No title

P1: FPN Archives of Sexual Behavior [asb] PL108-309 February 14, 2000 11:52 Style file version Nov. 19th, 1999 Arch...

Author: Kenneth J. Zucker (ed.)

134 downloads 286 Views 900KB Size Report

This content was uploaded by our users and we assume good faith they have the permission to share this book. If you own the copyright to this book and it is wrongfully on our website, we offer a simple DMCA procedure to remove your content from our site. Start by pressing the button below!
Report copyright / DMCA form

DOWNLOAD PDF

P1: FPN Archives of Sexual Behavior [asb]

PL108-309

February 14, 2000

11:52

Style file version Nov. 19th, 1999

Archives of Sexual Behavior, Vol. 29, No. 1, 2000

Homosexuality, Birth Order, and Evolution: Toward an Equilibrium Reproductive Economics of Homosexuality Edward M. Miller, Ph.D.1

The survival of a human predisposition for homosexuality can be explained by sexual orientation being a polygenetic trait that is influenced by a number of genes. During development these shift male brain development in the female direction. Inheritance of several such alleles produces homosexuality. Single alleles make for greater sensitivity, empathy, tendermindedness, and kindness. These traits make heterosexual carriers of the genes better fathers and more attractive mates. There is a balanced polymorphism in which the feminizing effect of these alleles in heterosexuals offsets the adverse effects (on reproductive success) of these alleles’ contribution to homosexuality. A similar effect probably occurs for genes that can produce lesbianism in females. The whole system survives because it serves to provide a high degree of variability among the personalities of offspring, providing the genotype with diversification and reducing competition among offspring for the same niches. An allele with a large effect can survive in these circumstances in males, but it is less likely to survive in females. The birth order effect on homosexuality is probably a by-product of a biological mechanism that shifts personalities more in the feminine direction in the later born sons, reducing the probability of these sons engaging in unproductive competition with each other. KEY WORDS: homosexuality; birth order; evolution; genetics.

INTRODUCTION Homosexuality is common. Its very commonness is a major evolutionary puzzle. How could genes for homosexuality have survived? Homosexuals, lacking attraction to females, produce relatively few descendants. Thus one would expect 1 Department

of Economics and Finance, University of New Orleans, New Orleans, Louisiana 70148. Fax: 504-280-6397. e-mail: [email protected]. 1 C 2000 Plenum Publishing Corporation 0004-0002/00/0200-0001$18.00/0 °


2

PL108-309

February 14, 2000

11:52


Miller

that whatever a population’s initial homosexuality rate was, that rate would soon diminish to virtually zero. Yet appreciable homosexuality persists. Moran (1972), after reporting a study in which 95 homosexuals over 40 (i.e., after the end of child-bearing) had only 37 children (at least 2 offspring per male are needed for a stable population), concluded “If male homosexuality is a biological phenomenon, it does not seem possible for it to have a genetic basis.” Hamer and Copeland (1994, p. 183), in their chapter on the evolution of homosexuality (the problem of this paper), report that “the openly gay young to middle-aged men we interviewed had approximately one tenth as many children as their heterosexual brothers,” although noting that the earlier Bell and Weinberg (1978) study found that the gay men had one-fifth as many children as their heterosexual reference group. Another study found that of men over 50 (i.e., who should have completed their families) who had had sex with another man within 5 years (which included many bisexuals and even a few heterosexuals, as well as homosexuals), most had been married (62.9%) and 56.4% had had children (Van de Ven et al., 1997). While there was no control group, these figures are clearly lower than would be found for a random sample of Australian men aged over 50 years in age. Rogers and Turner (1991), in their survey of studies, found that homosexuals were less likely to be married. This paper aims to show how such a low level of reproductive success could be consistent with homosexuality having a genetic basis. This is not the place to go into great detail on the evidence for a genetic role in homosexuality (surveys are given by McKnight, 1997; Pillard and Bailey, 1998), but family and twin studies (Bailey and Martin, 1995; Bailey and Pillard, 1991; Bailey et al., 1993) make it clear that there is an important genetic component. Pillard and Weinrich (1986) found evidence for the familial nature of male homosexuality by showing that brothers of male homosexuals were four times as likely to be homosexual as brothers of controls. Kallmann (1952) reported an incredible 100% concordance for homosexuality in monozygotic twins. Other studies, such as that by Whitam et al. (1993) found much lower concordance rates. Bailey and Pillard (1991) found that monozygotic twins are concordant for homosexuality 52% of the time, and dizygotic twins only 22% of the time, a statistically significant difference that points to a large role for genes. A similar study of lesbians found 48% concordance for monozygotic twins and 16% for dizygotic twins, again suggesting an important genetic component (Bailey et al., 1993). A later population-based study found somewhat lower concordance rates (Bailey and Martin, 1995; Bailey et al., in press) but still pointed to substantial heritability. In the above-cited Bailey et al. studies, the half or more of the monozygotic twins who were disconcordant in spite of identical genes and similar rearing suggests that some environmental factor [which may be prenatal or essentially random (see Miller, 1997a)] plays a role. There is a large body of literature trying to explain how genes for homosexuality could have survived (most recently summarized by McKnight, 1997).


PL108-309

February 14, 2000

11:52


Homosexuality, Birth Order, and Evolution

3

Some (Wilson, 1975; Weinrich, 1976) have argued that homosexuality has such a strong positive effect on the reproduction of siblings that genes coding only for homosexuality could survive. However, an extremely strong positive effect on the siblings’ reproductive success would be required for such a gene to survive, and any such effect would be very apparent (it is not). Also, as Weinrich (1987), LeVay (1993, pp. 128–129), and others have pointed out, if individuals are to devote their efforts to helping siblings, it would seem more productive for them to be asexual than to expend efforts pursuing members of their own sex (and being exposed to the risk of venereal disease that sexual activity brings). It might be noted that the interest in the evolutionary survival of homosexuality is independent of whether specific genes linked to homosexuality exist. There is evidence for such genes (Hamer et al., 1993; Hamer and Copeland, 1994; Hu et al., 1995). However, even if none of the variability in sexual orientation was genetic, there would still be the interesting question of how humans came to be genetically constituted so that a relatively large proportion (say 2%) were homosexual. Thus, to ask the question of why there are so many homosexuals does not require accepting that there is a “homosexual gene.” Suppose that an “environmental” explanation for homosexuality comes to be accepted. There will still be the evolutionary question of how humans evolved so as to have a genotype in which environmental factors could cause certain individuals to have a phenotype so poorly adapted to continuing the genotype as homosexuals are.

THEORETICAL EXPLANATIONS It is fairly easy to imagine how asexuality could occur (the complicated mechanisms needed to recognize potential mates and be attracted to them need merely have a critical link broken by a mutation). Since there may be a certain irreducible number of errors in the sexual attraction process, a certain amount of asexuality could easily be explained. However, attraction to the same sex is harder to imagine evolving from scratch. Yet since homosexuals do find themselves attracted to males, but not to females, it follows that brains do somehow reliably separate males from females. Such a finely tuned mechanism is highly unlikely to have withstood the rigors of natural selection unless it served a purpose. Most likely, the mechanism for attraction to males is present in the human genotype, but it is normally turned on only in females and in homosexuals. The obvious purpose for such a brain mechanism is to cause mature females to be attracted to mature males and, ultimately, to produce offspring. Since sex in humans is determined by the presence or absence of a Y chromosome, and this chromosome is very small (i.e., has a limited capacity for carrying information), it is very likely that the information that permits a homosexual or another


4

PL108-309

February 14, 2000

11:52


Miller

person to determine whether a person is male or female is carried on a chromosome other than the Y chromosome. Since it is hard to imagine a mechanism emerging just so homosexuals can recognize and be attracted to other males, it is very likely that homosexuality involves the activation of this mechanism in the few males that become homosexuals, when it would normally be inactivated in males. The general theory of sexual development is that it is controlled by hormonal signals (or the absence of such signals) and that, once the signal is given, it affects a wide range of development conditions, from the genitals to the brain (for good summaries see Gandelman, 1992; Ellis and Ames, 1987). Indeed, the prevailing wisdom is that humans are programmed to develop as females (which presumably includes a sexual attraction to males) and that testosterone from the fetal testes masculinizes the males, leaving the remainder to develop as females. Since sexual orientation is just one of a number of traits that normally separate females from males, it very likely that all or most of the sex-specific traits are activated (or turned off) by a single hormonal mechanism, which occasionally is partially activated in males producing homosexuality. Other traits (including personality ones) in which females differ from males presumably are partially activated by the same signal that produces homosexuality. As will be argued, these feminizing influences frequently contribute to reproductive success in heterosexual males and, thus, are enabled to perpetuate themselves. For an allele (a variation of a gene) which frequently produces an effect in some individuals (homosexuals here) that is opposed to reproductive success to survive over the long run,2 the allele must also contribute to reproductive success when in other individuals (which in this case are heterosexuals). Presumably two alleles at the same location produce homosexuality, but one allele produces a desirable effect in heterosexuals. Versions of this theory have been discussed by McKnight (1997; elaborating on MacIntrye and Estep, 1993). Another (and less discussed possibility) is for there to be pleitropic genes that affect sexual orientation. A pleitropic gene is simply one that has more than a single effect. One effect could be contributing to homosexuality (which has a negative effect on reproductive success). The other effect or effects could be to contribute to reproductive success in heterosexuals in some manner.3 2 In

considering how genes for homosexuality could survive, I find it very implausible that genes whose only effect was to produce homosexuality could survive. Homosexuality is just too negative for reproductive success. While, in theory, homosexual genes could survive if they increased the reproductive success of others carrying such genes (such as by being helpers at the nest, as is found in some birds), there is no real evidence for an effect anywhere near strong enough to ensure the survival of such genes (for discussions of such theories, see McKnight, 1997; Weinrich, 1987). No one has come up with plausible reasons why homosexuality would have emerged rather than mere asexuality. 3 The case where the other effects are adverse to reproductive success does not have to be considered in detail, since genes that both hindered reproduction in heterosexuals and produced homosexuality would be quickly eliminated from the gene pool.


PL108-309

February 14, 2000


11:52


5

There has been extensive research into the genetics of personality (see, e.g., Eaves et al., 1989; Plomin et al., 1994; Rowe, 1994). Consistently the models that give the best fit involve an additive genetic variance, along with nonfamilial environmental effects and sometimes familial effects. Sexual orientation can be viewed as just another aspect of personality, although a very important aspect. As discussed in detail later, sexual orientation correlates with femininity on measures of personality traits related to masculinity–femininity. Thus it seems very plausible to use a polygene additive model for homosexuality. Given that a beneficial effect on heterosexual’s reproductive success is the most plausible (I would argue the only plausible) mechanism by which genes contributing to homosexuality could have survived, the question is, how do these genes contribute to heterosexuals’ reproductive success? These genes should produce the same effects in heterosexuals that they do in homosexuals. Thus, it is necessary to look at the traits homosexuals exhibit to a greater extent than heterosexuals (only some of which would carry any particular allele that contributes to homosexuality). It is also necessary that the traits in question increase the reproductive success of the heterosexuals in which they will reside for most of the time. Thus, theory suggests that the genes of interest would contribute to homosexuality while also increasing heterosexual reproductive success. A plausible possibility for the heterosexual reproduction increasing effects of a pleitropic homosexuality producing gene would be found in the feminine traits of sensitivity, kindness, empathy, etc., that are frequently exhibited by homosexuals. These traits would often make for a better father (see discussion later). They may be more risk adverse and avoid the costs of intermale contests (this point was suggested by Mike Waller). Werner (1998) has made this point, suggesting a simple system where two “homosexual” alleles made for a homosexual, and none for a dominant male who died early in fighting, while one with a single allele of the homosexual type would be most successful. Amusingly, he ended his essay with Christ’s comment, “Blessed are the meek, for they shall inherit the earth.” It is easy to imagine that in most males these traits help attract females and, hence, lead to greater reproductive success. Indeed, one reason why they might be attractive to potential mates would be that they contribute to being good fathers and good providers. The typical male without homosexuality-related genes may be too masculine for optimal reproductive success (how this could come to happen is discussed later), and greater femininity on a number of dimensions could contribute to his reproductive success. Now imagine that there are a number of alleles that make for femininity. If the typical male inherits only a few of the alleles that make for femininity, his reproductive success is increased. Only if he inherits a large number of such alleles is his development pushed so far in the “feminine” direction that the brain circuits for mate choice and sexual orientation produce homosexuality. Such genes could survive because most of the time they would be in heterosexual males and be


PL108-309

February 14, 2000

11:52


6

Miller

contributing to reproductive success. Only occasionally would enough of these come together (probably along with unknown environmental factors) to produce homosexuality. Such alleles will be in a balanced polymorphism such that if they got any rarer, their contribution to reproductive success would be increased through making heterosexuals more successful. If they got much more common they would more often contribute to homosexuality and be selected against. Although the above discussion is purposively a little vague on the mechanism, given the evidence for prenatal hormones playing a key role in sexual differentiation, it is expected that genes affecting sexual orientation would have their effect through prenatal hormonal effects on sexual differentiation (Ellis and Ames, 1987). This same prenatal hormonal system seems also to affect sex typical behaviors of various types. For instance, that the behavior of human female twins who shared the womb with a brother is more masculine than that of those who shared it with a female suggests a hormonal effect on human behavior (Miller, 1994, 1997b). It is very plausible that there are pleitropic genes, one whose effect is to feminize the parts of the brain that control sexual orientation and another whose effect is to feminize brain areas that affect personality, choice of childhood play objects, or choice of role model. Such genes might change the level of hormones during prenatal critical periods, or the receptor density, or the level of enzymes that convert one steroid to another, or the level of binding proteins, or the permeability of the blood–brain barrier to hormones, etc. Just enumerating some of the possible pathways makes it plausible that multiple genes could be involved, along with several environmental factors. One of the prenatal factors could be the prenatal stress that has been argued to contribute to homosexuality (Dorner et al., 1975, 1983; Ellis, 1987; Ellis et al., 1987). Figure 1 illustrates the theory. The hormonal environment varies on a continuum from that which produces masculinity to that which produces femininity in

Fig. 1. Homosexuality as the extreme on the male masculinity–femininity continuum.


PL108-309

February 14, 2000

11:52



7

brain organization. Those males who are subject to the most femininity producing environments become homosexuals. Those who are less extreme exhibit varying degrees of bisexuality.

Illustrative Example To illustrate the effect, imagine that there are five genes that play a role in locating a male along a homosexual–hypermasculine continuum. Each gene has two alleles, one that moves the individual one step toward the feminine side and one that moves it toward the masculine side. For simplicity, imagine that each gene has the same effect. A male becomes homosexual only if he inherits all five homosexuality producing alleles. Computation shows that there is a 1 in 25 , or 1 in 32, chance of this happening. Thus, slightly more than 3% of the males will be homosexual. Males who inherit fewer than five such alleles, are heterosexual. If they inherit any such alleles, they benefit from an increase in sensitivity. Males who inherit none of these alleles are hypermasculine and lacking in the sensitivity, kindness, empathy, and other traits that make them most attractive to females. In this simple example all genes are identical in effects so we can analyze any one gene. There are 16 combinations of the alleles of the other four genes. Capital letters denote the alleles that make for homosexuality (in this case these genes are dominant, but that is not critical to the argument), and the genes are a, b, c, d, and f. Consider the F allele of the f gene. It will produce homosexuality only if it is inherited by an individual with the ABCD genotype. Only 1 of 16 individuals will have this. If it is inherited by individuals with one, two, three, or four of the femininity alleles, a, b, c, or d, it makes him more sensitive. This increases his reproductive success. These individuals are the other 15/16ths of the population. In this set of circumstances, the gene will make a contribution to the reproductive success of the majority of the males and could easily survive. In this example, if the homosexuals have no descendants (success of 0) and the other individuals receiving the allele have their reproduction increased to 16/15, or 1.066, the allele will be reproduced in the next population, permitting the allele to maintain its frequency. If the frequency of the homosexual allele F increases above .5 (and half of the other genes have the homosexuality producing alleles), in the next generation the reproductive success of the carriers of the F allele will be less than 1. Thus the F allele will tend to decrease in frequency. If the F allele is found at a frequency of less than .5, the reproductive success of the carriers will be greater than 1, and the gene will tend to increase in frequency. Thus, the frequency of the F allele would remain at .5. The argument is symmetrical, and exactly the same for every other gene. The above example is obviously very simple, but it does indicate how there could be a stable polymorphism, with a number of genes contributing to homosexuality. Thus


PL108-309

February 14, 2000

11:52


8

Miller

we should not reject the idea of a genetic role in homosexuality just because, at first glance, survival of a gene for homosexuality seems implausible. Such a model can be elaborated. For instance, it is quite possible that some males are already on the feminine side, so an additional dose of femininity is mildly adverse to their reproductive interests, while others are so masculine that there are greater than average benefits from being shifted in the feminine direction. But these are just complications, not essential alterations. One or more of the factors in the above example could be environmental or, possibly, random. Monozygous twins frequently grow up discordant for sexual orientation in spite of having identical genetic endowments and being raised in the same family in very similar manners (citations above). Judging from this fact, it is very likely that one element either is random or depends on some relatively minor environment factor (which acts almost as random), such as position in the womb. Thus, there is nothing in the above idea that is inconsistent with one or more environmental factors, including prenatal stress, playing a major role in the etiology of homosexuality. How large an effect is needed to sustain homosexuality? MacIntrye and Estep (1993) provide some calculations for simple genetic systems (not the one discussed above) and conclude that a 2% fertility advantage in the heterosexuals would be capable of ensuring the survival of genes for homosexuality. They point out that this is such a small number that it would probably be lost in the noise of most studies and, hence, would not be detected. WHY EXCESSIVE MASCULINITY The above argument started with a presumption that the typical heterosexual was overly masculine (i.e., overly masculine for maximal reproductive success). In turn, this implies that genes for certain feminine traits would increase the typical heterosexual’s reproductive success. While one can certainly imagine males being so high in stereotypical masculine traits that they are unattractive to women (such males might be very ruthless, selfish, insensitive, cruel, etc.), someone might object that evolution might not produce many such males. Would this destroy the above argument? How can we be sure that, in the absence of the genes contributing to homosexuality, such excessive masculinity would exist? If excessive genetic femininity exists and produces homosexuality, it follows that in equilibrium the typical heterosexual male will be excessively masculine. Imagine that the heterosexual males were on just the optimal position on the masculine–feminine continuum for maximal reproductive success. However, if this were the case, averaging in the effect of the induced homosexuality must imply an above-equilibrium frequency of the femininity producing alleles. These alleles would decrease in frequency. The situation would not be in equilibrium. Every so often, the allele would contribute to homosexuality, and this would happen with a finite probability. With the homosexual reproductive success well


PL108-309

February 14, 2000

11:52



9

below unity, and the reproductive success of the heterosexual carrier of the allele at its maximum (by the above assumption), the appropriately weighted average reproductive success of all the allele’s carriers would be below the maximum, while the maximum would normally be above 1. The alleles that contributed to homosexuality would have a lower reproductive success than those that moved these males toward hypermasculinity. The hypermasculinity producing alleles would increase in frequency. This increase in frequency would stop only when the shift to hypermasculinity had become sufficiently great that the benefits from tempering hypermasculinity were great enough to offset the loss of reproductive success from homosexuality, and carriers of both alleles had the same reproductive success. Thus the requisite (for the above theory) excessive masculinity can be presumed to exist if there are alleles that both contribute to homosexuality and femininize excessively masculine males. The disadvantage to having a high proportion of the genes that make for homosexuality includes not only homosexuality, but also being avoided for mating purposes by females. Why would females avoid the carriers of such genes? Because, with genetic reshuffling in the next generation, their descendents would have an above-average risk of homosexuality. For instance, in the above simple example, a female who mated with a male with five of the six homosexual-related genes would have an above-average chance of having her son prove to be homosexual, an event that would reduce the number of grandchildren she would have. From her viewpoint the ideal male might have, say, three of the alleles that made for homosexuality. Such a male might be “feminine” enough to make a good father and provider, yet be masculine enough to signal that he had few genes that made his offspring likely to be homosexual. This does not change the basic argument of the model because the stronger the disadvantage to being on the feminine side of the distribution, the more selection will lead to the male being on the hypermasculine side, where only the genes for femininity can temper his hypermasculinity. A more interesting possibility is that females may have evolved so as to adjust their choice of mate to the genes their own body is carrying. If the genes they carry would make for an appreciable risk of homosexuality in their sons, they should choose a mate who is on the strongly masculine side, thus minimizing the risk of homosexuality. At the other extreme, if the women carry genes for masculine traits, they can mate with men carrying more of the feminine traits without an exceptionally high risk of homosexuality in their sons. FEMALE MATE CHOICE When human females are asked to list the traits that are desirable in a mate, kindness is consistently listed of one of the most desirable (Buss, 1989, 1994; Buss and Barnes, 1989) in a study that collected data not just for Anglo-Saxon cultures but for 37 different cultures. Sprecher (1989) documented that both sexes


PL108-309

February 14, 2000

11:52


10

Miller

prefer more expressive partners. Later, Sprecher et al. (1994) reported that “women have expressed a greater preference than men for such personality characteristics as expressiveness, kindness, and considerateness.” These are traditionally considered feminine traits (McKnight, 1997), and it is plausible that one developmental mechanism could select for them and for a female typical choice of sexual partner (i.e., for a preference for male sexual partners). It should be noted that there are good biological reasons for a female to seek a mate who is kind and considerate. He is more likely to give her resources for raising her offspring and not to harm her physically or to harm her emotionally by making her jealous. The disadvantage to the male of being kind, considerate, empathetic, etc., may be that he devotes less time and resources to seeking second mating opportunities. Very likely, the best level of femininity, etc., for a male varies with time and location, making it optimal for parents to have children that vary in this trait, as in other traits (see the discussion below, under The Value of Male Variability). THE FEMINIZATION OF HOMOSEXUALS A testable implication of the above theory is that the brains, behavior, and perhaps even bodies of homosexuals would be more feminine. On tests, either the homosexuals would exhibit the female pattern or they would be shifted in the female direction. The theory predicts, furthermore, that this feminizing effect would be observed only for those characteristics that develop at the same time or are subject to the same developmental mechanism as sexual orientation. However, since at present we do not know which characteristics these are, this aspect of the theory cannot be directly tested. As to the timing of such effects, Hall and Kimura (1994) reported that the fingerprints of homosexuals are more often leftward shifted than those of heterosexuals. The volvar pads form on the fingertips by the 8th week of conception and the prints are fully formed by about the 16th week. The homosexual/heterosexual differentiation presumably occurs at least partially during this period. This observation dates hormonal effects that could also be affecting the brain and the personality. There is a large body of literature which points to prenatal hormonal effects on male/female differences and homosexual–heterosexual differences. Let us start with the physical ones (see the papers in Ellis and Ebertz, 1997). Schlegel (1966; as cited by Eysenck and Wilson, 1979, pp. 38–39) reports a difference in the pelvic structure of homosexuals. In females the pelvis is more barrel shaped, with a relatively broad outlet (to facilitate child bearing), while in males it is more funnel shaped (with the result that even though men are larger than women on average, their pelvic outlets measure much less than those of


PL108-309

February 14, 2000

11:52



11

women). He reports that homosexual males tended to have feminine-type pelvises. Furthermore, Schlegel claims that pelvic type correlates with personality. Quoting from Eysenck and Wilson’s (1979, pp. 38–39) summary, Masculine type pelvises correlated with leadership, an active sexual role, dominance and preference for younger sex partners in men and women alike. Feminine type pelvis correlated with empathy, suggestibility and compliance, as well as preference for older sex partners. . . . Schlegel even studied cows (whose pelvic outlets are more easily observed than those of human subjects!) and found that cows with narrow outlets, i.e. funnel-shaped pelvises, tended to mount other cows and generally behave in a more masculine manner.

The theory that the genes that lead to homosexuality also lead to feminine behavior explains the finding that homosexuals frequently report gender atypical boyhood behavior. Bailey and Zucker (1995) found in a meta-analysis of studies that there was a strong tendency for homosexuals to recall childhood gender atypical behavior. Green (1987) found that “sissy” boys often grow up to be homosexuals. Presumably constitutional behavioral differences persist from childhood into adulthood. THE FEMINIZATION OF HOMOSEXUALS’ BRAINS Having looked at physical differences, now let us look at psychological differences. For many traits homosexuals appear to be more like females than typical males. Pillard (1991) lists 31 studies in which psychological tests measuring putatively sex-dimorphic traits were administered. In only one case (two others were mixed) did the homosexual or lesbian group fail to have scores that differed from their own sex in the direction of the opposite sex. Those interested in the pre-1990 studies are referred to his paper for details. For homosexual males (the majority of the studies reported on) this implied that homosexuals were more feminine than the heterosexuals. More recently, Chung and Harmon (1994) found that gay men had lower masculinity scores, but not femininity scores, on the Bem Sex Role Inventory than did heterosexual males. Weinrich (1987) reports some research done by him and Pillard (not reported elsewhere) using the Strong–Campbell Vocational Interest Inventory. To be precise, for the jobs that were significantly preferred by heterosexual women according to the test’s norms, the homosexual men on average reported higher levels of interest than the heterosexual men did. The trend was so strong that we could “predict 65%–70% of the time whether a given subject was homosexual or heterosexual, knowing solely his Strong–Campbell scores. For a psychological test—and one not designed with homosexual/heterosexual discernment in mind—this figure is remarkably high.” The finding that male–female vocational interests are different is usually explained by socialization, girls are brought up to feel that certain occupations are more suitable for them, and boys are brought up to prefer other occupations.


12

PL108-309

February 14, 2000

11:52


Miller

However, the same explanation seems unlikely to apply to homosexuals since they are normally brought up as males and subjected to strong pressures to adopt male patterns of behavior, to play with male toys, and to act-out male occupational roles. Tuttle and Pillard (1991), using a measure of femininity (34 true–false questions that constituted the Femininity Scale of the Personal Values Abstract of the California Personality Inventory), found that homosexual males scored 19.00, versus 15.62 for heterosexual males and 20.74 for heterosexual females (high scores are more feminine). This difference was significant at the 1-in-10,000 level. Interestingly, the homosexual females scored 19.19, which is only slightly more feminine than the homosexual males. The homosexual female versus heterosexual female difference was statistically significant, although to a much weaker degree ( p < .041) than for the homosexual/heterosexual difference in males. Also, Salais and Foscher (1995) found gays to be more altruistic. Ellis et al. (1990) examined self-reports of male homosexual behavior and found that there was a negative relationship between most forms of violent or criminal behavior and homosexuality. This is consistent with the homosexual brains being less masculinized than heterosexual brains. Others (Gladue et al., 1990) report a more feminine pattern of spatial ability among homosexuals. For instance, Hall and Kimura (1995) show how, on a throwing accuracy task, men do better than women, but homosexual men are closer to the female pattern than are heterosexual males. McCormick and Witelson (1991) found that homosexual men do less well at certain spatial tests than heterosexual men, and women are known to do less well at these tasks than men. This is consistent with a shifting of the structure of the brain in homosexual males in the feminine direction. However, Tuttle and Pillard (1991) found that homosexual males did not have an ability pattern atypical of other males. One possible explanation for their results differing from the other studies is that homosexual subjects consistently did better than heterosexual males on all of the four tests used, a possible result of a recruitment bias arising from recruiting their homosexual subjects from readers of gay newspapers. This may have resulted in some restriction of range. Another study that did not fit the pattern is that by Halpern and Crothers (1997), who found homosexuals to be more masculine than heterosexual males. It is a popular observation that many homosexuals display “feminine” mannerisms and voice quality. Guadio (1994) has documented that most observers can tell which speakers are homosexual without being told in advance. Also, Blanchard and Bogaert (1996a) and Bogaert and Blanchard (1996) show that homosexuals have an earlier puberty onset than heterosexuals. Since female puberty is earlier than that of males, this represents a shift in the female direction. This is consistent with the homosexual brain being somewhat feminized. Hamer and Copeland (1998, p. 99), in a “highly preliminary result,” looked at the female relatives (mothers and daughters) who were either linked or unlinked for Xq28 (the location where a major gene for homosexuality is believed to be


PL108-309

February 14, 2000


11:52


13

located), reporting that “the women with the gay version of Xq28 . . . had begun puberty on average of six months earlier than the other mothers.” This supports the role of this gene in causing homosexuality, as well as in feminization. The hypothalamus is believed to be important in the timing and regulation of puberty. LeVay (1991) made a well-publicized finding that in homosexuals the size of a sexually dimorphic nucleus in the anterior hypothalamus was that of females rather than that of males. Other brain differences are known. Swaab and Hofman (1990; review by Swaab et al., 1997) found that the vasopressin part of the suprachiasmatic nucleus in homosexual men was twice as large in homosexual as in heterosexual men. The suprachiasmatic nucleus is known to be involved in regulating the circadian (daily) rhythms. Interestingly male rats treated with the aromatase inhibitor ATD (which hinders the conversion of testosterone into estrogen in the brain) and made bisexual prefer female rats when tested in the late dark phase and male rats when tested in the early dark phase (Bakker and Slob, 1997). The same ATD-treated bisexual rats had an increased number of vasopressin-expressing neurons in the suprachiasmatic nucleus (Swaab et al., 1995), suggesting a prenatal link between sex hormones and the brain that somehow produces homosexuality. Allen and Gorski (1992) reported that the size of the anterior commissure was about the same size in gay men as in straight women. As LeVay (1993, p. 123) points out, “The very fact that the anterior commissure is not involved in the regulation of sexual behavior makes it highly unlikely that the size differences result from differences in sexual behavior.” This makes it more likely that there is some process shifting certain male brains in the feminine direction. Alexander and Sufka (1993) did electroencephalographic measures on homosexuals, females, and straight males, measuring brain waves during baseline conditions and while the subjects performed experimental tasks. They found that homosexuals differed from “both male and female heterosexual groups during baseline recordings and different than heterosexual males during judgement for verbal and spatial stimuli, but not significantly different from heterosexual females” (p. 273). This is consistent with other findings in which homosexual males resemble heterosexual females and is consistent with a shift in the female direction during brain development. McKnight (1997), citing a personal communication from Alexander, states that preliminary findings from a large study support these findings and that “these EEG patterns are dynamic and change with the degree of homosexuality reported by the individual.” Reite et al. (1995) did magnetoencephalographic measurements on homosexual and heterosexual men, focusing on the M100 location in the superior temporal gyri. Straight men showed significantly more anterior reactions in the right hemisphere compared to the left one. Gay men did not demonstrate significant differences between the right and the left hemispheres. They resembled the female pattern more than the male pattern. In a study of event-related potentials, Wegesin (1998) found that slow-wave activity recorded during mental rotation was greater for heterosexual men than for heterosexual women and gay men.


