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Ardipithecus ramidus Contents Introduction and Author List
Research Articles
5 Light on the Origin of Man
29 Ardipithecus ramidus and the Paleobiology of Early Hominids Tim D. White et al.
Editorial 9 Understanding Human Origins Bruce Alberts
News Focus 10 A New Kind of Ancestor: Ardipithecus Unveiled 14 Habitat for Humanity 15 The View From Afar
Authors’ Summaries 18 Ardipithecus ramidus and the Paleobiology of Early Hominids Tim D. White et al. 19 The Geological, Isotopic, Botanical, Invertebrate, and Lower Vertebrate Surroundings of Ardipithecus ramidus Giday WoldeGabriel et al. 20 Taphonomic, Avian, and Small-Vertebrate Indicators of Ardipithecus ramidus Habitat Antoine Louchart et al. 21 Macrovertebrate Paleontology and the Pliocene Habitat of Ardipithecus ramidus Tim D. White et al. 22 The Ardipithecus ramidus Skull and Its Implications for Hominid Origins Gen Suwa et al. 23 Paleobiological Implications of the Ardipithecus ramidus Dentition Gen Suwa et al. 24 Careful Climbing in the Miocene: The Forelimbs of Ardipithecus ramidus and Humans Are Primitive C. Owen Lovejoy et al. 25 The Pelvis and Femur of Ardipithecus ramidus: The Emergence of Upright Walking C. Owen Lovejoy et al. 26 Combining Prehension and Propulsion: The Foot of Ardipithecus ramidus C. Owen Lovejoy et al.
Credit: copyright T. White, 2008
27 The Great Divides: Ardipithecus ramidus Reveals the Postcrania of Our Last Common Ancestors with African Apes C. Owen Lovejoy et al. 28 Reexamining Human Origins in Light of Ardipithecus ramidus C. Owen Lovejoy
41 The Geological, Isotopic, Botanical, Invertebrate, and Lower Vertebrate Surroundings of Ardipithecus ramidus Giday Wolde Gabriel et al. 46 Taphonomic, Avian, and Small-Vertebrate Indicators of Ardipithecus ramidus Habitat Antoine Louchart et al. 50 Macrovertebrate Paleontology and the Pliocene Habitat of Ardipithecus ramidus Tim D. White et al. 57 The Ardipithecus ramidus Skull and Its Implications for Hominid Origins Gen Suwa et al. 64 Paleobiological Implications of the Ardipithecus ramidus Dentition Gen Suwa et al. 70 Careful Climbing in the Miocene: The Forelimbs of Ardipithecus ramidus and Humans Are Primitive C. Owen Lovejoy et al. 78 The Pelvis and Femur of Ardipithecus ramidus: The Emergence of Upright Walking C. Owen Lovejoy et al. 84 Combining Prehension and Propulsion: The Foot of Ardipithecus ramidus C. Owen Lovejoy et al. 92 The Great Divides: Ardipithecus ramidus Reveals the Postcrania of Our Last Common Ancestors with African Apes C. Owen Lovejoy et al. 99 Reexamining Human Origins in Light of Ardipithecus ramidus C. Owen Lovejoy
See also related video, Science Podcast at www.sciencemag.org/ardipithecus/
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introduction
Light on the Origin of Man Charles Darwin’s seminal work On the Origin of Species, published 150 years ago next month, contains just one understated sentence on the implications of his theory for human evolution: “Light will be thrown on the origin of man and his history.” As Darwin implied in his introduction to The Descent of Man, he felt that those implications were obvious; he appreciated, as events quickly showed, that it would be only natural to look at evolution foremost from our human perspective and contemplate what makes us unique among other primates—our large brains and ability to communicate, to create, and to understand and investigate our history and nature; our culture, society, and religion; the ability to run fast on two legs and manipulate tools; and more innovations that separate us from our primate relatives. Tracing our evolution and how we came to acquire these skills and traits, however, has been difficult. Genetic data now confirm that our closest living primate relative is the chimpanzee. We shared and evolved from a common ancestor some 6 million or more years ago. But identifying our unique genes and other genetic differences between us and our primate cousins does not reveal the nature of that ancestor, nor what factors led to the genetic changes that underlie our divergent evolutionary paths. That requires a fossil record and enough parts of past species to assess key anatomical details. It also requires knowing the habitat of early humans well, to determine their diet and evaluate what factors may have influenced their evolution through time. Many early human fossils have been found, but with a few exceptions, these are all less than 4 million years old. The key first several million years of human evolution have been poorly sampled or revealed. This issue presents 11 papers authored by a diverse international team (see following pages) describing an early hominid species, Ardipithecus ramidus, and its environment. The hominid fossils are 4.4 million years old, within this critical early part of human evolution, and represent 36 or more individuals, including much of the skull, pelvis, lower arms, and feet from one female. The papers represent three broad themes. Five focus on different parts of the anatomy that are revealing for human evolution. These show that Ardipithecus was at home both moving along trees on its palms and walking upright on the ground. Three characterize Ardipithecus’s habitat in detail, through analysis of the hosting rocks and thousands of fossils of small and large animals and plants. These show that Ardipithecus lived and ate in woodlands, not grasslands. The first paper presents an overview, and it and the last two papers trace early human evolution and synthesize a new view of our last common ancestor with chimps. One conclusion is that chimps have specialized greatly since then and thus are poor models for that ancestor and for understanding human innovations such as our ability to walk.
These papers synthesize an enormous amount of data collected and analyzed over decades by the authors. Because of the scope of these papers and the special broad interest in the topic of human evolution, we have expanded our usual format for papers and coverage. The papers include larger figures, tables, and discussions, and the overview and two concluding papers provide extended introductions and analyses. In addition, to aid understanding and introduce the main results of each paper, the authors provide a one-page summary of each paper, with an explanatory figure aimed at the general reader. Our News Focus section, written by Ann Gibbons, provides further analysis and coverage, and it includes maps and a portrait of the meticulous and at times grueling field research behind the discoveries. Available online are a video interview and a podcast with further explanations. To accommodate this material and allow the full papers, this print issue presents an Editorial, News coverage, the authors’ summaries, and four papers in full: the overview paper and one key paper from each thematic group above. The other research papers, and of course all content, are fully available online. In addition, a special online page (www.sciencemag.org/Ardipithecus/) links to several print and download packages of this material for AAAS members, researchers, educators, and other readers. This collection, essentially an extra issue of Science in length, reflects efforts by many behind the scenes. Every expert reviewer evaluated, and improved, multiple papers, and several commented on all 11 of them. The authors provided the summaries on top of an already large writing and revision effort. Paula Kiberstis helped in their editing. The figures and art were drafted and improved by J. H. Matternes, Henry Gilbert, Kyle Brudvik, and Josh Carlson, as well as Holly Bishop, Nathalie Cary, and Yael Kats at Science. Numerous other Science copyediting, proofreading, and production staff processed this content on top of their regular loads. Finally, special thanks go to the people of Ethiopia for supporting and facilitating this and other research into human origins over many years, and for curating Ardipithecus ramidus for future research and for all of us to admire. Ardipithecus ramidus thus helps us bridge the better-known, more recent part of human evolution, which has a better fossil record, with the scarcer early human fossils and older ape fossils that precede our last common ancestor. Ardipithecus ramidus is a reminder of Darwin’s conclusion of The Origin: There is grandeur in this view of life, with its several powers, having been originally breathed into a few forms or into one; and that, whilst this planet has gone cycling on according to the fixed law of gravity, from so simple a beginning endless forms most beautiful and most wonderful have been, and are being, evolved. – Brooks Hanson
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The Authors
Giday WoldeGabriel Earth Environmental Sciences Division, Los Alamos National Laboratory, Los Alamos, NM 87545, USA. Antoine Louchart UMR 5125 PEPS CNRS, France, Université Lyon 1, 69622 Villeurbanne Cedex, France, and Institut de Génomique Fonctionnelle de Lyon, Université de Lyon, Université Lyon 1, CNRS, INRA, Ecole Normale Supérieure de Lyon, France. Gen Suwa The University Museum, the University of Tokyo, Hongo, Bunkyo-ku, Tokyo 113-0033, Japan.
C. Owen Lovejoy Department of Anthropology, School of Biomedical Sciences, Kent State University, Kent, OH 44240–0001, USA.
Stanley H. Ambrose Department of Anthropology, University of Illinois, Urbana, IL 61801, USA.
Berhane Asfaw Rift Valley Research Service, P.O. Box 5717, Addis Ababa, Ethiopia.
Doris Barboni CEREGE (UMR6635 CNRS/Université Aix-Marseille), BP80, F-13545 Aix-en-Provence Cedex 4, France. Raymond L. Bernor National Science Foundation, GEO:EAR:SEPS Sedimentary Geology and Paleobiology Program, Arlington, VA 22230, and College of Medicine, Department of Anatomy, Laboratory of Evolutionary Biology, Howard University, 520 W St., Washington, DC 20059, USA.
Michel Brunet Collège de France, Chaire de Paléontologie Humaine, 3 Rue d’Ulm, F-75231 Paris Cedex 05, France.
Brian Currie Department of Geology, Miami University, Oxford, OH 45056, USA.
Yonas Beyene Department of Anthropology and Archaeology, Authority for Research and Conservation of the Cultural Heritage, Ministry of Youth, Sports and Culture, P.O. Box 6686, Addis Ababa, Ethiopia. Michael T. Black Phoebe A. Hearst Museum of Anthropology, 103 Kroeber Hall, no. 3712, University of California Berkeley, Berkeley, CA 94720–3712, USA. Robert J. Blumenschine Center for Human Evolutionary Studies, Department of Anthropology, Rutgers University, 131 George St., New Brunswick, NJ 08901–1414, USA. Jean-Renaud Boisserie Paléobiodiversité et Paléoenvironnements, UMR CNRS 5143, USM 0203, Muséum National d’Histoire Naturelle, 8 Rue Buffon, CP 38, 75231 Paris Cedex 05, France, and Institut de Paléoprimatologie et Paléontologie Humaine, Évolution et Paléoenvironnements, UMR CNRS 6046, Université de Poitiers, 40 Avenue du Recteur-Pineau, 86022 Poitiers Cedex, France.
Mesfin Asnake Ministry of Mines and Energy, P.O. Box 486, Addis Ababa, Ethiopia.
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Laurent Bremond Center for Bio-Archaeology and Ecology (UMR5059 CNRS/Université Montpellier 2/EPHE), Institut de Botanique, F-34090 Montpellier, France.
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Raymonde Bonnefille CEREGE (UMR6635 CNRS/Université AixMarseille), BP80, F-13545 Aix-en-Provence Cedex 4, France.
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David DeGusta Department of Anthropology, Stanford University, Stanford, CA 94305–2034, USA.
Eric Delson Department of Anthropology, Lehman College/CUNY, Bronx, NY 10468; NYCEP; and Department of Vertebrate Paleontology, American Museum of Natural History; New York, NY 10024, USA. Stephen Frost Department of Anthropology, University of Oregon, Eugene, OR, 97403–1218, USA.
Nuria Garcia Dept. Paleontología, Universidad Complutense de Madrid & Centro de Evolución y Comportamiento Humanos, ISCIII, C/ Sinesio Delgado 4, Pabellón 14, 28029 Madrid, Spain. Ioannis X. Giaourtsakis Ludwig Maximilians University of Munich, Department of Geo- and Environmental Sciences, Section of Paleontology. Richard-Wagner-Strasse 10, D-80333 Munich, Germany.
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CREDITS: PHOTOS COURTESY OF THE AUTHORS
Tim D. White Human Evolution Research Center and Department of Integrative Biology, 3101 Valley Life Sciences Building, University of California at Berkeley, Berkeley, CA 94720, USA.
SPECIALSECTION Yohannes Haile-Selassie Department of Physical Anthropology, Cleveland Museum of Natural History, 1 Wade Oval Drive, Cleveland, OH 44106, USA.
Thomas Lehmann Senckenberg Forschungsinstitut, Senckenberganlage 25, D-60325 Frankfurt am Main, Germany.
Gina Semprebon Science and Mathematics, Bay Path College, 588 Longmeadow St., Longmeadow, MA 01106, USA.
William K. Hart Department of Geology, Miami University, Oxford, OH 45056, USA.
Andossa Likius Département de Paléontologie, Université de N’Djamena, BP 1117, N’Djamena, Chad.
Scott W. Simpson Department of Anatomy, Case Western Reserve University School of Medicine, Cleveland, OH 44106–4930, USA.
Jay H. Matternes 4328 Ashford Lane, Fairfax, VA 22032, USA.
Linda Spurlock Cleveland Museum of Natural History, Cleveland, OH 44106–4930, USA.
Alison M. Murray Department of Biological Sciences, University of Alberta, Edmonton AB T6G2E9, Canada.
Kathlyn M. Stewart Paleobiology, Canadian Museum of Nature, Ottawa, K1P 6P4, Canada.
Leslea J. Hlusko Human Evolution Research Center and Department of Integrative Biology, University of California at Berkeley, 3010 Valley Life Sciences Building, Berkeley, CA, 94720, USA. F. Clark Howell Human Evolution Research Center and Department of Anthropology, 3101 Valley Life Sciences Building, University of California at Berkeley, Berkeley, CA 94720, USA (deceased). M. C. Jolly-Saad Université Paris-Ouest La Défense, Centre Henri Elhaï, 200 Avenue de la République, 92001 Nanterre, France. Reiko T. Kono Department of Anthropology, National Museum of Nature and Science, Hyakunincho, Shinjuku-ku, Tokyo, 169-0073, Japan.
CREDITS: PHOTOS COURTESY OF THE AUTHORS
Daisuke Kubo Department of Biological Sciences, Graduate School of Science, the University of Tokyo, Tokyo, 113-0033, Japan.
Jackson K. Njau Human Evolution Research Center and Department of Integrative Biology, University of California at Berkeley, 3010 Valley Life Sciences Building, Berkeley, CA, 94720, USA. Cesur Pehlevan University of Yuzuncu Yil, Department of Anthropology, The Faculty of Science and Letters, Zeve Yerlesimi 65080 Van, Turkey.
Denise F. Su Department of Anthropology, The Pennsylvania State University, University Park, PA 16802, USA.
Mark Teaford Center for Functional Anatomy and Evolution, Johns Hopkins University School of Medicine, 1830 E. Monument St., Room 303, Baltimore, MD 21205.
Paul R. Renne Berkeley Geochronology Center, 2455 Ridge Road, Berkeley, CA 94709, and Department of Earth and Planetary Science, University of California at Berkeley, Berkeley, CA 94720, USA.
Bruce Latimer Department of Anatomy, Case Western Reserve University School of Medicine, Cleveland, OH 44106–4930, USA.
www.sciencemag.org
Haruo Saegusa Institute of Natural and Environmental Sciences, University of Hyogo, Yayoigaoka, Sanda 669-1546, Japan.
SCIENCE
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Elisabeth Vrba Department of Geology and Geophysics, Yale University, New Haven, CT 06520, USA.
Henry Wesselman P.O. Box 369, Captain Cook, Hawaii, 96704, USA.
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EDITORIAL
Understanding Human Origins RESPONDING TO A QUESTION ABOUT HIS SOON-TO-BE-PUBLISHED ON THE ORIGIN OF SPECIES,
CREDITS: (TOP) TOM KOCHEL; (RIGHT) ISTOCKPHOTO.COM
Bruce Alberts is Editorin-Chief of Science.
