The Road to Truth

Much more is now known about human origins and evolution than was the case almost 40 years ago, when I began to study primate reproductive biology. In the final essence, it is the fossil evidence of hominid evolution, reviewed briefly in the first chapter of this book, which provides the backcloth against which the sexual behaviour and reproductive anatomy and physiology of the extant primates may be viewed in true evolutionary perspective. This has been the approach adopted throughout this book, and the goal of this final chapter is to present overall conclusions concerning the origins of human mating systems, patterns of copulatory behaviour, and mate choice.

Darwin's insights concerning the probable African origin of human beings have been confirmed by palaeontological discoveries as well as by the results of research on comparative anatomy and molecular genetics. Anatomically modern human beings originated in Africa and our species has spread far beyond its origins to invade and colonize the rest of the world. The human genus (Homo) is most closely related to the chimpanzee and bonobo (Pan) among extant primates, and the common ancestors of these two genera existed in Africa approximately 8 million years ago. It is still the case that little is known of the putative stem forms, although on current evidence Ardipithecus is thought to be a possible candidate. Earlier still, perhaps 10-8 million years ago, the ancestors of modern gorillas diverged from the lineage which led to the precursors of Pan and Homo. Recently, fossilized remains of a robust ape (Chlorapithecus abyssinicus), which lived in Ethiopia about 10 million years ago, have been described by Suwa et al. (2007), who conclude that this new species 'may be a basal member of the gorilla clade'.

The earliest members of the hominid lineage, the australopithecines, were relatively small-brained and bipedal apes, which are known primarily from fossils discovered in Southern and Eastern Africa. These include more gracile species such as Australopithecus africanus and A. afarensis, as well as forms with more massive jaws and large molar teeth (e.g. Paranthropus boisei and P. robustus). It is interesting to cast one's mind back and to recall debates as to whether the australopithecines were efficient bipeds and whether they were ancestral to humans (Day 1973; Zuckerman et al. 1973). The discovery of more complete skeletal material from a specimen of A. afarensis ("Lucy": Johanson and White 1980) made it increasingly clear that bipedalism was well developed in these creatures, although the anatomy of their forelimbs is also indicative of the ability to climb well. Most recently, Whitcome, Shapiro, and Lieberman (2007) have reported that, like women, female A. africanus exhibited specializations of lumbar vertebral anatomy; serving to strengthen the spine during 'bipedal obstetric load' (i.e. when walking upright during pregnancy).

The cranial capacities of the australopithecines ranged from 400-500 cc, but their brains may have been larger, in relation to body size, than those of extant apes such as the chimpanzee (Martin 1983, 1990). Chimpanzees are able to make and use simple tools (McGrew 1992), so it is likely that the australopithecines also used rudimentary technologies. However, given the crude or ephemeral nature of tools used by the great apes, it should not surprise us that little trace has been found of those used by the earliest human precursors. Raymond Dart interpreted the remains of animals excavated from the same limestone caves as Australopithecus, as evidence that it had developed an 'osteodon-tokeratic' culture; making use of the bones, teeth, and horns of its prey to fashion tools. Although these early ideas were subsequently shown to be incorrect, it still remains a daunting task to reconstruct any credible picture of the lives of the austra-lopithecines or of the earliest representatives of the genusHomo. The relevance of possible sexual dimorphism in body size is a case in point. In Chapter 1, evidence was reviewed which indicates that some of these hominids were sexually dimorphic, adult males being much larger than females (see Table 1.1). Among the extant Old World anthropoids, extreme sex differences in body weight occur in species, such as the gorilla, which have polygynous mating systems. However, sex differences in body weight are also typical of monkeys and apes that have multi-male/multi-female mating systems, such as the macaques and chimpanzees. Although body size sexual dimorphism is on average less pronounced in such multi-male/multi-female forms, there is considerable inter-specific variability and overlap with the polygynous anthropoids. Where the sexes are similar in size, a monogamous mating system often occurs. Because it is so difficult to identify the sexes and to calculate body sizes from fragmentary fossil evidence, current estimates of sexual dimorphism in australopithecines and other extinct hominids must be treated with the utmost caution. A. afarensis, for example, has been characterized as being highly sexually dimorphic. If correct, this finding could be consistent with effects of intra-sexual selection for increased male body size within a polygynous mating system. Yet, detailed studies by Reno et al. (2003) led them to reject this conclusion, and to suggest that the sexes might have been very similar in size, as is more consistent with monogamy. Is it even possible that some larger and smaller specimens, currently assigned to A. afarensis, might represent members of two separate species, rather than being males and females of the same species?