PL108-309

February 14, 2000

11:52

14


Miller

There are also the controversial reports that homosexual brains, when challenged with estrogen, respond with release of luteinizing hormone (Dorner, 1975; Gladue et al., 1984), a result some have not found (Gooren, 1986). Since normal female brains respond with such a surge, this could be one more piece of evidence that homosexual brains are modified in the female direction. Family Implications A frequent finding of studies of families of homosexuals is that the father is much less dominant than is found in most heterosexual families. More often than normally the mother makes the key decisions and ran the family. For instance, Bell et al. (1981, p. 66) reported that fewer homosexuals than heterosexuals reported that their fathers had dominated their mothers, and more homosexual men said that their mothers dominated their fathers. This finding is traditionally interpreted as a characteristic of the structure of families that produce homosexuality. However, it could also be a reflection of the personality of the fathers. If the fathers of homosexuals are relatively feminine (as would be expected from sharing half of their genes with their homosexual sons), they might very well take less of a leadership role in the home and be less dominant. LESBIANISM This paper has focused primarily on male homosexuality. Much less is known about lesbianism. However, much of what is known indicates that lesbians are relatively masculine in their interest and personalities compared with male homosexuals. For instance, Spence and Helmreich (1978) used their Personal Attitudes Questionnaire to show that male homosexuals scored significantly lower on masculinity and significantly higher on femininity, while lesbians were significantly higher on masculinity and lower on femininity. Interestingly, lesbians actually scored higher on the masculinity scale than did male homosexuals. Perkins (1981) reported that lesbians had narrower hips and more muscular builds than nonlesbian women. Within lesbians, those that played the more dominant (more male-like) role were taller (dominants compared with passives gave a 2-in. difference, which was statistically different). The dominants also had broader shoulders and narrower hips than did lesbians who played passive or intermediate roles, although only the shoulder differences were statistically significant. These differences are consistent with one developmental process affecting masculinity both in build and in personality. The most powerful evidence for lesbianism being caused by prenatal masculinization comes from a comparison of the auditory systems of heterosexuals and homosexuals in which click-evoked otoacoustic emissions of lesbians resembled the male pattern rather than the female pattern (McFadden and Pasanen, 1998).


PL108-309

February 14, 2000

11:52



15

Since this is a physiological difference rather than a psychological one and the sex difference appears in infancy (and, from studies of opposite-sex twins, appears to be influenced by the prenatal hormonal environment), this provides strong evidence that lesbianism is caused by a prenatal masculinization. The explanation for the survival of lesbianism in spite of its apparent disadvantage could be similar to that for male homosexuals. Certain factors, environmental and genetic, lead the brain to develop more in a masculine direction. If development is shifted sufficiently far, the circuits that deal with mate choice take on a masculine character, and the female is sexually attracted to females. However, in the majority of females these genes and environmental factors merely serve to make the female personality and interests more masculine, and this frequently contributes to the female’s reproductive success. One may speculate that the greater reproductive success of those with masculinity producing genes is through greater success at mate acquisition. An example would be when a tomboy is later better able to acquire a mate, because of her ability to talk about sports and other masculine topics (in Africa, hunting perhaps). However, in many cases the advantage of a more masculine personality may not be in mate acquisition, but in being more effective in asserting herself and hence at acquiring the resources needed for her and her children. For instance, while the very feminine female may be most attractive to a male, one who is a little more tough-minded is better at competing with another wife or mistress for the resources he is able to provide. Depending on the environment, the optimal level of masculine traits, such as assertiveness varies. Thus, for lesbians as for male homosexuals, an occasional sexual orientation that is not conducive to reproductive success is the price paid for having mechanisms in place that provide optimal variability in personality. So far the empirical research seems inconsistent with there being one factor that affects both lesbianism and homosexuality. While there is evidence that a gene in the Xq28 region affects homosexuality, it appears not to affect lesbianism (Hu et al., 1995). The familial studies that have shown lesbianism or homosexuality to run in families have not found evidence that certain families have both conditions. However, it is not known if people have looked for evidence of unusually low rates of lesbianism in families with homosexuality. The lack of evidence of a single gene affecting the rates of both lesbianism and homosexuality is evidence (weak) that masculinity and femininity may have different causes. THE VALUE OF MALE VARIABILITY The above argument shows why a high degree of variability can contribute to male reproductive success. This provides the answer to a question arising from the earlier argument. Why is there the wide variability along the femininity– masculinity axis that creates the problem of some individuals being so far to


16

PL108-309

February 14, 2000

11:52


Miller

the feminine side as to become homosexuals? Why are human males not designed to produce the single optimum phenotype? Presumably, if the distribution shown was narrow enough, no individuals would fall into the range that produced homosexuals. Then there could be none that were so deficient in “sensitivity,” etc., as to be at a severe disadvantage in attracting and retaining females. The reason for the wide variability in phenotypes is that long-run reproductive success is facilitated by variability (for the argument in detail see Miller, 1997a). Part of the reason is that reproductive success is the geometric average of reproductive success over many generations, not the arithmetic average, and the geometric average is normally below the arithmetic average. This mathematical fact implies that the more variable reproductive success is across generations, the slower the population growth will be, and that there will be selection for reduced variability across generations. One way to achieve this is to have diversity in phenotypes within each generation so that at least one phenotype will be well adapted for whatever conditions occur. Thus humans have evolved to be different from each other. This is probably achieved by differences in the prenatal environment at some stage of development. An unfortunate (for reproductive success) implication of this overall desirable process exists. It occasionally produces a homosexual male who is not attracted to females and, hence, leaves few descendants. There is evidence (Hamer et al., 1993; Hamer and Copeland, 1994; Hu et al., 1995) that a gene that promotes homosexuality has a Xq28 location, i.e., one on a sex chromosome. The theory about optimal diversification makes a sex location for a such a gene more plausible. The need is to diversify the behavior of sons. A location of the key gene on the X chromosome ensures that there will be only one copy in sons. If such a gene were on an autosomal location (i.e., not on a sex chromosome), every so often a son would receive a double dose. If this allele had a very high probability of producing homosexuality at a double dose (a likely effect if a single dose often led to homosexuality), the combined effect of double doses producing homosexuality and single doses producing homosexuality when combined with other genes could make such an allele nonviable in the long run. The same gene on the X chromosome is protected from producing a double dose in males. Those with a double dose are daughters (by the genetic definition of female, XX). There is an additional factor. A gene on the X chromosome spends twice as much time in females as males. A positive effect on the reproductive success in females could counterbalance the disadvantage of occasionally producing homosexuality in males. A gene that contributed to “femininity” could be an asset in females. With genes occasionally shifting the chromosomes they are on, one would expect a gene that was prone to contribute to homosexuality to end up on the X chromosome. This would be especially likely if the gene were sufficiently “powerful” that a double dose in males had a very high probability of producing homosexuality (and a gene which had a sufficiently powerful effect to produce such an effect in a heterozygote might plausibly produce an even stronger effect


PL108-309

February 14, 2000

11:52



17

in homozygotes). An allele powerful enough to be detected by the method used by Hamer could possibly survive only if a location on the X chromosome protected males from ever inheriting a double dose. FREQUENCY OF HOMOSEXUALITY VERSUS LESBIANISM The theory of this paper may explain why male homosexuals are more common than female lesbians (McKnight, 1997, p. 7; Wellings et al., 1994, pp. 188– 190; Sundet et al., 1988). It is a commonplace of evolutionary psychology (Symons, 1990) that a male who is unusually successful in reproduction will have more grandchildren than an unusually successful female. (Unusually successful may be thought of as being in the top 10% of their sex.) This is because the capacity of the female womb is limited, while a male can fertilize many women. This makes risk taking more productive for males than for females. It also implies that it pays for parents to take greater risks with the personalities of their male offspring and to produce a wider variety of male personalities than of female personalities. Consider the benefits of producing a hypermasculine male offspring. If the environment (including its social aspects) is of the type where such a son is most likely to be reproductively successful (sometimes through multiple wives and mistresses), such an individual will leave many descendants. The cost of having such a hypermasculine offspring is that if the environment is of the opposite type, the number of grandchildren will be reduced. However, there is a limit to the shortfall, since the number of offspring cannot fall below zero. Thus, the gap between the reproductive failure’s offspring number and that of the average male cannot exceed the average male’s offspring number. Because a successful male can leave many offspring, while the shortfall from an unsuccessful one is limited, there are often gains from the apparently high-risk strategy of producing males that are well adapted for one environment, but a failure in another. This calls for producing sons with a wide range of personalities. In particular, this implies producing sons that vary on the masculinity–femininity continuum, and a wide variability can be desirable even if it increases the risk of homosexuality. As an illustration, imagine that there are several possible types of sons. An example is given in Table I. There are three types of environments and three types of sons. One type (A) has a specialized personality and is unusually empathetic Table I Environment Son type

a

b

c

A B C

0 2 8

3 4 3

8 2 0


PL108-309

February 14, 2000

11:52


18

Miller

and understanding. In the right social environment these traits translate into political skills, and he rises to leadership of the band and has two wives each with four children (for a total of eight). However, in the wrong environment, he is taken advantage of and leaves no children. Another type (C) is the opposite and has a hypermasculine personality. In the opposite type of social environment, the hypermasculine son is the successful one, leaving eight descendants, with the empathetic, feminine one having no offspring. The third type, B is best suited to average conditions, in which he produces four offspring, while in the other conditions he produces two. The example has been constructed so that there are 10 children born in each type of environment (with the only difference being which males father the offspring). For simplicity, imagine that the three environments are equally probable. The two extreme personality types produce 11 offspring averaged over the three environments, while the more average type produces only 8. Selection is for the genes that make for male variability here. In the above example, producing half sons of type A and half of type C produces 10 offspring in any environment and clearly wins out over producing all B’s (which are best adapted for average environments). A line that produced only A’s or only C’s would probably go extinct eventually when it hit environments for which its offspring were ill suited (type A in environment c or type C in environment a), but a line that produced highly diverse offspring would stay in competition (for an elaboration of this point see Miller, 1997a). In addition, parents who produce sons with both extreme types of personality have hedged their bets and, in the long run, do best. Now consider daughters. Table II shows a possible pattern. The biological limit here is taken to be five offspring born (fewer surviving), and this is achieved only for the daughters who are well adapted to the environment. In the most common environment, the unspecialized type B leaves five surviving children. In less favorable conditions she leaves four. The low variance is because she is near her capacity in all environments. Now consider the advantages of having a specialized daughter who is well suited for the extreme conditions that occur from time to time, when she has five children. In average conditions she has four. If the conditions are unfavorable for her personality type, she can fall well below her biological limit, in this example leaving only two children. Again, imagine that each of the environments occurs a third of the time. Now the most successful strategy is always to produce the unspecialized daughters who, Table II Environment Daughter type

a

b

c

A B C

2 4 5

4 5 4

5 4 2


PL108-309

February 14, 2000


11:52


19

in all conditions, bear and raise offspring at near the biological limit. Summed across all three environments, such daughters have 13 children. The more specialized daughters out-reproduce her if they hit it lucky and find an environment suited to their personalities, but they do not outreproduce the average type by much, because biology constrains them. However, if the conditions are poorly suited to their personalities, they have unusually poor reproductive success. Over all three environments, such specialized daughters produce only 11 offspring. The mother who produces only the single type of daughter out-reproduces the mother whose daughters are more variable. While the particular numbers are obviously only illustrative, the effect of having an upper biological limit on female reproductive success limits the payoff to producing specialized offspring who are best suited to environments that are only occasionally encountered. While in such cases a suitable son can have spectacular reproductive success (perhaps having more than one wife) as in the above example where he had 10 offspring, the similarly specialized daughter comes up against the biological limit (in this example, 5 offspring) and does not enjoy such a benefit. This argument is general and suggests that daughters should be less variable than sons. In the case relevant to homosexuality, the optimal variability along the masculinity–feminity continuum would be greater for males than for females. In both sexes a disadvantage to high variability is likely to be occasional homosexuality (lesbianism for females). For males this appears to be a tolerable cost of obtaining diversity in offspring. In females with a lower value for diversity, it is less often observed. In these circumstances, the optimal variability for daughters is small. They are well suited for the most likely conditions and able to function adequately in the less likely conditions. The risk of having daughters that are ideal for rare conditions is not worth running since these daughters will probably do poorly in the opposite conditions (and worse than if they had just the average type personalities). This argument suggests relatively small variability for females. The above theory for homosexuality and lesbianism proposes that they are by-products of adaptations to increase variability along the masculinity–femininity axis. For males a high degree of variability is selected for, and one of the costs for reproductive success of this high variability is the production of the occasional homosexual. For females, there is less benefit to variability and less variability exists. Thus, females are exposed less frequently to strong enough masculinizing influences to become lesbians. The above effect appears strong enough to more than offset the likely greater cost of homosexuality for reproductive success that arises from the male usually being the initiating party in intercourse. In many traditional societies, virtually all women marry and do not refuse their husbands sex. A lesbian would still marry and, even if she was not attracted to her husband, would be expected to have sex and become pregnant. The major reproductive cost to being a lesbian may be that she enjoys sex with her husband less, and this makes him a little less committed to


20

PL108-309

February 14, 2000

11:52


Miller

her. Also, she may not take advantage of some extramarital mating opportunities (especially important if her husband proves sterile). Thus being a lesbian would impose only a minor cost on the typical women in a prehistoric society. Of course, even this minor disadvantage does result in selection for heterosexuality and for females to be attracted to males. However, a male homosexual would be less likely to marry and, if married, would have much less sex with his wife (and perhaps none with other females). This would be expected to put male homosexuals at a substantial disadvantage and to select strongly against homosexuality. Given that the reproductive penalties for same-sex attraction appear to be much greater for males than for females, one might have anticipated that in equilibrium male homosexuality would be rarer than lesbianism. Yet the opposite is found. In the theory of this paper, the higher rate of homosexuality can be explained by the advantages to males of a high variability along the masculinity– femininity axis. This is much greater than for females, as shown above. What genetic mechanism could make for high variability? The simplest one is an allele that makes a big difference to masculinity–femininity. Perhaps it produces a much more sensitive receptor than normal. Suppose, for instance, that (in typical conditions) if a male inherits none of the masculinity producing alleles he is of type A, if he inherits a single copy he is of type B, and if he inherits two copies he is of type C. This gene is only part of a more complicated genetic system (with many other genes that have small effects). As shown above such a high degree of variability would be desirable for males. Such a powerful masculinity producing allele could survive because the variability contributes to male reproductive success. If the allele becomes too common, there are too many of type C, and the allele is selected against. If there are too few of the allele, it is selected for. Thus, in males such an allele could be in a balanced polymorphism and could be retained. The Xq28-located gene that Hamer and co-workers have found evidence for could be an example where a single gene has large effects, one of which is homosexuality. However, in females an allele with such a large effect would be selected against (being replaced with a series of alleles, each of which individually had smaller effects). Imagine that a series of genes, each one of which accounted for a small effect, existed. Selection would have caused these to be found in such proportions that the typical female was well adapted for the typical environment. Now imagine that such a gene with a major effect tried to invade in females. It shifts the typical female toward type C, (call that allele c). This lowers such a female’s reproductive success on average, and this allele would be selected against. Likewise, an allele that shifts the typical female toward type A, call that allele a, would be selected against. We cannot say whether the typical female would be aa or cc. Note that whether the individual is aa or cc, other minor genes would have changed in frequency to make B the average phenotype. If either aa or cc was the standard form, this would be a stable situation. If aa prevailed, c could not invade, because it would shift the individual into type C and put her at a disadvantage.


PL108-309

February 14, 2000

11:52



21

Likewise, if initially all females were cc, allele a could not invade because it would produce individuals of type A, and such individuals would be at a reproductive disadvantage. Note that the equilibrium aa and cc would both be realized with the other minor genes having evolved to have frequencies such that the typical female was of type B. In such circumstances, invasion by an allele that has a large effect in either direction cannot succeed. Note that the opposite would be true for a male. Suppose that the male’s minor genes made him type B and he had the genotype aa. A new mutation introduces the possibility of an ac genotype, making the individual now of type C. Since type C’s on average outreproduce type B’s, the c allele could invade. Likewise, if the typical male was of the cc genotype (and still type B because the minor genes would have adjusted in frequency to make this the most common type), type a could invade since it would produce heterozygotes ac, and these would be of type A. Thus for males, alleles with the power to produce large shifts along the masculinity–femininity continuum would be selected for, while for females these would be selected against. In general, there are expected to be more genes having a major effect in males than in females. Expressed in terms of game theory, with the choice of offspring personality viewed as a game against nature, a mixed strategy of playing randomly different personality types is more likely to be optimal for sons than for daughters. If this theory is correct, the search for a homosexual gene with effects large enough to be detected in a small sample is more likely to be successful than the search for a gene with a similar effect in females. Since we are just at the start of the search for genes that affect sexual orientation, the above argument suggests that such genes with major effects are much more likely to be found in males than in females. The finding of Hamer and associates (1993; Hamer and Copeland, 1994; Hu et al., 1995) of evidence for a homosexual gene, but not a lesbian gene, is consistent with this argument.

ALTERNATIVE THEORIES FOR THE SURVIVAL OF HOMOSEXUALITY The discussion up to this point has tried to present in a logical manner how genes conducive to homosexuality could have survived. However, there are other theories. These are not discussed in detail here because a recent book-length review has just been published (McKnight, 1997), which the reader can consult for references and a discussion of alternative theories. The only published theory that resembles the theory of this paper is that of Mellen (1981). He speculates (p. 250) that “it may well have been of adaptive value for protohuman males to become a little less brutally aggressive, a little more sensitive, a little more responsive to external influences, a little more communicative—all of which would have been possible through the retention of


PL108-309

February 14, 2000

11:52


22

Miller

certain psychological traits of early adolescence or through the acquisition of a few particular feminine traits.” Number of Older Brothers and Homosexuality So far a theory of homosexuality has been presented. The male sexual orientation somehow takes on the female pattern, probably because a series of prenatal events changes the fetal developmental pattern. This results from the summation of a number of genetic and environmental factors. Certain alleles shift the developing fetus in the female direction, tending to produce both a greater probability of homosexuality and a more feminine, more sensitive personality. Are there any other facts about homosexuality which might be explained within this framework? As noted, the theory explains why there are more male homosexuals than female ones or lesbians. There is another effect that might be explained, the birth order effect. In men, sexual orientation correlates with the number of older siblings (Blanchard, 1997; Blanchard and Bogaert, 1996a,b, 1998; Blanchard and Sheridan, 1992a,b; Blanchard and Zucker, 1994; Blanchard, et al., 1995a,b, 1998; Jones and Blanchard,1998). Evidence shows that the effect is due to the number of older brothers, rather than the number of older sisters. Each additional older brother increases the odds of homosexuality by approximately 33% (Blanchard and Bogaert, 1996b).Without going into great detail on the studies, this effect is not just a result of larger families being more likely to produce homosexuals, or of the parents of homosexuals being older, or similar confounding factors. A traditional multigene additive theory cannot explain such an effect because an individual’s genotype is a result of a random combination of genes from the parents and does not depend on birth order. However, of course genetic information could code for a mechanism by which the child’s development depended on birth order, with the mechanism being social learning or a change in the prenatal hormonal environment. If homosexuality were indeed promoted by certain prenatal hormonal environments (including differences in receptor distributions), the mechanism producing higher rates of homosexuality in later-born sons would also produce more feminine personalities. About the time that Blanchard and associates were documenting the homosexuality birth order effect, Sulloway (1996) brought out a book showing that there were differences in career patterns of scientists depending on birth order. In the course of this work, Sulloway did a meta-analysis of the birth order and personality literature. He looked only at studies that controlled for family size and socioeconomic effects. (Many of the studies had confused socioeconomic class or family size effects with birth order, since higher birth orders require large families to exist, and families tend to be larger in the lower socioeconomic classes.) He showed that there were indeed birth order effects even after these effects were controlled for.


PL108-309

February 14, 2000

11:52



23

Birth Order Effects on the Masculinity–Femininity Continuum Much of Sulloway’s personality research also can be interpreted as younger brothers adopting a more feminine life strategy. He states (p. 77), “Status-enhancing behavior is a firstborn tendency. It is also a ‘male tendency.’ Cooperation is a laterborn tendency and it is also a ‘female’ tendency.” Later, in discussing political trends, he states (pp. 284–285), “Tough-minded individuals tend to be leaders rather than followers, stubborn rather than flexible, and moralistic rather than empathetic. . . . Not surprisingly, men are more tough-minded than women. In addition to being a male propensity, tough-mindedness is a first born characteristic.” It is plausible that this trait is affected by prenatal hormonal mechanisms that differ in males and females, and between homosexual males and heterosexual females. If the mechanism is birth order related, such that the later born become more like the recent born, it would be expected that only children would choose more sex-appropriate activities than children with older like-sex siblings, and this has been found to be the case (t = 4.99, p < .01) (Fauls and Smith, 1956). This is true even though there is “no difference between the frequency with which children with older like-sex siblings perceive the parents as preferring sex-appropriate activities for the child and the frequency with which only children perceive parents as preferring sex-appropriate activities (t = 1.09, p > .05).” The latter finding goes against a simple learning theory in which parents of only children try harder to teach them to prefer sex-appropriate activities. This finding about birth order would be very consistent with the finding that homosexuals have a different pattern of interest when young, and a different pattern of occupational interests when adults. Brim (1958) has classified most of the traits found to be affected by birth order in Koch’s work (dealing with 6 year olds) as expressive versus instrumental, which is also interpreted as feminine versus masculine (instrumental). Sulloway (1996, p. 77) reanalyzed Koch’s data using Brim’s methodology and concluded that gender and birth order had a close relationship. Overall, he concluded that the influence of birth order was two-thirds as large as for sex. In dyads that included a first-born girl and a later-born boy, the first-born girl was actually the more masculine of the two. This is consistent with the postulated mechanism acting through affecting the brain’s tendency to act in a male- or female-typical way. Another finding (Eaton et al., 1989) is that birth order affects the activity levels in infants and in children. The first-born are more active. Since males are generally more active than females, that is consistent with being first-born producing more masculine behaviors. The National Collaborative Perinatal Survey data on 7018 children showed a decline in activity level with birth order at 8 months, 3 years, and 4 years (but not for 7 year olds or for newborns). The finding in 8-month-old infants (and, to a lesser degree, in older ones) is important because such infants are too young for socialization to explain the observed effect, suggesting a biological cause. They also found, from an observational study of children


PL108-309

February 14, 2000

11:52


24

Miller

aged 5 to 9 in child-care centers, that the first-born were more active than laterborns. An earlier study (Eaton and Dureski, 1986) had reported first-borns to be more active when infant activity was measured by actometers attached to the arms. Evolution frequently seizes mechanisms which have evolved originally for other purposes. There is strong evidence that many personality traits differ between males and females. The exact mechanism for this is not known, but much of the evidence points to a hormonal mechanism. Maccoby et al. (1979) have shown that the levels of testosterone in umbilical cord blood varies with birth order, and Jacklin et al. (1983) have shown that timidity varies with the level of hormones. Such a mechanism could be controlled by the mother’s genes. Precedents exist in the animal kingdom for biological control of behavior in accordance with birth order. Birds have been shown to have the ability to vary the amount of testosterone in the egg depending on the birth order, hence influencing their behavior (Schwabl et al., 1997). Indirect evidence for hormones varying with birth order is that testicular cancer decreases in frequency with birth order (Prener et al., 1992), with the most plausible explanation being differences in prenatal hormonal exposure with birth order. Adult Behavior and Birth Order Sulloway (1996) and others present evidence that birth order affects adult behavior. He has evidence that younger sons are more likely to support scientific revolutions. He has collected data on thousands of scientists who were involved in 42 scientific revolutions and shows birth order effects on the positions they took. For instance, his data on several hundred scientists who were involved in the Darwinian Revolution show that birth order was very important, with the later-born much more likely to be Darwinian. He documents birth order effects in such nonscientific areas as the French Revolution, the Protestant Reformation, and the voting of U.S. Supreme Court Justices. The tough-minded/tender minded distinction is important. The tough-minded tend to be first-born and are willing to take strong actions to further their interests, such as suppressing dissent by force. For instance, the votes to execute the king in the French Revolution could be predicted by birth order, with the first-born voting for execution. His chapter on politics (pp. 284–305) shows (among other things) that votes on the U.S. Supreme Court can be predicted (partially) from birth order. Socialization and Birth Order In ascribing the birth order effects found by Sulloway to a biological mechanism, this paper explicitly differs from Sulloway’s explanation and the other


PL108-309

February 14, 2000


11:52


25

socialization explanations often offered. Sulloway attributes the differences in behavior to childhood experiences. The environment of the first- and later-borns are quite different, and children develop different strategies for survival depending on their environments. This is true and his account is plausible. It is especially plausible when explaining why children of different birth orders should act differently in childhood. However, what Sulloway found was differences in adult outcomes, not childhood behavior. A major problem with his explanation is that the environments of laterborn adults are not very different from those of first-born adults. If all that was happening was that humans were again displaying their behavioral flexibility, we would expect that the differences observed in childhood would disappear as the children left home and moved out into the world, establishing their own families. One possible answer to this argument is that personality traits are “hardwired” so that they cannot be changed after maturation. Given what is known about brain development, and the persistence of personality traits from childhood to adulthood (most personality traits exhibited in childhood do persist into adulthood), the persistence of personality traits that differed by birth order into adulthood is plausible. Thus, a socialization explanation is possible. Yet there remains the question of why evolution would have designed humans so that personality traits that are useful in children necessarily persist into adulthood. Provision for changing behavior would be especially likely if the childhood environment with its sibling competition changed radically when the child grew up, left home, and no longer had to adjust to the presence of siblings. If desirable childhood behavior resulted in undesirable adult behavior, evolution would have made it easy for adults to adopt behaviors different from their childhood behaviors. Such changes in behavior with maturation clearly occur. For instance, males become more aggressive in adolescence. Presumably, if the adult behavior that maximized reproductive success did not depend on birth order, any behavioral differences would be counterproductive and, at first glance, selected against. Thus, it is very likely that the selective advantage of behavior that differs by birth order persists into adulthood, although the nature of the benefits might change. Thus, we should look for benefits of birth order effects that persist into adulthood. Beer and Horn (in press), using adoption study data from Texas and Colorado, compared first-born children in families with adopted children reared either as a social senior with a younger sibling or as a social junior with an older sibling (thus making it possible to control for biological order of birth effects). The only rearing order effect that was statistically significant was for conscientious. None of the other expected personality differences showed up. One commentator (Cohen, 1999, p. 28) notes, “The clear implication is that the birth order effect is uterine rather than social, physiological rather than familial.”


PL108-309

February 14, 2000

11:52


26

Miller

Diversification by Birth Order The author (Miller, 1997a) has shown that diversification pays in evolution as well as in the business world, and genes that make two siblings pursue different life strategies are sometimes to the advantage of the parents even if not to the individuals. Perhaps the simplest example is where there are major advantages to dispersal for the survival of the parent’s genes, but yet it is in the interest of both siblings to stay and to compete with their brothers for the niche that the parent occupies and will vacate as they age. An example is band leadership. If two brothers both bid for leadership, they may neutralize each other’s efforts and neither achieve leadership. Having one brother with a personality suited to a bid for leadership and the other with a more cooperative personality, inclined to support the first brother in his bid, is desirable. It would be in the parent’s genetic interest to have a mechanism such that offspring differed in personality and followed different strategies. A difference in dispersal strategies may also be desirable. The openness to experience that Sulloway found may serve the purpose of giving the older brothers the flexibility to concede the parental niche to a less flexible elder brother and to seek their fortunes elsewhere, in a different environment.One way to ensure diversification is to have some mechanism that keeps track of the number of older brothers and adjusts the personalities of the younger brothers, thus making it more likely that older and younger brothers have different personalities. The benefits of such diversification extend past childhood into adulthood. Such a mechanism could easily explain why natural selection has not limited birth order differences in behavior to childhood but has, instead, produced the variations in adult behavior found by Sulloway.

Mechanisms for the Birth Order Effects What could be the mechanisms that produce the birth order effects? Blanchard and Bogaert (1996b) and Blanchard and Klassen (1997) have presented a biological hypothesis for the birth order effect in homosexuality. It is hypothesized that this fraternal birth order effect reflects the progressive immunization of some mothers to Y-linked minor histocompatibility antigens (H-Y antigen) by each succeeding male fetus and the concomitantly increasing effects of H-Y antibodies on the sexual differentiation of the brain in each succeeding male fetus. At first glance, if such a mechanism appeared, it would seem that it would be subject to strong selection that caused it to disappear. The mechanism seems to require both that the mother’s body keep track of the number of sons she has borne and take actions that made later-born sons more likely to be homosexual. Any mutation that disrupted this mechanism in the mother and prevented her


PL108-309

February 14, 2000


11:52


27

from developing such progressive immunization would be expected to reduce the number of homosexual sons she bears. Any such birth order effect destroying mutation would thus be strongly selected for, unless there were strong benefits arising from keeping the mechanism intact. Thus, the Blanchard and Klassen mechanism (and any similar mechanism by which mothers kept count of the number of sons borne and then made the later-born sons more likely to be homosexual) would be easily disrupted by natural selection. It is a multistep process where any mutation disrupting one step would be selected for. Thus, it become critical to ask how a mechanism such as they propose could survive. If the mechanism could survive, it is at least a plausible mechanism for producing a birth order effect. Fortunately, the above discussion of why a birth order effect might contribute to diversification explains how an effect such as Blanchard and Klassen propose could survive. If homosexuality is merely a by-product of a mechanism that adjusts personality in a more feminine, more sensitive direction (possibly through prenatal hormonal effects), and there are advantages to younger sons being more feminine and less aggressively masculine, a mechanism that produces such a femininity shift could indeed survive, and even be selected for. A younger son being more sensitive and flexible facilitates his competing for resources during childhood. In adulthood, it avoids competition of the younger brothers with the older ones. There is scope for parent–offspring conflict regarding diversification. Each son maximizes his reproductive success if he competes for the most desirable niche, perhaps a leadership position. The parental reproductive interest is in diversification, and this may mean having one son (the first?) take the most attractive niche, and then others compete for other niches. A mechanism in the mother that moderated the younger sons’ competitive drive could be in the mother’s reproductive interest. The Blanchard and Klassen H–Y antigen mechanism might do this through somehow changing the “masculinarity” of the later sons. Such a mechanism coded into the mother’s genes could be selected for. However, such selection not to compete may not be in the interest of the later-born sons themselves. Although they share half of their genes with their brothers, their reproductive interest is still in competing for the niches that would give them the greatest number of offspring. The sons might evolve countermeasures to the mother’s attempts to direct their development. Any mechanism in the son (say a change in the blood/brain barrier) that kept the mother’s antibodies from affecting her son’s brain and increasing its probability of being homosexual would be selected for. It would lower the probability of that son being homosexual and, hence, increase the number of descendants he would have. If the effect on the later-born sons was to shift their personalities in a more feminine direction, the personality of these sons would be too feminine and not aggressive enough. Suppose that the evolution of these measures in the mothers had not changed the personalities of the elder sons. This implies that, averaged over


28

PL108-309

February 14, 2000

11:52


Miller

all sons, the personalities would be too feminine, too flexible. The average male would not be “masculine” enough for his own maximal reproductive success. This would produce a general selection in males for a more aggressive, more masculine personality, which is then moderated by the mother’s influence back toward the more optimal level. Selection for male masculinarity genes stops when the average male (average of first and later born ones) has the optimal genotype for these traits. Since the probability of a particular gene being passed on is the same for first- and later-borns, the selection acts on the average male (some first-born, some later-born). When the average male has the optimal genotype, the first-born males will be too masculine, too aggressive. The later-born males are shifted in a more feminine direction, with the possibility that the last-born are too feminine for maximal reproductive success. Note how, in equilibrium, average masculinity is probably unchanged from what would exist in the absence of the maternal mechanism which adjusts masculinity to birth order. The first-born males are more masculine and less likely to be homosexual than they would if this maternal mechanism did not exist. The later-born are more likely to be homosexuals, but the average rate of homosexuality is probably unchanged. One’s first reaction on hearing of a mechanism that might make later-borns sons more likely to be homosexual is that the resulting increase in homosexuality would reduce both the mother’s and the son’s reproductive success. It would hence be strongly selected against. The above argument shows that this need not be the effect in full equilibrium. A maternal mechanism that operates on the degree of “masculinity” can explain the homosexuality birth order effect. The homosexuality is just a by-product of shifting in the feminine direction. It is possible that some birth order effects are produced by other than a hormonal mechanism or through socialization. As Sulloway points out, not all birth order effects are parallel to gender. Conscientiousness is strongest in the firstborn. His literature review (p. 74) found 20 studies showing this result and none showing the opposite. Yet females are usually more conscientious than males. The explanation may be social, with parents devoting more effort to inculcating conscientiousness in their first-born (especially when they are young and the parents can devote their full efforts to the child), or as Sulloway speculates it could be related to the first-born seeking parental approval by conforming to parental norms. Conscientiousness (Beer and Horn, in press) is the one personality trait for which there is evidence that the social effects of having siblings can produce a “birth order” effect. There may be an evolutionary advantage to first-borns being unusually conscientious. Very often the older siblings help take care of the younger siblings. Doing so successfully requires a high degree of conscientiousness. Since the younger siblings are carrying many of the same genes as the older siblings, genes that made for conscientiousness in older siblings would be selected for. Given the low cognitive abilities of most children, rigidly following parental rules would make them


PL108-309

February 14, 2000


11:52


29

better caretakers for even younger children than a more flexible personality. Since conscientiousness usually increases with age, to achieve the level of conscientiousness in a child that would make him or her a good caregiver for younger siblings (or at least would keep them from using their greater size to harm the younger ones) would require the sort of design that would make for a highly conscientious, perhaps even rigid adult. The inflexibility and toughness in first-born adults that Sulloway found may be the result of a mechanism designed to ensure that they rigidly follow parental instructions when young. Younger siblings would not benefit as much from conscientiousness. They less often take care of even younger siblings. Because they are usually smaller and weaker than the older siblings, they do not need conscientiousness and a tendency to obey rules to avoid hurting the other siblings. Instead, openness to experience and flexibility may be required to obtain the resources needed for them to survive childhood. In considering the evolutionary probabilities, it should be noted that high conscientiousness in the first-born (and other early-born) is more strongly in the mother’s interest (her genes benefit from having the younger children cared for and not hurt) than in the interest of the first-born itself (who may be called on to sacrifice his immediate interest to care for the younger ones or to avoid hurting them). Mothers would be strongly selected for a mechanism which kept track of birth order and somehow modified the personalities of the offspring to achieve the optimal combination. The beauty of the mechanism proposed by Blanchard and Klassen is that it provides a way for the mother to keep track of the number of sons borne and to have the personalities differ. This ensures the desired diversification. The above mechanism could also explain why boys with gender identity disorder have a different sibling sex ratio (Zucker et al., 1997) since those with older brothers would have more feminizing effects. The same set of events could also cause certain boys to have the parts of their brain that related to gender identity femininized. Having behavior depend on birth order could be achieved by other mechanisms. Such mechanisms would require that somehow the mother’s body retain knowledge of how many previous children had been born and their sex. There is one other mechanism known which could retain this information. Male fetal progenitor cells persist in maternal blood for as long as 27 years postpartum (Bianchi et al., 1996). It is possible that the mother might somehow use this information to modify the personality of her sons, thus achieving optimal diversification.

