that are logical targets for human engineering? And are there a finite number of general solutions or strategies for management and manipulation of these targeted taxa that can be documented in the past and present day across different world areas? In this article, I present an overall framework of understanding, a predictive model, for human niche construction focused on wild species by small-scale societies during the Holocene which parallels that which has been developed for domesticates. The initial step in developing this model involved an explicitly inductive search for, and identification of, descriptions of potential human niche construction strategies involving wild plant and animal resources. This search was primarily focused on North America, which has both a rich diversity of different environmental zones and a substantial empirical corpus of archaeological, ethnohistoric and ethnographic descriptions of how indigenous small-scale societies manipulated the ‘natural’ world. Following this initial continent-wide search, a simple ‘pattern recognition’ process was employed in an effort to organize the identified examples of human niche construction into a coherent and all-inclusive set of distinct categories of management of different segments of natural biotic communities. This resulted in the identification of six general categories of human niche construction, based both upon the shared characteristics of the target species and upon generally similar patterns of human intervention in their life cycle.

— General modification of vegetation communities: creating mosaics and edge areas, and resetting successional sequences. — Broadcast sowing of wild annuals: creating wild stands of seed-bearing plants in river and lake edge zones exposed by receding high water. — Transplantation of perennial fruit-bearing species: creating ‘orchards’ and berry patches in proximity to settlements. Phil. Trans. R. Soc. B (2011)

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— In-place encouragement of perennial fruit and nutbearing species: creating landscapes patterned with point resources. — Transplantation and in-place encouragement of perennial root crops: creating root gardens and expanding the habitat of wild stands. — Landscape modification to increase prey abundance in specific locations: enhancing salmon streams and creating clam gardens, fish ponds and weirs, and drive lines. Characterization of each of these six general categories of environmental manipulation in the following sections of this article in turn provides the basis for a concluding formulation of a general predictive model of human niche construction efforts involving wild components of natural biotic communities. The primary purpose in developing such a predictive model or abstract explanatory framework is to encourage further efforts to identify both additional specific examples, and perhaps additional general categories, of human niche construction involving wild species in other world areas, while also providing a better understanding of the underlying general principles and commonalities in how human societies worldwide have modified and manipulated their natural landscapes throughout the Holocene. For a number of reasons, recognition of human niche construction involving wild as opposed to domesticated species of plants and animals can often prove difficult. Management and manipulation of free-living plant and animal populations and non-agricultural ecosystems are often carried out by small-scale societies. These hunter – gatherers and farmers, numbering a few hundred to a few thousand people [24], characteristically leave a relatively light footprint on the landscape. In addition, human niche construction involving non-domesticated or wild species often mimics natural events and processes, making it difficult to differentiate between the two. And finally, there has been a notable absence of shared terminology employed in the documentation of human management of wild plants and animals (table 1), and a corresponding lack of linkage to an appropriate overarching conceptual framework and paradigm for comparative analysis and pattern recognition of different general forms of human ecosystem engineering, worldwide. This final problem is easily addressed by adopting the concept of human niche construction, which provides a general unifying perspective for integrating consideration of human efforts at management and modification of ecosystems [30,31]. For well over a half century, scholars have been providing accounts of how small-scale pre-industrial societies situated in a variety of different ecosystem settings, from tropical and temperate forest zones to semi-arid grassland environments, modify non-agricultural landscapes and natural biotic communities in favour of particular target species that are valued as sources of food or for the manufacture of a range of material culture categories (e.g. clothing, tools, structures). These ‘ecosystem improvement’ efforts take a variety of different forms, target a wide range of species and vary considerably in terms of their

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Patterns of human niche construction

Table 1. Twenty five different terms for human niche construction. aboriginal agronomy [25] aboriginal land management [5,18] anthropogenic environment [18] anthropogenic ecology [12,18] anthropogenesis [26] anthropogenic forest [18] anthropogenic landscape [18] disturbance regime [18] domesticated landscape [6,27] domestication of the environment [25] engineered environment [18] environmental manipulation [1,12] forest management [1] hansaibai (‘half cultivation’) [2] forest modification [18] humanized landscape [1] human-modified environments [18] Indian environmental management [5] indigenous management [12,28] indigenous human intervention [18] indigenous resource management [15] semi-cultivation [29] taming of the forest [1] traditional resource management [14] woodland management [22]

scope or focus, from very general attempts to shift vegetation communities towards earlier successional stages (and their higher representation of economically valued species), to very specific activities focused on a particular species or species group. Given the range of different societies and environments that have been considered, worldwide, by scholars from different generations and different disciplinary perspectives, and the rich variety of different human ecosystem improvement behaviour strategies that have been encountered, it should not be surprising that a multitude of different terms and phrases have been coined to characterize human manipulation of environments (table 1). While certainly reflective of broad geographical, temporal and behavioural coverage, this profusion of different descriptive terms, unfortunately, has also served to focus attention on individual region-specific and often species-specific case study examples and has emphasized their seeming distinctively different and unique character. As a result, attention has been drawn away from broader more inclusive consideration of what all of these human behaviour patterns have in common—they all represent human strategies of ecosystem engineering or niche construction. With the adoption of niche construction as a unifying concept, all of these different human strategies for environmental manipulation, and all of the various descriptive terms that have been employed, come into broader focus as comprising a large and coherent category. This in turn opens the way to look for broad patterns and general categories of resource management and manipulation, as well as the underlying general principles of how small-scale human societies go about shaping their environments to their advantage. Phil. Trans. R. Soc. B (2011)

2. GENERAL MODIFICATION OF VEGETATION COMMUNITIES: CREATING MOSAICS AND EDGE AREAS, AND RESETTING SUCCESSIONAL SEQUENCES By far the most commonly documented form of human niche construction by small-scale societies, worldwide, is a general effort to alter the overall composition of vegetation communities in order to increase the relative abundance of early successional stage plants that provide a source of food for either humans or animals that play a role in human economies, at the expense of other species of plants of lesser economic value [26]. This overall modification of vegetation communities is directed towards disrupting the reproductive rate of slowly growing ‘climax’ vegetation, enhancing the short-term productivity of herbaceous plants, and increasing in-patch diversity [6]. In contrast to the variety of different efforts that are directed towards selectively enhancing individual plants or clusters of plants of known location, which will be discussed below, general strategies for shaping vegetation communities represent more diffuse efforts designed to result in larger scale patterns of modification. Interestingly, such general efforts to modify vegetation communities appear to be the primary way in which human societies attempt to increase biomass levels of animal species of economic importance [32]. As will be discussed later in this article, when compared with plants, relatively few species of wild animals are the subject of tightly focused human niche construction efforts, and the majority of these involve aquatic resources (fishes and bivalves). Fire has long provided small-scale societies with a relatively easy, low-cost and effective way of generally reshaping vegetation communities in ways that increase the relative abundance of a range of different plant and animal food resources. Small-scale, moderate-impact burning of open grassland and shrub communities as well as forest environments is directed towards creating and maintaining a mosaic of small patches of habitat at different stages of regeneration [14,32 – 39]. The vegetation patches at early stages of regeneration, and the edge or interface zones between them, support higher biomass levels of plant and animal species of economic importance to humans than do later successional communities. Food plants used by humans (and other species) across a broad range of environments often have a competitive advantage early in a successional sequence, but decline in abundance over time. This general strategy of establishing mosaic landscapes with a variety of early-stage vegetation communities and extensive interface edge areas also represents a very effective strategy for humans to employ in order to increase the carrying capacity of their environments for terrestrial prey species. In both tropical and deciduous forest environments, for example, clearing of the overstorey canopy and the creation of open areas increase the carrying capacity and density levels for a wide range of grazing and browsing species [32]. In the eastern woodlands of North America, intermediate-impact forest clearance, both pre-Columbian and present day, has resulted in an increase in white-tailed deer (Odocoileus virginianus) populations [5,39]. Small-scale mosaic burning in

Patterns of human niche construction more open grassland habitats has also been documented as increasing the abundance of game animals. In the spinifex (Triodia spp.) sandplains and dune fields in western Australia, for example, controlled fires have been shown to result in greater habitat heterogeneity at the spatial scale of the human day range, with the increase in landscape diversity resulting in an increase in small-animal hunting productivity [40]. Along with being a widely employed and relatively easy way of shifting vegetation communities towards earlier successional stage species and maintaining habitat heterogeneity within human resource catchment zones, fire is also the form of human niche construction that is most easily seen in past environmental and archaeological records. Although it is not always easy to distinguish between natural and anthropogenic fires, charcoal, pollen and fire scar tree ring records from a range of different environments, worldwide, have been cited in a steady stream of studies documenting the widespread practice of deliberate burning of vegetation by human societies throughout the Holocene [5,9,17,26,36,40 – 53]. While increasingly sophisticated analyses of fire records that combine different approaches and multiple datasets are improving our ability to establish the scale, frequency and causes (natural versus humans) of past burn episodes, other forms of human niche construction are much more difficult to document in the archaeological record.

3. BROADCAST SOWING OF WILD ANNUALS: CREATING NEW STANDS OF SEED-BEARING PLANTS IN RIVER AND LAKE EDGE ZONES EXPOSED BY RECEDING HIGH WATER Along with using fire as a relatively low-cost way of opening up landscapes to colonization by early successional stage plant species, small-scale human societies in different world regions also facilitated, with relatively little labour investment, the colonization by early succession annual seed plants of unoccupied habitat areas that opened up predictably on an annual basis—the river and lake edge zones exposed each year by receding high water. This effective filling-up of empty habitat patches by establishing new stands of wild seed-bearing plant species could be accomplished through the simple practice of broadcast sowing of harvested seed. Take, for example, the description provided by Le Page du Pratz in the early 1700s of Natchez women and children scattering the seeds of a plant he called choupichoul along the sandbank margins of the lower Mississippi River that had been newly exposed by receding spring floodwaters [54]. Following seed dispersal, the planters casually pushed sand over the seeds with their feet. No other investment of labour was involved. Today the plant in question, Chenopodium berlandieri (chenopod, lamb’s quarters, goosefoot), remains a commonly occurring pioneer of river valley settings in the eastern woodlands of North America. It colonizes a variety of open and disturbed soil environments, both anthropogenic and natural, but it is most frequently found in open sand bank settings exposed by the receding floodwaters of spring. Dependent Phil. Trans. R. Soc. B (2011)

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upon a variety of poorly documented vectors of seed dispersal in river valley settings, and impacted by modern herbicides and introduced European chenopods, C. berlandieri today is usually found only in small patches, often mixed with introduced chenopods, or as isolated plants, rather than in extensive stands. In full sun settings, individual free-living C. berlandieri plants can grow to six feet in height and produce up to 50 000 small seeds, and would have required very little, if any, attention from humans during the growing season [54]. In contrast to the small patches and isolated individual plants of today, the Natchez, through their concerted and well-timed human seed dispersal by broadcast sowing onto open sandbank situations, could have created large and very productive wild stands of this economically important annual seed plant with an investment of relatively little effort. It is interesting to note that such efforts would not have occurred in exactly the same locations from year to year. Spring floodwaters would have reshaped river valley topography, and shifted the locations of prime sandbank real estate on an annual basis, necessitating the relocation of anthropogenic chenopod stands each year. Unfortunately, it is not possible to establish whether the seeds scattered by the Natchez had been harvested from local wild stands of chenopod the preceding autumn, or whether they represented the seed stock of the domesticated C. berlandieri that had been grown in eastern North America for more than 3000 years [55]. Nor have any good archaeological markers of this form of niche construction yet been identified, so the time depth of broadcast sowing in river or lake edge habitats, in eastern North America or any other world areas, remains undocumented. Broadcast sowing following spring floods, however, could have had considerable time depth and could have been employed along many of the river valleys of the eastern woodlands, and could have involved a number of other wild floodplain pioneering seed plants in addition to chenopod, including marshelder (Iva annua), sunflower (Helianthus annuus), erect knotweed (Polygonum erectum) and cucurbits (Lagenaria secaria, Cucurbita pepo ssp. ovifera). Broadcast sowing of small-seeded annuals in areas recently exposed by receding floodwaters has also been described in a number of other locations in North America, including the Southwest and Great Basin [11,56]. In one of the best-documented examples [29], Cocopa societies of the lower Colorado are described as broadcast sowing in ‘dećrue’ fashion seeds that they had harvested the previous autumn, on thin, muddy nutrient-rich river-bank soils exposed by the receding floodwaters of the Colorado [56]. These floodplain plots were up to 50– 100 m wide and could extend several kilometres along the river. They received no further attention prior to harvest, and included any of five different identified species. Three of these were historic-period introductions of Eurasian origin, while two species of panic grass (Panicum) were indigenous and known to have been grown at least as far back as 1541, leading Castetter & Bell [29] to raise the possibility that this human environmental modification or ‘semi-cultivation’ of grasses may have preceded

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maize–bean–squash agriculture in the region. Although involving different plant species, and located in very different environmental settings, the Natchez & Cocopa case study examples of dećrue sowing of annual seed crops are similar in that human niche construction efforts in both situations took advantage of naturally occurring and reliably predictable open areas that held the additional dual benefits of high ground water levels for early seedling growth and fertile soils owing to nutrient-rich annual floodwaters. These attractive aspects of seasonally flooded floodplain settings (planting areas clear of competing vegetation, and having fertile soil and adequate soil moisture) also played a role, it is interesting to note, in other examples of broadcast sowing of wild seedbearing annuals by small-scale societies in North America. The broadcast sowing of a number of seedbearing annuals, including chenopod, Indian rice grass and busy blazingstar (Mentzelia dispersa), by Western Shoshone groups has been documented in the Great Basin near springs and seeps (locales with high soil moisture) [57,58]. Areas to be sown were also frequently burned over in preparation, thereby both returning some nutrients to the soil and clearing competing vegetation. Similar dećrue niche construction strategies have also been described for other world areas [6].

4. TRANSPLANTATION OF PERENNIAL FRUIT-BEARING SPECIES: CREATING ORCHARDS AND BERRY PATCHES IN PROXIMITY TO SETTLEMENTS In a form of niche construction that reflects several of the same principles at work in the creation of dense stands of annual seed plants adjacent to river and lake margins, small-scale human societies also establish new stands of fast-growing perennial fruitbearing trees and bushes in proximity to settlements and other frequently visited locales (e.g. major trails, active and fallow garden plots). Rather than planting seeds in naturally occurring open areas, this form of human niche construction involves digging up seedlings or young trees that are found scattered through the forest and transplanting them in anthropogenic disturbed habitat openings in closer proximity to human settlements, and in much greater density than they occur in the wild. Eastern North America again provides a good case study example of the key aspects of this fruit tree transplantation strategy. As Gremillion [59] has noted, the peach (Prunus persica) was one of the European domesticates most rapidly and widely adopted by indigenous societies of the eastern woodlands, owing in large measure to its key similarities to native wild trees that were already subject to transplantation and tending by indigenous societies. Along with the peach, these native species targeted for transplantation all share a number of key attributes: they are weedy colonizers and require a minimum of labour investment for transplantation or tending; they mature rapidly, bearing fruit within ca 3 – 5 years; and they are perennials with life spans of several decades or Phil. Trans. R. Soc. B (2011)

more, ensuring a sustained harvest of fruit each year with minimal maintenance. The eastern woodlands of North America have a dozen or more native fruit-bearing trees that flourish in open sunny forest edges and clearings, including honeylocust (Gleditsia triacanthos), gum (Nyssa spp.), elderberry (Sambucus canadensis), mulberry (Morus rubra), hackberry (Celtis occidentalis), sugarberry (Celtis laevigata), hawthorn (Crataegus spp.), plum and cherry (Prunus spp.) and persimmon (Diospyros virginiana), all of which were potential targets for transplantation [60]. William Bartram and other early travellers through the East mention plums, peaches, persimmons, beautyberry and red mulberry, among other species, growing in orchards adjacent to old Indian settlements [5,61]. Many early historical accounts in the eastern woodlands of North America also describe a variety of different berry crops growing in ‘old fields’ around Indian settlements [5,11,61]. Gremillion [60] lists wild strawberry (Fragaria virginiana), groundcherry (Physalis spp.) and Rubus species (dewberry and blackberry) as often observed thriving in open areas adjacent to settlements, with understorey shrubs that produced edible fruits such as blueberry and cranberry (Vaccinium spp.), serviceberry (Amelanchier alnifolia) and huckleberry (Gaylussacia spp.) recorded as commonly present in overgrown fields [60,62– 63]. Similarly, Doolittle [11] summarizes early European descriptions from the Northeast of raspberries and strawberries growing close to settlements, with accounts often mentioning their abundance in overgrown fallow fields, and occasional reports of transplanting. Transplantation of fruit and berry species adjacent to settlements has also been documented on the Plains of North America. Adair & Drass [64] discuss the greater abundance of fruit- and berry-producing perennial plants within the fields and on the margins of permanent and semi-permanent settlements on the Plains, and reference both the Pawnee transporting American plums (Prunus americana) with them to their Oklahoma reservations, and the descriptions and maps of fruit thickets adjacent to Hidatsa settlements. They also suggest that higher quantities of fruit remains in archeobotanical assemblages from late prehistoric sites (e.g. plum, chokecherry) may reflect an increased occurrence of perennial fruit-bearing species in association with large aggregate villages and accompanying farm fields. Documentation of indigenous societies in North America transplanting economically important species in proximity to their settlements is not, however, limited to the Plains and eastern woodlands, or to perennial fruit and berry crops. There are records of people relocating plants of economic value in the subarctic [65], Northwest Coast, California, Great Basin, Southwest and Mexico. A variety of tuberous species are frequently mentioned in the literature, for example, as potential transplants. Deur [66] discusses the transplanting of springbank clover (Trifolium wormskjoldii) and other estuarine root crops along the Northwest Coast, and onions (Allium) are mentioned as target species for transplantation in both eastern North America [11] and California. Similarly, Jerusalem

Patterns of human niche construction artichoke, the perennial cousin of the sunflower, is described as a frequent invader of old fields, and a possible target for transplantation throughout its broad geographical range across the Plains and eastern North America. In addition, the Hopi are noted as having relocated the cattail (Typha angustifolia) closer to their settlements [11], and plants of a ritual nature, including tobacco and, in the Southeast, Ilex vomitoria, are also documented as having been transplanted close to settlements. The Kumeyaay in California have also been described as having an extensive and far-reaching programme of transplantation and tending of a select yet broad assemblage of wild perennial food plants, including oaks, pines, palms, mesquite, agave, yucca, wild grapes and cacti [56,67]. Similarly, Bye & Linares [68] describe the relocation of dead trunks of morning glory trees adjacent to settlements in the Valley of Mexico to ensure a reliable harvest of a highly prized mushroom (Pleurotus ostreatus). As Gremillion [59] and Doolittle [11] both note, this general practice of transplanting long-lived species, from fruit trees to fungi, adjacent to settlements allowed for easier harvesting and shorter travel time. It would also have strengthened perceptions of ownership of the resources, reduced unwanted harvesting of crops by human and non-human interlopers and have facilitated the monitoring and harvesting of fruits, berries and other plant parts as they matured. As is the case with human broadcast sowing of annual seed plants, the establishment of transplantation orchards of fruit-bearing perennials has been difficult to document in the archaeological record. Transplantation of parthenocarpic fig trees (Ficus carica) in proximity to 11 000 year old settlements in the Jordan Valley has recently been proposed, providing the oldest potential evidence for transplantation of a fruit-bearing species [69]. Witness tree records obtained within a decade or two of initial abandonment of Native American settlements in the Southeast United States, before the re-establishment of an overstorey canopy, have also shown higher than expected frequencies of fruit-bearing trees, indicating either transplantation or selective culling [70]. Although quite unusual species characteristics such as parthenocarpy in figs, as well as witness tree records (which can reach back only a few decades) are of limited use as archaeological markers of transplantation of economically important plant species, pollen analysis targeting samples recovered from archaeological contexts holds much greater potential for documenting the transplantation of economically important perennials by past societies, worldwide. At the SGang Gway Midden site in British Columbia, for example, six samples from a 13 cm sequence of litter and shell midden debris provided a record of the vegetation composition within the village, and based on the high amounts of rose family pollen, Hebda et al. [71] suggest that fruit-producing members of the rose family such as salmonberry and perhaps Pacific crabapple may have been grown in the village. Similarly, using pollen samples taken from several Jomon period sites in Japan, Kitagawa & Yasuda [22,23] Phil. Trans. R. Soc. B (2011)

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document an increase in abundance of pollen from two economically important tree species—chestnuts (Castanea spp.) and horse chestnuts (Aesculus spp.)—beginning at ca 7000 – 4500 BP, suggesting selective encouragement and perhaps transplantation by Jomon groups.

5. IN-PLACE ENCOURAGEMENT OF PERENNIAL FRUIT- AND NUT-BEARING SPECIES: CREATING LANDSCAPES PATTERNED WITH POINT RESOURCES Along with identifying and transplanting young fruitbearing perennials closer to settlements, small-scale human societies could also, with minimum effort, practice in-place encouragement of established, mature fruit trees, as well as those nut-bearing tree species that were not good candidates for transplantation because of the long delay that would separate replanting of seedlings and first harvest. The economically valuable fruit- and nut-bearing perennials could be selectively spared as competing trees were culled or harvested for building material and firewood, as well as during general vegetation clearance in the creation of mosaic patches and edge areas. As settlements were periodically relocated, the established orchards of abandoned settlements could also be revisited, and competing vegetation could be cleared away from the human-created stands of fruit trees and berry bushes. Over time, as old settlements were abandoned and new ones established, this sustained practice of removing competing tree species in proximity to habitation sites, while maintaining old orchards and creating new ones, could substantially alter the species composition of vegetation communities over relatively large resource catchment areas. Turning again to the woodlands of eastern North America, slower growing, larger and later successional stage nut- and mast-bearing trees, such as oaks, hickories and walnut, while sometimes mentioned as occurring among the fruit- and berry-producing species of close-in transplanted orchards [59], are more often described as being scattered both within abandoned fields and beyond, reflecting a niche construction strategy involving selective in-place encouragement. Hammett [5,61], for example, outlines a general abstract pattern of landscape management by pre-European societies of North America that has settlements and their adjacent small gardens encircled by two resource catchment zones— a close-in area of actively cultivated and fallow fields, orchards and berry patches, and surrounding it, a wooded zone containing mast-, nut- and fruit-bearing trees as well as trees for construction and firewood, along with white-tailed deer and other prey species (see [3] for a similar abstract catchment zone pattern for Japan). Selective retention of overstorey nut- and mast-bearing trees during field clearance could have resulted in their scattered distribution in the close-in zone of active and fallow fields, with their relative abundance in outlying forest zones increased by a lower level of selective encouragement and culling of competitors in the absence of substantial clearing. Controlled burning in forest resource zones, along

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with other methods of thinning both understorey and canopy species, could have encouraged larger and higher yielding nut- and mast-bearing trees [5,61,72,73], and such a broad-scale niche construction practice has been suggested as having a deep time depth in eastern North America [46]. At the same time, as settlements and their concentric resource catchment zones were periodically relocated throughout forest zones of North America, they would have left behind a legacy of fallow-cycle vegetation communities that were substantially enriched in forest species of economic value in comparison to their composition prior to clearing. Following settlement abandonment, as overstorey canopies encroached on, and reduced the habitat of, early successional species, the larger, later successional stage trees of economic value that had been the target of earlier selective encouragement would have sustained their increased abundance in the restructured forests over a longer period of time [51,74]. Similar strategies of selective culling of competing species and encouragement of nut- and fruit-bearing trees have been documented in a number of different past and present-day low-latitude tropical forest environments [8,28,75], as well as in temperate forest and more open environments. Fowler [57], for example, documents the clearing away of vegetation from pinõn trees in the Great Basin, as well as ‘knocking’ branches and pinching growth tips to encourage additional cone development. In Japan, Kitagawa & Yasuda’s [22,23] analysis of pollen samples from Jomon period sites, as well as prior studies showing an increase in the size of nuts, provides evidence of selective encouragement of both chestnut (Castanea spp.) and horse chestnut (Aesculus spp.) as early as 5000 BP, and Nishidha [3] outlines broader patterns of management of wild plants in contemporary villages in rural Japan. In-place management and manipulation of longlived perennials also, of course, includes those species that can be harvested for raw material rather than food. A variety of different species in different environments are coppiced and pollarded (pruned) to maintain them in a physiologically young state, producing new growth each year to be used for firewood and a range of manufactured items, including baskets [57,68].

6. TRANSPLANTATION AND IN-PLACE ENCOURAGEMENT OF PERENNIAL ROOT CROPS: CREATING ROOT GARDENS AND EXPANDING THE HABITAT OF WILD STANDS Along with the transplantation and in-place encouragement of fruit- and nut-bearing perennial species, small-scale pre-industrial societies also direct similar niche construction efforts towards perennial plants of a different sort—those with starch-rich underground storage organs (roots, rhizomes, culms). These perennial ‘root’ crops differ from fruit-, berryand nut-bearing species, however, in three notable respects. Since it is the roots of the plants themselves that are of interest rather than ‘renewable’ products (fruits, nuts, berries, branches), the entire plant is harvested, requiring periodic addition of new replacement plants. In addition, unlike fruit- and nut-bearing Phil. Trans. R. Soc. B (2011)

species, where human niche construction efforts are primarily directed towards removal of competing plants, modifying the target species, and ensuring adequate sunlight, management of root crops usually focuses instead on issues of water management. And finally, in contrast to management of fruit- and nutbearing species, niche construction strategies for perennial root crops often involve considerable investments of human labour in habitat improvement features (e.g. dams, canals, rock mulching, soil retention walls, etc.). Three examples of human niche construction focusing on perennial root crops by small-scale societies located in different regions of North America help to illustrate these three points. One of the most remarkable examples of highinvestment human niche construction involving perennial root crops has been documented in the Owens Valley of the Great Basin area of California [57,58]. Owens Valley Paiute groups constructed an irrigation system that carried and dispersed water across extensive tracts of swampy low-lying floodplain meadows adjacent to the Owens River. The vegetation of these waterlogged, river valley resource zones included a number of bulbous hydrophytic food plant species that had long been an important component of Owens Valley subsistence economies (e.g. blue dicks or purplehead brodiaea (Dichelostemma capitatum ssp. capitatum), chufa flat sedge (Cyperus esculentus) and possibly spikerush (Eleochari spp.) [58]. This enhancement and expansion of the natural habitat of the water-meadow root crops was carried out on a large scale in several locations. Each year, construction and subsequent removal of temporary diversion dams along some of the tributary creeks of the Owens River called for the labour of all of the men of communities. Feeder ditches up to 6.5 km long carried nutrient-rich, early summer mountain run-off from dams to the river valley plots, the largest of which were 5.2 – 10.4 km2 in size [76]. No efforts were made at planting, tilling or tending either the wild root crops of these water meadows or the adjacent downstream stands of wild seed plants (including sunflower, chenopod and lovegrass) that also benefited from the irrigation efforts. Unfortunately, it is probably not possible to determine how far back in time prior to the 1840s these labour-intensive water management practices were carried out [58]. Like the Owens Valley groups, small-scale societies along the Northwest Coast of North America also invested considerable effort in enhancing and expanding the saturated soil habitats of indigenous starchy root crops. They encountered different challenges from those faced by Owens Valley groups, however. In the Owens Valley, the central hurdle in expanding and enhancing water meadow root crop production involved ensuring a reliable water supply. This was accomplished, with considerable human labour, through the construction of irrigation canals. Relatively little labour appears to have been invested in tilling the soil or weeding the water meadows themselves. Along the Northwest Coast, in contrast, human ecosystem engineering efforts focused not on waterdelivery systems, but on the artificial expansion of

Patterns of human niche construction the habitat zone of a number of estuarine food plant species, along with active and sustained efforts to improve the soil and selectively remove competing grasses within these expanded tidal ‘garden’ plots [66]. The root crop species in question, including springbank clover (Trifolium wormskjoldii), pacific silverweed (Potentilla anserine ssp. pacificia), northern riceroot lily (Fritillaria camschatcensis) and Nootka lupine (Lupinus nootkatensis), which all produce dense concentrations of thin, long starchy roots and rhizomes, have a particularly narrow range of distribution within the tidal column in undisturbed high salt marsh estuarine settings. Interestingly, this high marsh habitat zone, like the open sandbank settings selected for broadcast sowing of annuals discussed above, represents an ‘externally powered’ ecosystem. Just as floodwaters carry new soil and nutrients to riverbank settings, peak tides and floods deposit marine, riverine and estuarine sediments and organic debris into this high marsh habitat zone, dramatically increasing the nutrient composition of the soils, and making it one of the most productive environments in the world in terms of carbon produced per unit of area [66]. Both historical descriptions and recent research provide evidence for widespread ecosystem engineering of this high marsh zone by Northwest Coast societies, with substantial human effort invested in expanding the very narrow band in which the plant species with edible starchy root crops can grow. This was accomplished by the downslope mounding of soils and the construction of rock and wood reinforcing walls, which effectively extended the habitat of the target species [66]. Within these extended garden plots, the soil was periodically churned. This churning created a texturally diverse soil while also mixing in the most recent deposits of fresh organic matter. It also increased the porosity of the soil, thereby encouraging the growth of the larger, longer and straighter roots so highly prized by Northwest Coast societies. In addition to churning the soil, human management of these expanded cultivation areas also involved sustained weeding of grasses and other unwanted invaders throughout the growing season, and the vegetative replanting of root fragments and small plants at the time of harvest, in order to ensure future abundant yields. The Owens Valley and Northwest Coast examples of in-place enhancement and expansion of natural stands of perennial plants share a number of similarities. In both areas, the targeted species are all components of natural wet-soil communities, and human niche construction efforts are directed towards the deliberate and sustained enrichment and expansion of the habitat zones of these plant communities. Rather than focusing on a single species, a variety of perennials were involved in both regions. In the Southwest, a third example of considerable human labour being invested in wild perennial root crops involves human niche construction efforts to increase soil moisture in order to mimic the natural habitat of agave (Agave spp.). One of the best-documented examples of this form of niche construction consists of a checkerboard pattern of linear rock-bordered grid features (each square roughly Phil. Trans. R. Soc. B (2011)

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10 m on a side) situated on the broad cobble and boulder terraces adjacent to the alluvial plain of the Gila River in southern Arizona. A total of 36 grid clusters covering an a area of 82 hectares were mapped within 1 km on either side of Spring Wash, a tributary of the Gila River [77]. Constructed between about AD 750 and 1300, these rock grids were water control features that captured rainfall, retained surface runoff and created a mulch, reducing evaporation and increasing soil moisture levels (soil moisture within and adjacent to these liner rock features today measures twice that recorded outside of the features). Although still far below what would have been needed to grow maize or other domesticated crop plants, the increase in soil moisture resulting from these rock grid features was significant in terms of supporting indigenous perennials such as agave that could withstand seasonal moisture shortfalls. A series of roasting pits situated along Spring Wash and several other tributaries transecting the rock grid area yielded agave processing tools along with monocot tissue compatible with agave, as well as cf. agave leaf base fragments, confirming the large-scale cultivation of this wild plant for food and fibre. It is estimated that this rock grid system could have supported an estimated 44 500 agave plants at any one time. Small ‘offsets’ or ‘pups’ of mature parent plants were probably initially collected from relatively distant stands and then transplanted to the prepared rock grid mulch fields. Once established, mature plants within the rock grids could produce all the pups needed for the perpetuation of the cultivated stands of wild agave. This is only one of a growing number of locations across the Southwest where transplantation and cultivation of agave in rock mulch contexts have been identified. In the Phoenix, Tonto and Tucson Basins, more than 550 individual locations where agave plants were transplanted by Hohokam societies at ca AD 600 – 1350 have been documented [77]. Evidence of early human niche construction efforts involving water management is not, of course, limited to North America. Drainage canals associated with the cultivation of tree crops and dating to ca 7000 BP have been documented in the highlands of New Guinea [78], and artificial walls or ‘bunds’ designed to retain floodwaters and thereby expand the natural habitat of wild and early cultivated rice crops and dating as early as 7700 BP have been documented in the Yangtze Delta region of China [17].

7. LANDSCAPE MODIFICATION TO INCREASE PREY ABUNDANCE IN SPECIFIC LOCATIONS: ENHANCING SALMON STREAMS AND CREATING CLAM GARDENS, FISHWEIRS AND DRIVE LINES As mentioned earlier in this paper, while efforts by small-scale pre-industrial societies to increase the availability of economically important wild animals in their resource catchment areas primarily involve general and indirect efforts to enhance carrying capacity through vegetation modification, there are also scattered examples of human niche construction that are directly focused on specific animal species and particular locations on the landscape. These management

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strategies are of two general types: those designed to enhance and/or expand the habitat of particular species, and those designed to channel and constrain the movement of prey for easier harvesting. An excellent example of this first form of niche construction, habitat expansion and enhancement, is the ‘clam gardens’ of the Northwest Coast of North America. Employing a strategy analogous to that used to construct the root gardens discussed earlier, downslope rock walls, sometimes up to a metre in height, are constructed at extreme low tide lines adjacent to extant clam beds, and soil and shell ‘hash’ is filled in behind them, effectively extending the extant natural clam bed farther out from shore. Often situated in favourable locations adjacent to settlements, clam gardens have been mapped from Vancouver Island north to Alaska, with more than 400 being recorded on Vancouver Island alone [79]. The time depth of these ecosystem engineering efforts is not yet known. Interestingly, the bivalves that are ‘cultivated’ are more similar in several respects to the Northwest Coast root crops than they are to other species of animals. They are essentially a stationary resource, with specific and clearly discernible requirements in terms of water depth and nutrient flow, and as a result are worthwhile targets for location-specific habitat expansion and enhancement. Such location-specific niche construction efforts can also be employed for prey species that, while mobile, also have very predictable seasonal movements and specific habitat locations that can be enhanced through human intervention. Salmon streams can be enhanced through removing debris, and fish eggs can be transplanted between water systems [80] (J. Jones 2002, unpublished MA thesis). In contrast to niche construction meant to expand and enhance particular habitat locations, which are relatively poorly documented, examples of human alteration to the landscape designed to channel and constrain the movement of prey for easier harvesting are much more abundant, and primarily fall into two similar forms of construction: fishweirs—designed to direct fishes into enclosures for capture, and fences— placed to facilitate the driving of large herbivores into corrals for killing. The use of fishweirs has been documented in many inland and coastal areas, worldwide. In a comprehensive summary of fishweirs in North America, Connaway [81] describes three basic categories of fishweirs: flowing stream weirs, tidal weirs and longshore weirs. Constructed of both stone and wooden stakes, flowing stream fishweirs are usually ‘V’ shaped and are placed in shallow areas or shoals, with the downstream apex of the V acting as a funnel to direct fishes into a trap. In the Northwest, flowing stream Salmon weirs often take the form of a straight fencelike barricade, which blocks the fish running upstream and subjects them to spears and dip nets. Tidal or ebb weirs also take the form of bank to bank stone and wooden post barriers that are placed along the coast in tidal inlets and along streams subject to tidal flow and ebb. At high tide, fishes pass easily over the barrier, but are then trapped behind the barrier as the tide recedes. Longshore weirs consisted of a Phil. Trans. R. Soc. B (2011)

fence or a single wing extending out perpendicular from the shore in non-tidal inlets, river mouths, on the edges of lakes and along saltwater shorelines. Fishes swimming parallel to the shore will encounter the barrier and are then diverted along it into traps or pens. Generally comparable to fishweirs in function, game fences were constructed by small-scale societies in a variety of settings to facilitate the driving of large herbivores into corrals for killing. Drive lines designed for bighorn sheep and pronghorn antelope in the Great Basin date back more than 3000 years, including one pronghorn fence, constructed of dwarf cedars and bound together in some places by willow withes, which was more than 8 km long [82]. Similar pronghorn drive lines have been documented in the Southwest, and drive line fences were also employed for corralling bison at ca 3000 BP on the Great Plains. A caribou drive line submerged beneath the waters of Lake Huron and dating ca 10 000 BP has also recently been detected [83]. Small-scale societies also recognize and take advantage of the drawing power of edge areas, fields and garden plots close to their settlements in attracting prey species to them. The practice of ‘garden hunting’ where hunters take advantage of deer, waterfowl and other species’ efforts to browse on the early successional species of anthropogenic habitats is well documented in many regions of North America [66,84].

8. DISCUSSION: A PREDICTIVE MODEL The formulation of a predictive model for the management of wild resources by small-scale pre-industrial societies draws both on the broader theoretical perspective and paradigm provided by niche construction theory (NCT) [31], and on the numerous realworld examples of human niche construction briefly outlined above. These two seemingly disparate foundational influences or sources—derived theory on the one hand and inductively collated empirical examples on the other—are in fact interrelated in a number of important respects. Since small-scale human societies represent a subset of the larger set of species encompassed by the more inclusive general conceptual framework of NCT, it logically follows that the core principles and basic assumptions of NCT are applicable to the smaller nested subset. Note that these basic tenets and core principles, as applied to small-scale human societies, are derived and not deduced from NCT (see the discussion of universal laws, probabilistic laws and lawlike statements in [85,86]). As is often the case with theoretical models and explanatory frameworks in the biological and behavioural sciences, the concepts and ideas embodied in NCT fall under the heading of law-like statements rather than either universal or probabilistic laws, and as a result, their relative explanatory strength or utility rests entirely on their track record in accounting for or predicting events—how well they can be shown to fit the real world [85]. The predictive model outlined here for niche construction by small-scale human societies thus derives support from the general conceptual framework of

Patterns of human niche construction NCT not because of some radiant theoretical purity or elegance embodied in NCT (although that may certainly be present), but rather because it carries with it a large and diverse array of empirical examples that appear to conform to its predictions or test implications. The extensive documentation of niche construction activities by a wide range of different species that is presented by Odling-Smee et al. [31] illustrates and underscores the basic and obvious necessity of continually testing the relative strength of any proposed framework of explanation through assessing its ability to account for empirical reality. In a similar manner, the case study examples of human niche construction described above, and their organization into six general categories, which together form the second source or foundational element for the predictive model presented here, also reflect the basic cyclical nature of scientific inquiry, this time at the subset level. These case study examples further shape and support a framework of explanation specifically tailored to a particular nested subset of environmental engineering—the efforts by small-scale pre-industrial human societies to modify their natural surroundings. In both this small-scale human society subset and in the larger set of species encompassed by NCT, the seeking out and compiling of specific empirical examples from the real world with which to formulate, test and refine theoretical models represents an essential aspect of the scientific cycle. It is of course necessary to avoid the circularity of exclusively employing the same empirical data that were used in formulating a predictive model in subsequently assessing its utility—additional, independent datasets provide the true and ongoing measure of the strength of any explanatory framework in the biological and behavioural sciences. Future testing of this model will involve assessing the extent to which its predictions or test implications are confirmed in other regions of the world and in other cultural and environmental contexts. This predictive model of niche construction by small-scale human societies worldwide during the Holocene in their utilization of wild or non-domesticated plants and animals has a number of core principles or tenets. The most basic of these, as eloquently articulated in the quotation at the beginning of this article, is that humans have been intensive and extremely successful ecosystem engineers for more than 10 000 years: ‘What is certain is that the forest dwellers . . . were not passive in their environment but actively altered it.’ [1]. This simple observation might seem both obvious and non-controversial—that throughout the Holocene and for an unknown preceding span of time, Homo sapiens have not been simple passive components of biotic communities, with their diet choices constrained by the structure of extant pristine natural environments, but rather that they actively and sometimes extensively shaped their ecosystems. In fact, however, it directly calls into question a number of still quite popular conceptual models of human resource selection that lack consideration of the human capacity for ecosystem engineering, most notably the diet breadth and patch choice models of human behavioural ecology [87]. Phil. Trans. R. Soc. B (2011)

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A second basic tenet of the model is that one of the central goals of environmental engineering by human societies is to increase their share of the annual energy produced by the ecosystems they occupy by increasing the accessibility, abundance and reliability of the plant and animal resources they rely on for food and raw materials (see [11] for detailed descriptions of ecosystem engineering associated with agricultural landscapes). As seen in the North American case study examples briefly presented above, the timing and duration of human energy invested in such environmental modification efforts can vary widely between target species, from annually repeated and behaviourally imbedded lowcost activities (e.g. controlled burning and selective culling of vegetation) to the less frequent but higher initial investment construction (and maintenance) of longer lasting environmentally imbedded structures (e.g. fishweirs and drive lines, diversion dams, rock mulching and clam beds). But in all of these examples, a basic goal of the human niche construction initiatives by small-scale societies is to restructure the food web within their local resource catchment in ways that strengthen their position and their network of energy sources [88]. This predictive model also proposes that just as there are general characteristics that make particular plants and animals attractive targets for domestication, there are also certain sets of characteristics and certain taxa of wild plants and animals that are logical targets for human engineering, as well as a finite number of general solutions or strategies for management and manipulation of these targeted taxa. Each of the six strategies of niche construction described above identifies such a set of resources with particular characteristics that make them good targets for human manipulation, along with the general outline of the basic human strategy for how they can be successfully managed. Human niche construction intended to increase the abundance and harvest of wild animal species of economic importance to small-scale human societies is limited to two quite different strategies. On the one hand, burning and other low-cost efforts at general vegetation modification, and their influence in different environments (e.g. release of nutrients into the soil, reduced woody biomass, breaking of overstorey forest canopies, increased edge areas and a more mosaic vegetation landscape, shift to earlier successional sequence vegetation communities) all result in an increase in the plant foods relied on by prey species, and a corresponding potential increase in prey abundance. At the same time, structural modifications to the landscape (drive lines, fishweirs) serve to channel and constrain the movement of prey for easier harvesting. General niche construction strategies targeting plant species, in contrast, span a range of different approaches, depending on the characteristics of the species groups involved. Stand expansion of annual seed plants of economic importance is accomplished by human-mediated seed dispersal into areas recently cleared by burning or by the receding of seasonally high water. Transplantation of economically important species closer to settlements primarily involves perennial understorey berry- and fruit-bearing herbaceous

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and woody plants with a short time span to maturity, while overstorey nut- and fruit-bearing species with a longer growth to yield time span are selectively encouraged in place through culling of competing species. Finally, the availability of perennial species with underground storage organs is increased by habitat enhancement and expansion, and sustained transplantation, with specific strategies addressing environmentally variable soil moisture requirements. The composition and the structure of these general categories of human ecosystem engineering in turn reflect the obvious underlying challenges that human societies face in reshaping local plant and animal communities more to their liking. The essential recipe for the advantageous restructuring of plant communities includes: (i) the removal of unwanted vegetation that competes for sunlight, soil moisture and nutrients, (ii) increasing the localized abundance or patch size of desirable food plants by expanding their existing habitats, transplanting (perennials) or planting (annuals) in either anthropogenic or naturally created habitats, and (iii) ensuring that these resource patches, either already existing or newly created, receive sufficient sunlight, moisture and nutrients. Ecosystem engineering directed towards wild animal species involves both habitat improvement and the construction of fences designed to facilitate more dependable and higher yield harvests of fishes and wildlife. Future testing of this model will involve the seeking out of additional examples of management of wild plant and animal species by small-scale human societies worldwide, and establishing the extent to which they comfortably fall into the six categories. This may not be an easy exercise, since many of the specific methods of human niche construction outlined here represent anthropogenic analogues to events, processes and landforms that occur in nature—fire clearance of trees and grasslands, forest clearings owing to windfalls, flood-scoured sand banks, natural traps and drive line features, seasonal stranding of fishes in oxbow lakes, etc. This mimicking of natural processes will constitute a major challenge in continuing efforts to expand the list of documented small-scale human niche activities and general categories, particularly in the archaeological record.