Recent evidence of small skull size in an African specimen of H. erectus has also fuelled speculation about sexual dimorphism and polygyny in this species (Spoor et al. 2007). However, the cranial capacities of specimens of H. erectus vary tremendously and brain size enlarged progressively during the long time span that this taxon existed. Perhaps the small cranial capacity of the recently described African specimen relates to its greater geological age, as well as the degree of its geographical separation from specimens of H. erectus discovered in Asia (see Figure 1.10).

Lovejoy (1981) posited that monogamy is an ancient trait among hominids. However, many conflicting views have been expressed as to whether human ancestors had monogamous, polygynous, or multi-partner-mating systems. Cross-cultural anthropological evidence shows that the majority of recent human populations include polygyny, as well as monogamy within their mating system (Ford and Beach 1951; Murdock 1981). The phenomenon of romantic love is a human universal, as is the propensity for men and women to engage in long-term relationships, and to raise their children together. As David Buss has put it

Some continue to argue that people are fundamentally evolved to be monogamous____Others argue that humans are naturally promiscuous, and that marriage represents an unnatural cultural imposition. Both these simplistic notions are wrong.

Given the extreme difficulties of calculating sexual dimorphism in body size based upon existing fossil evidence, the conclusion reached in Chapter 1 was that it would be unwise to attempt to deduce the mating systems of the australopithecines, or of early members of the genus Homo, on this basis alone. In the circumstances, the best route that we may follow involves attempts to reconstruct the likely origins of human sexuality from comparative data on anatomy, physiology, and behaviour obtained by studying the extant non-human primates and other mammals. This approach, coupled with insights derived from anthropology and evolutionary psychology, may help us to understand the likely mating systems and sexual behaviour of extinct hominids.

It is a huge disappointment that none of the australopithecines or members of the genus Homo besides H. sapiens have survived to the present day; humankind is alone, although it was not always so. In the absence of any more closely related species, the chimpanzee and bonobo have been extensively studied and compared to H. sapiens. However, comparisons at the level of their sexuality are of limited value. To cite examples, Tanner and Zihlman (1976) attempted to construct an evolutionary scenario of human sexuality based upon a chimpanzee model.

Smith (1984) likewise injected a strong flavour of chimpanzee-like behaviour, involving multiple-partner matings and specializations for sperm competition, into his reconstruction of the mating system of Homo habilis. Such attempts are flawed because despite the much-vaunted close genetic relationships between Pan and Homo (Diamond 1991), the chimpanzee differs markedly from human beings as regards its mating system, reproductive anatomy, and sexual behaviour. The huge relative testes sizes of chimpanzees and bonobos relate to their multi-male/multi-female mating systems and represent the evolutionary outcome of intense sexual selection at the copulatory and post-copulatory levels. Sperm competition has profoundly influenced many other aspects of chimpanzee reproductive physiology and behaviour, in ways that are very different to the situation which pertains in H. sapiens.

Despite the fact that testes sizes are much smaller in man than in the chimpanzee, many authors adhere to the view that sperm competition must have played a significant role in the evolution of human reproductive biology (Smith 1984; Baker and Bellis 1995; Buss 2003; Shackelford et al. 2005; Shackelford and Pound 2006). This problem was not addressed by Darwin (1871), as he was unaware of the important role played by sexual selection in shaping the anatomy and physiology of the primary genitalia. These insights were achieved much later, principally as a result of Parker's (1970) pioneering work on sperm competition and Eberhard's (1985; 1996) seminal contributions to the concept of sexual selection by cryptic female choice. Unfortunately, when considered in isolation, comparative measurements of mammalian relative testes sizes are not sufficient to resolve the question of whether sperm competition has played any significant role in human evolution. This problem was discussed in some detail in Chapter 2. Cross-cultural data on testes size in relation to adult body weight were assembled for more than 7,000 men, representing 14 modern human populations (see Table 2.2). These range from the unusually small testes of Hong Kong Chinese to the much larger testes that occur in men of European and African descent. Although the acquisition of more data would clearly be desirable for comparative purposes, current evidence indicates that the testes are smaller in relation to body weight in some Asiatic populations than is the case for men from Africa and Europe. However, a consistent feature shared by all populations is the statistical tendency for the right testis to be slightly larger than the left testis.