Charles Darwin wrote in 1857 to Alfred Russel Wallace, “You ask whether I shall discuss ‘man’; I think I shall avoid the whole subject, as so surrounded with prejudices, though I freely admit that it is the highest and most interesting problem for the naturalist.” Only some 14 years later, in The Descent of Man, did Darwin address this “highest problem” head-on: There, he presciently remarked in his introduction that “It has often and confidently been asserted, that man’s origin can never be known: but . . . it is those who know little, and not those who know much, who so positively assert that this or that problem will never be solved by science.” Darwin was certainly right. The intervening years provide conclusive evidence that it is very unwise to predict limits for what can be discovered through science. In fact, it now seems likely that, through synergistic advances in many disciplines, scientists will eventually decipher a substantial portion of the detailed evolutionary history of our own species at both the morphological and molecular levels. First, what can we expect from paleoanthropology? In this 200th anniversary year of Darwin’s birth, Science is pleased to publish the results of many years of scientific research that suggest an unexpected form for our last common ancestor with chimpanzees. This issue contains 11 Research Articles involving more than 40 authors, plus News articles that describe the life and times of Ardipithecus ramidus, a hominid species that lived 4.4 million years ago in the Afar Rift region of northeastern Ethiopia. This region exposes a total depth of 300 meters of sediments that were deposited in rivers, lakes, and floodplains between about 5.5 and 3.8 million years ago. Even considering only this one site (there are many others), it is staggering to reflect on the huge number of hominid remains that can in principle be discovered, given sufficient time and effort. Moreover, the history of science assures us that powerful new techniques will be developed in the coming years to accelerate such research, as they have been in the past. We can thus be certain that scientists will eventually obtain a rather detailed record showing how the anatomy of the human body evolved over many millions of years. What can we expect from a combination of genetics, genomics, biochemistry, and comparative organismal biology? We will want to interpret the history of the morphological transformations in the humanoid skeleton and musculature in terms of the molecular changes in the DNA that caused them. Genes and their regulatory regions control the morphology of animals through very complex biochemical processes that affect cell behavior during embryonic development. Nevertheless, experimental studies of model organisms such as fruit flies, worms, fish, and mice are advancing our understanding of the molecular mechanisms involved. New inexpensive methods for deciphering the complete genome sequence of any organism will soon accelerate this process, allowing scientists to analyze the recurring evolutionary morphological transformations that have been identified by organismal biologists,* so as to determine the specific DNA changes involved. And the DNA sequences that have changed most rapidly during recent human evolution are being cataloged, providing a new tool for finding important molecular differences that distinguish us from chimpanzees.† The majesty of the discoveries already made represents a major triumph of the human intellect. And, as emphasized here, there will be many more discoveries to come. Darwin’s summary of his own efforts to understand human evolution is thus still relevant today: “Man may be excused for feeling some pride at having risen, though not through his own exertions, to the very summit of the organic scale; and the fact of his having thus risen, instead of having been aboriginally placed there, may give him hope for a still higher destiny – Bruce Alberts in the distant future.” 10.1126/science.1182387
*R. L. Mueller et al., Proc. Natl. Acad. Sci. U.S.A. 101, 3820 (2004). †S. Prabhakar et al., Science 314, 786 (2006).
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NEWSFOCUS
A New Kind of Ancestor: Ardipithecus Unveiled The oldest known hominin skeleton reveals the body plan of our very early ancestors and the upright origins of humankind
From the inside out. Artist’s reconstructions show how Ardi’s skeleton, muscles, and body looked and how she would have moved on top of branches.
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CREDITS: ILLUSTRATIONS © 2009, J. H. MATTERNES
Every day, scientists add new pages to the story of human evolution by deciphering clues to our past in everything from the DNA in our genes to the bones and artifacts of thousands of our ancestors. But perhaps once each generation, a spectacular fossil reveals a whole chapter of our prehistory all at once. In 1974, it was the famous 3.2-million-year-old skeleton “Lucy,” who proved in one stroke that our ancestors walked upright before they evolved big brains. Ever since Lucy’s discovery, researchers have wondered what came before her. Did the earliest members of the human family walk upright like Lucy or on their knuckles like chimpanzees and gorillas? Did they swing through the trees or venture into open grasslands? Researchers have had only partial, fleeting glimpses of Lucy’s own ancestors—the earliest hominins, members of the group that includes humans and our ancestors (and are sometimes called hominids). Now, in a special section beginning on page 60 and online, a multidisciplinary international team presents the oldest known skeleton of a potential human ancestor, 4.4-million-year-old Ardipithecus ramidus from Aramis, Ethiopia. This remarkably rare skeleton is not the oldest putative hominin, but it is by far the most complete of the earliest specimens. It includes most of the skull and teeth, as well as the pelvis, hands, and feet—parts that the authors say reveal an “intermediate” form of upright walking, consid-
Ardipithecus Ardipithecus ramidus ramidusNEWSFOCUS NEWSFOCUS ered ered a hallmark a hallmark of hominins. of hominins. “We “We thought thought LucyLucy was the wasfind the find of the of the “The“The authors authors … are …framing are framing the debate the debate that will that will inevitably inevitably follow,” follow,” century century but, in but, retrospect, in retrospect, it isn’t,” it isn’t,” says says paleoanthropologist paleoanthropologist Andrew Andrew because because the description the description and interpretation and interpretation of theoffinds the finds are entwined, are entwined, Hill of Hill Yale of Yale University. University. “It’s “It’s worth worth the wait.” the wait.” says says Pilbeam. Pilbeam. “My“My first first reaction reaction is to is betoskeptical be skeptical aboutabout somesome of theof the To some To some researchers’ researchers’ surprise, surprise, the female the female skeleton skeleton doesn’t doesn’t looklook conclusions,” conclusions,” including including that human that human ancestors ancestors nevernever wentwent through through a a muchmuch like alike chimpanzee, a chimpanzee, gorilla, gorilla, or any or of anyour ofclosest our closest livingliving primate primate chimpanzee-like chimpanzee-like phase. phase. Other Other researchers researchers are focusing are focusing intently intently on on relatives. relatives. EvenEven though though this species this species probably probably livedlived soonsoon afterafter the dawn the dawn the lower the lower skeleton, skeleton, where where somesome of the ofanatomy the anatomy is soisprimitive so primitive that that of humankind, of humankind, it was it was not transitional not transitional between between African African apesapes and and they they are beginning are beginning to argue to argue over over just what just what it means it means to beto“bipedal.” be “bipedal.” humans. humans. “We “We havehave seen seen the ancestor, the ancestor, and itand is not it isanot chimpanzee,” a chimpanzee,” says says The The pelvis, pelvis, for example, for example, offers offers onlyonly “circumstantial” “circumstantial” evidence evidence for for paleoanthropologist paleoanthropologist Tim White Tim White of theofUniversity the University of California, of California, BerkeBerkeupright upright walking, walking, says says Walker. Walker. But however But however the debate the debate aboutabout Ardi’s Ardi’s ley, co-director ley, co-director of theofMiddle the Middle Awash Awash research research group, group, which which discovered discovered locomotion locomotion and identity and identity evolves, evolves, she provides she provides the first the first hardhard evidence evidence and analyzed and analyzed the fossils. the fossils. that that will will inform inform and constrain and constrain future future ideasideas Instead, Instead, the skeleton the skeleton and pieces and pieces of at of least at least 35 additional 35 additional individuals individuals aboutabout the ancient the ancient hominin hominin bauplan. bauplan. of Ar.oframidus Ar. ramidus reveal reveal a new a new type type of early of early hominin hominin that was that was neither neither Digging it it chimpanzee chimpanzee nor human. nor human. Although Although the team the team suspects suspects that Ar. thatramidus Ar. ramidussciencemag.org sciencemag.org Digging may may havehave givengiven rise to riseLucy’s to Lucy’s genus, genus, Australopithecus, Australopithecus, the fossils the fossils The first The first glimpse glimpse of this ofstrange this strange creature creature camecame Podcast Podcast interview interview “show “show for the forfirst the first time time that there that there is some is some new new evolutionary evolutionary gradegrade of of on 17onDecember 17 December 19921992 whenwhen a former a former graduate graduate with author with author hominid hominid that isthat notisAustralopithecus, not Australopithecus, that isthat notisHomo,” not Homo,” says says paleontolpaleontol-Ann Gibbons student student of White’s, of White’s, Gen Gen Suwa, Suwa, saw saw a glint a glint Ann Gibbons on on Ardipithecus Ardipithecus and and ogistogist Michel Michel Brunet Brunet of theofCollege the College de France de France in Paris. in Paris. among among the pebbles the pebbles of the of desert the desert pavement pavement fieldwork in theinAfar. the Afar. near near In 11Inpapers 11 papers published published in this in issue this issue and online, and online, the team the team of 47of 47fieldwork the village the village of Aramis. of Aramis. It was It the waspolished the polished researchers researchers describes describes how how Ar. ramidus Ar. ramidus looked looked and moved. and moved. The skeleThe skelesurface surface of a of tooth a tooth root,root, and he andimmediately he immediately ton, ton, nicknamed nicknamed “Ardi,” “Ardi,” is from is from a female a female who who livedlived in a in woodland a woodland knewknew it wasit awas hominin a hominin molar. molar. OverOver the next the next few days, few days, the team the team scoured scoured (see (see sidebar, sidebar, p. 40), p. 40), stoodstood aboutabout 120 centimeters 120 centimeters tall, tall, and weighed and weighed the area the area on hands on hands and knees, and knees, as they as they do whenever do whenever an important an important piecepiece aboutabout 50 kilograms. 50 kilograms. She was She thus was thus as big asas biga chimpanzee as a chimpanzee and had and ahad of a hominin of hominin is found is found (see story, (see story, p. 41), p. and 41), collected and collected the lower the lower jaw of jaw a of a brainbrain size size to match. to match. But she But did shenot didknuckle-walk not knuckle-walk or swing or swing through through childchild with with the milk the milk molarmolar still attached. still attached. The molar The molar was so was primitive so primitive that that the trees the trees like living like living apes.apes. Instead, Instead, she walked she walked upright, upright, planting planting her her the team the team knewknew they they had found had found a hominin a hominin both both olderolder and more and more primitive primitive feet flat feeton flatthe onground, the ground, perhaps perhaps eating eating nuts,nuts, insects, insects, and small and small mammamthan than Lucy.Lucy. Yet the Yetjaw thealso jaw had alsoderived had derived traits—novel traits—novel evolutionary evolutionary char-charmalsmals in theinwoods. the woods. acters—shared acters—shared withwith Lucy’s Lucy’s species, species, Au. afarensis, Au. afarensis, suchsuch as anasupper an upper She was She awas “facultative” a “facultative” biped, biped, say the sayauthors, the authors, still living still living in both in both canine canine shaped shaped like alike diamond a diamond in side in view. side view. worlds—upright worlds—upright on the onground the ground but also but also able able to move to move on allonfours all fours on on The The teamteam reported reported 15 years 15 years ago in agoNature in Nature that that the fragmentary the fragmentary top of top branches of branches in theintrees, the trees, with with an opposable an opposable big toe bigtotoe grasp to grasp limbs. limbs. fossils fossils belonged belonged to the to“long-sought the “long-sought potential potential root root species species for the for the “These “These things things werewere veryvery odd odd creatures,” creatures,” says says paleoanthropologist paleoanthropologist Hominidae.” Hominidae.” (They (They first first called called it Au.it ramidus, Au. ramidus, then,then, afterafter finding finding AlanAlan Walker Walker of Pennsylvania of Pennsylvania StateState University, University, University University Park.Park. “You“You partsparts of the ofskeleton, the skeleton, changed changed it to it Ar.toramidus—for Ar. ramidus—for the Afar the Afar words words knowknow whatwhat Tim Tim [White] [White] onceonce said:said: If you If wanted you wanted to find to find something something for “root” for “root” and “ground.”) and “ground.”) In response In response to comments to comments that he thatneeded he needed leg leg that moved that moved like these like these things, things, you’dyou’d havehave to gototogo thetobar theinbar Star in Wars.” Star Wars.” bones bones to prove to prove Ar. ramidus Ar. ramidus was an wasupright an upright hominin, hominin, White White jokedjoked that that MostMost researchers, researchers, who who havehave waited waited 15 years 15 years for the forpublication the publication of of he would he would be delighted be delighted withwith moremore parts,parts, specifically specifically a thigh a thigh and an and an this find, this find, agreeagree that Ardi that Ardi is indeed is indeed an early an early hominin. hominin. TheyThey praise praise the the intactintact skull,skull, as though as though placing placing an order. an order. detailed detailed reconstructions reconstructions needed needed to piece to piece together together the crushed the crushed bones. bones. Within Within 2 months, 2 months, the team the team delivered. delivered. In November In November 1994,1994, as theasfosthe fos“This“This is anisextraordinarily an extraordinarily impressive impressive workwork of reconstruction of reconstruction and and sil hunters sil hunters crawled crawled up anupembankment, an embankment, Berkeley Berkeley graduate graduate student student description, description, well well worth worth waiting waiting for,” for,” says says paleoanthropologist paleoanthropologist David David Yohannes Yohannes Haile-Selassie Haile-Selassie of Ethiopia, of Ethiopia, now now a paleoanthropologist a paleoanthropologist at theat the Pilbeam Pilbeam of Harvard of Harvard University. University. “They “They did this did job thisvery, job very, veryvery well,” well,” Cleveland Cleveland Museum Museum of Natural of Natural History History in Ohio, in Ohio, spotted spotted two pieces two pieces of a of a agrees agrees neurobiologist neurobiologist Christoph Christoph Zollikofer Zollikofer of the of University the University of of bonebone fromfrom the palm the palm of a hand. of a hand. ThatThat was soon was soon followed followed by pieces by pieces of a of a Zurich Zurich in Switzerland. in Switzerland. pelvis; pelvis; leg, ankle, leg, ankle, and foot and foot bones; bones; manymany of theofbones the bones of theofhand the hand and and But not Buteveryone not everyone agrees agrees withwith the team’s the team’s interpretations interpretations aboutabout how how arm;arm; a lower a lower jaw with jaw with teeth—and teeth—and a cranium. a cranium. By January By January 1995,1995, it wasit was Ar. ramidus Ar. ramidus walked walked upright upright and what and what it reveals it reveals aboutabout our ancestors. our ancestors. apparent apparent that they that they had made had made the rarest the rarest of rare of finds, rare finds, a partial a partial skeleton. skeleton. CREDITS: (LEFT) C. O. LOVEJOY ET AL., SCIENCE; (TOP) G. SUWA ET AL., SCIENCE; (BOTTOM) C. O. LOVEJOY ET AL., SCIENCE; (RIGHT) C. O. LOVEJOY ET AL., SCIENCE
CREDITS: (LEFT) C. O. LOVEJOY ET AL., SCIENCE; (TOP) G. SUWA ET AL., SCIENCE; (BOTTOM) C. O. LOVEJOY ET AL., SCIENCE; (RIGHT) C. O. LOVEJOY ET AL., SCIENCE
Online Online
Unexpected Unexpected anatomy. anatomy. Ardi has Ardianhas opposable an opposable toe (left) toe (left) and flexible and flexible hand hand (right); (right); her canines her canines (top center) (top center) are sized are sized between between thosethose of a human of a human (top left) (topand left)chimp and chimp (top right); (top right); and the andblades the blades of herofpelvis her pelvis (lower(lower left) are left)broad are broad like Lucy’s like Lucy’s (yellow). (yellow).
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NEWSFOCUS NEWSFOCUS Ardipithecus Ardipithecusramidus ramidus FOSSILS FOSSILSOFOFTHE THEHUMAN HUMANFAMILY FAMILY
H. H. floresiensis floresiensis
HOMO HOMO
Indonesia Indonesia
H. H. heidelbergensis heidelbergensis Europe Europe
Kenyanthropus Kenyanthropus platyops? platyops? Kenya Kenya
H. H. habilis habilis H. H. erectus erectus
Sub-Saharan Sub-Saharan Africa Africa andand AsiaAsia Africa Africa
SAHELANTHROPUS SAHELANTHROPUS AUSTRALOPITHECUS AUSTRALOPITHECUS Ar.Ar. ramidus ramidus
Ethiopia Ethiopia
Ardi Ardi Ethiopia, Ethiopia, Kenya Kenya
Ethiopia Ethiopia
Kenya, Kenya, Ethiopia Ethiopia
Au.Au. africanus africanus Au.Au. robustus robustus Taung Taung Child Child South South Africa Africa
South South Africa Africa
Au.Au. bahrelghazali bahrelghazali ? ?