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Research

Foraging and farming as niche construction: stable and unstable adaptations Peter Rowley-Conwy1, * and Robert Layton2 1

Department of Archaeology, and 2Department of Anthropology, Durham University, South Road, Durham DH1 3LE, UK

All forager (or hunter – gatherer) societies construct niches, many of them actively by the concentration of wild plants into useful stands, small-scale cultivation, burning of natural vegetation to encourage useful species, and various forms of hunting, collectively termed ‘low-level food production’. Many such niches are stable and can continue indefinitely, because forager populations are usually stable. Some are unstable, but these usually transform into other foraging niches, not geographically expansive farming niches. The Epipalaeolithic (final hunter–gatherer) niche in the Near East was complex but stable, with a relatively high population density, until destabilized by an abrupt climatic change. The niche was unintentionally transformed into an agricultural one, due to chance genetic and behavioural attributes of some wild plant and animal species. The agricultural niche could be exported with modifications over much of the Old World. This was driven by massive population increase and had huge impacts on local people, animals and plants wherever the farming niche was carried. Farming niches in some areas may temporarily come close to stability, but the history of the last 11 000 years does not suggest that agriculture is an effective strategy for achieving demographic and political stability in the world’s farming populations. Keywords: hunter – gatherer; forager; farmer; niche construction; origins of agriculture; low-level food production

1. INTRODUCTION Niche construction has been much discussed by anthropologists and archaeologists, albeit under a variety of terminologies. In this contribution, we propose to look at hunting, gathering and farming as forms of niche construction. In humans, the creation of new niches may lead to both genetic and behavioural modifications or culture change. The modern farming environment or ‘artificial steppe’ is perhaps the ultimate form of niche construction by humans. But hunter– gatherers also construct niches in a variety of ways. Some of these are stable: once created, they may continue indefinitely, without any need for subsequent changes in human behaviour. Others are however unstable: change is inherent in such niches, and this sooner or later precipitates human cultural change. The outcome of instability is that the niche is reconstructed. Usually these reconstructed niches are altered forms of hunting and gathering. But in some cases the niche is transformed into what we conventionally term farming. In this paper we (i) explore a variety of niche types constructed by hunter–gatherers. Some of these involved small-scale cultivation that caused genetic changes in the plants—the most simple working definition of domestication [1]. We will ask why these and other activities did not take off but remained

small-scale. We then (ii) consider why just a few niches did take off and were transformed into what we consider ‘farming’; and finally we (iii) examine the ways in which the early farming niches were exported to cover a wide geographical area. The processes identified point to the conclusion that farming originated not as a deliberate process of intensifying resource production, but as a series of small, accidental changes in the way that niches were constructed.

* Author for correspondence ([email protected]).

(a) Concentration of wild plants The Nukak of the Columbian Amazon take fruit that needs to be processed before eating back to their

2. HUNTER –GATHERERS: STABLE AND UNSTABLE NICHES All hunter – gatherers remove animals and plants from the wild gene pool, and thus modify their ecological niche. In this section, we examine instances where their practices have gone beyond this and have amounted to active niche construction. We consider stable hunter – gatherer niches under four headings: the concentration of useful wild plants into accessible stands; small-scale plant cultivation; the burning of vegetation to encourage useful animals and plants; and hunting practices that modify animal populations. Only the second is likely to cause genetic change in the exploited species and thus qualify as ‘domestication’ (see above), but all four can usefully be termed ‘low-level food production’ [2,3].

One contribution of 13 to a Theme Issue ‘Human niche construction’.

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camp. By discarding non-edible parts of fruit, including seeds, near camp sites, they unconsciously intensify fruit tree production. This practice creates what Politis [4] calls ‘wild orchards’ in abandoned camp sites. Although old camp sites are not reoccupied, the concentration of fruit trees creates small patches in the ecosystem, reducing subsequent travel time to harvest fruit. Politis points out that because the forest canopy is not cleared (as it is in horticulture and swidden cultivation), weed growth that would otherwise choke wild food plants is prevented. The more intensive husbandry of nut trees during the later Jomon in Japan (see below) may represent a development of such practices. In view of the previously argued difficulties of hunting and gathering in tropical forests, might such behaviour have been more widespread in such environments? Archaeologists are divided on the capacity of tropical forests to support hunting and gathering. Various authors [5,6] have persuasively argued that hunter – gatherers could only survive in tropical forest if they had access to cultivated plant resources obtained from neighbouring farmers. More recently, Froment (2000, personal communication) and Fairbairn et al. [7] have argued for more nuanced interpretations. Fromont reports that wild yams are sufficiently dense in some parts of the African tropical forest to support pure hunting and gathering, but not in other parts [8]. Fairbairn et al. [7] agree that the forests of the New Guinea highlands contain few plant foods, but argue that the first human colonists may have used selective burning as early as 30 000 BP to increase the productivity of fruit-bearing pandanus plants. Altman [9] dispelled the myth created by McCarthy & McArthur [10] that hunter – gatherers in Arnhem Land (Northern Australia) need only work 4 to 5 h per day to obtain enough food. Altman lived with an Aboriginal band for an entire year, and discovered that in the days before purchased food was available the three wet season months would have been the most difficult to survive. Altman [8, pp. 80–1, 90–1] calculates that, if women had worked at gathering 63 h per week during the wet season (February– April), the highest productivity they could have achieved would have been 1600– 1800 kcal d21. Altman’s findings are supported by those of Jones [11] that, during the critical month of April, women would have had to dig for yams 28 out of 30 days to provide their 50 –60% contribution to the diet. Such seasonal bottlenecks may well explain why hunter – gatherers normally appear to live at below the carrying capacity of the land ([12] gives other examples). Jones & Meehan [13] documented the practice, in Arnhem Land, northern Australia, of leaving the top of the tubers of harvested long yams (Dioscorea transversa) in the ground, and one of us (R.L.) was present when, during a 1974 fieldtrip to Cape York, a local Aboriginal man, Bill McGreen, described the same practice to David Harris. Aboriginal women told Jones & Meehan that ‘plants left in this condition will grow again the following year’. Given the vital importance of yams in the annual food gathering cycle, why is their husbandry not intensified? Jones [11, p. 139] speculates as to why yams were not Phil. Trans. R. Soc. B (2011)

more intensively husbanded in Arnhem Land. He concludes that the prolonged dry season precludes intensification, in contrast to wetter environments in New Guinea Highlands. As we describe below, however, yams were intensively husbanded in southwest Australia until colonial expropriation of the land.

(b) Small-scale plant cultivation Various groups of humans conventionally regarded as hunter – gatherers have in fact cultivated plants on a small scale. In eastern North America before the arrival of maize cultivation from Mexico around AD 1000, several native species were cultivated. This is demonstrated by the genetic changes that cultivation caused; these species therefore qualify as ‘domestic’ under the definition put forward above. The seeds of squash (Cucurbita pepo ssp. ovifera) become larger from 2500 BC, testifying to human selection. Sumpweed (Iva annua) and sunflower (Helianthus annuus var. macrocarpus) provide similar evidence from 2000 BC. In goosefoot (Chenopodium berlandieri ssp. jonesianum) the domestic form has a thinner testa (seed coat) than the wild forms. A thinner testa means reduced dormancy, i.e. the seed germinates faster, so this suggests artificial selection for early germinating individuals. Cultivation of this plant started around 1500 BC and was recorded by Europeans until the eighteenth century; the cultivar is, however, now extinct and known only from the archaeological record. These genetic changes must have been engineered by the repeated planting of seeds from plants with the desired characteristics [3,14 – 16]. Maygrass (Phalaris caroliniana) and little barley (Hordeum pusillum) were not apparently genetically modified, but are found in archaeological contexts well outside their wild range, suggesting that their distributions were extended by cultivation [15]. Tobacco cultivation also has an antiquity of several millennia in this region, although it is not known whether this was of native Nicotiana attenuata or Nicotiana trigonophylla, or of domestic Nicotiana rustica introduced from Mexico, because the seeds are indistinguishable [17]. In Japan, rice cultivation arrived in the first millennium BC. Hunter – gatherers prior to this lived mainly on nuts and marine resources, but also made use of cultivated millets and/or their wild relatives. It is, however, impossible to distinguish between wild barnyard grass (Echinochloa crus-galli ) and its domestic relative Japanese millet Echinochloa esculenta, and the same is true for species of Setaria (domesticated foxtail millet and its wild relatives). Other plants including Chenopodium spp. and the beefsteak plant (Perilla frutescens) are also found. Genetic change has not been suggested for these plants, but it is possible that they might have been cultivated. None of these ever rivalled nuts or fish in importance [18,19]. Reduced genetic diversity has however been detected in archaeological remains of chestnuts (Castanea crenata) dating to ca 4500– 2500 BC. This suggests that chestnut trees were under prolonged human selection [20]. Early British explorers in Southwest Australia during the 1830s and 1840s reported that Native communities practised husbandry of wild Dioscorea.


Foraging and farming George Grey, quoted in Hallam [21, p. 139], described an extensive area perhaps measuring 5– 6 km by 2 km covered in a ‘light fertile soil quite overrun with warran plants . . . a species of Dioscorea, a sort of yam like the sweet potatoe’, approached by permanent paths and watered by deliberately constructed dykes. He also recorded two native villages containing substantial huts that were apparently permanently occupied, with ‘well-marked roads, deeply sunk wells and extensive warran grounds’, These were not exceptional, and Hallam quotes numerous similar records from the same region, some of which indicate that production of wild flags was also intensified to enable permanent residence during the time of year that yams were regenerating. Hallam interprets such practices as an intensification of the wild yam harvesting recorded by Jones in Arnhem Land (see above), and concludes that archaeological evidence indicates Dioscorea cultivation had been practised for about 4000 years. The Southwest Australian case may have resembled that recorded ethnographically among the Nuaulu of Eastern Indonesia, who both collect wild sago from Metroxylon palms, and cultivate these palms in swiddens. The Nuaulu have a mixed economy, combining hunting and gathering with cultivation of coconut and sago. Ellen [22] calculates that nondomesticated foods contribute 41 per cent of kcalories in the diet, but at least 56 per cent of energy expended in subsistence goes on obtaining wild resources. Part of these costs arise through travel and transport. Cultivating sago palms around villages reduces such costs, but imposes the burden of cutting and burning the swiddens. It thus appears that the relative effort the Nuaulu choose to allocate to the two modes of subsistence is relatively finely balanced, and could be tipped either way by a change in ecological or social circumstances.

(c) Burning of vegetation The Ju/’hoansi (!Kung) hunter– gatherers of the Kalahari used controlled burning in late winter and early spring to encourage the growth of new grass and hence to attract game [23]. While grass seeds appear to be a famine food in the Kalahari, they are, or were, more commonly eaten by native peoples in North America and Australia. Stewart [24] documented the widespread use of controlled burning in North America as a means to increase the yields of wild grass seeds and berry- and nut-bearing plants, as well as promoting the availability of forage for game animals (for a case study, see [25]). In Alberta, native people set controlled meadow fires in early spring, when grasses were dry enough to burn but the surrounding forest too damp to catch fire. This caused new grass to spring up two to three weeks earlier than would occur naturally, attracted game, and increased the yield of berries on sunlit forest margins. Reeds and grasses on lake margins were burned to improve the feeding and nesting areas of ducks and geese, and to improve the growth of the roots on which musk rats depended [26]. Phil. Trans. R. Soc. B (2011)


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The Alawa, living in savannah woodland south of the Gulf of Carpentaria, northern Australia, gave R.L. two principal reasons for burning the bush: to make walking easier by burning dead wood lying on the ground, and to clear vegetation so that new grass would provide feed for kangaroo. Responsibility for controlled burning is rigorously allocated to the sister’s sons of men born into the land-holding clan, since it is their responsibility to ensure that sacred trees are not damaged. Burning should take place at the start of the dry season. Among the Anangu of the Western Desert, where residence is more important than descent in determining a person’s local group affiliation, practising controlled burning is one of the traditional ways in which an individual demonstrated their commitment to ‘holding the country’ of a particular band, along with keeping waterholes clean and performing rites at sacred sites. After the Federal Australian National Parks Service allowed the resumption of controlled burning by traditional owners in the Uluru National Park, the impact of patch burning was studied. The Parks Service noted that spinifex grass, while providing shelter for small birds, mammals and reptiles, had little food value. Patch burning cleared areas of spinifex and allowed food plants to regenerate, on which both animals sheltering in nearby spinifex and humans could feed [27]. These findings have been reiterated and extended by Bliege Bird et al. [28], through their work with the Martu, in a more westerly district of Australia’s Western Desert. Bliege Bird et al. found that the majority of controlled burning takes place during women’s foraging for monitor lizards and other small- to medium-sized prey. Mature spinifex grass is burnt to reveal lizards’ burrows. The Martu know that burning allows food-bearing plants to regenerate. Aerial photographs show that human patch-burning creates a more fine-grained succession of vegetation types than do lightning-induced wild fires; the starker vegetational distribution caused by wildfires is most common furthest from Aboriginal camps [27,28]. The longer camps are occupied, the more visible the distinction becomes [28]. Stewart [24, p. 119] noted that Euro-American forestry practices had deprived the Klamath and Pomo peoples of the Western United States of much traditional hunting territory, by preventing seasonal burning and thus allowing the uncontrolled growth of trees and brushwood. Dods [29] has spelled out the disastrous consequences of such practices for wildlife. The Australian Northern Territory Government policy of discouraging Aboriginal residence at Uluru put a stop to the traditional practice of controlled burning, resulting in destructive wildfires during 1950 and 1976. The re-introduction of controlled burning in the Uluru National Park after it was returned to Aboriginal ownership similarly resulted in the return of the striated grasswren (Amytornis striatus), and protected the malgara, a rare carnivorous marsupial (Dasycersus cristicauda) [27]. Palynological evidence for increased frequency of fires in Australia, presumably the result of human activity, goes back to 38 000 BP [30], perhaps 60 000 BP [31].


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Prehistoric hunter –gatherers elsewhere can sometimes be shown to have burnt vegetation in analogous ways. Mellars [32, p. 16] concludes that ‘the deliberate and systematic burning of vegetation was an almost universal practice among recent hunting and gathering populations occupying forested or shrubland environments’ (and see [7]). In Britain, palynology has revealed signs of clearance attributed to human activity going back to about 9000 BC, early in the Mesolithic [33]. Very detailed work has been carried out at North Gill in Yorkshire covering the period 5000– 4000 BC. Eleven pollen profiles were examined over just 350 m of a shallow valley; high-resolution sampling enables changes to be examined over periods as short as three years. This has revealed short-term clearance, burning and regeneration, the clearings themselves being remarkably small: tens rather than hundreds of metres in diameter [34,35]. Such niche construction would benefit humans in two ways. First, the fire-resistant hazel would be encouraged, leading to an increase in the productivity of its highly nutritious nuts. Acorns have been widely eaten by recent hunter– gatherers, and Mesolithic people might also have used fire to encourage acorn productivity [36]. Second, ground vegetation such as grasses and herbs would be encouraged, and this would both attract game animals, such as red deer, and allow their overall numbers to increase. One estimate is that a systematic burning regime might cause deer populations to multiply as much as tenfold [32]. Jones [37] famously termed controlled burning ‘firestick farming’, and it is not unreasonable to regard swidden cultivation as an intensification of controlled burning.

(d) Hunting as niche construction Hunting may amount to niche construction in a variety of ways. Here we consider three. Competitor removal involves the displacement of competitor species whose niches overlap with that of the human hunters. When modern humans entered Ice Age Europe over 30 000 years ago, the continent was dominated by several large carnivores. By 20 000 years ago the cave lion and cave hyena had become extinct, followed by the largely vegetarian cave bear [38]. Whether humans ever actively hunted these animals or merely out-competed them is unknown. Their population densities were probably low, so indirect competition could have been sufficient. Neanderthals were also resident, and were extinct by 28 000 years ago [39]. Stable isotope analysis of Neanderthal bones shows that they were apex carnivores [40]. Climatic change as a cause of extinction is unconvincing, so competition with modern humans is probable [41]. The archaeological record reveals little about the nature of this competition, although a 30 000 year old probable Neanderthal mandible from Les Rois suggests that it was sometimes direct. The mandible was found in a stratum containing bones of modern humans, artefacts and ornaments of modern human manufacture, and bones of hunted animals. The Neanderthal mandible had cut marks on it identical Phil. Trans. R. Soc. B (2011)

to those on the bones of the prey species. One possibility is that this Neanderthal was hunted and eaten by the modern humans [42]. Whatever the truth of this, modern humans arriving in Europe encountered a variety of native carnivore species that had survived several previous glacial cycles. When the subsequent cycle ended, modern humans were the only remaining large carnivore. This can hardly be coincidence. Niche deterioration occurs when human hunting causes a hunted population to decrease or become extinct. According to Optimal Foraging Theory, resources may be ranked according to their energetic return per hour expended in their acquisition. Higher ranked resources should be exploited while lower ranked ones should not; the diet breadth model seeks to predict where on the rank scale this division should fall. One key point is that if a high ranked resource becomes less common, for example, through hunting reducing its numbers, it will be encountered less frequently. This may cause hunters to broaden their diet to include previously ignored prey species [43,44]. Particularly clear examples occur when hunter – gatherers colonize new habitats. The arrival of humans in the Americas led to the rapid disappearance around 11 000 BC of some 33 genera of animals weighing over 44 kg. The mammoth and mastodont were the largest of these, and may have been particularly important as ‘keystone species’ that maintained ecological diversity at patch level. Their extinction, and the consequent loss of this diversity, may have caused many of the other extinctions [45]. Faced with this utterly transformed niche, human behaviour altered radically as people began hunting bison and other species. Further north, Palaeoeskimo peoples spread across the American Arctic around 3000 BC. Population levels during the first few centuries appear to have exceeded those at any subsequent time. One probable explanation is that Palaeoeskimo people concentrated on the most easily available prey species, the musk ox, and enjoyed a population boom at its expense. When threatened, musk oxen do not flee but form a defensive phalanx. This deters wolves, but presents an easy target to missile-equipped humans. After a few centuries musk ox populations were much depleted, leading to a human population crash [46,47]. Faunal remains from Palaeoeskimo sites reveal a trend away from musk oxen and caribou, towards marine resources, with a concomitant development of the specialized technology needed to obtain these species [48]. Both these examples resulted in massive cultural change as humans adjusted to the changes they themselves had wrought. Niche enhancement occurs when hunters act to increase the numbers and availability of prey species. Animals may be introduced onto islands to found populations that can be hunted. The earliest known example is the introduction of a marsupial, the cuscus (Phalanger orientalis), from New Guinea to New Ireland around 23 500 years ago; other animals and plants were moved later [49]. Wild boar have been introduced to various islands long before farming was established anywhere nearby: Ireland [50], Okinawa [51] and the Izu Islands [52] were all


Foraging and farming populated in this way. Such introductions are conscious and deliberate acts by hunter– gatherers to construct new niches for themselves. Hunting may enhance a niche in another way. Biologists distinguish between r-selected species, with high rates of reproduction, catastrophic mortality and fluctuating population numbers; and K-selected species, with lower reproductive rates, densitydependent mortality and steadier population numbers. There is a continuum between the two, and behaviour may vary along the continuum depending on circumstances [53,54]. If hunting needs to be intensified, the deliberate targetting of many young can cause the adults to behave in a more r-selected manner and produce more young. In beaver, for example, if juveniles are culled the adults are ‘tricked’ into producing more young the next year [29]. Many Native American groups in the nineteenth century hunted beaver intensively to obtain pelts for sale, and knew exactly what they were doing. As one Ojibwa informant stated: ‘we would only kill the small beaver and leave the old ones to keep breeding. Then when they got too old, they too would be killed, just as a farmer kills his pigs, preserving the stock for his supply of young’ [55, p. 294]. Several aspects of this discussion come together in the Epipalaeolithic of the Near East, around 19– 12 000 years ago. This was a period of increasing warmth and moisture after the Last Glacial Maximum. Previous oscillations of this kind had been accompanied by an increase in fallow deer, because this species is suited to the expansion of woodland that occurred. This time, however, fallow deer decreased in frequency through time. Over-predation is the most probable cause of this, because human populations were increasing at this time [56]. The archaeological record reveals that people were living in larger and more sedentary groups, and this is likely to account for the increasing pressure on the fallow deer [57]. Two things reveal increased population and hunting intensity. First, diet broadened to include several smaller, less energetically productive resources. Previous such episodes had concentrated on slow, easy to catch prey such as tortoise. In the later Epipalaeolithic, however, these were replaced by faster, more elusive prey such as hare, partridge and fox [58], and wild grasses and legumes—the muchdiscussed ‘Broad Spectrum Revolution’. This fits with the prediction of the diet breadth model (see above) that human diets should broaden when high-ranked species become rare [59]. Second, young animals formed an increasing part of the kill of the remaining large mammal, the gazelle [56,57]. It is probable that the hunting of juveniles was a conscious strategy, as it was with the Ojibwa beaver hunter quoted above. The way it might operate is shown in figure 1. Mountain gazelle (Gazella gazella gazella) was the main species exploited in the Epipalaeolithic Levant. These animals rarely produce twins, but in better-watered areas usually produce two offspring per year, births occurring all year round [60, table II]. In the moister conditions of the Epipalaeolithic many, perhaps most, gazelle populations would have achieved this. Young male gazelle Phil. Trans. R. Soc. B (2011)


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remain with their mothers until the age of 15 –18 months, young females even longer [61]. Thus most females would be accompanied by two fawns of different ages. Since juvenile females in well-watered areas usually give birth at the age of 12 months [60,61], the older juvenile in figure 1 might herself be accompanied by another fawn. Encountering a female and two juveniles, a hunter could choose to shoot the mother. Figure 1 assumes that, without her protection, only one fawn will survive and breed. All other things being equal, after five years this will result in three adults (the surviving juvenile and her first two offspring) and two fawns. Alternatively, the hunter could choose to kill one of the juveniles. The other will probably survive to reproduce— and the adult will also continue to breed, resulting in many more gazelle after 5 years. If a gazelle fawn is lost, the mother generally becomes oestrous [61, p. 732], which suggests that gazelle might be ‘tricked’ into increased reproduction in the same way as the beavers described above. This strategy clearly enhances the hunter – gatherer niche. It runs counter to modern European notions of hunting and sportsmanship, but it conforms to our notions of farming and profit—as the Ojibwa informant (see above) was fully aware.

(e) Why did these activities not ‘take off’? We have shown that hunter – gatherers construct niches in a wide variety of ways, far more often than our common understanding of the label ‘hunter– gatherer’ would suggest. Hunter – gatherers are not merely passive recipients of environmental bounty, but are just as aware of the potential of niche construction as farmers. And yet for tens of millennia people continued to exist as what we conventionally term hunter – gatherers. Niche constructions of the types discussed above, and no doubt very many others unknown to us, did not turn into geographically expanding agricultural systems. Many of the niches were stable, bringing about no subsequent human cultural change. Plant domestication in eastern North America was just a small adjunct to the overall hunter – gatherer system. Tobacco provided no food value at all, but was cultivated for its narcotic effects. Trees like chestnut or hazel were not annuals, and must grow for a couple of decades before producing many nuts. Trees are not flexible enough to form the primary basis of an expanding agricultural system. There seems to have been no inherent instability in such niches. Unstable niches by definition cause human cultural change, but commonly result in new hunter – gatherer niches, not agricultural ones. The over-hunting of mammoths or musk oxen led not to agriculture but to transformed hunter – gatherer niches. While hunter – gatherers may thus practise ‘low-level food production’ [2,3], it may however be very difficult to go from here to ‘high-level food production’, i.e. to construct a predominantly agricultural niche. This is suggested by a survey of the economic attributes of over 200 recent ethnographically known societies (figure 2). Gathering contributes little or


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decision now year 1

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outcome in five years 3 adults, 2 fawns

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Figure 1. The choices facing a gazelle hunter upon encountering an adult female with two young of different ages. Left: the outcome if he kills the adult. Right: the outcome if he kills one of the juveniles.

nothing to farming societies, who make up a large percentage of the sample. It makes a progressively larger contribution to an ever smaller number of societies, so that very few depend on it for most of their livelihood. The result is a fairly regular fall-off curve. The same goes for hunting, fishing and herding. Agriculture is however very different. Many societies depend on it for 5 per cent or less of their subsistence—these are the hunter–gatherers. Most of the rest depend upon it for over about 50 per cent of their food. But there are remarkably few who depend upon it for between 5 and 50 per cent [62]. This suggests that hunter–gatherers rarely expand their minor cultivation activities. The 5–50% farming dependence zone is one that societies do not often venture into; it appears to be an unstable intermediate zone that the earliest farmers would have crossed rapidly. So how do hunter –gatherers become farmers? With hindsight, we know that the Epipalaeolithic of the Near East ended with the origins of agriculture, which endows the niche created by Epipalaeolithic intensification with a particular interest. Intensification does not inevitably lead to agriculture, however, and many local intensification trajectories never did so—because when agriculture did emerge in the Near East it did not involve the gazelle or hares or most plant species that had been the targets of local intensification, but a few of the minor ones, and for the most unpredictable of reasons. 3. UNSTABLE NICHES AND THE ORIGINS OF AGRICULTURE The major agricultural systems are classic examples of niche construction. Major agricultural systems appeared in various places around the world. Each involved human control of a restricted range of species; the integration of these species into a mutually supporting working system; Phil. Trans. R. Soc. B (2011)

and their genetic modification. Agricultural communities expanded geographically, spreading around the globe, and modifying as they encountered new environmental constraints and opportunities. Human cultures changed massively as a result of both (i) the development, and (ii) the geographical expansion of agriculture. We concentrate largely on the Near Eastern agricultural system, and stress that the developmental trajectories of other major systems were very different [63]. Agriculture is not just a further intensification of the hunter – gatherer niche but is a new and transformed niche of its own. We argue this in two ways: first, major long-term exploitation of wild cereals and animals does not necessarily lead to agriculture; and second, Near Eastern agriculture was based on species that played relatively minor roles in the Epipalaeolithic economy. (a) The development of the agricultural niche: cereal cultivation Certain cereal harvesting practices induced a cycle of positive feedback leading to full-scale cultivation, while others did not. In Western Asia and the Yangzhe Basin, cereals were harvested with a sickle, selectively favouring non-shattering seed heads that had to be replanted artificially (see below). In the Darling Basin of western New South Wales, Australia, Aboriginal people harvested wild grasses before the seeds had ripened, to prevent seed loss, building hayricks that were burnt when dry to separate seeds from stems, thus avoiding the unconscious selection of nonshattering heads. In 1839 the explorer Mitchell [64, p. 313] described ‘ricks or haycocks’ extending for miles. In sub-Saharan Africa, Jack Harlan has documented the ‘swinging basket’ technique of grass seed production, which favours the selection of shattering


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Figure 2. Percentage dependence on five major economic activities (redrawn after [62, fig. 3]). (a) Gathering; (b) hunting; (c) fishing; (d) herding; and (e) agriculture.

seed heads. Of these three harvesting techniques only one, harvesting with a sickle, creates a (unintended) process of positive feedback leading to full-scale cultivation once seeds are replanted. On Cooper’s Creek, in southwest Queensland, the explorer Gregory in 1887 described ‘fields of 1,000 acres’ of Panicum. He wrote that ‘The natives cut it down by means of stone knives, cutting down the stalk half way, beat out the seed, leaving the straw which is often met with in large heaps’ [64, p. 314]. There is however no record that seeds were replanted. Archaeological evidence for grass seed collection in Australia has been found at 40 000 BP [65]. Grindstones definitely used on plants go back to 30 000 BP [66], although Smith [67] points out the need to distinguish seed grinding from grindstones used more generally for plant processing. In arid Australia, grass seeds were a fall-back food, exploited when more easily harvested plants had been locally exhausted. Brokensha [68], who observed women collecting and processing wild millet, recording that it took three women 3 h to harvest 2 kg of seed and a further 2 h to process the seeds and cook them as damper (unleavened bread). In the Western Desert, grindstones with the distinctive polish created by the silica in grass seeds are only found during the last four thousand years, which Smith [67] interprets as the consequence of people living at a higher population density than in previous periods of higher rainfall, adapting to a new period of increasing aridity. In the Near East, the agricultural niche was completely different from its hunter – gatherer predecessor. The literature dealing with the phenomenon is huge, and we can do no more than allude to some relevant aspects. After millennia of ameliorating climate following the Last Glacial Maximum, the Phil. Trans. R. Soc. B (2011)

abrupt Younger Dryas oscillation at ca 10 500 – 9500 BC marked a major reversal to colder and drier conditions. Many have argued that this destabilized the Epipalaeolithic way of life [69,70]. Epipalaeolithic plant exploitation involved a wide array of species. At Abu Hureyra in Syria, over 250 species were probably consumed, some 120 of these being seed foods. Wild einkorn wheat and rye were among these, but the most important were clubrush (Bolboschoenus [¼Scirpus] maritimus), Euphrates knotgrass (Polygonum corrigioloides) and feather grasses (Stipa spp.) [71]. Species frequencies at other sites vary but wild wheats and barley were at best of modest importance [72]. Club-rush produces not just seeds but also tubers; relatively complex processing is required to turn these into edible flour, but the technology was available in the Epipalaeolithic [73]. Near the end of the Epipalaeolithic, when the Younger Dryas was exerting pressure, some plants appear to have been cultivated: einkorn wheat, rye and lentil are all found outside their natural habitats, accompanied by the weedy species that would thrive in cultivated fields; but apart from the enlargement of some seeds, domestication (defined as genetic modification) had not taken place [74]. Cereals were domesticated independently in several different regions of the Near East [63]. The genetic change taken as the definition of this is the development of a non-shattering seed head: wild grass seed heads shatter naturally but domestic ones do not, and cannot therefore reproduce unless they are resown by humans. How the change to intensive cereal cultivation in some areas came about is unclear. A switch from swinging-basket to sickle harvesting has been suggested: if done as the heads were beginning to ripen, sickling would dislodge and lose some seeds


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from wild-type shattering heads, while collecting all of the non-shattering form (this occurs as a rare mutant in wild cereal stands). The non-shattering form would thus be slightly more common in the collected seeds than in the wild stand. If people replanted part of what they had collected, the non-shattering mutant form would be increased. In theory this could lead to 100 per cent non-shattering forms in as little as 25– 200 years [75]. In reality it took somewhere between one and two millennia, as frequencies of the non-shattering form gradually increased on sites over this period [63,76,77]. The precise nature of the selective pressures that caused changes on such time scales needs further elucidation. But the final outcome was that minor Epipalaeolithic wild resources were transformed into major domestic ones that have had a huge influence on subsequent history. (b) The development of the agricultural niche: animal domestication Epipalaeolithic animal exploitation in Western Asia was based on gazelle and (further east) onager. Wild sheep, goat and cattle were relatively minor hunted resources. Yet it was these species that the early cereal farmers used as close-herded domesticates. The intensively hunted gazelle might have seemed a more logical choice—but in common with almost all antelope and deer species they do not form fixedmembership herd units suitable for domestication. Males become territorial during the rut, and frequently fight each other; subdominant males form loose groups moving around the territorial peripheries; and females with their young move fairly freely between territories despite the efforts of the dominant males to constrain them. This is true for almost all species of sub-Saharan ungulates [78], all species of gazelle [79], and all deer [80]. This loose social structure makes close-herding by humans an impossibility. One study of impala as a possible domesticate concluded that: ‘The behaviour of impala does not seem to be compatible with their domestication, for which animals with fixed-membership herds, like buffalo or eland, are more appropriate. The problems experienced by a territorial male impala trying to restrict the movements of a female herd should be observed by anyone who wishes to put himself in the male’s position’. [81, p. 880].

Various domestication experiments have shown that the culling of most males, and investment in fencing and pens, does not solve the problem. Penned males of various sub-Saharan species exhibit aggressive behaviour in seasons when they would be territorial, and attack females and young [82, p. 847]. Gazelle males, in the absence of rivals of their own sex, vent their aggression on females, young, inanimate objects and humans [79, pp. 214 – 215]. Penned red deer are similarly unpredictable and potentially dangerous to humans during the rut [83, pp. 57 – 59]. Rather few wild species have fixed-membership herds. Among them are sheep, goat and cattle. A few sub-Saharan antelope species are similar, but most of these are solitary; only the gregarious eland forms Phil. Trans. R. Soc. B (2011)

larger herds. Eland, like sheep, goat and cattle, do not become territorial during the rut, but maintain a male hierarchy within the herd. Consequently the males do not become territorial during the rut, and herds do not fission and scatter. As a result, ‘the eland, as every Masai herdsman knows, is more like an ox than an antelope’ [78, p. 194]. Experiments have shown that eland is effectively the only antelope species that is amenable to domestication and close human control—they can be managed and milked in exactly the same way as domestic cattle [82,84 – 87]. Animal domestication has thus moved along very narrow taxonomic pathways. The key animal behavioural attribute is the fixed-membership herd based on a male hierarchy within the herd. This behavioural trait renders these species amenable to close herding, because the herd units can be controlled and moved much more easily (figure 3). In the Near East shortly after the domestication of cereals, domesticated herds of sheep and goat rapidly became important, signalled by the presence on archaeological settlements of not just the young males that intensification produces, but also of the elderly females who had reached the end of their reproductive lives [88,89]. As these high-ranked resources became ubiquitous, diet narrowed and the small animals of the ‘Broad Spectrum Revolution’ all but disappeared [90]. Thus the genetics of certain wild grasses, and the social behaviour of certain wild ungulates, were what gave them the potential to be intensified to the point of domestication when the Younger Dryas climatic change brought the intensive Epipalaeolithic exploitation of wild resources to an end. They had not previously been major resources, and an observer would probably not have predicted that these particular species would form the basis of an agricultural system that would transform the face of the globe. Had they not been domesticated, human populations would have decreased and become more mobile— reverted, in other words, to the adaptations of their ancestors at the Last Glacial Maximum.

4. THE EXPORTING OF THE FARMING NICHE A small number of agricultural systems have spread to dominate food production almost everywhere on the planet. In the region where the Near Eastern agricultural system developed, agriculture can support more people per unit area than hunting and gathering. But agriculture as an integrated system closely controlled on a day to day basis by people has a further advantage: it is a niche that can be exported to areas outside the original heartland. Within a few millennia, the Near Eastern system extended from Ireland to northern China (where it encountered and was integrated with the Chinese agricultural system), and from the Urals to the Sudan. No hunter – gatherer niche could match this. The niche was not just transported, it was modified to be able to cope with new environments. Its early spread westward through the Mediterranean required few modifications, because the environment was largely similar to the Near East. The earliest cultivation




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Figure 3. Sheep and goat, demonstrating their amenability to close domestic control. The sheep follow the shepherd (right) or lead sheep, lining up nose to tail, while the goats are in open order formation. Jebel Oustani, Syria, 1983 (photo PR-C).

in eastern Spain used the same four cereals and five pulses as the Near East [91]. But when agriculture spread into temperate Europe the range diminished to just three cereals and the occasional pea and lentil [92]. When it spread further north into Scotland, some farmers initially cultivated a substantial proportion of emmer wheat. Within a few centuries this had been replaced by barley, a crop much better suited to the Scottish environment [93]. The frequency of animals was also adjusted to suit local conditions: in temperate European forests sheep and goat, dominant in the Mediterranean, gave way to cattle and pigs [94]. In a pioneering study, Clark [95] argued that the subsequent increase in sheep was a result of forest clearance and the creation of open grassland by farmers, a further modification of the farming niche. Forest clearance was a major outcome of the arrival of the Near Eastern farming niche almost everywhere. The transformation of local ecosystems, which continues to this day, involved the reduction of native plant and animal communities, and the destruction or absorption of local hunter – gatherers. The effects naturally varied depending on local circumstances. Some species such as roe deer have accommodated themselves reasonably well to the peripheries of the agricultural landscape. In Europe, wild oats and rye were initially native weeds that spread into wheat and barley fields, but eventually they did so well that they were taken into cultivation in their own right [96]. For many other species the arrival of agriculture spelt disaster; for example, when Polynesian agriculturalists arrived in New Zealand they eradicated the giant flightless moa in about three centuries [97]. Agricultural immigrants would face their biggest problem in their first months in a new area, before their newly planted crops could provide food. They coped in various ways. In Europe, the transport of lactating cattle Phil. Trans. R. Soc. B (2011)

may have enabled people to use dairy products in this interval [98]—dairying has recently been identified among the earliest agriculturalists in Anatolia [99]. This option was not available in the Pacific, so local wild resources bore more of the brunt. A wide variety of native species including large flightless birds and terrestrial crocodilians inhabited the various islands. One estimate is that as many as 8000 taxa became extinct across the Pacific as humans arrived [100].

(a) Can farming form a stable niche? Probably the biggest single process tending to destabilize farming as a form of niche construction is population increase. Contrary to many theorists (e.g. [101,102]), we do not regard the origin of farming as a response to population pressure. We have cited seasonal shortfalls of wild foods as one factor limiting hunter – gatherer population growth. Other factors include the difficulty of carrying children, and the low body fat levels sustained by mobile women living on wild resources. Richard Lee calculated that an adult Ju/’hoansi woman walked about 2400 km yr21. For the first two years of life, a child was carried on the mother’s back. From three years of age, children could be left at times in camp with a babysitter, but children were still carried long distances up to the age of four. These data enabled Lee to calculate that a Ju/’hoansi woman giving birth once every four years would carry an average child load of 9.2 kg d21, but one giving birth every two years would carry an average child load of 17.0 kg d21 [103, p. 325]. Wilmsen found that foraging !Kung suffered double the weight loss pastoral !Kung experienced during lean months. He concurred with other authors that foraging !Kung women averaged only 4.5 live births in their lifetime, while women who had adopted agro-pastoralism and sedentary


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village life had an average of 7 live births [104]. Wilmsen’s findings also agree with Jones’ conclusion that birth spacing among the contemporary Australian Gidjingali is half the 4 – 5 years it appears to have been before contact [11, pp. 134 – 135]. We do however consider population increase to be the main motive force behind the geographical spread of farming. Demographic expansion can be matched by emigration and the export of the farming niche— not an option available to most hunter– gatherers. Farming has however not always been sustainably implemented. It crossed Europe in a series of rapid moves punctuated by lengthy pauses [98]. On the Vistula River, farming reached to within 200 km of the Baltic coast by 5400 BC. The first farming settlements near the coast were established by 5000 BC—but this penetration failed and hunter – gatherers reoccupied the area [105]. Farming was only permanently established on the coast around 4000 BC, in another major spread. The spread at this time reached across the Baltic into Sweden, extending rapidly to north of Stockholm—but once again the advance was not sustained, and the farmers were replaced by hunter – gatherers shown by ancient DNA extracted from the human skeletons to come from the Northeast Baltic [106]. The northern edge of farming retreated to the southernmost part of Sweden for several centuries. Instability of the farming niche may also occur in more mature agricultural regimes. The Norse occupation of the Faroes, Iceland and Greenland from the ninth century AD introduced agriculture into pristine but simple environments. Considerable environmental damage ensued. As agriculture moved west, it was progressively less suited to the environments it encountered. In Greenland a combination of circumstances including environmental degradation and climate change led to the extinction of farming after some 400 years [107]. Britain provides a prehistoric analogue: farmers moving into the northern and western uplands cleared the oak and hazel woodland, exposing the soils to the increasing rainfall. This led to podsolization, acidity and the growth of peat over what had previously been agricultural land. Dartmoor provides a clear example: farming expanded and the woodland was cleared around 1600 BC, but after some centuries of animal grazing peat began to grow around 800 BC and the area was abandoned [108]. Much of Britain’s moorland is in fact not a ‘natural’ landscape at all, but was created by the self-destruction of the farming niche. Malthus [109] is famous for identifying the population cycles that accompanied European farming and recognized that the stability of farming depends crucially on the stabilising of the population practising it. After developing his hypothesis that populations increased faster than their food supply, Malthus travelled through Europe in search of supporting data. He was surprised to discover that Alpine populations appeared to have stabilized, and proposed a homeostatic regulatory mechanism to account for this. Malthus argued that the peak demand for labour occurred at harvest time, to collect sufficient hay to feed stabled livestock through the long winter. Since the productivity of meadows was determined by Phil. Trans. R. Soc. B (2011)

hay

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manure

labour

milk/cheese

Figure 4. Diagram showing Malthus’ view of the relationship between resources, labour and productivity in Alpine regions.

supply of manure, the available hay and livestock each limited the other. Food production, determined by the number of livestock, in turn limited the number of people who could survive and hence the available labour force (figure 4). A peasant to whom Malthus spoke near the Lac de Joux explained that, even though he himself had married young, late marriage was needed to prevent over-population and bring birth and death rates into equilibrium. Malthus noted that where cottage industry had provided alternative income, age at marriage fell and the population increased [109, pp. 210 – 212, 110]. Viazzo adds that the optimum population level is that at which average output per head is maximized. If it falls below a lower threshold, crucial communal activities cannot be performed; if it rises above a higher threshold the available labour will exceed productive capacity [110]. The U.S. anthropologist Netting studied records of birth, marriage and death over 300 years in a Swiss Alpine village, To¨rbel, which practises partible inheritance. Although the villagers never quite stabilized their population, and always relied on some outmigration, Netting found that each time the village had suffered a higher than usual death rate from an epidemic, the age at marriage fell, then gradually rose again as the population level was restored [111,112]. Franche-Comte´, on the French border with Switzerland, also practised late marriage and high celibacy during the nineteenth century [113]. Between 1650 and 1850 the population had been rising steadily. Although the French industrial revolution enabled those at the bottom of the social hierarchy (farm labourers and domestic servants) to escape to the cities and relieve population pressure, there were still some households in the mid twentieth century whose older members were celibate. Villagers some 20 km from the Lac de Joux told Layton that adult celibacy was a deliberate strategy to prevent the division of family land holdings under the local principle of partible inheritance. Division of the land could be averted by forming a joint holding in which all children have equal shares, although only one son was allowed to marry. The cadastral surveys of village fields show the average size of parcelles (strips) did not diminish


Foraging and farming between 1834 and 1965, despite the rule of partible inheritance. An area of land divided into 304 parcelles in 1834 was divided into 254 parcelles in 1965 [113, pp. 151 – 152]. We conclude that, viewed dispassionately, increasing food production does not appear to be an effective strategy for achieving demographic and political stability in the world’s farming populations. Whether farming will provide a stable solution to human subsistence, it is, as Zhou Enlai said of the supposed benefits of the French Revolution, ‘too early to say’.