Short's (1984) hypothesis, linking smaller-sized testes in Asiatic males to genetic factors governing gonadal function in both sexes, and to the lower frequencies of dizygotic twinning in these same populations, is supported by the cross-cultural comparisons included in Chapter 2 (Table 2.6). However, it is essential to keep in mind the caveat that diverse methods have been used to measure human testes volumes and that some of them (especially those involving orchidometers) can result in inaccuracies. Nonetheless, the smaller testes sizes of some modern Asiatic populations probably have no connection with the evolution of their mating systems or with sperm competition. It is more probable that selective forces acting upon gonadal function in women, to limit the likelihood of multiple ovulation and dizygotic twinning, may have also impacted genetic mechanisms which affect gonadal size in males. Reduced twinning rates among women in these populations may perhaps be linked to their lighter body build, and to the greater health risks associated with twin pregnancies and births.

Measurements of relative testes size provide only a crude index of the likelihood of sperm competition, albeit a most useful one. My own interpretation of the data on relative testes sizes in mammals (Figures 2.1, 2.2, and 2.3) remains that human testes are quite small, as is consistent with an evolutionary history involving monogamy or polygyny. However, given the continuing controversies which surround the question of human sperm competition, especially in the literature on evolutionary psychology, it is most helpful to explore the effects of sexual selection upon other reproductive traits and to consider sperm morphology, the structure and functions of the accessory reproductive glands, and the penis. Chapters 3 and 4 dealt with the roles played by sperm competition and cryptic female choice in the evolution of mammalian reproductive anatomy and physiology. Sperm competition has favoured the evolution of larger sperm midpiece volumes in mammals (Anderson and Dixson 2002; Anderson et al. 2005). This is not the case in birds (Immler and

Birkhead 2007). However, mammals and birds are widely separated in phylogeny, and avian gamete morphologies differ markedly from those of most mammals (Jamieson 2007).

Human sperm have small midpieces, and this indicates that sperm competition is unlikely to have played a significant role in the evolution of human gametes. This conclusion is strengthened by comparisons of in vitro staining of mitochondria in the sperm midpieces of man and the chimpanzee. The sperm midpiece is not only much larger in chimpanzees than in human males, but it also contains a larger volume of mitochondria, which stain red in response to the dye JC-1 (Anderson et al. 2007). Sexual selection may have favoured the evolution of greater mitochondrial loading in chimpanzees, and in other mammals where sperm competition is significant, in order to enhance the energy production required for sperm motility. Relative testes sizes and sperm midpiece volumes are positively correlated for a large sample of mammalian taxa (Anderson et al. 2005). Thus, sexual selection has acted to increase the volume of seminiferous tissue in the testes and to improve the energetics of individual gametes. Human sperm have even smaller midpieces than those of the gorilla (Figure 3.4 and Table 3.1).

Although human testes are of modest size in relation to body weight, one theoretical possibility is that selection might have increased the efficiency of human spermatogenesis, compared to that of other mammals. Thus, human testes might produce gametes more rapidly and hence make larger numbers than expected, given their size and the amount of seminiferous tissue they contain. This question was also considered in Chapter 3 but, far from being exceptional, human testes produce fewer spermatozoa per gram of parenchyma (seminiferous tissue) than in almost all mammals for which accurate data exist. This finding relates, in turn, to the fact that individual Sertoli cells in the human testis each support the development of relatively few sperm by comparison with other mammals. The total duration of spermatogenesis in men (74-76 days) is also long by comparison with many other mammals and the total daily production of sperm and numbers stored in the cauda epidi-dymis are comparatively low and unexceptional (see Table 3.2).

More unusual is the occurrence of significant numbers of morphologically abnormal sperm in the human ejaculate; sperm pleiomorphism is more pronounced in H. sapiens than in most other primates. Human founder populations are thought to have been quite small, and were subject to genetic bottlenecks during their migrations out of Africa and throughout the world (Manica et al. 2007). Abnormalities of sperm morphology may have been one of the consequences of the reductions in genetic variability in human founder populations. One interpretation of this might be that the occurrence of a small percentage of morphologically imperfect sperm in the ejaculate, once established, is more likely to persist under conditions where females copulate with a single principal male (as is the case in polygynous and monogamous mating systems) rather than with multiple partners. There is less possibility of sperm competition occurring and less selection pressure for improvements in sperm quality in such circumstances. Thus, if human founder populations had primarily polygynous or monogamous mating systems, a small degree of sperm abnormality might have persisted in the absence of negative selection pressure. Interestingly, sperm pleiomorphism is also pronounced in the gorilla, which is polygynous, whereas relatively few abnormal sperm occur in the ejaculates of bonobos and chimpanzees which have multi-male/multi-female mating systems. (Figure 3.7).