CONCLUSION The survival of a human predisposition for homosexuality can be explained by sexual orientation being a trait that is influenced by a number of pleitropic


PL108-309

February 14, 2000

11:52

30


Miller

genes. These operate during the development process to shift male development, including that of the brain, in the female direction. If, by chance, a male inherits numerous alleles that shift his development in the feminine direction, he becomes homosexual or bisexual. However, more often these alleles are inherited along with other genes that make the male heterosexual. Then the effect of the alleles is to make for greater sensitivity, empathy, tender-mindedness, and kindness. These traits make heterosexual carriers of the genes better fathers and more attractive mates. As long as such alleles sometimes lead to homosexuality, evolution will act so as to increase the frequency of other alleles that produce males who are too masculine for maximal reproductive success. This creates a balanced polymorphism in which the feminizing effect of these alleles in heterosexuals offsets the adverse effects (on reproductive success) of these alleles’ contribution to homosexuality. A similar effect probably occurs for genes that can produce lesbianism in females. The whole system survives because it serves to provide a high degree of variability among the personalities of offspring, providing the genotype with diversification and reducing competition among offspring for the same niches. Because extremes of personality are more advantageous to males, the variability along the masculine/femininity axis is greater for males. This is reflected in male homosexuals being more common than female ones. The birth order effect on homosexuality is probably a by-product of a mechanism that shifts personalities more in the feminine direction in the later-born sons, reducing the probability of these sons engaging in unproductive competition with each other. The above has implications for sociobiology. The requirement that a causal mechanism survive over evolutionary time imposes constraints on the set of possible mechanisms to explain homosexuality. A mechanism (i.e., a gene for homosexuality) which produces only homosexuality would be strongly selected against and could not survive. A pleitropic gene for which homosexuality was one of only several mechanisms could survive. The evolutionary perspective contributes to understanding the causes of a puzzling phenomenon.

REFERENCES Alexander, J. E., and Sufka, K. J. (1993). Cerebral lateralization in homosexual males? A preliminary EEG investigation. Int. J. Psychophysiol. 15: 269–274. Allen, L. S., and Gorski, R. A. (1992). Sexual orientation and the size of the anterior commissure in the human brain. Proc. Natl. Acad. Sci. USA. 89: 7199–7202. Bailey, J. M., and Martin, N. G. (1995). A twin registry study of sexual orientation. Poster presentation at the International Academy of Sex Research, 21st Annual Meeting, Provincetown, MA. Bailey, J. M., and Pillard, R. C. (1991). A genetic study of male sexual orientation. Arch. Gen. Psychiatry 48: 1089–1096. Bailey, J. M., and Zucker, K. J. (1995). Childhood sex-type behavior and sexual orientation: A conceptual analysis and quantitative review. Dev. Psychol. 31: 43–55.


PL108-309

February 14, 2000


11:52


31

Bailey, J. M., Pillard, R. C., Neale, M. C., and Agyei, Y. (1993). Heritable factors influence sexual orientation in women. Arch. Gen. Psychiatry 50: 217–223. Bailey, J. M., Finkel, E., Blackwelder, K., and Bailey, T. (1996). Masculinity, feminity, and sexual orientation (unpublished manuscript). Bailey, J. M., Kim, P., Hills, A., and Linsenmeier, J. (1999). Butch, femme, or straight-acting? Partner preferences of gay men and lesbians. J. Pers. Soc. Psychol. 73: 960–973. Bailey, J. M., Dunne, M. P., and Martin, N. G. (in press). Genetic and environmental influences on sexual orientation and its correlates in an Australian twin sample. J. Pers. Soc. Psychol. Baker, R., and Bellis, M. (1995.) Human Sperm Competition, Chapman and Hall, London. Bakker, J., and Slob, A. K. (1997). Sexual differentation of the brain and partner preferences in the male rat: Behavioral, neuroanatomical and neuroimmunocytochemical studies. In Ellis, L., and Ebertz, L. (eds.), Sexual Orientation: Toward Biological Understanding, Praeger, Westport, CT, pp. 91–106. Beer, J., and Horn, J. M. (1999). The influence of rearing order on personality development within two adoption cohorts. J. Personality (in press). Bell, A. P., and Weinberg, M. (1978). Homosexualities: A Study of Diversity Among Men and Women, Simon and Schuster, New York. Bell, A. P., Weinberg, M., and Hammersmith, S. (1981). Sexual Preference: Its Development in Men and Women, Indiana University Press, Bloomington. Bianchi, D. W., Zickwolf, G. K., Weil, G. J., and Sylvester, S. (1996). Male fetal progenitor cells persist in maternal blood for as long as 27 years postpartum. Proc. Natl. Acad. Sci. USA 93: 705–708. Blanchard, R. (1997). Birth order and sibling sex ratio in homosexual versus heterosexual males and females. Annu. Rev. Sex Res. 8: 27–67. Blanchard, R., and Bogaert, A. F. (1996a). Biodemographic comparisons of homosexual and heterosexual men in the Kinsey interview data. Am. J. Psychiatry 153: 27–31. Blanchard, R., and Bogaert, A. F. (1996b). Homosexuality in men and number of older brothers. Arch. Sex. Behav. 25: 545–573. Blanchard, R., and Bogaert, A. F. (1998). Birth order in homosexual versus heterosexual sex offenders against children, pubescents, and adults. Arch. Sex. Behav. 27: 595–603. Blanchard, R., and Klassen, P. (1997). H-Y antigen and homosexuality in men. J. Theor. Biol. 185: 373–378. Blanchard, R., and Sheridan, P. (1992a). Proportion of unmarried siblings of homosexual and nonhomosexual gender-dysphoric patients. Can. J. Psychiatry 37: 163–167. Blanchard, R., and Sheridan, P. (1992b). Sibship size, sibling sex ratio, birth order, and parental age in homosexual and nonhomosexual gender dysphorics. J. Nerv. Ment. Dis. 180: 40–47. Blanchard, R., and Zucker, K. (1994). Reanalysis of Bell, Weinberg, and Hammersmith’s data on birth order, sibling sex ratio, and parental age in homosexual men. Am. J. Psychiatry 151: 1375– 1376. Blanchard, R., Zucker, K., Bradley, S. J., and Hume, C. (1995a). Birth order and sibling sex ratio in homosexual male adolescents and probably prehomosexual feminine boys. Dev. Psychol. 31: 22–30. Blanchard, R., Zucker, Cohen-Kettenis, P., Gooren, L., and Bailey, J. M. (1995b). Birth order and sibling sex ratio in two samples of Dutch gender-dysphoric homosexual males. Arch. Sex. Behav. 25: 495–514. Blanchard, R., Zucker, K., Siegelman, M., Dickey, R., and Klassen, P. (1998). The relation of birth order to sexual orientation in men and women. J. Biosoc. Sci. 30: 511–519. Bogaert, A. F., and Blanchard, R. (1996). Physical development and sexual orientation in men: Height, weight, and age of puberty differences. Person. Indiv. Diff. 21: 77–84. Brim, O. G. (1958). Family structure and sex role learning by children: A further analysis of Helen Koch’s data. Sociometry 21: 1–16. Buss, D. M. (1989). The Evolution of Desire, Basic Books, New York. Buss, D. M. (1994). Sex differences in human mate preference: Evolutionary hypothesises tested in 37 cultures. Behav. Brain Sci. 12: 1–49. Buss, D. M., and Barnes, M. (1994). Preferences in human mate selection. J. Pers. Soc. Psychol. 50: 559–570. Chung, Y. B., and Harmon, L. W. (1994). The career interests and aspirations of gay men: How sex role orientation is related. J. Vocat. Behav. 45: 223–239.


32

PL108-309

February 14, 2000

11:52


Miller

Cohen, D. B. (1999). Stranger in the Nest: Do Parents Really Shape Their Child’s Personality, Intelligence, or Character? John Wiley & Sons, New York, p. 28. Dorner, G., Rohde W., Stahl, F., et al. (1975). A neuroendocrine predisposition for homosexuality in men. Arch. Sex. Behav. 4: 1–8. Dorner, G., Schenck, B., Shmiedel, B., and Ahrens L. (1983). Stressful events in prenatal life of bi and homosexual men. Exp. Clin. Endocrinol Diabetes. 81: 83–87. Eaton, W., and Dureski, C. M. (1986). Parent and actometer measures of motor activity in the young enfant. Infant Behav. Dev. 9: 383–393. Eaton, W., Chipperfield, J., and Singbeil, C. (1989). Birth order and activity level in children. Dev. Psychol. 25: 668–672. Eaves, L. J., Eysenck, H. J., and Martin, N. G. (1989). Genes, Culture, and Personality, Academic Press, London. Ellis, L. (1997). Perinatal influences on behavior and health, with special emphasis on sexual orientation and other sex-linked behavior. In Ellis, L., and Ebertz, L. (eds.), Sexual Orientation: Toward Biological Understanding, Praeger, Westport, CT, pp. 71–88. Ellis, L., and Ames, M.A. (1987). Neurohormonal functioning and sexual orientation: A theory of homosexuality-heterosexuality. Psychol. Bull. 101: 233–258. Ellis, L., and Ebertz, L. (eds.) (1997). Sexual Orientation: Toward Biological Understanding, Praeger, Westport, CT. Ellis, L., Ames, M. A., Peckham, W., and Burke, D. (1987). Sexual orientation of human offspring may be altered by severe maternal stress during pregnancy. J. Sex Res. 25: 152–157. Ellis, L., Hoffman, H., and Burke, D. M. (1990). Sex, sexual orientation and criminal and violent behavior. Person. Indiv. Diff. 11: 1207–1212. Eysenck, H. J., and Wilson, G. (1979). The Psychology of Sex, J. M. Dent and Sons, London. Fauls, L. B., and Smith, W. D. (1956). Sex role learning of five-year-olds. J. Genet. Psychol. 89: 105–117. Gallup, G., and Suarez, S. (1983). Homosexuality as a by-product of selection for optimal heterosexual strategies. Perspect. Biol. Med. 26: 315–322. Gandelman, R. (1992). Psychobiology of Behavioral Development, Oxford University Press, Oxford. Getz, W. (1993). Invasion and maintenance of alleles that influence reproductive success. J. Theor. Biol. 162: 515–537. Gettelman, T. E., and Thomas, J. K. (1993). Actual differences and stereotypical perceptions in body image and eating disturbance: A comparison of male and female heterosexual and homosexual samples. Sex Roles 29: 545–562. Gladue, B. A., Green, R., and Hellman, R. E. (1984). Neuroendocrine response to estrogen and sexual orientation. Psychoneurorendocrinology 20: 475–485. Gladue, B. A., Beatty, W. W., Larson, J., and Staton, R. D. (1990). Sexual orientation and spatial ability in men and women. Psychobiology 18(1): 101–108. Goode, E., and Troiden, R. R. (1980). Correlates and accompaniments of promiscuous sex among male homosexuals. Psychiatry 43: 51–59. Gooren, L. J. G. (1986). The neuroendocrine response of luteinizing hormone to estrogen administration in heterosexual, homosexual, and transsexual subjects. J. Clin. Endocrinol. Metab. 63: 588–593. Gorman, M. R. (1994). Male homosexual desire: Neurological investigations and scientific bias. Perspect. Biol. Med. 38(1). Green, R. (1987). The “Sissy Boy Syndrome” and the Development of Homosexuality, Yale University Press, New Haven, CT. Guadio, R. P. (1994). Sounding gay: Pitch properties in the speech of gay and straight men. Am. Speech 69(1). Hall, J. A. Y., and Kimura, D. (1994). Dermatoglyphic asymmetry and sexual orientation in men. Behav. Neurosci. 108: 1203–1206. Hall, J. A. Y., and Kimura, D. (1995). Sexual orientation and performance on sexually dimorphic motor tasks. Arch. Sex. Behav. 24: 395–407. Halpern, D. F., and Crothers, M. (1997). Sex, sexual orientation, and cognition. In Ellis, L., and Ebertz, L. (eds.), Sexual Orientation: Toward Biological Understanding, Praeger, Westport CT, pp. 181– 197. Hamer, D., and Copeland, P. (1994). The Science of Desire, Simon and Schuster, New York. Hamer, D., and Copeland, P. (1998). Living with Our Genes, Doubleday, New York.


PL108-309

February 14, 2000


11:52


33

Hamer, D., Hu, S., Magnuson, V., Hu, N. and Pattatuci, A. (1993). A linkage between DNA markers on the X chromosome and male sexual orientation. Science 261: 321–327. Hu, S., Pattatuci, A., Patterson, C., Li, L., Fulker, D. W., Cherny, S., Kruglyak, L., and Hamer, D. (1995). Linkage between sexual orientation and chromosome Xq28 in males but not in females. Nature Genet. 11: 248–256. Jacklin, C. N., Maccoby, E., and Doering, C. H. (1983). Neonatal sex-steroid hormones and timidity in 6–18-month-old boys and girls. Dev. Psychobiol. 16(3): 163–168. Jones, M. B., and Blanchard, R., (1998). Birth order and male homosexuality: Extension of Slater’s index. Hum. Biol. 70: 775–787. Kallmann, F. J. (1952). Comparative twin studies on the genetic aspects of male homosexuality. J. Nerv. Ment. Dis.115: 283–298. Laumann, E., Gagnon, J. H., Michael R. T., and Michaels, S. (1994). The Social Organization of Sexuality: Sexual Practices in the United States, University of Chicago Press, Chicago. LeVay, S. (1991). A difference in hypothalamic structure between heterosexual and homosexual men. Science 253: 1034–1037. LeVay, S. (1993). The Sexual Brain, MIT Press, Cambridge, MA. LeVay, S. (1996). Queer Science: The Use and Abuse of Research into Homosexuality, MIT Press, Cambridge, MA. Maccoby, E. E., Doering, C. H., Jacklin, C. N., and Kraemer, H. (1979). Concentrations of sex hormones in umbilical cord blood: Their relation to sex and birth order in infants. Child Dev. 50: 632–642. MacIntrye, F., and Estep, K. W. (1993). Sperm competition and the persistence of the genes for male homosexuality. Biosystems 31: 223–233. McCormick, C. M., and Witelson, S. F. (1991). A cognitive profile of homosexual men compared to heterosexual men and women. Psychoneurorendocrinology 16: 459–473. McFadden, D., and Pasanen, E. G. (1998). Comparison of the auditory systems of heterosexuals and homosexuals: Click-evoked otoacoustic emissions. Proc. Natl. Acad. Sci. USA 95: 2709–2713. McGuire, T. R. (1995). Is homosexuality genetic? A critical review and some suggestions. J. Homosex. 28(1/2): 115–144. McKnight, J. (1997). Straight Science: Homosexuality, Evolution and Adaptation, Routledge, New York. Mellen, S. L. (1981). The Evolution of Love, Freeman, San Francisco. Miller, E. M. (1994). Prenatal sex hormone transfer: A reason to study opposite-sex twins. Person. Indiv. Diff. 17: 511–529. Miller, E. M. (1997a). Could nonshared environmental variance have evolved to assure diversification through randomness? Evol. Hum. Behav. 18: 195–221. Miller, E. M. (1997b). Evidence from opposite-sex twins for the effects of prenatal sex hormones. In Ellis, L., and Ebertz, L. (eds.), Males, Females, and Behavior: Toward Biological Understanding, Praeger, Westport, CT. Moran, P. A. P. (1972). Familial effects in schizophrenia and homosexuality. Aust. N.Z. J. Psychiatry 6: 116–119. Murray, S. O. (1991). Homosexual occupations in Meso-America. J. Homosex. 21: 57–65. Perkins, M. W. (1981). Female homosexuality and body build. Arch. Sex. Behav. 10: 337–345. Pillard, R. C. (1991). Masculinity and femininity in homosexuality: “Inversion” revisited. In Gonsiorek, J. C., and Weinrich, J. D. (eds.), Homosexuality: Research Implications for Public Policy. Sage, Newbury Park, CA, pp. 32–43. Pillard, R. C., and Weinrich, J. D. (1986). Evidence of familial nature of male homosexuality. Arch. Gen. Psychiatry 43: 808–12. Pillard, R. C., and Bailey, J. M. (1998). Human sexual orientation has a heritable component. Hum. Biol.347–365. Plomin, R., Chipuer, H. M., and Neiderhiser, J. M. (1994). Behavior genetic evidence for the importance of nonshared environment. In Hetherington, E. M., Reiss, D., and Plomin, R. (eds.), Separate Social Worlds of Siblings: The Impact of Nonshared Environment on Development, Lawrence Erlbaum, Hillsdale, NJ. Prener, A., Hsieh, C., Engholm, G., Trichopoulos, D., and Jensen, O. (1992). Birth order and risk of testicular cancer. Cancer Causes Control 3: 265–272. Reite, M., Scheeder, J., Richardson, D., and Teale, P. (1995). Cerebral laterality in homosexual males: Preliminary communication using magnetoencephalography. Arch. Sex. Behav. 24: 585–593.


34

PL108-309

February 14, 2000

11:52


Miller

Rogers, S. M., and Turner, C. F. (1991). Male-male sexual contact in the USA: Findings from five sample surveys, 1970–1990. J. Sex Res. 28(4): 491–519. Rowe, D. C. (1994). The Limits of Family Influence: Genes, Experience, and Behavior, Guilford, New York. Saghir, M. T., and Robins, E. (1973). Male and Female Homosexuality, Williams and Wilkins, Baltimore. Salais, D., and Foscher, R. B. (1995). Sexual preference and altruism. J. Homosex. 28: 185–196. Schlegel, W. S. (19xx). Die Sexualinstinkte de Menschen, Tutten Verlag, Munich. Siever, M. D. (1994). Sexual orientation and gender as factors in socioculturally acquired vulnerability to body dissatisfaction and eating disorders. J. Consult. Clin. Psychol. 62: 252–260. Spence, J. T., and Helmreich, R. L. (1978). Masculinity and Feminity, University of Texas Press, Austin. Sprecher, S. (1989). The importance to males and females of physical attractiveness, earnings potential, and expressiveness in initial attraction. Sex Roles 21: 591–605. Sprecher, S., Sullivan, Q., and Hartfield, E. (1994). Mate selection preferences: Gender differences examined in a national sample. J. Pers. Soc. Psychol. 66: 1074–1080. Sulloway, F. J. (1996). Born to Rebel: Birth Order, Family Dynamics, and Creative Lives, Pantheon Books, New York. Sundet, J. M., Kvalem, I. L., Magnus, P., and Bakketeig, L. S. (1988). Prevalence of risk-prone behavior in the central population of Norway. In Fleming, A. F., Carballo, M., and Fitzsimons, D. F. (eds.), The Global Impact of AIDS, Alan R. Liss, London. Swaab, D. F., and Hofman, M. A. (1990). An enlarged suprachiasmatic nucleus in homosexual men. Brain Res. 537: 141–148. Swaab, D. F., and Hofman, M. A. (1995). Sexual differentiation in the human hypothalamus in relation to gender and sexual orientation. Trends Neurosci. 18: 264–270. Swaab, D. F., Slob, A. K., Houtsmuller, E. J., Brand, T., and Zhou, J. N. (1995). Increased number of vasopressin neurons in the suprachiasmatic nucleus (SCN) of “bisexual” adult male rats following perinatal treatment with the aromatase blocker ATD. Dev. Brain Res. 85: 273–279. Swaab, D. F., Zhou, J. N., Fodor, M., and Jofman, M. A. (1997). Sexual differentiation of the human hypothalamus: Differences according to sex, sexual orientation, and transsexuality. In Ellis, L., and Ebertz, L. (eds.), Sexual Orientation: Toward Biological Understanding, Praeger, Westport, CT, pp. 129–150. Symons, D. (1990). The Evolution of Human Sexuality, Oxford University Press, New York. Tuttle, G. E., and Pillard, R. C. (1991). Sexual orientation and cognitive abilities. Arch. Sex. Behav. 13: 427–439. Van de Ven, P., Rodden, P., Crawford, J., and Kippax, S. (1997). A comparative demographic and sexual profile of older homosexually active men. J. Sex Res. 34: 349–360. Wegesin, D. J. (1998). Event-related potentials in homosexual and heterosexual men and women: Sex-dimorphic patterns in verbal asymmetries and mental rotation. Brain Cogn. 36: 73–92. Weinrich, J. D. (1976). Human Reproductive Strategies (Doctoral dissertation, Harvard University), University Microfilms No. 77-8348. Weinrich, J. D. (1987). Sexual Landscapes, Scribner’s Sons, New York. Wellings, K., Field, J., Johnson, A., and Wadsworth, J. (1994). Sexual Behavior in Britain., Penguin Books, New York. Werner, D. (1998). On the evolution and cross-cultural variation in male homosexuality [Sobre a evolu¸c¨ıo e varia¸c¨ıo cultural na homossexualidade masculina]. In Pedro, J. M., and Grossi, M. P., (orgs.), Masculino, Feminino Plural, Mulheres, Florianópolis, pp.99–129. Whitam, F. L., Diamond, M., and Martin, J. (1993). Homosexual orientation in twins: A report on 61 pairs and 3 triplet sets. Arch. Sex. Behav. 22: 187–206. Wilson, E. O. (1975). Sociobiology: The New Synthesis, Harvard University Press, Cambridge, MA. Zucker, K. J., and Bradley, S. (1995). Gender Identity Disorder and Psychosexual Problems in Children and Adults, Guilford Press, New York. Zucker, K. J., Green, R., Coates, S., Zuger, B., Cohen-Kettenis, P. T., Zecca, G. M., Lertora, V., Money, J., Hahn-Burke, S., Bradley, S. J., and Blanchard, R. (1997). Sibling sex ratio of boys with gender identity disorder. J. Child Psychol. Psychiatry 38: 543–551.

P1: FLF/FNV

P2: FNN

Archives of Sexual Behavior [asb]

PL108-310

February 14, 2000

17:12



The Evolution of Sex Differences in Language, Sexuality, and Visual–Spatial Skills R. Joseph, Ph.D.1,2

The evolutionary neurological and physical foundations for human sex differences in language, sexuality, and visual spatial skills are detailed and primate and human studies are reviewed. Trends in the division of labor were established early in evolution and became amplified with the emergence of the “big brained” Homo erectus. A bigger brain necessitated a size increase in the birth canal and female pelvis. These and other physical changes, e.g., the swelling of the breasts and buttocks, may have paralleled the evolution of full-time sexual receptivity, the establishment of the home base, and exaggerated sex differences in the division of labor (hunting vs. gathering), which in turn promoted innate sex differences in visual spatial vs. language skills. For example, female primates produce more social and emotional vocalizations and engage in more tool use and gathering activities, whereas males tend to hunt and kill. Similar labor divisions are evident over the course of human evolution. “Woman’s work” such as child rearing, gathering, and domestic tool construction and manipulation contributed to the functional evolution of Broca’s speech area and the angular gyrus—which injects temporal sequences and complex concepts into the stream of language and thought. These activities gave rise, therefore, to a female superiority in grammatical (temporal sequential) vocabulary-rich language. Hunting as a way of life does not require speech but requires excellent visual–spatial skills and, thus, contributed to a male visual–spatial superiority and sex difference in the brain. Over the course of evolution males acquired modern human speech through genetic inheritance and because they had mothers who taught them language. KEY WORDS: evolution; sex differences; language; visual spatial skills; Homo erectus; Cro-Magnon; inferior parietal lobe; Broca’s area.

1 Brain Research Laboratory, San Jose, and Palo Alto V.A. Medical Center, Palo Alto, California. 2 To whom correspondence should be addressed at Brain Research Laboratory, 1515 The Alameda,

Suite 100, San Jose, California 95126. Fax: 408-286-9833. E-mail: [email protected]

35 C 2000 Plenum Publishing Corporation 0004-0002/00/0200-0035$18.00/0 °

P1: FLF/FNV

P2: FNN


PL108-310

February 14, 2000

17:12

36


Joseph

INTRODUCTION There have been numerous research reports examining the biological, psychological, cultural, and political influences which are presumed to influence and shape sex differences in cognition, emotion, language, and human behavior. With few exceptions (Joseph, 1985, 1992a, 1993, 1996a; Levy, 1972), little attention has been devoted to the evolutionary foundations which have given rise to these human sex differences or the fact that many of the same sex-specific cognitive traits are demonstrated by numerous other species. For example, it is well established that human females excel over males across a variety of language and articulatory-related tasks (Bayley, 1968; Broverman et al., 1968; Harris, 1978; Koenigsknecht and Friedman, 1976; Hampson and Kimura 1992; Harshman et al., 1983; Hyde and Lynn, 1988; Kimura, 1993; Lezak, 1983; McGlone, 1980; McGuiness, 1976; Moore, 1967). Human females produce more social–emotional vocalizations (Brody, 1985; Burton and Levy, 1989; Gilbert, 1969; Joseph, 1993, 1996b, 1999a; Tannen, 1990), and when in all-female groups or pairs, they tend to talk faster and to vocalize mutually more than males in all-male groups or pairs (Glass, 1993; Joseph, 1993; Tannen, 1990). Likewise, female monkeys and apes and primate mothers and female infants vocalize more frequently and more frequently engage in mutual social vocalizations (e.g., Cross and Harlow, 1965; Erwin, 1980; Mori, 1975; Mitchell, 1979). Primate mothers and daughters (e.g., chimpanzees) engage in mutual vocalizations and remain physically close for up to a decade or more, and mothers typically have several successive daughters or sons, thus forming mutually vocalizing family units. Male primates (e.g., chimpanzees), although more noisy, tend to vocalize only periodically, such as when threatening other males or females and when excited, frightened, and engaged in dominance displays (e.g., Erwin, 1980; Fedigan, 1992; Goodall, 1986, 1990; Mitchell, 1979). Hence, these trends toward a greater female facility for vocalizing were likely well established long before the emergence of modern Homo sapiens sapiens. Conversely, it is well established that human males excel over females across a variety of visual–spatial problem-solving and perceptual tasks (Broverman et al., 1968; Harris, 1978; Joseph, 1993; Kimura, 1993; Linn and Petersen, 1985; Thomas et al., 1973). Visual–spatial superiorities, however, are also demonstrated by other species including male rats (Dawson et al., 1975; Joseph, 1979; Joseph and Gallagher, 1980; Joseph et al., 1978). It is apparent that these same cross-species sex differences have become more pronounced in humans. However, rather than purely a product of societal, political, or parental pressures, the amplification of these sex differences, like other cognitive capabilities such as math, are also neurologically based and a product of our evolutionary heritage. This includes the differential environmental pressures exerted on males and females and their descendants over the course of the last

P1: FLF/FNV

P2: FNN


PL108-310

February 14, 2000

17:12


Evolution of Sex Differences

37

million years, possibly reaching their culmination with the close of the Upper Paleolithic (Joseph, 1993, 2000).

Homo erectus: SEXUALITY AND THE HOME BASE There is no general agreement as to the various phylogentic relationships shared by the wide variety of Plio-Pleistocene hominids so far discovered (Skelton and McHenry, 1992), and it is not yet established if present-day humans descended from Australopithecus, Homo habilis, or both (Grine, 1988; Leakey and Walker, 1988; McHenry and Berger, 1998; Skelton and McHenry, 1992). Nevertheless, following H. habilis and Australopithecus was a wide range of quite different individuals collectively referred to as Homo erectus. Homo erectus were big and robust, with thick brow ridges, large teeth, and bulging shoulder muscles (Day, 1996; Potts, 1996; Rightmire, 1990), and ranged throughout Africa, Europe, Russia, Indonesia, and China from approximately 1.9 million until about 300,000 years ago, with a few isolated populations possibly hanging on in the island of Java, until 27,000 years B.P. (Day, 1996; Potts, 1984, 1996; Rightmire, 1990). Presumably, H. erectus is the common ancestor for Neanderthals and modern humans. About 1.5 million years ago, H. erectus learned to harness fire, and by 500,000 B.P. the first hearths began to appear in China, France, Hungary, and elsewhere (Clark and Harris, 1985; Rightmire, 1990). By 500,000 B.P. H. erectus was regularly constructing crude shelters and home bases (Clark and Harris, 1985; Potts, 1984, 1996; Rightmire, 1990), achievements that may have coincided with a major change in female sexuality. For example, and as is well known, during the transition from hominoid to hominid, the vaginal canal underwent a reorientation which enabled males and females to face one another during sexual intercourse, thus promoting interpersonal intimacy. With the exception of the bonobos, which are more variable, all other primates and nonhuman animals generally assume a dorsal ventral posture when mating (Ford and Beach, 1951; Goodall, 1986, 1990; Wickler, 1973). Based on the evidence reviewed below, this vaginal reorientation may have coincided with alterations in the H. erectus pelvis and the emergence of full-time female sexuality receptivity. That is, with the evolution of H. erectus, the female estrous cycle and the hominoid menstrual cycle, which generally dictates sexually receptivity, may have undergone a transition such that, unlike all other (noncaptive) female species, but like modern-day woman, the H. erectus female became sexually receptive at all times. However, like modern woman (Masters and Johnson, 1966) and many other female mammals and primates such as the chimpanzee (Ford and Beach, 1951; Goodall, 1986, 1990), she likely retained the capacity to enjoy multiple sex partners (and to experience multiple orgasms) one after another.