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We would like to thank Gary Crawford, Gayle Fritz, Sandra Knapp, Natalie Munro and Jim Savelle for their assistance. Any imperfections remain our own.

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Research

Evolution of lactase persistence: an example of human niche construction Pascale Gerbault1,*, Anke Liebert1, Yuval Itan1,3, Adam Powell1,4, Mathias Currat5, Joachim Burger2, Dallas M. Swallow1 and Mark G. Thomas1,3,4,6 1

Research Department of Genetics, Evolution and Environment, University College London, Wolfson House, 4 Stephenson Way, London NW1 2HE, UK 2 Institute of Anthropology, Johannes Gutenberg University, AG Palaeogenetik, SBII-2 Stock-Raum 02-333, Colonel Kleinmann-Weg 2, 55128 Mainz, Germany 3 CoMPLEX (Centre for Mathematics and Physics in the Life Sciences and Experimental Biology), University College London, Physics Building, Gower Street, London WC1E 6BT, UK 4 AHRC Centre for the Evolution of Cultural Diversity, Institute of Archaeology, University College London, 31 – 34 Gordon Square, London WC1H 0PY, UK 5 Laboratory of Anthropology, Genetics and Peopling History (AGP), Department of Anthropology and Ecology, University of Geneva, 12 rue Gustave-Revilliod, 1227 Geneva, Switzerland 6 Evolutionary Biology Centre, Department of Evolutionary Biology, Uppsala University, Norbyvagen 18D, 752 36 Uppsala, Sweden Niche construction is the process by which organisms construct important components of their local environment in ways that introduce novel selection pressures. Lactase persistence is one of the clearest examples of niche construction in humans. Lactase is the enzyme responsible for the digestion of the milk sugar lactose and its production decreases after the weaning phase in most mammals, including most humans. Some humans, however, continue to produce lactase throughout adulthood, a trait known as lactase persistence. In European populations, a single mutation (213910*T ) explains the distribution of the phenotype, whereas several mutations are associated with it in Africa and the Middle East. Current estimates for the age of lactase persistence-associated alleles bracket those for the origins of animal domestication and the culturally transmitted practice of dairying. We report new data on the distribution of 213910*T and summarize genetic studies on the diversity of lactase persistence worldwide. We review relevant archaeological data and describe three simulation studies that have shed light on the evolution of this trait in Europe. These studies illustrate how genetic and archaeological information can be integrated to bring new insights to the origins and spread of lactase persistence. Finally, we discuss possible improvements to these models. Keywords: lactase persistence; niche construction; Neolithic; domestic animals; dairying; natural selection

1. THE BIOLOGY OF LACTASE PERSISTENCE (a) Niche construction, lactase persistence phenotype and genotypes In biological evolution, natural selection acts on traits that are heritable. The vast majority of these traits are inherited by the transmission of DNA sequences from parent to offspring, i.e. genetic inheritance. But other aspects of the biology of an organism can be inherited extra-genetically, such as certain culturally transmitted behaviours [1,2] and features of the environment that have been shaped by ancestral populations [3]. Since this kind of extra-genetic inheritance can play a key role in the survival of an organism and the

evolutionary trajectory of a species, it has been assigned the term ‘niche construction’ [4,5]. A deeper understanding of the relationship between genetic evolution and niche construction can come from evolutionary theory, notably by recognizing that humans are far from unique in their ability to change their own selective environments [6]. However, because human culture has strongly modified our environments with such remarkable ecological and evolutionary consequences [2], human gene – culture coevolution provides some of the clearest and most spectacular examples of niche construction. Gene – culture coevolutionary theory integrates cultural variation in the analysis of differential transmission of genes from one generation to the next [7]. This theory can be explicitly used to explore the evolutionary consequences of niche construction when a stable transmission of learned information is conveyed


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between successive generations [8,9]. Indeed, cultural processes can change the human selective environment and thereby affect which genotypes survive and reproduce [1,2]. If the cultural inheritance of an environment-modifying human activity persists for long enough to generate a stable selection pressure, it will be able to co-direct human evolution. There are many examples of this in human evolution [1 – 3,10] but none are so well studied, clear-cut, widespread and well supported as the coevolution of lactase persistence (LP) and dairying [4,11– 13]. Lactose is the main carbohydrate in milk and is a major energy source for most young mammals. The enzyme responsible for hydrolysis of lactose into glucose and galactose is lactase (or lactase-phlorizinhydrolase, LPH). Without this enzyme, mammals are unable to break down and thus use lactose, and since milk is the essential component of young mammals’ diet, lactase activity is fundamental to the early development of most mammals. After the weaning period is over, lactase production usually declines, although the mechanisms and evolutionary reasons for this downregulation are not fully understood. However, some humans continue to express lactase throughout adult life, and are thus able to digest the lactose found in fresh milk. This trait is called LP. The LP trait frequency is found in around 35 per cent of adults living in the world today [14,15], but varies widely among human populations, both between and within continents (figure 1a). High frequencies of LP are generally observed in northern European populations. Indeed, LP frequency can vary from 15 – 54% in eastern and southern Europe to 62 – 86% in central and western Europe, and to as high as 89– 96% in the British Isles and Scandinavia [15,16]. In India, LP frequency is higher in the north (63%) than further south (23%) or east [17]. There are relatively little data on East Asians but it seems that the trait is rare there. In Africa, the distribution of LP is very patchy, with high frequencies being observed mainly in traditionally pastoralist populations [14,18 –20]. For example, LP reaches 64 per cent in Beni Amir pastoralists (Sudan), whereas in Dounglawi (Sudan), a neighbouring non-pastoralist population, LP frequency is around 20 per cent [11,21,22]. In recent years, a number of single nucleotide polymorphisms (SNPs) have been found in association with the LP trait in different populations. The first to be identified, 213910*T, is found not in the LCT gene (the lactase gene) but within an intron of a neighbouring gene, MCM6 [23]. In vitro studies indicate that this nucleotide change affects lactase promoter activity [24,25] and thus is highly likely to cause LP, although it is currently not possible to exclude tight linkage disequilibrium with another, as yet unobserved, functional variant. An interpolated map showing the global distribution of 213910*T can be seen in figure 1b, using published data [14,15,26 – 30] supplemented with recently collected data. A cursory comparison of figure 1a,b shows that while the 213910*T allele may explain the distribution of LP in Europe, it cannot explain the distribution of LP in Africa or the Middle East. Indeed, Mulcare et al. [31] Phil. Trans. R. Soc. B (2011)

showed this formally using a robust statistical framework, and other studies have identified additional LPassociated alleles that explain much of the distribution of LP in Africa [16,20,32]. Interestingly, all these variants are located within 100 nucleotides of 213910*T in the same intron of the MCM6 gene, a region that is functionally important for the expression of lactase in vitro [24,33]. Because these various LP-associated alleles are found on several different haplotypic backgrounds [14,20,34], it is now clear that LP has evolved multiple times and is thus an example of convergent evolution [35]. Using genetic variation in regions surrounding LCT, it is possible to obtain estimates of the age of specific LP-associated alleles. Dates of origin for 213910*T ranging between 2188 and 20 650 years ago [36], and between 7450 and 12 300 years ago [37] have been obtained using extended haplotype homozygosity (EHH) and variation at closely linked microsatellites, respectively. Similar dates (1200– 23 200 years old) were also obtained for one of the major African variants (214010*C) using EHH [20]. These date estimates are remarkably recent for alleles that are found at such high frequencies in multiple populations. It is easy to envisage recent alleles being rare since they change in frequency slowly, and in a directionless way, by genetic drift. However, a recent allele that has reached such high population frequencies requires more than genetic drift alone; it requires the extra ‘kick’ of natural selection. Indeed, the estimated selection strengths required to explain the age/frequency distributions of 213910*T [36]—and of 214010*C [20]—are enormous (1.4–19 and 1–15%, respectively), which are among the highest estimated for any human genes in the last approximately 30 000 years [36,38].

(b) Selection hypotheses on lactase persistence The reasons why LP should provide such a selective advantage are still open to debate (see discussion below). However, since this trait has been mainly identified in dairying-practising or pastoralist populations [11] and since fresh milk and some milk products are the only known naturally occurring sources of lactose, it is unlikely that LP would be selected without a supply of fresh milk. Interestingly, the date estimates for the emergence of 213910*T and 214010*C bracket archaeological dates for the spread of domestic animals and dairying into Europe and the spread of pastoralism in Africa (south of the Sahara, into Kenya and northern Tanzania), respectively [11,20,39– 42]. This supports the idea that LP coevolved with the cultural adaptation of dairying as a gene –culture coevolution process. Nonetheless, the correlation between LP and milk consumption is not complete [11,16,31,32]. In lactase non-persistent individuals, the fermentation by colonic bacteria and osmotic effects of undigested lactose often cause symptoms such as abdominal pain, bloating, flatulence and diarrhoea. However, it has been shown that some lactase non-persistent individuals can consume lactose-containing products without any obvious ill effects. For example, the low LP



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Figure 1. Interpolated maps of the distribution of LP and the 213910*T allele in the ‘old world’. (a) LP phenotype distribution. Data points (dots) were taken from the literature (see text and [14] for details). (b) Distribution of the allele 213910*T, associated to LP. Dots represent sample data taken from a previous review [14,26–30]; crosses represent data for new locations not previously tested and diamonds correspond to locations where additional data have been added. Regularly updated frequency data are available at http://www.ucl.ac.uk//mace-lab/GLAD/ website.

frequency of Somali people living in Ethiopia does not prevent them from drinking more than 500 ml of milk per day without any obvious discomfort [16]. This inter-individual variation of the amount of lactose tolerated by lactase non-persistent people may be a result of variation in the composition of the gut flora (particularly the presence of lactic acid bacteria) [16,43]. Also, fermented dairy products (i.e. yoghurt or cheese) contain less lactose, allowing consumption by non-persistent individuals without any of the expected symptoms [43]. Two contrasting theories have been proposed to explain the co-distribution of LP and dairying practices. The culture-historical hypothesis [11,12,44] argues LP developed, and was consequently selected, after milk production and dairy consumption spread. The opposing hypothesis (mentioned in McCracken [12] as the reverse-cause hypothesis) proposes that only populations whose frequency of LP was high enough adopted dairying. In other words, human groups were differentiated with regards to LP frequency by a process unrelated to milk consumption—through genetic drift [45]—before the invention of dairying. This view specifically assumes that drinking milk would not Phil. Trans. R. Soc. B (2011)

necessarily have conferred any selective advantage. The culture-historical hypothesis is better supported by recent findings from archaeological research (see §1c for details). In particular, organic residues preserved in archaeological pottery provided evidence for the use of milk after 8500 BP in the western part of Turkey [40], a region where LP frequency is low today (figure 1a). It suggests that domestic animals were milked before LP arose or was present at appreciable frequencies.

(c) The advantage of being lactase persistent Several explanations have been proposed for how and why LP may have been selected. For example, it may simply be that milk is a good source of calories, or specifically an important source of protein and fat. The milk production of a prehistoric cow has been estimated to range between 400 and 600 kg per weaning period. Even when the milk necessary for the raising of the calves is subtracted, some 150 – 250 kg remains [46]. This is almost equivalent to the calorie gain from the meat of a whole cow. Hence, over the years, milking may have resulted in a greater energy


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yield than the use of cattle for meat. But it is likely that the benefits LP gave to early dairying populations extend beyond simply increasing the food supply or making more economic use of livestock. Furthermore, the specific benefits of dairying may have varied in space and time. Strong selective pressures on LP may have been episodic and occurred only under certain extreme circumstances, such as drought, epidemic or famine. For example, milk would have represented an alternative food resource in between periods of crop cultivation. When no cereal food was available, for example between harvesting seasons or in periods of crop failure, LP individuals would have had an advantage. This is especially true for children after the period when lactase production is normally downregulated, a phase of life that shows an increased mortality according to osteological investigation of prehistoric skeletal collections [47,48]. In addition, Cook & Al-Torki [49] hypothesized that in regions where water was scarce, milk would have been used by pastoralist groups as relatively pathogen-free fluid. If by drinking fresh milk, lactase non-persistent individuals were at risk from the potentially dehydrating effects of diarrhoea under such conditions, selection may have been strong in lactase-persistent individuals. However, this arid climate hypothesis is less likely to have been relevant in Europe, where LP frequencies are at their highest. The observed correlation between latitude and LP frequency in Europe led Flatz & Rotthauwe [50] to propose the calcium assimilation hypothesis. Calcium is essential for bone health and its absorption in the gut is dependent on the presence of vitamin D. While some food sources such as fish are rich in this vital nutrient, most people in the world produce the majority of their vitamin D photochemically in the skin through the action of UVB on 7-dehydrocholesterol. However, UVB exposure is insufficient to produce the required quantities of vitamin D in people living at high latitudes for much of the year. This is unlikely to have been a problem for preNeolithic European hunter– gatherers who would have had a vitamin D-rich diet through their consumption of marine foods [51], but may have been a problem for early agriculturalists. Additionally, it has been proposed that a fibre-rich diet, owing to high consumption of cereal grains, can lead to a reduction in the amount of plasma 25-hydroxyvitamin D3 [52]. Thus, the consumption of milk has been suggested to have conferred an advantage to early LP farmers in regions such as the circum Baltic/North Sea area, where climatic conditions allowed high crop cultivation and consumption. Because milk contains small quantities of vitamin D and plenty of calcium, it can provide a valuable supplement at low-sunlight latitudes. Bloom & Sherman [53] formulated the ecological dairying barrier hypothesis to complement the culture-historical model. They suggested that dairying, and therefore the evolution of LP, required environments that are favourable for raising milk-producing ungulates. Others proposed that the LP distribution is related to malaria [54]. They implied that LP is the ancestral phenotype and that lactase nonPhil. Trans. R. Soc. B (2011)

persistence would have been selected in regions where the disease was frequent. However, this hypothesis was not supported by studies of lactase non-persistence prevalence in glucose-6-phosphate dehydrogenase deficient subjects from Sardinia [55,56]. In a contrasting hypothesis, it has been suggested that a milk diet would provide protection against malaria by impairing a part of plasmodia metabolism (folate synthesis) [52] and thus lead to selection for LP. Pointing to the tight relation between dairying and LP, it has also been hypothesized that milk drinking was a privilege restricted to some individuals in highly hierarchical societies and that it spread as prestige class behaviour [13,44,57]. (For further discussion on the spread of a prestige-associated culture, see [58].) A common feature of most populations with high frequencies of LP is a history of dairying activity [11]. The availability of fresh milk to some human groups has challenged their niche, thereby creating a potential genetic feedback for a need of continuous lactase expression throughout adult life. As they appear to be interdependent feedback processes, analyses of LP genetic and cultural diversity can hardly be conducted separately [13]. Hence, it is likely that the study of the process of when, how and why some populations kept and exploited ungulates will shed new light on our understanding of the distribution of LP. Indeed, archaeological data can be used to provide evidence for the presence of this cultural behaviour in past populations. For example, the analysis of milk residues [59] and the determination of kill-off patterns of animals on archaeological sites [60] constitute two archaeological methods that can inform on the emergence of dairying. Consequently, to fully understand the origins and evolution of LP, it is necessary to consider archaeological and archaeozoological research on the origins of domestication and dairying. In Europe, the spread of domestic animals is tightly associated with the diffusion of the Neolithic from the Near East.

2. LACTASE PERSISTENCE, THE NEOLITHIC TRANSITION AND THE HISTORY OF DAIRYING (a) The spread of the Neolithic Before 8400 BP, hunter – gathering was the only subsistence strategy in Europe, but by 6000 BP, when farming had spread over most of the continent (figure 2), it had become rare. The spread of farming into Europe was dependent on earlier developments in the Neolithic core zone of the Near East and Anatolia. Archaeologically, this process defined a new period referred to as the ‘Neolithic revolution’. It is characterized by the presence of polished stone tools and pottery, a more sedentary lifestyle and the management and subsequent domestication of certain animal and plant species. These features are often characterized as the ‘Neolithic package’, and this term has been widely used to define Neolithic sites, even though all these features are not always present together at these sites. Chronologically and geographically, the Neolithic culture spread from its original core zone to other parts of western Eurasia and simultaneously to north


Evolution of lactase persistence Africa. There are two opposing models for the spread of farming into Europe [62]. One, the cultural diffusion, or acculturation model, favours the idea that local hunter – gatherers adopted Neolithic practices once they gained access to them from farming neighbours. The alternative demic diffusion model holds that the Neolithic was carried throughout Europe by the movement of farming peoples (and consequently their genes) spreading into the territory of foragers. It is highly unlikely that the Neolithic transition could be wholly explained by either of these models alone. The reality is likely to have been more complex and involved local heterogeneity of farming adoption processes [63]. Analyses of European genetic diversity have attempted to address the relative role of acculturation and migrations on the European gene pool during the spread of farming and yielded contrasting results, depending on the methodology employed, the loci studied and the proxies for ancestral source populations used [64 –70]. Recently, Bramanti et al. [71] presented ancient DNA evidence for a genetic discontinuity between late hunter – gatherers and early farming populations, at the beginning of the central European Neolithic 7500 BP, thus providing support for a migrating farmers model in this region. A full Neolithic lifestyle was established within a few generations in this area and cultural contact between farmers and local foragers persisted for some time. But the way in which Mesolithic hunter– gatherers and the Early Neolithic farmers interacted and how this led to an environment peopled exclusively by farmers is still debated [10,63,72].

(b) Domestic animals associated with the Neolithic transition Archaeozoological data on domestic animals have been particularly valuable in establishing a more precise picture of the spread of the Neolithic and the new subsistence strategies associated with it. This involves bone analysis (animal species, sex, age at death, morphology, presence of cutting and cooking signs [14], C direct dating and ancient DNA analyses) and placing this within their archaeological context. Morphological changes [73] and culling strategies [74] can be used to identify where and when wild animals started to become herded livestock. During the prepottery Neolithic B phase (PPN B) in the Neolithic core zone, several human groups started to manage wild animals at approximately the same time, in different places. After a period of hundreds or even thousands of years, this process finally resulted in phenotypes characteristic of domesticates. These domestication-associated phenotypes illustrate one of the consequences of human cultural niche construction on the evolution of other species [3,8,10,75]. In the context of the Neolithic, the oldest evidence for domestication is for goat and sheep (11 000 BP) followed by pig and cattle (10 500 BP) [73,74,76,77]. These domesticates soon spread from the Neolithic core region to a large part of the Near East, including Cyprus [77,78] and central Anatolia. However, true animal husbandry as a major economic activity in the Phil. Trans. R. Soc. B (2011)


Near East only began during the 10th millennium BP. Subsequently, but not earlier than 9000 BP, these domesticates spread into western and southern Anatolia [72,79]. From there, the spread of domesticates together with husbandry techniques followed two main routes (figure 2): (i) the Mediterranean route via the Aegean and Adriatic Seas, then moving further west to southern Italy, the Thyrennic Islands, southern France and the Iberian Peninsula; and (ii) a Danubian route via the Balkan Peninsula, further to the southwestern part of central Europe and finally into central and northern Europe. The two routes might have met in Greece, in the Rhine valley and in the northwest of the continent before crossing to the British Isles [80]. Domestic goat (Capra aegagrus) and sheep (Ovis aries) must have been introduced to these areas by humans, as there is no evidence of indigenous wild progenitors in Europe. Ancient DNA studies indicate that cattle (Bos taurus) were also imported from Anatolia and, once in Europe, did not mix substantially with European wild cattle, the aurochs (Bos primigenius) [81 – 83]. This is probably because humans managed to keep these two forms of cattle reproductively separate, although substantial size differences and other consequences of domestication may also have limited interbreeding. In contrast, while domestic pigs seem to have been introduced into Europe from the Neolithic core zone, ancient DNA evidence indicates that they mixed substantially with local wild boar [84]. In terms of dairying, the further development of herd structure after the arrival of early domesticates in Europe is crucial. Indeed, neither the Early Neolithic in the Balkans (8200– 7500 BP) nor the earliest Neolithic in central Europe (Linearbandkeramik, 7500 –7000 BP) yield clear archaeozoological signs of highly specialized dairying. However, in the following periods, especially in central Europe, there is evidence of a progressive increase in herding associated with dairying, i.e. prevalence of female over male animals. This particularly holds true for cattle and goat [46]. Similarly, in southeast Europe, a transition to a more specialized dairying economy becomes increasingly apparent as early as the 7th millennium BP. It should be noted that it is very likely that dairying was practised long before this period [40,42] and may have represented a means of managing wild animals as early as the beginning of the domestication process. However, it did not become a substantial economic factor before the 7th millennium BP in most parts of Europe.

(c) Evidence of the consumption of dairy products In addition to faunal remains, the detection of dairy fats associated with archaeological pottery is a powerful line of evidence for dairying activities in prehistory [59,85]. Investigations of organic residues in archaeological pottery have revealed a wide range of compound types, including dairy fats [85]. Using this method, the processing of milk has been identified in the western part of the present day Turkey as early as 8500 BP [40]. Similarly, evidence for the use of dairy products has been shown in Neolithic sites of


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Romania and Hungary around 7900–7450 BP [39], Britain around 6100 BP [86] and Scotland around 3000 BP [87]. Thus, the archaeozoological and residual lipid data clearly indicate that dairying was practised early in Neolithic Europe. However, ancient DNA data from central and northern Europe suggest that LP frequency was low during this period [88]. Thus, we may hypothesize that Early Neolithic people, among whom LP was rare or absent, initially practised dairying in south-eastern Europe and later migrated towards central and northern Europe, an area inhabited by foragers that occupied a different niche [10]. Indeed, stable isotope studies of bone collagen show that while hunter – gatherers largely relied on marine food, the farmers’ diet, even on coastal sites, was mainly terrestrial [51]. However, other authors found no evidence of this switch in diet [89– 91]. This may be because the localization of hunter– gatherers compared with farmer sites is biased towards coastal regions [90,92], or there may be other methodological issues [91,92]. An additional possibility is that in regions with abundant aquatic resources, the process of subsistence change offered by Neolithic farmers would have been slower. For example, in Scandinavia, where marine resources are abundant, there is no direct evidence of a sudden dietary transition [90]. In fact, instead of a replacement of hunter – gatherers by farmers, hunters from the Pitted Ware Culture (PWC) [89] coexisted for nearly 1000 years with the Neolithic Funnel Beaker Culture (TRB). However, it Phil. Trans. R. Soc. B (2011)

should be noted that recent ancient DNA evidence indicates little genetic continuity between PWC hunter – gatherers and modern Scandinavians [93]. In summary, LP and the main LP-associated allele in Europe, 213910*T, are found at highest frequencies in northwest Europe where dairying arrived latest (figures 1a,b and 2). A simple—phylogeographic— interpretation of the latter would be that LP first evolved in northwest Europe. But computer simulation studies have shown that when a population expands, the centre of distribution of an allele can be far removed from its location of origin [94,95]. This process is called ‘allele surfing’ and is thought to have occurred with the spread of farmers in Europe [65]. Furthermore, selection has—to an extent— shaped the distribution of LP [14,36,37], although it is unclear whether this selection was continuous or episodic, and whether it varied by latitude [50] or ecological zones [53]. It is therefore clear that to obtain a more complete picture of the coevolution of LP and dairying in Europe it is necessary to integrate cultural, demographic and selective processes. Computer simulation represents one of the most promising approaches to understand these processes because it can combine multiple sources of information. However, as with all modelling approaches, it is necessary to identify the key evolutionary parameters that have shaped the observed data. This is a non-trivial task when one considers the range of proposed hypotheses to explain the current distribution of LP in Europe


Evolution of lactase persistence today. In the following section, we review three of the simulation studies that have deepened our understanding of the coevolution of LP and dairying in Europe.

3. REVIEW OF SIMULATION STUDIES (a) Aoki’s model of lactase persistence and niche construction The coevolution for LP and dairying simulated by Aoki [96] captures many of the features of niche construction, as later proposed by Laland et al. [5]. The evolution of populations, made up of four compound phenotypes (two genetic: LP versus non-LP individuals and two cultural: milk users versus non-users), was simulated. The compound phenotype of being an LP milk user was selectively advantageous (fitness of 1), whereas the other three phenotypes were assigned a selective value of 12s (where s is the coefficient of selection). The effective population size (Ne) assumed was 100 individuals. At each generation, the model considered: (i) random mating between individuals (the random combinations of alleles and cultural behaviour from a parental generation to the next), (ii) the transmission of the cultural trait occurred with distinct probabilities of becoming a milk user, i.e. f(y) for an LP individual and g(y) for a lactase non-persistent individual, and (iii) random sampling of the individuals after the action of selection. At the end of the process, a correlation between the fixation of both the LP trait and the cultural behaviour was measured, and an average time until fixation of LP was calculated. This study addressed three questions: (i) if the evolution of both LP and milk consumption is mutually dependent, what would the correlation between their frequencies be? (ii) Does the type of selection, either strictly genetic or culturally induced, produce differences in the rate at which an allele reaches fixation? (iii) Do the frequency estimates of European LP (falling in the interval (0.05 – 0.70)) fit the hypothesis of a gene – culture coevolution process that started 6000 years ago? Although this model did not take into account cultural diffusion from neighbouring populations, an interesting feature is the use of distinct probabilities for transmission of the culture of milk consumption according to the LP phenotype of an individual. A key result was that an incomplete correlation between LP and milk consumption frequencies is expected. This actually represents inter-individual variability in the non-persistence phenotype, and corresponds either to LP individuals that do not drink milk or to lactase non-persistent individuals that do drink milk. It explicitly shows that the gene– culture coevolution hypothesis is still credible even if the correlation between the genetic and the cultural traits is incomplete. This is in accordance with previous analytical gene – culture coevolution studies [7,97,98] which have notably shown that genotype – phenotype correlation can be reduced by a factor depending on environmental and selection variances [97]. Another observation drawn from this model is that the change in LP frequency is slower when the selection is conditioned by culture. This means that in order to explain such high frequency of LP in Phil. Trans. R. Soc. B (2011)


north-western Europe, we must consider that either every LP individual actually did drink milk, or that other processes have been involved to generate this distribution. The author consequently suggested that to be able to detect such a change in allele frequency since the start of dairying (then considered to have occurred 6000 years ago), either the effective population (Ne) was relatively small (100 individuals as simulated in the study), or the selection coefficient in favour of the phenotype was very high (more than 5% if Ne ¼ 500). Such a high value of 5 per cent falls well within the confidence intervals ((1.4 – 19%) and (1– 15%)) of recent studies ([20,36], respectively) inferred directly from genetic data. However, lower values of the selection coefficient may be expected to fit the observed LP pattern, as it is now known that the start of dairying was much earlier than 6000 years ago [40], leaving more time for the genotype to be selected. In addition, both genetic and archaeological studies point to the importance of the demographic process when studying the Neolithic diffusion in Europe [99,100], whereas Aoki’s simulations were performed with a constant population size of 100 individuals. Moreover, demographic expansion has been shown to have a potentially dramatic effect on the diffusion of new mutations [94,95,101]. Hence, we may expect that the assumption of a constant population size could lead to an overestimation of the rate of frequency change and of the selection coefficients.

(b) Spatial variation in selection intensity While the selection coefficients explored in Aoki’s model were assumed to be constant, in a recent study, Gerbault et al. [18] modelled a geographical structuring of selection pressure by latitude, thereby testing explicitly the calcium assimilation hypothesis [50]. The evolution of a dominant allele associated with LP was simulated in four Near-Eastern and 22 European populations since the Neolithic transition in their respective regions, according to two demographic models: cultural diffusion and demic diffusion [63]. Each of these models was tested using either a constant selection coefficient or a selection coefficient varying with latitude. Thus, a total of four scenarios were tested combining the two selection models and the two demographic models. The program used (called SELECTOR) models four parametrized processes: (i) random genetic drift, (ii) logistically regulated population growth, (iii) positive selection varying between 0 and 3 per cent, and (iv) time elapsed since the onset of the Neolithic. To simulate the cultural diffusion model, the initial LP allele frequency was set at 1 per cent in all 26 populations and evolved according to the above processes. One important assumption is thus that the LP-associated allele was already present in Europe before the Neolithic but at a low frequency (1%). Under the demic diffusion model, three populations were used as sources in the Near East (Lebanon, Syria and Iran). The remaining populations, including the fourth Near Eastern population (Cyprus), were populated by sampling from neighbouring populations along the presumed route of the spread of farming, and at


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the times indicated from archaeological data [41]. A maximum-likelihood test was performed to evaluate independently in each sample what selection coefficient best fitted the observed data (the LP frequency for each of the 26 populations). Moreover, the four simulated scenarios were formally compared using an approximate Bayesian computation (ABC) approach [102] based on LP frequencies within samples [103]. In this study [18], the scenario that gave the highest relative probability of obtaining the observed data was the demic diffusion model combined with a selection coefficient varying with latitude. Indeed, according to this model, genetic drift alone can explain frequencies as low as those observed in southern Europe, as previously suggested by Nei & Saitou [45]. However, in northern Europe, positive selection coefficients were required to drive LP frequencies to their observed values (figure 3). This result supports the calcium assimilation hypothesis. A complementary explanation for increased selection strength at higher latitudes is that the lower temperatures would allow milk to remain fresh for longer [44,57]. If this applies, LP would illustrate a specific case of niche construction where localized access to a resource is variable [5], i.e. fresh milk. Indeed, niche construction modelling [104] has shown that in such a situation a strong association between a cultural and a genetic trait is expected, as is observed for LP and dairying in northern Europe. Even though the model of Gerbault et al. [18] does not simulate a wave of advance, it illustrates the importance of demography, since the demic diffusion model with variation in the selection coefficient was far more likely (99.1%) than the cultural diffusion model (0.9%). The selection coefficients estimated range between 0.8 and 1.8 per cent, and the authors suggested that if the simulations were closer to a wave of advance model, this range might have been lower. It should be noted that these estimates are not constant over all the populations considered, as under the best-fitted models the selection coefficient varied latitudinally and approached zero in southern Europe.

(c) Demic and cultural diffusion of farming In a more complex spatially explicit model, Itan et al. [105] simulate the spread of farmers from the Near East to Europe over the last 9000 years, taking into account potential interactions with hunter – gatherers. The geographical unit of this simulation was a deme, and in total the simulated world was made of 2375 land demes, each containing three interacting populations: hunter – gatherers, dairying farmers and non-dairying farmers. At each generation, each population underwent a succession of seven processes: (i) logistically regulated population growth, in which each deme had a fixed carrying capacity determined by climatic and elevation factors. The carrying capacities of dairying and non-dairying farmers were equal, whereas those of hunter– gatherers were 50 times smaller [106,107]. (ii) Unidirectional migration process modelled as a stochastic Gaussian random walk from one deme to another (a process equivalent Phil. Trans. R. Soc. B (2011)

to demic diffusion). (iii) Cultural diffusion, where a proportion of individuals from one culture ‘converted’ to one of the two other cultural groups, based on the relative ‘dominance’ of the other groups in the focal and eight surrounding demes. (iv) Intra-demic gene flow between different cultural groups within a deme. (v) Inter-demic gene flow between neighbouring demes belonging to the same cultural group. (vi) Selection acting on an LP allele only in the dairying farmers cultural group. (vii) Drift of the LP allele in all cultural groups in all demes, modelled as a binomial sampling process. The LP-associated allele was set to appear in a randomly chosen location when the population size of dairying farmers in this deme reached a critical value (20 individuals). This ensured that the LP-associated allele appeared on, or near, the wavefront of dairying farmer diffusion. Its frequency was updated according to the evolution of a dominant allele with parametrized selective advantage [108], which remained constant in each simulation. This selection in turn drove additional increases (over and above the logistically regulated population growth) in the population sizes of dairying farmers [108]. After the simulations, the authors estimated parameters of the model using ABC [102] with a particular focus on two related questions: (i) when and where in Europe did LP-dairying coevolution begin, and (ii) what factors drove the spread of LP to get the observed European pattern of LP frequencies? Simulations were fitted to both observed 213910*T frequencies at 12 European locations and the corresponding dates of arrival of farmers [41] at 11 of these locations. Both the dates estimated (between 6256 and 8683 years BP) and the geographical area identified (the region between central Europe and northern Balkans—figure 4) for the origin of LPdairying coevolution correlate well with the time and location of the emergence of the Linearbandkeramik (LBK) culture (figure 2). The LBK is recognized to have been the direct forerunner of a Neolithic cattlebased economy [109], whereas on the Mediterranean Neolithic sites, faunal assemblages are more variable in composition and in some places dominated by sheep and goat [42,46,109]. Indeed, cows provide quantitatively more milk than sheep or goats, allowing cattle-based farmers to have a better supply, thereby supporting a stronger selection for LP. Even though these origin time and location estimates were not independently derived, as simulations were conditioned on known farming arrival dates [41], recent results from spatially explicit niche-construction modelling [9] corroborate this hypothesis. In this latter model [9], local mating of niche constructors (i.e. LBK-economy distribution and diffusion) has the effect of increasing the local concentration of the resource (i.e. fresh milk), thereby generating stronger selection in favour of the resource-dependent trait (i.e. LP). Indeed, from the study of Itan et al. [105], the selection coefficients necessary to explain the 213910*T allele frequency distribution in Europe were estimated to range from 5.2 to 15.9 per cent. Although very high, this range falls within the range estimated (1.4 – 19%) from molecular data [36], but shows less overlap with the range estimated by Gerbault et al. [18].


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Figure 3. Scenarios simulated in [18] and selection coefficients required to fit the observed estimates of LP frequencies (taken from [18]). Bars represent the 95% confidence interval of the selection coefficient estimated for the population and the central point is the MLE (maximum-likelihood estimate). Populations are ordered from the highest to the lowest latitude: Danish (Dan), Irish (Iri), German from Bremen (Bre), German from Berlin (Ber), English (Eng), Polish (Pol), Czech (Cze), German from Stuttgart (Stu), German from Munchen (Mun), Austrian (Aus), French from Nantes (Nan), Swiss (Swi), Slovenian (Slo), Italian from Brescia (Bre), French from Nice (Nic), Spanish from Santiago de Compostela (Com), Italian from Roma (Rom), Italian from Napoli (Nap), Sardinian (Sas), Spanish from Valencia (Val), Greek (Gre), Sicilian (Sic), Cypriot (Cyp), Lebanese (Leb) and Iranian (Ira) (doi:10.1371/journal.pone.0006369.g002). (a) Demic diffusion, gene– culture coevolution; (b) demic diffusion, calcium assimilation; (c) cultural diffusion, gene –culture coevolution; and (d) cultural diffusion, calcium assimilation.

However, as the selection strength inferred by Itan et al. [105] applies to less than half of the overall population (dairying farmers), the population-wide selection coefficient is likely to be around half of the value reported. A key difference between the two studies is that Gerbault et al. [18] explicitly modelled, and found support for, a latitudinal effect on LP selection coefficients [50] while Itan et al. [105] did not. Even though it is difficult to separate the effects of selection and demography in their model (as demographic parameters and the selection coefficient were estimated simultaneously), Itan et al. [105] argued that such a latitudinal effect is not necessary to explain the higher observed frequencies of LP in northern Europe. Indeed, they found that without any assumption of a latitudinal effect on selection, their model under the estimated parameters predicted higher LP frequencies in northern Europe than observed, and typically lower frequencies in southern Europe than observed. Thus, the addition of latitudinal effect on selection should drive an even poorer fit to the LP data and so could be thought of as having ‘negative explanatory power’. However, it should be noted that Itan et al. [105] did not explicitly model a latitudinal effect on selection, and so have not formally rejected it. Another key difference between both studies is the values estimated for the selection coefficient, which are larger in Itan et al. [105] than in Gerbault et al. Phil. Trans. R. Soc. B (2011)

[18]. In the study of Itan et al. [105], the best fit was obtained when the allele was first selected in dairy farmers, in central Europe/the northern Balkans, and subsequently spread into neighbouring regions. High selection coefficients were thus required to obtain the high frequencies currently observed in north and central Europe in a relatively short period of time. In the model of Gerbault et al. [18], the allele was assumed to have reached non-negligible frequencies before it had spread into central Europe as it was already present in the Near East at the onset of the Neolithic transition. Hence, while selection was required, this was to a lesser extent than if it had started in central Europe. There is a potential ‘tradeoff ’ between selection intensity and the timing and location of origin of the gene – culture coevolutionary process, and in future work, combinations of values for these parameters will bring insights into the means of diffusion not only of LP but of other genetic traits as well.

4. DISCUSSION AND PERSPECTIVES (a) Simulation overview Although simulation studies are unlikely to recover the precise evolutionary history of LP and dairying, they have two main advantages over purely genetic or purely archaeological studies. First, they allow the integration of information from multiple sources


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Figure 4. Approximate posterior density of region of origin for LP—dairying coevolution (taken from [105]). Points represent regression-adjusted latitude and longitude coordinates from simulations accepted at the 0.5% tolerance level. Shading was added using two-dimensional kernel density estimation (doi:10.1371/journal.pcbi.1000491.g003).

(genetics, archaeology, ecology). Second, they provide a formal comparison of alternative scenarios, according to the parameters taken into account. Many combinations of parameters can be tested, and extreme scenarios (such as cultural or demic diffusion) can be evaluated statistically, and potentially excluded. Furthermore, ABC methods [102,103] have proved to be very useful when evaluating the fit of observed data on complex scenarios tested, adding power to simulation studies [18,105]. Clearly, simulations performed at the continental scale help to understand general features and processes of the European Neolithic transition, and to explore alternative possibilities that may have led to observed patterns of genetic diversity.

(b) Demography and niche construction The above simulation studies of LP/dairying coevolution, as well as ecological and archaeological information, suggest that selection on LP is unlikely to have been constant over time and space during its spread throughout Europe, and show that the role of demography in its diffusion cannot be ignored. The extent to which combinations of these two phenomena have shaped the LP distribution as it is observed in Europe remains unanswered. While Itan and colleagues [105] used a complex demographic model, the population growth was logistically regulated for each group, with no direct consequence of the growth of one group on the growth of the others (i.e. competition between cultural groups for land resources). But as almost no hunter – gatherers survive in Europe today, it is logical to assume that niche modification by farmers may have had an effect on the distribution of hunter – gathers that led ultimately to their disappearance (because of the distinct abilities Phil. Trans. R. Soc. B (2011)

of both populations to niche construct [10]). As an adaptation of the model of Itan et al. [105], an alternative dynamic could be proposed to investigate how demographic constraints may have affected the diffusion of the trait. Inclusion of density-dependent competition, as implemented by Currat & Excoffier [110], should bring new insights into the effect of these demographic processes. This improvement would allow regional variation in the simulation of the Neolithic spread, with a higher carrying capacity of hunter – gatherer populations in areas where marine resources are abundant, thereby potentially changing the competition dynamics between hunter– gatherers and farmers. This would also enable account to be taken both of localized resource availability and spatially structured populations for investigating the evolution of the association of LP (i.e. the resource-dependent trait) and dairying (i.e. the niche-constructing practice) [9,104]. This may be relevant for the co-habitation of hunters from the PWC [89] with the TRB farmers, who coexisted for nearly 1000 years in Scandinavia. Further analyses assessing this co-habitation would be appropriate to explicitly evaluate how the co-influences of genes, environment and pre-existing culture affect differential transmission of Neolithic cultural forms [111]. The spread of LP is a good example of niche construction for two reasons. First, because human groups who started to drink milk modified their pre-existing selection pressure, thereby generating an evolutionary feedback that may have advantaged some individuals against others in certain environmental conditions. Second, by perpetuating this behaviour from the Neolithic to modern days, the coevolution of LP and dairying illustrates how culture can affect the genetic diversity of human populations. That is why niche construction factors should be considered


Evolution of lactase persistence when studying human adaptation. Gene – culture coevolution studies have shown that both genes and culture exert distinct, but interacting, influences in the evolution of human phenotypes [98,111]. More precisely, cultural processes have been shown to alter the outcome expected under purely genetic transmission [7,97,98]. Even though dairying culture has been taken into account, it should be noted that the effect of differential cultural transmission has not been explicitly modelled in the three simulation studies described above. It is thus expected that the combination of demographic information and differential cultural and genetic transmission influenced by selection would enlarge the possible evolutionary conditions that may have shaped the worldwide LP distribution observed today. (c) Migration and environment Other environmental parameters are likely to have affected the distribution of the culturally distinct populations, and the speed of the Neolithic transition. Indeed, niche-construction studies have shown that environmental variables should not be seen as static but as dynamic features that change according to climate and human activities [5], thereby modifying the selection pressure to which humans are subjected [35]. For example, Itan et al. [105] took into account environmental factors to determine different carrying capacities according to the economy type of the populations. In addition to this, other environmental pressures, such as vegetation cover and natural water access, may have conditioned the movement of farming populations with their domesticated animals [57]. These environmental variables can allow the modelling of potential regional variation in the spread of the Neolithic, as suggested by archaeological studies [112]. This will have an initial advantage of bringing a better understanding of the effect of the environment on the spread of agriculture and farming. Then, the relative importance of environmental variables that influence migrations can be evaluated. However, it should be noted that increasing the number of parameters in a model is generally to be avoided unless necessary. In particular, because the more complex a model is (the closer to the reality it is), the more difficult it becomes to interpret, as isolating the effects of different processes, and parameters, can be extremely complicated. Furthermore, the parameter space of a complex model can be very difficult to explore by simulation. (d) The importance of an interdisciplinary approach While selection on LP has been inferred, it has not been shown directly [113]. Other pleiotropic factors may be involved that affect the ability to digest milk on the one hand or that affect selection on LCT on the other. What is clear from the study of LPassociated genetic variants is that it has emerged independently in different regions of the world [14,20,23,31,32,114]. While some alleles show evidence of strong directional selection, soft selective sweeps [115]—whereby ancestral genetic variation is associated with different adaptive substitutions Phil. Trans. R. Soc. B (2011)


[116]—have been invoked [16] to explain how several alleles can be maintained in a population through mutation and migration processes. It would be of interest to assess whether such a process applies more widely than in Africa and the Middle East. Ongoing research on the LCT gene and the regulation of its expression, and further sampling, with associated sequencing and phenotyping will be necessary to give a more complete picture of the structure of LP-associated genetic diversity [15]. Additionally, archaeological assemblage studies will provide useful information on the time and location of the development of milk-drinking behaviour. Finally, simulation studies can assess different possible scenarios by taking into account information obtained from different fields of study, particularly by employing ABC methods [102,103]. LP evolution will be better understood by combining data from these different fields, and by generating expectations of different data types in simulations. More broadly, the study of LP evolution is likely to shed light on the interactions and relative contributions of distinct processes involved in shaping human variation.