Contrary to these interpretations, the notion that pleiomorphic human sperm represent distinct morphs, which evolved in order to undertake specialized roles during sperm competition, was advanced by Baker and Bellis (1988; 1995). They posited that Kamikaze sperm exist in human ejaculates, and that these serve to block the progress of the gametes of rival males within the female reproductive tract. Kamikaze sperm thus increase the chances that specialized egg-getter sperm can reach the oviduct. These theories and others concerning the functions of pleiomorphic human sperm are not supported by credible experimental evidence, and have been rebutted by critical authorities (Harcourt 1991; Short 1997; Dixson 1998a; Moore et al. 1999; Dixson and Anderson 2001; Birkhead 2000; Lloyd 2005).

Studies of gamete biology provide little support for the idea that sperm competition has played a significant role in the evolution of human reproduction. Indeed, this conclusion is strengthened when one considers the results of comparative studies of the accessory reproductive organs of mammals. For example, the vasa deferentia are relatively shorter and more muscular in those mammals in which females mate with multiple partners during the fertile period. Sperm competition has presumably favoured the evolution of such specializations in order to maximize the efficiency of rapid sperm transport during sexual activity. In particular, it is the thicknesses of the two layers of longitudinal muscles in the wall of the duct which have increased due to sperm competition (Anderson et al. 2004). By contrast, mammals in which females mate primarily with a single male, and which are monogamous or polygynous, have less well-developed longitudinal muscles, and a relatively thicker (central) layer of circular muscles in the wall of the vas deferens. The human vas is structurally of this latter type (see Figures 3.13 and 3.14). This fact provides further evidence that sperm competition is unlikely to have played a significant role in the evolution of the human reproductive system. These findings are contrary to the ideas advanced by Smith (1984), who suggested that specializations for sperm competition might be revealed by studying the structure of the human vas deferens. However, at the time Smith wrote his review no quantitative studies had been carried out to test such ideas.

The sizes and functions of the seminal vesicles vary tremendously in different groups of mammals, and their secretions constitute 60 per cent of the human ejaculate. From an evolutionary standpoint it is interesting that the seminal vesicles of primate species in which sperm competition pressures are greatest are significantly larger than those of monogamous and polygynous species (Dixson 1998b). Likewise, seminal coagulation and copula-tory plug formation are more pronounced in primates which engage in multi-partner matings and sperm competition (Dixson and Anderson 2002). The seminal vesicles are of medium size in human males, and seminal coagulation is likewise less pronounced than in primates where sperm competition is significant (see Figures 3.16 and 3.17). This example of sexually selected variations of male reproductive physiology is further bolstered by molecular studies of rates of evolution of the genes that encode for production of the semenogelins; these are the proteins which act as substrates for seminal coagulation (Dorus et al. 2004).

Comparisons of mammalian testicular function, sperm morphology, and the structures and functions of the reproductive ducts and accessory glands, all support the view that human sexual behaviour does not spring from an evolutionary background involving specializations for sperm competition. Despite this, numerous authors argue that human penile morphology is exceptional and specialized by comparison with other primates (Fisher 1982; Smith 1984; Baker and Bellis 1995; Diamond 1997; Jolly 1999; Miller 2000; Buss 2003; Rolls 2005). Gallup and Burch (2004) attempted to test hypotheses advanced by Baker and Bellis, proposing that the human penis is morphologically specialized to displace the semen of rival males during copulation. Gallup et al. (2003) have also argued that penile size and the large glans with its pronounced coronal ridge aid sperm displacement during bouts of deep pelvic thrusting. Such patterns of deep thrusting are said to occur if men suspect that their partners have previously engaged in extra-pair copulations. Mechanisms of semen displacement were not assessed in vivo during these experiments. Instead, models of the human genitalia were used (vaginae, dildos, and artificial semen formulated using cornstarch solutions: Gallup et al. 2003). The results of these experiments are likely to be invalid, due to the unrealistic nature of the models employed and the risks of subjective bias in using them to simulate natural events that occur during copulation.

Quantitative comparisons of penile morphologies in forty-eight primate genera, including Homo, confirm that human phallic morphology is not exceptional, and is consistent with an evolutionary background of either monogamy or polygyny rather than one that involved any significant degree of sperm competition (see Figure 3.22). Aside its breadth, the human penis is not unusually large, and some monkeys also have large and thick penes (e.g. spider and woolly monkeys: Figure 3.20). Moreover, the possession of a rounded or helmet-shaped glans penis is a phylogenetically ancient trait, present in many Old World monkeys and also in the gorilla. The chimpanzee, in accord with its other specializations for sperm competition, has a highly derived penile morphology, involving loss of a distinct glans to produce an elongated, filiform structure.