O. O. tugenensis tugenensis
Au.Au. boisei boisei Eastern Eastern Africa Africa 2 2
4 4
5 5
3 3
Abel Abel Chad Chad Au.Au. aethiopicus aethiopicus Eastern Eastern Africa Africa
Millennium Millennium Man Man Kenya Kenya 6 6
Worldwide Worldwide
Eastern Eastern Africa Africa
Au.Au. afarensis afarensis Lucy Lucy Ethiopia, Ethiopia, Tanzania Tanzania
ORRORIN ORRORIN
Pliocene Pliocene Epoch Epoch
H. H. sapiens sapiens
? ? Au.Au. rudolfensis rudolfensis
Pleistocene Pleistocene Epoch Epoch
Today Today
Ar.Ar. kadabba kadabba
Toumaï Toumaï Chad Chad
7 Million Years Ago 7 Million Years Ago
S. tchadensis S. tchadensis
Miocene Miocene Epoch Epoch
Au.Au. garhi garhi
Au.Au. anamensis anamensis
Europe Europe andand AsiaAsia
1 Million Years Ago 1 Million Years Ago
ARDIPITHECUS ARDIPITHECUS
H. H. neanderthalensis neanderthalensis
Holocene Holocene Epoch Epoch
CREDITS: (TIMELINE LEFT TO RIGHT) L. PÉRON/WIKIPEDIA, B. G. RICHMOND ET AL., SCIENCE 319, 1662 (2008); © T. WHITE 2008; WIKIPEDIA; TIM WHITE; TIM WHITE; (PHOTO) D. BRILL
It It is is one one ofof only only a half-dozen a half-dozen such such skeletons skeletons known known from from more more than than onon thethe task. task. “You “You gogo piece piece byby piece.” piece.” 1 million 1 million years years ago, ago, and and thethe only only published published one one older older than than Lucy. Lucy. Once Once hehe had had reassembled reassembled thethe pieces pieces in in a digital a digital reconstruction, reconstruction, hehe It was It was thethe find find ofof a lifetime. a lifetime. But But thethe team’s team’s excitement excitement was was tempered tempered and and paleoanthropologist paleoanthropologist Berhane Berhane Asfaw Asfaw ofof thethe Rift Rift Valley Valley Research Research byby thethe skeleton’s skeleton’s terrible terrible condition. condition. The The bones bones literally literally crumbled crumbled when when Service Service in in Addis Addis Ababa Ababa compared compared thethe skull skull with with those those ofof ancient ancient and and touched. touched. White White called called it road it road kill. kill. And And parts parts ofof thethe skeleton skeleton had had been been living living primates primates in in museums museums worldwide. worldwide. ByBy March March ofof this this year, year, Suwa Suwa trampled trampled and and scattered scattered into into more more than than 100 100 fragments; fragments; thethe skull skull was was was was satisfied satisfied with with hishis 10th 10th reconstruction. reconstruction. Meanwhile Meanwhile in in Ohio, Ohio, crushed crushed to to 4 centimeters 4 centimeters in in height. height. The The researchers researchers decided decided to to remove remove Lovejoy Lovejoy made made physical physical models models ofof thethe pelvic pelvic pieces pieces based based onon thethe origorigentire entire blocks blocks ofof sediment, sediment, covering covering thethe blocks blocks in in plaster plaster and and moving moving inal inal fossil fossil and and thethe CTCT scans, scans, working working closely closely with with Suwa. Suwa. HeHe is also is also satsatthem them to to thethe National National Museum Museum ofof isfied isfied that that thethe 14th 14th version version ofof thethe Ethiopia Ethiopia in in Addis Addis Ababa Ababa to to finish finish pelvis pelvis is is accurate. accurate. “There “There was was anan excavating excavating thethe fossils. fossils. Ardipithecus Ardipithecus that that looked looked just just like like It It took took three three field field seasons seasons to to that,” that,” hehe says, says, holding holding upup thethe final final uncover uncover and and extract extract thethe skeleton, skeleton, model model in in hishis lab. lab. repeatedly repeatedly crawling crawling thethe site site toto Putting Putting their their heads heads together together gather gather 100% 100% ofof thethe fossils fossils prespresent. ent. AtAt last last count, count, thethe team team had had AsAs they they examined examined Ardi’s Ardi’s skull, skull, cataloged cataloged more more than than 110 110 specispeciSuwa Suwa and and Asfaw Asfaw noted noted a number a number mens mens ofof Ar.Ar. ramidus, ramidus, notnot to to menmenofof characteristics. characteristics. Her Her lower lower face face tion tion 150,000 150,000 specimens specimens ofof fossil fossil had had a muzzle a muzzle that that juts juts outout less less than than plants plants and and animals. animals. “This “This team team a chimpanzee’s. a chimpanzee’s. The The cranial cranial base base is is seems seems to to suck suck fossils fossils outout ofof thethe short short from from front front to to back, back, indicatindicatearth,” earth,” says says anatomist anatomist C.C. Owen Owen inging that that herher head head balanced balanced atop atop thethe Lovejoy Lovejoy ofof Kent Kent State State University University spine spine asas in in later later upright upright walkers, walkers, in in Ohio, Ohio, who who analyzed analyzed thethe postpost- Fossil rather than than to to thethe front front ofof thethe spine, spine, Fossil finders. finders. TimTim White White and and local local Afar Afar fossil fossil hunters hunters pool pool their their finds finds after after rather scouring thethe hillside hillside at Aramis. at Aramis. cranial cranial bones bones butbut didn’t didn’t work work in in scouring asas in in quadrupedal quadrupedal apes. apes. Her Her face face is is thethe f ield. f ield. InIn thethe lab, lab, hehe gently gently in in a more a more vertical vertical position position than than in in unveils unveils a cast a cast ofof a tiny, a tiny, pea-sized pea-sized sesamoid sesamoid bone bone forfor effect. effect. “Their “Their chimpanzees. chimpanzees. And And herher teeth, teeth, like like those those ofof allall later later hominins, hominins, lack lack thethe obsessiveness obsessiveness gives gives you—this!” you—this!” daggerlike daggerlike sharpened sharpened upper upper canines canines seen seen in in chimpanzees. chimpanzees. The The team team White White himself himself spent spent years years removing removing thethe silty silty clay clay from from thethe fragile fragile realized realized that that this this combination combination ofof traits traits matches matches those those ofof anan even even older older fossils fossils at at thethe National National Museum Museum in in Addis Addis Ababa, Ababa, using using brushes, brushes, skull, skull, 6-million 6-million to to 7-million-year-old 7-million-year-old Sahelanthropus Sahelanthropus tchadensis, tchadensis, syringes, syringes, and and dental dental tools, tools, usually usually under under a microscope. a microscope. Museum Museum techtech- found found byby Brunet’s Brunet’s team team in in Chad. Chad. They They conclude conclude that that both both represent represent anan nician nician Alemu Alemu Ademassu Ademassu made made a precise a precise cast cast ofof each each piece, piece, and and thethe early early stage stage ofof human human evolution, evolution, distinct distinct from from both both Australopithecus Australopithecus and and team team assembled assembled them them into into a skeleton. a skeleton. chimpanzees. chimpanzees. “Similarities “Similarities with with Sahelanthropus Sahelanthropus areare striking, striking, in in that that it it Meanwhile Meanwhile in in Tokyo Tokyo and and Ohio, Ohio, Suwa Suwa and and Lovejoy Lovejoy made made virtual virtual also also represents represents a first-grade a first-grade hominid,” hominid,” agrees agrees Zollikofer, Zollikofer, who who diddid aa reconstructions reconstructions ofof thethe crushed crushed skull skull and and pelvis. pelvis. Certain Certain fossils fossils were were three-dimensional three-dimensional reconstruction reconstruction ofof that that skull. skull. taken taken briefly briefly to to Tokyo Tokyo and and scanned scanned with with a custom a custom micro–computed micro–computed Another, Another, earlier earlier species species ofof Ardipithecus—Ar. Ardipithecus—Ar. kadabba, kadabba, dated dated tomography tomography (CT) (CT) scanner scanner that that could could reveal reveal what what was was hidden hidden inside inside thethe from from 5.55.5 million million to to 5.85.8 million million years years ago ago butbut known known only only from from teeth teeth bones bones and and teeth. teeth. Suwa Suwa spent spent 9 years 9 years mastering mastering thethe technology technology to to and and bits bits and and pieces pieces ofof skeletal skeletal bones—is bones—is part part ofof that that grade, grade, too. too. And And reassemble reassemble thethe fragments fragments ofof thethe cranium cranium into into a virtual a virtual skull. skull. “I “I used used 6565 Ar.Ar. kadabba’s kadabba’s canines canines and and other other teeth teeth seem seem to to match match those those ofof a third a third pieces pieces ofof thethe cranium,” cranium,” says says Suwa, Suwa, who who estimates estimates hehe spent spent 1000 1000 hours hours very very ancient ancient specimen, specimen, 6-million-year-old 6-million-year-old Orrorin Orrorin tugenensis tugenensis from from
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Filling Filling a gap. a gap. Ardipithecus Ardipithecus provides provides a link a link between between earlier earlier andand later later hominins, hominins, as as seen seen in in thisthis timeline timeline showing showing important important hominin hominin fossils fossils andand taxa. taxa.
Ardipithecus Ardipithecusramidus ramidus NEWSFOCUS NEWSFOCUS Kenya, ered awhich hallmark alsoofhas hominins. a “We thought Lucy was the find of the “The authors … are framing the debate that will inevitably follow,” thighbone century but, thatinappears retrospect, it isn’t,” says paleoanthropologist Andrew because the description and interpretation of the finds are entwined, to Hill have of been Yale University. used for “It’s worth the wait.” says Pilbeam. “My first reaction is to be skeptical about some of the upright Towalking some researchers’ (Science, surprise, the female skeleton doesn’t look conclusions,” including that human ancestors never went through a 21 much Marchlike 2008, a chimpanzee, p. 1599). gorilla, or any of our closest living primate chimpanzee-like phase. Other researchers are focusing intently on So,relatives. “this raises Even though the in-this species probably lived soon after the dawn the lower skeleton, where some of the anatomy is so primitive that triguing of humankind, possibility it was that not transitional between African apes and they are beginning to argue over just what it means to be “bipedal.” we’re humans. looking “We at have the same seen the ancestor, and it is not a chimpanzee,” says The pelvis, for example, offers only “circumstantial” evidence for genus” paleoanthropologist for specimens Tim White of the University of California, Berke- upright walking, says Walker. But however the debate about Ardi’s now ley,put co-director in three of genera, the Middle Awash research group, which discovered locomotion and identity evolves, she provides the first hard evidence says andPilbeam. analyzed the But fossils. the that will inform and constrain future ideas discoverers Instead, of theO. skeleton tuge- and pieces of at least 35 additional individuals about the ancient hominin bauplan. nensis of Ar. aren’t ramidus so sure. reveal “Asafor new Ardi type andofOrrorin early hominin being thethat same was genus, neither Digging it no,chimpanzee I don’t thinknor this human. is possible, Although unless theone team really suspects wantsthat to accept Ar. ramidus an sciencemag.org unusual may have amount given of variability” rise to Lucy’s within genus, a taxon, Australopithecus, says geologistthe Martin fossils The first glimpse of this strange creature came Podcast interview Pickford “show of forthe theCollege first time dethat France, therewho is some found new Orrorin evolutionary with Brigitte grade of on 17 December 1992 when a former graduate with author Senut hominid of thethat National is not Australopithecus, Museum of Natural thatHistory is not Homo,” in Paris.says paleontolstudent of White’s, Gen Suwa, saw a glint Ann Gibbons on Ardipithecus and ogist Whatever Michel theBrunet taxonomy of theofCollege Ardipithecus de France and in theParis. other very ancient among the pebbles of the desert pavement fieldwork in the Afar. hominins, In 11they papers represent published “an enormous in this issue jumpand to Australopithecus,” online, the team the of 47 near the village of Aramis. It was the polished next researchers hominin indescribes line (see timeline, how Ar. ramidus p. 38), says looked australopithecine and moved. The expert skelesurface of a tooth root, and he immediately William ton, nicknamed Kimbel of“Ardi,” ArizonaisState fromUniversity, a female who Tempe. livedFor in example, a woodland knew it was a hominin molar. Over the next few days, the team scoured although (see sidebar, Lucy’s p. brain 40),isstood only aabout little 120 larger centimeters than that oftall, Ardipithecus, and weighed the area on hands and knees, as they do whenever an important piece Lucy’s aboutspecies, 50 kilograms. Au. afarensis, She was was thus an as adept big as biped. a chimpanzee It walked upright and had a of hominin is found (see story, p. 41), and collected the lower jaw of a like brain humans, size toventuring match. Butincreasingly she did not knuckle-walk into more diverse or swing habitats, through child with the milk molar still attached. The molar was so primitive that including the treesgrassy like living savannas. apes.And Instead, it hadshe lost walked its opposable upright,big planting toe, asher the team knew they had found a hominin both older and more primitive seen feet in flat 3.7-million-year-old on the ground, perhaps footprints eating at Laetoli, nuts, insects, Tanzania, and reflecting small mam- than Lucy. Yet the jaw also had derived traits—novel evolutionary charan mals irreversible in the woods. commitment to life on the ground. acters—shared with Lucy’s species, Au. afarensis, such as an upper Lucy’s She was direct a “facultative” ancestor is widely biped,considered say the authors, to be Au. still anamensis, living in both canine shaped like a diamond in side view. a hominin worlds—upright whose skeleton on the ground is poorly but known, also ablealthough to move its on shinbone all fours on The team reported 15 years ago in Nature that the fragmentary suggests top of branches it walkedinupright the trees, 3.9with million an opposable to 4.2 million big toeyears to grasp agolimbs. in Dream fossils belonged thein“long-sought root species team. Gen Suwato (left) Tokyo focused onpotential the skull; C. Owen Lovejoyfor (topthe in Kent, Ohio,(They studiedfirst postcranial Yohannesthen, Haile-Selassie and Kenya “These andthings Ethiopia. wereArdipithecus very odd creatures,” is the current says leading paleoanthropologist candidate right) Hominidae.” calledbones; it Au.and ramidus, after finding and analyzed key itfossils in ramidus—for Ethiopia. forAlan Au. anamensis’s Walker of Pennsylvania ancestor, ifState onlyUniversity, because it’sUniversity the only putative Park. “You Berhane partsAsfaw of thefound skeleton, changed to Ar. the Afar words hominin know what in evidence Tim [White] between once 5.8said: million If you andwanted 4.4 million to find years something ago. for “root” and “ground.”) In response to comments that he needed leg Indeed, that moved Au. anamensis like these things, fossils you’d appear have in the to goMiddle to the bar Awash in Star region Wars.” climber probably moved on flatanhands andhominin, feet on top of branches bonesthat to prove Ar. ramidus was upright White joked that just 200,000 Most researchers, years after who Ardi.have waited 15 years for the publication of in he thewould midcanopy, a type of locomotion known as palmigrady. For an be delighted with more parts, specifically a thigh and this find, agree that Ardi is indeed an early hominin. They praise the example, four bones in theplacing wrist ofanAr. ramidus gave it a more flexible intact skull, as though order. Making strides detailed reconstructions needed to piece together the crushed bones. hand that could be bent the backward at the wrist. This is in contrast thefosWithin 2 months, team delivered. In November 1994, astothe But“This the team not connectingimpressive the dots between Au.reconstruction anamensis andand hands is anisextraordinarily work of of knuckle-walking chimpanzees and Berkeley gorillas, which havestudent stiff sil hunters crawled up an embankment, graduate Ar.description, ramidus justwell yet, worth awaiting morefor,” fossils. now they are focusing waiting saysFor paleoanthropologist David wrists that absorb forces on of their knuckles. Yohannes Haile-Selassie Ethiopia, now a paleoanthropologist at the on Pilbeam the anatomy of ArdiUniversity. and how she moved world. of Harvard “They didthrough this jobthe very, veryHer well,” Cleveland However, Museum several researchers soin sure about thesetwo inferences. of Naturalaren’t History Ohio, spotted pieces of a foot agrees is primitive, neurobiologist with an opposable Christophbig Zollikofer toe like that of the used University by living of Some skeptical that of thea crushed pelvis the by anatomical bonearefrom the palm hand. That wasreally soonshows followed pieces of a apes to grasp branches. But the bases of the four other toe bones details Zurich in Switzerland. needed to demonstrate bipedality. Theofpelvis is “suggestive” pelvis; leg, ankle, and foot bones; many the bones of the handofand were oriented so that they reinforced forefoot into a more rigid But not everyone agrees with the the team’s interpretations about how bipedality but notjaw conclusive, says paleoanthropologist Carol Ward of itthewas arm; a lower with teeth—and a cranium. By January 1995, lever she pushed off.upright In contrast, the toes of a chimpanzee curve University Ar. as ramidus walked and what it reveals about our ancestors. Missouri, Columbia. “does not appear to apparentofthat they had made theAlso, rarestAr.oframidus rare finds, a partial skeleton. as flexibly as those in their hands, say Lovejoy and co-author have had its knee placed over the ankle, which means that when walkBruce Latimer of Case Western Reserve University in Cleveland. ing bipedally, it would have had to shift its weight to the side,” she says. Ar. ramidus “developed a pretty good bipedal foot while at the same Paleoanthropologist William Jungers of Stony Brook University in time keeping an opposable first toe,” says Lovejoy. New York state is also not sure that the skeleton was bipedal. “Believe The upper blades of Ardi’s pelvis are shorter and broader than in me, it’s a unique form of bipedalism,” he says. “The postcranium alone apes. They would have lowered the trunk’s center of mass, so she could would not unequivocally signal hominin status, in my opinion.” Paleobalance on one leg at a time while walking, says Lovejoy. He also anthropologist Bernard Wood of George Washington University in infers from the pelvis that her spine was long and curved like a Washington, D.C., agrees. Looking at the skeleton as a whole, he says, human’s rather than short and stiff like a chimpanzee’s. These “I think the head is consistent with it being a hominin, … but the rest of changes suggest to him that Ar. ramidus “has been bipedal for a very the body is much more questionable.” long time.” All this underscores how difficult it may be to recognize and Yet the lower pelvis is still quite large and primitive, similar to define bipedality in the earliest hominins as they began to shift from African apes rather than hominins. Taken with the opposable big toe, trees to ground. One thing does seem clear, though: The absence of and primitive traits in the hand and foot, this indicates that Ar. ramidus many specialized traits found in African apes suggests that our didn’t walk like Lucy and was still spending a lot of time inArdi thehas trees. ancestors never knuckle-walked. Unexpected anatomy. an opposable toe (left) and flexible hand (right); But it wasn’t suspending its body beneath branches African apes That ofthrows a monkey wrench her canines (toplike center) are sized between those a human (top left) and chimpinto a hypothesis about the last or climbing vertically, says Lovejoy. (top Instead, wasthea blades slow, of careful of living apes and humans. Ever since Darwin right);itand her pelvis common (lower left) ancestor are broad like Lucy’s (yellow). CREDITS: (LEFT) C. O. LOVEJOY ET AL., SCIENCE; (TOP) G. SUWA ET AL., SCIENCE; (BOTTOM) C. O. LOVEJOY ET AL., SCIENCE; (RIGHT) C. O. LOVEJOY ET AL., SCIENCE
CREDITS (TOP TO BOTTOM): TIM WHITE; BOB CHRISTY/NEWS AND INFORMATION, KENT STATE UNIVERSITY; TIM WHITE
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Habitat for Humanity ARAMIS, ETHIOPIA—A long cairn of black stones marks the spot where a skeleton of Ardipithecus ramidus was found, its bones broken and scattered on a barren hillside. Erected as a monument to an ancient ancestor in the style of an Afar tribesman’s grave, the cairn is a solitary marker in an almost sterile zone, devoid of life except for a few spindly acacia trees and piles of sifted sediment. That’s because the Middle Awash research team sucked up everything in sight at this spot, hunting for every bit of fossil bone as well as clues to the landscape 4.4 million years ago, when Ardipithecus died here. “Literally, we crawled every square inch of this locality,” recalls team co-leader Tim White of the University of California, Berkeley. “You crawl on your hands and knees, collecting every piece of bone, every piece of wood, every seed, every snail, every scrap. It was 100% collection.” The heaps of sediment are all that’s left behind from that fossil-mining operation, which yielded one of the most important fossils in human evolution (see main text, p. 36), as well as thousands of clues to its ecology and environment. The team collected more than 150,000 specimens of fossilized plants and animals from nearby localities of the same age, from elephants to songbirds to millipedes, including fossilized wood, pollen, snails, and larvae. “We have crates of bone splinters,” says White. A team of interdisciplinary researchers then used these fossils and thousands of geological and isotopic samples to reconstruct Ar. ramidus’s Pliocene world, as described in companion papers in this issue (see p. 66 and 87). From these specimens, they conclude that Ardi lived in a woodland, climbing among hackberry, fig, and palm trees and coexisting with monkeys, kudu antelopes, and peafowl. Doves and parrots flew overhead. All these creatures prefer woodlands, not the open, grassy terrain often conjured for our ancestors. The team suggests that Ar. ramidus was “more omnivorous” than chimpanzees, based on the size, shape, and enamel distribution of its teeth. It probably supplemented woodland plants such as fruits, nuts, and tubers with the occasional insects, small mammals, or bird eggs. Carbon-isotope studies of teeth from five individuals show that Ar. ramidus ate mostly woodland, rather than grassland, plants. Although Ar. ramidus probably ate
suggested in 1871 that our ancestors arose in Africa, researchers have debated whether our forebears passed through a great-ape stage in which they looked like proto-chimpanzees (Science, 21 November 1969, p. 953). This “troglodytian” model for early human behavior (named for the common chimpanzee, Pan troglodytes) suggests that the last common ancestor of the African apes and humans once had short backs, arms adapted for swinging, and a pelvis and limbs adapted for knuckle walking. Then our ancestors lost these traits, while chimpanzees and gorillas kept them. But this view has been uninformed by fossil evidence because there are almost no fossils of early chimpanzees and gorillas. Some researchers have thought that the ancient African ape bauplan was more primitive, lately citing clues from fragmentary fossils of apes that lived from 8 million to 18 million years ago. “There’s been growing evidence from the Miocene apes that the common ancestor may have been more primitive,” says Ward. Now Ar. ramidus strongly supports that notion. The authors repeatedly
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Past and present. Ardipithecus’s woodland was more like Kenya’s Kibwezi Forest (left) than Aramis today.