5. CONCLUSION The coevolution of LP and dairying appears to be not as straightforward a process as it may have first seemed. While several alleles seem to be associated with LP, the pattern of LP in Europe appears peculiar, as a single variant (213910*T ) has been identified as explaining most of the modern distribution of LP [15]. In this continent, the spread of dairying-associated practices goes back to Early Neolithic periods, and it is likely that archaeological studies will soon give a more precise picture of the early development of dairying in Europe. Archaeology notably underlines how complex the migration processes may have been. It may not be surprising then, even though the models were different, that simulation studies on the spread of LP in Europe highlight the importance of demography on the distribution of the 213910*T allele. Some of these simulation studies also hint that selection may not have been constant over time and space. It thus appears that, in order to disentangle the effects of selection from those of demography on the distribution of both LP phenotype and genotypes, there is a need to better understand spatial patterns of genetic variation under neutrality [66,101,117,118]. In turn, the extent to which LP-associated genetic variation can be explained by these patterns will determine what can be said about the adaptation process [119]. Inference on the coevolution of LP (and its associated alleles) and dairying is likely to provide a useful framework for future studies on the evolution of other adaptive traits in which niche construction is invoked. We thank two anonymous referees for their comments. P.G. and A.L. are funded by an EU Marie Curie FP7 Framework Programme grant (LeCHE, grant ref: 215362-2). Y.I. was funded by the B’nai B’rith/Leo Baeck London Lodge and Annals of Human Genetics scholarships. We also thank the AHRC Center for the Evolution of Cultural Diversity (CECD) and the Center for Mathematics and Physics in


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the Life Sciences and Experimental Biology (CoMPLEX), UCL, for supporting this research. 19

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Review

Gene – culture coevolution and the nature of human sociality Herbert Gintis1,2,* 1

Santa Fe Institute, 1399 Hyde Park Road, Santa Fe, NM 87501, USA 2 Central European University, Nador u. 9, 1051 Budapest, Hungary

Human characteristics are the product of gene– culture coevolution, which is an evolutionary dynamic involving the interaction of genes and culture over long time periods. Gene – culture coevolution is a special case of niche construction. Gene – culture coevolution is responsible for human other-regarding preferences, a taste for fairness, the capacity to empathize and salience of morality and character virtues. Keywords: gene – culture coevolution; sociobiology; epistatic information transfer

1. GENE – CULTURE COEVOLUTION Because of the importance of culture and complex social organization to the evolutionary success of Homo sapiens, individual fitness in humans depends on the structure of social life. Because culture is both constrained and promoted by the human genome, human cognitive, affective and moral capacities are the product of an evolutionary dynamic involving the interaction of genes and culture. We call this dynamic gene– culture coevolution [1 –4]. This coevolutionary process has endowed us with preferences that go beyond the self-regarding concerns emphasized in traditional economic and biological theory, and with a social epistemology that facilitates the sharing of intentionality across minds. Gene – culture coevolution is responsible for the salience of such other-regarding values as a taste for cooperation, fairness and retribution, the capacity to empathize, and the ability to value such character virtues as honesty, hard work, piety and loyalty. Gene – culture coevolution is the application of sociobiology, the general theory of the social organization of biological species, to humans—a species that transmits culture in a manner that leads to quantitative growth across generations. This is a special case of niche construction, which applies to species that transform their natural environment so as to facilitate social interaction and collective behaviour [5]. The genome encodes information that is used both to construct a new organism and to endow it with instructions for transforming sensory inputs into decision outputs. Because learning is costly and time-consuming, efficient information transmission will ensure that the genome encodes those aspects of the organism’s environment that are constant, or that change only very slowly through time and space, as

compared with an individual lifetime. By contrast, environmental conditions that vary rapidly can be dealt with by providing the organism with phenotypic plasticity in the form of the capacity to learn. For instance, suppose the environment provides an organism with the most nutrients where ambient temperature is highest. An organism may learn this by trial and error over many periods, or it can be hard-wired to seek the highest ambient temperature when feeding. By contrast, suppose the optimal feeding temperature varies over an individual’s lifetime. Then there is no benefit to encoding this information in the individual’s genome, but a flexible learning mechanism will enhance the individual’s fitness. There is an intermediate case, however, that is efficiently handled neither by genetic encoding nor learning. When environmental conditions are positively but imperfectly correlated across generations, each generation acquires valuable information through learning that it cannot transmit genetically to the succeeding generation, because such information is not encoded in the germ line. In the context of such environments, there is a fitness benefit to the epigenetic transmission of information concerning the current state of the environment; i.e. transmission through non-genetic channels. Several epigenetic transmission mechanisms have been identified [6], but cultural transmission in humans and to a lesser extent in other animals [7,8] is a distinct and extremely flexible form. Cultural transmission takes the form of vertical (parents to children), horizontal (peer to peer) and oblique (elder to younger), as in Cavalli-Sforza & Feldman [9], prestige (higher influencing lower status), as in Henrich & Gil-White [10], popularityrelated as in Newman et al. [11] and even random population-dynamic transmission, as in Shennan [12] and Skibo & Bentley [13]. The parallel between cultural and biological evolution goes back to Huxley [14], Popper [15] and James [16]—see Mesoudi et al. [17] for details. The idea of treating culture as a form of epigenetic

* [email protected] One contribution of 13 to a Theme Issue ‘Human niche construction’.

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Review. The nature of human sociality transmission was pioneered by Dawkins [18], who coined the term ‘meme’ in The Selfish Gene to represent an integral unit of information that could be transmitted phenotypically. There quickly followed several major contributions to a biological approach to culture, all based on the notion that culture, like genes, could evolve through replication (intergenerational transmission), mutation and selection.1 Cultural elements reproduce themselves from brain to brain and across time, mutate and are subject to selection according to their effects on the fitness of their carriers [2,20]. Moreover, there are strong interactions between genetic and epigenetic elements in human evolution, ranging from basic physiology (e.g. the transformation of the organs of speech with the evolution of language) to sophisticated social emotions, including empathy, shame, guilt and revenge-seeking [21–23]. Because of their common informational and evolutionary character, there are strong parallels between models of genetic and cultural evolution [17]. Like biological transmission, culture is transmitted from parents to offspring, and like cultural transmission, which is transmitted horizontally to unrelated individuals, so in microbes and many plant species, genes are regularly transferred across lineage boundaries [6,24,25]. Moreover, anthropologists reconstruct the history of social groups by analysing homologous and analogous cultural traits, much as biologists reconstruct the evolution of species by the analysis of shared characters and homologous DNA [26]. Indeed, the same computer programs developed by biological systematists are used by cultural anthropologists [27,28]. In addition, archeologists who study cultural evolution have a similar modus operandi as palaeobiologists who study genetic evolution [17]. Both attempt to reconstruct lineages of artifacts and their carriers. Like palaeobiology, archaeology assumes that when analogy can be ruled out, similarity implies causal connection by inheritance [29]. Like biogeography’s study of the spatial distribution of organisms [30], behavioural ecology studies the interaction of ecological, historical and geographical factors that determine distribution of cultural forms across space and time [31]. Perhaps the most common criticism of the analogy between genetic and cultural evolution is that the gene is a well-defined, discrete, independently reproducing and mutating entity, whereas the boundaries of the unit of culture are ill-defined and overlapping. In fact, however, this view of the gene is outdated. We now know that overlapping, nested and movable genes have some of the fluidity of cultural units, whereas quite often the boundaries of a cultural unit (a belief, icon, word, technique, stylistic convention) are quite delimited and specific. Similarly, alternative splicing, nuclear and messenger RNA editing, cellular protein modification and genomic imprinting, which are quite common, undermine the standard view of the insular gene producing a single protein, and support the notion of genes having variable boundaries and having strongly context-dependent effects. Moreover, natural selection requires heritable variation and selection, but does not require discretely transmitted units. Phil. Trans. R. Soc. B (2011)

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Dawkins [32] added a second fundamental mechanism of epigenetic information transmission in The Extended Phenotype, noting that organisms can directly transmit environmental artifacts to the next generation, in the form of such constructs as beaver dams, bee hives and even social structures (e.g. mating and hunting practices). The phenomenon of a species creating an important aspect of its environment and stably transmitting this environment across generations, known as niche construction, is a widespread form of epigenetic transmission [5]. Niche construction includes gene – environment coevolution, because a genetically induced environmental regularity becomes the basis for genetic selection, and gene mutations that give rise to novel niche elements will survive if they are fitness-enhancing for their constructors. An excellent example of gene – environment coevolution is the honeybee, in which the origin of its eusociality probably lay in the high degree of relatedness fostered by haplodiploidy, but which persists in modern species despite the fact that relatedness in the hive is generally quite low, due to multiple queen matings, multiple queens, queen deaths and the like [33 – 35]. The social structure of the hive is transmitted epigenetically across generations, and the honeybee genome is an adaptation to the social structure laid down in the distant past. Gene – culture coevolution in humans is a special case of gene –environment coevolution in which the environment is culturally constituted and transmitted [36]. The key to the success of our species in the framework of the hunter – gatherer social structure in which we evolved is the capacity of unrelated, or only loosely related, individuals to cooperate in relatively large egalitarian groups in hunting and territorial acquisition and defence [4,37]. While some contemporary biological and economic theorists have attempted to show that such cooperation can be supported by self-regarding rational agents [38 – 40], the conditions under which their models work are implausible even for small groups [41,42]. Rather, the social environment of early humans was conducive to the development of prosocial traits, such as empathy, shame, pride, embarrassment and reciprocity, without which social cooperation would be impossible [43]. Neuroscientific studies exhibit clearly the genetic basis for moral behaviour. Brain regions involved in moral judgements and behaviour include the prefrontal cortex, the orbitalfrontal cortex and the superior temporal sulcus [44]. These brain structures are virtually unique to or most highly developed in humans and are doubtless evolutionary adaptations [45]. The evolution of the human prefrontal cortex is closely tied to the emergence of human morality [46]. Patients with focal damage to one or more of these areas exhibit a variety of antisocial behaviours, including the absence of embarrassment, pride and regret [47,48], and sociopathic behaviour [49]. There is a probable genetic predisposition underlying sociopathy, and sociopaths comprise 3– 4% of the male population, but they account for between 33 and 80 per cent of the population of chronic criminal offenders in the United States [50].


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Review. The nature of human sociality

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Figure 1. The dynamics of gene– culture coevolution.

It is clear from this body of empirical information that culture is directly encoded into the human brain with symbolic representations in the form of cultural artifacts. This, of course, is the central claim of gene– culture coevolutionary theory. 2. CULTURE IS NOT A BY-PRODUCT OF GENETIC EVOLUTION It might be thought that the complex and intimate interaction of genes and culture outlined above is overdrawn, and that human genetic evolution is the effect of genetic inclusive fitness maximization, culture being an effect of genes that can be factored out in the long run. For instance, the eminent evolutionary psychologist David Buss holds that ‘Culture is not an autonomous casual process in competition with biology for explanatory power’ [51, p. 407]. This denial of gene–culture coevolution can be shown to be prima facie untenable. To see this, suppose we have a vector g of genetic variables, a vector c of cultural variables, and a vector e of environmental variables, including the prevalence of predators and prey, weather and the like. In an evolutionary model, the rate of change of variables is a function of the variables, so we have g˙ ¼ Fðg; c; eÞ; c˙ ¼ Gðg; c; eÞ e˙ ¼ HðeÞ:

ð2:1Þ ð2:2Þ ð2:3Þ

Note that it is plausible for c to affect the nature and pace of environmental change, in which case it should be included in equation (2.3). We abstract from this causal path in order to strengthen the case for Buss’ argument. The contention that culture is an effect of genetic fitness maximization in this framework is the assertion that c can be eliminated from these equations. Under what conditions can this occur? Taking the derivative of equation (2.1), and substituting equations (2.2) and (2.3) into equation (2.1), we get g¨ ¼ Fg ðg; c; eÞFðg; c; eÞ þ Fc ðg; c; eÞGðg; c; eÞ ð2:4Þ þ Fe ðg; c; eÞHðeÞ: If c is to be absent from this second order differential equation, the derivative of the right-hand side of equation (2.4) with respect to c must be identically zero. Thus, we have 0 ; Fgc F þ Fg Fc þ Fcc G þ Fc Gc þ Fec H: Phil. Trans. R. Soc. B (2011)

ð2:5Þ

All five of the above terms must then be identically zero, so Fc ; 0, implying that c does not enter on the right-hand side of the defining equations (2.1) – (2.3); i.e. genes are not a function of culture. This is obviously not appropriate for humans, since both genes and culture are functions of culture. Figure 1 illustrates this dynamical process. Note that as long as there is high fidelity cultural transmission over multiple generations (signified by the middle row of horizontal arrows), genetic and cultural evolution are inextricably intertwined. By contrast, for species that do not have cumulative learning, these arrows are absent, and despite the fact that genes affect culture in every period, there is no cumulative interrelatedness of genes and culture. We will give two examples of understanding human evolution using gene – culture evolution, the repositioning of the larynx and other physiological changes facilitating linguistic communication [52], and the role of culture in creating a genetic predisposition for cooperative activity in humans [53].

3. GENE– CULTURE COEVOLUTION AND THE PHYSIOLOGY OF COMMUNICATION The evolution of the physiology of speech and facial communication is a dramatic example of gene – culture coevolution. The increased social importance of communication in human society rewarded genetic changes that facilitate speech. Regions in the motor cortex expanded in early humans to facilitate speech production. Concurrently, nerves and muscles to the mouth, larynx and tongue became more numerous to handle the complexities of speech [54]. Parts of the cerebral cortex, Broca’s and Wernicke’s areas, which do not exist or are relatively small in other primates, are large in humans and permit grammatical speech and comprehension [55,56]. Adult modern humans have a larynx low in the throat, a position that allows the throat to serve as a resonating chamber capable of a great number of sounds [57]. The first hominids that have skeletal structures supporting this laryngeal placement are the Homo heidelbergensis, who lived from 800 000 to 100 000 years ago. In addition, the production of consonants requires a short oral cavity, whereas our nearest primate relatives have much too long an oral


Review. The nature of human sociality cavity for this purpose. The position of the hyoid bone, which is a point of attachment for a tongue muscle, developed in Homo sapiens in a manner permitting highly precise and flexible tongue movements. Another indication that the tongue has evolved in hominids to facilitate speech is the size of the hypoglossal canal, an aperture that permits the hypoglossal nerve to reach the tongue muscles. This aperture is much larger in Neanderthals and humans than in early hominids and non-human primates [58]. Human facial nerves and musculature have also evolved to facilitate communication. This musculature is present in all vertebrates, but except in mammals it serves feeding and respiratory functions alone [59]. In mammals, this mimetic musculature attaches to the skin of the face, thus permitting the facial communication of such emotions as fear, surprise, disgust and anger. In most mammals, however, a few wide sheetlike muscles are involved, rendering fine information differentiation impossible, whereas in primates, this musculature divides into many independent muscles with distinct points of attachment to the epidermis, thus permitting higher bandwidth facial communication. Humans have the most highly developed facial musculature by far of any primate species, with a degree of involvement of lips and eyes that is not present in any other species. In short, humans have evolved a highly specialized and very costly complex of physiological characteristics that both presuppose and facilitate sophisticated aural and visual communication, whereas communication in other primates, lacking as they are in cumulative culture, goes little beyond simple calling and gesturing capacities. This example is quite a dramatic and concrete illustration of the intimate interaction of genes and culture in the evolution of our species.

4. SOCIALIZATION AND THE INTERNALIZATION OF NORMS Human society is held together by moral values that are transmitted from generation to generation by the process of socialization. These values are instantiated through the internalization of norms [60– 63], a process in which the initiated instill values into the uninitiated (usually the younger generation) through an extended series of personal interactions, relying on a complex interplay of affect and authority. Through the internalization of norms, initiates are supplied with moral values that induce them to conform to the duties and obligations of the role-positions they expect to occupy. The internalization of norms, of course, presupposes a genetic predisposition to moral cognition that can be explained only by gene – culture coevolution. The human openness to socialization is perhaps the most powerful form of epigenetic transmission found in nature. This epigenetic flexibility in considerable part accounts for the stunning success of the species Homo sapiens, because when individuals internalize a norm, the frequency of the desired behaviour will be higher than if people follow the norm only instrumentally—i.e. when they perceive it to be in Phil. Trans. R. Soc. B (2011)

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their interest to do so on other grounds. The increased incidence of prosocial behaviours is precisely what permits humans to cooperate effectively in groups [64]. There are, of course, limits to socialization [65,66], and it is imperative to understand the dynamics of emergence and abandonment of particular values, which in fact depend on their contribution to fitness and well-being, as economic and biological theory would suggest [53,67]. Moreover, there are often swift society-wide value changes that cannot be accounted for by socialization theory [68,69]. However, socialization theory has an important place in the general theory of culture, strategic learning and moral development. The susceptibility to socialization is controlled by neuronal structures and is hence the product of genetic evolution. The socialized individual is highly sensitized to the particular rewards offered for prosocial behaviour and penalties imposed for antisocial behaviour. But this sensitivity is characteristic of all creatures who live in social settings. The distinguishing characteristic of the internalization of norms is that individuals behave prosocially even when there is no possibility of being rewarded for prosocial or penalized for antisocial behaviour. Such altruistic behaviour has been confirmed in scores of laboratory and field studies across a wide variety of societies [42,70,71]. Gintis [53] provides a plausible evolutionary scenario in which the genetic predisposition to internalize norms may have developed. The prerequisite is a cultural system sufficiently complex that the learning process for youth in acquiring facility with this system extends throughout childhood, and hence takes the form of an authoritarian imposition carried out by elders. Because the skills acquired in this manner (e.g. hunting, recognizing and preparing nutritious foodstuffs) do not have immediate intrinsic payoffs for the learner, those who respond to the rewards and sanctions of teachers will reproduce at the expense of those who do not. Internalizing the norms associated with instrumental skills will then be directly fitness-enhancing, and hence the neural structures that support internalization will be privileged in human evolution. Once these neural structures are in place, they can be deployed for more general purposes, including internalizing moral values and deriving pleasure from helping others and punishing those who act contrary to social norms.

5. ALTRUISM IS AN EMERGENT PROPERTY OF HUMAN GENE –CULTURE EVOLUTION Many empirical findings from behavioural game theory [70] show that human subjects regularly exhibit altruistic behaviours towards enhancing cooperative payoffs [42, ch. 4]. Indeed, it is likely that such altruistic predispositions account for the remarkable evolutionary success of our species [64]. Among such predispositions are the character virtues (honesty, courage, trustworthiness, considerateness and the like) and strong reciprocity, which is a predisposition to cooperate with others in a collective task, and to


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punish those who fail to cooperate, even when a selfregarding individual would simply free-ride on the effort of others [72]. These behaviours are altruistic in the sense that they enhance the payoffs to other group members at a cost to the cooperator. Of course, in a framework of biological evolution, where payoffs are fitnesses, altruism could not evolve unless the fitness cost of altruism were somehow recouped in the long run. Some question calling the behaviour altruistic in this case, but requiring altruism to be fitness-reducing in the whole population in the long run amounts to excluding the possibility of altruism by definition [73]. I shall stick to a more fruitful definition of altruism, according to which the behaviour of an individual is altruistic if it benefits other members of the group and the individual would increase his own payoff by switching to another behaviour [74]. Those who deny the causal importance of culture in human evolution generally argue that the altruistic behaviour exhibited in modern societies is simply a maladaptation to current environmental conditions. Thus, altruistic cooperation and punishment, they argue, stem from mental confusion due to the difficulty in avoiding detection when behaving anti-socially in our evolutionary past. Throughout most of the history of our species, they argue, hunter–gatherer societies offered little room for the sorts of anonymous interaction and covert behaviour found in modern society [75,76]. Because of our evolutionary past, they argue, modern humans are hyper-sensitive to even remote possibilities that their actions may be observed and their reputations sullied. For this reason, those who hold the maladaptation position suggest that modern humans tend to behave as though every social interaction were publicly observable. However, our understanding of contemporary hunter– gatherer societies indicates the lack of credibility of this argument, as do analyses of trade and migration patterns in Pleistocene [77,78]. If the altruism-as-maladaptation view were correct, we should expect similar behaviour from our closest primate relatives. Many non-human primates live in hunter– gatherer type groups and there is constant migration among groups for reasons of exogamous mating. Primates are also able to distinguish kin from non-kin, and engage in repeated interactions, much as humans do. Nevertheless, there is no evidence of behaviors akin to altruistic cooperation and punishment in any primate group [79,80]. Even in such ‘unnatural’ situations as living in large groups in zoos and protective environments, such primates do not exhibit the ‘confusions’ that the mistake hypothesis attributes to humans. The maladaptation explanation of altruistic cooperation suggests that humans find it difficult to distinguish between one-shot and repeated interactions because humans experienced only repeated interaction prior to the appearance of settled communities some 10 000 years before the present. However, humans are perfectly capable of distinguishing shortfrom long-term interactions, and they cooperate much more in the latter case than in the former [81– 83]. Phil. Trans. R. Soc. B (2011)

Moreover, if altruism results from confusion, we would not expect individuals to adjust their level of altruistic contribution rationally according to the costs and benefits. The evidence is that they do. Preferences for altruistic acts entail transitive preferences as required by the notion of rationality in decision theory [84]. In the Dictator Game, the experimenter gives a subject, called the dictator, a certain amount of money and instructs him to give any portion of it he desires to a second, anonymous, subject, called the receiver. The dictator keeps whatever he does not choose to give to the receiver. Obviously, a self-regarding dictator will give nothing to the receiver. Suppose the experimenter gives the dictator m points (exchangeable at the end of the session for real money) and tells him that the price of giving some of these points to the receiver is p, meaning that each point the receiver gets costs the giver p points. For instance, if p ¼ 4, then it costs the dictator 4 points for each point that he transfers to the receiver. The dictator’s choices must then satisfy the budget constraint ps þ ppo ¼ m, where ps is the amount the dictator keeps and po is the amount the receiver gets. The question, then, is simply, is there a preference function u( ps, po) that the dictator maximizes subject to the budget constraint ps þ ppo ¼ m? If so, then it is just as rational, from a behavioural standpoint, to care about giving to the receiver as to care about consuming marketed commodities. Varian [85] developed a generalized axiom of revealed preference (GARP) that ensures that individuals are rational as in the sense of traditional consumer demand theory. Andreoni & Miller [84] worked with 176 students in an elementary economics class and had them play the Dictator Game multiple times each, with the price p taking on the values p ¼ 0.25, 0.33, 0.5, 1, 2, 3 and 4, with amounts of tokens equaling m ¼ 40, 60, 75, 80 and 100. They found that only 18 of the 176 subjects violated GARP at least once and that of these violations, only four were at all significant. By contrast, if choices were randomly generated, we would expect that between 78 and 95 per cent of subjects would have violated GARP. As to the degree of altruistic giving in this experiment, Andreoni and Miller found that 22.7 per cent of subjects were perfectly selfish, 14.2 per cent were perfectly egalitarian at all prices, and 6.2 per cent always allocated all the money so as to maximize the total amount won (i.e. when p . 1, they kept all the money, and when p , 1, they gave all the money to the receiver). Fischbacher et al. [86] also found that subjects adjust their altruistic behaviour strategically when strategic parameters change. They staged an Ultimatum Game with one proposer and several responders, who had to respond simultaneously to the proposal.2 If no responder accepted the offer, both responders and the proposer received zero payoff. If more than one responder accepted the offer, one of the accepting responders was chosen randomly to receive the proposed amount, and the proposer received the remainder, rejecting responders receiving zero. If rejecting a positive offer is simply muddle-headed or blindly emotional, this new setting should not change responder behaviour. If responders reject offers


Review. The nature of human sociality with the goal of punishing proposers, then the frequency of rejection should be very low in the new situation, because no single responder could ensure that punishment would take place. If, however, there are adaptive reasons for altruistic punishment, then we would expect the punishing behaviour to occur only when it can be instrumentally effective, which it cannot in the multiple-recipient version of the Ultimatum Game. The experimenters found that with multiple responders, the rejection rate fell significantly in the two-responder case, and even more in the five-responder case. For instance, whereas in the traditional single-responder case, offers of 20 per cent of the pie are rejected with 80 per cent probability, such offers are rejected with 15 per cent probability when there are five responders. Moreover, the average share of the pie accruing to the responders falls from about 40 per cent with one responder to 20 per cent with two responders, and to about 15 per cent with five responders. Many additional examples can be given suggesting that other-regarding and moral behaviour in humans is part of our adaptive repertoire, rather than being the results of misdirected attempts at maximizing long-term self-interest.

6. THE RATIONALITY OF ALTRUISTIC BEHAVIOUR: THEORY AND EXPERIMENTAL EVIDENCE Morality is an emergent property of the gene –culture evolutionary dynamic that gave rise to our species. We can frame and test propositions concerning moral behaviour using the methods of game theory, involving subjects from a variety of social backgrounds and cultures. Moral behaviour is often held to be incompatible with rational choice. This is incorrect. The rational actor model of economic theory presupposes that people have consistent preferences, but does not require that preferences be self-regarding or materialistic. We can just as easily measure how much people value honesty or loyalty as we can chart how much they value fried chicken or cashmere sweaters. Because the use of the word ‘rational’ in the rational actor model is so circumscribed compared with the general usage of the word, we often call the rational actor model the beliefs, preferences and constraints model (BPC), because this captures the notion of consistent preference, the centrality of beliefs and the notion of making trade-offs subject to informational and material constraints. In the BPC model, choices give rise to probability distributions over outcomes, the expected values of which are the payoffs to the choice from which they arose. Game theory extends this analysis to cases where there are multiple decision makers. In the language of game theory, players are endowed with strategies, and have certain information, and for each array of choices by the players, the game specifies a distribution of payoffs to the players. Game theory predicts the behaviour of the players by assuming each is rational; in other words, each maximizes a preference function subject to beliefs as well as informational and material constraints. Phil. Trans. R. Soc. B (2011)

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The experiments described below are all based on using game theory to set up the choices available to subjects, the knowledge they have on which their choices are based and the payoffs to each subject as a function of their joint strategy choices. We assume the subjects are rational (i.e. consistent) decision-makers, so that their choices reflect their subjective trade-offs among heterogeneous payoffs—some material and some moral and/or other-regarding.

(a) Conditional altruistic cooperation A social dilemma is a situation in which members of a group can gain by cooperating, but cooperation is costly, so each individual does better personally by not cooperating, no matter what the others do. For instance, suppose if a member of a group of size n 2 pays the cost c . 0, he benefits the others by a total amount b . c. We then have a social dilemma: each member can enhance the net gain of the group by cooperating, but a selfish individual will not do so. If all cooperate, each will earn b 2 c . 0, but in a group of self-regarding individuals, each will earn zero. Conditional altruistic cooperation is a predisposition to cooperate in a social dilemma as long as the other players also cooperate. Consider the above social dilemma, with n ¼ 2, called the Prisoner’s Dilemma. In this game, let CC stand for ‘both players cooperate’, let DD stand for ‘both players defect’, let CD stand for ‘player 1 cooperates but his partner defects’, and let DC stand for ‘player 1 defects and his partner cooperates’. A self-regarding player 1 will prefer DC to CC, CC to DD and DD to CD, while an altruistic cooperator will prefer CC to DC, DC to DD and DD to CD; i.e. the self-regarding individual prefers to defect no matter what his partner does, whereas the conditional altruistic cooperator prefers to cooperate so long as his partner cooperates. Kiyonari et al. [87] ran an experiment based on this game with real monetary payoffs using 149 Japanese university students. The experimenters ran three distinct treatments, with about equal numbers of subjects in each treatment. The first treatment was a standard ‘simultaneous’ Prisoner’s Dilemma, the second was a ‘second-player’ situation in which the subject was told that the first player in the Prisoner’s Dilemma had already chosen to cooperate, and the third was a ‘first-player’ treatment in which the subject was told that his decision to cooperate or defect would be made known to the second player before the latter made his own choice. The experimenters found that 38 per cent of the subjects cooperated in the simultaneous treatment, 62 per cent cooperated in the second-player treatment and 59 per cent cooperated in the first-player treatment. The decision to cooperate in each treatment cost the subject about $5 (600 yen). This shows unambiguously that a majority of subjects were conditional altruistic cooperators (62%). Almost as many were not only cooperators, but were also willing to bet that their partners would be (59%), provided the latter were assured of not being defected upon, although under standard conditions, without this assurance, only 38 per cent would in fact cooperate.


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(b) Altruism and cooperation in groups The Public Goods Game, an n-person social dilemma, captures many areas of altruistic cooperation in social life, including voluntary contribution to team and community goals. Researchers [88– 91] uniformly find that groups exhibit a much higher rate of cooperation than can be expected assuming the standard model of the self-regarding actor. A typical Public Goods Game consists of a number of rounds, say 10. In each round, each subject is grouped with several other subjects—say 3 others. Each subject is then given a certain number of points, say 20, redeemable at the end of the experimental session for real money. Each subject then places some fraction of his points in a ‘common account’ and the remainder in the subject’s ‘private account’. The experimenter then tells the subjects how many points were contributed to the common account and adds to the private account of each subject some fraction, say 40 per cent, of the total amount in the common account. So if a subject contributes his whole 20 points to the common account, each of the four group members will receive 8 points at the end of the round. In effect, by putting the whole endowment into the common account, a player loses 12 points but the other three group members gain in total 24 (8 times 3) points. The players keep whatever is in their private accounts at the end of the round. A self-regarding player contributes nothing to the common account. However, most of the subjects do not in fact conform to the self-regarding model. Subjects begin by contributing on average about half of their endowments to the public account. The level of contributions decays over the course of the 10 rounds until in the final rounds most players are behaving in a self-regarding manner. This is, of course, exactly what is predicted by the strong reciprocity model. Because they are altruistic contributors, strong reciprocators start out by contributing to the common pool, but in response to the norm violation of the selfregarding types, they begin to refrain from contributing themselves. How do we know that the decay of cooperation in the Public Goods Game is due to cooperators punishing free riders by refusing to contribute themselves? Subjects often report this behaviour retrospectively. More compelling, however, is the fact that when subjects are given a more constructive way of punishing defectors, they use it in a way that helps sustain cooperation [92 – 96]. Fehr & Ga¨chter [82], for instance, used 6- and 10-round Public Goods Games with group sizes of 4, and with costly punishment allowed at the end of each round, employing three different methods of assigning members to groups. There were sufficient subjects to run between 10 and 18 groups simultaneously. Under the partner treatment, the four subjects remained in the same group for all 10 periods. Under the stranger treatment, the subjects were randomly reassigned after each round. Finally, under the perfect stranger treatment, the subjects were randomly reassigned but assured that they would never meet the same subject more than once. Fehr & Ga¨chter [82] performed their experiment for 10 rounds with punishment and 10 rounds Phil. Trans. R. Soc. B (2011)

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Figure 2. Average contributions over time in the partner, stranger and perfect stranger treatments when the punishment condition is played first [82].

without. Their results are illustrated in figure 2. We see that when costly punishment is permitted, cooperation does not deteriorate, and in the partner game, despite strict anonymity, cooperation increases almost to full cooperation even in the final round. When punishment is not permitted, however, the same subjects experienced the deterioration of cooperation found in previous Public Goods Games. The contrast in cooperation rates between the partner treatment and the two stranger treatments is worth noting because the strength of punishment is roughly the same across all treatments. This suggests that the credibility of the punishment threat is greater in the partner treatment because in this treatment the punished subjects are certain that, once they have been punished in previous rounds, the punishing subjects are in their group. The prosociality impact of strong reciprocity on cooperation is thus more strongly manifested the more coherent and permanent the group in question.

(c) Character virtues Character virtues are ethically desirable behavioural regularities that individuals value for their own sake, while having the property of facilitating cooperation and enhancing social efficiency. Character virtues include honesty, loyalty, trustworthiness, promise-keeping and fairness. Unlike such other-regarding preferences as strong reciprocity and empathy, these character virtues operate without concern for the individuals with whom one interacts. An individual is honest in his transactions because this is a desired state of being, not because he has any particular regard for those with whom he transacts. Of course, the sociopath Homo economicus is honest only when it serves his material interests to be so, whereas the rest of us are at times honest even when it is costly to be so and even when no one but us could possibly detect a breach. Common sense, as well as the experiments described below, indicates that honesty, fairness and promise-keeping are not absolutes. If the cost of virtue is sufficiently high, and the probability of detection of a breach of virtue is sufficiently small, many individuals will behave dishonestly. When one is


Review. The nature of human sociality aware that others are unvirtuous in a particular region of their lives (e.g. marriage, tax paying, obeying traffic rules, accepting bribes), one is more likely to allow one’s own virtue to lapse. Finally, the more easily one can delude oneself into inaccurately classifying an unvirtuous act as virtuous, the more likely one is to allow oneself to carry out such an act. One might be tempted to model honesty and other character virtues as self-constituted constraints on one’s set of available actions in a game, but a more fruitful approach is to include the state of being virtuous in a certain way as an argument in one’s preference function, to be traded off against other valuable objects of desire and personal goals. In this respect, character virtues are in the same category as ethical and religious preferences and are often considered subcategories of the latter. Numerous experiments indicate that most subjects are willing to sacrifice material rewards to maintain a virtuous character even under conditions of anonymity. Sally [97] undertook a meta-analysis of 137 experimental treatments, finding that face-to-face communication, in which subjects are capable of making verbal agreements and promises, was the strongest predictor of cooperation. Of course, face-to-face interaction violates anonymity and has other effects besides the ability to make promises. However, both Bochet et al. [98] and Brosig et al. [99] report that only the ability to exchange verbal information accounts for the increased cooperation. A particularly clear example of such behaviour is reported by Gneezy [100], who studied 450 undergraduate participants paired off to play three games of the following form, all payoffs to which were of the form (b,a), where player 1, Bob, receives b and player 2, Alice, receives a. In all games, Bob was shown two pairs of payoffs, A : (x,y) and B : (z,w) where x, y, z and w are amounts of money with x , z and y . w, so in all cases B is better for Bob and A is better for Alice. Bob could then say to Alice, who could not see the amounts of money, either ‘option A will earn you more money than option B’, or ‘option B will earn you more money than option A’. The first game was A : (5,6) versus B : (6,5) so Bob could gain 1 by lying and being believed while imposing a cost of 1 on Alice. The second game was A : (5,15) versus B : (6,5), so Bob could gain 1 by lying and being believed, while still imposing a cost of 10 on Alice. The third game was A : (5,15) versus B : (15,5), so Bob could gain 10 by lying and being believed, while imposing a cost of 10 on Alice. Before starting play, Gneezy asked the various Bobs whether they expected their advice to be followed. He induced honest responses by promising to reward subjects whose guesses were correct. He found that 82 per cent of Bobs expected their advice to be followed (the actual number was 78%). It follows from the Bobs’ expectations that if they were self-regarding, they would always lie and recommend B to Alice. The experimenters found that, in game 2, where lying was very costly to Alice and the gain from lying was small for Bob, only 17 per cent of Bobs lied. In game 1, where the cost of lying to Alice was only 1 but the gain to Bob was the same as in game 2, 36 Phil. Trans. R. Soc. B (2011)

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per cent of Bobs lied. In other words, Bobs were loath to lie but considerably more so when it was costly to Alices. In game 3, where the gain from lying was large for Bob and equal to the loss to Alice, fully 52 per cent of Bobs lied. This shows that many subjects are willing to sacrifice material gain to avoid lying in a one-shot anonymous interaction, their willingness to lie increasing with an increased cost to them of truth telling, and decreasing with an increased cost to their partners of being deceived. Similar results were found by Boles et al. [101] and Charness & Dufwenberg [102]. Gunnthorsdottir et al. [103] and Burks et al. [104] have shown that a socio-psychological measure of ‘Machiavellianism’ predicts which subjects are likely to be trustworthy and trusting. 7. CONCLUSION Population biology traditionally takes the environment as exogenous. However, we know that life-forms affect their own environment and the environments they produce change the pattern of genetic evolution they undergo. Niche construction augments population biology by rendering environmental change itself part of the evolutionary dynamic. Gene – culture coevolution is the application of niche-construction reasoning to the human species, recognizing that both genes and culture are subject to similar dynamics, and human society is a cultural construction that provides the environment for fitness-enhancing genetic changes in individuals. The resulting social system is a complex dynamic nonlinear system. Such systems have emergent properties, some of which have been analysed in this paper: social norms, morality, other-regarding preferences and the internalization of norms. I would like to thank the editors of this volume for suggesting improvements in my analysis, and the European Science Foundation and the Hungarian Scientific Research Fund (OTKA) for financial support.

ENDNOTES 1

Dawkins recognized that the extended phenotypic expression of a genotype should affect the fitness of that genotype, but opposes considering that this expression can also have the niche-constructive effect of modifying the selective environment for other genotypes (see Dawkins [19]). 2 In the standard Ultimatum Game, the proposer is given some money (the ‘pie’), and is instructed to offer any fraction he desires to an anonymous second player, the responder. If the responder accepts, they divide the money accordingly. If the responder rejects the offer, neither player receives anything.

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Research

Evolution of culture-dependent discriminate sociality: a gene – culture coevolutionary model Yasuo Ihara* Department of Biological Sciences, University of Tokyo, Hongo 7-3-1, Bunkyoku, Tokyo 113-0033, Japan Animals behave cooperatively towards certain conspecifics while being indifferent or even hostile to others. The distinction is made primarily according to kinship as predicted by the kin selection theory. With regards to humans, however, this is not always the case; in particular, humans sometimes exhibit a discriminate sociality on the basis of culturally transmitted traits, such as personal ornaments, languages, rituals, etc. This paper explores the possibility that the human faculty of cultural transmission and resultant cultural variation among individuals may have facilitated the evolution of discriminate sociality in humans. To this end, a gene– culture coevolutionary model is developed focusing on competition over control of resource as a context in which discriminate sociality may have evolved. Specifically, two types of culture-dependent discriminate sociality are considered: ingroup favouritism, with ingroup and outgroup being distinguished by the presence or absence of a cultural trait; and prestige hierarchies, with the prestige being conferred on the bearer of a cultural trait. The model specifies the conditions under which emergence and evolutionary stability of the two types of discriminate sociality are promoted by the presence of cultural variation among individuals. Keywords: cultural niche construction; Hawk– Dove game; ingroup favouritism; Middle/Upper Palaeolithic transition; prestige; tag-based cooperation

1. INTRODUCTION Cooperative behaviours in most animals are primarily directed towards close kin. Kin selection is believed to have shaped the innate predispositions in these animals to behave cooperatively to certain individuals but not to others [1]. Human individuals can also establish a strong emotional tie with certain individuals and behave cooperatively towards them while at the same time being indifferent or even hostile to others. In contrast to most non-human animals, however, human decisions regarding whether or not to behave cooperatively towards certain individuals are not necessarily based on kinship. Indeed, the flexibility in the choice of allies to whom cooperation is offered may be a salient feature of human sociality [2,3]. Evolution of cooperative behaviour among unrelated individuals has been studied extensively within the framework of Prisoner’s Dilemma (PD) [4 – 6]. In a two-person PD, two individuals behave either cooperatively or uncooperatively towards each other and obtain a benefit from mutual cooperation, while each individual gains most from unilateral cooperation by the partner and loses most by cooperating unilaterally. Evolution of cooperation in groups has also been investigated by using n-person PD [7 –9].

Resource-sharing is a form of cooperative behaviour. It is not hard to imagine that during the history of human evolution, there were times of resource scarcity owing to climate change, excessive exploitation, dispersal into an unfamiliar environment, and so on. Scarcity of critical resources leads to intraspecific competition, in which individuals may either try to monopolize the available resources or share them with others. Although each individual gains most when it successfully monopolizes the resources, others may also try to do the same, in which case aggressive fights may result. In species such as humans, aggressive fight over control of resource can be extremely costly, especially during the time of resource scarcity, so that individuals may be better off sharing the resource with others rather than running the risk of deadly conflict. Dyadic competition over control of resource can be investigated using Hawk– Dove games [10,11]. In the conventional terminology, a Hawk– Dove game represents a contest between two players, each of whom either escalates the contest (Hawk) or displays first but retreats if the opponent escalates the contest (Dove). In the present context, the contest is rephrased as a dyadic interaction in which each individual either tries to monopolize a resource or is willing to share it with the opponent. Key assumptions are as follows: first, if both individuals contend for the resource, the winner of an aggressive fight takes it and the loser suffers injury; second, if one contends for the resource

*[email protected] One contribution of 13 to a Theme Issue ‘Human niche construction’.