P1: FLF/FNV

P2: FNN


38

PL108-310

February 14, 2000

17:12


Joseph

It has also been inferred, based in part on the evidence reviewed below, that the breasts and buttocks of the human female may have become permanently enlarged during this evolutionary time period, serving continually to signal her new sexual status and availability. Indeed, these same sexual signals are employed by other species when in estrus. For example, some female primates, such as the gelada baboon, advertise their sexual status via sexual swellings of the chest nodules which flush red (Fedigan, 1992; Jolly, 1985). These nodules form a necklace-like pattern which mimics the pattern of her rump—an enlarged derriere being a common sexual advertisement among many species (see below). Moreover, female rhesus monkeys have been observed to pull and suck on their own nipples when they enter estrus and to display them to potential consorts (Carpenter, 1942), and others, such as the male baboon, will lip smack on the female’s teats, presumably as a sign of affection (Ford and Beach, 1951). In fact, it is not uncommon for the swollen teats of the female primate to serve as a social signal, to decrease aggression or to promote bonding and feelings of security (Eible-Eibesfelt, 1990; Wickler, 1973). However, in these latter instances, the female is usually lactating. In contrast, human females are the only animal on this planet who possess breasts which remain enlarged even when she is incapable of nursing or producing milk or becoming impregnated. In other primates, if the teats swell, turn red, or enlarge, it is only when she is in estrus or lactating. Moreover, the nipples of the human female will grow and stiffen, and the breasts will expand by almost a third when she becomes sexually aroused (Masters and Johnson, 1966), thus signaling her sexual interest. Indeed, human females not uncommonly artificially exaggerate the size of the breasts so as to emphasize her possible sexual availability and to attract male sex partners. In fact, in one recent study, women with breast implants admitted to having on average 14 different male sex partners (versus an average 4 for other women) and to have a greater incidence of terminated pregnancies (Cook et al., 1997). Hence, it can be concluded that over the course of human evolution, the female breast increased in size so as to signal her continual sexual availability. If these great changes in sexual status and the development of secondary sexual attributes occurred during the rein of H. erectus, it likely contributed to the development of long term male–female mating relationships as is suggested by the creation of the home base and semipermanent shelters. For example, among chimpanzees, its not uncommon for a dominant male to threaten and physically force a high-status estrous female to accompany him away from the troop and to establish a home base where he provides her with an inordinate amount of attention; that is, until she ceases to be sexually receptive at which point he loses interest and returns to the troop (Goodall, 1986, 1990). Likewise, when the human female became continually sexually receptive, and continually advertised this fact, this may have motivated some human males to respond in a similar fashion and to form a long-term mating relationship and to establish a personal home base, as is common among modern humans. Although a few other species mate for life,

P1: FLF/FNV

P2: FNN


PL108-310

February 14, 2000

17:12



39

and/or limit their seasonal breeding to one mate, with the exception of gibbons and some New World monkeys, this is not the case with other primates or most mammals, and is true in less than 1% of birds (Kleiman, 1977; Stacey, 1982; Wickler, 1973). Hence, the emergence of full-time sexual receptivity (and associated physical changes) likely contributed to the formation of the home base, long-term mating relationships (or at least serial monogamy), and perhaps even the first “families.” The development of full-time sexual receptivity and accompanying changes in the breasts and buttocks (see below) may also explain why H. erectus (or archaic H. sapiens) began utilizing various earth pigments (ochre), possibly for artistic or cosmetic purposes or to emphasize female sexual availability. In one site, lumps of red ocher, many pointed like pencils, were found, and redness of the female primate genitalia is an obvious signal of sexual receptivity. EVOLUTION OF THE FEMALE PELVIS, BUTTOCKS, AND THE “BIG BRAIN” It was during the latter stages of H. erectus evolution that the brain became significantly enlarged. The brain in fact doubled in size with the transition from Australopithecus (440 cm3 ) to H. erectus (937 cm3 ), approaching within 15% that of present-day humans (Conroy, 1998; Potts, 1996; Rightmire, 1990; Tobias, 1971). However, with the advent of the big brain, human sex differences, including those related to full-time female sexuality receptivity, appear to have become even more pronounced. Because a bigger brain comes in a bigger head, this required a larger birth canal and an increase in the sexual physical differentiation in the size and width of the H. erectus (and modern) female pelvis so as to accommodate the birth of a big brained baby (Day, 1996; Jacob, 1973; Potts, 1996; Rightmire, 1990; Riscutia, 1973). Specifically, with the evolution of a bigger brain and with the transition from Australopithicus to H. habilis to H. erectus, the pelvic opening became longer and more round and ovoid (see Fig. 1) as it expanded from front to back (Day, 1982, Lovejoy, 1988; Sigmon, 1982). As with modern woman, this adaptation likely forced the female erectus’ upper legs wider apart and her knees closer together, thus altering her gait and balance, causing her to wiggle her derriere when walking. Presumably, this alteration, coupled with the evolution of new muscles to aid in the upright stance, accentuated and drew attention to the female derriere and her sexual availability (Joseph, 2000)(see Figs. 2–5): a sexual–social signal accentuated in modern women through high heels and tight clothes, in the last century via the bustle and hoop skirts, and in previous centuries via dresses designed to exaggerate grossly the width of the hips. These same sexual signals are characteristic of other primates (Ford and Beach, 1951; Wickler, 1973). When female chimps and other apes and monkeys

P1: FLF/FNV

P2: FNN


40

PL108-310

February 14, 2000

17:12


Joseph

Fig. 1. The pelvis of an Australopithecus female “Lucy” (bottom) from 3 million years B.P. and the pelvis of a present-day female (top). Note the expanded ovoid inner configuration and enlarged birth canal. (Courtesy of C. Owen Lovejoy.)

P1: FLF/FNV

P2: FNN


PL108-310

February 14, 2000

17:12



41

Fig. 2. An estrous female chimpanzee. (Courtesy of the Royal Society.)

enter estrus, their dorsally oriented genitals/vaginal lips turn pink or a bright crimson, balloon outward, and in fact they become so huge and distended that the animals have difficulty sitting down. Moreover, the estrous chimp or other primate, including baboons and the gorilla, go to great lengths to focus male attention on her buttocks, which she may flaunt and display by swaying them “enticingly” (Fedigan, 1992; Ford and Beach, 1951; Goodall, 1986, 1990; MacKinnon, 1979; Nadler, 1976; Wickler, 1973). She may also approach the male by walking backward, and may sway her swollen derriere in his face, at which point she may run away, only to repeat her performance if he does not respond (Ford and Beach, 1951; Nadler, 1976; Shaller, 1964). Not just female primates but other mammals, including dogs, wolves, porcupines, pigs, and cows, will offer the male a view of her rump, and may even back into him and shove her genitals into his face (Beach, 1965; Ford and Beach, 1951; Wickler, 1973). Hence, the female genitalia and a derriere that is swollen or emphasized are obvious sexual signals which are employed to solicit male sexual attention. Likewise, modern human females accentuate and call attention to the derriere by wearing tight skirts and high heels,

P1: FLF/FNV

P2: FNN


PL108-310

February 14, 2000

42

17:12


Joseph

Fig. 3. An elegant 19th-century female wearing a bustle.

which emphasize the buttocks by puffing it out. When attired in this fashion she is assuming a sexually receptive posture and advertising her sexual availability. The transformation of the human female hips and pelvis, however, also limited her ability to run and maneuver in space, at least, compared to most males (Day, 1996). This is because, be it H. erectus or modern H. sapiens sapiens, “these changes are less pronounced in the . . . male pelvis” (Lovejoy, 1988, p. 123). “The size of the canal in men is controlled mainly by locomotor, not reproductive factors” (Campbell, 1985, p. 152). Moreover, her pelvis became more fragile (e.g., Comas, 1960) and subject to fracture if stressed by continous hard running and jumping. This condition plagues even female soldiers, who suffer an unusually high incidence of pelvic and leg fractures, although their training and duties are not as strenuous or arduous as males’ (1995 U.S. Marines Report, Paris Island). The female pelvis is in fact less massive, lighter, and thus weaker than the male pelvis (Comas, 1960, p. 337). Moreover, as the human femoral neck expanded and became longer so

P1: FLF/FNV

P2: FNN


PL108-310

February 14, 2000

17:12



43

Fig. 4. The daughter of Philip IV of Spain. (Painting by Velazquez.)

Fig. 5. A 19th-century hoop skirt, with cutaway.

as to accommodate these changes in the pelvic girdle, it became more porous and thus weaker (Lovejoy, 1988), as well as subject to stress-related injury, due, in part, to the greater transverse and sagittal diameter of the female pelvic inlet (Comas, 1960, p. 337). As summarized by Day (1996, p. 5), “The female bony pelvis is a compromise between the needs of childbirth and those of locomotion with heavy selection

P1: FLF/FNV

P2: FNN


PL108-310

February 14, 2000

17:12

44


Joseph

pressure on the need for successful reproduction. The male pelvis, with no reproductive function to parallel that of the female, evolved for efficiency in bipedal locomotion.” This helps “explain the differences in peak achievements between men and women in running and jumping.” Hence, be it modern woman or female H. erectus, in accommodating the birth of big-brained babies, these physical changes not only advertised her sexual status, but likely interfered with her ability to endure and keep up with males on their long hunting sojourns—a function also of her reduced upper-body strength and the prolonged dependency of her big-brained babies (Day, 1996; Joseph, 1996a, 2000; Lovejoy, 1981; Murdock and Provost, 1973). As such, with the evolution of H. erectus (and their descendants), males and females became increasingly specialized to perform certain tasks, e.g., hunting versus gathering—a division of labor characteristic of all hunting and gathering groups (Dahlberg, 1981; Hiatt, 1970; Martin and Voorhies, 1975; Murdock and Provost, 1973; Zilman, 1981) including chimpanzees (Goodall, 1990). THE EVOLUTION OF THE DIVISION OF LABOR: HUNTERS AND GATHERERS The Hunting Homo erectus Female primates, including chimps (whose activated DNA is 98.6% identical to human DNA), sate their hunger, and that of their infants, through systematic gathering of foodstuffs and insects, most of which is shared with their young (Goodall, 1990). Although male primates gather, they also hunt and become exceedingly excited when killing not only other animals (Hamburg, 1971; Harding and Strum, 1978), but other primates, including former members of their troop which they may ambush and beat to death (Goodall, 1986, 1990). Be it other animals or a chimp from a neighboring band, the entire troop will gather and excitedly beg for a tiny morsel of the bloody flesh (Goodall, 1986). Be it human, nonhuman primate, or mammal, males tend to be violent (Elia, 1988; Fedigan, 1992; Goodall, 1986, 1990; Hamburg, 1971; Johnson, 1972; Lorenz, 1966; Manning, 1972; Mitchell, 1979; Moyer, 1974), and the male proclivity to hunt appears to be a direct extension of these proclivities (Joseph, 1993). Indeed, over 80% of all violent crimes and murders are committed by human males (Uniformed Crime Reports, 1990–1996). Likewise, male chimpanzees initiate attack five times as frequently as females and are responsible for 90% of all aggressive encounters (Bygott, 1979; Van Lawick-Goodall, 1968). Sex differences in violence and belligerence are apparent as early as the first 2 months of life, even in chimps and other primates (Ransom and Rowell, 1972; Mitchell, 1979). Indeed, the primate/human (male) tendency toward violence may well have been demonstrated millions of years ago by Australopithecus, which

P1: FLF/FNV

P2: FNN


PL108-310

February 14, 2000

17:12



45

hunted not only small animals, but possibly each other. According to Dart (1949), Australopithecines “were confirmed killers; carnivorous creatures that seized others by violence, battered them to death, tore apart their broken bodies, dismembered them limb from limb, and slaking their ravenous thirst with the hot blood of the pitiful victims and greedily devouring their writhing flesh.” Although Dart’s conclusions have been challenged, as noted above, male chimps not uncommonly engage in violent, murderous, and even cannibalistic interactions with other troop members (Goodall, 1986, 1990). Like modern humans, gangs of male chimpanzees will also engage in surprise attacks on neighboring colonies, beating and killing the old, infirm, and young alike, including former friends, and even drinking their blood. That Australopithecus were killers and hunters of meat, thus, should not be surprising. In fact, from an examination of Australopithecine teeth it is apparent that these were meat eaters whose main diet consisted of vegetable matter—as is the case for modern hunting gathering groups (Dahlberg, 1981; Lee and DeVore, 1968; Martin and Voorhies, 1975; Murdock and Provost, 1973; Zilman, 1981) and chimpanzees. Thus sex differences in aggression and trends in the division of labor had probably been established with the evolution of hominoids (as is suggested by modern day chimps) and likely continued to develop with the emergence of Australopithecus. These same trends, however, were likely exaggerated with the evolution of the big brained H. erectus. A bigger, more complex brain confers upon the bearer increased cognitive and intellectual capabilities, and the male H. erectus employed that greater intelligence in the pursuit of bigger game, including deer, bisons, horses, and even bear and elephant (Potts, 1996; Rightmire, 1990). His killing technique, however, remained rather primitive. He either would surround his prey and stone them to death or would use fire to frighten and stampede all manner of animals over cliffs or into swamps, typically killing more animals than could possibly be eaten (Potts, 1996; Rightmire, 1990). Hunting, however, does not require language (Joseph, 1993, 1996a). Rather, successful hunting requires prolonged silence, excellent visual–spatial and gross motor skills, and the capacity to endure long treks in the pursuit of prey. These are abilities at which males excel, including modern H. sapiens sapiens (Joseph, 1988, 1996a). As detailed below, it is not until the emergence of modern (Upper Paleolithic) H. sapiens sapiens that “modern language” evolved. The Maternal H. erectus Just as primate males hunt, whereas most primate females are not so inclined, it is unlikely that the female H. erectus, burdened by pregnancy, crying children, and her fragile pelvis and awkward gait, would have behaved otherwise. Rather, whereas most primate males, including male humans, tend to have little interest in

P1: FLF/FNV

P2: FNN


46

PL108-310

February 14, 2000

17:12


Joseph

infants or caring for the young (Belsky et al., 1984; Clarke-Stewart, 1978; Frodi et al., 1982) it is likely that the female H. erectus, like other female primates, would have pursued her own inclinations including the desire to bear babies and nurture the young. In fact, be it chimpanzee, baboon, rhesus macaque, or human, females demonstrate an extraordinary interest in babies and will engage in playmothering during even the earliest phases of their own childhood (Berman, 1983; Berman and Goodman, 1984; Blakemore, 1981, 1985, 1990; Devore, 1964; Elia, 1988; Fedigan, 1992; Frodi and Lamb, 1978; Goodall, 1971, 1990; Jolly 1972; Kummer, 1971; Melson and Fogel, 1982; Mitchell, 1979; Nash and Fledman, 1981; Strum 1987; Suomi, 1972; Zahn-Waxler et al., 1983). Female humans (Ainsworth and Wittig, 1969; Berman, 1983; Blakemore, 1990) and nonhuman (group-living) female primates will eagerly cuddle, groom, and hold babies that are not their own (Jolly, 1972; Devore, 1964; Kummer, 1971; Strum, 1987; Suomi, 1972; Mitchell, 1979; Goodall, 1971). Although there are exceptions such as the pigtail macaque (Fedigan, 1992; Kaufman, 1974), in general, female humans, apes, or monkeys with babies become the center of female attention (Elia, 1988; Fedigan, 1992; Jolly, 1972; Mitchell, 1979; Strum, 1987). In contrast, human men and boys and nonhuman male primates have little interest in babies or young children and generally provide little or no nurturant care even for their own offspring, though they may form alliances with siblings (Fedigan, 1992; Kummer, 1968, 1971; Mitchell, 1968, 1979, Goodall, 1971; Gordon and Draper, 1982; Rossi, 1985; Rowell et al., 1968), one of the few exceptions being owl monkeys and, to a lesser extent, baboons (Devore, 1977; Fedigan, 1992; Kummer, 1968). Human males and fathers rarely behave in any manner that approximates normal female maternal behavior (Belsky et al., 1984; Clarke-Stewart, 1978; Frodi et al., 1982). As noted, males tend to be aggressive and violent and the desire to nurture infants may not be compatible with these tendencies. Indeed, males are responsible for over 70% of all murders involving infants and children (U.S. Justice Department, 1996–1997). Likewise, among many other primates (gorillas, Barbary apes, and rhesus, howler, and red-tailed monkeys), males stereotypically kill infants not their own (Fedigan, 1992; Hrdy, 1979). THE INFANT–MATERNAL ROOTS OF EMOTIONAL LANGUAGE Considerable vocalizing occurs between mothers and infants (reviewed by Barnett, 1995; Joseph, 1999a). The infants of many species will often sing along or produce sounds in accompaniment to those produced by their mothers (Bayart et al., 1990; Jurgens, 1990; Wiener et al., 1990). These interactions reinforce and promote mutual vocalization, attachment, and contribute to survival. Hence, the first forms of complex social–emotional communication may have been produced in a maternal context (Joseph, 1993, 1996b; MacLean, 1990) and, as in nonhuman animals, were limbic in origin (Joseph, 1992b), a function of sex differences in the Amygomia and Cingulaie gyrus.

P1: FLF/FNV

P2: FNN


PL108-310


February 14, 2000

17:12


47

Because the big-brained infant H. erectus likely required long-term care, it can be assumed that there was an impetus for female H. erectus to vocalize with her young for years at a time. Indeed, a big brain requires more time to grow and mature, which in turn results in prolonged immaturity and helplessness. In consequence, the female tendency to vocalize more than males may have been given additional impetus well over 500,000 years ago. Among most social animals and gathering groups, the production of sound is very important with regard to infant care. If an infant becomes lost, separated, or in danger, this is best conveyed via a cry of distress and fear: cries which would cause a mother to come running to the rescue. Conversely, vocalizations produced by the mother and her cogatherers enable an infant (or a lost gatherer) to orient and find its way back if perchance it gets lost or separated. In this regard, the tendency to vocalize may have ensured breeding success. Among animals, and present-day human mothers, much of this initial mutual sound production is emotional and prosodic (Cooper and Aslin, 1990; Fernald, 1991, 1992; Fernald et al., 1989; Jurgens, 1990) and constitutes what has been referred to as “limbic language” (Joseph, 1982, 1993, 1996b, 1999a). Emotional sound production is mediated by the amygdala, cingulate gyrus, and other limbic and subcortical nuclei but is also hierarchically represented in humans and produced and perceived by the right frontal and right temporal–parietal area (Joseph, 1982, 1988, 1992b, 1993, 1996a,b, 1999a). These emotional–language areas appear to be more extensively developed in human females (see below). In contrast, the denotative and vocabulary-rich grammatical components of modern human speech are mediated by the left frontal and temporal–parietal area, i.e., Broca’s and Wernicke’s speech areas and the inferior parietal lobule. Because infants are emotionally oriented and have little or no understanding of nonemotional speech, these mutual mother–infant vocalizations usually consist of exaggerated emotional prosody (Cooper and Aslin, 1990; Fernald, 1991, 1992, 1993; Fernald et al., 1989; Joseph, 1982, 1996b). Indeed, human infants prefer listening to, and are more responsive to, these exaggerated emotional vocalizations, particularly when produced by a female (Cooper and Aslin, 1990). Moreover, human (and nonhuman) females demonstrate superiorities in this regard, and not only produce more mutual social–emotional vocalizations than males (Brody, 1985; Burton and Levy, 1989; Gilbert, 1969; Glass, 1992; Tannen, 1990) but tend to employ five or six different prosodic variations and utilize the higher registers when conversing (Joseph, 1993). They are also more likely to employ glissando or sliding effects between stressed syllables (Brend, 1975; Coleman, 1971; Edelsky, 1979). Men tend to be more monotone, employing two or three variations on average, most of which hover around the lower registers (Brend, 1975; Coleman, 1971; Edelsky, 1979). Even when trying to emphasize a point, males are less likely to employ melodic extremes but instead tend to speak louder. Although influenced by sex differences in the oral–laryngeal structures, these differential vocalizing abilities are also reflected in the greater capacity of the

P1: FLF/FNV

P2: FNN


48

PL108-310

February 14, 2000

17:12


Joseph

female brain (and right hemisphere) to express and perceive emotional vocalizations (Burton and Levy, 1989; Hall, 1978; Joseph, 1993, 1996b; Soloman and Ali, 1972). This superior sensitivity includes the ability to understand, perceive, and express empathy and social–emotional nuances (Burton and Levy, 1989; Brody, 1985; Buck, 1977, 1984; Buck et al., 1974, 1982; Card et al., 1986; Eisenberg et al., 1989; Fuchs and Thelan, 1988; Harackiewicz, 1982; Kemper, 1978; Lewis, 1983, Rubin, 1983; Safer, 1981; Shennum and Bugental, 1982; Soloman and Ali, 1972; Strayer, 1980) and a greater willingness to express emotional issues and discuss personal problems (Gilbert, 1969; Gilligan, 1982; Lutz, 1980; Walker et al., 1987; Lombardo and Levine, 1981). In fact, from childhood to adulthood, females appear to be much more emotionally expressive than males (Brody, 1985; Burton and Levy, 1989; Gilbert, 1969; Tannen, 1990), who, in contrast, have difficulty discussing personal difficulties or expressing their emotions other than through anger, happiness, and sexual arousal (Balswick, 1982, 1988; Goldberg, 1976; O’Neil, 1982; Joseph, 1993; Sattel, 1989; Tannen, 1990). Like chimpanzees and present-day human females, female H. erectus probably engaged in mutual mother–infant vocalizations and probably engaged in more mutual social–emotional vocalization. However, as based on an analysis of H. erectus’ tool technology, and the fact that it was somewhat crude and lacking in temporal sequential sophistication (though certainly a lot of time was put into their construction), it can be assumed that the brain of H. erectus was not capable of thinking in terms of complex temporal sequences (Joseph, 1996a). Hence, it can be assumed that H. erectus did not speak in the temporal sequential and grammatical manner characteristic of present-day humans. Nor is it likely that H. erectus uttered complex words, though some scientists have argued otherwise (e.g., Wilkins and Wakefield, 1995). Rather, H. erectus probably tended to use gesture, body language, and facial expression, as well as grunts, groans, mimicry, and the production of emotional sounds, in order to convey needs, fears, feelings, and desires. On the other hand, as gathering and the construction of domestic tools were probably an ongoing female H. erectus activity (see below), these activities likely eventually gave rise to improvements in bilateral, temporal, and sequential fine-motor skills, thus providing what would become the neurological foundation for the development of complex grammatical, vocabulary-rich, human language.

TOOLMAKING, TEMPORAL SEQUENCING, AND LANGUAGE Whereas the big-brained male H. erectus refined his hunting techniques and became a hunter of bigger game, females refined their gathering and food preparation techniques as suggested by the creation of crude tools such as choppers, scrapers, cleavers with a stright cutting edge on one side (Day, 1996; Rightmire,

P1: FLF/FNV

P2: FNN


PL108-310


February 14, 2000

17:12


49

1990), and probably digging sticks, as is characteristic of female chimpanzees (Goodall, 1990; McGrew and Marchant, 1992). That these tools were fashioned by a female hand can be deduced by their domestic use. Among hunting and gathering groups, it is females and not males that make and use tools (Niethhammer, 1977), the only exception being hunting implements and weapons of war, which females are not allowed to touch (Tabet, 1982). Similarly, females chimps use food/gathering-related tools much more frequently than males (Goodall, 1986; McGrew and Marchant, 1992), which in turn are more likely to use sticks and rocks to threaten other males (Bygott, 1979; Goodall, 1990; Van Lawick-Goodall, 1968). As with other male primates, and given his penchant for big-game hunting, it was probably the male H. erectus that created the first hand ax, a killing tool which made its appearance about 650,000 years ago (Potts, 1996; Rightmire, 1990). As similar “gathering” versus “hunting” (and, later, more advanced) tools were fashioned throughout Africa, Europe, Asia, and the Middle East until around 10,000 years ago, it can be assumed, with the exception of the European Neanderthals (Joseph, 1996a), that this division of labor prevailed throughout the Middle Paleolithic, well after H. erectus was replaced by archaic H. sapiens. Males continued to hunt and kill (and to invent more efficient killing tools), whereas females cared for the young, maintained the home base, and were responsible for the gathering of food and related “domestic” activities. However, this is not to imply that females never killed small animals, or never collaborated or assisted in the hunt, as that is not the case with humans (Gusinde, 1961; Wantanabe 1964) or chimpanzees (Goodall, 1986). By the close of the Middle Paleolithic (around 30,000 B.P.) and the emergence of “modern” Upper Paleolithic H. sapiens sapiens, such as the Cro-Magnon, hunting had become the center of religious and artistic life. Nevertheless, 60–80% of the Cro-Magon diet consisted of fruits, nuts, grains, honey, roots, and vegetables (Clark, 1952; Prideaux, 1973), which were probably gathered by females. Among the hunting and gathering societies in existence during the last few centuries, women have been and are the gatherers and main providers of food, whereas spoils from the hunt account for only about 35% of the diet (Dahlberg, 1981; Lee and DeVore, 1968; Martin and Voorhies, 1975; Murdock and Provost, 1973; Zilman, 1981). In grubbing for roots and bulbs the Upper Paleolithic female-gatherer probably used a digging stick which she periodically sharpened by using stone flakes. These gatherers also fashioned hammerstones for cracking nuts and grinding the produce she collected. As in recent hunting gathering groups (Lee, 1974; Murdock and Provost, 1973), her duties would include the preparation of any meats she scavenged or which the men brought home from their hunting sojourns. In addition to food preparation, clothes were sewn and fashioned out of hides (Clark, 1952, 1967; Prideaux, 1973), and these, too, are tasks associated with women (Gusinde,

P1: FLF/FNV

P2: FNN


50

PL108-310

February 14, 2000

17:12


Joseph

1961; Lee, 1974; Neithhammer, 1977), including, presumably, the Cro-Magnon females of the Upper Paleolithic. Thus the duties of the Upper Paleolithic female were much more multifaceted and complex than her predecessors’ and included cleaning hides via a scraper, drying and curing the skin over the smoke of a fire, and then using a knife or cutter to make the general desired shape. The Upper Paleolithic female was also employing a punch to make holes in these hides, through which leather straps or a vine could be passed so as to create a garment that could keep out the cold (Clark, 1952, 1967; Prideaux, 1973). They were also weaving and using a needle to sew garments together, “domestic” tasks which are associated almost exclusively with “women’s” work (Murdock and Provost, 1973; Neithhammer, 1977). The necessary skills required for tool construction and the efficient gathering of vegetables, fruits, seeds, and berries and the digging of roots include rapid, temporal sequential fine-motor maneuvers with the arms, hands, and, particularly, the fingers (Hamrick et al., 1998; Marzek, 1997; Susman, 1994). Similarly, most tools are made in a stepwise, temporal sequential manner, with specific fine-motor movements, and considerable precision (Bradshaw and Rogers, 1992; Greenfield, 1992; Hamrick et al., 1998; Marzke, 1997; Susman, 1994; Toth, 1985), abilities which enable the toolmaker to construct the same implement over and over again. This also requires that the toolmaker be in possession of a brain that can control the hand and can use foresight and planning in order to carry out the steps involved in the implement’s manufacture. In this regard, although males were also fashioners of tools (i.e., those used for killing), it is noteworthy that females tend to excel at fine-motor activities, such as those involving rapid, repetitive temporal sequencing (Broverman et al., 1968; Hampson and Kimura, 1992). As detailed elsewhere (Joseph, 1993, 1996a), these “domestic” activities, coupled with her innate tendency to engage in mutual vocalizations, and to vocalize with her young and fellow gatherers, likely coincided with, and stimulated the development of, the temporal sequential neurological foundations of what would become a female superiority in the evolution of grammatical, vocabularyrich human language. However, as the tools made by H. erectus and archaic (Middle Paleolithic) H. sapiens remained relatively crude, whereas a creative explosion in toolmaking technology typifies the onset of the Upper Paeleolithic (Clark, 1952, 1967; Joseph, 1996a; Mellars, 1989; Prideaux, 1973), it appears that the human brain did not become fully adapted for perceiving and expressing temporal sequential, grammatically complex, vocabulary-rich language, until the emergence of the Upper Paleolithic human female. As detailed below, the emergence of these linguistic capabilities was promoted by and thus coincided with advances in tool technology and associated fine-motor skills—activities which gave rise to the functional evolution of Broca’s speech area and the angular gyrus.

P1: FLF/FNV

P2: FNN


PL108-310

February 14, 2000

17:12



51

THE INFERIOR PARIETAL LOBE, APRAXIA, AND TEMPORAL SEQUENCING The angular gyrus of the inferior parietal lobule (IPL) is unique to humans (Geschwind, 1965) and is crucially evolved in controlling temporal sequential hand movements including the manipulation of external objects and internal impressions (De Renzi and Lucchetti, 1988; Heilman et al., 1982; Kimura, 1993; Strub and Geschwind, 1983). As detailed elsewhere (Joseph, 1993, 1996a), the evolution of the angular gyrus enabled humans to engage in complex activities involving a series of related steps, to create and utilize tools, to produce and comprehend complex gestures, such as American Sign Language, and to express and perceive grammatical relationships—capacities which are disrupted with lesions localized to the IPL (Joseph, 1990). In fact, the motor engrams that make possible temporal and sequential motor acts, including those involved in grammatical verbal expression, are localized partly within the IPL (De Renzi and Lucchetti, 1988; Heilman et al., 1982; Kimura, 1993; Strub and Geschwind, 1983). In fact, the IPL not only interacts with but appears to program the frontal motor areas for the purposes of producing fine motor, temporal sequential movements, including the vocalization of speech units. Those devoid of an angular gyrus/IPL, or those who have suffered a severe injury to this area, are generally unable correctly to manipulate or fashion complex tools—much less utilize them in a complex temporal sequence. This condition is referred to as apraxia, i.e., an inability to perform tasks involving interrelated steps and sequences (De Renzi and Lucchetti, 1988; Geschwind, 1965; Joseph, 1990; Heilman et al., 1982; Kimura, 1993). With severe IPL injuries, the individual may be unable to make a cup of coffee or put on clothes, much less fashion or sew them together. Moreover, grammatical speech is disrupted and patients may suffer extreme word finding difficulty, or a conduction aphasia. That is, speech is no longer produced, as Broca’s area is disconnected from the IPL and Wernicke’s area (Geschwind, 1965; Joseph, 1990, 1993). Likewise, reading ability is disrupted, as the IPL comprehends and produces not only gestures but visual symbols including written language. Hence, the IPL/angular gyrus (including the frontal motor areas) makes possible the ability to fashion and manipulate tools and organizes speech into vocabulary-rich, temporal sequential grammatical units. As apes do not possess an angular gyrus (Geschwind, 1965), it appears that over the course of evolution, with the development of right-handedness and selective pressures acting on gene selection across gathering/toolmaking generations, the IPL/angular gyrus emerged as an extension of the auditory area in the temporal lobe and the superior parietal visual–hand area. Indeed, the parietal lobes are considered a “lobe of the hand” and contain neurons which guide hand movements (Hyvarinen, 1982; Kaas, 1993; Lynch, 1980; Mountcastle et al., 1975, 1980) and which respond to visual input from the periphery and lower visual fields—the

P1: FLF/FNV

P2: FNN


PL108-310

February 14, 2000

17:12


52

Joseph

regions in which toolmaking hands are most likely to come into view (Joseph, 1993, 2000). Because most individuals would use the right hand for toolmaking and the left for holding the tool, it is the left parietal lobe (which monitors the right lower visual field and controls the right hand) that guides and visually observes, learns, and memorizes hand movements when gathering, gesturing, or manipulating some object or constructing a tool (Joseph, 2000). Over the course of evolution and as experience and the environment act on gene selection and induce neural plasticity (e.g., Joseph, 1999b, 2000), the parietal (and superior temporal) lobe expanded, the angular gyrus emerged, and neuroplastic alterations were induced in the adjoining motor–hand area in the frontal lobe including what would become Broca’s speech area. THE EVOLUTION OF THE SPEECH AREAS The angular gyrus sits at the junction of the posterior–superior temporal and the occipital–parietal lobes, and is critically involved in naming, word finding, and grammatical speech organization, and is in part an extension of and links Wernicke’s with Broca’s area (Joseph, 1982, 1988, 1990; Geschwind, 1965; Goodglass and Kaplan, 2000; Kimura, 1993). Through its extensive interconnections with the adjacent sensory association areas, the IPL/angular gyrus receives and assimilates complex associations, thereby forming multimodal concepts, and acts to classify and name this material, which is then injected into the stream of language and thought (Joseph, 1982, 1990). The IPL/angular gyrus, in concert with Wernicke’s area, transmits this information to Broca’s speech area, which in turn organizes the immediately adacent oral, laryngeal motor areas (Foerster, 1936; Fox, 1995; Joseph, 1990). However, primates only lack not an angular gyrus, but a functional Broca’s area. Among nonhuman primates, the left frontal lobe, including the tissues homologous to Broca’s area, does not subserve speech or vocalization (Jurgens et al., 1982; Myers, 1976). Rather, vocalization in primates and other nonhuman mammals is the province of the limbic system and brain stem, e.g., the cingulate gyrus, amygdala, hypothalamus, and periaqueductal gray (Joseph, 1992, 1996b; Jurgens, 1990; MacLean, 1990; Robinson, 1967, 1972), and has a nonsegmented organization, consisting of moans, screams, barks, grunts, pants, and pant-hoots (Erwin, 1975; Fedigan, 1992; Goodall, 1986, 1990; Hauser, 1997). Thus, although damage to Broca’s area in humans results in a profound expressive aphasia, similar destruction in nonhuman primates has no effect on vocalization rate, the acoustical structure of primate calls, or social–emotional communication (Jurgens et al., 1982; Myers, 1976). Rather, in primates, “Broca’s area” is directly involved in manual activity (Rizzolatti et al., 1988), and the neural pathways linking the primate IPL with the homologous primate “Broca’s area” are only weakly developed (Abolitiz and Garcia, 1997).