figs and other fruit when ripe, it didn’t consume as much fruit as chimpanzees do today. This new evidence overwhelmingly refutes the once-favored but now moribund hypothesis that upright-walking hominins arose in open grasslands. “There’s so much good data here that people aren’t going to be able to question whether early hominins were living in woodlands,” says paleoanthropologist Andrew Hill of Yale University. “Savannas had nothing to do with upright walking.” Geological studies indicate that most of the fossils were buried within a relatively short window of time, a few thousand to, at most, 100,000 years ago, says geologist and team co-leader Giday WoldeGabriel of the Los Alamos National Laboratory in New Mexico. During that sliver of time, Aramis was not a dense tropical rainforest with a thick canopy but a humid, cooler woodland. The best modern analog is the Kibwezi Forest in Kenya, kept wet by groundwater, according to isotope expert Stanley Ambrose of the University of Illinois, Urbana-Champaign. These woods have open stands of trees, some 20 meters high, that let the sun reach shrubs and grasses on the ground. Judging from the remains of at least 36 Ardipithecus individuals found so far at Aramis, this was prime feeding ground for a generalized early biped. “It was the habitat they preferred,” says White. –A.G.
note the many ways that Ar. ramidus differs from chimpanzees and gorillas, bolstering the argument that it was those apes that changed the most from the primitive form. But the problem with a more “generalized model” of an arboreal ape is that “it is easier to say what it wasn’t than what it was,” says Ward. And if the last common ancestor, which according to genetic studies lived 5 million to 7 million years ago, didn’t look like a chimp, then chimpanzees and gorillas evolved their numerous similarities independently, after gorillas diverged from the chimp/human line. “I find [that] hard to believe,” says Pilbeam. As debate over the implications of Ar. ramidus begins, the one thing that all can agree on is that the new papers provide a wealth of data to frame the issues for years. “No matter what side of the arguments you come down on, it’s going to be food for thought for generations of graduate students,” says Jungers. Or, as Walker says: “It would have been very boring if it had looked half-chimp.” –ANN GIBBONS SCIENCE
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CREDITS (LEFT TO RIGHT): TIM WHITE; ANN GIBBONS
NEWSFOCUS
The crawl. Researchers hunt down every fossil at Aramis.
PALEOANTHROPOLOGY
The View From Afar
CREDITS (TOP TO BOTTOM): HENRY GILBERT; SOURCE: TIM WHITE
How do you find priceless hominin fossils in a hostile desert? Build a strong team and obsess over the details
MIDDLE AWASH VALLEY, THE AFAR DEPRESSION, ETHIOPIA—It’s of how upright walking evolved and how our earliest ancestors difabout 10 a.m. on a hot morning in December, and Tim White is fered from chimpanzees (see overview, p. 60, and main Focus text, watching a 30-year-old farmer inch his way up a slippery hill on his p. 36). But Aramis is just one of 300 localities in the Middle Awash, knees, picking through mouse-colored rubble for a bit of gray bone. which is the only place in the world to yield fossils that span the entire The sun is already bleaching the scrubby badlands, making it diffi- saga of hominid evolution. At last count, this team had gathered cult to distinguish a fragment of bone in the washed-out beige and 19,000 vertebrate fossils over the past 19 years. These include about gray terrain. The only shade in this parched gully is from a small, 300 specimens from seven species of hominins, from some of the thorny acacia tree, so the fossil hunters have draped their heads with first members of the human family, such as 5.8-million-year-old kerchiefs that hang out from under their “Cal” and “Obama for Pres- Ar. ramidus kadabba, to the earliest members of our own species, ident” baseball caps, making them look like a strange tribe of Berke- Homo sapiens, which lived here about 160,000 years ago. ley Bedouins. If there are fossils here, As they work in different places in the White is conf ident that the slender WESTERN AFAR RIFT, ETHIOPIA valley, the team members travel back and farmer, Kampiro Kayrento, will f ind forth in time. Today, this core group is HADAR GONA them. “Kampiro is the best person in the working in the western foothills near the world for f inding little pieces of fosBurka catchment, where an ancient river silized human bone,” says White, 59, a laid down sediments 3 million to 2 milpaleoanthropologist at the University of lion years ago and where the team has California, Berkeley, who has collected found specimens of Australopithecus Awash fossils in this region since 1981. garhi, a species they suspect may have River Watching Kayrento is a sort of spectagiven rise to the f irst members of our Afar tor sport, because he scores so often. Just genus, Homo. Rift Aramis minutes earlier, he had walked over the This season, after a rough start, the 25 crest of a small hill, singing softly to himscientists, students, cooks, and Ethiopian Addis Ababa self, and had spotted the fossilized core of and Afar officials and guards in camp are ETHIOPIA a horn from an ancient bovid, or antelope. working well together. Their tented camp is Bouri Peninsula hours from any town, graded road, or fresh Then he picked up a flat piece of gray bone Middle Awash Yardi Lake Hominid Localities nearby and showed the fossil to Ethiopian water. (They dug their own well to get Burka Ardipithecus paleoanthropologist Berhane Asfaw, askwater.) “The 1st week, it’s like an engine Australopithecus Homo ing, “Bovid?” Asfaw, 55, who hired that’s running but not running smoothly,” Kayrento when he was a boy hanging out says White, who, with Asfaw, runs a wellat fossil sites in southern Ethiopia, looked Ancestral territory. The area where Ardi was found is rich in organized camp where every tool, map, and over the slightly curved piece of bone the hominin fossil sites, including these worked by the Middle shower bag has its proper place. “By the size of a silver dollar and suggested, “Mon- Awash research team. 3rd week, people know their jobs.” key?” as he handed it to White. White The 1st week, White and a paleontoloturned it over gently in his hands, then said: “Check that, Berhane. We gist were sick, and White is still fighting a harsh cough that keeps just found a hominid cranium. Niiiice.” him awake at night. The 2nd week, some aggressive Alisera tribesAs word spreads that Kayrento found a hominin, or a member of men who live near the Ar. ramidus site threatened to kill White and the taxon that includes humans and our ancestors, the other fossil Asfaw, making it difficult to return there. (That’s one reason the hunters tease him: “Homo bovid! Homo bovid! Niiiice.” team travels with six Afar policemen armed with AK-47s and The Middle Awash project, which includes 70 scientists from 18 Obama caps, dubbed “The Obama Police.”) The day before, a stunations, is best known for its discovery of the 4.4-million-year-old dent had awakened with a high fever and abdominal pain and had to partial skeleton of Ardipithecus ramidus at Aramis, about 34 kilo- be driven 4 hours to the nearest clinic, where he was diagnosed with meters north of here. That skeleton is now dramatically revising ideas a urinary tract infection, probably from drinking too little water in www.sciencemag.org
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the 35˚C heat. “The best laid plans change every day,” says White, who has dealt with poisonous snakes, scorpions, malarial mosquitoes, lions, hyenas, flash floods, dust tornadoes, warring tribesmen, and contaminated food and water over the years. “Nothing in the field comes easy.” Calling the “A” team Nothing in the Afar, for that matter, comes easy. We are reminded of that as we drive across the dusty Saragata plain to the target fossil site at 8 a.m., making giant circles in the dust with the Toyota Land Cruiser so we can find our tracks home at the end of the day. Men clad in plaid wraps, with AK-47s slung over their shoulders, flag us down seeking help. They bring over a woman who looks to be in her 70s but is probably much younger. Her finger is bleeding, and the men tell White and Asfaw, in Afar, that a puff adder bit her the night before while she was gathering wood. A quick-thinking boy had sliced her finger with a knife, releasing the venom and probably saving her life. White gets out a first-aid kit, removes a crude poultice, and cleans and bandages the wound, putting on an antibiotic cream. “It’s good she survived the night,” he says as we drive off. “The danger now is infection.” After inching down the sandy bank of a dry river, we reach the socalled Chairman’s site. This is one of dozens of fossil localities discovered in the Burka area since 2005: exposed hillsides that were spotted in satellite and aerial photos, then laboriously explored on foot. The plan was to search for animal fossils to help date a hominid jawbone discovered last year. But in the 1st hour, with Kayrento’s discovery, they’re already on the trail of another individual instead. As soon as White identifies the bit of skull bone, he swings into action. With his wiry frame and deep voice, he is a commanding presence, and it soon becomes clear how he earned his nickname, “The General.” In his field uniform—a suede Australian army hat with a rattlesnake band, blue jeans, and driving gloves without fingers—he uses a fossil pick to delineate the zones in the sandstone
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Division of labor. Kampiro Kayrento (top left) homes in on fossils; he and others sweep the surface, and Giday WoldeGabriel dates sediments.
where he wants the crew deployed. “Get everybody out of the area,” he calls to the 15 people already fanned out over the gully, scanning for fossils. “I want the ‘A’ team.” He singles out Kayrento and three others and hands them yellow pin-flags, saying, “Go back to the bottom.” As he watches them move up the slope, he warns: “Go slowly. You’re moving too fast. … Don’t squash the slope. Move like a cat, not a cow.” By looking at the relatively fresh fractured edge of the bone fragment, White knows that it comes from a larger piece of skull that broke after it was exposed, not while it was buried. As Kayrento and the others find other bits of bone, they place yellow pin-flags at those spots. “This process establishes the distributional cone,” White explains. The top flag marks the highest point on the surface where the skull came out of the ground; the bottom boundary marks the farthest point where a fragment might finally have come to rest, following the fall line down the slope. This discovery also illustrates one reason why the team comes to the field right after the rainy season. If they’re lucky, rain and floods will cut into the ancient sediments, exposing fossils. But they have to get there before the fossils disintegrate as they are exposed to the elements or are trampled by the Afar’s goats, sheep, and cattle. Timing is everything, and this season they’re a bit late. “The ideal situation is to find a fossil just as it is eroding out of the bank,” says White. As they crawl the entire length of the gully, they turn over every rock, mud clod, and piece of carbonate rubble to make sure it doesn’t contain a fossil fragment. “Not good,” says Kayrento. “This is yucky,” agrees Asfaw, co-director of the team and the first Ethiopian scientist to join it, in 1979 when he was invited to earn his Ph.D. at Berkeley (Science, 29 August 2003, p. 1178). After 2 hours, the team has collected a few more pieces of skull around the temple, forehead, and ear. “It’s getting bigger by the minute,” White says. “If we’re lucky, we’ll find it buried right in here.” The team has to wait until the next day to find out just how lucky. At 9:45 a.m. Thursday, they return with reinforcements: Asfaw has hired two Afar men to help with the heavy lifting of buckets of dirt. With a button-down Oxford cloth shirt and a pistol stuck in the waistband of his khakis, Asfaw commands respect, and he is the best at negotiating with the Afar. In this case, he settles an argument by letting clan leaders select which men, among a large group, will get jobs. At the site, White sets up a perimeter of blue pin-flags that look like a mini slalom course, outlining the gully that he calls the “Hot Zone” where fossil pieces are most likely to be buried. The plan is to excavate all the rock and dirt around those flags, down to the original layers of sediment. White explains that the ancient landscape would have been flatter and more verdant before tectonic movements of Earth’s crust cracked and tilted the sediment layers. But the original soil is still there, a red-brown layer of clay beneath a gray veneer of sandstone. “Throw every piece of stone out of the channel,” he orders. “If you see a hominid, I need to know right away!” White and Kayrento literally sweep off the gray lag with a push broom and then scrape back the layers of time with a trowel to the ancient surface underneath. “Once we brush out the slopes, we’ll be
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sure no fossil is left in place,” says White. In case they miss a fragment, the loose sediment is carried to giant sieves where the crew sifts it for bits of bone or teeth. The sifted rubble is taken to a circle of workers who then empty it into small aluminum pans, in which they examine every single, tiny piece—a job that gives new meaning to the word tedium. “Sieving 101,” observes Asfaw, who supervises sieving and picking today. By 11:10 a.m., the pace of discovery has slowed. When the A team tells White it’s “not good,” he tries to infuse them with some of his energy, reminding everyone to stay focused, to keep going, to not step on fossils. But by midday, White is grumbling, too, because they’ve scoured the Hot Zone and it’s clear the skull is not there. “We’ve eliminated every hope of finding it in situ.”