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and the other is willing to share, the former takes the resource without aggressive fight; and third, if both individuals are willing to share, the resource is shared equally. It is certainly not a good idea to always try to share the resource because then those who are not willing to share will take all the resource. In Hawk – Dove games, a population of individuals who always try to share is evolutionarily unstable, being vulnerable to invasion by those who always contend for the resource. On the other hand, it may not be a good idea either to always try to monopolize the resource since in that case one will be frequently involved in dangerous fights. In Hawk–Dove games, a population of individuals who always contend for the resource is evolutionarily unstable if the cost of injury is substantial relative to the value of the resource. Note that if the cost of injury is sufficiently small that an aggressive fight on average pays for individuals, resource-sharing as described here can be formulated as a two-person PD. When the cost of injury is substantial, contingent strategies that modify the behaviour according to with whom they are interacting can be evolutionarily stable. For strategies with such discriminate sociality to be possible, individuals need to differ in some ways. For example, the strategy called Assessor evaluates the relative fighting abilities, or resource-holding powers (RHPs), of individuals and tries to monopolize resources if it has a greater RHP than its opponent [10,11]. In addition, natural selection can also favour discriminate sociality for individual variations that are not correlated with RHP. For example, the strategy called Bourgeois, which contends for resources only if it is the ‘owner’ of them, can be evolutionarily stable [10,11]. Among humans, there exists an abundance of individual variations apparently uncorrelated with RHP. Human faculty of cultural transmission seems to play an essential role in creating such variations [12–15]. If solving a problem as represented by a Hawk–Dove game has been crucial in survival and reproduction of human individuals, especially during the times of resource scarcity, it is theoretically plausible that natural selection may have shaped a culture-dependent discriminate sociality in humans, that is, a predisposition to choose certain unrelated individuals on the basis of cultural variations and behave cooperatively only to them. Since natural selection would not have worked in this way without the human faculty of cultural transmission, this scenario is coherent with the niche construction perspective, which emphasizes the capability of humans (and other organisms) to modify their environment and consequently alter the selective pressure acting on them [16,17] (see also Gintis [18] for gene–culture coevolution of human sociality). Theoretical models have been developed to investigate possible effects of cultural transmission on human niche construction [19–21]. Humans have been suggested to have a distinct set of psychological mechanisms designed by natural selection causing them to exhibit discriminate sociality [22]. More specifically, Kurzban & Leary [22] argued that stigmatization, or exclusion of individuals with certain characteristics from social exchanges, may be caused Phil. Trans. R. Soc. B (2011)

by a set of psychological mechanisms that has played a role in avoiding poor social exchange partners, forming dominant social groups, and keeping distance from infectious diseases through the history of human evolution. Another possibility is that discriminate sociality and the underlying psychological mechanisms may have been selectively favoured even though the distinction is based on arbitrary cultural variations that have nothing to do with the quality or health conditions of individuals. Ingroup favouritism, or the tendency of human individuals to treat ingroup members more favourably than outgroup members, is an example of discriminate sociality. Tajfel et al. [23] conducted experiments on intergroup behaviour in which subjects were told that they were divided into two groups on the basis of a nominal criterion, such as whether they overestimated or underestimated numbers of dots projected on a screen or whether they preferred abstract paintings by one or the other painters. When asked to allocate rewards, the subjects transferred larger amounts of money to ingroup members than to outgroup members although there was no personal advantage in doing so and the group membership was completely anonymous. This and other studies have suggested that ingroup favouritism can emerge in the laboratory from mere categorization even if it is based on trivial and arbitrary criteria (see also [24]; reviewed in Yamagishi et al. [25]). Another example of discriminate sociality arises from social hierarchy; that is, individuals sometimes behave discriminately in favour of those who occupy higher social status [26]. Henrich & Gil-White [27] highlighted the distinction between two types of social status: dominance and prestige. According to their definitions, dominance hierarchies are supported predominantly by force or force threat, while prestige hierarchies involve non-coerced deference by subordinates. In the context of the present study, dominance and prestige hierarchies may be regarded as consequences of RHP-dependent and RHP-independent discriminate sociality, respectively. Furthermore, Henrich & Gil-White [27] postulated a distinct set of psychological mechanisms through which prestige hierarchies emerge, advocating the view that these psychological mechanisms have been favoured by natural selection since subordinates have been able to acquire fitness-inducing skills and knowledge by conferring deference to those who have such useful cultural traits. Alternatively, but not incompatible with this view, prestige hierarchies may have been advantageous for subordinates in which such hierarchies facilitate avoidance of aggressive fights when difference in RHP is not clearly observable. Variations among individuals in cultural traits (such as personal ornaments, languages, rituals, etc.) may have played a role in the evolution of human behaviour by promoting the emergence of discriminate sociality and underlying psychological mechanisms. In this paper, I explore this possibility using a simple gene – culture coevolutionary model (see [28]). A related issue is the evolution of ‘tag-based’ cooperation, in which cooperation is established among individuals sharing the same arbitrary trait [29– 34]. In contrast

Culture-dependent discriminate sociality to the previous studies, this paper explicitly incorporates the vertical and horizontal transmission of a cultural trait [12] and focuses on the competition between two unrelated individuals over control of resources as a context in which the evolution may have taken place. Analysis of simple models such as PD and Hawk– Dove games has played a crucial role in studies of human behaviour. If used appropriately, simple models have the merits of clarifying the logical coherence of a hypothesis that is very complicated for verbal arguments, elucidating minimal assumptions required to explain complex phenomena, and providing qualitative predictions to be tested empirically. In the following sections, I first introduce a general modelling framework in which genetic inheritance of behavioural strategies and cultural transmission of an arbitrary trait are considered. Secondly, I introduce competition over control of resource into the general framework and specify two competing strategies, one of which exhibits culture-dependent discriminate sociality. Finally, I examine whether culture-dependent discriminate sociality can emerge in a population without it and whether it can be evolutionarily stable. Through the analysis, I suggest that cultural variation among individuals can facilitate the evolution of discriminate sociality, which in turn may stimulate the spread of culturally transmitted traits. 2. MODEL (a) The general framework We examine whether a mutant strategy can invade a population of a resident strategy assuming that the fitness of a strategy depends on cultural variation among individuals. To this end, let us first introduce a gene – culture coevolutionary model that includes vertical and horizontal transmission of a cultural trait [12] and differential reproduction owing to culture-dependent fitness difference. Consider a population of asexually reproducing individuals with discrete generations. Suppose that each individual has either strategy A or B. Individuals are also dichotomized for the presence or absence of a cultural trait. Thus, there are four phenogenotypes in the population: strategy A without the cultural trait (A0), strategy A with the cultural trait (A1), strategy B without the cultural trait (B0) and strategy B with the cultural trait (B1) (table 1). Population dynamics are modelled by assuming the following life cycles. First, individuals are born. Second, individuals may acquire the cultural trait via cultural transmission from their parents (vertical transmission). Third, the cultural trait may be transmitted within the offspring generation (horizontal transmission). Fourth, viability and/or fertility selection act on individuals through fitness difference, where an individual’s fitness depends on cultural variation among individuals. Fifth, individuals give birth and die after the phase of cultural transmission to their offspring. Further details of the population dynamics are described in appendix A. (b) Competition over control of resource Suppose that individuals compete over control of a resource that affects their fitness. Competition occurs Phil. Trans. R. Soc. B (2011)

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Table 1. The four phenogenotypes.

phenogenotype

strategy

cultural trait

frequency

fitness

A0 A1 B0 B1

A A B B

absent present absent present

uA0 uA1 uB0 uB1

WA0 WA1 WB0 WB1

Table 2. The expected payoff to the self according to behaviours of the interacting individuals. b . 0, c . 0. behaviour (opponent) behaviour (self)

peaceful

aggressive

peaceful aggressive

b 2b

0 b2c

as a dyadic interaction in which each individual is either aggressive or peaceful. When aggressive, an individual contends with the opponent for the resource and is prepared for an aggressive fight, whereas a peaceful individual is willing to share the resource with the opponent but will abandon it if necessary to avoid fighting. If both individuals are peaceful, the resource is shared equally and each of them gains a payoff b (b . 0). If both individuals are aggressive, an aggressive fight occurs, and one of them eventually wins the resource gaining a payoff 2b, while the loser pays a cost 2c from injury (c . 0). If one individual is aggressive and the other peaceful, the former monopolizes the resource, which results in a payoff 2b, while the payoff to the latter is 0. Assume that two interacting individuals always differ in RHP and the one with a greater RHP wins an aggressive fight with the probability d (1/2 , d , 1). Following previous studies, assume further that each individual is equally likely to have a greater RHP than its opponent [10,11]. Table 2 shows the expected payoffs from an interaction. Fitness of an individual is determined by a baseline value, w (w . 0), the frequencies of the phenogenotypes, uA0, uA1, uB0 and uB1 (uA0 þ uA1 þ uB0 þ uB1 ¼ 1; see table 1) and the expected payoffs from the competition over resource, WA0, WA1, WB0 and WB1 (see table 1): WA0 ¼ w þ uA0 V ðA0jA0Þ þ uA1 V ðA0jA1Þ þ uB0 V ðA0jB0Þ þ uB1 V ðA0jB1Þ;

ð2:1Þ

WA1 ¼ w þ uA0 V ðA1jA0Þ þ uA1 V ðA1jA1Þ þ uB0 V ðA1jB0Þ þ uB1 V ðA1jB1Þ;

ð2:2Þ

WB0 ¼ w þ uA0 V ðB0jA0Þ þ uA1 V ðB0jA1Þ þ uB0 V ðB0jB0Þ þ uB1 V ðB0jB1Þ

ð2:3Þ

and WB1 ¼ w þ uA0 V ðB1jA0Þ þ uA1 V ðB1jA1Þ þ uB0 V ðB1jB0Þ þ uB1 V ðB1jB1Þ;

ð2:4Þ

where V(XjY ) denotes the expected payoff to phenogenotype X when interacting with phenogenotype Y.

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(c) The strategies The following two strategies are considered. First, Assessor is a strategy that evaluates the relative RHPs of interacting individuals and behaves aggressively if and only if its RHP is perceived to be greater than the opponent’s [10,11]. Roughly speaking, Assessor is peaceful to the stronger and aggressive to the weaker. In addition, assume that RHP is not always evaluated accurately: Assessor’s evaluation is incorrect in the proportion e of all cases (0 , e , 1/2). Note that Assessor’s behaviour is not affected by cultural variation among individuals. Second, consider a strategy that alters the behaviour based on the presence or absence of the cultural trait in interacting individuals. The strategy, which is called Culture-dependent discriminator (CDD), is aggressive against its opponent with the probability fij, where i signifies the presence (i ¼ 1) or absence (i ¼ 0) of the cultural trait in the self, and j signifies the presence ( j ¼ 1) or absence ( j ¼ 0) of the same trait in the opponent (0 fij 1) (table 3). Assume that the cultural trait is so conspicuous that its presence or absence is clearly observable and always recognized accurately. Table 4 shows the expected payoffs, V(XjY ), under these assumptions (appendix B). 3. ANALYSIS Let strategies A and B be Assessor and CDD, respectively (see appendix C for a more general treatment). A special emphasis is on the following two behaviour rules for CDD. The first rule is specified by f00 ¼ f11 ¼ 0 and f01 ¼ f10 ¼ 1 (rule I), in which CDD is always peaceful towards someone who is concordant with itself for the presence or absence of the cultural trait while always aggressive against someone who is discordant in this respect. When following rule I, CDD can be regarded as exhibiting an ingroup favouritism, with ingroup and outgroup being defined by the cultural variation among individuals. The second rule is given by f01 ¼ f11 ¼ 0 and f00 ¼ f10 ¼ 1 (rule II); that is, CDD is always peaceful towards those with the cultural trait and always aggressive against those without it. Rule II may apply if the cultural trait is perceived by CDD as indicative of prestige. In other words, CDD with rule II can be regarded as following a prestige hierarchy, with the prestige being defined by the cultural variation among individuals. When the cultural trait is newly introduced into a population consisting only of Assessors by invention or transmission from other populations, the frequency of individuals having the trait may either increase or decrease in succeeding generations. The frequency decreases and eventually becomes 0 if vA ,

1 ; ð1 þ hA Þ

ð3:1Þ

where vA and hA represent, respectively, the rates of vertical and horizontal transmission for Assessor (0 , vA , 1, 0 , hA , 1; see appendix A). Intuitively, when (3.1) holds, the rates of vertical and/or horizontal transmission are not sufficiently high to allow the cultural trait to spread; hence, cultural trait is absent in the equilibrium population of Assessor. In contrast, Phil. Trans. R. Soc. B (2011)

Table 3. CDD’s probability of aggression ( fij ) according to the presence or absence of the cultural trait in the interacting individuals. cultural trait (opponent) cultural trait (self)

absent

present

absent present

f00 f10

f01 f11

the frequency of the cultural trait increases and eventually converges to y2 if the inequality in (3.1) is reversed, where y2 ¼ ½ð1 þ hA ÞvA 1=ðhA v2A Þ. Note that y2 increases as either vA or hA increases. Thus, there are some individuals with the trait in the equilibrium population of Assessor when the inequality in (3.1) is reversed. Suppose that a small frequency of CDD is introduced, by mutation of immigration, into the equilibrium population of Assessor. If the frequency of CDD increases in the succeeding generations, CDD is said to invade the population. On the contrary, if the frequency can never increase and always converges to 0, the population of Assessor is referred to as stable against invasion by CDD. Whether CDD can invade the equilibrium population of Assessor is examined for each of the two behaviour rules for CDD (rules I and II) (see appendix D for details). Similarly, a population consisting only of CDDs will converge either to an equilibrium state in which the cultural trait is absent or to another in which some individuals possess the trait. Whether the equilibrium population of CDD can be stable against invasion by Assessor is examined for each of the behaviour rules (see appendix E for details). (a) Rule I: ingroup favouritism Suppose that CDD follows rule I ( f00 ¼ f11 ¼ 0, f01 ¼ f10 ¼ 1). Whether CDD with Rule I can invade the equilibrium population of Assessor is examined as follows. First, consider the case when the ratio of the benefit from resource acquisition to the cost from injury, b/c, is low, specifically, b , 2eð1 eÞ: c

ð3:2Þ

In this case, CDD with rule I can invade the equilibrium population of Assessor in which the cultural trait is absent. This is consistent with intuition since when the cultural trait is absent, CDD with rule I is always peaceful, and this behaviour pays off given that b/c is sufficiently low. When the inequality in (3.1) is reversed and thus the cultural trait is present in the equilibrium population of Assessor, invasion by CDD with rule I is possible if either of the following two conditions is met: and vB , vB ; vA , v A vA . vA and vB . vB ;

ð3:3Þ ð3:4Þ

where vB is the rate of vertical transmission for CDD (0 , vB , 1; see appendix A) and the threshold rates of vertical transmission, vA , v A and vB are given in

Culture-dependent discriminate sociality (a)

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(b)

1.0 0.8

vB

0.6 0.4 0.2 0

(c)

(d)

1.0 0.8

vB

0.6 0.4 0.2

0

0.2

0.4

0.6

0.8

1.0

0

vA

0.2

0.4

0.6

0.8

1.0

vA

Figure 1. Regions on the vAvB-plane for which CDD with rule I can invade the population of Assessor (the shaded regions) and combinations of parameter values for which the population of CDD with rule I is stable (the filled circles) or unstable (the empty circles) against invasion by Assessor, where vA and vB denote the rates of vertical transmission for Assessor and CDD, respectively. The dashed lines represent vA ¼ 1/(1 þ hA). (a) b ¼ 4; (b) b ¼ 5; (c) b ¼ 9; and (d) b ¼ 15. Other parameter values are: w ¼ 20, c ¼ 10, d ¼ 0.6, e ¼ 0.4, hA ¼ 0.5 and hB ¼ 0.8. Table 4. The expected payoff to the self according to the strategies (Assessor or CDD) and the cultural trait (present or absent) in the interacting individuals. a ¼ b/2 2 ce(1 2 e), b ¼ 3b/2 2 (b þ c)(e þ d 2 2ed), g ¼ b/2 þ (b þ c)(1 2 e 2 d þ 2ed). opponent self

Assessor (absent)

Assessor (present)

CDD (absent)

CDD (present)

Assessor (absent) Assessor (present) CDD (absent) CDD (present)

b/2 þ a b/2 þ a b/2 þ f00b b/2 þ f10b

b/2 þ a b/2 þ a b/2 þ f01b b/2 þ f11b

3b/2 2 f00g 3b/2 2 f01g 2 b cf00 b(1 2 f01 þ f10) 2 cf01f10

3b/2 2 f10g 3b/2 2 f11g b(1 þ f01 2 f10) 2 cf01f10 2 b cf11

appendix D. Note that 1=ð1 þ hA Þ , v A , vA in this case. Figure 1a illustrates the regions on the vAvB-plane in which CDD with rule I can invade the equilibrium population of Assessor (the shaded regions) when (3.2) holds. Second, when the benefit-to-cost ratio is intermediate so that

2eð1 eÞ ,

b e þ d 2ed eð1 eÞ , ; c 1 e d þ 2ed

ð3:5Þ

CDD with rule I can never invade the equilibrium population of Assessor whether or not individuals having the cultural trait exist (figure 1b). Phil. Trans. R. Soc. B (2011)

Third, consider the case when the benefit-to-cost ratio is high, specifically, b e þ d 2ed eð1 eÞ . : c 1 e d þ 2ed

ð3:6Þ

When (3.1) holds so that the cultural trait is absent in the equilibrium population of Assessor, CDD with rule I cannot invade the population. Nevertheless, if both CDD and the cultural trait are introduced simultaneously into the population, their frequencies may increase in a coevolutionary manner, even though either one of them cannot increase in the absence of the other (given that (3.1) and (3.6) hold). This type of gene – culture coevolution is possible if CDD’s rate

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(b)

1.0

cultural trait

0.8 0.6 0.4 0.2 0 0

0.2 0.4 0.6 0.8 CDD with rule I

1.0

0

0.2 0.4 0.6 0.8 CDD with rule I

1.0

Figure 2. Sample trajectories of changes in the frequencies of CDD with rule I (uB0 þ uB1) and the cultural trait (uA1 þ uB1). The arrows indicate directions of changes. The filled and empty circles represent locally stable and unstable equilibrium states, respectively. (a) b ¼ 5, vA ¼ 0.2, vB ¼ 0.8; (b) b ¼ 9, vA ¼ 0.2, vB ¼ 0.95. Other parameter values are: w ¼ 20, c ¼ 10, d ¼ 0.6, e ¼ 0.4, hA ¼ 0.5 and hB ¼ 0.8.

of vertical transmission is sufficiently high, namely, vB .

w þ b=2 þ a ; w þ b=2 þ b

ð3:7Þ

where a ¼ b/2 2 ce(1 2 e) and b ¼ 3b/2 2 (b þ c)(e þ d 2 2ed). When the inequality in (3.1) is reversed so that a proportion, y2 , of individuals possess the cultural trait in the equilibrium population of Assessor, invasion by CDD with rule I is possible if either of the following two conditions is met: vA , vA

and

vB . vB ;

ð3:8Þ

vA . v A

and

vB , vB ;

ð3:9Þ

where 1=ð1 þ hA Þ , vA , v A in this case. Figure 1c,d shows the parameter region in which CDD with rule I can invade the equilibrium population of Assessor when (3.6) holds (parameter combinations satisfying (3.9) do not exist in these examples). Inequality (3.8) means that invasion by CDD with rule I is possible if the rate of vertical transmission for Assessor is low and the corresponding rate for CDD is high. This is explained as follows: when (3.8) is met, the cultural trait will become statistically associated with CDD, and consequently, CDD’s ingroup favouritism induces aggressive behaviour against Assessor, which gives a fitness advantage to CDD as the benefit-tocost ratio of aggressive fight is high (i.e. (3.6)). Similarly, according to (3.9), invasion by CDD with rule I is also possible if vA is large and vB is small. This is because though in this case the cultural trait will become associated with Assessor, CDD’s ingroup favouritism still promotes aggression against Assessor. Let us now turn to the stability of the population of CDD. Assessor can always invade the equilibrium population of CDD with rule I if no-one has the cultural trait. However, when some individuals have the trait at the equilibrium state, the population of CDD with rule I can be stable for some combinations of parameter values satisfying either (3.2), (3.5) or (3.6) as shown in figure 1 (the filled circles). Figure 2 shows sample trajectories of changes in the frequencies of CDD with rule I and the cultural Phil. Trans. R. Soc. B (2011)

trait for parameter values satisfying (3.5) (figure 2a) or (3.6) (figure 2b). (b) Rule II: prestige hierarchies Suppose that CDD follows rule II ( f01 ¼ f11 ¼ 0, f00 ¼ f10 ¼ 1). Whether CDD with rule II can invade the equilibrium population of Assessor is examined as follows. First, consider the case when the benefit-to-cost ratio, b/c, is low so that (3.2) holds. In this case, CDD with rule II cannot invade the equilibrium population of Assessor in which the cultural trait is absent. When the inequality in (3.1) is reversed and thus the proportion y2 of individuals have the cultural trait at the equilibrium state, invasion by CDD with rule II is possible if vA . vA :

ð3:10Þ

Thus, the presence of the cultural trait can also facilitate the invasion by CDD with rule II, which is never possible in the absence of the trait. Figure 3a illustrates the parameter region in which CDD with rule II can invade the equilibrium population of Assessor (the shaded region) when (3.2) holds. It is worth mentioning that (3.10) does not depend on vB or hB, the rates of vertical and horizontal transmission for CDD. This is explained as follows. CDD with rule II perceives others as prestigious and thus behaves peacefully towards them whenever they possess the cultural trait. Hence, when CDD is rare, an individual CDD’s fitness does not vary depending on whether or not the individual has the trait, although it does vary depending on the prevalence of the trait among Assessors. As the benefit-to-cost ratio of aggressive fight is low, CDD with rule II gains a greater payoff when the trait is more common (recall that y2 increases with vA). Second, when the benefit-to-cost ratio is intermediate so that (3.5) is satisfied, CDD with rule II can never invade the equilibrium population of Assessor, irrespective of the presence or absence of the cultural trait in the population (figure 3b). Third, consider the case when the benefit-to-cost ratio is high so that (3.6) holds. CDD with rule II can invade the equilibrium population of Assessor in which the cultural trait does not exist. This is


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(b)

1.0 0.8

vB

0.6 0.4 0.2 0

(c)

(d)

1.0 0.8

vB

0.6 0.4 0.2

0

0.2

0.4

0.6

0.8

1.0

vA

0.2

0.4

0.6 vA

0.8

1.0

Figure 3. Regions on the vAvB-plane for which CDD with rule II can invade the population of Assessor (the shaded regions) and combinations of parameter values for which the population of CDD with rule II is stable (the filled circles) or unstable (the empty circles) against invasion by Assessor, where vA and vB denote the rates of vertical transmission for Assessor and CDD, respectively. The dashed lines represent vA ¼ 1/(1 þ hA). (a) b ¼ 4; (b) b ¼ 5; (c) b ¼ 9; and (d) b ¼ 15. Other parameter values are: w ¼ 20, c ¼ 10, d ¼ 0.6, e ¼ 0.4, hA ¼ 0.5 and hB ¼ 0.8.

because CDD with rule II is always aggressive when no one has the cultural trait, and behaving in this way pays off given that b/c is sufficiently high. When the inequality in (3.1) is reversed so that the cultural trait exists in the equilibrium population of Assessor, invasion by CDD with rule II is possible if vA , vA :

ð3:11Þ

Figure 3c,d shows the parameter regions in which CDD with rule II can invade the equilibrium population of Assessor when (3.6) is satisfied. Let us now examine the stability of the population of CDD. Assessor can invade the equilibrium population of CDD with rule II in which the cultural trait is absent if b e þ d 2ed , : c 1 e d þ 2ed

ð3:12Þ

On the contrary, when some individuals have the trait at the equilibrium state, the population of CDD with rule II can be stable against invasion by Assessor, even for parameter combinations satisfying (3.12) (the filled circles in figure 3). Figure 4 shows sample trajectories of the population dynamics for parameter combinations satisfying (3.2) (figure 4a) or (3.5) (figure 4b). Phil. Trans. R. Soc. B (2011)

4. DISCUSSION Evolution of culture-dependent discriminate sociality is explored by analysing a gene – culture coevolutionary model in which competition over control of resource is assumed to have a significant impact on the fitness of individuals. The competition is formulated as a Hawk– Dove game (table 2), in which two strategies, CDD and Assessor, are considered. CDD alters its behaviour depending on the presence or absence of a culturally transmitted trait among individuals (table 3), while Assessor’s behaviour depends not on the cultural variation, but on the relative RHPs of individuals. Two behaviour rules, rules I and II, that determine how CDD responds to given patterns of cultural variation are examined. When behaving under rule I, CDD is regarded as exercising ingroup favouritism, with ingroup and outgroup being categorized based on the cultural variation. When rule II is assumed, on the other hand, CDD is regarded as following a prestige hierarchy, with the prestige being identified based on the cultural variation. An aggressive fight over control of resource results in a benefit of resource acquisition, b, to the winner and a cost of injury, c, to the loser. Whether CDD can invade the population of Assessor is investigated for each of the three ranges of the benefit-to-cost ratio, b/c, specified by (3.2), (3.5) and (3.6). When b/c is low so that (3.2) holds, aggressive fighting is extremely costly and hence a strategy that is always peaceful would

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(b)

1.0

cultural trait

0.8 0.6 0.4 0.2 0 0

0.2 0.4 0.6 0.8 CDD with rule II

1.0

0

0.2 0.4 0.6 0.8 CDD with rule II

1.0

Figure 4. Sample trajectories of changes in the frequencies of CDD with rule II (uB0 þ uB1) and the cultural trait (uA1 þ uB1). The arrows indicate directions of changes. The filled and empty circles represent locally stable and unstable equilibrium states, respectively. (a) b ¼ 4, vA ¼ 0.9, vB ¼ 0.6; (b) b ¼ 5, vA ¼ 0.6, vB ¼ 0.6. Other parameter values are: w ¼ 20, c ¼ 10, d ¼ 0.6, e ¼ 0.4, hA ¼ 0.5 and hB ¼ 0.8.

invade the population of Assessor. Similarly, CDD with rule I can invade the population of Assessor without the cultural trait since this strategy is always peaceful in the absence of cultural variation (figure 1a). In contrast, CDD with rule II cannot invade the population of Assessor without the cultural trait as this strategy is always aggressive in the absence of cultural variation. Nonetheless, CDD with Rule II may invade the population of Assessor if more than a threshold proportion of the resident individuals have the cultural trait (figure 3a). That is, the presence of the cultural trait can facilitate the invasion by CDD with rule II. When b/c is intermediate so that (3.5) is satisfied, the population of Assessor is not invaded by a strategy that is always peaceful or one that is always aggressive. Accordingly, neither CDD with rules I nor II can invade the population of Assessor without the cultural trait. Thus, if CDD could invade the population of Assessor in the presence of the cultural trait, that would be an even stronger support for the claim that the presence of the cultural trait facilitates the evolution of discriminate sociality. This turns out, however, not to be the case: invasion by CDD is not possible even if the cultural trait exists in the equilibrium population of Assessor (figures 1b and 3b). When b/c is high so that (3.6) holds, aggressive fighting is relatively less costly (though b , c may still hold) and thus a strategy that is always aggressive can invade the population of Assessor. Hence, CDD with rule II can also invade the population of Assessor without the cultural trait (figure 3c,d ). On the other hand, CDD with rule I cannot invade the population of Assessor if the cultural trait does not exist at all. Nonetheless, the frequencies of CDD with rule I and the cultural trait may increase in a coevolutionary manner if both are introduced into the population (figure 1c,d ). In other words, ingroup favouritism and cultural variation on which it depends can emerge, through gene – culture coevolution, where none of them initially exists. The coevolutionary process takes place when Assessor’s rate of vertical transmission is low and CDD’s rate is high (see (3.1), (3.7) and (3.8)). This might be possible if individuals are strongly motivated to acquire the cultural Phil. Trans. R. Soc. B (2011)

trait through vertical transmission only if they have the innate predisposition to culture-dependent ingroup favouritism; that is to say, while individuals without the predisposition are indifferent to having or not having the cultural trait, those with the predisposition may be more sensitive about and thus inclined to display what they regard as their group identity. Whether the population of CDD can be stable against invasion by Assessor is also examined. The population of CDD in which no one has the cultural trait can never be stable when rule I is assumed, and cannot be stable unless (3.12) is violated when rule II is assumed. However, the population of CDD with either rules I or II can be stable in the presence of cultural variation among CDDs. Combination of parameter values are found for which the population of CDD is stable within each of the three ranges of the benefit-to-cost ratio (figures 1 and 3). The presence of cultural variation, therefore, can always stabilize the population of individuals possessing discriminate sociality. Two things about the model assumptions are worth mentioning. First, I intend to keep the model as simple as possible primarily for logical clarity and mathematical tractability. More realistic but less simple assumptions are also possible; for example, one can assume that each individual has a constant RHP rather than a constant probability of having a greater RHP than its opponent. In this sense, the model presented in this paper can serve as a basis for future studies that incorporate more realistic assumptions. Second, although I assume throughout this paper that the strategies (i.e. Assessor and CDD) are genetically transmitted, the model is consistent with the interpretation that they are culturally transmitted. In the latter case, the transmission of the strategies follows replicator dynamics where the probability with which the strategy of a given individual is imitated is proportional to its ‘fitness’ (see [35]).

(a) Evolution of discriminate sociality Evolution of discriminate sociality for phenotypic similarity has been studied in the recent literature on

Culture-dependent discriminate sociality tag-based cooperation [29 – 34]. Riolo et al. [29], using agent-based computer simulations, suggested that evolution of cooperation is facilitated if each agent discriminates other agents to make costly donations only to those that are similar to itself in an arbitrary tag. Axelrod et al. [30] conducted another series of simulations, in which coevolution of an arbitrary tag and behavioural strategy in a two-person PD was considered. They found that a tag-based discriminate altruism can emerge through the coevolutionary process, but only if there is a spatial structure (or, viscosity) (see also [31]). Throughout this paper, the population is assumed to be well-mixed and no spatial structure is considered. Since spatial structure can favour the evolution of cooperation by promoting non-random interactions [36,37], future study may find that cultural variation plays an even greater role in facilitating the evolution of discriminate sociality in structured populations. Efferson et al. [38] showed that cultural groups can emerge endogenously among subjects in laboratory while initially meaningless arbitrary symbols play a role as cultural markers, becoming associated with either of the groups. Each subject of the experiment chose a behaviour (A or B) and an arbitrary symbol (circle or triangle) and played a coordination game with another subject (in a coordination game, the players gain the maximum payoff when they choose the same behaviour). Though behaviours of other subjects were unknown before interaction, each subject could choose her partner on the basis of the symbols assigned to them. As sessions proceeded, statistical association between behaviour and symbol built up and the subjects showed a preference for partners having the same symbol. Efferson et al. [38] interpreted this preference as a form of ingroup favouritism in the choice of partners, which is slightly different from ingroup favouritism in the choice of behaviours as considered in the present study. Effects of ingroup favouritism in the choice of partners on the maintenance of cultural diversity have been examined theoretically by McElreath et al. [39], also assuming a coordination game. Castro & Toro [40,41] analysed mathematical models to study the evolution of ingroup favouritism in the choice of partners based on arbitrary tags.

(b) The Middle/Upper Palaeolithic transition If the mechanism proposed in this paper has indeed played a role in the evolution of human discriminate sociality, when and where did it take place? Let me finish with an attempt to situate the model in the history of human evolution. Various lines of evidence suggest that Cro-Magnons (Homo sapiens), or early modern humans, replaced Neanderthals (Homo neanderthalensis) in Europe by 30 000 years ago (possibly with some level of hybridization; see [42,43]). It is reasonable to speculate that extinction of the Neanderthals may have been caused by difference in behaviour between the two species. Behavioural difference is partially inferred from difference in artefacts: artefacts created by Neanderthals, which are usually assigned to Mousterian Industry or Middle Palaeolithic, are rather uniform through time Phil. Trans. R. Soc. B (2011)

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and space, while Cro-Magnons manufactured a much wider variety of artefacts using specialized techniques (Aurignacian Industry or Upper Palaeolithic). Furthermore, there is little unequivocal evidence of art and personal ornaments among Mousterian people [44,45], whereas thousands have been known from Upper Palaeolithic. On the one hand, the Middle/Upper Palaeolithic transition may be attributable to a new cognitive (neurological) capability acquired by modern humans around 50 000 years ago, not long before the beginning of Upper Palaeolithic [45]. An obstacle to this hypothesis is Chaˆtelperronian Industry, which is associated with Neanderthals in a certain area of Western Europe, but includes such artefacts as bone tools and personal ornaments exhibiting Upper Palaeolithic characteristics [46]. Chaˆtelperronian Industry indicates that the Neanderthals were cognitively capable of creating those artefacts at least by imitating Aurignacian people. Moreover, the hypothesis does not explain the presence of art and ornamentation in African Middle Stone Age about 75 000 years ago [47–49] (see [50]). Alternatively, on the other hand, the cognitive capability may have existed both in early modern humans and the Neanderthals, though it was fully manifested only in early modern humans and a small minority of the Neanderthals. Proponents of this view regard the Middle/Upper Palaeolithic transition as having been stimulated by social and demographic changes [44,51]. The present study demonstrates the logical coherence of a third possibility: the Neanderthals and early modern humans alike were equipped with the cognitive capability required to produce art and personal ornamentation, possibly as a part of more general cognitive adaptation, while early modern humans were far more highly motivated to use the capability for creating those artefacts. My suggestion is that the enhanced level of motivation might have been due to a discriminate sociality that emerged through a gene – culture coevolutionary process as proposed above in Homo sapiens after their appearance in Africa. To put it in another way, while the Neanderthals were not concerned much about their personal or group identity, the Cro-Magnons were innately sensitive about cultural variation among individuals and as a result more motivated to display their social identity. According to this view, the Neanderthals could have created art and ornaments if motivated exogenously, perhaps through contact with early modern humans. It also explains why anatomically modern humans did not exhibit fully modern behaviour until the beginning of Upper Palaeolithic, if the gene– culture coevolution can be regarded as a gradual process. My hypothesis is partially in line with the claim that genetic difference between the Neanderthals and early modern humans played a role in the Middle/Upper Palaeolithic transition (e.g. [45]), and partially with the argument that art and ornaments became commonplace in Upper Palaeolithic because of the increasing importance of displaying individual or personal identity (e.g. [52]). I thank K. Aoki, J. R. Kendal, O. Kondo, J. Odling-Smee, J. Tehrani and two reviewers for their comments.

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APPENDIX A. THE POPULATION DYNAMICS Let uA0, uA1, uB0 and uB1 denote the frequencies (uA0 þ uA1 þ uB0 þ uB1 ¼ 1) of the four phenogenotypes, A0, A1, B0 and B1, respectively, in the parental generation after horizontal transmission. Also, let WA0, WA1, WB0 and WB1 represent the fitness of the four phenogenotypes (table 1). The frequencies of the phenogenotypes in the offspring generation after vertical transmission, u0A0 , u0A1 , u0B0 and u0B1 , are given by W u0A0 ¼ WA0 uA0 þ ð1 vA ÞWA1 uA1 ;

ðA 1Þ

W u0A1 W u0B0

¼ vA WA1 uA1 ;

ðA 2Þ

¼ WB0 uB0 þ ð1 vB ÞWB1 uB1

ðA 3Þ

and

W u0B1

ðA 4Þ

¼ vB WB1 uB1 ;

where vA and vB represent the rates of vertical transmission for strategies A and B, respectively (0 , vA , 1, 0 , vB , 1), and W ¼ WA0uA0 þ WA1uA1 þ WB0uB0 þ WB1uB1 is the mean fitness. The frequencies of the phenogenotypes in the offspring generation after horizontal transmission, u00A1 , u00A1 , u00B0 and u00B1 , are given by u00A0 ¼ ½1 hA ðu0A1 þ u0B1 Þu0A0 ;

ðA 5Þ

u00A1 u00B0

ðA 6Þ

u0A1

¼ þ hA ðu0A1 þ u0B1 Þu0A0 ; ¼ ½1 hB ðu0A1 þ u0B1 Þu0B0 and u00B1 ¼ u0B1 þ hB ðu0A1 þ u0B1 Þu0B0 ;

ðA 7Þ ðA 8Þ

where hA and hB are the rates of horizontal transmission for strategies A and B, respectively (0 , hA , 1, 0 , hB , 1).

Thirdly, when a CDD interacts with another CDD, the expected payoff again depends on the cultural trait; for example, the expected payoff to a CDD without the cultural trait when interacting with a CDD with the trait is ð1 f01 Þð1 f10 Þb þ f01 ð1 f10 Þ2b þ f01 f10 ðb cÞ:

Other expressions in table 4 are obtained similarly.

APPENDIX C. LOCAL STABILITY OF A POPULATION FIXED WITH STRATEGY A We ask whether a population fixed with strategy A can be invaded by strategy B. Suppose that the population dynamics have an equilibrium state given by (uA0, uA1, uB0, uB1) ¼ (1 2 ^y, ^y, 0, 0), where 0 ^y 1. An equilibrium state is regarded as locally stable if and only if the Jacobian matrix around that state has the leading eigenvalue that is larger than 21 and smaller than 1. One of the eigenvalues of the 3 3 Jacobian matrix obtained from (A 1)– (A 8) is ! ^ A1 W l ¼ vA Fð^yÞ^y þ ^ W " !# ^ A1 W ; ðC 1Þ 1 þ hA 1 2vA ^y ^ W where F( ^y) is the partial derivative of WA1/W with respect to uA1 evaluated at the equilibrium state. Hence, jlj , 1

APPENDIX B. HOW TO CONSTRUCT TABLE 4 First, when an Assessor interacts with another Assessor, the expected payoff does not depend on the presence or absence of the cultural trait. For example, the expected payoff to an Assessor without the cultural trait when interacting with another Assessor without the trait is given by: fð1 eÞ2 2b þ ð1 eÞe½d2b ð1 dÞ2c þ eð1 eÞbg=2 þ fð1 eÞeb þ eð1 eÞ½ð1 dÞ2b d2c þ e2 2bg=2;

ðB 1Þ

which simplifies to the corresponding expression in table 4. The first term of (B 1) represents the case when the self has the greater RHP than the opponent and the second term represents the opposite case. Secondly, when an Assessor interacts with a CDD, the expected payoff depends on the cultural trait. For example, the expected payoff gained by an Assessor without the cultural trait from an interaction of the CDD with the trait is

d2cg=2: Phil. Trans. R. Soc. B (2011)

ðB 2Þ

ðC 2Þ

is a necessary condition for the equilibrium state to be locally stable. Note that eigenvalue l has the corresponding eigenvector given by (uA1, uB0, uB1) ¼ (1, 0, 0), which means that if the inequality in (C 2) is reversed, the rare cultural trait spreads in the population in the absence of individuals with strategy B. The two other eigenvalues are identical with those of the following matrix: 0 1 ^ ^ ^ ^ 1hB vA ^y WÂ1 W^B0 ð1vB Þ 1hB vA ^y WÂ1 W^B1 B W W W h iW C J¼@ A: ^ B0 ^ A1 W ^ A1 W ^ B1 W W hB vA ^y ^ ^ vB þð1vB ÞhB vA ^y ^ ^ W

W

W

W

ðC3Þ It is shown that the absolute value of the leading eigenvalue of J is smaller than unity if and only if both of the following conditions are met: ^ ^ B0 ^ A1 =W hB vA ^yW W ,1þ ^ ^ ^ A1 =W vB ½1 hB vA ^yW W ! 1 vB ; 1 ^ ^ B1 =W 1 vB W

fð1 eÞð1 f10 Þ2b þ ð1 eÞf10 ½d2b ð1 dÞ2c þ eð1 f10 Þbg=2 þ fð1 eÞð1 f10 Þb þ eð1 f10 Þ2b þ ef10 ½ð1 dÞ2b

ðB 3Þ

and

^ B1 1 W : , ^ v B W

ðC 4Þ ðC 5Þ

Taken together, the equilibrium state is locally stable if and only if (C 2), (C 4) and (C 5) are satisfied.

Culture-dependent discriminate sociality APPENDIX D. CAN CULTURE-DEPENDENT DISCRIMINATOR INVADE THE POPULATION OF ASSESSOR? There always exists an equilibrium state, E1, given by (uA0, uA1, uB0, uB1) ¼ (1, 0, 0, 0), which represents a population consisting only of Assessor without the cultural trait. From (C 2), (C 4) and (C 5), the equilibrium state is locally stable if and only if all of the following are satisfied: ð1 þ hA ÞvA , 1;

ðD 1Þ

a . f00 b

ðD 2Þ

and

vB ,

w þ b=2 þ a ; w þ b=2 þ f10 b

ðD 3Þ

where a ¼ b/2 2 ce(1 2 e) and b ¼ 3b/2 2 (b þ c)(e þ d 2 2ed). If the inequality in (D 1) is reversed, the rare cultural trait spreads in the absence of CDD. If the inequality in (D 2) is reversed, rare CDD increases in the absence of the cultural trait (since one of the eigenvalues of matrix J corresponds to the eigenvector given by (uA1, uB0, uB1) ¼ (0, 1, 0), and (D 2) specifies the condition under which the absolute value of the eigenvalue is smaller than unity (see appendix C)). If the inequality in (D 3) is reversed, CDD and the cultural trait can increase when both are rare but not absent. When the inequality in (D 1) is reversed, there exists another equilibrium state, E2, given by (uA0, uA1, uB0, uB1) ¼ (1 2 y2 , y2 , 0, 0), where y2 ¼ [(1 þ hA)vA 2 1]/(hA v2A ). Equilibrium state E2 represents a population in which everyone is CDD and some but not others have the cultural trait. Local stability of E2 is analysed for each of rules I and II assuming that the inequality in (D 1) is reversed. First, suppose that CDD follows rule I ( f00 ¼ f11 ¼ 0, f01 ¼ f10 ¼ 1). For E2 to be unstable, it is necessary that either b , a , 0 or 0 , a , b is satisfied. When b , a , 0, E2 is unstable if and only if either (3.3) or (3.4) is satisfied, where the threshold rates of vertical transmission are given as follows: vA is the smaller solution of a quadratic equation for vA, hA ðb aÞv2A ð1 þ hA ÞbvA þ b ¼ 0;

ðD 4Þ

v A is the smaller solution of another quadratic equation, hA av2A ð1 þ hA ÞbvA þ b ¼ 0;

ðD 5Þ

and vB is given by vB ¼

w þ b=2 þ a w þ b=2 þ ð1 y2 Þb hB vA y2 ð1 y2 Þb a 1þ : 1 hB vA y2 y2 b a

ðD 6Þ

When 0 , a , b, equilibrium state E2 is unstable if and only if either (3.8) or (3.9) is satisfied. Second, when rule II ( f01 ¼ f11 ¼ 0, f00 ¼ f10 ¼ 1) is assumed, either b , a , 0 or 0 , a , b is necessary for E2 to be unstable. When b , a , 0, E2 is unstable if and only if (3.10) is met. When 0 , a , b, it is unstable if and only if (3.11) holds. Phil. Trans. R. Soc. B (2011)

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APPENDIX E. CAN ASSESSOR INVADE THE POPULATION OF CULTURE-DEPENDENT DISCRIMINATOR? There always exists an equilibrium state, E3, given by (uA0, uA1, uB0, uB1) ¼ (0, 0, 1, 0), representing a population fixed with CDD without the cultural trait. The equilibrium state is locally stable if and only if all of the following are satisfied: ð1 þ hB ÞvB ,

2 w þ b cf00 ; w þ bð1 f01 þ f10 Þ cf01 f10

b cf00 ð1 f00 Þ , f00 b 2 2 w þ b cf00 and vA , ; w þ 3b=2 f01 g

ðE 1Þ ðE 2Þ ðE 3Þ

where l ¼ b/2 þ (b þ c)(1 2 e 2 d þ 2ed). If the inequality in (E 1) is reversed, the rare cultural trait spreads in the absence of Assessor. If the inequality in (E 2) is reversed, Assessor can invade the population without the cultural trait. If the inequality in (E 3) is reversed, Assessor and the cultural trait can increase when both are rare but not absent. Depending on parameter values, there may be other equilibrium states in which Assessor is absent. Such equilibrium states exist if the following equation for uB1 has one or more solutions satisfying 0 , uB1 , 1: WB1 WB1 1 þ hB 1 vB uB1 1 ¼ 0; GðuB1 Þ ¼ vB W W ðE 4Þ where WB1 ¼ w þ b[1 2 uB0( f01 2 f10)] 2 c(uB0 f01 f10 þ 2 2 ) and W ¼ w þ b 2 c(u2B0 f00 þ 2uB0uB1 f01 f10 þ uB1 f11 2 ). Local stability of these equilibrium states are anau2B1 f11 lysed numerically by using (C 2), (C 4) and (C 5), with subscripts A and B interchanged.