P1: FLF/FNV

P2: FNN


PL108-310


February 14, 2000

17:12


53

Fig. 6. Schematic diagram of the left hemisphere depicting Broca’s Wernicke’s areas, the angular gyrus, Exner’s (Ex) writing area, the frontal eye fields (FEF), and the orbital frontal lobe (OF). Heavy lines indicate arcuate fasciculus pathways. (From Joseph, 1982.)

In contrast, 90% of primate auditory cortex neurons are activated by speciesspecific calls (Newman and Wollberg, 1973), whereas destruction of the left superior temporal lobe disrupts that ability to make sound discriminations (Heffner and Heffner, 1984; Hupfer et al., 1977; Schwarz and Tomlinson, 1990). Moreover, asymmetries in the planum temporal are apparent in chimpanzees (Gannon, 1998), and the primate left hemisphere (Fig. 6) has also been shown to be dominant for the perception of primate vocalizations (Hauser and Anderson, 1994; Peterson and Jusczyk, 1984; Peterson et al., 1978). Presumably, left planum temporal and hemisphere dominance for vocal perception and comprehension gradually increased in the transition from Australopithecus, to H. habilis, to H. erectus, to Neanderthals. As first proposed and detailed elsewhere (Joseph, 1993, 1996a,b), as Wernicke’s area, the parietal–hand areas and the IPL expanded, merged, and collectively gave rise to the angular gyrus, auditory input began to be sequenced, and Wernicke’s area became specialized to perceive and comprehend language units. In addition, the arcuate fasciculus axonal pathways leading from the IPL to Broca’s areas also significantly expanded and increased in density, and Wernicke’s area became tightly linked with and began transmitting auditory–linguistic signals to Broca’s area, thus inducing neurplastic alterations in these tissues (for related discussion see, e.g., Joseph, 1999b– d). Hence, Wernicke’s area began sequencing auditory input, and Broca’s area was transformed from a hand area to a speech area and ceased to control hand

P1: FLF/FNV

P2: FNN


PL108-310

February 14, 2000

17:12


54

Joseph

movements. Instead Broca’s area began to organize the adjacent primary motor oral–laryngeal areas so as to express the words and sentences transmitted from the IPL and Wernicke’s area. Moreover, as the right and left frontal vocalization areas are richly interconnected with the anterior cingulate vocalization centers, whereas the temporal lobe is tightly linked with the amygdala, once these neural–plastic transformations took place, “limbic language” (emotional speech) became hierarchically represented, yoked to the neocortex, and subject to fractionization, temporal sequencing, and multiclassification. Wernicke’s area was now able to communicate with Broca’s area, with the angular gyrus injecting temporal sequences and assimilated associations into the stream of language and thought. Hence, in addition to manipulating tools in a temporal sequential fashion, the evolution of the IPL/angular gyrus enabled humans to manipulate the internal environment and to transmit linguistic impulses to the frontal motor areas controlling the oral– laryngeal musculature, thereby reorganizing Broca’s area in order to vocalize units of speech. However, as based on an analysis of tool technology, it can be concluded that Australopithecus, H. habilis, H. erectus, and Neanderthals did not possess the neurological sophistication for vocalizing complex human language and had not yet evolved an angular gyrus or a functional Broca’s area (Joseph, 1996a). Rather, the evolution of modern speech likely corresponded to the evolution of the Upper Paleolithic female gatherer and toolmaker.

THE FEMALE BRAIN AND THE UPPER PALEOLITHIC The frontal motor area representing the hand is immediately adjacent to and intimately interconnected with the primary motor areas mediating oral, laryngeal, and mandibular movements, including Broca’s area (Fox, 1995; Joseph, 1982, 1988). Hence, manual activity, right-handedness, and expressive speech are directly related (Bradshaw and Rogers, 1992; Corbalis, 1991; Hicks, 1975; Joseph, 1982; Kimura, 1993; Kinsbourne and Cook, 1971), which is why, when speaking, humans commonly gesture with the hands, the right hand in particular. However, it was not until the late Middle Paleolithic that up to 90% of Paleolithic humans may have become right-handed (Cornford, 1986). Similarly, it was not until the Middle to Upper Paleolithic transition, 35,000 years ago, that toolmaking became literally an art and complex multifaceted features were incorporated in their construction and utilization (Chauvet et al., 1996; Joseph, 1993, 1996a; Leroi-Gourhan, 1964, 1982; Mellars, 1989). The Middle/Upper Paleolithic transition is characterized by the creation of complex bone tools, the sewing needle, and personal adornments such as carefully shaped beads of bone, ivory and animal teeth, animal engravings, perforated shells, statuettes, drawings, and paintings of animal and female figures (Chauvet et al., 1996; Clark, 1967; Leroi-Gourhan, 1964, 1982; Mellars, 1989).

P1: FLF/FNV

P2: FNN


PL108-310

February 14, 2000

17:12



55

As the creation and wearing of personal adornments and domestic tool construction and use are associated with the human female, and as toolmaking and gathering often involve both hands (albeit the right more than the left), it might be expected that the human female frontal–parietal areas may have functionally evolved in a manner different from men. That is, both the left and the right half of the female brain may have become organized for producing motor sequences and grammatically complex vocabulary-rich speech. Moreover, as the parietal lobe and IPL/angular gyrus act on and program the frontal motor and speech areas (De Renzi and Lucchetti 1988; Heilman et al., 1982; Kimura, 1993; Strub and Geschwind, 1983), it might be expected that sex differences would be more pronounced in Broca’s and the parietal areas. In fact, Broca’s area appears to be larger in the female. Moreover, the posterior corpus callosum, which interconnects the right and left parietal lobes, appears to be significantly larger in women than men (for evidence pro and con, see Holloway et al., 1993), whereas language appears to be represented in the right half of the female brain to a greater extent than it is represented in the right half of the male brain (Bradshaw et al., 1977; Joseph, 1993; McGlone, 1980; Shaywitz et al., 1995)—a sex difference which may also account not only for her superior language capabilities (due to bilateral representation) but also her relatively inferior visual–spatial abilities (due to functional crowding). Left-hemisphere dominance for verbal functioning and right-hemisphere language (and greater emotional language) representation, coupled with the enhanced ability of the right and left female IPLs to communicate via the corpus callosum, may account for why women (versus men) are less likely than men to become aphasic with a left parietal lesion (Kimura, 1993; Mateer et al., 1982); i.e., women have language-related brain tissues in reserve and are able to continue talking as long as Broca’s expressive speech area is uninjured. SEX DIFFERENCES IN LANGUAGE Over the course of the last 500,000 years, women have been engaging in group and domestic activities including child rearing that promoted the evolution of the neural substrates which subserve the development of human speech. Likewise, human females display clear language, articulation, word knowledge, syntactic, and related linguistic superiorities over males (Bayley, 1968; Broverman et al., 1968; Harris, 1978; Koenigsknecht and Friedman, 1976; Hampson and Kimura, 1992; Harshman et al., 1983; Hyde and Lynn, 1988; Kimura, 1993; Levy and Heller, 1992; Lezak, 1983; McGlone, 1980; McGuiness, 1976; Moore, 1967) and demonstrate bilateral cerebral activation during certain language tasks as demonstrated by functional imaging (Shaywitz et al., 1995). In contrast to males, human females vocalize more, engage in more social speech, display superior linguistic skills, and excel over males on word fluency tests, for example, naming as many words containing a certain letter or words belonging to a certain category. Females also vocalize more as infants, speak their first words, and develop larger vocabularies

P1: FLF/FNV

P2: FNN


PL108-310

February 14, 2000

17:12


56

Joseph

at an earlier age. Their speech as children is easier to understand, they improve their articulation and grammatical skills at a faster rate, and the length and complexity of their sentences are greater than those of males (Bayley, 1968; Harris, 1978; Hyde and Lynn, 1988; Koenigsknecht and Friedman, 1976; Levy and Heller, 1992; Lezak, 1983; McGlone, 1980; McGuiness, 1976; Moore, 1967). Females also speak more rapidly than males. In contrast, males suffer from more language-related disturbances such as stuttering (Corballis and Beale, 1983; Lewis and Hooker, 1983). Moreover, males lose language-related capabilities as they become aged, are more likely to become aphasic following stroke, and do not recover language as quickly or as fully as females (reviewed by Joseph, 1993). In addition, girls learn how to read more quickly and more proficiently than males, who are more likely to suffer from reading difficulties including dyslexia (Corballis and Beale, 1983). Not only do females demonstrate superior reading comprehension and writing and spelling skills (Lewis and Hoover, 1983), but in 1993 the U.S. Department of Education reported that the writing skills of a 9-yearold girl in fourth grade are equal to those of a 13-year-old boy in eighth grade, and in 1997 the U.S.D.E. reported that “at all age levels females continue to outscore males in reading proficiency . . . and females of all ages outscore males in writing.” Reading and writing are directly associated with the functional integrity of the IPL/angular gyrus (Joseph, 1990; Goodglass and Kaplan, 2000).

VISUAL–SPATIAL SKILLS OF THE SILENT HUNTER In contrast to females, language appears to be unilaterally represented in the left half of the male brain (Bradshaw et al., 1977; Joseph, 1993; McGlone, 1980). For example, among males only left-hemisphere lesions result in these language deficits, whereas women are more likely to suffer word finding difficulty and a reduction in vocabulary with right- or left-hemisphere lesions (Kimura and Harshman, 1984). However, because the left half of the male brain is more specialized for language, the right half of the male brain appears to be more lateralized and functionally specialized to analyze (and sequence) visual–spatial relationships (Levy, 1972, 1974; McGee, 1979; McGlone, 1980; Witelson, 1985)—perceptual functions directly related to skill at hunting. Whereas female gatherers are free to talk to one another and their children, hunting does not promote linguistic development, as the successful hunter must be silent and capable of analyzing the spatial coordinates which separate yet link him to a potential prey. These male activities do not promote speech. Wolves and wild dogs spend a considerable part of each morning and evening tracking and hunting, and there is no evidence of speech among these creatures. Speech confers few advantages to a group of human hunters, who must maintain long periods of silence so as to not scare off potential game.

P1: FLF/FNV

P2: FNN


PL108-310


February 14, 2000

17:12


57

Aspects of hunting, however, also put a premium on parietal–temporal lobe and right cerebral cognitive development. Tracking, aiming, throwing, geometric analysis of spatial relationships, and environmental sound analysis are also directly related to the functional integrity of the right half of the brain (Guiard, 1983; Haaland and Harrington, 1990; Joseph, 1988). The right parietal area is associated with the mediation of visual–spatial perceptual functions (Joseph, 1988), especially in males, including providing the sensory feedback which would enable a hunter to aim and throw a spear: guidance which is transferred, via the corpus callosum, to the left-hemisphere somatomotor areas controlling the right upper extremity. Hence, given 500,000 years of multigenerational male experience in hunting, which usually required days or even weeks of wandering hundreds of miles from the home base, present-day males therefore demonstrate superior visual–spatial skills including superior maze learning, tracking, aiming, and related nonverbal abilities, compared to females (Broverman et al., 1968; Dawson et al., 1975; Harris, 1978; Joseph, 1993, 1996a; Kimura, 1993; Levy and Heller, 1992). This includes a male superiority in the recall of geometric shapes, detecting figures that are hidden and embedded within a complex array, constructing three-dimensional figures from two-dimensional patterns, visually rotating and detecting the number of objects in a three-dimensional array, and playing and winning at chess (which requires superior spatial abilities). Males possess a superior geometric awareness and directional sense and geographic knowledge, are better at solving tactual and visual mazes or mentally manipulating spatial relations on paper, and are far superior to females in aiming, throwing, and tracking such as in coordinating one’s movements in relationship to a moving target (Broverman et al., 1968; Harris, 1978; Kimura, 1993; Levy and Heller, 1992; Linn and Petersen, 1985; Porteus, 1965; Thomas et al., 1973). Only about 25% of females in general exceed the average performance of males on tests of such abilities (Harris, 1978). As detailed elsewhere (Joseph, 1988) various aspects of mathematical ability are directly related to visual–spatial functioning, such as geometry and the sequencing of space. However, whereas the female brain has an advantage when it comes to sequencing language, the male brain is more adept at sequencing space. Hence, males are far more likely than females to be mathematical geniuses. Even when the sample consists of females who are scholastically gifted, males achieve higher scores, for example, on the math portion of the college entrance exam and outperform females by a ratio of 13 to 1 (Benbow and Benbow, 1984). Moreover, some of these differences are present during childhood and early adolescence and have been demonstrated in other species (Dawson et al., 1975; Harris, 1978; Linn and Petersen, 1985; Joseph, 1979; Joseph and Gallagher, 1980; Joseph et al., 1978). For example, male rats consistently demonstrate superior visual–spatial and maze learning skills as compared to females (Joseph, 1979; Joseph and Gallagher, 1980; Joseph et al., 1978). If reared in an enriched

P1: FLF/FNV

P2: FNN


PL108-310

February 14, 2000

17:12

58


Joseph

environment, males continue to outperform females, whereas enriched females perform similarly to deprived males, who in turn outperform deprived females (Joseph, 1979; Joseph and Gallagher, 1980). Hence, although the environment can exert profound influences on brain, emotion, and cognitive functioning (Joseph, 1998, 1999b–e), when subject to similar environmental influences, these sex differences are maintained. This also explains why, despite the fact that both sexes have experience with drinking from glass containers, males outperform females when asked to specify the horizontal water level in a tilted glass (Morris, 1971; Thomas et al., 1973). In general, these and related sex differences in cognition and behavior may be reversed only if the developing brain is subject to considerable stress (thus altering steroid secretion), or if deprived of sufficient masculinizing (testicular, steroidal) hormones, and/or if the female brain is exposed to testosterone or other steroids during the critical period of sexual differentiation (Beatty, 1992; Joseph et al., 1978; Meyer-Bahlburg, 1993; Reinisch and Sanders, 1992). For example, female rats exposed to testosterone during early brain development perform similarly to males on maze learning tasks, whereas castrated infant males later perform similarly to females (Joseph et al., 1978). Likewise, homosexual men [whose brains, in some cases, may have been feminized prenatally (e.g., Meyer-Bahlburg, 1993)] tend to perform more poorly than heterosexual men on spatial tasks and similarly to females on verbal tasks (Gladue et al., 1990; however, see Gladue and Baily, 1995). Moreover, human and nonhuman females exposed to high levels of masculinizing hormones and androgens during early brain development demonstrate superior visual–spatial skills and are more competitive and aggressive compared to normal females (Dawson et al., 1975; Money and Ehrhardt, 1972; Ehrhardt and Baker, 1974; Joseph et al., 1978; Reinisch and Sanders, 1992; Mitchell, 1979). As noted, hunting and the killing of prey are related to visual–spatial perceptual functioning and the tendency to behave in an aggressive fashion. CONCLUSION For much of human evolution females have engaged in tasks promoting, requiring, and involving rapid temporal sequential bilateral fine-motor skills such as gathering and domestic-tool construction and manipulation. Given an innate tendency to vocalize more than males, these activities, coupled with prolonged child care and mutual child–mother vocalizations, gave impetus to the evolution of the neocortical speech areas and a female language (and social emotional speech) superiority. In contrast to gathering groups, in which females could vocalize with each other and their young, males instead pursued their own violent tendencies and became silent hunters of big game. Over the course of evolution the male proclivity to travel long distances silently in the pursuit of prey exaggerated an already innate male visual–spatial perceptual superiority.

P1: FLF/FNV

P2: FNN


PL108-310

February 14, 2000

17:12



59

Nevertheless, although hunting does not promote the evolution of speech, males also acquired language skills through maternal genetic inheritance and as he had a mother who would talk to him and teach him language. Thus, like the proverbial Eve, woman, the gatherer, provided man, the hunter, with the fruit of linguistic knowledge and what would become grammatically complex, vocabularyrich speech, language, and linguistic consciousness. ACKNOWLEDGMENTS The author expresses his appreciation for the helpful and expert comments and criticisms of the reviewers. REFERENCES Aboitiz, F., and Garcia V. A. (1997). The evolutionary origin of the language areas of the brain. A neuroanatomical perspective. Brain Res. Rev. 25: 381–396. Ainsworth, M. D. S., and Witig, B. A. (1969). Attachment and Exploratory Behavior of One Year Olds in a Strange Situation, Lawrence Erlbaum, Hillsdale, NJ. Barrett, M. (1996). Early lexical development. In Fletcher, P., and MacWhinney, B. (eds.), The Handbook of Child Language, Blackwell, New York, pp. 363–392. Bayart, F., Hayashi, K. T., Faull, K. F., Barchas, J. D., and Levine, S. (1990). Influence of maternal proximity on behavioral and physiological responses to separation in infant rhesus monkeys (Macaca mulatta). Behav. Neurosci. 104: 98–107. Bayley, N. (1968). Behavioral correlates of mental growth. Am. Psychol. 23: 1–17. Beach, F. (1965). Sex and Behavior, Wiley, New York. Beatty, W. W. (1992). Gonadal hormones and sex differences in nonreproductive behaviors. In Gerall, A. A., Moltz, H., and Ward, I. L. (eds.), Handbook of Behavioral Neurobiology, Vol. 11. Sexual Differentiation, Plenum, New York, pp. 85–128. Belsky, J., Gilstrap, B., and Rovine, M. (1984). The Pennsylvania infant and family development project. I. Child Dev. 55: 692–705. Benbow, C. P., and Benbow, R. M. (1984). Biological correlates of high mathematical reasoning ability. In De Vries, G. J., De Bruin, J. P. C., Uylings, H. B. M., and Corner, M. A. (eds.), Progress in Brain Research, Vol. 61. Sex Differences in the Brain, Elsevier, Amsterdam, pp. 469– 490. Berman, P. (1983). Children’s nurturance to younger children. Soc. Res. Child Dev. 27: 33–67. Berman, P., and Goodman, W. (1984). Age and sex differences in childrens responses to babies. Child Dev. 55: 1071–1077. Blakemore, J. E. O. (1981). Age and sex differences in interactions with a human infant. Child Dev. 52: 386–388. Blakemore, J. E. O. (1985). Interaction with a baby by young adults. Sex Roles 13: 405–411. Blakemore, J. E. O. (1990). Children’s nurturant interactions with their infant siblings. Sex Roles 22: 43–57. Blakemore, J. E. O., Baumgardner, S. R., and Keniston, A. H. (1988). Male and female nurturing. Sex Roles 18: 449–459. Bradshaw, J. L., and Rogers, L. J. (1992). The Evolution of Lateral Asymmetries, Language, Tool Use, and Intellect, Academic Press, San Diego. Brend, R. (1975). Male–female intonation patterns in American English. In Thorne, B., and Henley, N. (eds.), Language and Sex, Newbury House, Boston. Brody, L. (1985). Gender differences in emotional develoment. A review of theories and research. In Steward, A., and Lyko, M. (eds.), Gender and Personality, Duke University Press, Durham, NC. Broverman, D. M., Vogel, W., Klaiber, E. L., Majcher, D., Shead, D., and Paul, V. (1968). Roles of activation and inhibition in sex differences in cognitive abilities. Psychol. Rev. 48: 328–331.

P1: FLF/FNV

P2: FNN


60

PL108-310

February 14, 2000

17:12


Joseph

Buck, R. (1977). Nonverbal communication of affect in preschool children. J. Personal. Soc. Psychol. 35: 225–236. Buck, R. (1984). The Communication of Emotion, Guilford, New York. Buck, R., Miller, R., and Caul, W. (1974). Sex, personality and physiological variables in communication of affect via facial expressions. J. Personal. Soc. Psychol. 30: 587–596. Buck, R., Baron, R., and Barrette, D. (1982). The temporal organization of spontaneous nonverbal expression. J. Personal. Soc. Psychol. 42: 506–517. Burton, L. A., and Levy, J. (1989). Sex differences in the lateralized processing of facial emotion. Brain Cogn. 11: 210–228. Bygott, J. D. (1979). Agonistic behviour, dominance, and social structure in wild chimpanzees. In Hamburg, D. A., and McGown, E. R. (eds.), The Great Apes, Benjamin/Cummings, Menlo Park, CA. Campbell, C. C. (1985). Human Evolution, Aldine, New York. Card, A. L., Jackson, L. A., Stollak, G. E., and Ialongo, N. S. (1986). Gender role and person-perception accuracy. Sex Roles 15: 159–171. Carpenter, C. R. (1942). Sexual behavior of the free ranging rhesus monkey. J. Comp. Psychol. 33: 113–162. Chauvet, J.-M., Deschamps, E. B., and Hillaire, C. (1996). Dawn of Art: The Chauvet Cave, H. N. Abrams, New York. Clark, G. (1967). The Stone Age Hunters, McGraw-Hill, New York. Clark, J. G. D. (1952). Prehistoric Europe: The Economic Basis, Methuen, London. Clark, J. D., and Harris, J. W. K. (1985). Fire and its role in early hominid lifeways. Afr. Archaeol. Rev. 3: 3–27. Clarke-Stewart, K. A. (1978). And daddy makes three. The father’s impact on the mother and young child. Child Dev. 44: 466–478. Clayton, D. E. (1932). A comparative study of the non-nervous elements in the nervous system of invertebrates. J. Entomol. Zool. 24: 3–22. Coleman, R. (1971). Male and female voice quality and its relationship to vowel formant frequencies. J. Speech Hear. Res. 14: 123–133. Comas, J. (1960). Manual of Physical Anthropology, Thomas, Chicago. Conroy, G. C. (1998). Endocranial capacity in an early hominid cranium from Sterkfontein South Africa. Science 280: 1730–1732. Cook, L. S., Darling, J. R., Voigt, L. F., deHart, P. M., Malone, K. E., Stanford, J. L., Weiss, N. S., Brinton, L. A., Gammon, M. D., and Brogan, D. (1997). Characteristics of women with and without breast augmentation. JAMA 277: 1612–1617. Cooper, R. P., and Aslin, R. N. (1990). Preference for infant-directed speech in the first month after birth. Child Dev. 61: 1584–1595. Corballis M. C., and Beale, I. L. (1983). The Ambivalent Mind: The Neuropsychology of Left and Right, Nelson-Hall, Chicago. Corina, D. P., Poizner, H., and Bellugi, U. (1992). Dissociation between linguistic and nonlinguistic gestural systems: A case for compositionality. Brain Lang. 43: 414–447. Cornford, J. M. (1986). Specialized resharpening techniques and evidence of handedness. In Callow, P., and Cornford, J. M. (eds.), Excavations, Geo Books, New York. Cross, H. A., and Harlow, H. F. (1965). Prolonged and progressive effect of partial isolation on the behavior of macaque monkeys. J. Exp. Res. Person. 1: 39–49. Dahlberg, F. (1981). Woman the Gatherer, Yale University Press, New Haven, CT. Dart (1949). The predatory implemental technique of Australopithecus. Am. J. Phys. Anthropol. 7: 1–38. Dawson, J. L. M., Cheung, Y. M., and Lau, R. T. S. (1975). Developmental effects of neonatal sex hormones on spatial and activity skills in the white rat. Biol. Psychiatry 3: 213–229. Day, M. H. (1982). The Homo erectus pelvis: Punctuation or gradualism. Proc. 1st Congr. Int. Paleontol. Hum. 1: 411–421. Day, M. H. (1996). Guide to Fossil Man, University of Chicago Press, Chicago. DeRenzi, E., and Lucchetti, F. (1988). Ideational apraxia. Brain 111: 1173–1185. Devore, I. (1964). Primate behavior. In Tax, S. (ed.), Horizons of Anthropology, Aldine, Chicago. Devore, I. (1977). Male dominance and mating behavior in baboons. In Beach, F. A. (ed.), Sex and Behavior, Wiley, New York.

P1: FLF/FNV

P2: FNN


PL108-310


February 14, 2000

17:12


61

Edelsky, C. (1979). Question intonation and sex role. Lang. Soc. 8: 15–32. Ehrhardt, A. K., and Baker, W. W. (1974). Fetal angrodgens, Human central nervous system differentation and behavior sex differences. In Freidman R. C., Richart, and Vande Wiele (eds.), Sex Differences in Behavior, Wiley, New York. Eisenberg, N., Fabes, R. A., and Miller, P. A. (1989). Relation of sympathy and personal distress to prosocial behavior. J. Person. Soc. Psychol. 57: 55–66. Elia, I. (1988). The Female Animal, Holt, New York. Erwin, J. (1975). Rhesus monkey vocal sounds. In Bourne, G. (ed.), The Rhesus Monkey, Academic Press, New York. Fedigan, L. (1992). Primates and Paradigms: Sex Roles and Social Bonds, Elden Press, Montreal. Fernald, A. (1991). Prosody in speech to children: Prelinguistic and linguistic functions. In Vasta, R. (ed.), Annals of Child Development, Academic Press, San Diego. Fernald, A. (1992). Meaningful melodies in mother’s speech to infants. In Papousek, H., Jurgens, U., and Paplousek, M. (eds.), Origins and Development of Nonverbal Communication: Evolutionary, Comparative, and Metholodogical Aspects, Cambridge University Press, Cambridge. Fernald, A. (1993). Approval and disaproval: Infant responsiveness to vocal affect in familiar and unfamiliar languages. Child Dev. 64: 657–674. Fernald, A., Taescherner, T., Dunn, J., Papousek, M., Boysson-Bardies, B., and Fukui, I. (1989). A cross-language study of prosodic modifications in mothers’ and fathers’ speech to preverbal infants. J. Child Lang. 16: 477–501. Foester, O. (1936). The motor cortex of man in light of Hughlings Jackson’s doctrines. Brain 59: 135–159. Ford, C. S., and Beach, F. A. (1951). Patterns of Sexual Behavior, Harper, New York. Fox, P. T. (1995). Broca’s area. Motor encoding in somatic space. Behav. Brain Sci. 18: 344–345. Frodi, A. M., and Lamb, M. E. (1978). Sex differences in responsiveness to infants. Child Dev. 49: 1182–1188. Frodi, A. M., Lamb, M. E., Hwang, C. P., and Frodi, M. (1982). Father-mother-infant interaction in traditional and nontraditional Swedish families. Altern. Lifestyles 4: 6–13. Fuchs, D., and Thelen, M. H. (1988). Children’s expected interpersonal consequences of communicating their affective state and reported likelihood of expression. Child Dev. 59: 1314–1322. Gannon, P. J. (1998). Asymmetry of chimpanzee planum temporal: Humanlike pattern of Wernicke’s area homolog. Science 279: 348–351. Geschwind, N. (1965). Disconnexion syndromes in animals and man. Brain 88: 585–644. Geschwind, N., and Levitsky, W. (1968). Human brain: Left right asymmetries in temporal speech regions. Science 161: 186–187. Gilbert, D. (1969). The young child’s awareness of affect. Child Dev. 40: 629–640. Gilligan, C. (1982). In a Different Voice, Harvard University Press, Cambridge, MA. Gladue, B. A., and Bailey, M. J. (1995). Spatial ability, handedness, and human sexual orientation. Psychoendocrinology 20: 487–497. Gladue, B. A., Beatty, W., Larson, J., and Staton, D. (1990). Sexual orientation and spatial ability in men and women. Psychobiology 18: 101–108. Glass, L. (1992). He Says, She Says, G. P. Putnam’s Sons, New York. Glees, P., Cole, J., Whitty, C. W. M., and Cairns, H. (1950). The effects of lesions in the cingulate gyrus and adjacent areas in monkeys. J. Neurol. Neurosurg. Psychiat. 13: 178–190. Goldberg, H. (1976). The Hazards of Being Male, Plainville Press, Nashville. Goodall, J. (1971). In the Shadow of Man, Houghton Mifflin, Boston. Goodall, J. (1986). The Chimpanzees of the Gombe: Patterns of Behavior, Cambridge University Press, Cambridge. Goodall, J. (1990). Through a Window, Houghton Mifflin, Boston. Goodglass, H., and Kaplan, E. (2000). Boston Diagnostic Aphasia Examination, Lange, New York. Gordon, T., and Draper, T. W. (1982). Sex bias against male day care workers. Child Care Q. 10: 15–17. Greenfield, P. M. (1992). Language, tools and brain: The ontology and phylogeny of hierarchically organized sequential behavior. Behav. Brain Sci. 14: 531–595. Grine, F. E. (1988). Evolutionary History of the “Robust” Australopithecines, Aldine, New York. Guiard, Y. G. (1983). Left-hand advantage in right-handers for spatial constant error: Preliminary evidence in a unimanual ballistic aimed movement. Neuropsychologia 21: 111–115.