NEWSFOCUS
Intensive care. Tim White uses dental tools and a gluelike adhesive to extract fragile fossils from matrix.
Time travel It’s a good time to take a walk with the four geologists, who are combing the terrain, hoping to find sediments with volcanic minerals to Luckily, the fossil hunters help them date the locality and its fossils precisely. While fossil have found a pig known to hunters move slowly, stooped at the waist and focused on the ground, have lived about 2.6 million the geologists move fast, heads up, scanning the next horizon for a to 2.7 million years ago, rock face with a layer cake of sediments, like those exposed in road which suggests that the sedicuts. The 6-million-year record of Middle Awash sediments is not ments and the new discovery are also that old. stacked neatly in one place, with oldest rocks on the bottom and At 9 a.m. Friday, 12 December, we’re back at the Chairman’s site youngest on top. (If it were, the stack would be 1 kilometer thick.) for a 3rd day, this time with a film crew from Sweden. After White Instead, the rocks are faulted and tilted into different ridges. By trac- and Kayrento jokingly reenact the discovery of the skull bone for the ing a once-horizontal layer from ridge to ridge, sometimes for kilo- film crew, they resume sweeping and sifting, exactly where they left meters, the geologists can link the layers and place different snap- off. At first, there’s little return. Berkeley postdoc Cesur Pehlevan shots of time into a sequence. from Ankara hands White a piece of bone: “Nope, tough luck. Right Today, Ethiopian geologist Giday WoldeGabriel of the Los color, right thickness. Nope, sorry.” Alamos National Laboratory in New Mexico, also a co-leader of the Finally, someone hands White something special. “Oh nice, frontal team (he joined in 1992), is searching for a familiar-looking motif— bone with frontal sinus. This is getting better. That’s what we’re after,” a distinct layer of volcanic tuff called the SHT (Sidiha Koma Tuff), says White. “If we can get that brow ridge, we can match it with the previously dated to 3.4 million years ago by radiometric methods. known species.” He turns over the new piece of frontal bone in his So far, the team has found just one species of hominin— hand, examining it like a diamond dealer assessing a gemstone. Au. garhi—that lived at this time in the Middle Awash (Science, By the end of 3 days, the team of 20 will have collected a dozen 23 April 1999, p. 629), although a more robust pieces of one skull, an average yield for this region. species, Au. aethiopicus, appears 2.6 million years “Nothing in the field Taken together, says White, those pieces show that ago in southern Ethiopia and Kenya. That’s also when “It’s an Australopithecus because it has a small braincomes easy.” the earliest stone tools appear in Gona, Ethiopia, case, small chewing apparatus.” There’s still not –TIM WHITE, UNIVERSITY enough to identify the species, though White thinks it 100 kilometers north of here. The earliest fossils of our genus Homo come a bit later—at 2.3 million years ago OF CALIFORNIA, BERKELEY is Au. garhi. He notes that “it’s a big boy, big for an at Hadar, near Gona, also with stone tools. That’s why australopithecine.” If it is Au. garhi, that would be it is important to date Au. garhi precisely: Was it the maker of the one more bit of evidence to suggest that Au. afarensis gave rise to stone tools left in the Afar? The team thinks Au. garhi is the direct Au. garhi; males are bigger than females in Au. afarensis—and so descendant of the more primitive Au. afarensis, best known as the perhaps in Au. garhi, too. species that includes the famous 3.2-million-year-old skeleton of For now, White and Asfaw are pleased with the new snapshot Lucy, also from Hadar. But did Au. garhi then evolve into early they’re getting of Au. garhi. On our way back to camp, White stops Homo? They need better dates—and more fossils—to find out. so we can take a photo of the moon rising over Yardi Lake in front “Now that we have the SHT as a reference point here, we have of us, the sun setting behind us. The landscape has changed since to try to trace it to where the new fossils are,” says WoldeGabriel. the australopithecines were here. But one thing’s been constant in The only problem is that the SHT is several ridges and basins over the Middle Awash, he notes: “Hominids have been right here lookfrom the excavation; linking the two will be difficult if not impos- ing at the moon rising over water for millions of years.” –ANN GIBBONS sible. The team will also use other methods to date the new fossils. www.sciencemag.org
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AUTHORS’SUMMARIES Ardipithecus ramidus and the Paleobiology of Early Hominids Tim D. White, Berhane Asfaw, Yonas Beyene, Yohannes Haile-Selassie, C. Owen Lovejoy, Gen Suwa, Giday WoldeGabriel
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CREDIT: ILLUSTRATION OF AR. RAMIDUS: COPYRIGHT J. H. MATTERNES
C
harles Darwin and Thomas Huxley were forced to ponder human origins and evolution without a relevant fossil record. With only a few Pan Pan Neanderthal fossils available to troglo paniscus Gorilla dytes g o r i l a l supplement their limited knowlCLCA edge of living apes, they specu• Partially arboreal • Striding terrestrial biped • Palmigrade lated about how quintessentially • Enlarged brain • Facultative biped • Postcanine megadontia GLCA arborealist human features such as upright • Dentognathic reduction • Feminized canine • Pan-African • Dimorphic canines • Technology-reliant • Woodland omnivore • Wide niche walking, small canines, dexterous • Forest A us • Old World range A hands, and our special intelligence r tralo dipi frugivore/ Ho pithe thecu mo ( s (~ 6 to 4 Ma) cus ( omnivore had evolved through natural selec< ~ 4 to 1 Ma) ~ 2.5 Ma ) tion to provide us with our complex way of life. Today we know of early Homo from >2.0 million Evolution of hominids and African apes since the gorilla/chimp+human (GLCA) and chimp/human (CLCA) last common ancestors. Pedestals on the left show separate lineages leading to the extant apes (gorilla, and chimp and years ago (Ma) and have a record bonobo); text indicates key differences among adaptive plateaus occupied by the three hominid genera. of stone tools and animal butchery that reaches back to 2.6 Ma. These demonstrate just how deeply tech- probably was more omnivorous than chimpanzees (ripe fruit specialnology is embedded in our natural history. ists) and likely fed both in trees and on the ground. It apparently conAustralopithecus, a predecessor of Homo that lived about 1 to 4 Ma sumed only small amounts of open-environment resources, arguing (see figure), was discovered in South Africa in 1924. Although slow to against the idea that an inhabitation of grasslands was the driving force gain acceptance as a human ancestor, it is now recognized to represent in the origin of upright walking. an ancestral group from which Homo evolved. Even after the discovAr. ramidus, first described in 1994 from teeth and jaw fragments, eries of the partial skeleton (“Lucy”) and fossilized footprints is now represented by 110 specimens, including a partial female (Laetoli) of Au. afarensis, and other fossils that extended the antiquity skeleton rescued from erosional degradation. This individual weighed of Australopithecus to ~3.7 Ma, the hominid fossil record before about 50 kg and stood about 120 cm tall. In the context of the many Australopithecus was blank. What connected the small-brained, small- other recovered individuals of this species, this suggests little body canined, upright-walking Australopithecus to the last common ances- size difference between males and females. Brain size was as small as tor that we shared with chimpanzees some time earlier than 6 Ma? in living chimpanzees. The numerous recovered teeth and a largely The 11 papers in this issue, representing the work of a large inter- complete skull show that Ar. ramidus had a small face and a reduced national team with diverse areas of expertise, describe Ardipithecus canine/premolar complex, indicative of minimal social aggression. ramidus, a hominid species dated to 4.4 Ma, and the habitat in which Its hands, arms, feet, pelvis, and legs collectively reveal that it moved it lived in the Afar Rift region of northeastern Ethiopia. This species, capably in the trees, supported on its feet and palms (palmigrade substantially more primitive than Australopithecus, resolves many clambering), but lacked any characteristics typical of the suspenuncertainties about early human evolution, including the nature of the sion, vertical climbing, or knuckle-walking of modern gorillas and last common ancestor that we shared with the line leading to living chimps. Terrestrially, it engaged in a form of bipedality more primchimpanzees and bonobos. The Ardipithecus remains were recovered itive than that of Australopithecus, and it lacked adaptation to from a sedimentary horizon representing a short span of time (within “heavy” chewing related to open environments (seen in later 100 to 10,000 years). This has enabled us to assess available and pre- Australopithecus). Ar. ramidus thus indicates that the last common ferred habitats for the early hominids by systematic and repeated ancestors of humans and African apes were not chimpanzee-like and sampling of the hominid-bearing strata. that both hominids and extant African apes are each highly specialBy collecting and classifying thousands of vertebrate, invertebrate, ized, but through very different evolutionary pathways. and plant fossils, and characterizing the isotopic composition of soil samples and teeth, we have learned that Ar. ramidus was a denizen of See pages 62–63 6–7 forfor authors’ affiliations. authors’ affiliations. woodland with small patches of forest. We have also learned that it When citing, please refer to the full paper, available at DOI 10.1126/science.1175802.
AUTHORS’SUMMARIES Authors’Summaries
The Geological, Isotopic, Botanical, Invertebrate, and Lower Vertebrate Surroundings of Ardipithecus ramidus Giday WoldeGabriel, Stanley H. Ambrose, Doris Barboni, Raymonde Bonnefille, Laurent Bremond, Brian Currie, David DeGusta, William K. Hart, Alison M. Murray, Paul R. Renne, M. C. Jolly-Saad, Kathlyn M. Stewart, Tim D. White
A
rdipithecus ramidus was found in exposed sediments flanking the Awash River, Ethiopia. The local geology and associated fossils provide critical information about its age and habitat. Most of Africa’s surface is nondepositional and/or covered by forests. This explains why so many discoveries related to early hominid evolution have been made within eastern Africa’s relatively dry, narrow, active rift system. Here the Arabian and African tectonic plates have been pulling apart for millions of years, and lakes and rivers have accumulated variably fossil-rich sediments in the Afar Triangle, which lies at the intersection of the Red Sea, Gulf of Aden, and Main Ethiopian Rifts (see map). Some of these deposits were subsequently uplifted by the rift tectonics and are now eroding. In addition, volcanoes associated with Map showing the Middle Awash area (star) and rift locations (red lines). Photo shows the this rifting have left many widespread deposits that we 4.4 Ma volcanic marker horizon (yellow bed) atop the locality where the skeleton and holocan use to determine the age of these fossils using type teeth of Ar. ramidus were discovered. Also shown are some of the fossil seeds. modern radioisotopic methods. Several of the most important hominid fossils have been found near between two key volcanic markers, each dated to 4.4 Ma. Their simithe Afar’s western margin, north and west of the Awash River (star on lar ages and sedimentology imply that the fossils themselves date to map), including Hadar (the “Lucy” site), Gona [known for the world’s 4.4 Ma and were all deposited within a relatively narrow time interval oldest stone tools at 2.6 million years ago (Ma)], and the Middle Awash lasting anywhere from 100 to 10,000 years. Today the unit is exposed (including Aramis). Cumulatively, these and nearby study areas in across a 9-km arc that represents a fortuitous transect through the Ethiopia have provided an unparalleled record of hominid evolution. ancient landscape. The western exposure, in particular, preserves a Fossil-bearing rocks in the Middle Awash are intermittently rich assemblage of plant and animal fossils and ancient soils. exposed and measure more than 1 km in thickness. Volcanic rocks Fossilized wood, seeds, and phytoliths (hard silica parts from near the base of this regional succession are dated to more than 6 Ma. plants) confirm the presence of hackberry, fig, and palm trees. There Its uppermost sediments document the appearance of anatomically is no evidence of a humid closed-canopy tropical rainforest, nor of near-modern humans 155,000 years ago. As is the case for many river the subdesertic vegetation that characterizes the area today. and lake deposits, fossil accumulation rates here have been highly Invertebrate fossils are abundant and include insect larvae, broodvariable, and the distribution and preservation of the fossils are balls and nests of dung beetles, diverse gastropods, and millipedes. uneven. Alterations of the fossils caused by erosion and other factors The terrestrial gastropods best match those seen in modern groundfurther complicate interpretation of past environments. To meet this water forests such as the Kibwezi in Kenya. Aquatic lower vertechallenge, beginning in 1981, our research team of more than 70 sci- brates are relatively rare and probably arrived episodically during entists has collected 2000 geological samples, thousands of lithic flooding of a river distal to the Aramis area. The most abundant fish artifacts (e.g., stone tools), and tens of thousands of plant and animal is catfish, probably introduced during overbank flooding and/or by fossils. The emergent picture developed from the many Middle predatory birds roosting in local trees. Awash rock units and their contents represents a series of snapshots Our combined evidence indicates that Ar. ramidus did not live in taken through time, rather than a continuous record of deposition. the open savanna that was once envisioned to be the predominant Ar. ramidus was recovered from one such geological unit, 3 to 6 m habitat of the earliest hominids, but rather in an environment that thick, centered within the study area. Here, the Aramis and adjacent was humid and cooler than it is today, containing habitats ranging drainage basins expose a total thickness of 300 m of sediments largely from woodland to forest patches. deposited in rivers and lakes, and on floodplains, between ~5.5 and 3.8 Ma. Within this succession, the Ar. ramidus–bearing rock unit See pages 62–63 6–7 forfor authors’ affiliations. authors’ affiliations. comprises silt and clay beds deposited on a floodplain. It is bracketed When citing, please refer to the full paper, available at DOI 10.1126/science.1175817.
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Authors’Summaries AUTHORS’SUMMARIES
Taphonomic, Avian, and Small-Vertebrate Indicators of Ardipithecus ramidus Habitat Antoine Louchart, Henry Wesselman, Robert J. Blumenschine, Leslea J. Hlusko, Jackson K. Njau, Michael T. Black, Mesfin Asnake, Tim D. White
T
Coliidae 6.0 to 300 m of radioisotopically and paleomagnetically calibrated, sporadically fossiliferous strata dating between 5.55 and 3.85 Ma. Centered in its stratigraphic column are two prominent and widespread volcanic marker horizons that encapsulate the Lower Aramis Member of the Sagantole Formation (Fig. 1). These, the Gàala (“camel” in Afar language) Vitric Tuff Complex (GATC) and the superimposed Daam Aatu (“baboon” in Afar language) Basaltic Tuff (DABT), have indistinguishable laser fusion 39 Ar/40Ar dates of 4.4 Ma. Sandwiched between
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Ardipithecusramidus ramidus Ardipithecus the two tuffs are fossiliferous sediments averaging ~3 m in thickness and cropping out discontinuously over an arc-shaped, natural erosional transect of >9 km (28). The rich fossil and geologic data from these units provide a detailed characterization of the Pliocene African landscape inhabited by Ardipithecus. We first surveyed the CAC during 1981 in attempts to understand the distribution of fossils within the region. We launched a systematic program of geological, geochronological, and paleontological investigation in 1992. Initial visits to the CAC’s northeastern flank documented abundant fossilized wood and seeds in the interval between the two tuffs. We collected and identified a highly fragmented sample of vertebrates, including abundant cercopithecid monkeys and tragelaphine bovids. The first hominid fossils were found at Aramis vertebrate paleontology locality 1 (ARA-VP-1) on 17 December 1992. Two initial seasons of stratigraphic and geochronological studies yielded 649 cataloged vertebrates, including a minimum number of 17 hominid individuals represented mostly by teeth (10). Because of its content, the Lower Aramis Member became the focus of our paleontological
efforts. Fourteen sublocalities within the original ARA-VP-1 locality were circumscribed and subjected to repeated collecting of all biological remains, based on multiple team crawls (35) across the eroding outcrops between 1995 and 2005. Analogous collections were made at adjacent localities (ARA-VP-6, -7, and -17), as well as at the eastern and western exposures of the Ardipithecus-bearing sedimentary units (KUSVP-2 and SAG-VP-7) (KUS, Kuseralee Dora; SAG, Sagantole). The Lower Aramis Member vertebrate assemblage (table S1) now totals >6000 cataloged specimens, including 109 hominid specimens that represent a minimum of 36 individuals. An additional estimated 135,000 recovered fragments of bone and teeth from this stratigraphic interval are cataloged by locality and taxon as pooled “bulk” assemblages. Analogous samples were collected from the Lower Aramis Member on the eastern transect pole (SAG-VP-1, -3, and -6). Fossils from localities higher and lower in the local Middle Awash succession (7, 12, 32) and at nearby Gona (36) are reported elsewhere. The ARA-VP-6/500 partial hominid skeleton. Bones of medium and large mammals were usually ravaged by large carnivores, then embedded
in alluvial silty clay of the Lower Aramis Member. Once exposed by erosion, postdepositional destruction of the fossils by decalcification and fracture is typical. As a result, the larger vertebrate assemblage lacks the more complete cranial and postcranial elements typically recovered from other African hominid localities. The identification of larger mammals below the family level is therefore most often accomplished via teeth. The hominid subassemblage does not depart from this general preservational pattern (29). There was consequently little initial hope that the stratigraphic interval between the two tuffs would yield crucially needed postcranial elements of Ardipithecus. The only relevant postcrania (arm elements) had come from slightly higher in the section in 1993 (10). However, on 5 November 1994, Y.H.S. collected two hominid metacarpal fragments (ARA-VP-6/500-001a and b) from the surface of an exposed silty clay ~3 m below the upper tuff (DABT), 54 m to the north of the point that had 10 months earlier yielded the Ardipithecus holotype dentition. Sieving produced additional hominid phalanges. The outcrop scrape exposed a hominid phalanx in situ, followed by a femur shaft and nearly complete tibia. Subsequent excavation during 1994
Fig. 1. Geography and stratigraphy of the Aramis region. Two dated volcanic horizons constrain the main Ardipithecusbearing stratigraphic interval in the Aramis region. The top frame shows these tephra in situ near the eastern end of the 9-km outcrop. The dark stripe in the background is the riverine forest of the modern Awash River running from right to left, south to north, through the Middle Awash study area of the Afar Rift. The lower frames are contemporaneous helicopter viewsoverARA-VP-1(Yonas Molar Site) to show the geographic position of the top photo and to depict the extensive outcrop of the upper tuff horizon (dotted lines show the DABT) across the local landscape. Vehicles are in the same position to provide orientation. Sediments outcropping immediately below this 4.4-million-year-old horizon yielded the floral, faunal, and isotopic contexts for Ar. ramidus. The frame to the left shows the slight eastward dip of the Sagantole Formation toward the modern Awash River. The contiguous frame to the right is a view up the modern upper Aramis catchment. The ARA-VP-6 locality where the partial Ardipithecus skeleton was excavated is near its top right corner (Fig. 2).