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Research

The influence of social niche on cultural niche construction: modelling changes in belief about marriage form in Taiwan Mikhail Lipatov2,3,4,†, Melissa J. Brown1,3,*,† and Marcus W. Feldman2,4 1

Department of Anthropology, 2Department of Biology, 3Institute for Research in the Social Sciences, and 4Morrison Institute for Population and Resource Studies, Stanford University, Stanford, CA 94305, USA

With introduction of social niche effects into a model of cultural change, the frequency of a practice cannot predict the frequency of its underlying belief. The combination of a general model with empirical data from a specific case illustrates the importance of collaboration between modellers and field researchers, and identifies the type of quantitative data necessary for analysing case studies. Demographic data from colonial-period household registers in Taiwan document a shift in marriage form within 40 years, from a mixture of uxorilocal marriages and virilocal marriages to the latter’s dominance. Ethnographic data indicate marriage-related beliefs, costs, ethnic effects and colonial policies as well as the importance of horizontal cultural transmission. We present a formal model for the effects of moral beliefs about marriage and a population economic index on the decline of uxorilocal marriage. We integrate empirical marriage rates and an estimated economic index to produce five projections of the historical frequencies of one belief. These projections demonstrate how economic development may affect a cultural niche. They also indicate the need for future research on the relationship between wealth and cultural variability, the motivational force of cultural versus social factors, and the process of cultural niche construction. Keywords: horizontal cultural transmission; economic index; uxorilocal marriage; virilocal marriage; colonial household registers; cultural change

1. INTRODUCTION Humans are inextricably social and cultural animals. We are, each of us, born into a particular society with its specific structure and a particular culture with its specific languages and beliefs. For humans, then, society and culture constitute niches at least as much as the ecological environment. Other scholars of this issue discuss ways in which aspects of human societies and cultures have constructed the ecological niches in which people live. Here, we view the theory of niche construction within the realm of human society and culture in order to explore how these niches—which can powerfully influence the ecological environment and genetic evolution (e.g. [1,2])—are themselves constructed and passed on by humans who live within them. We view the social niche of a population as the sum of all the social selection pressures to which the population is exposed and the cultural niche of a population as the sum of all the cultural selection pressures to which the population is exposed (modifying the definition of an ecological niche from Odling-Smee et al. [1]; see also

Ihara & Feldman [3] for a mathematical formulation of cultural niche construction). Social selection pressures derive from the fact that all human societies have an organization, or order, constituted by a series of overlapping, hierarchical role-structures [4–6] (see also Runciman [7] for a different but compatible view of social selection). These structures are defined by expectations of behaviour for role holders, expectations that are socially negotiated in a process we consider social selection [8]. Cultural selection pressures derive from the fact that human culture is a series of overlapping, nested sets of meaningful ideas [9] often referred to as symbolic or meaning systems. Note that ‘meaningful ideas’ is used as an anthropological technical term, referring to information that is shared, abstract, public (i.e. external to individuals) and either believed as truth by some percentage of the referent population or else closely associated with other ideas so believed [8,10] (see also [9,11–13]). Such ideas are expressed and learned behaviourally, yet internalized in individual minds [14,15]. Under cultural selection, ideas that an individual already has internalized influence his/her broadcasting, reception or internalization of subsequent ideas to which she/he is exposed [8] (see also [16–21]). Thus, human social niche construction occurs when social precedents feedback to change shared expectations of roles [8]. Human cultural niche construction occurs when belief

*Author for correspondence ([email protected]). † M.J.B. and M.L. contributed equally to this manuscript. One contribution of 13 to a Theme Issue ‘Human niche construction’.

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or disbelief influences whether particular ideas are accepted as meaningful (believed or associated with belief ) in a population [8] (see also [1,3,22]). We focus on the interaction of society (role-structures) and culture (ideas) and the potential for their distinct dynamics to reshape the cultural niche (see also [3,8,23 – 25]). Demographic and ethnographic data document a change in marriage practices in Taiwan during the early twentieth century, from a plurality of ways to select a mate to dominance of one form. Here, we present a formal model exploring the interaction of cultural ideas (represented by moral beliefs about marriage) and social structure (represented by an ability to pay brideprice), the phenotypic expression of this interaction in mate preferences (as represented by the actual marriage form practised), and the niche-constructing feedback to the content of the population ideational pool or cultural niche. Unlike Lansing & Fox’s discussion [26] of the complex set of ideas in the Balinese water temples’ ritual calendar, we focus on two specific cultural ideas in order to explore some of the nuanced interactions between cultural ideas and social structure.

2. DATA ON MARRIAGE CHANGE IN TAIWAN, 1906 – 1945 (a) Marriage forms In rural Danei Township and Jibeishua village (in Dongshan Township) in Taiwan’s southwestern county of Tainan (figure 1), frequencies of marriage forms changed between 1906 and 1945, both among the ethnic Han (Chinese) majority and the plains Aborigine (Austronesian) minority [27 – 29]. Although Han in Taiwan practised a range of marriage forms [27,30,31], there were primarily two forms of marriage in Danei and Jibeishua at the beginning of the twentieth , lit. century [28,32]. Virilocal ‘major’ marriage ( for a woman to leave her natal household as a man’s wife)—where a young woman, after puberty, was transferred from her father’s household to her husband’s— was the Han cultural ideal, and it was common among both Han and plains Aborigines [27– 29]. The cost of such a marriage—brideprice, feasting and fees for the go-between—was significant for the groom’s family and was not offset by the dowry provided by the bride’s family. The brideprice alone was often equivalent to a year’s income for a farm family and could require 10– 15 years of saving to accumulate [30]. (Note: In China and Taiwan studies, unlike African studies, ‘brideprice’ is the standard and , not ‘bridewealth’, appropriate translation for because the cash and gifts included in brideprice were culturally viewed as buying a woman and all rights to her labour and children [30,33– 35]. Additionally, virilocal major marriages and uxorilocal marriages are generally referred to as ‘marriage forms’ rather than just post-marital residence because the terms encompass related rituals and jural rights and duties as well as residence; moreover, they are frequently compared with other forms of marriage which are also virilocal). or , lit. bringing Uxorilocal marriage ( in a son-in-law)—where an adult man moved into his wife’s household—was a persistent minority of Phil. Trans. R. Soc. B (2011)

marriages, of variable frequency [27,28,30,32]. Uxorilocal marriage required no brideprice, feasting, fees or dowry, for Han or plains Aborigines. Moreover, the concept of uxorilocal marriage in Taiwan included a range of practices that elsewhere in the world would be treated as distinct marriage forms. According to Wolf & Huang [30], the most common version of uxorilocal marriage among the Han was where a sonin-law would agree to give his father-in-law’s surname to one or more of his sons, and only those boys would have rights of property inheritance of their maternal grandfather’s property. Ethnographic evidence suggests that the most common form of uxorilocal marriage among plains Aborigines in the villages of Toushe (in Danei Township), Jibeishua (in Dongshan Township) and Longtian (in Guantian City) was essentially a form of brideservice, where no surname changes would be made, no property inheritance rights would be granted, and after 10 years or so of working for his father-in-law, a son-in-law would move his wife and children out and establish his own household [28]. Such variation fits within a larger Han acceptance of a wide range of marital forms. Unlike Christian Europe, where there was a largely uniform marriage type (serial monogamy) but wide variation in form of inheritance, in Han China and Han diasporas, there was a largely uniform inheritance form (all brothers inherited equally) but families could contract virtually any form of marriage mutually agreed upon [28,30,33,36– 38]. One of the best predictors of uxorilocal marriage was sibling composition [30,39– 41]. Han women who reached age 15 with no brothers or only very young brothers living in their household were much more likely to marry uxorilocally than women with at least one living older brother. Generally, these women’s natal families had at least minimal property or tenancy rights, which could be used to entice a Han man into an uxorilocal marriage. These trends also appear to hold for plains Aborigines, but plains Aborigine women with older living brothers might also marry uxorilocally [27– 29]. Poverty affected mortality rates, and thus sibling composition, but so too did stochastic effects. Elderly women Brown interviewed frequently reported having lost a brother or a husband when an oxcart flipped over on him. Whether such accidents left a household without male labour was a stochastic effect, for it depended on the existing sibling composition as determined by the prior history of the household. Pandemics, war and natural disasters also yielded stochastic effects. For Han men, conditions of poverty, which meant they could not pay a brideprice, caused, for example, by having five or more living brothers, or one or more parents deceased by the time a man reached marriageable age, best predicted whether he would marry uxorilocally. Among plains Aborigine men, the correlation with poverty appears to be less strong. (Note: Wolf used quantitative data to assess these correlations for a northern Taiwanese Han township; Brown used qualitative data from in-depth interviews in three southwestern plains Aborigines villages, discussed further below.) Han viewed uxorilocal marriage as shameful; thus Han men who resorted to this form of marriage were



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often viewed with suspicion by their in-laws and the local community [29,30,40]. By contrast, because uxorilocal marriage among plains Aborigines in the early twentieth century has generally been viewed as a holdover from seventeenth century matriliny (e.g. [27,28,42]), its ‘traditional status’ for Aborigines has led to the expectation ‘that the factors that weaken uxorilocal marriage among the Han, especially the denigrated status of the in-marrying son-in-law and even the lack of trust in the relations of son-in-law to parents-in-law would be diminished among the plains [A]borigines’ [29]. Further expectations that divorce rates for the uxorilocally married would be lower among plains Aborigines than among Han were not realized [29]. However, late nineteenth century European missionary reports that marriage was lax among plains Aborigines and divorce common— presumably also derived from matriliny—preclude the conclusion that uxorilocal marriages were not ‘culturally honoured’ [29]. Ethnographic research in the plains Aborigine villages of Toushe (Danei Township), Jibeishua Phil. Trans. R. Soc. B (2011)

(Dongshan Township) and Longtian (Guantian City), all in Tainan County, suggests that plains Aborigine residents there may have viewed uxorilocal marriage more neutrally than the Han. Some 79 elderly villagers (surviving, mentally capable villagers, aged 60 and older, interviewed in 1991 – 1992) who had been considered plains Aborigines in their youth reported on a total of 85 marriages in their parents’ and grandparents’ generation (which occurred roughly 1900 – 1920): 40 per cent of the 18 Longtian marriages were uxorilocal, 44 per cent of the 44 Jibeishua marriages and 70 per cent of the Toushe marriages [28]. These same villagers reported lower rates of uxorilocal marriage for their own generation (which occurred roughly 1925 – 1940): 35 per cent of the 20 Longtian marriages were uxorilocal, 31 per cent of the 35 Jibeishua marriages and 23 per cent of the 44 Toushe marriages [28]. Brown found that these ‘plains Aborigine’ villagers demonstrated no shame or reluctance in speaking of their own, their parents’ or their grandparents’ uxorilocal marriages. Nor did their reports describe maltreatment of uxorilocally married men within their community. The only


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uxorilocally married Han man who spoke ill of his plains Aborigine in-laws (who did not give him any property) confessed to not having honoured the terms of the marriage agreement by refusing to give any of his sons his father-in-law’s surname. Given the sharp contrast of shame, reluctance and reports of discrimination about uxorilocal marriages in the ethnographic interviews in Han areas of Taiwan and China by Brown (during field research in 1991– 1992, 1994, 1996, 2002 and 2009) and other anthropologists (e.g. [40]), the consistently neutral tenor of these responses provides strong, qualitative evidence that, in the early twentieth century, uxorilocal marriages did not hold the same stigma for plains Aborigines in these villages as they did for Han. (b) Ethnic relations The Hoklo variety of Han were the ethnic majority of Taiwan and Danei Township, but plains Aborigines constituted a numerical majority of Toushe village (in Danei Township) and Jibeishua village (in nearby Dongshan township) [28,32]. By the beginning of Japanese colonial rule (1895), ethnic relations between Han and plains Aborigines were peaceful, and plains Aborigines had adopted (Hoklo) Han language and many Han customs [28]. Plains Aborigines were stigmatized and identified primarily because they did not bind their daughters’ feet, in contrast to the Han who lived in Danei and Jibeishua. The ethnic border also served as a marital border. Some Han and plains Aborigines did marry, but such marriages were mostly regarded as shameful— poor Han men marrying uxorilocally to plains Aborigine women, or poor Han widows remarrying virilocally to plains Aborigine men. According to one elderly Jibeishua man, interviewed in 1992, The women [of his parents’ and grandparents’ generation] were all fierce. The men of surrounding villages [who were Han] did not want to marry them; they [the Han men] called them [Jibeishua women] hoan-a-pho [savage biddies], so the [Jibeishua] village men had to marry them [28].

In other words, Han would not arrange virilocal marriages for their sons with women stigmatized as ‘savages’. Similarly, Han would generally not marry their daughters to plains Aborigine men as first-time brides (i.e. young women marrying for the first time). (Note that multiple marriages occurred via the practice of women remarrying following widowhood or divorce, which was common among both Han and plains Aborigines despite Han disapprobation (see [29,30]). Polygyny was accepted but relatively rare in China and Taiwan, as documented by the low frequency of concubine marriages in our database; see also [43].) Plains Aborigines were poorer on average than Han in Tainan County [28,44]. However, plains Aborigines were economically better off in Jibeishua than Danei, owing to agricultural conditions. Danei was partly rich flood plains with paddy agriculture, dominated by Han, and partly foothills with limited irrigation, where most of the plains Aborigine minority lived. Jibeishua was on the Jianan plain, surrounded by paddy fields. Phil. Trans. R. Soc. B (2011)

(c) Economic development The Japanese colonial government (which ruled Taiwan 1895 –1945) invested heavily in developing Taiwan between 1895 and 1930 [28,45] (see also [46,47]), constructing roads, bridges, a railroad system, hospitals, schools, sewage systems, dams, factories, sugar mills and more. Irrigation systems expanded the number of rice crops possible per year; in Jibeishua after 1925, when the Jianan irrigation system was in place, people could plant three rice crops per year. Public health measures effectively controlled plague, malaria and tuberculosis, reducing mortality rates across the board [48,49]. Although universal compulsory education was never achieved, most people, even in rural areas, had at least 2 years of primary education in Japanese. Many Taiwanese had the opportunity to attend middle school, making them suitable for entry-level employment in Japanese-run factories, businesses, government offices and banks. This economic and educational development resulted in non-elite Taiwanese (both Han and plains Aborigines) having more money. Thus, poor men were increasingly able to accumulate sufficient cash to pay a brideprice. Such development produced fundamental changes in Taiwan’s social niche. As defined above, a social niche is the sum of all social selection pressures, and social selection is the social negotiation process over expectations in the behaviour of role holders in hierarchically organized and networked role-structures. Economic development created new roles and new structures, for example, in factories, railroad systems and public health organizations. It also allowed many changes in continuing role-structures, such as the kinship system (for which marriage is an important means of recruitment). For example, Wolf [39] has documented quantitatively that the ‘minor’ form of virilocal marriage (where a family would adopt a young girl and raise her to be the wife of one of their sons) was common among Han in northern Taiwan at the beginning of the Japanese period but declined in frequency by 1925. Wolf uses qualitative, ethnographic evidence to attribute this decline to the ability of young people to buy themselves out of such marriages owing to the increased economic opportunities that came with colonial development (cf. Lim case study in Brown [45]). Here, young people used the resources available from modifications in the social niche to renegotiate the expected behaviour of sons and adopted daughtersin-law to such an extreme that they actually did away with the latter role entirely. Also related to economic development, the Japanese colonial government, beginning in 1915, enforced a ban on the practice of footbinding. Elderly Han interviewed in 1991 – 1992 in Danei and Dongshan townships reported that Japanese police who supervised the unbinding of their mother’s (or in one woman’s case, her own feet) said the unbinding was for women to be able to work in the paddy fields. The footbinding ban was intended to expand female participation in agricultural labour, but it also unintentionally removed the ethnic boundary between plains Aborigines and Han and drove the subsequent assimilation of plains Aborigines in Toushe and


Jibeishua to a Han identity [28,45]. This removal shifted marriage patterns in Danei and Jibeishua by increasing the rates at which Han allowed their daughters to marry plains Aborigine men (as first-time brides) and at which Han brought in plains Aborigine brides for their sons [28]. In other words, the footbinding ban coincides with an overall decrease in uxorilocal marriage rates, both for plains Aborigines in relation to Han and for everyone overall (figure 2). The resulting change in ethnic identity also had consequences for villagers’ customs (practices) and cultural ideas [23,28,50]. By 1991, people practised customs largely indistinguishable from neighbouring villages that had always been considered Han (except for one part of their religious practices). Toushe and Jibeishua villagers whose identities changed from plains Aborigine to Hoklo Han also believed many more Han cultural ideas over time, although a lag in the adoption of ideas was still apparent [28,50]. Such evidence that the spread of cultural ideas in a population can follow the spread of an associated practice suggests that behaviour itself (phenotype) may be an important factor in cultural niche construction (i.e. changes in whether particular ideas are accepted as meaningful; cf. [8,23]). The frequency of cultural ideas in the early-twentiethcentury plains Aborigine population in these villages is unknown. The only evidence available is from retrospective ethnographic interviews from a surviving sample (e.g. [28]) or occasional historical claims, often by Western missionaries, about the cultural ideas of an entire village, county or even ethnic group (e.g. [29,51–53]). There is debate among Taiwan scholars about the degree to which southwestern plains Aborigines had adopted Han cultural ideas by 1900 (e.g. [28,29,42,50,54,55]).

(d) Demographic data To monitor Taiwan’s population, the colonial government developed a household registration system, in which every person had to register with the police as a member of one, and only one, household [30]. Information registered included name, age, sex, relation to the head of the household, marital status, and, in the early part of the Japanese period, ‘class,’ ‘race’ as inherited from one’s biological father and (for females) whether feet were bound. Japanese-period registers for many localities have been computerized and archived. Some information in the original registers is not available in the public-use database, affecting some potential analyses. For example, all names have been replaced by identification numbers, which means that quantitative assessment of surname changes is not possible. Each locality database contains the above information for every single person alive between 1906 and 1945 who resided in that locality for at least 1 day. In other words, the people represented in the database for each locality (village, township, small city and urban neighbourhood) are the entire population for that 40 year period, not merely a sample. The entire population, so defined, includes migrant households as well as long-term residents. Taiwan’s Phil. Trans. R. Soc. B (2011)

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Figure 2. Proportion of uxorilocal marriages for Aborigine and Han women from Danei and Aborigine women from Jibeishua, by 10 year marriage cohorts. Green bars, Jibeishua Aborigines; violet bars, Toushe Aborigines; blue bars, Danei Aborigines; red bars, Danei Han. Note: Toushe Aborigines are a subset of the Danei Aborigine population.

population during the colonial period was extremely mobile, but the Japanese colonial government took measures to reduce the impact of such mobility on the household registers. Most importantly for our purposes, household registers reflect Taiwanese concepts of family ( ), not merely residence. Individuals could be registered in their family’s household but physically resident elsewhere. If individuals reported that they would be gone from the locality for a period of time, for example, for work, the local police merely added a pasted-on rice-paper strip to the comments section of their permanent household register indicating the sojourn. (They also had to register with the police in the locality to which they were going, but registered as sojourners, not as permanent residents.) Any marriages or other events that occurred during this period would be recorded on the permanent household register page in their home locality. There were relatively few sojourners in Danei and Jibeshua, since these localities include no major urban centres. In our analyses, we have excluded sojourners from consideration. Thus, only migrations that included the entire household are included in our effective populations. The Danei and Jibeishua databases (recording information on 21 151 and 3268 people, respectively) provide the following information for every marriage that occurred between 1906 and 1945: date, form (uxorilocal or virilocal), first- or high-order marriage (indicating serial remarriage), community address of post-marital household (which allows us to identify residence in Toushe village within the larger Danei Township database). The databases also provide detailed information on spouses including, in many cases, their natal households. In our analyses, we only examine first marriages for two reasons. First, we want to be able to compare our results to previously published studies of the Taiwan household registers, which focus on first marriages (e.g. [27,29– 31,38,39,40,56]). Second, remarriages occurred with different social expectations, under different economic conditions, and with different cultural views from first marriages. Moreover, first marriage form does not necessarily predict remarriage


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form. Wolf & Huang [30] suggest that remarriages have a higher frequency of uxorilocal marriages than first marriages. For example, a virilocally married woman whose husband died young (especially if he left young sons and no brothers) was highly likely to marry uxorilocally, either arranged by her parentsin-law or herself, since there was likely to be both property and need of adult male labour. We also focused on uxorilocal and virilocal major forms of marriage because other forms of marriage were relatively rare in these particular sites. For local women married from their natal homes in first marriages, occurring any time between 1906 and 1945, there were 2003 virilocal major marriages in all Danei Township, 374 uxorilocal marriages, 166 minor marriages (only nine of which included plains Aborigines) and 27 concubine marriages. In Jibeishua village, there were 342 virilocal major marriages, 99 uxorilocal marriages, 17 minor marriages (eight of which included plains Aborigines) and six concubine marriages. (Note: Concubine marriages were always to virilocally married men). Here, we present uxorilocal marriage rates for women from the township of Danei and the villages of Toushe and Jibeishua between 1906 and 1945. We define the uxorilocal marriage rate, U, as the ratio u/(u þ v), where u is the number of first uxorilocal marriages among all the women from a particular village or township during a particular period of time, and v is the corresponding number of first virilocal (major) marriages. These data count women who were living in households in Danei or Jibeishua at the time when the woman either left her household to marry (virilocally) or had a husband brought in for her. Thus, we are counting the marriages of women from that locality at the time of marriage. Those whose first marriages contributed to the Toushe rate are women who were living in households in Toushe on their 15th birthday, generally the earliest age at which first marriages occurred (e.g. [30]), although plains Aborigine women tended to marry at later ages than Han women [29]. (Note: This qualification reduces the number of women in migrant households included in the Toushe figures.) We calculate the marriage frequencies in terms of marital cohorts (e.g. figure 2) because this calculation captures period effects—larger historical factors that affected all marriages at a particular time, such as the 1915 footbinding ban. Note that no error range is indicated because the data are not a sample; rather, they represent the entire population of specified women. The first cohort shows the plains Aborigines with a clearly higher rate of uxorilocal marriage than Han. We do not know how these frequencies of the practice of uxorilocal marriage relate to cultural ideas. There follow two cohorts where the Aborigine rates drop and approach the Han rates, and finally a cohort that shows no significant difference between the Han and Aborigine rates. (A two-sample test of equality of proportions with continuity correction indicated that the Danei Aborigine and the Danei Han uxorilocal marriage proportions in the fourth cohort are the same.) There is a more-or-less steady decline in uxorilocal marriage in all groups over the colonial Phil. Trans. R. Soc. B (2011)

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Figure 3. Rates of uxorilocal marriage for all women from Danei, by 10 year marriage cohorts.

period to a low of about 5 per cent in the final cohort, but the decline in the Aborigine rates from the first to second cohort is strongest. We primarily use the data in figure 3 from Danei only, which combine the rates for Han and plains Aborigine women, to inform construction of a basic model of declining uxorilocal marriage rates, because this combination simplifies the mathematical calculations. (The marital-cohort rates in figure 3 can be understood as weighted averages of the Danei Han and Danei Aborigine rates presented in figure 2.) However, in the analysis, we do use data on Danei Han only (UH1) from figure 2 to calculate the historical projections of changing beliefs.

3. MATHEMATICAL MODEL Based on the qualitative and quantitative evidence summarized above, we identified the following key factors that might have affected uxorilocal marriage rates in Taiwan: a set of cultural ideas about the shamefulness of uxorilocal marriage (including association with son preferences), economic conditions affecting the cost of a virilocal marriage (especially the brideprice), and sibling composition (which is affected by both economic and stochastic effects on mortality rates). As discussed above, it is unknown—and unlikely to ever be known—what the frequency of cultural ideas regarding marriage was at the beginning of the Japanese colonial period in Taiwan. It is, however, clear that economic and public health conditions improved dramatically over the course of the colonial period, resulting in greater wealth in the population and lower mortality rates. Given the importance of poverty and sibling composition in predicting the probability of uxorilocal marriages (e.g. [27,30]), and given evidence that practices can and do change before cultural ideas [28,50], the influence of cultural niche construction is not clear. In other words, it is not clear whether or how cultural ideas about marriage form must have changed before, during or even after the decline in uxorilocal marriage rates. Thus, we turn to a mathematical model to indicate the possible dynamics of cultural ideas, given the known changes in the social niche. In constructing the model, we allow for direct influence of cultural ideas and a population economic index. We also include an indirect representation of stochastic influences on sibling composition.


Belief about marriage in Taiwan (a) Transmission of cultural ideas We suppose that every person in the locality has a cultural idea about the morality of virilocal and uxorilocal marriages, which affects the relative desirability of each form. Each person either has an idea (s1) that uxorilocal marriages are immoral and thus undesirable or an idea (s0) that uxorilocal and virilocal marriages are equally moral and desirable. In other words, people with s0 are neutral; they have no clear preference between the two forms of marriage. An interesting consequence of the empirically based conceptualization of these cultural ideas as a preference and neutral idea is that under certain conditions, discussed below in ‘calculating the uxorilocal marriage rate’, s1 is dominant over s0. (For any individual, s is assumed to be independent of monetary wealth.) We define x as the proportion of people who have s ¼ s0 at a given time in a particular population, and 12x is the proportion of people with s ¼ s1. Our model includes horizontal transmission of s [16]. We allow for the possibility that the empirical decline in uxorilocal marriage was driven by a change in beliefs. The rapidity of this decline (less than a generation), especially for plains Aborigines, means that cultural influence must have come horizontally rather than vertically. Moreover, once marriage form was already changing, individuals may well have been influenced in their opinion of marriage forms practised by their own and adjacent cohorts. Consequently, our model assumes that vertical transmission does not produce a change in the value of x between the parental and offspring generations (it is unbiased) and also that whether a person believes uxorilocal marriages are immoral (s1) or neutral (s0) is affected by the beliefs of others within the same biological generation. (Note: The model assumes that cultural selection operates by ideas directly influencing each other, but empirically we would expect individuals’ ideas to be influenced both by the expressed ideas of their peers and observations of the outcomes (e.g. divorce) of actual marriages (phenotype) in the adjacent cohorts—siblings, cousins, neighbours and classmates.) For simplicity, we assume that both vertical and horizontal transmissions of ideas are gender-blind, so that the system quickly reaches a state where x is the same in both genders.

(b) Population economic index We introduce W, a population-level economic index. Given that colonial Taiwan was economically highly stratified, we conceptualize W not as wealth in general but as the proportion of individuals in the population that had sufficient wealth to pay a brideprice. This view of W makes the model slightly more realistic because the range of variation in brideprice was considerably less than the range of variation in overall wealth in the population [30]. W ranges between 0 and 1. When W ¼ 0, poverty is so great that no one can afford to pay brideprice and everyone marries uxorilocally. When W ¼ 1, societal wealth is sufficiently high that everyone has enough money to pay a brideprice and, thus, everyone can marry according to his/her cultural beliefs. Since one Phil. Trans. R. Soc. B (2011)


of the two beliefs in the model is neutral, having enough money for a brideprice will not automatically make a person with s0 marry virilocally. Taiwan’s overall wealth increased during the colonial period, so we would say that W increased. Thus, in contrast to Shennan [57], we consider an industrializing context in which access to resources increases over time and for a larger percentage of the population. We recognize that using a population-level economic index is not ideal. We use a population-level index because, first, although we do not have villageor township-wide, individual-level data on wealth, we do have reliable qualitative evidence of the population-wide increase in wealth. Second, the poor, rural character of Danei Township and Jibeishua Village suggests that the within-population variation in the ability to pay brideprice can be approximated by the proportion W. We are not assuming that the level of brideprice in this poor rural area of Taiwan would not itself increase with increasing population wealth. Rather, based on Brown’s ethnographic interviewing about the arrangement of marriage in different generations and Wolf ’s [39] ethnographic evidence discussed above about young people buying themselves out of minor marriages, we assume that, with economic development, more poor men in Danei and Jibeishua had the option of sojourning in an industrial centre and thereby accumulating the needed wealth to return to their rural homes with enough cash for a brideprice. As more men tapped into the industrializing economy outside of Danei, W, the proportion able to pay a brideprice, increased.

(c) Indirect effects on s1 The model includes a constant parameter, s, which ranges between 0 and 1, and measures the degree to which the cultural belief s1 influences a person’s marriage practice. We include this parameter in the model because empirical evidence suggests that, despite viewing uxorilocal marriage as shameful, Han arranged uxorilocal marriages for their daughters if they had no sons. When s is low, the influence of s1 is low because the cultural idea is swamped by mitigating effects. As discussed above, sibling composition is a reliable predictor of uxorilocal marriages, and sibling composition is strongly correlated with mortality rates, which are in turn affected by both poverty and stochastic occurrences. The parameter s is intended to capture the stochastic effects on sibling composition, such as farm accidents. Stochastic events that could affect sibling composition and make s low include the 1918 influenza pandemic and colonial conscription of men as coolie labour for the Japanese Imperial Army during World War II (table 1). (Plains Aborigines and Han in Danei and Jibeishua were affected by both of these events.) Decreasing s increases the proportions of uxorilocal marriages for people with s1 (rows 2 and 3 in table 2). When s is high, the cultural idea has a strong influence on practice because mitigating effects have little significance (they are minor events, or fewer in number). For example, although hurricanes occur in Taiwan, there


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Table 1. List of variables and symbols. name

definition

s

cultural idea held by individual regarding morality of uxorilocal and virilocal marriage forms, which affects the relative desirability of each form. Takes one of two values. idea that uxorilocal and viriilocal marriages are equally moral and desirable. idea that uxorilocal marriages are immoral and undesirable. proportion of individuals in the population with s ¼ s0 at a given time. a population-level economic index. The proportion of individuals in the population having sufficient wealth to pay a brideprice. Varies between 0 and 1. degree of influence of s1 on a person’s marriage practice, due to stochastic mitigating effects. Varies between 0 and 1. total effective proportion of uxorilocal marriages in the population. U ¼ x2 ð1 12W Þ þ 2 xð1 xÞð1 12 W ½1 þ sÞ þ ð1 xÞ2 ð1 12 W ½2 ð1 sÞ2 Þ horizontal transmission. The difference between the proportion of people switching to s0 and the proportion of people switching to s1. H ; H10 2 H01. Ranges between –1 and 1.

s0 s1 x W s U H

Table 2. The probability of uxorilocal marriage by pairing type. marriage pairing type

s0 s0 2. s0 s1 3. s1 s1

1.

frequency of these marriage pairings

Pr[uxorilocal marriage]

x2 2x(1 2 x) (1 2 x)2

1 2 12 W 1 2 12 W (1 þ s) 1 2 12 W [22(1 2 s)2]

was no mention of hurricane-related deaths in ethnographic interviews. Because s is a constant—it is the same for everyone in the population—we operationalize it as saying that people are subject to the same risk of stochastic events that might affect their sibling composition. For example, people were at the same risk that a male in their household would die from the flu pandemic, would die because an oxcart laden with sugarcane would overturn or would be pressed into labour service for the army. This assumption, entailed in making s a constant, does not take into account the influence of poverty or household occupation in the probability that such events affect any particular household. We make this simplification for tractability of the model, but we also suggest that economic influences on the impacts of these events can be conceptualized as being incorporated into the economic index, W. (d) Calculating the uxorilocal marriage rate In table 2, we present the probabilities that hypothetical couples with specified cultural ideas (s0 or s1) will marry uxorilocally, assuming pairing is random with regard to s in order to keep the model as simple as possible. In row 1, we see that the frequency of couples both having s0 is x 2. Empirically, mating is probably not entirely random with regard to s. However, the ethnographic evidence discussed above of the potential effects of poverty and sibling composition on marriage forms does suggest some randomness of mating with respect to s, since poverty or sibling composition could lead people with a strong personal belief in the cultural idea s1, that uxorilocal marriages are Phil. Trans. R. Soc. B (2011)

shameful, to marry uxorilocally. If everyone in the population is wealthy enough to afford brideprice and thus to marry as they like (i.e. W ¼ 1), then the probability that a s0 s0 couple will marry uxorilocally is 12, because both individuals are neutral about marriage form. (Here, we ignore the possibility that a desire to save the brideprice for other uses might bias the frequency towards uxorilocal marriages.) Hence, from the third column of table 2, Pr[uxorilocal marriage j s0 s0] ¼ 12 12 W. In row 3 of table 2, the probability that a s1 s1 couple will nevertheless marry uxorilocally is strongly influenced by the direct effects of wealth (the proportion of people who can afford a brideprice) and the indirect effects of s on s1: Pr[uxorilocal marriage j s1 s1] ¼ 12 12 W [22(12s)2]. If the population is so poor that no one can afford a brideprice (i.e. W ¼ 0), then 100 per cent of these couples will marry uxorilocally, despite their cultural belief s1. If, at the other extreme, the population is wealthy enough that everyone can marry according to preference (i.e. W ¼ 1), then the rate at which they marry uxorilocally will be determined by s, which affects both individuals in the couple. If the effect of s1 is negligible (s ¼ 0) and if everyone can afford brideprice (W ¼ 1), uxorilocal marriage occurs randomly (Pr[uxorilocal marriage j s1 s1 and W ¼ 1 and s ¼ 0] ¼ 12). There is no influence from s1, leaving s0 as the only cultural belief, and since s0 is neutral with regard to marriage form, its influence is to push the frequency of uxorilocal marriages towards neutrality (i.e. 12). If the effect of s1 is maximized (s ¼ 1) and if everyone can afford brideprice (W ¼ 1), the probability of uxorilocal marriage is 0 because couples are able to follow their beliefs and s1 s1 couples have a strong preference against uxorilocal marriage. In row 2, the probability that a s0 s1 couple will marry uxorilocally is directly affected by societal wealth (W ) and also indirectly affected by s. If the population is so poor that no one can afford a brideprice (i.e. W ¼ 0), then 100 per cent of these couples will marry uxorilocally, despite the cultural belief s1 of one of the couple. If, at the other extreme, the population is wealthy enough that everyone can marry according to preference (i.e. W ¼ 1), then the rate at which they marry uxorilocally will be determined by


Belief about marriage in Taiwan s, which affects only one individual in the couple (since only one has s1). If the effect of s1 is negligible (s ¼ 0), then, even if everyone can afford brideprice (W ¼ 1), uxorilocal marriage occurs randomly (Pr[uxorilocal marriage j s0 s0 and W ¼ 1 and s ¼ 0] ¼ 12) because the other member of the couple is neutral with respect to marriage form. If the effect of s1 is maximized (s ¼ 1) and if everyone can afford brideprice (W ¼ 1), the probability of uxorilocal marriage is 0 because couples are able to follow their beliefs and one member of the couple has a strong preference against uxorilocal marriage while the other is neutral (hence the one with the strong belief will hold sway). In other words, s1 is dominant over s0. When s ¼ 1, the proportion of uxorilocal marriages for s1 s1 and s0 s1 couples is at its lowest value of 12W. We can use table 2 to calculate U, the total effective proportion of uxorilocal marriages in the population: U ¼ x2 1 12W þ 2xð1 xÞ 1 12W ½1 þ s ð3:1Þ þ ð1 xÞ2 1 12W ½2 ð1 sÞ2 : In other words, the number of expected uxorilocal marriages in the population is the sum, for each of the random pairings, of the frequency of the pairing multiplied by the probability that pairing will result in an uxorilocal marriage. (e) Horizontal transmission Couples in cohort t match up, marry and transmit beliefs to cohort t þ 1. We refer to couples in different cohorts, rather than generations, because the passage of time between the cohorts is generally not sufficient for biological reproduction and we have assumed that vertical transmission is unbiased. Horizontal transmission of cultural ideas can occur in a variety of ways. For example, a person with idea s0 in cohort t þ 1 can receive a broadcast expression from a person with idea s1 and change his/her idea to s1. Alternately, a person with belief s0 in cohort t þ 1 can observe a marriage as practised by a couple in cohort t and change his/her belief to s1. The probability of a change from s0 to s1 is H01, and the probability for a change from s1 to s0 is H10. Horizontal transmission influences cultural selection. It is viewed as different from the more subtle effects of cultural niche construction, where a person with idea s0 in cohort t þ 1 receives a broadcast expression from a person with idea s1 and this reception changes his/ her perception of which idea is generally believed and thus meaningful in the larger population. At the conclusion of this horizontal transmission process, the proportion of people with belief s0 is equal to xnext ¼ x þ Hxð1 xÞ;

ð3:2Þ

where H is defined as the difference between the proportion of people switching to s0 and the proportion of people switching to s1 (H ; H10 2H01). H ranges between 21 and 1. When everyone is switching to s1 (H ¼ 21), the reduction in x is the greatest, and x decreases quadratically: xnext ¼ x 2. When everyone Phil. Trans. R. Soc. B (2011)


is switching to s0 (H ¼ 1), the increase in x is the greatest: 2x2x 2.

4. SOCIAL MEDIATION OF THE EXPRESSION OF CULTURAL IDEAS At the origins of cultural evolution modelling, CavalliSforza & Feldman [58] made a simplification in the cultural transmission process for modelling facility (which did not interfere with their goal of countering Arthur Jensen’s racist claims by demonstrating that non-genetic effects could lead to the educational inequalities he cited as support, see also [59]). Although culture was defined as learned information, transmission was modelled more simply as the imitation of behaviour (the effects of parental phenotype directly on children’s phenotype). The precedent of this simplification established an expectation for modelling cultural transmission that became standard in the field (e.g. [1,16,17].) (Note: Durham [60] did not make this simplification, but because he did not mathematically model the alternative cultural transmission process he proposed, modelling practices did not shift.) This simplification implies a one-to-one correspondence between cultural information and human behaviour—in other words, an implication that once individuals acquire information they act on it. This highly unrealistic implication has contributed to wider social science scepticism of cultural evolution modelling, for anthropologists, sociologists, historians and other scholars have long recognized that individuals often have ideas in their heads that they are not interested in or able to implement in practice (cf. [10,14,18,23,60,61]; e.g. [30,39,40,62]). The general model we present here moves away from that simplification towards realism by treating cultural ideas (which are learned information stored in the mind) as analogous to genotype: mediated by external, ‘environmental’ factors—here, factors in the social niche—which affect the expression of these ideas in behaviour (phenotype). Two sample theoretical scenarios explore how the frequency of cultural ideas (x) can be environmentally mediated by societal wealth (W ) and stochastic events (s) to affect the frequency of uxorilocal marriage in practice (U ). (In §5, we apply this general model to the Danei data.) In both scenarios, x0 ¼ 0.3, s ¼ 0.7 and H ¼ 21. We set the initial frequency of s0 in the population at x0 ¼ 0.3, which is approximately the frequency of uxorilocal marriage (U) in the overall Danei population at the beginning of the Japanese period (figure 3). In other words, we assume that any disjuncture between behaviour and belief prior to cohort 1 (married between 1906 and 1915) was accounted for by s—for example, among Han who viewed uxorilocal marriage as shameful but arranged uxorilocal marriages when they had no sons—but that cultural ideas have since come into one-to-one correspondence with behaviour (cf. [28,50]). We set the initial values of belief and behaviour roughly equal to show that incorporating relatively simple economic (W ) and stochastic (s) effects yields the more realistic result of a disjuncture of belief and behaviour, even with initial values working


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against this outcome. We choose a negative value for H because, based on ethnographic research [28,50], we expect x to decrease over time, albeit after the change in practice. We set the influence of cultural belief s1 as mitigated by stochastic events, s, at an intermediate value in its empirically derived range (see appendix and table 3). W, the population economic index, differs between the two scenarios. In scenario 1, W is held constant at 0.8, a relatively wealthy level at which 80 per cent of people can afford brideprice. In scenario 2, we allow W to change over time (W ¼ 1 2 ke2at, a standard way of expressing exponential decay, where k ¼ 0.3 and a ¼ 0.5), in order to introduce more realism into the model as we know that economic development increased the wealth of Taiwanese society over the course of the colonial period. Thus, in scenario 2, W starts at 0.7 and increases exponentially up to 1, yielding an average value of W close to 0.8 (very close to the value in scenario 1). We use equations (3.1) and (3.2) to calculate the proportion of s0 in cohort t þ 1, given the proportion in cohort t. Since H 0 in both scenarios, x decreases towards 0, and U tends to the proportion of uxorilocal marriage among s1 s1 couples. (If we were to set H greater than zero, x would increase towards 1, and U would tend to the proportion of uxorilocal marriage among s0 s0 couples.) In figure 4, we plot x and U for cohorts 1 through 4 in these two theoretical scenarios. In both scenarios, x (plotted in purple) is the same (since H is the same). In scenario 1, U (plotted in green) tends to 12 12 W [22(12s)2] ¼ 0.236. In scenario 2, U (plotted in blue) tends asymptotically to 12 (12s)2 ¼ 0.045, and it spans a greater range of values than in scenario 1. Figure 4 shows the disjuncture between the frequency of a custom, in this case uxorilocal marriage (U ), and the frequency (x) of an associated belief (s0) when economic (W ) and indirect, stochastic effects (s) are introduced. In scenario 1, where U (plotted in green) and x (plotted in purple) are initially equal and W is constant at a relatively wealthy level, the divergence is clear. Moreover, the divergence is stable, since U approaches 24 per cent. In scenario 2, where W changes over time, U tracks the decline in x over time, but there is a significant time lag. Even at the (unrealistic) extreme of x ¼ 0 and W ¼ 1 in the fourth cohort, U is still over 10 per cent. Thus, marriage form frequency gives little guidance on underlying cultural beliefs about marriage (mating preferences). The results of these theoretical scenarios—which are in agreement with the observed persistence of uxorilocal marriages even in the apparent absence of supporting beliefs—suggest the presence of an additional crucial factor to the construction of human cultural niches. We identify this factor as society, in which we include political economy (cf. [7,8]).

5. PROJECTIONS OF THE CULTURAL NICHE By linking our general mathematical model (from the previous section) to the empirical data from Danei, here, we estimate the model’s parameters and produce Phil. Trans. R. Soc. B (2011)

five possible projections of the historical changes behind the decline in uxorilocal marriage rates. These projections allow us to assess the relative effects of each of the parameters (x, s and W ) on the uxorilocal marriage rate (U ) and also to explore how the cultural niche is constructed—in other words, whether and how the content of the population ideational pool changes.