P1: FLF/FNV

P2: FNN


62

PL108-310

February 14, 2000

17:12


Joseph

Gusinde, M. (1961). The Yamana, Human Relations Area Files, New Haven, CT. Haaland, K., and Harrington, D. L. (1990). The role of the right hemisphere in closed loop movements. Brain Cogn. 16: 104–122. Hall, J. (1978). Gender effects in decoding nonverbal cues. Psychol. Rev. 85: 845–857. Hamburg, D. A. (1971). Aggressive behavior of chimpanzees and baboons in natural habitats. J. Psychiatr. Res. 8: 385–398. Hampson, E., and Kimura, D. (1992). Sex differences and hormonal influences on cognitive function in humans. In Becker, J. B., Breedlove, S. M., and Crews, D. (eds.), Behavioral Endocrinology, MIT Press, Cambridge, MA, pp. 357–398. Hamrick, M. W., and Inouye, S. E. (1995). Thumbs, tools and early humans. Science 268: 586–587. Harackiewicz, J. N., and DePaulo, B. M. (1982). Accuracy of person perception. Personal. Soc. Psychol. Bull. 8: 247–256. Harding, R. S. O., and Strum, S. C. (1978). The predatory baboons of Kekopey. Nat. Hist. 85: 46–53. Harris, L. J. (1978). Sex differences in spatial ability. In Kinsbourne, M. (ed.), Asymmetrical Function of the Brain, Cambridge University Press, Cambridge. Harshman, R. A., Hampson, E., and Berenbaum, S. A. (1983). Individual differences in cognitive abilities. Part I: Sex and handedness differences in ability. Can. J. Psychol. 37: 144–192. Hauser, M. D. (1997). The Evolution of Communication, MIT Press, Cambridge, MA. Hauser, M. D., and Anderson, K. (1994). Left hemisphere dominance for processing vocalizations in adult, but not infant rhesus monkeys: First experiments. Proc. Natl. Acad. Sci. USA 91: 3946– 3948. Heffner, H. E., and Heffner, R. S. (1984). Temporal lobe lesions and perception of species-specific vocalizations in macaques. Science 226: 75–76. Heilman, K. M., Rothi, L. J., and Valenstein, E. (1982). Two forms of ideomotor apraxia. Neurology 32: 342–346. Heller, W., and Levy, J. (1981). Perception and expression of emotion in right-handers and left-handers. Neuropsychologia 19: 263–272. Hicks, R. E. (1975). Intrahemispheric response competition between vocal and unimanual performances in normal adult human males. J. Comp. Physiol. Psychol. 89: 50–60. Holloway, R. L., Anderson, P. J., Defendini, R., and Harper, C. (1993). Sexual dimorphism of the human corpus callosum from three independent samples: Relative size of the corpus callosum. Am. J. Phys. Anthropol. 92: 481–498. Hiatt, B. (1970). Woman the gatherer. In Gale, F. (ed), Woman’s Role in Aboriginal Society, Australian Institute of Aboriginal Studies, Canberra. Hrdy, S. B. (1979). Infanticide among animals: A review, classification and examination of the implications for the reproductive strategies of females. Ethol. Sociobiol. 1: 13–40. Hupfer, K., Jurgens, U., and Ploog, D. (1977). The effect of superior temporal lesions on recognition of species-specific calls in the squirrel monkey. Exp. Brain Res. 30: 75–87. Hyde, J. S., and Linn, M. C. (1988). Gender differences in verbal ability: A meta-analysis. Psychol. Bull. 104: 53–69. Hyvarinen, J. (1982). The Parietal Cortex of Monkey and Man, Spinger Verlag, Berlin. Jacob, T. (1973). Morphology and paleocology of early man in Java. In Tuttle, R. H. (ed.), Paleoanthroplogy, Mouton, Paris, pp. 311–326. Johnson, R. N. (1972). Aggression in Man and Animals, W. B. Saunders, Philadelphia. Jolly, A. (1985). The Evolution of Primate Behavior, Macmillan, New York. Joseph, R. (1979). Effects of rearing and sex on maze learning and competitive exploration. J. Psychol. 101: 37–43. Joseph, R. (1982). The neuropsychology of development: Hemispheric laterality, limbic language, and the origin of thought. J. Clin. Psychol. 38: 3–34. Joseph, R. (1985). Competition between women. Psychology 22: 1–11. Joseph, R. (1988). The right cerebral hemisphere: Emotion, music, visual-spatial skills, body image, dreams, and awareness. J. Clin. Psychol. 44: 630–673. Joseph, R. (1990). The left cerebral hemisphere: Aphasia, alexia, agraphia, agnosia, apraxia, schizophrenia, language and thought. In Puente, A. E., and Reynolds C. R. (ser. eds.), Neuropsychology, Neuropsychiatry, Behavioral Neurology, Plenum Press, New York. Joseph, R. (1992a). Speculations on the evolution of mind, woman, man, and brain. In The Right Brain and the Unconscious, Plenum, New York.

P1: FLF/FNV

P2: FNN


PL108-310


February 14, 2000

17:12


63

Joseph, R. (1992b). The limbic system: Emotion, laterality, and unconscious mind. Psychoanal. Rev. 79: 405–456. Joseph, R. (1993). The Naked Neuron: Evolution and the Languages of the Body and Brain, Plenum Press, New York. Joseph, R. (1996a). Paleo-neurology and the evolution of the human mind and brain. In Neuropsychiatry, Neuropsychology, Clinical Neuroscience, Williams & Wilkins, Baltimore. Joseph, R. (1996b). Limbic language, social-emotional intelligence, development and attachment. In Neuropsychiatry, Neuropsychology, Clinical Neuroscience, Williams & Wilkins, Baltimore. Joseph, R. (1998). Traumatic amnesia, repression, and hippocampal injury due to corticosteroid and enkephalin secretion and stress. Child Psychiat. Hum. Dev. 29: 169–186. Joseph, R. (1999a). The limbic language/language axis theory of speech. Behav. Brain Sci. (in press). Joseph, R. (1999b). Environmental influences on neuroplasticity, the limbic system, and emotional development. Child Psychiat. Hum. Dev. 29: 187–200. Joseph, R. (1999c). The neurology of traumatic “dissociative” amnesia. Child Abuse Negl. 23: 715– 727. Joseph, R. (2000). The evolution of human female sexuality. In Clinical Neuroscience, Neuropsychology, Neuropsychiatry, Academic Press, San Diego. Joseph, R., and Gallagher, R. E. (1980). Gender and early environmental influences on activity, overresponsiveness, and exploration. Dev. Psychobiol. 13: 527–544. Joseph, R., Hess, S., and Birecree, E. (1978). Effects of sex hormone manipulations and exploration on sex differences in maze learning. Behav. Biol. 24: 364–377. Jurgens, U. (1990). Vocal communication in primates. In Kesner, R. P., and Olton, D. S. (eds.), Neurobiology of Comparative Cognition, Erlbaum, Hillsdale, NJ. Jurgens, U., Kirzinger, A., and von Cramon, D. (1982). The effects of deep-reaching lesions in the cortical face area on phonation. A combined case report and experimental monkey study. Cortex 18: 125–140. Kaas, J. H. (1993). The functional organization of somatosensory cortex in primates. Ann. Anat. 175: 509–518. Kaufman, C. (1974). Mother and infant relationships in monkeys and humans. In White, N. F. (ed.), Ethology and Psychiatry, Toronto Press, Toronto, p. 51. Kemper, T. (1978). Toward a sociology of emotions. Am. Soci. 13: 30–41. Kimura, D. (1993). Neuromotor Mechanisms in Human Communication, Oxford University Press, New York. Kimura, D., and Harshman, R. A. (1984). Sex differences in brain organization for verbal and nonverbal functions. Prog. Brain Res. 61: 423–441. Kinsbourne, M., and Cook, J. (1971). Generalized and lateralized effect of concurrent verbalization on a unimanual motor skill. Q. J. Exp. Psychol. 23: 341–345. Kleiman, D. G. (1977). Monogamy in mammals. Q. Rev. Biol. 52: 39–69. Koenigsknecht, R. A., and Friedman, R. (1976). Syntax development in boys and girls. Child Dev. 47: 1109–1115. Kummer, H. (1971). Primate Societies, Aldine, Chicago. Leakey, R. E. F., and Walker, A. (1988). New Australopithecus boisea specimens from East and West Lake Turkana, Kenya. Am. J. Phys. Anthropol. 76: 1–24. Lee, R. B. (1974). Male-female residence arrangements and political power in human hunter-gatherers. Arch. Sex. Behav. 3: 167–173. Lee, R. B., and DeVore, I. (1968). Man the Hunter, Aldine, New York. Leroi-Gourhan, A. (1964). Treasure of Prehistoric Art, H. N. Abrams, New York. Leroi-Gourhan, A. (1982). The archaeology of Lascauz Cave. Sci. Am. 24: 104–112. Levy, J. (1972). Lateral specialization of the human brain: Behavioral manifestations and possible evolutionary basis. In Kliger, J. A. (ed.), The Biology of Behavior, Oregon State University Press, Corvallis. Levy, J. (1974). Psychological implications of bilateral asymmetry. In Dimond, S., and Beaumont, J. G. (eds.), Hemisphere Function in the Human Brain, Paul Elek, London, pp. 121–183. Levy, J., and Heller, W. (1992). Gender differences in human neuropsychological function. In Gerall, A. A., Moltz, H., and Ward, I. L. (eds.), Handbook of Behavioral Neurobiology, Vol. 11. Sexual Differentiation, Plenum, New York, pp. 245–274.

P1: FLF/FNV

P2: FNN


64

PL108-310

February 14, 2000

17:12


Joseph

Lewis, H. (1983). Freud and Modern Psychology, Plenum, New York. Lewis, J., and Hoover, H. D. (1983). Sex Differences on Standardized Academic Achievement Tests, American Educational Research Association, Montreal Quebec, Apr. Lezac, M. D. (1983). Neuropsychological Assessment, 2nd ed., Oxford University Press, New York. Linn, M. C., and Petersen, A. C. (1985). Emergence and characterization of sex differences in spatial ability: A meta-analysis. Child Dev. 56: 1479–1498. Locke, J. L. (1996). Development of the capacity for spoken language. In Fletcher, P., and MacWhinney, B. (eds.), The Handbook of Child Language, Blackwell, New York, pp. 278–302. Lombardo, J. P., and Lavine, L. O. (1981). Sex-role stereotyping and patterns of self-disclosure. Sex Roles 7: 403–411. Lorenz, K. (1966). On Aggression, Harcourt, Brace, Jovanovich, New York. Lovejoy, C. O. (1982). The origin of man. Science 211: 341–350. Lovejoy, C. O. (1988). Evolution of human walking. Sci. Am. Nov.: 118–125. Lutz, C. (1980). Emotional Words and Emotional Development, Doctoral dissertation, Harvard University, Cambridge, MA. Lynch, J. C. (1980). The functional oranization of posterior parietal association cortex. Behav. Brain Sci. 3: 485–499. MacKinnon, J. (1979). Reproductive behavior in wild organutans populations. In Hamburg, D. A., and McCowan, E. R. (eds.), The Great Apes, Benjamin/Cummings, Menlo Park, CA, pp. 257– 273. MacLean, P. (1990). The Evolution of the Triune Brain, Plenum, New York. Manning, A. (1972). An Introduction to Animal Behavior, Addison-Wesley, Menlo Park, CA. Martin, M. K., and Voorhies, B. (1975). Female of the Species, Columbia University Press, New York. Marzek, M. W. (1997). Precision grips, hand morphology, and tools. Am. J. Phys. Anthropol. 102: 91–110. Masters, W. H., and Johnson, V. E. (1966). Human Sexual Response, Little Brown, Boston. Mateer, C. A., Polen, S. B., and Ojemann, G. A. (1982). Sexual variation in cortical localization of naming as determined by stimulation mapping. Behav. Brain Sci. 5: 310–311. McGee, M. G. (1979). Human spatial abilities: Psychometric studies and environmental, genetic, hormonal, and neurological influences. Psychol. Bull. 86: 889–918. McGone, J. (1980). Sex differences in human brain asymmetry. Behav. Brain Sci. 3: 215–263. McGrew, W. C. (1995). Thumbs, tools and early humans. Science 268: 586. McGrew, W. C., and Marchant, L. F. (1992). Chimpanzees, tools, and terminates: Hand preference or handedness. Curr. Anthropol. 33: 114–119. McGuiness, D. (1976). Sex differences in the organization of perception and cognition. In Loyd, B., and Archer J. (eds.), Exploring Sex Differences, Academic Press, New York. McHenry, H. M., and Berger, L. R. (1998). Body proportions in Australopithecus aferensis and A. Africana and the origin of the genus Homo. J. Hum. Evol. 35: 1–22. Mellars, P. (1989). Major issues in the emergence of modern humans. Curr. Anthropol. 30: 349–385. Melson, G. F., and Fogel, A. (1982). Young children’s interest in unfamiliar infants. Child Dev. 53: 693–700. Meyer-Bahlburg, H. F. L. (1993). Psychobiological research on homosexuality. Child Adolesc. Psychiat. Clin. North. Am. 2: 489–500. Mitchell, G. (1979). Behavioral Sex Differences in Nonhuman Primates, Van Nostrand, New York. Money, J., and Ehrhard, A. A. (1972). Man and Woman, Boy and Girl, Johns Hopkins University Press, Baltimore. Moore, T. (1967). Language and intelligence. Hum. Dev. 10: 88–106. Mori, A. (1975). Signals found in the grooming interactions of wild Japanese monkeys. Primates 16: 107–140. Mori, U., and Kawai, M. (1975). Social relations and behavior of gelada baboons. In Mori, U., and Kawai, M. (eds.), Contemporary Primatology, Karger, Basel. Morris, B. B. (1971). Effects of angle, sex, and cue on adults’ perception of the horizontal. Percept. Motor Skills 32: 827–830. Morris, D. (1967). The Naked Ape, McGraw-Hill, New York. Mountcastle, V. B., Lynch, J. C., and Georgopoulos, A. (1975). Posterior parietal assocation cortex of the monkey. J. Neurophysiol. 38: 871–908.

P1: FLF/FNV

P2: FNN


PL108-310


February 14, 2000

17:12


65

Mountcastle, V. B., Motter, B. C., and Andersen, R. A. (1980). Some further observations on the functional properties of neurons in the parietal lobe of the waking monkey. Behav. Brain Sci. 3: 520–529. Moyer, K. E. (1974). Sex differences in aggression. In Friedman, R. C., Richart, R. M., and Vande Wiele R. L. (eds.), Sex Differences in Behavior, Wiley, New York. Murdock, G. P., and Provost, C. (1973). Factors in the division of labour by sex: A cross-cultural analysis. Ethnology 12: 203–225. Myers, R. F. (1976). Comparative neurology of vocalization and speech: Proof of a dichotomy. Ann N.Y. Acad. Sci. 280: 755–757. Nader, R. D. (1976). Sexual behaviour of captive lowland gorillas. Arch. Sex. Behav. 5: 487–502. Nash, S. C., and Feldman, S. S. (1981). Sex-role and sex-related attributions. In Lamb, M. E., and Brown, A. L. (eds.), Advances in Developmental Psychology, Erlbaum, Hillsdale, NJ. Neithammer, C. (1977). Daughters of the Earth, Collier, New York. Newman, J. D., and Wollberg, Z. (1973). Multiple coding of species-specific vocalizations in the auditory cortex of squirrel monkey. Brain Res. 54: 287–304. Peterson, M. R., Beecher, M. D., Zoloth, S. B., Moody, D. B., and Stebbins, W. C. (1978). Neural lateralization of species-specific vocalization by Japanese macaques. Science 202: 324–326. Peterson, M. R., and Jusczyk, P. (1984). On perceptual predispostions for human speech and monkey vocalizations. In Marler, P., and Terrace, C. E. (eds.), The Biology of Learning, Springer-Verlag, Berlin, pp. 585–616. Potts, R. (1996). Humanity’s Descent, William Morrow, New York. O’Neil, J. M. (1982). Gender and sex role conflicts in men’s lives. In Soloman, K., and Levy, M. (eds.), Men in Transition, Plenum, New York. Porteus, S. D. (1965). Porteus Maze Test: Fifty Years’ Application, Pacific Books, Palo Alto, CA. Potts, R. (1984). Home bases and early hominids. Am. Sci. 72: 338–347. Prideaux, T. (1973). Cro-Magnon, Time-Life, New York. Ransom, T. W., and Powell, T. E. (1972). Early social development of feral baboons. In Poirer, F. E. (ed.), Primate Socialization, Random House, New York. Reinisch, J. M., and Sanders, S. A. (1992). Prenatal hormonal contributions to sex differences in human cognitive and personality development. In Gerall, A. A., Moltz, H., and Ward, I. L. (eds.), Handbook of Behavioral Neurobiology, Vol. 11. Sexual Differentiation, Plenum, New York, pp. 221– 244. Rightmire, G. P. (1990). The Evolution of Homo Erectus, Cambridge University Press, New York. Riscutia, C. (1973). A study of the Modjokerto infant calvarium. In Tuttle, R. H. (ed.), Paleoanthropology, Mouton, Paris, pp. 373–380. Rizzolatti, C., Camarda, R., Fogassi, L., Gentilucci, M., Luppino, G., and Matelli, M., (1988). Functional organization of inferior area 6 in the macaque monkey. II. Area F5 and the control of distal movements. Exp. Brain Res. 71: 491–507. Robinson, B. W. (1967). Vocalizations evoked from forebrain in Macaca mulatta. Physiol. Behav. 2: 345–352. Robinson, B. W. (1972). Anatomical and physiological contrasts between human and other primate vocalizations. In Washburn, S. L., and Dolhinow, P. (eds.), Perspectives on Human Evolution, Vol. 2, Liss, New York. Rossi, A. (1985). Gender and parenthood. In Rossi, A. (ed.), Gender and the Life Cycle, Aldine, Hawthorne. Rowell, T. E. (1968). The social development of baboons in their first three months. J. Zool. 155: 461–483. Rowell, T. E. (1991). On the significance of the concept of the harem when applied to animals. In Schubert, G., and Masers, R. D. (eds.), Primate Politics, Southern Illinois University Press, Carbondale. Rubin, L. (1983). Intimate Strangers, Harper and Row, New York. Safer, M. (1981). Sex and hemisphere differences in access to codes for processing emotional expression and faces. J. Exp. Psychol. Gen. 110: 86–100. Sattel, J. W. (1989). Men, inexpressiveness and power. In Richardson, L., and Taylor, V. (eds.), Feminist Frontiers II, Random House, New York. Schaller, G. B. (1964). The Year of the Gorilla, University of Chicago Press, Chicago.

P1: FLF/FNV

P2: FNN


66

PL108-310

February 14, 2000

17:12


Joseph

Schwarz, D. W. F., and Tomlinson, R. W. (1990). Spectral response patterns of auditory cortex neurons to harmonic complex tones in alert monkey. J. Neurophysiol. 64: 282–298. Shaywitz, B. A., Shaywitz, S. E., and Pugh, K. R. (1995). Sex differences in the functional organization of the brain for language. Nature 373: 607–609. Shennum, W., and Begental, D. (1982). The development of control over affective expression in nonverbal behavior. In Feldman, R. S. (ed.), Development of Nonverbal Behavior in Children, Springer-Verlag, New York. Skelton, R. R., and McHenry (1992). Evolutionary relationships among early hominids. J. Hum. Evol. 23: 303–349. Sigmon, B. A. (1982). Comparative morphology of the locomotor skeleton of Homo Erectus and other fossil hominids with special reference to the trautavel inominte and femora. Proc. 1st Congr. Int. Paleontol. Hum. 1: 422–446. Soloman, D., and Ali, F. (1972). Age trends in the perception of verbal reinforcement. Dev. Psychol. 7: 238–243. Stacey, P. B. (1982). Female promiscuity and male reproductive success in social birds and mammals. Am. Nat. 51–64. Strayer, J. (1980). A naturalistic study of emphatic behaviors and their relation to affective states and perspective-taking skills in preschool children. Child Dev. 51: 815–822. Strub, R. L., and Geschwind, N. (1983). Localization in Gerstmann syndrome. In Kertesz, A. (ed.), Localization in Neuropsychology, Academic Press, New York. Strum, S. C. (1987). Almost Human, Random House, New York. Suomi, S. J. (1972). Social development of rhesus monkeys reared in an enriched laboratory environment. In Proc. 20th Int. Congr. Psychol., Japanese Science Press, Tokyo. Susman, R. L. (1995). Thumbs, tools and early humans. Science 268: 589. Tabet, P. (1982). Hands, tools, weapons. Femin. Issues 2: 3–63. Tannen, D. (1990). You Just Don’t Understand, Ballantine, New York. Tobias, P. V. (1971). The Brain in Hominid Evolution, Columbia University Press, New York. Toth, N. (1985). Archeological evidence for preferential right-handedness in lower and Middle Pleistocene, and its possible implications. J. Hum. Evol. 14: 607–614. Thomas, H., Jamison, W., and Hummel, D. D. (1973). Observation is insufficient for discovering that the surface of still water is invariantly horizontal. Science 181: 173–174. Uniform Crime Reports (1990–1996). Crime in the United States, U.S. Department of Justice, Federal Bureau of Investigation, Washington, DC. Van Lawick-Goodall, J. (1968). The behavior of free-living chimpanzees in the Gombe Stream Reserve. Anim. Behav. Monogr. Part III. Walker, L. J., de Vries, B., and Trevethan, S. D. (1987). Moral stages and moral orientations in real life and hypothetical dilemmas. Child Dev. 58: 842–858. Watanabe, H. (1964). The Ainu. J. Faculty Sci. 2: 1–87. Wickler, W. (1973). The Sexual Code, Doubleday, Garden City, NY. Wiener, S. G. Bayart, F., Faull, K. F., and Levine, S. (1990). Behavioral and physiological response to maternal separation in squirrel monkeys (Saimiri sciureus). Behav. Neurosci. 104: 108–115. Wilkins, W. K., and Wakefield, J. (1995). Brain evolution and neurolinguistic preconditions. Behav. Brain Sci. 18: 161–226. Witelson, S. F. (1985). Sex and the single hemisphere: Specialization of the right hemisphere for spatial processing. Science 194: 425–427. Woolsey, C. N. (1958). Organization of somatic sensory and motor areas of the cerebral cortex. In Harlow, H. F., and Woolsey, C. N. (eds.), Biological and Biochemical Bases of Behavior, University of Wisconsin Press, Madison. Zahn-Waxler, C., Friedman, S. L., and Cummings, E. M. (1983). Children’s emotions and behaviors in response to infant cries. Child Dev. 54: 1522–1528. Zilman, A. L. (1981). Women as shapers of the human adaptation. In Dalhberg, F. (ed.), Woman the Gatherer, Yale University Press, New Haven, CT.

P1: FOM Archives of Sexual Behavior [asb]

PL108-311

February 14, 2000

12:47



Sexual Partner Age Preferences of Homosexual and Heterosexual Men and Women Zebulon A. Silverthorne, B.A.,1 and Vernon L. Quinsey, Ph.D.1,2

The sexual age preferences of 192 adults (equal groups of heterosexual men, heterosexual women, homosexual men, and homosexual women) were examined. Participants rated the sexual attractiveness of pictures of 15 male and 15 female faces arranged into five apparent average age categories ranging from 18 to 60 years. It was predicted that homosexual and heterosexual men would prefer younger partners of their preferred sex than would homosexual and heterosexual women and that age preference would not vary with participant age. Both predictions were supported, although homosexual women preferred older partners than expected. Results suggest that age and sex preferences develop independently. KEY WORDS: sexual preferences; homosexuality; heterosexuality; gender preferences; attractiveness.

INTRODUCTION Perceptions of physical attractiveness show a remarkable consistency across cultures. Cunningham et al. (1995) examined perceptions of physical attractiveness across cultural groups. Different groups of men showed interrater correlations on female attractiveness ranging between .91 and .94. Exposure to Western media was not responsible for the high level of agreement; American men, rural Chinese men, and rural African men shared high levels of agreement (r = .90) on female attractiveness. Bernstein, Lin, and McCellan (1982) performed the same type of study with female respondents and found similar results. Women from various cultures agreed in their judgments of the physical attractiveness of men (r = .93) independently of culture or Western media exposure. Korthase and Trenholme (1982), and Bradshaw et al. (1994) presented heterosexual men of various ages and cultures with pictures of women arranged into 1 Department of Psychology, Queen’s 2 To whom correspondence should be

University, Kingston, Ontario, Canada K7L 3N6. addressed. 67 C 2000 Plenum Publishing Corporation 0004-0002/00/0200-0067$18.00/0 °


68

PL108-311

February 14, 2000

12:47


Silverthorne and Quinsey

specific age categories. The men, independent of their age or culture, consistently perceived women aged 15–25 years to be most physically attractive. Alley (1993) performed the same study with heterosexual female respondents by presenting women of different cultures and ages with pictures of men categorically arranged by age. Alley found that the women, independent of their age or culture, perceived men aged 30–45 years to be of greatest physical attractiveness. However, Alley noted that heterosexual women’s judgments were more variable than those of heterosexual men. The observed constancy of heterosexual attractiveness judgments and of heterosexual age preference patterns across cultures suggests that evolutionary forces might be responsible for shaping the physical and agerelated characteristics that heterosexual men and women perceive as attractive in members of the opposite sex. Natural selection would have shaped heterosexual age preference, and consequent attractiveness judgments, via the effects that age preferences have on reproductive success (e.g., Quinsey and Lalumière, 1995). Evolution would favor men who favored female sexual partners of an age between maximum reproductive value and maximum fertility (Cunningham et al., 1979). Other things being equal, evolution would likewise favor women who sought out men who possessed the social and material resources required to support children. To the extent that male social status was correlated with age in ancestral environments, it would be expected that women would be selected to prefer somewhat older men (Townsend and Wasserman, 1997). Jankowiak et al. (1992) offer an evolutionary explanation for the greater observed variability in heterosexual female age preferences compared to heterosexual male age preferences. They argue that some of the cues signaling the potential of a male as a reproductive partner are not visible physical characteristics; the male potential in child-rearing rests more in generosity, social position, and wealth than in physical appearance. Heterosexual men depend more on visual cues of a female’s health and youth to signal the reproductive value of a female partner (Quinsey and Lalumière, 1995). Because the cues signaling youth and health are physically similar across cultures, there is very little variance in heterosexual men’s perceptions of physical attractiveness. Although evolutionary psychology has created a theory to explain heterosexual age preference patterns, including the increased variability of heterosexual female judgments, a more complex explanation involving proximal causes appears to be required for the explanation of homosexual sexual age preferences. According to the androgen organizational hypothesis of male homosexuality, the brains of homosexual men are only partially masculinized during critical stages of fetal development (Ellis and Ames, 1987; Ellis et al., 1988). Given that the androgen hypothesis predicts that homosexual men will develop a sexual gender preference similar to heterosexual women, it is surprising that previous research indicates that the sexual behavior and age preferences of homosexual men are more similar to heterosexual men than heterosexual women. Homosexual men report more casual


PL108-311

Sexual Partner Age Preferences

February 14, 2000

12:47


69

sex than heterosexual men, who in turn report more casual sex than heterosexual women (Bailey et al., 1994), indicating that, in certain respects, homosexual male courtship patterns are more similar to those of heterosexual men than heterosexual women. Several past studies have examined the age preference of homosexual men compared to heterosexual men and women. Freund et al. (1973) presented adult heterosexual and homosexual men with pictures of nude men and women of various ages and measured penile tumescence changes. Homosexual and heterosexual men were similar in their arousal to young-adult-age pictures, but opposite in their preferred sex of partner. Bailey and co-workers’ (1994) survey found that homosexual men were identical to heterosexual men in reporting a preference for young sexual partners. Jankowiak et al. (1992) presented groups of homosexual men, heterosexual men, and heterosexual women with visual pictures of men and women aged “university to middle-age.” The researchers found that homosexual men and heterosexual men both perceived the university-aged pictures to be of greatest attractiveness, whereas the heterosexual women perceived the middleaged pictures to be of greatest attractiveness. However, both of these studies found that the homosexual responses showed the increased variability that was more characteristic of heterosexual women than heterosexual men. That homosexual men are similar to heterosexual women in their preference for male sexual partners, yet at the same time similar to heterosexual men in sexual behavior and age preference, strongly suggests sexual preferences are modular (Quinsey and Lalumière, 1995). This modularity means that sexual gender preference, preferred courtship behavior, and age preference, although all components of sexuality, may develop during different stages of fetal growth or be subject to different hormonal influences. The observed modularity of sexual preference could indicate either that sexual behavior and age preference are developed during fetal growth prior to the hormonal failure theorized by the androgen hypothesis or that sexual behavior and age preference are more resistant to lack of in utero androgens than sexual gender preference (Lalumière et al., 1998; Quinsey and Lalumière, 1995). There are, however, limitations to the androgen hypothesis and previous studies of homosexual age preferences. It is unclear whether the androgen hypothesis can account for female homosexuality (Blanchard and Klassen, 1997). Further, there is a paucity of past research that examines homosexual female sexual behavior or age preferences, so it is as yet unclear if lesbian sexuality follows the modular sexuality observed in homosexual men. Studies of homosexual male age preference are also limited but in a different manner. The Freund et al. (1973) study was possibly compromised because the homosexual men used in the study were selected to be sexually attracted to adult, but not teenaged, males. The Bailey et al. (1994) study was limited in that it did not present participants with objective stimuli but simply asked participants to


PL108-311

February 14, 2000

70

12:47



report what age of sexual partner they preferred. Although the Jankowiak et al. (1992) study did present participants with controlled visual stimuli, this study was limited in two ways; the homosexual male participants had a limited age range of “middle-aged professionals” and the stimuli presented to participants were also of a limited age range (“university to middle-aged”). The current study was intended to expand Jankowiak and co-workers’ study by recruiting a wider age range of homosexual male participants and by categorically arranging the stimuli into specific age groups between 15 and 50 years of age. An interesting result of both Jankowiak et al. (1992) and Bailey et al. (1994) was an increased amount of variance in homosexual male responses compared to heterosexual male responses. However, neither group of researchers examined the increased variance to determine if there might have been two types of homosexual male responses (one group preferring young males and another group preferring older males). The final limitation of all three studies is that neither the Jankowiak et al. (1992) study, the Bailey et al. (1994) study, nor the Freund et al. (1973) study examined homosexual female age preference with visual stimuli. The current study was designed to avoid this limitation by concurrently examining homosexual female age preference. The current study systematically examined the age preferences of heterosexual women, heterosexual men, homosexual men, and homosexual women. This study presented participants with pictures of human faces; the stimuli were arranged into five apparent age categories ranging from 18 to 60 years. It was predicted that homosexual and heterosexual men would prefer younger partners of their preferred sex than would homosexual and heterosexual women and that age preference would not vary with participant age. It was expected that heterosexual men, regardless of their age, would find 20- to 25-year-old women to be the most sexually attractive and that heterosexual women would rate 30- to 40-year-old men to be the most sexually attractive. METHOD Participants A total of 192 people participated in this study (equal groups of heterosexual men, heterosexual women, homosexual men, and homosexual women). Homosexual participants were recruited from weekly meetings of a metropolitan Bowling Society. Heterosexual participants were recruited from two coffee shops in Kingston, Ontario. Mean participant age was 33.62 years (SD = 9.07). Heterosexual men averaged 33.14 years of age (SD = 9.91, range 18–52). Heterosexual women averaged 34.43 years of age (SD = 8.55, range 20–50). Homosexual men averaged 33.24 years of age (SD = 9.46, range 18–50). Homosexual women averaged 33.44 years of age (SD = 8.36, range 21–52). Respondents were assigned


PL108-311

February 14, 2000


12:47


71

to one of the four sex-orientation groups on the basis of their stated sexual orientation. No financial inducement was offered to encourage participation. Four people refused to participate (1 homosexual male and 3 homosexual women). Materials The Kinsey Scale (Kinsey et al., 1953) was used to assess sexual orientation. The stimulus set consisted of 30 facial pictures, 15 pictures of female faces, and 15 pictures of male faces. The faces of each sex category were constructed with 3 pictures from 5 apparent age groups; 15 years, 20 years, 30 years, 40 years, and 50 years of age. The stimulus set therefore consisted of 15 male faces (3 from each of the 5 age categories) and 15 female faces (3 from each of the 5 age categories). To ensure that the researchers had assigned particular facial pictures to the correct age category a homosexual man, homosexual woman, heterosexual man, and heterosexual woman were recruited for calculations of interrater agreement. These raters were presented with all of the stimuli used in the current study and asked to write how old, in 5-year intervals, they believed the face to be. The raters were instructed that the pictures varied between 15 and 50 years of age. The four raters showed high agreement in categorizing the faces (the lowest of the six interrater correlations was .95). However, because the categorization of the faces was based upon one researchers’ opinion (Z.A.S.), a further examination of the apparent ages of the stimuli was conducted. Three heterosexual women and three heterosexual men, of average age 39 and 38 years, respectively, independently estimated the age of each face without knowledge of its prior categorization. The average interrater agreement was .93. The average age estimates of the five male face age categories were 18, 23, 32, 44, and 58 years; the average age estimates of the five female face age categories were 19, 25, 28, 42, and 60 years. These average ages were employed in all subsequent analyses. The stimuli were organized into three separate sets, identified as A, B, and C. The study used a double-randomization process. One picture of each sex at each age category was randomly assigned to an order, such that each order consisted of 10 pictures (1 picture of each age and sex). The order of the pictures of within each set was then randomized with the use of a random number table. To prevent order effects, the three stimulus sets were then counterbalanced across participants by use of an all-possible-combinations matrix, creating six possible combinations of the three stimuli sets. Participant assignment to a particular order was determined by order of recruitment within each of the four groups. For example, the first eight homosexual male participants were assigned to order ABC, the second eight participants were assigned to ACB, and so forth. Participants were asked to indicate how sexually attractive a particular face was to them by circling the appropriate number on a 7-point Likert scale; a score of 0 indicated that the participant perceived the face as very sexually unattractive


PL108-311

February 14, 2000

72

12:47



and a score of 7 indicated that the participant perceived the face as very sexually attractive (Quinsey et al., 1993).