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Research Articles RESEARCH ARTICLES and the next field season (at a rate of ~20 vertical mm/day across ~3 m2) revealed >100 additional in situ hominid fragments, including sesamoids (Fig. 2 and table S2). Carnivore damage was absent. The bony remains of this individual (ARAVP-6/500) (Fig. 3) (37) are off-white in color and very poorly fossilized. Smaller elements (hand and foot bones and teeth) are mostly undistorted, but all larger limb bones are variably crushed. In the field, the fossils were so soft that
they would crumble when touched. They were rescued as follows: Exposure by dental pick, bamboo, and porcupine quill probe was followed by in situ consolidation. We dampened the encasing sediment to prevent desiccation and further disintegration of the fossils during excavation. Each of the subspecimens required multiple coats of consolidant, followed by extraction in plaster and aluminum foil jackets, then additional consolidant before transport to Addis Ababa.
Fig. 2. The ARA-VP-6/500 skeletal excavation. Successive zooms on the ARA-VP-6/500 partial skeleton discovery are shown. Insets show the application of consolidant to the tibia shaft and removal of the os coxae in a plaster jacket in 1994–1995. No skeletal parts were found articulated (the mandible excavation succession shows the close proximity of a proximal hand phalanx and trapezium). Only in situ specimens are shown on the plan and profile views. Note the tight vertical and wider horizontal distributions of the remains. Local strata dip ~5° to the east. The lower inside corner of each yellow pin flag marks the center point for each in situ specimen from the 1994–1995 excavation. The 1995–1996 excavation recovered additional, primarily craniodental remains between these flags and the vehicle. The boulder pile emplaced at the end of the 1996–1997 excavation marks the discovery site today. www.sciencemag.org
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Pieces were assigned number suffixes based on recovery order. Back-dirt was weathered in place and resieved. The 1995 field season yielded facial fragments and a few other elements in northern and eastern extensions of the initial excavation. Further excavation in 1996 exposed no additional remains. Each fragment’s position, axial orientation, and dip were logged relative to a datum (strata here dip east at ~4° to 5°). A polygon representing the outer perimeter and vertical extent of the hominid fragment constellation (based on each bone’s center point) was demarcated by a carapace of limestone blocks cemented with concrete after excavation, then further protected by a superimposed pile of boulders, per local Afar custom.
Fig. 3. The ARA-VP-6/500 skeleton. This is a composite photograph to show the approximate placement of elements recovered. Some pieces found separately in the excavation are rejoined here. Intermediate and terminal phalanges are only provisionally allocated to position and side.
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Ardipithecusramidus ramidus Ardipithecus The skeleton was scattered in typical Lower Aramis Member sediment (Fig. 2): fine-grained, massive, unslickensided, reddish-brown alluvial silty clay containing abundant decalcified root casts, fossil wood, and seeds. A 5- to 15-cm lens of poorly sorted sand and gravel lies immediately below the silty clay, and the spread of cranial parts to the north suggests that the bones of the carcass came to rest in a shallow swale on the floodplain. There is no evidence of weathering or mammalian chewing on ARA-VP-6/500. Bony elements were completely disarticulated and lacked anatomical association. Many larger elements showed prefossilization fragmentation, orientation, and scatter suggestive of trampling. The skull was particularly affected, and the facial elements and teeth were widely scattered across the excavated area. Bioturbation tilted some phalanges and metacarpals at high dip angles (Fig. 2). A few postcrania of a large Aquila (eagle) and other birds were recovered during excavation, as were a few micromammals. No largemammal remains (except isolated cercopithecid teeth and shaft splinters from a medium-to-large mammal limb bone) were associated. The cause of death is indeterminate. The specimen is judged to be female. The only pathology is a partially healed osteolytic lesion suggestive of local infection of the left proximal ray 5 pedal phalanx (ARA-VP-6/500-044). Laboratory exposure and consolidation of the soft, crushed fossils were accomplished under binocular microscope. Acetone was applied with brushes and hypodermic needles to resoften and remove small patches of consolidant-hardened encasing matrix. Microsurgery at the interface between softened matrix and bone proceeded millimeter by submillimeter, rehardening each cleaned surface with consolidant after exposure. This process took several years. The freed specimens remain fragile and soft, but radiographic accessibility is excellent. Most restoration and correction for distortion were accomplished with plaster replicas or micro–computed tomography digital data to preserve the original fossils in their discovery state. Environmental context. The Lower Aramis Member lacks any evidence of the hydraulic mixing that afflicts many other hominid-bearing assemblages. The unwarranted inference that early hominids occupied “mosaic habitats” (38) is often based on such mixed assemblages, so the resolution and fidelity of the Aramis environmental data sets are valuable. We estimate that the interval of time represented by the strata between the two tuffs at Aramis is 6.0 to 4.2 Ma). By priority, the name Ardipithecus may encompass other named genera at this adaptive plateau (12, 15). The question of whether Ar. ramidus is ancestral to later hominids is moot for some cladists because they consider ancestors inherently unrecognizable and therefore recognize only sister taxa (76). The fossils reported here make it even more obvious that Ar. ramidus is the cladistic sister to Australopithecus/Homo because it shares primitive characters with earlier hominids and apes but at the same time exhibits many important derived characters that are shared exclusively only with later hominids (Table 1). Species-level phylogenetics are more difficult to discern given the sparse geographic and temporal distribution of available fossils (Fig. 5). Primitive characters seen in Ar. ramidus persist most markedly in its apparent (but still poorly sampled) sister species Au. anamensis and, to a lesser degree, in Au. afarensis. The known dental and mandibular remains of Au. anamensis are temporally and morphologically intermediate between those of Ar. ramidus and Au. afarensis, with variation that overlaps in both directions. Its constellation of primitive and derived features of the mandible, CP3 complex, lower dm1 (lower first deciduous molar), and postcanine dentition lends support to the hypothesis of an evolutionary sequence of Ar. ramidus → Au. anamensis → Au. afarensis (7, 8, 77). Circumstantial evidence supporting this hypothesis is the temporal and geographic position of Ar. ramidus directly below the first known appearance of Au. anamensis within the Middle Awash succession. Here, these taxa are stratigraphically superimposed in the same succession, separated by ~80 vertical meters representing ~200,000 to 300,000 years (7). Au. afarensis appears later in the same sequence [3.4 Ma, at Maka (53)]. Therefore, at one end of a spectrum of phylogenetic possibilities, Ar. ramidus may have been directly ancestral to the more derived chronospecies pair Au. anamensis → Au. afarensis across the full (still unknown, presumably African) species range (7, 8, 77) (Fig. 5A). Although Au. afarensis is well represented in craniodental remains and postcrania, its apparent earlier chronospecies Au. anamensis is still woefully underrepresented in both, and because Ar. ramidus is so far known only from limited time horizons and locations, its last appearance, date, and potential relationship to these later taxa are still indeterminate. Given the dramatic differences in postcranial anatomy seen in later Australopithecus and hinted at in known Au. anamensis, it seems likely that a major adaptive shift marked the Ardipithecus-to-Australopithecus transition (whenever and wherever the transition might have occurred and whatever its population dynamics). This transition may not have occurred through
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Research Articles RESEARCH ARTICLES pan-specific phyletic evolution (Fig. 5A). Figure 5 presents two other phylogenetic hypotheses that are also, at present, impossible to falsify. If diagnostic contemporary fossils of Au. anamensis are someday found in rocks of >4.4 Ma, the hypothesis that the Afar population of Ar. ramidus is the phyletic ancestor of Au. anamensis (Fig. 5A, B) would be falsified. In such an eventuality, Aramis Ar. ramidus would represent a persisting relict population of the mother species (Fig. 5C). Given the lack of relevant fossils, it is currently impossible to determine whether there was a geologically rapid phyletic transition between Ardipithecus and Australopithecus in the Middle Awash or elsewhere. Nevertheless, the morphological and ecological transition between these two adaptive plateaus is now discernible. Ardipithecus and Australopithecus. For Darwin and Huxley, the basic order in which human anatomies, physiologies, and behaviors were assembled through time was unknown— indeed unknowable—without an adequate fossil record. They were forced to employ extant ape proxies instead. The latter are now shown to be derived in ways unrelated to the evolution of hominids. The Aramis fossils help clarify the origin of the hominid clade (27, 31), and reveal some paleobiological dimensions of the first hominid adaptive plateau (Ardipithecus). The primitive characters of Ar. ramidus simultaneously provide a new perspective on the evolutionary novelties of Australopithecus. Even in the wake of the Aramis and Gona discoveries, the morphological envelopes, phylogenetic relationships, and evolutionary dynamics of early hominid species remain incompletely understood (Fig. 5). However, the paleobiology of Ar. ramidus—even when viewed through its geographically and temporally restricted Afar samples—now reveals that the basal hominid adaptive plateau comprised facultatively bipedal primates with small brains, reduced nonhoning canines, unspecialized postcanine dentitions, and arboreally competent limb skeletons. Their ecological niche(s) were probably more restricted— and their geographic distribution(s) possibly smaller and more disjunct—than those of later hominid species and genera. The derived postcranial elements of Australopithecus provide a strong contrast to their more primitive homologs in Ardipithecus (78). Relative to the generalized anatomy of the latter, the highly evolved specializations of the foot, ankle, knee, pelvis, wrist, and hand of Au. afarensis (79–81) indicate that this species lineage had largely abandoned locomotion in the arboreal canopy (and its resources). Given the strong selection predicted to have been associated with the emergence of new ranging and feeding patterns in Australopithecus, the transition from Ardipithecus to Australopithecus could have been rapid, and anatomically particularly so in hindlimb structure. The forelimb
(especially the hand) was probably under less intensive selection. It is possible that modification of general cis-regulatory pathways may have generated the striking and novel morphology of the hindlimb, especially the foot, because the autopod seems to be the most morphologically compliant to such mechanisms of modification. The dentognathic shifts could have been more gradational, whatever the mode of phylogenesis. Homo and Australopithecus are the only primates with nongrasping feet, and this particular transformation was probably far-reaching, with consequences for key behavioral constancies in higher primates related to arboreal feeding and nesting. Without stabilizing selection for Ardipithecus-like arboreal capacities involving slow and careful climbing, the foot, pelvis, and thigh would have experienced directional selection to optimize bipedal locomotion during prolonged walking (also in more limited running bouts). With expanded ranging and social adaptations associated with terrestrial feeding in increasingly open environments, the transition could have been profound, but probably rapid, and therefore difficult to probe paleontologically. One possible dynamic of an Ardipithecusto-Australopithecus transition would have involved microevolution within a deme or regional group of demes. Being more ecologically flexible, the derived, potentially speciated populations would have undergone rapid range expansion, perhaps even encountering relict Ardipithecus populations. Unfortunately, the phylogeographic details remain obscure given the poor spatial and temporal resolution of the current fossil record (Fig. 5). This provides a strong incentive for pursuing that record by actively increasing sampling of sediments from different African basins with dates between ~5 and ~3.5 Ma. Currently, Australopithecus appears relatively abruptly in the fossil record at about 4.2 Ma. Relative to Ar. ramidus, available early Australopithecus is now revealed to have been highly derived: a committed biped with slightly enlarged brain, a nongrasping arched foot, further derived canines, substantially specialized postcanine teeth with thick molar enamel, and expanded ecological tolerances and geographic ranges. It is widely recognized that this is the adaptive plateau antecedent to Homo, which is now definable as the third such major adaptive shift in human evolution. Commitment to the terrestrial ranging behaviors of Australopithecus well before the Pleistocene appear to have catalyzed the emergence of what must have been even more highly specialized social and ecological behaviors remarkably elaborated in descendant Homo— the ultimate global primate generalist. Conclusions. Besides hominids, the only apes to escape post-Miocene extinction persist today as relict species, their modern distributions centered in forested refugia. The markedly primitive Ar. ramidus indicates that no modern ape is a realistic proxy for characterizing early hominid
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evolution—whether social or locomotor—as appreciated by Huxley. Rather, Ar. ramidus reveals that the last common ancestor that we share with chimpanzees (CLCA) was probably a palmigrade quadrupedal arboreal climber/clamberer that lacked specializations for suspension, vertical climbing, or knuckle-walking (24–27). It probably retained a generalized incisal/postcanine dentition associated with an omnivorous/frugivorous diet less specialized than that of extant great apes (22, 23). The CLCA probably also combined moderate canine dimorphism with minimal skull and body size dimorphism (22, 23), most likely associated with relatively weak male-male agonism in a male philopatric social system (22, 23, 31). Ardipithecus reveals the first hominid adaptive plateau after the CLCA. It combined facultative terrestrial bipedality (25, 26) in a woodland habitat (28–30) with retained arboreal capabilities inherited from the CLCA (24–27). This knowledge of Ar. ramidus provides us, for the first time, with the paleobiological substrate for the emergence of the subsequent Australopithecus and Homo adaptive phases of human evolution. Perhaps the most critical single implication of Ar. ramidus is its reaffirmation of Darwin’s appreciation: Humans did not evolve from chimpanzees but rather through a series of progenitors starting from a distant common ancestor that once occupied the ancient forests of the African Miocene. References and Notes
1. C. Darwin, The Descent of Man, and Selection in Relation to Sex (John Murray, London, 1871). 2. We here consider Hominidae to include modern humans and all taxa phylogenetically closer to humans than to Pan (common chimpanzee and bonobo), that is, all taxa that postdate the split between the lineage leading to modern humans and the lineage that led to extant chimpanzees. 3. T. H. Huxley, Evidence as to Man’s Place in Nature (London, 1863). 4. V. M. Sarich, A. C. Wilson, Proc. Natl. Acad. Sci. U.S.A. 58, 142 (1967). 5. D. C. Johanson, M. Taieb, Y. Coppens, Am. J. Phys. Anthropol. 57, 373 (1982). 6. M. D. Leakey et al., Nature 262, 460 (1976). 7. T. D. White et al., Nature 440, 883 (2006). 8. W. H. Kimbel et al., J. Hum. Evol. 51, 134 (2006). 9. G. WoldeGabriel et al., Nature 371, 330 (1994). 10. T. D. White, G. Suwa, B. Asfaw, Nature 371, 306 (1994). 11. Y. Haile-Selassie, Nature 412, 178 (2001). 12. Y. Haile-Selassie, G. Suwa, T. D. White, in Ardipithecus kadabba: Late Miocene Evidence from the Middle Awash, Ethiopia, Y. Haile-Selassie, G. WoldeGabriel, Eds. (University of California, Berkeley, CA, 2009), pp. 159–236. 13. B. Senut et al., Comptes Rendus de l’Academie des Sciences, Series IIA: Earth and Planetary Science 332, 137 (2001). 14. M. Brunet et al., Nature 418, 145 (2002). 15. Y. Haile-Selassie, G. Suwa, T. D. White, Science 303, 1503 (2004). 16. J. Moore, in Great Ape Societies, W. C. McGrew et al., Eds. (Cambridge Univ. Press, Cambridge, 1996), pp. 275–292. 17. B. G. Richmond, D. R. Begun, D. S. Strait, Yearb. Phys. Anthropol. 44, 70 (2001). 18. R. Wrangham, D. Pilbeam, in All Apes Great and Small, Volume 1: African Apes, B. Galdikas et al., Eds. (Kluwer Academic/Plenum, New York, 2001), pp. 5–17. 19. J. T. Stern, R. L. Susman, Am. J. Phys. Anthropol. 60, 279 (1983).