(a) Linking the model and the empirical data We denote marriage cohorts in the time periods 1906– 1915, 1916– 1925, 1926 –1935 and 1936– 1945 by subscripts 1 through 4, respectively. Accordingly, U1 through U4 refer to the empirical Danei-wide uxorilocal marriage rates during these four time periods, as documented in figure 3. (Thus, U4 has the lowest value.) Similarly, UH1 refers to the uxorilocal marriage rate between 1906 and 1915 for a subsection of the Danei population: Danei Han women who lived and married outside of Toushe. (This rate is documented in figure 2 by the red column in the 1906– 1915 range.) These rates are the empirical data incorporated into the model. We denote the population economic indices in the time periods 1906– 1915, 1916– 1925, 1926 –1935 and 1936– 1945 by W1 to W4, the prevalence of s0 for the same time periods by x1 to x4, and the prevalence of s0 in 1906 – 1915 for the Danei Han outside of Toushe by xH1. We make several assumptions to simplify the model. The first two are empirically derived. First, we assume that xH1 ¼ 0, given ethnographic accounts of Han moral disapproval of uxorilocal marriage (discussed above [30,40]). (Note: we do not make assumptions about the value of x for the plains Aborigine population because of the existing debate, discussed above, over whether Aborigine cultural ideas had changed (e.g. [28,29,42,44,54,55]). Second, we assume that, for the 1936– 1945 period, any remaining s0 s0 couples marry uxorilocally about as often as they marry virilocally. In other words, given historical evidence of Taiwan’s increasing economic development over the colonial period, we assume that in time period 4, there is no economic pressure to marry in either fashion (i.e. W4 ¼ 1, the maximum possible value of the population economic index). This assumption parallels Wolf ’s [39] findings, discussed above, that young people were able to buy themselves out of minor marriages by the end of the colonial period. Furthermore, we assume that s and H remain constant between 1906 and 1945, that W is constant for each cohort (since it represents the proportion of people in the cohort who can afford brideprice) but variable between time periods, and that U and x can vary between time periods of the population. Finally, we assume that equation (3.1) holds across subsections of the population and across time, despite the evidence that before 1915 the marriage market was segregated in the township of Danei. Demographic data do show that, before 1915, uxorilocal marriage rates were different for the Aborigine and Han populations (figure 2) and each ethnic group was largely




Table 3. Five projections of the historical events behind the empirical values of U1, U2, U3, U4 and UH1 in figures 2 and 3. projection

1

2

3

4

5

s H

0.673 20.872

0.755 20.157

0.837 0.00337

0.918 0.0636

1.000 0.0691

0.799 0.857 0.925 1.000 0.195 0.195 0.196 0.196

0.791 0.851 0.921 1.000 0.233 0.244 0.256 0.268

0.788 0.849 0.920 1.000 0.284 0.298 0.313 0.328

0.833 0.865 0.926 1.000 0.150 0.0390 0.00634 0.000848

W1 W2 W3 W4 x1 x2 x3 x4

0.813 0.866 0.929 1.000 0.168 0.146 0.126 0.109

endogamous (i.e. most Han married other Han, and most Aborigines married other Aborigines; see [29]). Moreover, ethnographic reports about the social treatment of uxorilocally married men also suggest that Han individuals were more likely than Aborigine individuals to have s ¼ s1. However, in order to simplify the model, we suppose that the marriage market was random with respect to s, so that equation (3.1) holds for the Danei population between 1906 and 1915.

calculate x2 and x3: x2 ¼ x1 þ H x1 ð1 x1 Þ and x3 ¼ x2 þ H x2 ð1 x2 Þ:

Having found the range, we start with s just above the lower bound of its range, s ¼ 0.673, then compute x4, W1 and x1 (see appendix equations (A 3), (A 4), (A 5), (A 6) and (A 7)): pffiffiffiffiffiffiffiffiffi 1 2U4 ; ð5:2Þ x4 ¼ 1 s 2ð1 UH1 Þ ð5:3Þ W1 ¼ 1 þ sð2 sÞ pffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi 1 2ðððU1 1Þ=W1 Þ þ 1Þ and x1 ¼ 1 : ð5:4Þ s Now we consider how horizontal transmission (H ) affects the frequency of cultural beliefs (x). Equation (3.2) describes the transitions between cohorts 1 and 2, cohorts 2 and 3 and cohorts 3 and 4. Thus, we obtain the following identity (see appendix equation (A 10)): x4 ¼ x1 ½1 3Hð1 x1 Þ þ 3H 2 ð1 x1 Þð1 2x1 Þ H 3 ð1 x1 Þð1 9x1 9x21 Þ þ 5H 4 x1 ð1 x1 Þ2 þ H 5 x1 ð1 x1 Þ2 ð1 8x1 þ 8x21 Þ þ 2H 6 x21 ð1 2x1 Þð1 x1 Þ3 þ H 7 x31 ð1 x1 Þ4 :

ð5:5Þ

This identity allows us to calculate H, given x1 and x4, which in turn allows us to use equation (3.2) to Phil. Trans. R. Soc. B (2011)

ð5:7Þ

Once we have x2 and x3, we can use equation (3.1) to obtain W2 and W3: W2 ¼

(b) Calculating the projections In order to calculate the historical projections, we begin by obtaining the range of s. Given a particular value of s, we can calculate numerical values for H, xi and Wi that represent one projection behind the empirical values of U1, U2, U3, U4 and UH1. We find that pffiffiffiffiffiffiffiffiffi ð5:1Þ 1 2U4 , s 1:

ð5:6Þ

2ð1 U2 Þ 1 þ sð1 x2 Þð2 s½1 x2 Þ

ð5:8Þ

2ð1 U3 Þ : 1 þ sð1 x3 Þð2 s½1 x3 Þ

ð5:9Þ

and W3 ¼

In sum, given s ¼ 0.673, we have calculated numerical values for H, x1, x2, x3, x4, W1, W2 and W3, which constitute projection 1 in table 3 and figure 5. To calculate the remaining projections in table 3, we use s ¼ 1, the upper limit of the parameter’s range (in column 5), and choose the three values of s that divide its range into four equal segments. We then compute H, xi and Wi for each of these values, using the process described above for s ¼ 0.673. We incorporate the empirical data for Ui from figures 2 and 3 into the model. Using this method, equation (A 10) yields exactly one real value of H between 21 and 1 in each of the four additional projections. Results of these computations are presented as projections 2 to 5 in table 3 and figure 5.

(c) Discussion: relative effects on marriage form and cultural belief The projections in table 3 allow us to assess the relative contributions of cultural and economic factors on marriage form (phenotype) because the five projections differ in the causal factors lowering the uxorilocal marriage rate (U ). In projections 1 and 2, the drop is partly due to the increase in the proportion of people who can afford brideprice (W ) and partly due to a decrease in the prevalence (x) of the cultural idea (s0) of neutrality towards uxorilocal marriage. In projection 3, the drop is caused chiefly by an increase in W, because the prevalence of s0 does not change very much. In projections 4 and 5, a rise in W explains


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0.4

frequency

0.3 0.2 0.1

1

2 cohort

3

4

x-prevalence of neutrality belief

Figure 4. x and U for two theoretical scenarios (x in purple, U in green for scenario 1 where W is constant, U in blue for scenario 2 where W increases exponentially).

0.35 0.30 0.25 0.20 0.15 0.10 0.05 0 1906–1915 1916–1925 1926–1935 1936–1945 marriage cohort

Figure 5. The frequency (x) of cultural belief s0 across cohorts for projections 1–5. Dark blue diamonds, projection 1; pink squares, projection 2; yellow triangles, projection 3; light blue crosses, projection 4; purple asterisks, projection 5.

the decrease in U, even though the prevalence of s0 slightly increases. Figure 5 plots x1, x2, x3 and x4, the frequency (x) of the cultural belief (s0) in marriage cohort 1 (1906 – 1915), 2 (1916 – 1925), 3 (1926 – 1935) and 4 (1936 – 1945), respectively, for each of the five projections in table 3. Figures 2 and 3 demonstrated that U, the rate of uxorilocal marriages, declines across the same marriage cohorts depicted in figure 5. However, in figure 5, the frequency (x) of the cultural belief (s0) does not necessarily decline. In projections 4 and 5, the frequency of the belief (s0) in the neutrality of uxorilocal marriage actually rises (x4 . x1), albeit modestly. Projection 3 rises so imperceptibly that it could easily be mistaken for stationary (x4 ¼ x3 ¼ 0.196 . x2 ¼ x1 ¼0.195; table 3). Projections 1 and 2 do show declines in the frequency of this cultural belief, but they follow different trajectories. Projection 2 declines linearly, still leaving a frequency (x) of the belief (s0) of over 10 per cent in cohort 4, when the uxorilocal marriage rate (U ) was already under 10 per cent (data in figure 3). Only projection 1 shows an exponential decrease in the frequency (x) of the belief (s0). However, this projection nears 0 in cohort 3, when the rate of uxorilocal marriage (U ) was still over 10 per cent (data in figure 3). The Phil. Trans. R. Soc. B (2011)

clear conclusion is that there is no necessary correspondence between custom and belief, since it is possible for custom to diverge from belief, sometimes quite widely. We expect the prevalence (x) of cultural belief s0 to have decreased over time because qualitative evidence (discussed above) suggests that, by the 1990s, many Han cultural ideas had become dominant in the former plains Aborigine communities of Toushe, Jibeishua and Longtian [28]. Consequently, the first two projections, where x decreases with time, meet our expectations better than the latter two, where x increases. That two of the projections lead to an increase in x, however, suggests that in the absence of quantitative empirical data on x, we cannot be certain of its prevalence and thus we cannot resolve the debate over the actual historical frequency of Han cultural ideas among plains Aborigines in Danei at the beginning of the colonial period. The model suggests the possibility that the prevalence was 0—i.e. that there was no belief in neutrality at all—at the beginning of the colonial period. However, the qualitative evidence, discussed above, regarding the lack of shame and discrimination attached to uxorilocal marriage in Toushe, Jibeishua and Longtian suggests that the cultural idea of neutrality existed, even if at low frequency. In those projections that meet our expectations, there is still a range of possible frequencies of the cultural idea, from near 0 to over 10 per cent. This range raises questions about the other influences on U in the model: W and s. Table 3 shows that, within a single projection, a small change in the economic situation, represented by W, implies a larger change in culture (indicated by x). In other words, within any single projection, influences of the frequency (x) of cultural ideas on changes in the uxorilocal marriage rate (U) are sensitive to small changes in W. In considering the effects of W and s, we must bear in mind that, to simplify the model, we assumed that economic development led to a general level of wealth sufficient for everyone to afford a brideprice (i.e. W ¼ 1), and thus that cultural beliefs could potentially prevail in determining marriage form. However, as the stochastic effects mitigating the cultural effects of s1 weaken—for example, as public health measures reduce mortality— and thus the cultural effects of s1 become stronger (i.e. as s goes to 1), the frequency (x) of s0 also increases. Thus, ironically, these assumptions mean that the increasing importance of the idea s1 for the frequency (U) of the practice (an effect that might be thought of as the increasing ‘strength’ of the belief in the population) allows a concurrent spread of the neutral belief s0. This result of combining the general model with the Danei data runs directly counter to the prediction of the general model (discussed above) that as s goes to 1, s1 should be dominant over s0. This unexpected result could be interpreted to mean that there is more cultural variability in the wealthier population. On the surface, this interpretation seems compatible with current marriage practice in Taiwan, where ethnographic evidence suggests that rural marriages are overwhelmingly virilocal and urban marriages are increasingly neolocal (i.e. where bride and


Belief about marriage in Taiwan groom establish an independent household), perhaps the ultimate expression of neutrality (cf. [63 – 67]). The result could also mean either that cultural ideas are less important in general than anticipated (and allowed for in the general model), or that cultural niche construction—changes in whether particular ideas are accepted as meaningful (i.e. shared, abstract, public and truth to some percentage of the population)—is more important and thus leads to a qualitatively different outcome from expectations. The model also yields a lower bound for s (0.673) that is higher than we would expect based on empirical data of sibling composition as an effective predictor of uxorilocal marriage. As discussed above, when s is high, the cultural idea strongly influences practice, and s ¼ 0.673 is a fairly high value for s. Recall that sibling composition is one of the best predictors of uxorilocal marriage [30,39 – 41]. This empirically documented sensitivity suggests that we ought to find a low value for the lower bound of s, yet we do not. Several assumptions in the model could affect the empirical validity of this lower bound: random mating with regard to s, unbiased vertical transmission, gender neutrality with regard to s and s, and s constant. Changing any of these assumptions would make the model substantially more cumbersome, but these may be valuable changes to consider in the future.

6. CONCLUSIONS This model and its connections to the empirical case of changing marriage form in Taiwan yield several general conclusions about the construction of human cultural niches and the value of distinguishing between social and cultural niches. They indicate the kind of empirical data that would facilitate future models, and they suggest a potential for building bridges to the social sciences. (a) Culture is in constant flux Table 3 and figure 5 together demonstrate that, in all projections, the frequency (x) of the cultural idea s0 changes. Even in projection 3, x changes slightly (x4 ¼ x3 ¼ 0.196 . x2 ¼ x1 ¼0.195). In other words, human cultural niches—like ecological niches—are in constant flux. This conclusion fits with our conception of a cultural niche as the sum of all cultural selection pressures, which in turn derive from transmission processes (including broadcasting, reception and internalization of ideas) and interactions between cultural ideas. Shifts in belief by individuals constitute bits of change—constant flux—constructing the cultural niche. Such incremental change would only be noticeable at a population level when a significant number of people changed in the same way. Thus flux goes on constantly at the individual level but is only visible at the population level under certain kinds of conditions, which suggests both that we should expect drift (i.e. stochastic effects in small populations) to influence cultural change [16] and that cultural persistence (e.g. [7,68]) requires explanation. Phil. Trans. R. Soc. B (2011)


(b) Phenotype is not a reliable indicator of culture Figures 4 and 5 show that the frequency of a cultural unit—an idea or belief—need not correspond to the frequency of the associated practice (phenotype). Consequently, we cannot determine the content of the ideational pool—the cultural niche—on the basis of the frequency of customs. (c) Culture is sensitive to society Table 3 indicates that even small society-wide changes in economic development may result in larger shifts in cultural content, measured in the increasing frequency (x) of the belief s0, and the stronger influence (s) of the belief s1, providing further evidence of the importance of including social factors in cultural evolution models. The results of linking the general model to the Danei data raise several possibilities for future exploration. Wealth may increase the cultural variability in the population. Cultural ideas may be less important motivators of behaviour than social factors. Cultural niche construction may result in change that qualitatively departs from expectations based on cultural selection pressures alone. All of these possibilities would be best explored using models integrated with empirical data. (d) Including culture and society yields more realistic models The introduction of even highly simplified social effects leads to a more realistic model of cultural change. The modelled sensitivity of the uxorilocal marriage form to population-level economic development agrees with Wolf ’s [39] conclusions about the sensitivity of minor marriage to economic development in northern Taiwan. Moreover, when s is understood as mitigating social effects, its inclusion can realistically result in a Han population with a high frequency of disapprobation of uxorilocal marriage (the idea s1) that nevertheless maintains a noticeable frequency of uxorilocal marriage (phenotype) owing to stochastic effects on sibling composition. (e) Modifying the model requires quantitative empirical data This model is linked to one specific case study, which has allowed us to obtain specific estimates of the model parameters and projections of changes in the economy (W ) and the frequency (x) of the culturally neutral idea (s0) that may underlie the changes in the uxorilocal marriage rate (U ). However, the model can be generalized to examine the contributions of cultural and economic factors in other case studies of changes in human customs, or further specialized to be more realistic for a particular case study, if adequate quantitative data are available. For example, fitting this model to a case study of rapid change in a different time or place requires reliable data on the changing frequency of the practice over time as well as a general estimate of the economic population index for at least one cohort in the time period under consideration. To make our model


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more realistic, for example, to consider whether the coefficient of horizontal transmission (H ) depends on the prevalence of uxorilocal marriage (U ) or more directly on the prevalence (x) of cultural belief s0, would require reliable quantitative data not only on the frequency of practices across individuals but also on the frequency of associated ideas. It would also be beneficial to have an empirical understanding—and even better, an estimate—of H, the influence of peers on ideas or beliefs. Thus, the model suggests the importance of developing reliable methods for quantifying ideas independently of quantifying behaviours (see [10,50,61] for brief discussion of such methods).

(f) Realistic models promote social science collaborations We suggest that the potential for increased specificity and realism generated by niche-construction models that incorporate social as well as cultural effects on human culture can facilitate building bridges to the social sciences. We think that the implications of the findings presented here move evolutionary models of cultural change towards empirically based research in anthropology and sociology. Niche-construction models have the potential to capture many realistic elements: separation of custom (phenotype) from belief, influence of economics, social stratification, family composition and—perhaps most importantly—the recognition that culture and society are cumulative and inherited, not reinvented in each generation. We thank Yang Wen-shan, current director of the Programme for Historical Demography at the Academia Sinica in Taiwan, as well as Arthur Wolf and Chuang Ying-chang, for permission to use the Danei and Jibeishua demographic databases. M. J. Brown’s ethnographic research was funded by the American Council of Learned Societies, the Chiang Ching-Kuo Foundation, the Pacific Cultural Foundation and the Institute of Ethnology at the Academia Sinica in Taiwan. The collaborative modelling project was supported by Stanford University’s Institute for Research in the Social Sciences, Freeman Spogli Institute for International Studies, Morrison Institute for Population and Resources Studies and Center for East Asian Studies. The research was supported in part by NIH GM28016 to M. W. Feldman. Contributions: M.J.B. conducted the empirical research; M.L. and M.J.B. analysed the demographic data; M.L. produced the model in collaboration with M.J.B. and M.W.F.; and all three authors wrote the paper. M.J.B. and M.L. contributed equally to this manuscript.

APPENDIX In order to calculate the lower and upper bounds for s, shown in equation (5.1) in the text, we begin by re-writing equation (3.1) as W ¼

2ð1 U Þ : 1 þ sð1 xÞð2 s½1 xÞ

ðA 1Þ

We also solve equation (3.1) for x, keeping in mind that, by definition, 0 x 1: pffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi 1 2ð1 ð1 U Þ=W Þ x¼1 : ðA 2Þ s Phil. Trans. R. Soc. B (2011)

Solving for s, we can rewrite equation (A 2) as pffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi 1 2ð1 ð1 U Þ=W Þ : s¼ 1x

ðA 3Þ

To obtain the lower bound for s, we note that, because W4 ¼ 1 and U4 is lowest value of U, the numerator of the right-hand side of equation (A 3) will be lowest for cohort 4 (1936– 1945) as well. Moreover, horizontal transmission cannot reduce a non-zero value of x to zero. In other words, if we assume that x is non-zero in any of cohorts 1 to 3, then x4 can approach, but may not equal 0 (i.e. x4 . 0). Finally, we substitute U ¼ U4, W ¼ W4 ¼ 1 and x ¼ x4 ¼ 0 into equation (A 3) to calculate the lower bound on s: pffiffiffiffiffiffiffiffiffi slow ¼ 1 2U4 : ðA 4Þ From (A 4), since U4 ¼ 36/671 (data in figure 2), slow ¼ 0.6724293. Because x4 is strictly greater than 0, we know that s is strictly greater than slow. Moreover, since x4 may approach 1, and s 1 by definition, a similar analysis of equation (A 3) shows that s is bounded above by 1. In sum, s could be anywhere within the interval (slow, 1). In order to calculate x4, shown in equation (5.2) in the text, we substitute U ¼ U4, W ¼ W4 ¼ 1 into equation (A 2) and obtain x for time period 4 (1936– 1945) in terms of s and U4: pffiffiffiffiffiffiffiffiffi 1 2U4 slow : ðA 5Þ ¼1 x4 ¼ 1 s s To solve for x4, we must choose a value within the half-closed interval for s. We start with s just above the lower bound of its range, s ¼ 0.673. Given this value, x4 ¼ 0.000847994. In order to calculate W1, we remember that W is constant for the entire population but variable between time periods. We focus on one subsection of the population for which we have U and an estimate of x in time period 1 (1906 – 1915): the Danei Han who lived and married outside Toushe. Thus, we set U ¼ UH1 and x ¼ xH1 ¼ 0 in equation (A 1) to obtain W1 in terms of s and UH1: W1 ¼

2ð1 UH1 Þ : 1 þ sð2 sÞ

ðA 6Þ

For a given value of UH1, W1 is strictly less than the value obtained when s ¼ slow. If we substitute the empirical value of UH1 ¼ 69/326 (data in figure 2) and s ¼ 0.673 into equation (A 6) we obtain W1 ¼ 0.8328727. In order to calculate x1, we modify equation (A 2) to calculate the overall prevalence of s0 in time period 1: pffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi 1 2ð1 ð1 U1 Þ=W1 Þ : ðA 7Þ x1 ¼ 1 s Entering the empirical values of U1 (103/423, data in figure 2), s ¼ 0.673, and W1 ¼ 0.8328727 into equation (A 7), we obtain x1 ¼ 0.150437. In order to calculate H, we begin by writing down equation (3.2) for the transitions between cohorts 1


Belief about marriage in Taiwan and 2, cohorts 2 and 3 and cohorts 3 and 4: x2 ¼ x1 þ H x1 ð1 x1 Þ;

ðA 8aÞ

x3 ¼ x2 þ H x2 ð1 x2 Þ

ðA 8bÞ

and x4 ¼ x3 þ H x3 ð1 x3 Þ:

ðA 8cÞ

We substitute all instances of x2 in the right-hand side of equation (A 8b) with the right-hand side of equation (A 8a). The result is a cubic polynomial in H: 2

x3 ¼ x1 ½1 2Hð1 x1 Þ þ H ð1 x1 Þð1 2x1 Þ þ H 3 x1 ð1 x1 Þ2 :

2

x4 ¼ x1 ½1 3Hð1 x1 Þ þ 3H ð1 x1 Þð1 2x1 Þ H 3 ð1 x1 Þð1 9x1 9x21 Þ þ 5H 4 x1 ð1 x1 Þ2 þ H 5 x1 ð1 x1 Þ2 ð1 8x1 þ 8x21 Þ þ 2H 6 x21 ð1 2x1 Þð1 x1 Þ3 þ H 7 x31 ð1 x1 Þ4 : ðA 10Þ In general, equation (A 10) will yield seven possible values of H for any particular values of x1 and x4. However, up to six of these values may be complex. Any of the values that are real, greater than 21 and less than þ1, constitute a possible value for H that satisfies all the requirements for this parameter within our model. For instance, we can substitute the values of x1 and x4 that correspond to s ¼ 0.673 (i.e. x1 ¼ 0.150437 and x4 ¼ 0.000847994) into equation (A 10), obtaining: 0:000847994 ¼ 0:150437 ð1 þ 2:54869H þ 1:78185H 2 0:127648H 3 0:379552H 4 þ 0:00243713H 5 þ 0:0194036H 6 0:00177356H 7 Þ: ðA 11Þ Using MATHEMATICA, we solve this equation and obtain the following seven possible values for H, 23.06104, 21.16266 2 0.137671 i, 21.16266 þ 0.137671 i, 20.871687, 3.11696, 6.41389 and 7.66765. (Here, i equals the square root of 21.) Since only one of these is a real number between 21 and 1 (H ¼ 20.871687), that is the value we use to calculate x2 and x3. Given H ¼ 20.871687 and x1 ¼ 0.150437, we can solve equation (A 8a) to obtain x2 ¼ 0.03903042. Substituting this value of x2 and the same value of H (20.871 687) into equation (A 8b) yields x3 ¼ 0.006 336 015. Once we have x2, we can substitute U2 and x2 into equation (A 1) to yield W2 in terms of these variables and s: 2ð1 U2 Þ : 1 þ sð1 x2 Þð2 s½1 x2 Þ


Once again, we can substitute the empirical value U2 ¼ 92/488 (data in figure 2) along with s ¼ 0.673 and x2 ¼ 0.03903042 into equation (A 12) to obtain W2 ¼ 0.8654805. The method for calculating W3 is similar: W3 ¼

2ð1 U3 Þ : 1 þ sð1 x3 Þð2 s½1 x3 Þ

ðA 13Þ

Substituting U3 ¼ 93/744 (data in figure 2), x3 ¼ 0.006336015 and s ¼ 0.673 into equation (A 13) yields W3 ¼ 0.9257966.

ðA 9Þ

A similar substitution of equation (A 9) into the right-hand side of equation (A 8c) yields a 7th-degree polynomial in H:

W2 ¼


ðA 12Þ

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Research

Property and wealth inequality as cultural niche construction Stephen Shennan* UCL Institute of Archaeology, 31– 34 Gordon Sq, London WC1H 0PY, UK In contrast to other approaches, evolutionary perspectives on understanding the power and wealth inequalities in human societies view wealth and power not as ends in themselves but as proximate goals that contribute to the ultimate Darwinian goal of achieving reproductive success. The most successful means of achieving it in specific times and places depend on local conditions and these have changed in the course of human history, to such an extent that strategies focused on the maintenance and increase of wealth can even be more successful in reproductive terms than strategies directed at maximizing reproductive success in the short term. This paper argues that a major factor leading to such changes is a shift in the nature of inter-generational wealth transfers from relatively intangible to material property resources and the opportunities these provided for massively increased inequality. This shift can be seen as a process of niche construction related to the increasing importance of fixed and defensible resources in many societies after the end of the last Ice Age. It is suggested that, despite problems of inference, the evidence of the archaeological record can be used to throw light on these processes in specific places and times. Keywords: Inter-generational resource transfers; reproductive success; property rights; partible and impartible inheritance; parental investment; archaeological evidence for property

1. INTRODUCTION Attempts to find an explanation for the emergence of huge wealth and power inequalities in human societies have a very long history in the social sciences. Most of those attempts have focused on the wealth and the power as ends in themselves although the motors for the different models that have been advanced vary enormously on a spectrum from exploitation to managerial mutualism. Many of them also draw a strong contrast with hunter – gatherer societies seen as characterized by a ‘zen’ ethic that attaches little importance to material goods. What is different about the evolutionary models that have been developed in more recent years (e.g. [1 – 5]) is that they take the achievement of wealth, power and status not as ends in themselves but as proximal goals whose achievement contributes to the ultimate goal of reproductive success. However, this still raises the question of how these proximate goals came to be important. In other words, in contrast to non-evolutionary approaches to the question of how and why societies changed from ‘zen’ to materialist values, this evolutionary perspective proposes that the ultimate human goal in all societies, including modern industrial and post-industrial societies on some views [6], has been the maximization of reproductive success, but that the means of achieving it have altered. Not only did reproductive success come to depend on the achievement

and holding of material wealth, but strategies focused on the maintenance and increase of wealth could even become more successful in reproductive terms than strategies directed at maximizing reproductive success in the short term (cf. [7]). This paper will examine the general processes that led to this situation, from the perspective of niche construction. In their characterization of ecological inheritance Odling-Smee et al. [8] point out that it only exists if the consequences of modifications to the selective environment are not wiped out with each generation, but are passed on through the generations and change the selection pressures faced by the organisms concerned. They make it clear that ecological inheritance is very different from genetic inheritance and suggest that it is more like the inheritance of property. It is this idea that is the focus of this paper. Human niche construction, like that of other species, involves modifications to the physical environment, but at least as importantly, it includes the creation of new social institutions, which produce novel ecologies for human action and are arguably rather curious new niches existing at the boundary of cultural and ecological inheritance.

2. INTER-GENERATIONAL RESOURCE TRANSFERS In many species differences in parental condition are passed on to their offspring by a variety of mechanisms (see [9] for a review), including the inheritance of maternal rank (e.g. [10]). The same is true of human societies, even those hunter – gatherer societies

*[email protected] One contribution of 13 to a Theme Issue ‘Human niche construction’.

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Property and wealth inequality that are generally regarded as strongly egalitarian. This is hardly surprising given the very strong evidence that the emergence of a long period of childhood dependence was central to the evolution of the modern human life-history pattern and required massive investment from parents and other close relatives [11,12]. Lee [13] has shown how the nature and extent of inter-generational resource transfers are crucial to the evolution of species-specific mortality patterns where offspring are dependent on those transfers for survival and reproductive success, and how they explain the existence of post-reproductive survival. A consequence of this is that we would never expect the inequality scale to be re-set all the way to zero in each generation in human or indeed other animal societies where differences in parental condition are heritable. In a series of major recent studies, albeit on limited data sets, Borgerhoff-Mulder and colleagues [14– 20] have characterized three different types of intergenerational resource transfers and obtained measures of their importance in a given society, of the extent to which they are transmitted, and of their association with different degrees of inequality. Embodied wealth refers to investment in nutrition affecting offspring body weight, for example, or training in practical skills; relational wealth refers to networks of useful social contacts that may be passed on from parents to their children; material wealth obviously refers to property, such as land and animals. They were not able to obtain a corresponding measure of the transmission of ritual knowledge and its impact, although they note its potential importance (cf. [21 – 23]). In the study of hunter – gatherer inter-generational resource transfers, Smith et al. [19] concluded, unsurprisingly, that material wealth was much less important as a transmitted resource than embodied or relational wealth, but still found that values of the intergenerational wealth transmission coefficient were such that the offspring of an individual in the top 10 per cent of the population would be at least three times more likely to be in that top 10 per cent than the offspring of an individual from the bottom 10 per cent. Moreover, degrees of inequality in these societies were not insignificant, coming out close to those for present-day industrial Denmark, based on the value of the Gini coefficient (a measure of inequality generally based on the income distribution of a society that ranges between 0, for complete equality, when everyone has the same share of the total income, and 1, for complete inequality, corresponding to a situation in which one member of the society monopolizes all the income and the rest have nothing). The relationship between transmission and inequality was borne out by the correlation of 0.79 between the corresponding Gini values and transmission of embodied and relational wealth, the most significant forms in these societies, weighted by their estimated importance in each society (n ¼ 8, p ¼ 0.02), excluding two cases where the embodied wealth is represented by body weight, which does not follow the general pattern (see [20, fig. 5]). The emergence of differential rights to specific material resources within a given social entity, held Phil. Trans. R. Soc. B (2011)

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by groups such as lineages, expanded the range of variation enormously. This claim is strongly borne out by the results of the recent studies referred to above (see especially [14,20]). The Gini coefficients for pastoralist societies (0.4 overall), and even more so for agriculturalists (0.51 overall), are far higher than for hunter – gatherers (0.19), indicating much higher degrees of inequality. Moreover, the contribution of material, as opposed to embodied or relational, wealth to inequalities in the former societies is much greater, as is the rate of inter-generational material wealth transmission: 0.53 for landed wealth and 0.67 for livestock. When the transmissibility of wealth and the importance of the different types are taken into account, it appears that children whose parents are from the top 10 per cent of the wealth distribution are 16 times more likely to be there than children whose parents were in the bottom 10 per cent. For agricultural and pastoral societies taken together the correlation between the transmission of material wealth, weighted by its estimated importance in each society, and the Gini coefficient of inequality is 0.59 (n ¼ 9, p ¼ 0.092). In short, the existence of rights to inheritance of productive material resources has enormous consequences and enables the rich to get richer on previously unimaginable scales, for a variety of reasons: the increased mitigation of risk that wealth provides; the economies of scale available in the management of larger herds and estates [24]; and the ‘complementarities’ between different resources [20], whereby greater material wealth can lead to greater relational wealth, for example, in the form of followers vital in intra-elite factional competition (e.g. [23,25]). The result is the Pareto power law distributions of wealth that are so familiar to us, in which the majority of the population have very little and a small number have the majority of the wealth, together with the political power and influence that go with being at the top end of the scale (cf. [26]). A key factor here is the characteristics of the resources themselves; specifically, the extent to which they are excludable and divisible and thus amenable to some sort of private ownership [27]. All production involves the application of land, labour and capital (understood in the most general terms) and the transactions associated with the distribution of the results, but these processes always take place within the context of a set of institutions that define the rights that groups and individuals have to use those resources and to exclude others from their use. Like DysonHudson & Smith [27], North [28] argues that the basis of the property rights that emerge in particular situations arises from the benefits that the rights provide in relation to the costs of enforcing them when compared with those of the status quo. Thus, if a resource becomes scarce then it may become worthwhile for some individuals or groups to pay the costs of changing the nature of the existing property rights and start excluding people who previously had rights. In effect, a changed distribution of costs and benefits may pay at least some parties to press for renegotiation of the existing institutions, which may then feedback into the content of social norms. Moreover, to the

extent that such property rights are predictable and sustainable, then the ‘bird in the hand is worth two in the bush’ principle may be weakened and it may become worthwhile to invest in resources for the future. Many important foraged resources are neither densely nor predictably enough distributed to meet this requirement and mobility is essential to their successful exploitation. Others, however, certainly do satisfy the requirement, particularly those that come to be exploited when groups intensify and have to shift down the hierarchy of preferred resources; examples include groves of productive trees or good fishing sites (e.g. [29,30]). Such intensification is generally associated with increasing sedentism, both appearing at the end of the last Ice Age, most probably in connection with increasing population [31] and greater climatic stability [32]. As the authors note, Smith et al.’s analyses [19] described above did not include any of this type of hunter–gatherer society because none are still extant. Of course, agriculture provides the most obvious basis for the creation of ownable resources, but it is important to realize that this will not always be the case (cf. [17]). Just as some foraged resources lend themselves to ownership whereas others do not, the same is true of agriculture. It is not a matter of foraging versus farming but of resource permanence and potential for ownership in terms of excludability and divisibility. Thus, the swidden clearings of shifting horticulture have less potential than fixed fields or herds of animals. This is reflected in the fact that in Smith et al.’s [20] comparisons horticultural societies show a pattern of both inequality and transmission of the different wealth categories much more similar to hunter – gatherers than to pastoralists and agriculturalists. Adler’s [33] cross-cultural survey of land tenure found that the duration of access to resource areas tended to increase with the amount of labour invested in the resource. He also found that while the size of the access group initially increases with the amount of labour invested, it then declines, so that at high levels of investment it is households/individuals that become the primary access group. At the same time, the size of the communities in which the access groups are embedded and which are involved in the resolution of access disputes also increases (figure 1). The rights of these individuals/households to their resources may also include inheritance: their passingon to a new generation, at the death of the individuals concerned or during life, in institutions such as bridewealth and dowry. Thus, as agricultural input intensifies, rights become more permanent and more exclusive. Among the Hopi of the North American Southwest, for example, spring-fed terraced land was owned and passed down by individual households, and among the Zuni irrigated land belonged to individual households while less intensively used land was open to the broader community ([33]; cf. [34, pp. 24– 25]; [35, pp. 60 – 67]) for similar arrangements among European Alpine communities). For Adler then, land tenure systems are social institutions concerned with specifying rights of access to resources over varying Phil. Trans. R. Soc. B (2011)

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Figure 1. Idealized relationship between primary resource access group size, level of horticultural labour invested in production and size of community within which primary resource access groups are found. As intensity of agricultural labour increases, community size increases. At the same time the size of the primary resource access group first increases then decreases (from [33, fig. 2]. Copyright (1996), with permission).

periods of time, where the length of time tends to increase with the degree of intensification, and at more intensive levels they provide ‘long-term insurance’ concerning the future availability of valued resources thus created. Of course, they only provide this so long as the social system that assigns the relevant rights continues to exist. Equally obviously, the possessors of rights to superior resources recognized by the social group will have a competitive advantage. Many modern hunter – gatherers are known to resist the institution of ownership and to insist on sharing when group members try to establish private property rights, but the number of cases where individuals in sedentarizing hunter – gatherer groups succeed in establishing such rights, and the relationship demonstrated by Adler between intensification and increasing rights, suggest that this is a general tendency in many circumstances. Moreover, while hunter – gatherers depend on sharing to mitigate risk, horticultural households are much more self-sufficient [17], and generalized sharing may even be deleterious for them in some circumstances as a risk mitigation strategy [36,37]. Thus, transitions from sharing to private property should not necessarily be seen simply as a triumph of one set of interests over another; rather the benefits of sharing as a means of risk reduction may have been decreasing and therefore less worth defending against those attempting to assert property rights. In this context it is worth adding that while stronger rights to tenure with increasing intensification, resulting in the recovery of the costs of investment, do provide an incentive for increased economic activity,

Property and wealth inequality it should not be assumed that improved economic efficiency is the sole, or even the most important result. The existence of power differentials within society, where the powerful are able to create institutions that are largely in their own interest, will have a major impact on outcomes, especially in situations where there are poor dispersal opportunities for lower ranking individuals and groups, and/or where levels of competition between elite factions seeking followers are low (cf. [38]). The inherited ownership rights and privileges jealously maintained by aristocracies against commoners the world over are ample evidence of this. Aristocracies also have the strongest reasons to contest both factional struggles within their own polity and wars between polities since defeat can result in the wholesale reallocation of ownership, especially at higher levels in the social hierarchy.

3. WEALTH AND REPRODUCTIVE SUCCESS It is now well established that in societies where there is heritable private property in land and/or animals, the availability or otherwise of inherited resources makes a major difference to individual reproductive success (e.g. [39,40]). In other words, the new ecological/ institutional conditions change the nature of the reproductive strategies that will be successful. In this respect animals and land have rather different characteristics. Animal herds are a special kind of property in that they reproduce themselves at timescales that are short in relation to human lifetimes. Herds can be divided between several children (usually sons) so long as each has a herd of minimal threshold size that makes it less vulnerable to major risks. Given a strong correlation between wealth and reproductive success, richer individuals will have to make less severe tradeoffs and generally, other things being equal, the natural increase of animals means that partible inheritance will continue to be successful over the generations, with the rich, over time, being massively more successful than those who can, for example, only endow a single child. In the case of the Gabbra pastoralists of east Africa, Mace [3] showed that the optimum strategy to maximize the number of grandchildren involved giving herds of a certain size to as many sons as possible, dependent on the wealth available. Sons not given herds were at a reproductive disadvantage. Clearly, for poor households there would be risks in only endowing a single son but in principle, for poor households, this would give greater reproductive payoffs than splitting a small herd between several. In fact, for very poor households it would make more sense to invest in daughters, for the bridewealth they attract, as Cronk [41] showed for the Mukogodo. It has often been argued in the literature that pastoral systems tend to be egalitarian and to have wealth-levelling mechanisms, while wealth differences are likely to be unstable owing to the incidence of natural disasters that can decimate herds. However, as we have seen, this does not correspond to the results of Borgerhoff-Mulder et al.’s [15] analyses, and the literature they survey indicates that disasters actually tend to generate increased inequality, because wealthy Phil. Trans. R. Soc. B (2011)

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households are far more likely to survive them (cf. [42]) while poor households are likely to be pushed out of the pastoral system altogether. Moreover, livestock transfers from rich households to poorer ones can be a basis for patron – client relations at least as much as levelling mechanisms. Despite the existence of an ideology of equality in pastoralist societies, there tend to be major wealth differentials, they are inherited and they have significant reproductive consequences. Similarly, wealth in land is also associated with greater reproductive success, with less severe tradeoffs for the rich. For example, Pettay et al.’s [43] study of natural selection effects on female life histories, based on data from farming families in 18th century Finland, found that there were highly significant differences between women from different wealth categories in their number of grandchildren: the least squares mean number of grandchildren for women from the Rich, Middle and Poor groups was, respectively, 15.77, 11.16 and 6.08. Equally important from the niche construction perspective is that the wealth stratification affects the selection pressures. Thus, for women in the Poor group, earlier age at first reproduction was more strongly selected than later age at last reproduction, while for women in the Rich group this was reversed. More generally, ‘If the population is subdivided by lifelong access to resources, selection may lead to divergent evolution on life-history traits, as each wealth class has its own optimal life-history trait combination’ ([43]; cf. [3]). However, wealth in land, where land is an excludable and divisible resource for which it is worth paying the costs of defence, is different from wealth in animals because it cannot be expanded in the same way, thus constraints are even tighter. In rural Ireland in the nineteenth century, for example, though ownership of the land was often vested in distant Protestant landlords, poor Catholic farming families inherited tenancies. Because of the scarcity of land, only one child in each generation was allowed to inherit and only the heir could both marry and stay at home; any other siblings who remained had to stay single. Strassmann & Clarke’s [44] study demonstrates the conditionality of this rule on ecological constraints, since the introduction of the potato, by making it possible to support more people per hectare than previous crops and also allowing the extension of cultivation to areas unsuitable for those crops, made partible inheritance and the creation of new landholdings a viable option for a while and led to increased local marriage rates, though it was followed by consolidation and the reversal of this trend. In contrast to members of farming families, labourers had no possibility of owning land and no reason to delay marriage, though they still ended up having lower average reproductive success than women from farming families. Strassmann & Clarke postulate that the strict rules against downward mobility for non-inheriting sons and daughters without a dowry represented a strategy for maintaining the wealth of the lineage. Moreover, as they also point out, the fact that farms were passed on through the generations by genetically related males is in keeping

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with the argument that maintaining wealth is the key to ensuring reproductive success, since a purely economic motivation cannot account for this. As with the Gabbra herd sizes, maintaining and transmitting a minimal holding size was critical. In fact, given the low probability of inheritance for most people in most families, dispersal, i.e. in this context emigration, gave the best fitness payoff. Netting’s famous study of an Alpine community [35] also shows that the introduction of the potato raised the local population ceiling and led to a period of population growth in what was otherwise a tightly constrained situation demographically; again it was accompanied by increased out migration, for which the possibilities had also increased with the growth of industrialization. Here too, ‘inheritance formed the crucial link from the land supply to the reproductive potential of the people’ [35, p. 226], and though inheritance was partible, a variety of mechanisms kept the number of households from expanding beyond what was viable in terms of size of holding, and resulted in great stability of family lines. There were laws preventing male in-migration and giving political rights only to male descendants of village families, while the dependence of marriage on the acquisition of sufficient resources to form a household led to late marriage and high rates of celibacy, reinforced by Catholic moral values (cf. [45]). It is clear that any system of land inheritance must have mechanisms for restricting the number of heirs or wealth will be swiftly dissipated. Cuneiform documents from the 2nd millennium BCE state of Sippar show that land was inherited patrilineally and that inheritance was partible [46]. However, celibate sisters who were nuns/priestesses could also inherit an equal share, which then returned to male members of her family on her death. Harris [46, p. 132] suggests that this may have been a device invented by wealthy families to reduce the effects of partibility. These societies were also socially monogamous and Fortunato & Archetti [5] have shown that social monogamy can be a stable strategy reproductively advantageous to males where division of resources leads to a loss of their value, or where wives provide greater paternity certainty in exchange for exclusive transmission of wealth to their children. This is the reason, they argue, for the prevalence of monogamy in the historical societies of Eurasia because they were based on intensive agriculture in conditions of land scarcity, so that landownership provided a major productive and therefore reproductive advantage. Systems of unigeniture, the transmission of wealth to one offspring only, take things a stage further. We have seen above that unigeniture is a sensible strategy where only a small amount of wealth is available for transmission and there is some minimal threshold below which transmission does not lead to improved reproductive success. What accounts for situations where a large landed estate could be divided into several lots giving improved reproductive success but unigeniture prevails anyway? Baker & Miceli [24] suggest that such a rule will exist when economies of scale are available and a fixed rule can prevent competition between heirs, but does not explain why heirs Phil. Trans. R. Soc. B (2011)

with different interests do not contest the rule. Indeed, there is evidence that when competition for a viable amount of land reaches a certain level, this is precisely what happens (e.g. [47]). Chu [48] provides a contrasting model, much more in keeping with the argument of this paper. Starting from the considerable historical and ethnographic evidence that family heads have often been explicitly concerned with ensuring the continuation of the family line, and also from the assumption that in traditional societies with limited if not non-existent capital markets, children who start with wealth stand a greater chance of themselves becoming rich, he creates a model of the division of inherited resources through the generations that minimizes the probability of lineage extinction and shows that primogeniture is a probable outcome. He proposes therefore that the policy of unequal division leads to the desired goal of lineage prosperity and is preferred by family heads, ‘so that at least one of their children is more likely to stay (or become) rich, hence making their succession lines more firm’ [48, p. 97]. It also emerges from his model that although unequal bequests increase inequality within a given generation they may actually increase upwards social mobility, in that they give a greater probability of occasional members of lower social groups becoming rich. Voland’s historical demographic analysis of the community of Krummhorn in north Germany in the eighteenth century supports these conclusions. In this agricultural community in a fully occupied landscape, farms were kept together by a system of unigeniture, in this case where the youngest son inherited the farm, and subsequent records demonstrate that elite farmers had much greater reproductive success than the general population over the long term: ‘a prosperous farming couple of the eighteenth century had almost twice as many gene replicates in the local population 100 years after wedding than an average family’ [49]. The predictions are also borne out by a recent study of resource competition and reproduction in Karo Batak villages in Indonesia by Kushnick [50]. He found that in those families with large landholdings, inter-birth intervals were longer following the birth of a son with at least one brother than in those families with no brothers, the opposite of the effect in landless families. First-born sons in landholding families also had much lower mortality than later ones; the difference was much slighter in landless families. Similar points are made by Boone [40] in his study of the fifteenth century Portugese nobility, and by Hill [51] in her evolutionary analysis of the situation of medieval religious women. Summers’ paper on the evolutionary ecology of despotism [52] makes an argument on similar lines in many respects to that presented here, noting that aristocratic endogamy was a further means of ensuring the continuing existence of lineage land holdings (cf. the discussion by Smith et al. [20] about the importance of positive assortment in marriage partners for wealth transmission). In addition, as noted above, Boone & Kessler [42] show that over the long term, investing in higher status can also lead to greater fitness than

having more children if catastrophic events occur with any regularity and higher status individuals are more likely to survive them. McNamara & Houston [53] provide a general framework for considering the reproductive consequences of different behavioural strategies when inter-generational effects are strong. In a simple model where individuals are genetically the same but in two quality states, the higher the correlation between the state of parent and offspring as high quality is passed on over the generations, the greater the reproductive value of high quality relative to low quality individuals in the long term. In the light of what we have seen above, such effects are likely to be relevant even in hunter– gatherer societies where only embodied and relational wealth are relevant, but much stronger in the case of the material capital represented by domestic animals and by land or other fixed assets, when they are the object of long-term investment and justify the potential payment of defence costs. The effects of this situation are profound because the existence of the inter-generational transmission of quality means that the fitness of a strategy is given by ‘the annual growth rate of numbers of descendants far into the future’ [53, p. 72]. Thus we cannot simply look at the number of, say, grandchildren, to evaluate it. ‘. . . when there are strong inter-generational effects . . . maximization of fitness does not necessarily maximize expected numbers of offspring or even grandchildren or great grandchildren’ [53]. In the particular model case they illustrate, individuals are defined as either high quality (H) or low quality (L). Low quality individuals have one strategy available (L(1)): they leave on average 1 surviving offspring, and that offspring is low quality with probability 0.8, high quality with probability 0.2. High quality individuals have two strategies available: under H(1.5) 1.5 offspring survive on average, each high quality with probability 0.9, low quality with probability 0.1; under H(2.0) 2 offspring survive on average, each with probability 0.5 of being high or low quality. Strategy 1 involves taking action L(1) when low quality and H(1.5) when high quality; strategy 2 takes L(1) when low quality and H(2.0) when high quality. Suppose that at time 0 equal numbers follow each of the two strategies and all are in the high quality state (figure 2). Because strategy 2 produces more offspring, there are less individuals following strategy S1 than strategy S2 to start with, though they are of higher mean quality. However, this difference in quality of individuals following strategy S1 (H(1.5) when they are high quality) does not win out over S2 (H(2.0) when high quality), in terms of the number of individuals following it, until the fifth generation. After that the success of strategy S1 goes on to far outstrip S2 into the future; in this case after 100 generations the relative number following S1 compared with S2 is 34 851, even though the superior fitness of strategy S1 would not have been reflected in the number of grandchildren, or even great grandchildren. As they go on to point out, a number of authors have considered wealth inheritance in the context of intergenerational effects on reproductive fitness (e.g. [7,54]), but the former simply assumes an Phil. Trans. R. Soc. B (2011)

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Figure 2. The relative number of offspring produced by the strategy of having less offspring but investing more in them (S1) compared with having more but investing less (S2). In the first time step S1 does markedly less well than S2; after that it begins to do better though the proportion of individuals following S1 does not exceed the proportion following S2 until the fifth generation. From [61].

equal allocation of wealth to offspring while the latter looks only at short-term impacts. The key point that McNamara & Houstons’ model explicitly demonstrates is that where there are strong intergenerational effects it pays to give continuing priority through the generations to maintaining high quality at the expense of immediate reproductive success (cf. [6]). These strong intergenerational effects change the nature of the selection pressures and where they act. As we have seen, the best strategy for maintaining high quality over the generations when it comes to wealth inheritance will vary depending on the nature of the resources, but at least when the resource is land, it appears that a combination of social monogamy and unigeniture or other means of restricting inheritance will be an extremely successful strategy in many situations.