Procedure Upon recruitment, all participants completed a standard consent form. The consent form assured complete confidentiality and informed participants that “this research attempts to compare what homosexuals and heterosexuals find attractive in human faces.” Participants were then asked to give their age and sex and to complete the Kinsey scale. Participants were then presented, in the appropriate balanced order, the three stimulus sets. Each picture was presented until the participant responded by circling the appropriate point on the Likert scale, and then the next picture was shown until the set was completed. The participant then moved on to the next stimulus set. Following a completed viewing and response to all three stimulus sets, the participants were given a debriefing form that explained the rationale of the study, the predictions of the study, and a list of related articles. All participants were thanked for their participation.

RESULTS The average ratings are shown in Fig. 1. A factorial ANOVA indicated that sex-orientation groups significantly differed in their responses to male and female facial pictures [F(3,187) = 622.85, p < .001]. In the next ANOVA, the betweensubject factors were Participant Sex and Participant Orientation (heterosexual or homosexual) and the within-subject factors were Stimulus Sex and Stimulus Age. All four of these variables had significant ( p < .001) main effects. Significant interactions indicated that there were different age and sex facial preferences among the four sex-orientation groups and differences in the response to facial pictures of different ages within each of the sex-orientation groups. The third set of analyses performed consisted of a series of eight trend analyses intended to provide an more in depth examination of the age preferences of each of the four sex-orientation groups. The eight sets of data were constructed by decomposing the responses of the four sex-orientation groups into responses to male faces and responses to female faces. The trend analyses of a sex-orientation groups’ nonpreferred group (i.e., heterosexual male responses to male faces) yielded no significant trends, as expected. The trend analyses of sex-orientation groups’ preferred groups did show significant trends. Heterosexual male responses to female faces indicated a quadratic trend [F(1,47) = 201.49, p < .001]; the greatest mean response was to 25-year-old and the lowest to 58-year-old female faces. Heterosexual female responses to male faces showed a quadratic trend [F(1,47) = 119.06, p < .001]; the greatest response


PL108-311

February 14, 2000


12:47


73

Fig. 1. Mean sexual attractiveness ratings as a function of rater sex, rater sexual orientation, and sex of stimulus person.

was to 32-year-old and the lowest to 18-year-old male faces. Homosexual male responses to male faces followed a linear trend [F(1,47) = 117.57, p < .001]; the greatest response was to 18-year-old male faces and the lowest to 58-year-old male faces. Homosexual female responses to female faces also followed a linear trend [F(1,47) = 60.39, p < .001]; the highest responses were to 42- to 60-year-old and the lowest to 19-year-old female faces. The fourth and final set of analyses was designed to determine if participant age may have interacted with stimulus age preference. The only significant correlation between participant age and preferred age category within participants’ preferred sex occurred among male homosexuals (r = .29, p < .05), although all but 9 of the 48 homosexual men preferred the youngest two male age categories. The correlation between participant age and stimulus age preference was of a similar magnitude and approached significance among female heterosexuals (r = .27, p < .06).

DISCUSSION Heterosexual men showed a strong sexual preference for young adult (twentyish) female faces and heterosexual women showed a strong sexual preference for somewhat older (thirtyish) male faces, as expected from past studies of heterosexual


74

PL108-311

February 14, 2000

12:47



age preferences. The prediction that homosexual and heterosexual men would prefer younger partners of their preferred sex than would homosexual and heterosexual women was confirmed. Also as predicted, participants’ age preferences were weakly or unrelated to their own age. Men who preferred male partners preferred younger partners than those who preferred female partners. Women who preferred female partners preferred older partners than those who preferred male partners. Thus, sexual age and gender preferences can develop independently of each other and independently of biological sex, supporting the view that sexual preferences are modular (Quinsey and Lalumière, 1995). The preferred partner age of female homosexuals was considerably older than expected but the use of even older stimuli may have permitted the detection of a quadratic effect. One interpretation of these data is that homosexuality is associated with a downward shift in age preference among men (i.e., compared to heterosexual men) and with an upward shift among women (compared to heterosexual women). One line of future inquiry suggested by the present results is the determination of the relationship of sexual partner age preference and the masculine–feminine (butch-fem) dimension among both homosexual men and women. Based on the findings reported here, more masculine homosexuals of both sexes would be expected to prefer younger same-sex partners than would more feminine homosexuals. It is also possible that more masculine heterosexuals of both sexes would prefer younger-aged opposite-sexed partners than more feminine heterosexuals. Although these self-reported ratings of sexual interest were generally in accord with prediction, they may nevertheless have been affected by subjects’ embarrassment, political conviction, or legal concerns. Phallometric assessment can partially circumvent problems of dissimulation for male subjects (Harris et al., 1999; Freund and Watson, 1991; Freund et al., 1988; Quinsey and Chaplin, 1988) and possibly the use of vaginal pulse amplitude could accomplish the same with female subjects (Laan and Everaerd, 1995; Letourneau and O’Donohue, 1997). On the other hand, covertly measured viewing time offers a simpler and more convenient, if somewhat less accurate, method of more directly measuring sexual preferences and does so using the same metric for men and women (Harris et al., 1996; Quinsey et al., 1996). The difference between male heterosexuals’ ratings of 25-year-old female faces and those of 18 and 28 year olds was in the expected direction but much larger than expected. The size of this difference suggests that the 25-year-old female faces may have been artifactually attractive in that more attractive individuals may have been sampled by chance in the 25-year-old category. Future research could eliminate this possible confounding of age category and attractiveness either by using the same individuals photographed at different ages or by employing large random samples of faces from different age categories. Although age category– attractiveness confounding could affect the shape of the age preference function, it would not be expected to affect the between-preference group differences.


PL108-311

February 14, 2000

12:47



75

ACKNOWLEDGMENTS We thank Yaletown Coffee Co. and Scrubbies Laundry Cafe of Kingston, Ontario, and the Metropolitan Bowling League for allowing access to their members and clients. We thank Tracey Skilling for her help in data analysis, Grant Harris, Martin Lalumière, Marnie Rice, and Tracey Skilling for their comments on an early version of the manuscript, and Bob Konopasky, Center for Psychological Services, Halifax, Nova Scotia, for permission to use some of his stimuli. This research formed part of an undergraduate thesis prepared by the first author under the supervision of the second. Preparation of this paper was facilitated by a research contract from the Kingston Psychiatric Hospital and a Senior Research Fellowship from the Ontario Mental Health Foundation to the second author. REFERENCES Alley, T. R. (1993). The developmental stability of facial attractiveness: New longitudinal data and review. Merrill-Palmer Q. 39: 265–278. Bailey, J. M., Gaulin, S., Agyei, Y., and Gladue, B. (1994). Effects of gender and sexual orientation on evolutionary relevant aspects of human mating psychology. J. Person. Soc. Psychol. 66: 1081– 1093. Bernstein, I. H., Lin, T., and McCellan, P. (1982). Cross-vs. within-racial judgments of attractiveness. Percept. Psychophy. 32: 495–503. Berry, D. (1991). Attractive faces are not all created equal: Joint effects of facial babyishness and attractiveness on social perception. Person. Soc. Psychol. Bull. 17: 523–531. Blanchard, R., and Klassen, P. (1997). H-Y antigen and homosexuality in men. J. Theor. Biol. 187: 373–378. Bradshaw, R. H., Bubier, N. E., and Sullivan, M. (1994). The effects of age and gender on perceived facial attractiveness: A reply to McLellan and McKelvie. Can. J. Behav. Sci. 26: 199–204. Cunningham, M. R., Roberts, A. R., Barbee, A. P., Druen, P. B., and Wu, C. (1995). Their ideas of beauty are, on the whole, the same as ours: Consistency and variability in cross-cultural perception of female attractiveness. J. Pers. Soc. Psychol. 68: 261–279. Eagly, A. H., Ashmore, R. D., Makhijani, M. G., and Longo, L. C. (1991). What is beautiful is good, but . . . : A meta-analytic review of research on the physical attractiveness stereotype. Psychol. Bull. 110: 109–128. Ellis, L., and Ames, M. A. (1987). Neurohormonal functioning and sexual orientation: A theory of homosexuality-heterosexuality. Psychol. Bull. 101: 233–258. Ellis, L., Ames, M. A., Peckham, W., and Burke, D. (1988). Sexual orientation of human offspring may be altered by severe maternal stress during pregnancy. J. Sex Res. 25: 152–157. Freund, K., and Watson, R. J. (1991). Assessment of the sensitivity and specificity of a phallometric test: An update of phallometric diagnosis of pedophilia. Psychol. Assess. J. Consult. Clin. Psychol. 3: 254–260. Freund, K., Langevin, R., Cibiri, S., and Zajac, Y. (1973). Heterosexual aversion in homosexual males. Br. J. Psychiatry 122: 163–169. Freund, K., Watson, R., and Rienzo, D. (1988). Signs of feigning in the phallometric test. Behav. Res. Ther. 26: 105–112. Harris, G. T., Rice, M. E., Quinsey, V. L., and Chaplin, T. C. (1996). Viewing time as a measure of sexual interest among child molesters and normal heterosexual men. Behav. Res. Ther. 34: 389–394. Harris, G. T., Chaplin, T. C., Rice, M. E., and Quinsey, V. L. (1999). Dissimulation in phallometric testing of rapists’ sexual preferences. Arch. Sex. Behav. 28: 223–232.


76

PL108-311

February 14, 2000

12:47



Jankowiak, W., Hill, E., and Donovan, J. (1992). The effect of sex and sexual orientation on attractiveness judgments: An evolutionary interpretation. Ethol. Sociobiol. 13: 73–85. Kinsey, A. C., Pomeroy, W. B., Martin, C. E., and Gebhard, P. H. (1953). Sexual Behavior in the Human Male, Saunders, Philadelphia. Korthase, K. M., and Trenholme, I. (1982). Perceived age and perceived physical attractiveness. Percept. Motor Skills 54: 1251–1258. Laan, E., and Everaerd, W. (1995). Habituation of female sexual arousal to slides and films. Arch. Sex. Behav. 24: 517–541. Lalumière, M. L., Harris, G. T., Quinsey, V. L., and Rice, M. E. ( 1998). Sexual deviance and number of older brothers among sexual offenders. Sex. Abuse 10: 5–15. Letourneau, E. J., and O’Donohue, W. (1997). Classical conditioning of female sexual arousal. Arch. Sex. Behav. 26: 63–78. McKelvie, S. J., and Coley, J. (1993). Effects of crime seriousness and offender facial attractiveness on recommended treatment. Soc. Behav. Pers. 555(21): 265–277. Quinsey, V. L., and Chaplin, T. C. (1988). Preventing faking in phallometric assessments of sexual preference. In Prentky, R. A., and Quinsey, V. L. (eds.), Human Sexual Aggression: Current Perspectives. Ann. N.Y. Acad. Sci. 528: 49–58. Quinsey, V. L., and Lalumière, M. L. (1995). Evolutionary perspectives on sexual offending. Sex. Abuse 7: 301–315. Quinsey, V. L., Rice, M. E., Harris, G. T., and Reid, K. S. (1993). The phylogenetic and ontogenetic development of sexual age preference in males: Conceptual and measurement issues. In Barbaree, H. E., Marshall, W. L., and Hudson, S. M. (eds.), The Juvenile Sex Offender, Guilford, New York, pp. 143–163. Quinsey, V. L., Ketsetzis, M., Earls, C., and Karamanoukian, A. (1996). Viewing time as a measure of sexual interest. Ethol. Sociobiol. 17: 341–354. Symons, D. (1979). The Evolution of Human Sexuality, Oxford University Press, New York. Townsend, J., and Wasserman, M. (1997). The perception of sexual attractiveness: Sex differences in variability. Arch. Sex. Behav. 26: 243–268.


PL108-312

January 28, 2000

9:28



Can Self-Reported Drug Use Data Be Used to Assess Sex Risk Behavior in Adolescents? Joseph S. Wislar, M.S.,1 and Michael Fendrich, Ph.D.1,2

To better understand and control the spread of sexually transmitted diseases among high-risk youth, we must first acquire reliable reports of sexual risk behavior. This study evaluates one potential method for validating such reports. We examined the association between marijuana and cocaine use reporting patterns and the number of reported recent sexual partners in a sample of juvenile arrestees/detainees. Using urinalysis to validate self-reported drug use, we categorized drug use reporting patterns into four groups: overreporters, underreporters, honest users, and honest nonusers. Analyses showed, in general, that overreporters reported more sexual partners than either underreporters or accurate reporters, suggesting that overreporters of drug use may also exaggerate sex partner reports. Findings suggest a new method for validating self-reported sexual behavior and provide a challenge to theories of juvenile delinquency. KEY WORDS: sexual partners; self-disclosure; validity; substance abuse; juveniles; arrestees.

INTRODUCTION Self-reports of sexual behavior (e.g., condom use, number of partners, etc.) are often used to estimate the risk of contracting sexually transmitted diseases, including HIV/AIDS (Catania et al., 1990a). Certain subpopulations are known to provide inaccurate reports (e.g., adolescent males) which weaken epidemiological estimates (see Catania et al., 1990a; Weinhardt et al., 1998). A subgroup of “falsifiers” that overreport sex-related HIV risk (e.g., prostitution, homosexuality) has been identified among addicts seeking treatment (Grella et al., 1995). 1 Department of Psychiatry, Institute for Juvenile Research, University of Illinois at Chicago, Chicago,

Illinois.

2 To whom correspondence should be addressed at Institute for Juvenile Research, University of Illinois

at Chicago, 907 South Wolcott Avenue, m/c 747, Chicago, Illinois 60612. e-mail: [email protected]. Fax: 312-413-1036. 77 C 2000 Plenum Publishing Corporation 0004-0002/00/0200-0077$18.00/0 °


78

PL108-312

January 28, 2000

9:28


Wislar and Fendrich

Since there are no “gold standards” in sex research, it is impossible to validate these estimates, so their accuracy remains uncertain. Without objective measures, self-report validity can be estimated only indirectly (Kirk and Miller, 1986). Studies evaluating reliability shed some light on the quality of sex behavior measures. Previous studies (Catania et al., 1990a,b; Gibson and Young, 1994; Grella et al., 1995) have demonstrated the limitations in the test–retest reliability of sex behavior measures. This form of reliability is sensitive to both the frequency of the behavior and the duration between assessments. Given concerns about the potential for exaggeration in the reporting of sexual behavior, there is a need for research in this area that goes beyond the assessment of reporting reliability. It is difficult to assess directly the exaggeration of sexual behavior without objective measures. While partner verification (see Catania et al., 1990a; Weinhardt et al., 1998) and biological measures (Udry and Morris, 1967) have been previously employed, these methods are expensive and often not feasible (Catania et al., 1990a). Alternative methods of validation may be available. Studies have shown that those who exaggerate one type of high-risk behavior may be prone to exaggerate other high risk behaviors. For example, in a sample of adolescent volunteers, Metzler et al. (1992) found moderate correlation between alcohol, marijuana, and other drug use and a sexual risk-taking scale. Validity assessment, therefore, might focus on potential mechanisms for screening out those prone to the exaggeration, or overreporting, of high-risk behaviors. In particular, researchers might identify one high-risk behavior for which “exaggeration” might be more easily validated; the sexual behavior reports of those classified as exaggerators on the validated measure may then be discounted as invalid or statistically adjusted. More valid prevalence and correlational analyses of high-risk sexual behavior may ensue from such a screening process. Drug use is one type of high-risk behavior for which the tendency to exaggerate can be validated. Studies utilizing drug surveys along with drug tests [e.g., urinalysis, hair assay (see Cone, 1997)] facilitate the classification of respondents into one of four reporting categories: overreporters (test negative but report recent use), underreporters (test positive but deny use), honest users (test positive and report use), and honest nonusers (test negative and deny use). Can drug use reports be used to assess the validity of self-reported sex risk behaviors? More specifically, is the propensity to provide inaccurate information about drug use associated with a similar propensity to inaccurately report sexual behavior? This study examines the association between substance use reporting status and the number of reported sexual partners; specifically, we focused on marijuana and cocaine/crack (referred to only as “cocaine” throughout this paper). Most studies validating sensitive behaviors have assumed that risky behaviors are underreported and, therefore, have focused on underreporting. Similarly, few sexuality research studies have addressed overreporting (Catania et al., 1990a, 1996). This study emphasizes exaggerated reports of sex behavior within a


PL108-312

January 28, 2000

Substance Use and Sex Reporting

9:28


79

high-risk adolescent sample. We hypothesized that drug use overreporters would report more sex partners than either underreporters or honest reporters. METHODS We analyzed 13,048 interviews of juvenile arrestees/detainees collected by the Drug Use Forecasting (DUF) program from 1993 through 1995. The DUF program has been described in detail elsewhere (Chaiken and Chaiken, 1993; Fendrich and Xu, 1994). Briefly, these face-to-face interviews were conducted in holding facilities in select cities3 throughout the United States. Only arrestees/detainees under the age of 18 are included in the juvenile DUF data set. A participation rate of approximately 90% is reported for each year [National Institute of Justice (NIJ), 1996]. Respondents were asked about their arrest history, as well as their lifetime, past 30-day and past 72-hr drug use. A question was also included asking “How many different persons have you had sex with in the past year?” After completion of the interview, respondents were asked to provide a urine specimen for analysis; specimens were analyzed for drug metabolites using the standard EMIT procedure (Visher, 1991). Data Analysis Gender-stratified bivariate crosstabulations were used to evaluate the association between drug use reporting status and sex partner reporting. In addition, we conducted follow-up logistic regression to evaluate these associations controlling for subject age, race/ethnicity, and top arrest charge. Age was grouped into three levels: 12–13, 14–16, and 17–18 years old. Juveniles under the age of 12 (1.7%) or over the age of 18 (0.2%) were excluded from these analyses. Top arrest charge, which has been shown to be associated with drug use reporting (Fendrich and Xu, 1994), was categorized into one of three general types of crime: violent crime (e.g., robbery), drug-related crime (e.g., drug sales), and other miscellaneous crimes (e.g., outstanding warrant). Bivariate crosstabulations and logistic regression analyses were employed to evaluate the relationships between drug use reports and sex partners. Logistic regressions, however, were cluster-adjusted based on the following rationale. Since the surveys were collected in 12 sites, there is the possibility that responses within any particular site might cluster together for any number of reasons (e.g., interviewer style or ability, local norms, homogeneity of subjects, etc.). Therefore, it may be unreasonable to treat responses obtained from juveniles interviewed 3 Juvenile

DUF sites include Birmingham, AL, Cleveland, OH, Denver, CO, Indianapolis, IN, Los Angeles, CA, Phoenix, AZ, Portland, OR, St. Louis, MO, San Antonio, TX, San Diego, CA, San Jose, CA, and Washington, DC.


PL108-312

January 28, 2000

9:28


80

Wislar and Fendrich

within the same site as independent. Failure to account for this potential clustering of observations violates the assumptions upon which conventional parameter variance estimates are derived in regression models. Various strategies for addressing such clustering effects in regression analyses have been proposed (Hedeker and Gibbons, 1994, 1996). In the present analysis, we address potential clustering of observations within site by employing a robust variance estimator through the Stata statistical software (StatCorp, 1997). This procedure is a variant of the procedure outlined by Huber (1967) and White (1980, 1982). Note that the use of this procedure limits the generalizability of the results to repeated samples collected from the same 12 sites in this particular study. RESULTS Table I shows the demographic distribution for the 3 years of arrestee interviews. Boys, African Americans, and middle teens (14–16) comprised the modal demographic categories. Only a small minority of interviewees had been arrested for a drug-related offense. We found extreme variability in sex partner reporting, with one youth reporting as many as 1300 partners over the past year: boys reported a mean of Table I. Demographic Distribution by Gender: 1993–1995 % (n) Boys (n = 11,212) Age 12–13 14–16 17–18 Mean (SD) Race/ethnicity African American Hispanic White/Other Top arrest charge Violent Drug Other Number of sex partners 0 1 2 3 4 or more Refused Mean (SD)

Girls (n = 1836)

Total (N = 13,048)

14.5 (1625) 65.9 (7393) 19.6 (2194) 15.2 (1.5)

21.7 (398) 67.2 (1234) 11.1 (204) 14.7 (1.4)

15.5 (2023) 66.1 (8627) 18.4 (2398) 15.1 (1.5)

45.2 (5019) 28.4 (3150) 26.5 (2940)

31.1 (563) 29.2 (529) 39.7 (718)

43.2 (5582) 28.5 (3679) 28.3 (3658)

28.9 (3229) 10.3 (1156) 60.8 (6798)

18.3 (336) 4.0 (74) 77.7 (1425)

27.4 (3565) 9.4 (1230) 63.2 (8223)

17.3 (1994) 16.4 (1844) 13.6 (1526) 12.4 (1386) 38.8 (4355) 1.4 (157) 5.2 (16.1)

19.9 (365) 29.7 (546) 18.7 (344) 11.5 (211) 19.9 (366) 0.2 (4) 2.8 (12.3)

17.7 (2309) 18.3 (2390) 14.3 (1870) 12.2 (1597) 36.2 (4721) 1.2 (161) 4.8 (15.6)


PL108-312


January 28, 2000

9:28


81

5.2 partners (median = 3.0) and girls reported a mean of 2.8 partners (median = 2.0). These reporting trends suggest considerably higher numbers of reported partners in this sample than in other samples of youth in a comparable age range (Lowry et al., 1994; Seidman and Rieder, 1994). We collapsed four or more partners into one level for comparability with the National Youth Risk Behavior Survey (Lowry et al., 1994). The distribution of reported sex partners among the different marijuana reporting strategies is presented in Table IIa. Boys tended to report multiple partners regardless of their marijuana reporting status. Over half of the overreporters and honest users reported four or more recent sex partners, while honest nonusers reported fewer partners ( p < .001). A different pattern emerged for girls. As with the boys, a greater proportion of female overreporters disclosed more recent partners, but more than half of the underreporters and honest nonusers reported one or no recent partners ( p < .001). Table IIb shows the distribution of reported sex partners within each cocaine reporting strategy. As was observed with marijuana, boys tended to report numerous partners regardless of their cocaine reporting strategy. Overreporters, however, were significantly more likely to report four or more partners than those classified into any other drug reporting category ( p < .001). A parallel pattern was found for girls; overreporters reported more sex partners than underreporters and honest nonusers, although there was little difference between overreporters and honest users. Since our underlying question was about extreme reporting, we further reduced the sex partners variable into two levels: three or fewer versus four or more partners. Stratified logistic regression models were fitted using drug use reporting status to predict four or more reported sex partners, adjusting for age, race/ethnicity, and top arrest charge. Previous research has suggested that interviewer gender may influence reports of sex behavior (Catania et al., 1996; Schopper et al., 1993), but it did not contribute meaningfully in our analyses (analyses not shown). Table III shows the stratified, cluster-adjusted regression models. In the marijuana model, overreporters of both genders had significantly increased odds of reporting four or more partners relative to either underreporters or honest nonusers. Male overreporters had 1.6 times the odds of reporting high numbers of partners relative to underreporters (1.61; 95% CI, 1.35–1.93) and more than twice the odds relative to honest nonusers (2.15; 95% CI, 1.95–2.37). Female overreporters had nearly six times the odds of reporting extreme numbers of sex partners relative to underreporters (5.70; 95% CI, 2.84–11.46) and more than twice the odds relative to honest nonusers (2.12; 95% CI, 1.58–2.84). There were no significant differences between overreporters and honest users for either gender. In general, cocaine overreporters had significantly increased odds of reporting high numbers of sex partners relative to all other reporting categories. Male overreporters had nearly three times the odds of reporting extreme numbers of

20.1 (54) 23.6 (25) 18.3 (32) 18.2 (233) 18.8 (344)

14.2 (38) 12.3 (13) 16.0 (28) 10.3 (132) 11.5 (211)

11.5 (148) 14.1 (211) 15.4 (349) 11.3 (678) 12.5 (1386)

3

31.3 (84) 7.5 (8) 26.3 (46) 17.8 (228) 20.0 (366)

50.5 (648) 41.8 (624) 50.9 (1155) 32.1 (1928) 39.4 (4355)

4 or more

14.6 (268) 5.8 (106) 9.6 (175) 70.0 (1283) 100.0 (1832)

11.6 (1282) 13.5 (1494) 20.5 (2268) 54.4 (6011) 100.0 (11,055)

Total

9:28

2 2 χdf=12 = 624.38, p < .001. Girls: χdf=12 = 73.18, p < .001.

23.5 (63) 40.6 (43) 27.4 (48) 30.6 (392) 29.8 (546)

10.8 (29) 16.0 (17) 12.0 (21) 23.2 (298) 19.9 (365)

12.7 (163) 15.9 (237) 13.1 (296) 13.8 (830) 13.8 (1526)

2

Reported sex partners [% (n)]

January 28, 2000

a Boys:

13.9 (178) 17.0 (254) 13.4 (303) 18.4 (1109) 16.7 (1844)

1

11.3 (145) 11.2 (168) 7.3 (165) 24.4 (1466) 17.6 (1944)

None

PL108-312

Boys Overreport Underreport Honest user Honest nonuser Total Girls Overreport Underreport Honest user Honest nonuser Total

Reporting strategy


Table IIa. Distribution of Reported Sex Partners Among Marijuana Reporting Strategies: DUF, 1993–1995a

P1: FPN Style file version Nov. 19th, 1999

82 Wislar and Fendrich

25.0 (6) 21.6 (11) 20.0 (7) 18.6 (320) 18.8 (344)

4.2 (1) 17.6 (9) 20.0 (7) 11.3 (194) 11.5 (211)

15.5 (20) 12.5 (85) 20.7 (37) 12.4 (1244) 12.5 (1386)

3

45.8 (11) 19.6 (10) 42.9 (15) 19.2 (330) 20.0 (366)

58.1 (75) 49.6 (337) 41.3 (74) 38.4 (3869) 39.4 (4355)

4 or more

1.3 (24) 2.8 (51) 1.9 (35) 94.0 (1722) 100.0 (1832)

1.2 (129) 6.1 (679) 1.6 (179) 91.1 (10,068) 100.0 (11,055)

Total

9:28

2 = 98.18, p < .001. Girls: χdf=12 = 36.91; 25% of cells had an expected count of less than 5, therefore the chi-square test is not valid for girls.

16.7 (4) 29.4 (15) 14.3 (5) 30.3 (522) 29.8 (546)

8.3 (2) 11.8 (6) 2.9 (1) 20.7 (356) 19.9 (365)

10.1 (13) 13.4 (91) 11.2 (20) 13.9 (1402) 13.8 (1526)

2

January 28, 2000

a Boys: χ 2 df=12

10.9 (14) 14.3 (97) 19.6 (35) 16.9 (1698) 16.7 (1844)

1

5.4 (7) 10.2 (69) 7.3 (13) 18.4 (1855) 17.6 (1944)

None

PL108-312

Boys Overreport Underreport Honest user Honest nonuser Total Girls Overreport Underreport Honest user Honest nonuser Total

Reporting strategy

Reported sex partners [% (n)]


Table IIb. Distribution of Reported Sex Partners Among Cocaine/Crack Reporting Strategies: DUF, 1993–1995a


Substance Use and Sex Reporting 83

1.90–2.97 0.82–1.28 —

2.38 1.03 1.00 0.99 1.04 1.00 0.62 0.97 0.47 1.00

Top arrest charge Violent offense Drug offense Other offense

Drug use report Underreport Honest user Honest nonuser Overreport

0.45 0.46 0.35 1.00

0.31–0.64 0.30–0.70 0.27–0.45 —

0.27 0.80 0.27 1.00

0.93 1.27 1.00

0.87 0.63 1.00

0.81 1.08 1.00

OR

0.06–1.28 0.25–2.58 0.12–0.60 —

0.66–1.33 0.79–2.04 —

0.50–1.52 0.42–0.93 —

0.49–1.34 0.87–1.34 —

95% CI

a Hosmer

2 2 = 6.0, df = 7 ( p =.54); cocaine—χ 2 and Lemeshow goodness of fit: Marijuana—χboys = 6.3, df = 8 ( p = .62), and χgirls boys = 2 = 9.5, df = 7 ( p = .22). 12.7, df = 8 ( p = .12), and χgirls

0.09–0.35 0.56–1.08 0.35–0.63 —

0.84–1.13 0.97–1.33 —

1.96–2.99 0.84–1.13 —

0.27–0.40 0.77–0.92 —

95% CI

Girls (n = 1832)

84

0.18 0.77 0.47 1.00

0.97 1.14 1.00

2.42 1.07 1.00

0.33 0.84 1.00

OR

Cocaine

9:28

0.52–0.74 0.80–1.16 0.42–0.51 —

0.68–1.31 0.74–1.95 —

0.47–1.47 0.41–0.89 —

0.46–1.37 0.81–1.36 —

95% CI

Boys (n = 11,055)

January 28, 2000

0.94 1.20 1.00

0.83 0.61 1.00

0.79 1.05 1.00

OR

Girls (n = 1832)

PL108-312

0.86–1.14 0.87–1.25 —

0.28–0.42 0.77–0.92 —

95% CI

0.34 0.84 1.00

OR

Age 12–13 14–16 17–18 Race/ethnicity African American Hispanic White/Other

Variable

Marijuana


Boys (n = 11,055)

Table III. Cluster-Adjusted Logistic Regression Model Predicting Four or More Sexual Partners in the Past Year Stratified by Gender a


Wislar and Fendrich


PL108-312

January 28, 2000


9:28


85

partners relative to honest nonusers (OR = 2.84; 95% CI, 2.20–3.65), and more than twice the odds relative to honest users (OR = 2.20; 95% CI, 1.43–3.37), or underreporters (OR = 2.24; 95% CI, 1.57–3.19). A similar association was observed for girls, with one exception. Consistent with the bivariate analysis [Table IIb], there was no statistically significant difference between overreporters and honest users or underreporters in the regression analysis. Like males, however, female overreporters were significantly more likely to report large numbers of sex partners relative to honest nonusers (OR = 3.70; 95% CI, 1.68–8.18). DISCUSSION In general, our results indicate that drug use overreporters disclose more sex partners. Specifically, these findings suggest that male cocaine overreporters may exaggerate their number of sex partners. Our hypothesis was not so clearly supported in the marijuana model for boys, or in either model for girls. While females who overreported marijuana use reported more partners than either underreporters or honest nonusers, they were not statistically different from honest users. This pattern held for the male marijuana model as well. Since the reporting of cocaine use is a rare event for girls, caution needs to be used when interpreting these results. Catania et al. (1990a) have noted that it is usually assumed that bias in sex research occurs in a downward direction (i.e., underreporting) but that this may not be the case in cultures that value sexual prowess. We observed high numbers of reported partners among male, relative to female, arrestees/detainees, which may be suggestive of sexual bragging. Given the unusually high number of partners reported in this sample, it may be that at-risk youth, particularly males, view surveys as an opportunity to demonstrate their sexual potency and therefore exaggerate their behavior. It is possible that the distribution of sex partner reports in this sample is reflective of actual behavior. This, however, would not explain the differences we found between those utilizing different drug use reporting strategies. More research is needed to understand the large number of sexual partners reported in this sample. For this study, we used four or more partners to demarcate extreme numbers of partners as have other studies (Lowry et al., 1994). Given the range observed, we considered the possibility that this cutoff was too low. We reanalyzed the boys’ models with six or more partners indicating extreme reporting. Results did not change significantly after making this adjustment, thus supporting the use of our original four-partner cutoff. We found an association between extreme sex partner reporting and cocaine overreporting but not for marijuana overreporting. This lack of association may be explained by the difference in the relative societal acceptance of the two


86

PL108-312

January 28, 2000

9:28


Wislar and Fendrich

drugs.4 Since marijuana is less stigmatized, perhaps even normative among youths (Measham et al., 1998), it may be more accurately reported. Cocaine, on the other hand, is accompanied by harsher legal and social consequences. Respondents who are willing to overreport one stigmatized behavior (cocaine use) may be more willing to report other stigmatized or risky behaviors (multiple sex partners). Likewise, respondents who underreported the less stigmatized drug (marijuana) also tended to report fewer sex partners. This may be indicative of a general tendency among a subset of youth to avoid disclosing any risky behavior regardless of its relative societal acceptance. Respondents honestly reporting recent cocaine use in a criminal justice setting, however, may be reflective of some motivation to accurately report other sensitive behaviors. We hypothesized that the tendency toward “overreporting” or the exaggeration of risky behaviors is a trait that may manifest itself in a variety of survey responses. This is exemplified further in our data set by associations between overreporting and polysubstance use. We examined the association between drug use reporting strategies and another risk behavior, polysubstance use. For both males and females, overreporters of both drugs reported significantly more substances than those in other reporting categories.5 After excluding marijuana from the count, male marijuana overreporters reported more than twice as many substances as male underreporters and honest users (1.19 vs. 0.71; p < .001), while female overreporters reported nearly twice as many other drugs (1.51 vs. 0.74; p < .001) as other females. Likewise, male cocaine overreporters reported more than twice as many other substances not including cocaine or crack (2.96 vs. 1.19; p < .001); female cocaine overreporters reported the use of nearly three times as many substances as other respondents (3.25 vs. 1.19; p < .001). Given the implications of this trait for sex research, further validation is needed; studies are needed to develop psychometrically valid scales assessing exaggeration tendencies. Given that our study is based on face-to-face interviews from a criminal justice sample, we need to address the generalizability of our findings. In general, studies examining mode effects in sex behavior surveys have found that respondents in face-to-face interviews (the mode used in this study) are more prone to underreporting sexual behavior than when more private modes are utilized (Boekeloo et al., 1994; Romer et al., 1997; Turner et al., 1998; Weinhardt et al., 1998). There is, however, inconsistent evidence for mode effects in drug use surveys (Aquilino and LoSciuto, 1990; Johnson et al., 1999). Thus, it is not clear whether data collection under more private modes would affect the pattern of association we observed. 4 Support for the social acceptability of marijuana is apparent by (1) higher prevalence rates of marijuana

than cocaine (Johnston et al., 1998), (2) generally less severe penalties for marijuana possession, and (3) recent support in many states for legalizing the medical use of marijuana. 5 Substances included alcohol, amphetamines, barbiturates, black tar heroin, cocaine, crack, crystal methamphetamine, Darvon, designer drugs, Dilaudid, heroin, “ice,” inhalants, LSD, mushrooms, PCP, Quaalude, street methadone, and Valium.