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Ardipithecusramidus ramidus Ardipithecus 20. J. T. Stern, Evol. Anthropol. 9, 113 (2000). 21. B. Latimer, in Origines de la Bipedie chez les Hominides, B. Senut, Y. Coppens, Eds. (Editions CNRS, Paris, 1991), pp. 169–176. 22. G. Suwa et al., Science 326, 69 (2009). 23. G. Suwa et al., Science 326, 68 (2009). 24. C. O. Lovejoy et al., Science 326, 70 (2009). 25. C. O. Lovejoy et al., Science 326, 71 (2009). 26. C. O. Lovejoy et al., Science 326, 72 (2009). 27. C. O. Lovejoy et al., Science 326, 73 (2009). 28. G. WoldeGabriel et al., Science 326, 65 (2009). 29. A. Louchart et al., Science 326, 66 (2009). 30. T. D. White et al., Science 326, 67 (2009). 31. C. O. Lovejoy, Science 326, 74 (2009). 32. H. Gilbert, B. Asfaw (Eds.), Homo erectus: Pleistocene Evidence from the Middle Awash, Ethiopia (Univ. California Press, Berkeley, CA, 2008). 33. Y. Haile-Selassie, G. WoldeGabriel (Eds.), Ardipithecus kadabba: Late Miocene Evidence from the Middle Awash, Ethiopia (Univ. California Press, Berkeley, California, 2009). 34. P. R. Renne, G. WoldeGabriel, W. K. Hart, G. Heiken, T. D. White, Geol. Soc. Am. Bull. 111, 869 (1999). 35. In 1994, the Middle Awash project instituted “crawls” of sedimentary outcrop between the GATC and DABT to collect all available fossil material. Crawls were generally upslope in direction, done by teams of 5 to 15 collectors who crawled the surface on hands and knees, shoulder to shoulder, collecting all fossilized biological materials between a prescribed pair of taut nylon cords. Surfaces were repeatedly collected with this technique, invariably resulting in successively depressed specimen recovery numbers in subsequent field seasons. 36. S. Semaw et al., Nature 433, 301 (2005). 37. No surface or in situ fragments of the ARA-VP-6/500 specimen are duplicate anatomical elements. Only 7.3% of 136 total pieces (table S2) were surface recoveries at the excavation site. All other pieces were excavated in situ. Preservation is identical across the entire recovered set. There is no evidence of multiple maturational ages among the 136 pieces, and many of them conjoin. Given the close stratigraphic and spatial association (Fig. 2), and given no evidence of any other individual from the carefully excavated spatiostratigraphic envelope, we conclude that the parts of the ARA-VP-6/500 specimen represent a single individual’s disarticulated skeleton. 38. S. Elton, J. Anat. 212, 377 (2008). 39. A. K. Behrensmeyer, Paleobiology 8, 211 (1981). 40. S. M. Kidwell, K. W. Flessa, Annu. Rev. Earth Planet. Sci. 24, 433 (1996). 41. D. Western, A. K. Behrensmeyer, Science 324, 1061 (2009). 42. R. Pik, B. Marty, J. Carignan, J. Lavé, Earth Planet. Sci. Lett. 215, 73 (2003). 43. A. V. Fedorov et al., Science 312, 1485 (2006). 44. T. D. White, G. Suwa, B. Asfaw, Nature 375, 88 (1995). 45. A. Hill, S. Ward, Yearb. Phys. Anthropol. 31, 49 (1987). 46. M. G. Leakey, J. M. Harris, Eds., Lothagam: The Dawn of Humanity in Eastern Africa (Columbia Univ. Press, New York).
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75. 76. 77. 78.
79. 80. 81. 82. 83.
Without such selection, Ar. ramidus as a species probably contained regional populations that varied in premolar root number (22). B. Senut, M. Pickford, C. R. Palevol. 3, 265 (2004). H. Gee, Deep Time: Cladistics, the Revolution in Evolution (Free Press, London, 1999). C. V. Ward, A. C. Walker, M. G. Leakey, Evol. Anthropol. 7, 197 (1999). We use genera to express both phyletic proximity and circumscribed adaptive systems, with ecobehavioral and morphological conditions being integral parts of the latter. This use employs the broadly defined genus Australopithecus, without recognizing the now commonly used Paranthropus (82). This is because both “robust” and “nonrobust” Australopithecus species are characterized by a commonly derived heavy masticatory apparatus (albeit to differing degrees), and also because we cannot—even to this day—be certain that the “robust” species are monophyletic. C. O. Lovejoy, Gait Posture 21, 95 (2005). C. O. Lovejoy, Gait Posture 21, 13 (2005). C. O. Lovejoy, Gait Posture 25, 325 (2007). T. D. White, in The Primate Fossil Record, W. Hartwig, Ed. (Cambridge Univ. Press, Cambridge), pp. 407–417. For funding, we thank NSF (this material is based on work supported by grants 8210897, 9318698, 9512534, 9632389, 9729060, 9727519, 9910344, and 0321893 HOMINID-RHOI), the Institute of Geophysics and Planetary Physics of the University of California at Los Alamos National Laboratory (LANL), and the Japan Society for the Promotion of Science. D. Clark and C. Howell inspired this effort and conducted laboratory and field research. We thank the coauthors of the companion papers (22-30), with special thanks to the ARA-VP-6/500 and -7/2 excavation teams, including A. Amzaye, the Alisera Afar Clan, Lu Baka, A. Bears, D. Brill, J. M. Carretero, S. Cornero, D. DeGusta, A. Defleur, A. Dessie, G. Fule, A. Getty, H. Gilbert, E. Güleç, G. Kadir, B. Latimer, D. Pennington, A. Sevim, S. Simpson, D. Trachewsky, and S. Yoseph. G. Curtis, J. DeHeinzelin, and G. Heiken provided field geological support. D. Helgren, D. DeGusta, L. Hlusko, and H. Gilbert provided insightful suggestions and advice. We thank H. Gilbert, K. Brudvik, L. Bach, D. Paul, B. Daniels, and D. Brill for illustrations; G. Richards and A. Mleczko for imaging; the Ministry of Tourism and Culture, the Authority for Research and Conservation of the Cultural Heritage, and the National Museum of Ethiopia for permissions and facilitation; and the Afar Regional Government, the Afar people of the Middle Awash, and many other field workers who contributed directly to the research efforts and results.
Supporting Online Material www.sciencemag.org/cgi/content/full/326/5949/64/DC1 SOM Text Tables S1 and S2 References 4 May 2009; accepted 8 September 2009 10.1126/science.1175802
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The Geological, Isotopic, Botanical, Invertebrate, and Lower Vertebrate Surroundings of Ardipithecus ramidus Giday WoldeGabriel,1* Stanley H. Ambrose,2 Doris Barboni,3 Raymonde Bonnefille,3 Laurent Bremond,4 Brian Currie,5 David DeGusta,6 William K. Hart,5 Alison M. Murray,7 Paul R. Renne,8 M. C. Jolly-Saad,9 Kathlyn M. Stewart,10 Tim D. White11* Sediments containing Ardipithecus ramidus were deposited 4.4 million years ago on an alluvial floodplain in Ethiopia’s western Afar rift. The Lower Aramis Member hominid-bearing unit, now exposed across a >9-kilometer structural arc, is sandwiched between two volcanic tuffs that have nearly identical 40Ar/39Ar ages. Geological data presented here, along with floral, invertebrate, and vertebrate paleontological and taphonomic evidence associated with the hominids, suggest that they occupied a wooded biotope over the western three-fourths of the paleotransect. Phytoliths and oxygen and carbon stable isotopes of pedogenic carbonates provide evidence of humid cool woodlands with a grassy substrate.
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rdipithecus ramidus and abundant associated faunal and floral fossils were recovered from sedimentary rocks in the Central Awash Complex (CAC) of the Middle Awash study area. The CAC is a complexly faulted dome centered 25 km east of the western rift margin, Afar, Ethiopia. Today, 300 m of strata deposited between 5.6 and 3.9 million years ago (Ma) are exposed in the CAC (1). The hominidbearing Lower Aramis Member of the Sagantole Formation lies midway in this stratigraphic succession and crops out along an erosional arc >9 km across, extending from the Ounda Sagantole drainage in the southeast to Aramis Locality 6 in the north, and to Kuseralee Locality 2 to the southwest (Fig. 1). Here, we describe regional and local geology, and present isotopic, paleobotanical, invertebrate, and lower vertebrate fossil evidence that illuminates local conditions at the time the vertebrate fossils were deposited. Geology. The Aramis Member directly overlies the Gàala (“Camel”) Tuff Complex (GATC), 1
Earth Environmental Sciences Division, Los Alamos National Laboratory, Los Alamos, NM 87545, USA. 2Department of Anthropology, University of Illinois, Urbana, IL 61801, USA. 3 CEREGE (UMR6635 CNRS/Université Aix-Marseille), BP80, F-13545 Aix-en-Provence Cedex 4, France. 4Center for BioArchaeology and Ecology (UMR5059 CNRS/Université Montpellier 2/EPHE), Institut de Botanique, F-34090 Montpellier, France. 5Department of Geology, Miami University, Oxford, OH 45056, USA. 6Department of Anthropology, Stanford University, Stanford, CA 94305, USA. 7Department of Biological Sciences, University of Alberta, Edmonton, Alberta T6G 2E9, Canada. 8Berkeley Geochronology Center, 2455 Ridge Road, Berkeley, CA 94709, USA, and Department of Earth and Planetary Science, University of California, Berkeley, CA 94720, USA. 9Université Paris-Ouest La Défense, Centre Henri Elhaï, 200 Avenue de la République, 92001 Nanterre, France. 10 Paleobiology, Canadian Museum of Nature, Ottawa, Ontario K1P 6P4, Canada. 11Human Evolution Research Center and Department of Integrative Biology, 3101 Valley Life Sciences Building, University of California, Berkeley, CA 94720, USA. *To whom correspondence should be addressed. E-mail:
[email protected] (T.D.W.);
[email protected] (G.W.)
which has a 40Ar/39Ar age of 4.419 T 0.068 Ma (2, 3). This vitric tuff is 0.5 to 2 m thick and is rich in pumice and crystals. The Aramis Member includes light salmon (hue 5YR) to deep redbrown silt, clay, and sand of variable thickness and induration, deposited on a floodplain. These strata show a general increase in thickness toward the east, and they range from an average of 3 m up to 6 m. They are overlain by the Daam Aatu (“Baboon”) Basaltic Tuff (DABT), which has a 40 Ar/39Ar age of 4.416 T 0.031 Ma (1). We define the Lower Aramis Member as the entirety of both tuffs and all sediments between them. A patchwork of variably fossiliferous localities along the outcrop arc has yielded a combined total of more than 6000 individually cataloged vertebrate fossils between the widespread volcanic marker horizons. The vertebrate assemblages are in close association with sedimentological and structural information, botanical and invertebrate fossils, and oxygen and carbon isotopic data on pedogenic carbonates in soil horizons. Integration of these data allows reconstruction of the physical and biological aspects of the depositional setting. The Middle Awash was a persistent sedimentary basin during the Pliocene (4). The basin axis during deposition of the entire Aramis Member was southeast of the Ardipithecus localities, as evidenced by deltaic and lake margin deposits generally disposed to the southeast, in the direction of paleocurrent orientations and erosional features. Active volcanic centers of the CAC were located to the south (1). Paleoenvironmental data and structural reconstructions suggest that the overall elevation may have been greater than today’s ~600 m, although kinematic models are equivocal (5, 6). The lower tuff (GATC) is underlain by a widespread cobble conglomerate. In the central part of the exposure arc, fossiliferous Lower
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Aramis Member sediments comprise predominantly massive and bioturbated silty clays deposited primarily on a low-relief floodplain far from the main river channel(s). Reworked GATC pumices and glass are present locally, but evidence of channels is limited to rare sandstone lenses generally situated below the fossiliferous strata. Massive (1.5 box lengths from quartile box boundary)].