4. THE ARCHAEOLOGICAL RECORD The problem with trying to trace evidence of these niche construction processes in prehistory on the basis of the archaeological record is that we have no direct evidence of reproductive success except in the most general terms, for example the greater reproductive success of farming compared with foraging strategies at the time of the expansion of farming into Europe, on the basis of the population growth this produced ([55,56]; cf. [45]). Less difficult, but still problematical, is the making of inferences about prehistoric property rights, from which inferences about inheritance may then be made. Hayden [29,30] argued that property rights in favoured fishing sites and raw material sources could be identified at a site on the Canadian Plateau in British Columbia and that the long span of time over which the pattern of differential resource use was present at the site indicated that the rights must have been inherited, a proposal entirely in keeping with what is known ethnographically about both the inequality present in the hunting-fishing-gathering societies from this region

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and the private property rights over resources like favoured fishing locations that existed within them and provided the basis for the inequality. Kuijt & Finlayson [57] have identified early granaries at the Pre-Pottery Neolithic A site of Dhra’ in the Levant, ca 11 500 – 11 000 BP, at a time when cereals were being cultivated but not yet domesticated, and have shown that the earliest granaries were located in extramural locations between houses. A thousand years later, it appears that food storage begins to take place inside houses, while by 9500 cal BP, houses have dedicated storage rooms. The authors suggest that this is indicative of a shift from communal to private ownership. In the same region at 7000 cal BP there is evidence for the existence of property differentials on a much greater scale. At the site of Tel Tsaf, Garfinkel et al. [58] have shown that some individual courtyards with nuclear family-sized houses contained grain storage silos with a capacity 12– 24 times greater than the annual grain needs of such a family. Moreover, the cultivated area required to produce such massive quantities of grain would have been beyond the capacity of a single family to cultivate and harvest, suggesting both differential landownership and a source of dependent labour, or at least some means of extracting surplus from other households. Ethnographically, cattle are almost invariably an important form of property and source of wealth, more important for their milk yields, labour and use in social transactions than as a source of meat (cf. discussion in [59]). The fact that they may be communally managed does not mean that they are communally owned. The high percentages of cattle bones found on the sites of the earliest farming societies of Central Europe 7500– 7000 BP [60], together with contemporary evidence for the human consumption of milk [61], provide strong evidence for the existence of private property in cattle (cf. [62]). The fact that they often appear to be communally consumed in feasts does not contradict this. When cattle are killed there is so much meat that it is hardly an exaggeration to suggest that feasting is virtually inevitable, and the political credit to be gained by powerful households from holding feasts is obvious. Bogaard’s [63] argument that the crop-growing system in these early farming societies depended on the intensive use of small areas of land also points to the existence of private property rights, while van der Velde’s [64] analysis of settlement evidence of the earliest farmers in the Netherlands and western Germany pointed to the existence of long-term social patterns: particular households and groups of households seem to have continued through time, with continuing inheritance of status witnessed by the rebuilding of houses of the same type in the same places, and greater differentiation between houses over time suggesting increased inequality, a pattern associated with populations reaching local carrying capacities [65]. In some areas this was associated with the first appearance of cemeteries, which a number of authors have regarded as representing an ancestral claim to territory in the face of increasing competition, and there may be significant differentials in burial wealth [66]. Such arguments as these are also supported by other indirect lines of evidence. By applying the Phil. Trans. R. Soc. B (2011)

phylogenetic comparative approach to cross-cultural data, Fortunato & Mace [67] showed that in societies speaking Indo-European languages an association of bridewealth with polygyny and of dowry with monogamy does not arise as a result of historical relatedness but because the practices of bridewealth and dowry, on the one hand, and polygyny and monogamy, on the other, evolved together, with the implication that there might be a functional relationship between them. Dowry with monogamy represents the most probable ancestral state at the root of the Indo-European tree and a statistical analysis of the most probable evolutionary path from this state shows that bridewealth with polygyny and dowry with monogamy represent relatively stable configurations whereas the converse combinations do not. As we have seen, monogamous marriage can be a stable strategy reproductively advantageous to males where division of resources leads to a loss of their value, or where wives provide greater paternity certainty in exchange for exclusive transmission of wealth to their children [5]. A connection between such postulated practices and early farmers in Europe is suggested by recent estimates of the date of the root of the Indo-European language tree to between 8000 and 10 000 years ago [68], which potentially links their spread to the spread of farming and farmers [69]. It is also in keeping with strontium isotope evidence for patrilocality among the earliest Central European farmers [70]. In short then, while such arguments about the existence of inheritance institutions related to material wealth remain speculative, inferences about their existence in the prehistoric past are not wholely beyond our reach.

5. CONCLUSION The long-standing tradition within the social sciences of assuming that wealth and power are ends in themselves largely misses the point. They became the focus of human attention and competition in contexts, in particular of agricultural intensification and the scarcity of land, where the inheritance of property and the vastly increased importance of intergenerational effects that it produces changed the nature of reproductive competition. The emergence of private property rights has niche constructing properties that affect selection pressures on reproductive strategies in several related ways. First, it drastically changes the relative importance of the different types of inter-generational transfers that affect reproductive success and greatly extends the range of inequality (cf. [1]). Second, the wealth stratification introduced creates reproductive stratification in populations in terms of selection on the best reproductive strategies to follow; the strategies that are most successful for the wealthy are not the same as those that produce the best outcomes for the poor [6]. Third, the different characteristics of wealth in animals and land lead to different best reproductive strategies in cases where one or other is clearly dominant, tending to involve polygyny on the one hand and monogamy on the other. Fourth, the enhancement of the importance of inter-generational transfers means that in the case of

Property and wealth inequality land and other relatively fixed resources greater longterm reproductive success can be achieved not by maximizing the number of grandchildren but by strategies that focus on keeping wealth intact through the generations, a strategy that has further benefits for success in intra-elite competition, where failure can be disastrous (cf. [25]). Despite appearances to the contrary, it is these factors affecting reproductive success that are responsible for the focus on wealth and power as apparent ends in themselves by social actors, once inter-generationally transmissible productive property rights come into existence. There are many indications that social actors themselves are aware of this (e.g. [48]), even though most social science studies have not been, because, in contrast to evolutionary approaches, they have been fixated on production and blind to reproduction. I would like to thank James Conolly, the editors and an anonymous referee for comments on a previous version of this paper. Of course, none of them is responsible for its shortcomings.

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Research

Niche construction on Bali: the gods of the countryside J. Stephen Lansing1,2,3,* and Karyn M. Fox1 1

School of Anthropology, University of Arizona, Tucson, AZ 85721-0030, USA 2 Santa Fe Institute, 1399 Hyde Park Road, Santa Fe, NM 87501, USA 3 Stockholm Resilience Centre, Kra¨ftriket 2B, 106 91 Stockholm, Sweden

Human niche construction encompasses both purely biological phenomena, such as the evolution of lactose tolerance, and dual inheritance theory, which investigates the transmission of cultural information. But does niche construction help to explain phenomena in which conscious intention also plays a role? The creation of the engineered landscape of Balinese rice terraces offers a test case. Population genetic analysis and archaeological evidence are used to investigate whether this phenomenon emerged historically from trial and error by generations of farmers, or alternatively was designed by Bali’s rulers. In light of strong support for the former hypothesis, two models are developed to explore the emergence of functional structure at both local and global scales. As time goes forward and selected patterns of irrigation schedules are implemented, local variation in rice harvests influences future decisions by the farmers, creating a coupled human– natural system governed by feedback from the environment. This mathematical analysis received a measure of empirical support when government agricultural policies severed the local feedback channels, resulting in the almost instantaneous collapse of rice harvests. The historical process of niche construction may also have included an evolution of religious consciousness, reflected in the beliefs and practices of the water temple cult. Keywords: emergence; adaptive agents; evolutionary games; NRY haplotypes; Hegel

1. INTRODUCTION: NICHE CONSTRUCTION IN A COMPLEX SOCIETY Humans, like beavers and termites, are vigorous practitioners of what biologists call ‘niche construction’: the active modification of their habitat, which can alter selection pressures on behaviour through feedback relationships [1]. Well-known examples include the coevolution of animal domestication and adult tolerance to lactose, and the coevolution of sickle cell anaemia and malaria in response to increasingly settled communities [2,3]. Here, we consider a different process, one that appears to be uniquely human: the deliberate, intentional modification of the natural world. Marx believed that this process defined our species. ‘It is as clear as noon-day,’ he wrote, ‘that man, by his industry, changes the forms of materials furnished by Nature, in such a way as to make them useful to him’ [4]. This process was already so successful in his own time, according to Marx, that nature untouched by human labour had vanished ‘except perhaps on a few Australian coral islands’ [5]. But does the theory of niche construction help us to understand what Marx called ‘humanized nature’? Or is it better suited to cases where there is no question of conscious intention, like lactose tolerance? Here we

consider an environment that brings this question into sharp focus. The irrigated rice terraces of the Indonesian island of Bali are among the world’s most productive agroecosystems. A lattice-like structure of canals, tunnels and aqueducts is managed by organized groups of farmers, using specialized networks of ‘water temples’. Is this an example of niche construction? While some scholars argue that the terraced landscape was built by trial and error, others believe that it was created by Balinese kings. The former view may be consistent with niche construction, but the latter is probably not. Presently, there is little role for conscious planning in the theory of niche construction, which explains the intricate architecture of environments like termite mounds as products of Darwinian selection. But in cases like the rice terraces, the role of conscious intention cannot be ignored. As Marx observed, ‘a spider conducts operations that resemble those of a weaver, and a bee puts to shame many an architect in the construction of her cells. But what distinguishes the worst of architects from the best of bees is this, that the architect raises his structure in imagination before he erects it in reality’ [6]. Current theories of human niche construction, such as dual inheritance, do not directly address this question because they focus on cultural mechanisms of transmission for innovations like dairying or cooking. If human niche construction is to account for historical phenomena like the Balinese case, the analytical focus must be broadened to


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include the global-scale consequences of conscious innovation as well as the transmission of existing repertoires of cultural information. We return to this point in the discussion.

2. NICHE CONSTRUCTION OR ROYAL ENGINEERING? The first question is whether the rice terraces are indeed an example of niche construction. A longstanding debate about the history of irrigation in Bali bears on this question [7]. Elsewhere in Southeast Asia, the spread of irrigated rice agriculture was usually associated with the expansion of precolonial kingdoms. Typically, the earliest irrigation systems were constructed by villages, and later consolidated and expanded by their rulers [8]. But because of Bali’s steep volcanic topography, ‘the spatial distribution of Balinese irrigation canals, which by their nature cross community boundaries, made it impossible for irrigation to be handled at a purely community level’ [9]. The problem was solved by the creation of a new institution called subak, which began to appear in eleventh century royal inscriptions. Subaks were associations of farmers who managed irrigation water from a common source, such as a spring or irrigation canal. Most ancient irrigation systems encompassed more than one village. For example, an inscription dated AD 1072 refers to a single subak comprising fields located in 27 named hamlets [10]. But the spread of irrigation in Bali was not well documented because Balinese kingdoms never entered an imperial phase, and stopped issuing inscriptions altogether by the middle of the fourteenth century. Half a millennium later, in 1811, Sir Stamford Raffles visited Bali and recorded his surprise that the rajahs of Bali were merely one group of landowners among many others: ‘The sovereign (that is, the Raja of Buleleng) is not here considered the universal landlord; on the contrary, the soil is almost invariably considered as the private property of the subject, in whatever manner it is cultivated or divided’ [11]. The marginal role of Balinese kings in irrigation, also noted by later colonial observers [12], prompted a question that has been debated for nearly a century: Does Bali provide an exception to the thesis that the expansion of irrigation encourages the centralization of power? Some scholars envision a slow process of irrigation expansion driven by the needs of villagers, while others argue that the key role was played by the rajahs, with the subaks serving as merely a reservoir of manpower [7,13]. These alternatives can be formalized as follows: one scenario envisions the expansion of irrigation as organized by princes, who mobilized labour to construct irrigation systems in previously forested regions [14]. An alternative ‘budding model’ predicts that the irrigation works were created as a result of local initiatives, with new settlements budding off downstream as a result of population growth. The budding process makes specific predictions about the population genetic structure of the villages, and can therefore be tested through analysis of neutral genetic markers. If the expansion of irrigation was accomplished by the farmers themselves, then population movements of Phil. Trans. R. Soc. B (2011)

men (patrilineages) would occur as a result of demographic pressure, leading to the formation of new daughter settlements close to parent villages. The budding model would thus predict the formation of small communities located along irrigation systems, with the oldest settlements located at the irrigation outtakes nearest to the most ancient weirs or springs. Alternatively, if large, multi-subak dams were built in virgin territory, there would be no reason for farming communities closest to those dams to be older than those located further downstream. To evaluate these alternatives, we compared population genetic structure for subaks located in two regions of Bali (figure 1). The first group consisted of 287 farmers who belong to 13 subaks associated with a water temple network in the vicinity of the village of Sebatu, on the upper reaches of the Petanu river. Archaeological evidence suggests that these are among the oldest rice terraces and water temples in Bali [15,16]. The second group consists of 120 farmers belonging to eight subaks located along the Sungi river in the district of Tabanan. The genetic structure of these two groups was compared with the background level of genetic diversity from an additional sample of 100 men, randomly selected from each of the nine geographical regions of Bali. The results of genetic analyses of these populations are fully explored by Lansing et al. [17,18]; here, we summarize the relevant findings. Subaks located at the furthest positions upstream on their respective irrigation systems on both rivers demonstrate greater levels of genetic differentiation and diversity, suggesting that they came into existence before their downstream neighbours. The budding model predicts decreases in diversity among subpopulations as the process continues in time. Consistent with this prediction, diversity parameters were also higher for the older Sebatu subaks located furthest upstream in their respective irrigation systems than those known to be younger. There was a strong correlation between Y-STR and mitochondrial (mt)DNA structure in the Sebatu subaks (r ¼ 0.629). There were also strong correlations between Y-STR variation and geography (r ¼ 0.541), and mtDNA and geography (r ¼ 0.361), possibly reflecting the same events in population history. No such correlations existed for the Tabanan subaks, or the all-Bali sample (table 1).1 It is worth noting that the budding deme model implies a very restrictive set of constraints on the genetic structure of these farming villages. These include strong founder effects accompanied by genetic drift and directional micro-movements; more structure in patrilineages than in matrilineages; and a strong contrast between subaks versus the background relatedness of the whole population. These are not the expected patterns under the alternative scenario of state-controlled expansion of irrigation; that is, the rajahs encouraging migrations to newly constructed irrigation areas, or alternatively bringing settlers from nearby villages. The evidence from the Y chromosome is consistent with the principal features of the budding deme model: patrilocal residence with very little movement on the landscape, except for occasional micro-movements to nearby daughter settlements.


Niche construction on Bali

J. S. Lansing & K. M. Fox 929

Buleleng Bangli

Jambrana

Karangasem

Tabanan Badung

lakes boundaries of administrative districts

Gianyar

peaks above 1500 m

featured rivers (Sungi and Petanu)

Klungkung

studied subaks along the Sungi river, Tabanan studied subaks in the vicinity of Gunung Kawi Temple, Sebatu, Gianyar 0

10

20

Denpasar

Nusa penida

30

km

Figure 1. Map of Bali showing locations of Sebatu and Tabanan subaks, and boundaries of the nine districts from which samples were taken. While the older Sebatu subaks are tightly clustered, the Tabanan subaks are spread along the full length of the river. The average geographical distance between the Sebatu subaks is only 3.2 km; it is 13.9 km for those along the Sungi river. Table 1. FST parameters for Y-SNP haplogroups and mtDNA HVS1 sequences. Y-SNP

Sebatu subaks (n ¼ 13) Tabanan subaks (n ¼ 8) Bali regions (n ¼ 9)

mtDNA

FST

p

FST

p

0.141 0.009 0.075

0 0.274 0.011

0.086 0.052 0.008

0 0 0.097

The older the subak, the more evidence for this pattern [18].

3. FEEDBACK AND THE EMERGENCE OF FUNCTIONAL STRUCTURE The genetic evidence is consistent with a process of niche construction pursued by generations of farmers, rather than the execution of a royal blueprint for the expansion of irrigation. But the concept of niche construction implies more than the simple spread of an adaptation. Specifically, niche construction ‘introduces feedback into the evolutionary dynamic . . . (and) creates an ecological inheritance of modified selection pressures for descendant populations’ [19]. Here we consider whether these two features, evolutionary feedback and ecological inheritance, apply to the Balinese case. We begin with evolutionary feedback. As noted above, Balinese rice farmers manage their fields collectively in organizations called subaks. Because irrigation depends on seasonal rainfall, each subak’s choice of an irrigation schedule affects the availability of water for their neighbours downstream. The timing of irrigation Phil. Trans. R. Soc. B (2011)

can also be used to reduce losses caused by rice pests like rats, insects and insect-borne diseases. This is accomplished by synchronizing rice harvests and then briefly flooding the fields, depriving the pests of their habitat. The larger the area that is encompassed by the post-harvest flooding, the fewer the pests. But if too many subaks try to flood their fields at the same time, there will not be enough water. This creates a feedback relationship between the selection of irrigation schedules and the occurrence of water shortages or pest infestations. To explore the effects of this environmental feedback on the behaviour of the farmers, we created two models. The first model explores the effects of feedback on the strategic decisions taken by individual farmers. The second model embeds this logic in an ecological simulation of an entire watershed, and explores feedback effects at a global scale. The first model consists of a game in which two subaks decide whether or not to synchronize their irrigation schedule [20]. One subak is located upstream of the other, and so controls the flow of water. The subaks can adopt one of two possible cropping patterns, A and B (for example, A could represent planting dates for 1 January and 1 May, while B implies planting on 1 February and 1 June). The water supply is assumed to be adequate for both subaks if they stagger their cropping pattern. But if both plant at the same time, the downstream subak will experience water stress and its harvests will be somewhat reduced. Assume further that pest damage will be higher if plantings are staggered (because the pests can migrate from one field to the next), and lower if plantings are synchronized. Let p(0 , p , 1) represent the damage caused by the diffusion of pests between the fields, and w(0 , w , 1) represent the damage caused by water shortage. Given


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these assumptions, the pay-off matrix is as shown in table 2, where U and D designate the actions of the upstream and downstream subaks, respectively. In table 2, the first number in each cell is the pay-off for the upstream subak and the second is the pay-off for the downstream subak. For example, if both plant on schedule A, the pay-off for the upstream subak is 1, but it is 1 2 w for the downstream subak because of insufficient irrigation water. Several conclusions follow from this simple model. The upstream subaks are never affected by water stress, but their downstream neighbours may be. (This is known to rural sociologists as the ‘tail-ender’ problem: the farmers at the ‘tail end’ of an irrigation system are at the mercy of their neighbours upstream, who control the irrigation flow.) However, the upstream farmers do care about pest damage, because pests, unlike water, can often move upstream. So a strategy of synchronized cropping patterns to control pests will always produce higher yields for the upstream subaks. When p . w, the downstream player will also achieve higher yields by synchronizing. Note that if he does so, the aggregate harvest is higher (i.e. the total harvest for both farmers goes up). If p , w, the upstream farmer does better by staggered planting, which eliminates his water shortage. Interestingly, adding more pests to the fields until p . w actually increases the aggregate harvest for the pair of subaks, because it encourages the upstream farmer to cooperate in a synchronized schedule (even though he must give up some water). But, if the farmers are not worried about pests, the upstream player has no incentive to give up some of his water. Based on this logic, behaviour in accordance with the model may be predicted. In general, the downstreamers should prefer greater offsets in irrigation schedules, and be willing to accept higher losses from pests as a result, up to p . w. The upstreamers, meanwhile, should be willing to give up some of their water to enable the downstreamers to synchronize their irrigation schedule. Both then benefit from a coordinated fallow period, and consequently fewer pests. Put another way, the presence of pests in the ecosystem gives the downstream farmers a bargaining lever they can use to persuade their upstream neighbours to give them the water they need to avoid shortages. This analysis was subjected to two tests. First, we investigated whether the preferences predicted by the model are reflected in the views of the farmers. To that end, we conducted a survey of 150 farmers in 10 subaks. The results are consistent with the model: upstream farmers tend to worry about pests, while downstream farmers are more concerned about water shortages (table 2). Second, we explored the effects of these choices on the ecological processes defined by the model: irrigation flows and pest damage. To do so, we embedded the decision model in an ecological simulation of rice growth in 172 subaks located along two Balinese rivers, the Oos and Petanu (figure 2). This combined model simulates the effects of decisions about irrigation on the growth of rice and rice pests in the entire watershed. As time goes forward and selected patterns of irrigation schedules are implemented, local variation in rice harvests influences Phil. Trans. R. Soc. B (2011)

Oos

N Petanu catchment basin weir river irrigation canal subak water temple

Figure 2. Map of subaks in the simulation model of the Oos and Petanu rivers [21].

Table 2. Pay-offs for synchronized or unsynchronized irrigation schedules for upstream (U) and downstream (D) subaks.

UA UB

DA

DB

1, 1 2 w 12p, 1 2 p

12p, 1 2 p 1, 1 2 w

Table 3. Responses of 117 farmers in 10 subaks to the question, ‘which is worse, pest damage or water shortages?’, according to the location of their fields within the subak. Pearson x2 14.083, p , 0.001. location of farmer’s field

pest damage

water shortage

upper middle lower

20 8 7

18 29 35

future decisions by the farmers, creating a coupled human – natural system governed by feedback from the environment [22] (table 3). The 172 subaks that obtain water from the Oos and Petanu rivers are indicated by small squares in figures 2 and 3. At the beginning of each year, the artificial subaks in the model are randomly assigned a schedule of crops to plant for the next 12 months, which defines their irrigation needs. Then, based on historic rainfall data, the model simulates rainfall, river flow, crop growth and pest damage. Rainfall varies by season and elevation, and in combination with groundwater inflow determines river flow. Harvest yields may be reduced by water stress or pest infestations. Pest


Niche construction on Bali


Figure 3. Effects of increasing pest virulence on the synchronization of irrigation schedules in a simulation model of subaks along the Oos and Petanu rivers in Bali. Subaks are depicted by arbitrary symbols representing their cropping schedule for the year; for example a star could mean ‘plant rice in April and October’, a downward triangle ‘plant in March and August’. The outcomes reflect three levels of pest damage (p): low (left), current (middle) and high (right). As synchronized irrigation schedules expand, pest damage is reduced by effective fallowing, but water shortages increase [20].

population density in each field depends on dispersal from neighbouring fields, as well as growth in situ on locally available food. At the end of the year, harvests are tallied, and each subak selects its cropping schedule for the following year by comparing its harvest with those of k neighbouring subaks, and chooses the schedule that produced the best harvests. Through a process of trial and error, within a few years, subaks form different-sized clusters that share identical cropping patterns. These simulated groupings closely resemble the real clusters of subaks that coordinate their irrigation schedules via the water temple networks (about which more anon). The rate at which groupings of subaks appear, and their size, is determined by the relative magnitude of p and w. Figure 3 shows the effect of increasing p, the virulence of pests, on the expansion of synchronized irrigation schedules. If pests are not a factor, there is no need to synchronize harvests, and irrigation schedules are uncoordinated. But when crop losses to pests are high, subaks adapt by synchronizing their irrigation schedules with those of their neighbours, until their losses from water shortages exceed those owing to pests. The result is the aggregation of subaks into different-sized groups with identical cropping patterns. As these groups form, rice harvests improve and variance in harvest yields declines (figure 4). This model captures an evolving feedback relationship between the decisions of the subaks and the responses of the environment. As shown in figure 3, simple trial and error at the local level produces a patchwork of synchronized irrigation schedules, which over time improves harvests and also reduces variance in harvests. The reduction in variance is potentially significant, because large differences in harvests could discourage cooperation by farmers with suboptimal harvests. These simulated results are supported by responses from farmers to another question in the survey: 97 per cent stated that their own harvest is about the same as that of the other farmers in their subak [23]. Over time, incremental feedback learning becomes consolidated in the social norms of the subak institutions that encourage cooperation among farmers [24]. Phil. Trans. R. Soc. B (2011)

The formation of different-sized clusters of subaks practising synchronized cropping creates an ecological inheritance of modified selection pressures for descendant populations, and is thus consistent with a process of niche construction. A real-world test of the functional significance of the subak clusters began in the 1970s as an unintended consequence of changes in agricultural policy. At that time, the Asian Development Bank became involved in an effort to boost rice production in Indonesia. The Bank’s consultants saw two ways to improve harvests in Bali. The first was to encourage the farmers to grow higher yielding ‘Green Revolution’ rice varieties, which produce more grain than native Balinese rice. The second recommendation took advantage of another feature of the new rice: it grows faster than native rice. Consequently, the farmers could plant more frequently. The Ministry of Agriculture adopted both recommendations, and competitions were created to reward the farmers who produced the best harvests. By 1977, 70 per cent of the southern Balinese ricebowl was planted with Green Revolution rice, and subaks stopped coordinating their irrigation schedules. At first, rice harvests improved. But a year or two later, Balinese agricultural and irrigation workers began to report ‘chaos in water scheduling’ and ‘explosions of pest populations’. At the time, planners dismissed these occurrences as coincidence, and they urged the farmers to apply higher doses of pesticides, while still competing to grow as much rice per year as possible. This actually intensified both the pest problem [21,25] and water shortages [26]. It was only when farmers spontaneously returned to synchronized planting schemes that harvests began to recover, a point subsequently acknowledged by the final evaluation team from the Asian Development Bank: ‘Substitution of the “high technology and bureaucratic” solution in the event proved counter-productive, and was the major factor behind the yield and cropped area declines experienced between 1982 and 1985 . . . .The cost of the lack of appreciation of the merits of the traditional regime has been high’ [21]. Similar results can be achieved by running the simulation model in reverse: beginning the simulation


annual harvest of three rice crops (tons ha–1)

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J. S. Lansing & K. M. Fox Niche construction on Bali 30 25 20 15 10 5 0

1

6 simulated years

11

Figure 4. Reduction in variance of harvest yields as cooperation spreads in the simulation model of the Oos and Petanu watersheds. Rainfall, rice and pest parameters based on data collected in Lansing [21]. Thick line, mean yield.

with the evolved cluster patterns of subaks, and instructing the subaks to plant as often as possible. This quickly leads to the fragmentation of subak clusters, triggering increases in pests and water shortages.

4. SUBAKS AND WATER TEMPLES In the models described above, the role of conscious intention is limited to the readiness of adaptive agents to seek better harvests by imitating their neighbours. But in reality, more is required. Balinese irrigation systems consist of physically fragile tunnels, canals and aqueducts, which often extend for several kilometres, require constant maintenance and are vulnerable to water theft. While the models provide some insight into the functional structure of this system, they do not account for the high levels of cooperation, planning and social investment that are required to sustain it. Part of the answer lies in the secular institutions of the subaks. Subaks are self-governing assemblies of farmers, which hold regular meetings and assess fines on members who do not abide by their decisions. However, in surveys, farmers report that punitive fines and sanctions are seldom needed. From their perspective, the most important responsibility of the subaks is the performance of calendrical rites in water temples. By encouraging the farmer’s awareness of their shared dependence on Nature’s bounty, these rites clearly have functional significance. But they also raise a deeper question. Historically, the first references to water temples in royal inscriptions appear soon after the earliest mention of subaks (AD 1071). For example, an inscription provisionally dated to the twelfth century mentions ritual offerings from several subaks in the Sebatu region [18]. If the expansion of subaks and irrigation systems was closely linked to the spread of a specialized cult of water temples, did the process of niche construction encompass a historical evolution of religious consciousness? One way to approach this question is to ask whether the forms of worship in the water temples have diverged from other practices of Balinese religion. Phil. Trans. R. Soc. B (2011)

Beginning in the late first millennium AD, Balinese rulers established monasteries for both Hindu and Buddhist sects, which originated in India. But the rich mythologies of these foreign religions play virtually no part in the temple rituals, although they are well known to the Balinese from the literature and the performing arts [27]. In contrast to the fully scripted high gods patronized by the rulers, the water temple deities are mere ciphers, usually lacking any attributes beyond their names. Interestingly, in this respect, they resemble the agrarian gods of ancient Rome. The Romans, like the Balinese, imported an entire pantheon of foreign gods, like Zeus, Athena, Dionysius and Hephaestus. But while these deities became the pillars of the state religion, they are largely absent from the Roman countryside. As in Bali, the Roman gods worshipped in the annual calendar of agrarian rites lacked any personality or mode of existence except for instrumental names, which ‘imprisoned them’, as Dumezil observes, ‘in the minor definition of a function, in an act or a fraction of an act, gods like Sarritor (weeding), Occator (harrowing) and Messor (harvesting)’ [28]. Unlike both the Greek and Hindu gods, the imagined capacities of these agrarian temple deities do not exceed their named functions, and their mode of worship consists in the performance of calendrical rites, which provide a ritual template for agricultural labour. In the Balinese temple cult, the colourful and capricious personalities of the foreign gods are backgrounded in favour of the clockwork regularity of the temple rites and irrigation schedules. It is the farmers, rather than the gods, who thus assert control over their engineered landscape. This interpretation is consistent with the views of Cicero, who recognized these gods as personified abstractions: ‘what shall we say of Ops (fortune)? What of Salus (well-being)? Of Concordia, Libertas, Victoria? As each of these things has a power too great to be controlled without a god, it is the thing itself which has received the title of god’ [29].

5. DISCUSSION Unlike the evolution of lactose tolerance, the construction of the engineered landscape of Balinese rice terraces suggests an expanding role for conscious human agency. Some aspects of this process can be modelled within a Darwinian framework, but others cannot. A Darwinian perspective proved helpful in understanding the choices made by subaks, not because these choices are actually based on mere trial and error, but because they showed that trial and error is sufficient to allow the system to efficiently explore its space of possibilities. In the watershed-scale model, the key to the emergence of global functional structure is the ability of each subak to respond to local ecological feedback involving just two parameters, pests and water. This mathematical analysis might seem suspiciously simple, given the complexity of the Balinese agricultural landscape, but it received a measure of empirical support when government agricultural policies severed the local feedback channels, resulting in the almost instantaneous collapse of rice harvests.


Niche construction on Bali But a Darwinian perspective is less useful in understanding the principal tool used by the farmers to manage the ecology of the rice terraces: the agricultural calendar. This hybrid instrument grafts a permutational calendar of 10 concurrent weeks, which vary in duration from 1 to 10 days, to the ancient luni-solar Icaka calendar. The Balinese calendar enables groups of subaks to organize complex interlocking irrigation schedules, composed of varying combinations of water turns and planting schedules, and is the main instrument for irrigation management [21]. Over the centuries, the uses of this calendar have expanded to encompass many other phenomena besides irrigation, including musical notation and cosmology. The historical development of this concept of nested temporal cycles and its successive application to many aspects of the phenomenal world is not well captured by a Darwinian perspective. Instead, it appears to reflect what Hegel described as the desire of Reason to make the world congruent to itself. Thus, as Hegel observed, the human world is partly made up of ‘objectified ideas’ (buildings, technologies, laws and other products of mental activity). Evolution in the Hegelian sense occurs as the mind encounters its own creations. This process gathers historical momentum as the world appears to become more orderly and comprehensible. In Bali, the concept of nested cycles was extended to personal identity through the adoption of teknonyms (in which a person’s name changes at each step in the life cycle, as they become parents, grandparents and great-grandparents) and birth order names, which cycle from first to fourth born and then repeat (thus the same birth order name is used for the first and fifth born child in a family). Similarly, Balinese literature is full of references to temporal cycles, and the regularity of cyclical progressions is a major theme in Balinese literature. The consistent application of this abstract notion to so many aspects of the Balinese world contributed to a mental and physical landscape of pleasing harmonies and perceptible coherence, in which (to borrow again from Hegel) the workings of Reason appear to pervade the phenomenal world: ‘only then did they feel a real interest in the universe, when they recognized their own Reason in the Reason that pervaded it’ [30]. Should this sort of process be considered in the context of niche construction? We suggest that the answer is yes, if we are to account for phenomena like the engineered landscape of Balinese rice terraces and water temples. ‘In our universe’, writes the molecular biologist François Jacob in a Hegelian vein, ‘matter is arranged in a hierarchy of structures by successive integrations.’ Mind plays no role in the integrations achieved by ordinary Darwinian evolution, but it has tangible effects in human niche construction. Thus, to account for the adoption of innovations like dairying, dual inheritance theory invokes a minimal model of conscious choices. To account for the next hierarchical step—the origin of innovations—requires a less constrained view of mental activity. In Brian Arthur’s view, the growth of technologies is described as an evolutionary process: ‘the collective of technology builds itself from itself Phil. Trans. R. Soc. B (2011)


with the agency of human inventors and developers much as a coral reef builds itself from the activities of small organisms’ [31]. Something akin to Darwinian selection may be involved, he argues: ‘the many versions of a technology improve in small steps by the selection of better solutions to their internal design problems. But designers also improve technologies by deliberate efforts of their own, and invoking Darwin does not tell us how they do this’. To explain how technologies undergo what Arthur calls ‘structural deepening’ requires a further step, bringing us closer to Hegel: the active engagement of mind with its own products. Mere tinkering can explain how Balinese farmers engage with their calendars, names, musical compositions or irrigation schedules, but it cannot explain how their world comes to be experienced as a coherent and rational whole. To account for the role of mind at this level, we need to consider the emergence of meaningful patterns in social institutions. An example is Ju¨rgen Habermas’ theory of social learning. Following Hegel, Habermas emphasizes not the end product—the particular congeries of concepts that become dominant in a society—but rather the historical process by which social institutions facilitate or impede the spread of ideas and processes of social learning [32]. The question is, should we attempt to extend the concept of human niche construction to the very summit of Jacob’s hierarchy of integration? Or reserve it for cases that can be made to fit comfortably within a more straightforward biological framework, like dual inheritance theory? To the extent that human niche construction involves mental activity more complex than trial and error, it may become necessary to restore some older philosophers to the pantheon of evolutionary theorists. As the greatest Roman pastoral poet observed, ‘felix qui potuit cognoscere causas . . . fortunatus et ille deos qui nouit agrestis (it is well for one to understand causes . . . fortunate also to comprehend the gods of the countryside)’ [33]. This research was supported by the National Science Foundation, the James McDonnell Foundation Robustness programme at the Santa Fe Institute, the Yayasan Somia Pretiwi and the Eijkman Institute for Molecular Biology, Jakarta Indonesia. Permission for these studies was granted by the Indonesian Institute of Sciences. Genetic samples were obtained by J.S.L., Sang Kaler Surata and Tatiana M. Karafet with the assistance of Indonesian Public Health clinic staff, following protocols for the protection of human subjects established by both the Eijkman Institute and the University of Arizona Institutional Review Boards. The simulation model of irrigation along the Oos and Petanu rivers was developed by James N. Kremer and J.S.L.

ENDNOTE 1

Y-SNP, Y-STR and HVSI are neutral genetic markers used in phylogenetic analysis of genetic samples. Y-SNPs are single nucleotide polymorphisms on the Y chromosome; Y-STRs are short tandem repeats on the Y chromosome; HVSI is a hypervariable region in mtDNA used to track matrilineal ancestry.

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volume 366

. number 1566 . pages 783–934

Human niche construction Papers of a Theme issue compiled and edited by Jeremy R. Kendal, Jamshid J. Tehrani and John Odling-Smee Preface The entangled (and constructed) human bank E. Jablonka

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Introduction Human niche construction in interdisciplinary focus J. Kendal, J. J. Tehrani & J. Odling-Smee

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Articles Adaptation and niche construction in human prehistory: a case study from the southern Scandinavian Late Glacial F. Riede

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From hominins to humans: how sapiens became behaviourally modern K. Sterelny

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Runaway cultural niche construction L. Rendell, L. Fogarty & K. N. Laland

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Foraging and farming as niche construction: stable and unstable adaptations P. Rowley-Conwy & R. Layton

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Evolution of lactase persistence: an example of human niche construction P. Gerbault, A. Liebert, Y. Itan, A. Powell, M. Currat, J. Burger, D. M. Swallow & M. G. Thomas

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Gene–culture coevolution and the nature of human sociality H. Gintis

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Evolution of culture-dependent discriminate sociality: a gene–culture coevolutionary model Y. Ihara

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The influence of social niche on cultural niche construction: modelling changes in belief about marriage form in Taiwan M. Lipatov, M. J. Brown & M. W. Feldman

901

Property and wealth inequality as cultural niche construction S. Shennan

918

Niche construction on Bali: the gods of the countryside J. S. Lansing & K. M. Fox

927

Founded in 1660, the Royal Society is the independent scientific academy of the UK, dedicated to promoting excellence in science Registered Charity No 207043

rstb.royalsocietypublishing.org Published in Great Britain by the Royal Society, 6–9 Carlton House Terrace, London SW1Y 5AG

Human niche construction

General patterns of niche construction and the management of ‘wild’ plant and animal resources by small-scale pre-industrial societies B. D. Smith

Phil. Trans. R. Soc. B | vol. 366 no. 1566 pp. 783–934 | 27 Mar 2011

27 March 2011

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