PL108-312


January 28, 2000

9:28


87

Since the youth in this study were all involved in the criminal justice system, it is not clear that the pattern of results reported here would be found in a general population study of this age group. On the other hand, these participants represent youth that engage in multiple risky behaviors and who may need immediate intervention. Effective targeting of interventions relies on accurate information derived from self-reports. This study helps build critical understanding of the validity of survey reports from at-risk samples. One potential limitation of this study is that urine screening is not perfectly accurate. The EMIT procedure, like all other biological measures, has false negatives and positives; the proportion of each depends largely on the sensitivity and specificity cutoff levels defined for the test. There is the possibility that some of those classified as overreporters were actually false negatives; that is, even though a respondent was screened negative, he/she may have ingested the drug (Visher, 1991). False negatives in the EMIT procedure occur when subthreshold levels of the drug or its metabolites are present in the specimen (Visher, 1991). This would mean that the respondent had either (a) used the drug, but not in the past 3 days, (b) ingested a very low dose, or (c) consumed large quantities of liquid before providing a sample (Christine Moore, Toxicologist, U.S. Drug Testing Laboratory, July 16, 1998, personal communication). For our purposes, a participant who had not used within the past 3 days, but reported use, would still be considered an overreporter. Respondents who had tried to flush their system with liquids would be unlikely to report use in the first place and, therefore, would not affect this study. The greatest concern is for respondents who had consumed low doses of the drug. We have no reason to expect that low-dose users are more likely to report their drug use than high-dose users. Thus, we believe that it is unlikely that our results are a consequence of the inaccuracy of the EMIT urine screen. Future studies should examine issues of false negatives more closely than we were able to with these data. False results become much less of a concern when confirmation procedures, such as GC/MS (gas chromatography/mass spectrometry), are used. The DUF program confirms specimens only for the presence of amphetamine (NIJ, 1996). Sensitivity can also be improved by lowering the cutoff level for detection; during the years included in these analyses, DUF used standard NIDA cutoff levels (NIJ, 1996).6 DUF began testing some urine specimens for marijuana with both the standard (100 ng/ml) and a lower (50 ng/ml) cutoff in 1994. Our results did not change when we analyzed these data using the lower marijuana cutoff level (analyses not shown). Finally, our findings not only suggest a potentially useful method for validating adolescent reports of sexual behavior, but also present a challenge to theories of adolescent behavior. Problem Behavior Theory (Jessor and Jessor, 1977) maintains that “problem” behaviors, like drug use and risky sex, tend to covary. Our results 6 Until

1996, DUF used the 100-ng/ml cutoff level for marijuana; SAMHSA now recommends a 50-ng/ml level.


PL108-312

January 28, 2000

9:28

88


Wislar and Fendrich

suggest that it may be that these behaviors do not occur together but, instead, are simply reported together. While it is probably true that problem behaviors often occur together, we hypothesize that for a subset of adolescents prone to exaggeration, problem behaviors may be indiscriminately exaggerated. We suggest that additional research needs to be carried out to identify the prevalence of this tendency and its implications for problem behavior theory. ACKNOWLEDGMENTS This research was supported by National Institute on Drug Abuse Grant DAO9286-02. An earlier version of this paper was presented at the Annual Meeting of the American Public Health Association, Indianapolis, IN, on November 12, 1997. The authors thank Julia Y. Kim, M.A., and Timothy P. Johnson, Ph.D., for their review of the manuscript and for their helpful comments. REFERENCES Aquilino, W. S., and LoSciuto, L. (1990). Effects of interview mode on self-reported drug use. Publ. Opin. Q. 54: 362–395. Boekeloo, B. O., Schiavo, L., Rabin, D. L., Conlon, R. T., Jordan, C. S., and Mundt, D. J. (1994). Selfreports of HIV risk factors by patients at a sexually transmitted disease clinic: Audio vs written questionnaires. Am. J. Public Health 84(5): 754–760. Catania, J. A., Gibson, D. R., Chitwood, D. D., and Coates, T. J. (1990a). Methodological problems in AIDS behavioral research: Influences on measurement error and participation bias in studies of sexual behavior. Psychol. Bull. 108: 339–62. Catania, J. A., Binson, D., Canchola, J., Pollack, L. M., Hauck, W., and Coates, T. J. (1996). Effects of interviewer gender, interviewer choice, and item wording on responses to questions concerning sexual behavior. Publ. Opin. Q. 60: 345–375. Catania, J. A., Gibson, D. R., Marin, B., Coates, T. J., and Greenblatt, R. M. (1990b). Response bias in assessing sexual behaviors relevant to HIV transmission. Eval. Prog. Plan. 13: 19–29. Chaiken, J. M., and Chaiken, M. R. (1993). Understanding the Drug Use Forecasting (DUF) Sample of Adult Arrestees, National Institute of Justice, Lincoln, MA. Fendrich, M., and Xu, Y. (1994). The validity of drug use reports from juvenile arrestees. Int. J. Addict. 29: 971–985. Gibson, D. R., and Young, M. (1994). Assessing the reliability and validity of self-reported risk behavior. In Battjes, R. J., Sloboda, Z., and Grace, W. C. (eds.), The Context of HIV Risk Among Drug Users and Their Sexual Partners, National Institute on Drug Abuse Research Monograph 143, NIH Publ. No. 94-3750, National Institute on Drug Abuse, Rockville, MD. Grella, C. E., Chaiken, S., and Anglin, M. D. (1995). A procedure for assessing the validity of selfreport data on high-risk sex behaviors from heroin addicts entering free methadone treatment. J. Drug Issues 25(4): 723–733. Hedeker, D., and Gibbons, R. (1994). A random-effects ordinal regression model for multilevel analysis. Biometrics 50: 933–944. Hedeker, D., and Gibbons, R. (1996). MIXOR: A computer program for mixed-effects ordinal regression analysis. Comput. Methods Programs Biomed. 49: 157–176. Huber, P. J. (1967). The behavior of maximum liklihood estimates under non-standard conditions. Proceedings of the Fifth Berkeley Symposium in Mathematical Statistics and Probability, 1, University of California Press, Berkeley, CA. Jessor, R., and Jessor, S. L. (1977). Problem Behavior and Psychosocial Development: A Longitudinal Study of Youth, Academic Press, New York.


PL108-312


January 28, 2000

9:28


89

Johnson, T. P., Fendrich, M., Sudman, S., Wislar, J. S., and Severns, E. (1999). An experiment to improve drug use reports during survey interviews. 1998 Proceedings of the Section on Survey Research Methods, American Statistical Association, Alexandria, VA, pp. 888–893. Johnston, L. D, O’Malley, P. M., and Bachman, J. G. (1998). Monitoring the Future 1998 Data Tables/Figures [online]. Available: Http://www.isr.umich.edu/src/mtf. Kirk, J., and Miller, M. L. (1986). Reliability and Validity in Qualitative Research, Sage University Paper Series on Qualitative Research Methods, Vol. 1, Sage, Beverly Hills, CA. Lowry, R., Holtzman, D., Truman, B. I., Kann, L., Collins, J. L., and Kolbe, L. J. (1994). Substance use and HIV-related sexual behaviors among US high school students: Are they related? Am. J. Public Health 84: 1116–1120. Measham, F., Parker, H., and Aldridge, J. (1998). The teenage transition: From adolescent recreational drug use to the young adult dance culture in Britain in the mid-1990’s. J. Drug Issues 28(1): 9–32. Metzler, C. W., Noell, J., and Biglan, A. (1992). The validation of a construct of high-risk sexual behavior in heterosexual adolescents. J. Adolesc. Res. 7(2): 223–249. National Institute of Justice (1996). 1995 Drug Use Forecasting Annual Report on Adult and Juvenile Arresstees, National Institute of Justice, Washington, DC. Nunnally, J. C., and Bernstein, I. H. (1967). Psychometric Theory, McGraw-Hill, New York. Romer, D., Hornik, R., Stanton, B., Black, M., Li, X., Ricardo, I., and Feigelman, S. (1997). “Talking” computers: A reliable and private method to conduct interviews on sensitive topics with children. J. Sex Res. 34(1): 3–9. Schopper, D., Doussantousse, S., and Orav, J. (1993). Sexual behaviors relevant to HIV transmission in a rural African population. Soc. Sci. Med. 37(3): 401–412. Seidman, S. N., and Rieder, R. O. (1994). A review of sexual behavior in the United States. Am. J. Psychiatry 151(3): 330–341. StatCorp (1997). Stata Statistical Software: Release 5.0, Stata Corporation, College Station, TX. Turner, C. F., Ku, L, Rogers, S. M., Lindberg, L. D., Pleck, J. H., and Sonenstein, F. L. (1998). Adolescent sexual behavior, drug use, and violence: Increased reporting with computer survey technology. Science 280(5): 867–873. Udry, J., and Morris, N. (1967). A method for validation of reported sexual data. J. Marriage Family 29(3): 422–446. Visher, C. (1991). A Comparison of Urinalysis Technologies for Drug Testing in Criminal Justice, National Institute of Justice and the Bureau of Justice Assistance, Washington, DC. Weinhardt, L. S., Forsyth, A. D., Carey, M. P., Jaworski, B. C., and Durant, L. E. (1998). Reliability and validity of self-report measures of HIV-related sexual behavior: Progress since 1990 and recommendations for research and practice. Arch. Sex. Behav. 27(2): 155–180. White, H. (1980). A heteroskedasticity-consistent covariance matrix estimator and a direct test for heteroskedasticity. Econometrica 48: 817–830. White, H. (1982). Maximum liklihood estimation of misspecified models. Econometrica 50: 1–25.

P1: FPY Archives of Sexual Behavior [asb]

PL108-313

January 31, 2000

9:52



Correlates of Heterosexual Behavior Among 23–87 Year Olds in Denmark and Sweden, 1992–1998 Ane Bonnerup Jæger,1 Anne Gramkow, M.D.,1 Per Sørensen, M.Sc.,1 Mads Melbye, M.D., Ph.D.,1 Hans-Olov Adami, M.D., Ph.D.,2 Bengt Glimelius, M.D., Ph.D.,3 and Morten Frisch, M.D., Ph.D.1,4

Correlates of heterosexual behavior, with a particular focus on early and high sexual activity, anal intercourse, prostitute visits, and HIV test activity, were studied. Telephone interviews were conducted with 852 randomly chosen persons who participated as controls in nationwide case–control studies of anogenital cancers in Denmark and Sweden, 1992–1998. While partner numbers and the practice of anal intercourse increased, age at sexual debut declined by 4–5 years (p < 0.001) and the maturation interval between menarche and first coitus halved (from 7 to 3 years, p < 0.001) between persons born in or before 1920 and those born in or after 1960. Women having high sexual activity were more often tested for HIV than less sexually active women, but men visiting prostitutes and those with prior STDs were not HIV tested more than other men. The increasing practice of anal intercourse, particularly among women with many partners, deserves attention, since this practice may erroneously be considered a safe sexual activity. Along with their partners, men with a history of STDs and those visiting prostitutes should be targeted in future safe sex campaigns, since these men appear to be inadequately HIV tested. KEY WORDS: sexual debut; HIV testing.

1 Department of Epidemiology Research, Danish Epidemiology Science Centre, Statens Serum Institut,

Copenhagen, Denmark. of Medical Epidemiology, Karolinska Institute, Stockholm, Sweden.

2 Department

3 Department of Oncology, Radiology and Clinical Immunology, University Hospital, Uppsala, Sweden. 4 To

whom correspondence should be addressed at Department of Epidemiology Research, Danish Epidemiology Science Centre, Statens Serum Institut, 5 Artillerivej, DK-2300 Copenhagen S, Denmark. e-mail: [email protected]. 91 C 2000 Plenum Publishing Corporation 0004-0002/00/0200-0091$18.00/0 °


PL108-313

January 31, 2000

9:52


92

Jæger et al.

INTRODUCTION Since the outbreak of the HIV epidemic studies of high-risk sexual behavior— both in the general population and in selected subgroups—have attracted increasing interest (Sundet et al., 1988; ACSF, 1992; Melbye and Biggar, 1992; Johnson et al., 1994; Michael et al., 1998). Because an important aim of the studies has been to allow improved control of HIV spread, many have focused on younger age groups, since they are more sexually active and thus more at risk for contracting STDs in general and HIV in particular. Such studies have given a baseline knowledge of sexual behavior in the younger part of general populations. Our analysis was undertaken to study correlates of sexual behavior, with particular focus on early and high sexual activity in a broad age span of the general populations in Denmark and Sweden.

SUBJECTS AND METHODS Participants During 1992–1996 a case–control study of risk factors for anal cancer was conducted in Denmark and Sweden (study 1). A total of 915 persons drawn from the general populations of the two countries was invited as controls; 554 volunteered to be interviewed (participation rates: 61% among women, 60% among men). Controls were frequency-matched with anal cancer patients within each country for sex and age in 5-year intervals (Frisch et al., 1997). A similarly designed case– control study of risk factors for penile cancer and vulvovaginal cancer is currently being conducted in Denmark (study 2), so far including 298 population controls. Participating population controls from both studies constitute the study group of the present investigation. Interview Subjects were asked by letter to participate in a telephone interview and to return a card by prepaid mail stating whether they wanted to participate. Persons who did not respond to this letter—or a reminder sent approximately 1 month later—were contacted by telephone. Participants in the study were those who were interviewed after the first or second invitation letter (letter participants) or the telephone contact (telephone participants). Nonparticipants were those who declined the invitation to participate and those who, for whatever reason, were unreachable. To minimize problems due to indiscernible self-selection, the invitation letter did not mention the specific contents of the telephone interview. Study 1 was


PL108-313

January 31, 2000

9:52

Sexual Behavior in Denmark and Sweden


93

mentioned to be a study of intestinal cancer, study 2 a study of cancer without mention of the anatomic regions in question, and invited subjects were informed that interviews would contain questions on a broad range of health-related matters and lifestyle measures. However, although the intimacy of parts of the interview was not explicitly stated, the invitation letter asked respondents to indicate a time at which they could be alone for an uninterrupted interview. National scientific ethics committees in Denmark and Sweden approved the studies. Statistical Analyses Men and women were analyzed separately. Before combining data from the two original studies we examined country specific differences in major sexual behavior variables between Danish and Swedish participants. This was done using likelihood-ratio tests with adjustment for age in 10-year age groups (≤35, 36–45, . . . , >75 years) in a logistic regression model with country as the dependent variable. Similarly, using logistic regression within the subgroup of Danish participants, we tested whether letter participants and telephone participants differed with respect to sexual behavior when adjusting for age. We also compared participants and nonparticipants in study 1 with respect to gender, birth cohort (1960), place of birth, and residence by means of chisquare test. Places of birth and residence, obtained for 73% of Danish participants, were divided into three categories: Copenhagen area (Copenhagen and its suburbs), towns (cities with 10,000 inhabitants or more), and rural communities (cities or rural communities with fewer than 10,000 inhabitants). Logistic regression analysis served to identify correlates of selected measures of sexual activity. These measures included sexual debut at or before age 16, a partner number ≥3 before age 20, a lifetime number of ≥10 partners, HIV test activity, the practice of receptive anal intercourse among women, and men’s visits to prostitutes. Odds ratios were adjusted for age (≤35, 36–45, . . . , >75 years) and country. In tests for trend we treated categorized continuous variables as continuous using medians as category values. Although distributions of some covariates (e.g., tobacco and alcohol consumption) differed between Danish and Swedish participants, introduction of interaction terms for country of residence in the models revealed no statistical interaction between such covariates and the sexual behavior variables examined. Consequently, Danes and Swedes were combined in all analyses. Logistic regression analyses were carried out using the GENMOD procedure in SAS (SAS Institute, 1996). Correlations between year of birth, on one side, and age at menarche, first intercourse, interval between menarche and first intercourse, and number of sexual partners, on the other, were evaluated by means of Spearman’s rank correlation test. The Mantel–Haenszel chi-square test was used to evaluate trends in proportions of subjects. The level of significance was set at p < 0.05 (two-sided).


PL108-313

January 31, 2000

9:52


94

Jæger et al.

RESULTS Overall, 852 persons aged 23–87 years participated in the study; 586 respondents were from Denmark and 266 were from Sweden. Selected demographic and other background characteristics of the study participants are listed in Table I. Sexual practices did not differ significantly between Danish and Swedish participants (all p values > 0.05), except for the practice of heterosexual receptive Table I. Demographic and Other Background Variables n(%)

No. participants Study groupa Study 1 Study 2 Country Denmark Sweden Age (years) ≤35 36–45 46–55 56–65 66–75 >75 Year of birth Before 1920 1920–1929 1930–1939 1940–1949 1950–1959 1960 or after Years of school ≤7 8–9 ≥10 Further education None ≤3years >3 years Residenceb Rural communities Towns Copenhagen area Stay abroad >6 months No Yes

Women

Men

600 (70)

252 (30)

349 (58) 251 (42)

205 (81) 47 (19)

425 (71) 175 (29)

161 (64) 91 (36)

33 (6) 85 (14) 129 (22) 128 (21) 139 (23) 86 (14)

13 (5) 17 (7) 51 (20) 49 (19) 72 (29) 50 (20)

81 (14) 133 (22) 121 (20) 131 (22) 96 (16) 38 (6)

47 (19) 73 (29) 49 (19) 50 (20) 20 (8) 13 (5)

223 (37) 127 (21) 249 (42)

124 (49) 45 (18) 83 (33)

188 (31) 300 (50) 111 (19)

61 (24) 137 (54) 54 (21)

88 (30) 94 (32) 112 (38)

45 (34) 40 (30) 48 (36)

513 (86) 87 (15)

203 (81) 48 (19)

a Study 1 refers to the study of anal cancer; study 2 refers

to the study of penile and vulvovaginal cancer. on place of residence available only for a subgroup of Danish respondents.

b Information


PL108-313

January 31, 2000

9:52



95

anal intercourse, which was more commonly reported by Danish women. Likewise, there was no significant difference in reported sexual behavior between letter participants and telephone participants. Participants and nonparticipants were similar with respect to gender and places of birth and residence, but participants were on average considerably younger than nonparticipants. Participation rates were 81% among women and 73% among men born in 1960 or later, compared with 31% of women and 43% of men born before 1920 (p trend < 0.01 for each sex).

Age at Sexual Debut and Partner Numbers Measures of sexual behavior of the study group are presented in Table II. Age at sexual debut decreased in successive birth cohorts [Spearman’s correlation coefficient (ρ) = −0.41 in men and ρ = −0.51 in women; p < 0.001 for each sex], with medians being 21 years for women and 20 years for men born before 1920 and 16 years for both sexes among those born in 1960 or later (Fig. 1). In addition, the total number of sexual partners increased over time (ρ = +0.24 in men and ρ = +0.40 in women; p < 0.001 for each sex). While the median lifetime number of partners for women and men born before 1920 was one and three, respectively, the corresponding figure for both women and men born 1960 or later was seven

Fig. 1. Age at menarche and coitarche, median and 25th and 75th percentiles.


PL108-313

January 31, 2000

9:52


96

Jæger et al. Table II. Distribution of Marital Status and Basic Sexual Behavior n(%)

No. participants Marital status Married Widowed Unmarried Separated/divorced Age at sexual debut ≤16 17 18 19 20 ≥21 Number of partners before age 20 0 1 2 ≥3 Lifetime number of partners of the opposite sex 0 1 2–4 5–9 ≥10 Tested for HIV Yes No History of STDa Ever Never Visited female prostitute Ever Never Receptive anal intercourseb Ever Never

Women

Men

600 (70)

252 (30)

346 (58) 130 (22) 50 (8) 74 (12)

175 (69) 26 (10) 25 (10) 26 (10)

121 (20) 91 (15) 106 (18) 63 (11) 70 (12) 141 (24)

49 (20) 33 (14) 36 (15) 23 (10) 33 (14) 67 (28)

219 (37) 192 (32) 88 (15) 95 (16)

111 (45) 33 (13) 30 (12) 75 (30)

2 (0.3) 186 (32) 229 (39) 86 (15) 83 (14)

5 (2) 40 (17) 72 (30) 51 (21) 75 (31)

65 (11) 533 (89)

32 (13) 220 (87)

80 (13) 520 (87)

36 (14) 216 (86)

— —

39 (16) 204 (84)

79 (13) 510 (87)

— —

a Includes

one or more of the following: Chlamydia, gonorrhea, syphilis, genital warts, and genital herpes. b Of women engaging in anal intercourse, 74 were Danish and 5 were Swedish.

(Fig. 2). For women and men aged >75 years the proportions with ≥10 lifetime partners were 1 and 17%, respectively, as contrasted with 42% of both women and men aged ≤35 years. Compared with respondents in unbroken marriages (married or widowed), unmarried women and separated/divorced women and men were significantly more likely to have had ≥10 partners (Table III). Among women, longer school attendance was associated with later sexual debut and fewer partners before age 20


PL108-313

January 31, 2000

9:52



97

Fig. 2. Lifetime number of partners of the opposite sex, median and 25th and 75th percentiles.

but not with the lifetime number of partners. Men with ≥8 years of school tended to have more partners than those with ≤7 years of school education. Danish participants living in the Copenhagen area tended to have higher lifetime partner numbers than persons living in smaller towns or rural areas. A stay abroad for more than 6 months was significantly associated with having a total of ≥10 partners (OR = 3.6 among women and OR = 4.0 among men). Smoking was strongly associated with early sexual debut, particularly among men. Indeed, the odds of having had a sexual debut before age 16 were more than 25-fold higher among men with an average consumption of >10 cigarettes per day [OR = 26.0; 95% confidence interval (CI), 3.1–216] and almost 10-fold higher among those who smoked while in their twenties (OR = 9.9; 95% CI, 2.1–46.2) (Table III). Tobacco and alcohol consumption was also positively associated with having a high number of sexual partners (Table III). The median age at menarche decreased from 14 years among women born before 1920 to 13 years among those born in 1960 or later (ρ = −0.22, p < 0.001), while the median interval between menarche and coitarche decreased from 7 to 3 years (ρ = −0.35, p < 0.001) (Fig. 1). Women whose age at menarche was ≥15 years had a higher age at sexual debut and a lower lifetime number of partners than those having menarche at a younger age (Table III). Basic measures of high sexual activity were closely associated. Participants who started sexual activity at age ≤16 years were more likely to accumulate

Marital status Married/widowed Unmarried Separated/divorced Years of school ≤7 8–9 ≥10 Residenceb Rural communities Towns Copenhagen area Stay abroad >6 months No Yes Smoking status Never Former Current Average No. cigarettes/dayc 0 1–10 >10 Smoking status, age 20–29 Never Ever 1.0 (ref.) 1.8 (0.6–5.8) 1.7 (0.6–4.9) 1.0 (ref.) 0.5 (0.2–1.6) 1.2 (0.5–2.9) 1.0 (ref.) 2.4 (0.8–7.4) 1.3 (0.4–4.3) 1.0 (ref.) 1.9 (0.8–4.3) 1.0 (ref.) 23.3 (2.7–200) 19.8 (2.3–167) 1.0 (ref.) 12.8 (1.4–117) 26.0 (3.1–216) 1.0 (ref.) 9.9 (2.1–46.2)

1.0 (ref.) 0.7 (0.3–1.7) 1.7 (0.9–3.1 ) 1.0 (ref.) 0.4 (0.2–0.7) 0.2 (0.1–0.4) 1.0 (ref.) 1.2 (0.6–2.6) 1.1 (0.5–2.3) 1.0 (ref.) 0.6 (0.3–1.1) 1.0 (ref.) 3.6 (2.1–6.1) 2.3 (1.3–4.3) 1.0 (ref. ) 2.8 (1.6–4.9) 3.4 (1.9–5.9) 1.0 (ref.) 3.0 (1.9–4.8)

1.0 (ref.) 4.3 (1.8–10.2)

1.0 (ref.) 1.8 (0.6–5.1) 5.1 (2.1–12.6)

1.0 (ref.) 2.8 (1.7–4.9)

1.0 (ref.) 2.9 (1.6–5.4) 1.9 (0.98–3.6)

1.0 (ref.) 2.1 (1.1–3.7) 2.9 (1.5–5.7)

1.0 (ref.) 2.6 (1.2–5.6)

1.0 (ref.) 1.7 (0.7–4.5) 3.3 (1.4–7.5)

1.0 (ref.) 3.6 (1.5–8.6) 2.1 (0.9–4.9)

1.0 (ref.) 4.0 (1.9–8.2)

1.0 (ref.) 1.1 (0.4–3.0) 2.6 (1.0–6.7)

98

1.0 (ref.) 2.8 (1.7–4.7)

1.0 (ref.) 2.5 (1.4–4.6) 2.7 (1.5–5.0)

1.0 (ref.) 4.0 (1.5–10.3) 3.6 (1.4–9.0)

1.0 (ref.) 3.6 (2.0–6.4)

1.0 (ref.) 1.7 (0.7–4.5) 2.4 (0.98–6.0)

1.0 (ref.) 1.9 (0.8–4.4) 1.9 (0.9–3.9)

1.0 (ref.) 1.1 (0.4–2.9) 3.9 (1.5–9.8)

9:52

1.0 (ref.) 2.4 (1.3–4.2) 3.1 (1.6–5.9)

1.0 (ref.) 1.7 (0.8–3.3)

1.0 (ref.) 0.6 (0.2–1.6) 0.9 (0.4–2.2)

1.0 (ref.) 0.9 (0.4–2.1) 1.8 (0.9–3.8)

1.0 (ref.) 3.6 (1.6–7.9) 4.5 (2.4–8.4)

January 31, 2000

1.0 (ref.) 1.2 (0.7–2.3)

1.0 (ref.) 1.2 (0.5–2.8) 1.0 (0.4–2.4)

1.0 (ref.) 1.7 (0.7–3.9) 1.5 (0.7–3.1)

1.0 (ref.) 0.9 (0.4–2.4) 1.3 (0.5–3.3)

Men

≥10 partners (lifetime) Women

PL108-313

1.0 (ref.) 0.5 (0.2–0.99) 0.6 (0.3–1.1)

1.0 (ref.) 0.8 (0.3–2.0) 2.7 (1.5–5.1)

Women

Men

≥3 partners before age 20 years

Women


Men

Age at sexual debut ≤16 years

OR((95% CI)

Table III. Correlates of Basic Measures of Sexual Activity: Odds Ratiosa (OR) and 95% Confidence Intervals (CI)

P1: FPY Style file version Nov. 19th, 1999

Jæger et al.

1.0 (ref.) 1.6 (0.2–14.3) 6.2 (0.7–55.0) — — — — — — —

1.0 (ref.) 0.9 (0.4–2.0) 1.4 (0.5–3.7) 2.2 (1.4–3.7) 1.0 (ref.) 0.5 (0.3–0.8) — — — —

— —

23.4 (8.8–62.5) 1.0 (ref.)

— — —

1.0 (ref.) 2.3 (0.5–11.0) 6.9 (1.4–33.8)

of interview (current smokers).

1.0 (ref.) 20.2 (9.2–44.5)

6.6 (3.0–14.7) 1.0 (ref.)

— — —

— 1.0 (ref.) 3.9 (2.1–7.4)

cessation (former smokers) or the time

1.0 (ref.) 5.8 (3.3–10.2)

1.9 (1.1–3.4) 1.0 (ref.)

0.7 (0.4–1.2) 1.0 (ref.) 0.4 (0.2–0.8)

1.0 (ref.) 1.9 (0.6–5.9) 5.4 (1.5–19.4)

PL108-313

— —

4.2 (2.5–7.2) 1.0 (ref.)

0.9 (0.5–1.6) 1.0 (ref.) 0.7 (0.4–1.2)

1.0 (ref.) 1.5 (0.6–3.9) 1.2 (0.4–3.9)


a Odds ratios are adjusted for country and age (≤35, 36–45, 46–55, 56–65, 66–75,

No title

No title

No title

No title

No title

No title

No title

No title

No title

No title

No title

No title

No title

No title

No title

No title

No title

No title

No title

No title

No title

No title

No title

No title

No title

No title

Recommend Documents