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Lateral metatarsals. ARA-VP-6/1000 is a right Mt2 lacking its head and the plantar portion of its base (Fig. 4). However, both plantar cornua are preserved, thereby permitting reasonable reconstruction of its length. The base is large. The ratio of basal height as preserved (no reconstruction or estimation) to metatarsal length lies in the upper range of Homo (fig. S4). ARAVP-6/1000 exhibits only minimal longitudinal curvature (Fig. 4) but exhibits substantial shaft torsion, which orients it for opposition with the Mt1, as in extant African apes (fig. S5). ARA-VP6/500 lacks an intact Mt2, but its intermediate cuneiform also allows comparison of the joint’s dorsoplantar Mt2 facet height with an estimate of body size. This ratio lies near the upper limit of the human range and outside the ranges of the African apes (fig. S6), suggesting a similarly robust base size in ARA-VP-6/500. The Mt2’s large base is readily explicable in light of its role as the foot’s medial mainstay during bipedal toe-off. The dorsal edge of ARAVP-6/1000’s proximal joint surface exhibits paired chondral invaginations (Fig. 4) that are rare in the Mt2s of either gorillas or chimpanzees [one single (lateral) facet in N = 50]. These cannot reflect habitual contact with the intermediate cuneiform, as this would require impossible joint cavitation. Nor does the intermediate cuneiform of ARA-VP-6/500 or any other higher primate bear matching projections; there are, instead, slight corresponding invaginations of its dorsal surface as well. Each invagination of the Mt2’s dorsal surface lies just proximal to medial and lateral rugosities. In humans, these mark receipt of medial and lateral expansions of the joint’s dorsal capsule [(34); this study]. Habitual, intermittent pressure against these local tarsometatarsal joint expansions almost certainly induced the paired subchondral depressions in the Aramis bone’s dorsal surface. Their probable etiology [chondral modeling; type 4 (4)] is therefore informative. Substantial spiraling of the Mt2 shaft places the bone’s distal end into functional opposition to the Mt1 in African apes and would have done so in Ar. ramidus (35). Such torsion is most pronounced in the Mt2 because it lies adjacent to the hallux, and because Mt2 rotation is restricted by the mortising of its base between the medial cuneiform and lateral cuneiform/Mt3 laterally. The bases of the more lateral rays are less restricted and thus have (progressively) less prestructured torsion. The developmental biology of tendon and ligament attachments is complex (36), but a markedly rugose insertion likely signals substantial Sharpey fiber investment via pattern formation (37). This is especially the case for eutherian tarsometatarsal joints, which appear to have sacrificed their proximal metapodial growth plate to encourage a more rigid syndesmosis (38). The markedly rugose tarsometatarsal joint capsule in the Ar. ramidus Mt2 suggests that it was an adaptation [direct selection acting on
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Research Articles RESEARCH ARTICLES morphogenetic fields; type 1 (4)] to upright walking and running, absent any substantial loadsharing by a still abducent great toe. Moreover, the total morphological pattern of the Ar. ramidus foot suggests that it exhibited a noninverted footflat during midstance [i.e., unlike that of Pan (23–27)]. The primary terrestrial role of the hallux, as in apes, would have been for balance rather than for propulsion (but see below). Powerful fulcrumation occurred only on the lateral metatarsal heads in Ar. ramidus, especially that of the Mt2, whose role in humans remains especially prominent in bipedality even after having been reinforced by the addition of a permanently adducted Mt1. ARA-VP-6/505 is a virtually intact left Mt3 (Fig. 4). Its preserved head shows two particularly important characters. First, it exhibits dorsal doming in excess of African ape metatarsals. Second, a deep-angled gutter isolates the head
from the shaft at the dorsal epiphyseal junction. Although a similar gutter is also found in ape metatarsals, it is considerably shallower, consistent with substantially less loading and excursion during metatarsophalangeal joint (MP) dorsiflexion [cartilage modeling; type 4 (4)]. Moreover, in ARA-VP-6/505, the angle between the head’s dorsoplantar axis and the dorsoplantar axis of its base shows slight external torsion of the shaft, which would have optimized MP joint alignment during toe-off. This implies that growth plate loading during terrestrial bipedality predominated over that generated during grasping (i.e., it exhibits far less torsion than the Mt2, and also lacks the medial and lateral joint capsule compression facets present in ARA-VP-6/1000). The gutter also implies that loading during terrestrial bipedality was applied during substantial toe-out during and after heel-off, coupled with external rotation of the foot during late toe-off. Pro-
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nounced doming is entirely absent in the ARAVP-6/500 Mt1, confirming that the first ray did not participate substantially in propulsion (fig. S12). Doming is present in the Au. afarensis Mt1, again implying terrestrial bipedality with a permanently adducted great toe. The shaft of the ARA-VP-6/505 Mt3 is only slightly curved (Fig. 4) and its base is well preserved, lacking only a minor portion of its superomedial corner. Its base morphology is remarkably similar to that of the human Mt3 in having a dorsoplantarly tall proximal articular surface (Fig. 4 and fig. S7). African ape Mt3 bases are instead regularly subdivided into distinct upper and lower portions by deep semicircular notches of their medial (for Mt2) and lateral (for Mt4) surfaces (Fig. 4 and Table 1). These serve as passageways and surfaces for tarsometatarsal and transverse intermetatarsal ligaments. The abbreviated dorsoplantar height and distinctly rhom-
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Fig. 3. Natural history of the hominoid midfoot. (A) The os peroneum. This sesamoid (white arrow in a ligamentous preparation of Papio anubis) is a large and prominent inclusion in the fibularis longus tendon of Old World monkeys, residing on an appropriately D E large inferolateral facet of the cuboid. In Old World monkeys, the muscle inserts at the Mt1 base, acting as both plantarflexor and hallucal adductor. Because some flexion can occur at both the calcaneocuboid and tarsometatarsal joints during climbing and terrestrial walking (9, 23, 24, 27), the fibularis longus tendon also aids plantar rigidity during plantarflexion. (B to E) Plantar surfaces of hominoid cuboids. (B) Chimpanzee (CMNH-1726). In apes, the cuboid is anteroposteriorly short and the groove in which the fibularis longus tendon lies is narrow and deep, usually with high walls. It is converted to a retaining tunnel by a homolog of the human short plantar ligament (56–58). Ape cuboids essentially lack functional os peronei [they occasionally contain small, nonfunctional, chondral bodies (31)]. (C) ARA-VP6/500-081. In Ar. ramidus the surface medial to the facet over which the tendon must pass is rugose and subperiosteal, confirming that a laterally placed os peroneum elevated its travel on the facet. (D) Human (KSU-01206). (E) OH-8 (cast; reversed). In these later hominids, the fibularis longus no longer lies in the cuboidal groove, but is instead elevated above and posterior to it by the os peroneum residing on a facet located proximolateral on the groove’s proximal wall (white arrows) (32). Unlike Ar. ramidus, the fibularis longus inserts into the medial cuneiform and no longer adducts the first ray. Scale bar, 2 cm. (F) Natural log-log scatterplot of medial cuboid length and cube root of estimated body mass in extant anthropoids (42). A regression line (reduced major axis; y = 1.184x + 1.666; r = 0.836, N = 26) has been fitted to the combined cercopithecines and colobines. The most parsimonious interpretation of these data is that cuboid length in Ar. ramidus is primitive, and that the bone was elongated in later hominids (including elongation of its calcaneal process) but shortened in African apes in order to enhance hallucal grasping and plantar compliance to substrates during vertical climbing. The ranges and medians for a similar metric clarify these relationships in fig. S2. 2 OCTOBER 2009
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Ardipithecusramidus ramidus Ardipithecus boidal form of African ape Mt2 and Mt3 bases [direct selection acting on morphogenetic fields; type 1 (4)] permit more plantar conformity and tarsometatarsal laxity during grasping, consistent with recent observations that the midtarsal break combines motion at both the lateral tarsometatarsal and midtarsal joints (figs. S4 and S6 to S9) (9, 23, 24, 27). ARA-VP-6/505 lacks this distinctive central notching morphology. This presumably reflects retention of soft tissue structures similar to those of humans. These enhance midtarsal and tarsometatarsal bending resistance from foot-flat through toe-off, ultimately culminating in the emergence of the proximal part of the long plantar ligament, which is likely derived in humans (13, 33). These conclusions receive strong support from geometric analysis of joint surface section moduli of the Mt3 (figs. S8 and S9). Phalanges. Several proximal pedal phalanges from the lateral rays of Ar. ramidus preserve a base. Three are complete with proximal ends evincing clear, typically hominid dorsiflexive cants (figs. S10 and S11). Canting is more pronounced in modern humans as a consequence of the reduction of phalangeal curvature (39) (fig. S10) and abbreviation of the intermediate phalanx (figs. S12 and S13). Phalangeal shape ratios (40) are not particularly informative, but they do show that Ar. ramidus phalanges are moderately robust (i.e., like those of Pan and Proconsul and unlike those of Ateles or Hylobates), with moderately deep trochleas. Midshaft robusticity is similar to that in Pan, Proconsul, and most Old World monkeys. Manual/pedal phalangeal ratios are like those in extant hominoids and unlike those in Proconsul [for discussion see (40, 41)]. When complete phalanges from ray 4 of ARA-VP-6/500 are normalized by body size, their lengths fall near the Gorilla mean but below values in Pan, which may have therefore witnessed substantial phalangeal elongation since the last common ancestor of African apes and humans (fig. S13) [for further discussion, see (42)]. Pedal phalanges in Ar. ramidus are relatively shorter than those of New World monkeys
(regardless of locomotor pattern), orangutans, and gibbons. Phalangeal curvature is moderate to large. The included angle of ARA-VP-6/500-094, an intact proximal phalanx of the fourth pedal ray, is 58°. However, its base is substantially canted, which obscures its joint angulation in lateral view. Expansion of the apical tufts of the terminal phalanges is moderate. The first ray during terrestrial gait. The dorsal articular margin of the Mt1 head of ARAVP-6/500 preserves detailed evidence of how Ar. ramidus used its foot in some locomotor settings. Its dorsal surface bears two symmetrically placed and equal-sized V-shaped facets separated by a central nonarticular isthmus (Fig. 3). Each facet appears to have been generated by axial rotation of the ray’s proximal phalanx at its MP joint [cartilage modeling; type 4 (4)]. The Mt1’s dorsolateral facet was presumably generated during grasping by external rotation of both the Mt1 and its proximal phalanx, which would have brought the hallux into opposition with the lateral foot. The Mt1’s dorsomedial facet would then have been generated by internal rotation that occurred when the foot was emplaced on a terrestrial substrate with the first ray in substantial abduction (because it exhibits no doming; see above). This Ar. ramidus morphology is especially notable because of its remarkable symmetry. Although similar rotation facets occur regularly on the Mt1s of both Pan and Gorilla, they are most often asymmetrical and also appear to be generally deeper. In some Gorilla specimens, the medial facet is more prominent than the lateral, which suggests that during terrestrial locomotion, greater relative loads were imposed on its Mt1s than in Ar. ramidus. This would at first seem to be a paradox, because the African apes are not habitual bipeds. However, Ar. ramidus retained primitive features [a prominent os peroneum, substantial tarsometatarsal joint rigidity, a long midtarsus, and soft tissue characters that likely accompanied these (Table 2)] that allowed powerful plantarflexion
about its lateral metatarsal heads, including what must have been a substantial contribution by its peroneal compartment. The African apes, by contrast, have lost such capacity in favor of substantial midtarsal laxity. This has greatly compromised the plantarflexor impulse on their lateral metatarsal heads. Partial accommodation appears to be provided by occasional or even regular impulse by their Mt1 during terrestrial gait. The Mt1s of Australopithecus lack any evidence of comparable facets (15). This, and the prominent doming of their Mt1, now serve as further confirmation that the taxon lacked any first-ray abduction, and almost certainly exhibited a longitudinal arch—features that are consistent with their derived ankle morphology (8, 9, 15, 23, 24) and the Laetoli footprints (43). Interpretations and dynamics. Ar. ramidus is the only known hominid with an abducent great toe (15, 16, 44). Its foot, along with other postcranial elements, indicates that the Late Miocene hominid precursors of Ar. ramidus practiced mixed arboreal and terrestrial locomotion during which the lateral forefoot became extensively adapted to upright walking, even as the medial forefoot retained adaptations for arboreal exploitation. During the gait cycle, fibularis longus contraction would also have stabilized the proximal ankle joints. The moderate to strong talar declination of the angle between the trochlea and that of the ankle’s axis of rotation, in combination with clear evidence of abductor stabilization of the hip during stance phase (11), together suggest that the foot was placed near midline. The knee may have been in greater external rotation than is typical in human and Australopithecuslike (i.e., accentuated) valgus (10), with compensation by means of a more extensive range of knee rotation throughout stance phase. Ar. ramidus therefore may have lacked the consistently elevated bicondylar angle of Australopithecus. Ar. ramidus likely relied on situationally dependent lordosis to generate functional hip abduction (minimum pelvic tilt) during stance
Table 1. Talus, cuboid, Mt1, Mt5, and Mc5 (fifth metacarpal) metrics in Ar. ramidus and other anthropoids. Values in parentheses, except for the leftmost column, denote standard deviation. Taxon (N) Old World monkeys (27) New World monkeys (11) Homo (30) Australopithecus and early Homo (12) ARA-VP-6/500 Pan (26) Gorilla (29) Pongo (16)
Angle between trochlear axis and talocrural rotation axis (°)*
Max. cuboid length†/body size‡
Mt1/body size‡
Mc5/body size‡
Mt5/body size‡
Mc5/Mt5
13.2 (2.2)§
1.51 (0.13) 1.48 (0.12) 1.81 (0.10)
4.4 (0.40) 4.7 (0.22) 3.9 (0.18)
4.2 (0.30) 4.5 (0.85) 2.6 (0.17)
6.6 (0.43) 6.6 (0.14) 4.6 (0.13)
0.73 (0.07) 0.80 (0.06) 0.75 (0.04)
1.41 1.15 (0.06) 1.14 (0.08) 1.18 (0.16)
4.1 4.1 (0.31) 3.6 (0.25) 3.6 (0.22)
3.2 4.3 (0.26) 3.8 (0.24) 5.3 (0.39)
4.9 5.1 (0.07) 4.9 (0.10) 6.7 (0.11)
0.87 1.12 (0.07) 1.02 (0.03) 1.03 (0.05)
10.2 (2.3) 7.4 (1.4) 14.5¶ 15.5 (2.9) 17.8 (2.7)║ 18.4 (3.5)
*Data from (9); Australopithecus and early Homo sample is composed of Stw-102, Stw-363, Stw-486, Stw-88, TM-1517, A.L. 288-1, Omo323-76-898, KNM-ER 813, 1464, 1476, 5428, and OH-8. †In Homo this usually includes the calcaneal process. ‡Body size estimated as equal contributions of the geometric means of metrics of the wrist and talus (42). Old World monkey taxa include Papio, Mandrillus, Macaca, Trachypithecus, Semnopithecus, Colobus, Cercocebus, and Presbytis. New World monkey taxa are Ateles and Alouatta. §Old World monkey taxa for trochlear angle are from Papio (9). ¶See fig. S1. ║Data for Gorilla (9) are a weighted mean for both species.
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Fig. 4. Metatarsals of Ar. ramidus and extant hominoids, right Mt2 (top) and left Mt3 (bottom). (A) Enlarged CT rendering of dorsal surface of ARA-VP-6/1000. Facets interpreted to be induced by rotation of its base during toe-off and grasping are indicated by arrows. These facets are shown to the right in proximal view [provided to the right in all panels except (E)]. (B) Medial view of entire original specimen (photograph). Although the head is missing, both cornua are preserved, allowing reasonable estimation of original length. Areas of postmortem damage are indicated by hatching. (C) Mt2 of Pan (CMNH-B1718). Note distinctive notching for centrally located tarsometatarsal ligaments. Damage to this area in ARA-VP-6/1000 prevents interpretation of its complete basal form. (D) Modern human Mt2. Proximal surface is superoinferiorly elongate and lacks dorsal facets, consistent with adaptation to bipedality absent an abducent great toe. (E and F) Dorsal (CT) and lateral (photograph) views of ARA-VP-6/505, an Mt3. Hatching shows minor postmortem damage. (G and H) Mt3s of Pan and Homo specimens whose Mt2s are shown in (C) and (D). As is typical of the chimpanzee, the Mt3 shows bilateral notching, although it is not as pronounced in this specimen as in most. Note the striking similarity in the basal morphology of the two hominid Mt3 bases, which suggests that this morphology is likely primitive rather than derived, given the exceptionally great differences in locomotor behavior. CT methods: ARA-VP-6/ 1000, pQCT at 150 mm; ARA-VP-6/505, microCT at 80 mm. Scale bar, 2 cm. 2 OCTOBER 2009
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phase (11). Combined with the pedal characters described here, this suggests a form of primitive terrestrial bipedality in which the foot was emplaced at or only slightly lateral to midline, with the great toe typically in abduction (as often occurs in African apes) and the lateral forefoot in external rotation. Fulcrumation occurred along the oblique axis (fig. S12) and was obviously achieved by the triceps surae, likely substantially aided by a powerful and particularly robust fibularis longus. Balance before and during propulsion was achieved by the opposing actions of (i) a medially emplaced great toe, and (ii) plantarflexion by the fibularis longus, which would also tend to evert the foot. Thus, the lateral compartment must have been very powerful and central to its gait pattern. Indeed, the large os peroneum suggests that once the great toe was restrained by friction against the substrate, contraction of the fibularis longus could further enhance plantarflexion during heel-off through toe-off, while simultaneously maintaining rigidity in the midtarsal and tarsometatarsal joints and preventing inversion induced by substrate disconformities. At the same time, the symmetric rotary facets of the Mt1’s distal joint surface, induced by MP joint motion, suggest that any eversion was prevented by a broadly abducted first ray. Indeed, by the time of emergence of Au. afarensis, hominids had evolved substantially more advanced adaptations to bipedality than were present in Ardipithecus. In the former, the knee had become tibial dominant (10) with accentuated valgus (exceeding even that of modern humans). Hip abduction had been established with a human-like distribution of proximal femoral cortical and trabecular bone (45–47). Moreover, in all known subsequent hominids, the more posterior location and elevation of the os peroneum facet on the cuboid [direct selection acting on morphogenetic fields; type 1 (4)] signals the presence of longitudinal and transverse arches, and thereby the addition of the transverse axis of fulcrumation (fig. S12). The facet’s position in the OH-8 cuboid is virtually human, as is the length of its calcaneal process (Fig. 2). Doming and the simpler unnotched dorsal surface of the Mt1 head characterize both Au. afarensis (A.L. 333-21) (15, 48) and Au. africanus, confirming an immobile first ray with fundamentally human-like propulsion during toe-off (43). The feet of extant African apes are so prehensile that some early anatomists regarded them as hand homologies [reviewed and refuted in (49)]. Compared to the primitive condition of a long midtarsus as seen in taxa such as Proconsul (5), enhanced grasping required the abandonment of forceful plantarflexion on the lateral metatarsal heads in favor of increased plantar laxity at the midtarsal and tarsometatarsal joints. Primitive morphology was replaced by a shortened hindfoot and a talocrural joint modified for enhanced dorsiflexion and inversion. African apes eliminated the os peroneum, plantaris (50), and a
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Ardipithecusramidus ramidus Ardipithecus Table 2. Primitive and derived states of the foot in extant taxa. Extant state
Structure
Primitive*
Old World monkey
Chimpanzee
Gorilla
Human
Thick and dense Separate Fib. to toes 1, 3, 4 Tib. to toes 1, 2, (4), 5
43% 50% (diminutive if present) Minimal Separate Fib. to toes 1, 3, 4 Tib. to toes 2 and 5
Absent 29% (diminutive if present) Minimal Separate Fib. to toes 1, 3, 4 Tib. to toes 2 and 5
90% present Constant with novel medial head Thick and dense Fused Fib. to toes 1, 2, 3 Tib. to toes 2, 3, 4, 5
0.97 (29)