Given these facts, it is difficult to understand why so many authors continue to state that human beings have exceptionally large and complex penes, as the morphological evidence does not support this conclusion. The problem may result, in part, from the use of inaccurate or incomplete data on penile sizes in the great apes (as cited by Smith 1984) that have entered the literature and have been repeated by authors, often at several removes from original sources. Indeed, a lack of first-hand experience characterizes many of these comparisons between the human genitalia and those of other primates. There also appears to be a certain coyness where metric studies are involved, as if the measurement of penile morphology is a less acceptable topic than measurements of other external structures. In reality, the human penis is unremarkable when compared to those of many non-human primates and other mammals. There is no substance to the notion that the evolution of human penile morphology has been affected by sperm competition.

Eberhard (1985; 1996) has proposed that the intromittent organs of animals may also function as internal courtship devices; especially so in those cases where females mate with multiple partners. Sexual selection may thus have influenced the evolution of phallic morphology via cryptic female choice, as well as through sperm competition. In practice, both these processes are likely to entwine during the co-evolution of the male and female genitalia.

Chapter 4 explored the relevance of cryptic female choice to studies of mammalian genitalia and cop-ulatory behaviour. Primate penile morphologies are, indeed, most complex in those species where females mate with multiple partners. This finding represented the first quantitative test of Eberhard's (1985) ideas to be reported for a vertebrate group (Dixson 1987a). The inclusion of human phallic morphology in a new analysis reported in Chapter 3 confirms that the human condition is relatively simple, and like those of the other polygynous or monogamous primates. In the chimpanzee, by contrast, the penis is morphologically specialized. It is elongated and filiform in order to deposit ejaculates close to the cervical os, and to negotiate the female's large sexual skin swelling, which increases vaginal length by up to 50 per cent during the fertile period (see Figure 4.2).

A second possible avenue for cryptic female choice concerns the transport or storage of sperm. Because women as well as men have the capacity to exhibit orgasm during sexual activity, it has been suggested that female orgasm may have evolved in relation to patterns of sperm transport and sperm competition. Thus, Baker and Bellis (1993b; 1995) proposed that high sperm retention and low sperm retention orgasms occur in women, and that the former may be activated during extra-pair copulations with preferred partners. These ideas have frequently been cited in the literature on evolutionary psychology. However, at the opposite pole of opinion, Symons (1979) interpreted the occurrence of orgasm in women as a non-adaptive homologue of the male phenomenon. This view aroused criticism from some quarters (e.g. Hrdy 1979), fuelled perhaps by a clash between scientific reasoning and feminist or sociological perspectives concerning the significance of orgasm in women.

In fact, there is no robust evidence that female orgasm plays any role in human sperm transport or fertility. Unfortunately, this subject has not received the experimental attention it deserves, and some of the few studies which do exist have been cited selectively and given undue weight in the literature. A recent and most thorough critique of work in this area by Elisabeth Lloyd (2005) shows how limited evidence or flawed experiments have been over-interpreted to promote the view that women's orgasms might influence sperm transport. These matters were discussed in some detail in Chapter 4, so that it is not necessary to repeat the arguments here. Suffice it to say that whilst female orgasm certainly does occur in some primates, it probably represents a non-adaptive homologue of the male capacity to exhibit orgasm during ejaculation. Male primates also display non-adaptive homologues of feminine traits, such as nipples and (in some species) an atrophic uterus masculinus. What is worrying, as Lloyd (2005) points out, is the extent to which poorly grounded arguments and limited evidence concerning female orgasm have been incorporated into the literature of evolutionary psychology, as if they represent established facts of human physiology.

The oviduct constitutes the final arena for sperm competition, or cryptic choice, within the female reproductive tract. Indeed, it is likely that differential activation or suppression of motility in subpopulations of sperm within the isthmus of the oviduct may play a key role in mammalian sperm selection (Sakate et al. 2006). Fertilization of ova occurs in the ampullary portion of the human oviduct, as is the case among mammals in general. Studies of insects point the way to effects of sexual selection upon the evolution of female sperm storage organs (spermathecae) and their associated ducts (Eberhard 1996; Simmons 2001). Among mammals, it is of considerable interest that oviductal length varies with respect to the mating system (Anderson, et al. 2006). Thus, the oviducts are longest in those mammals where females commonly mate with multiple partners, and in which males have larger testes in association with increased sperm competition pressures (see Figures 4.5 and 4.6). Perhaps elongation of the oviduct in some way tests the relative fitness of gametes from rival males. In women, the oviducts are relatively short in relation to body size. There is no support from this quarter for possible effects of sexual selection upon the evolution of the human genitalia via cryptic female choice.

The limited data currently available on mammalian cryptic female choice are consistent with conclusions reached by studying the anatomy and physiology of the male reproductive system. Homo sapiens exhibits traits consistent with a long history of polygyny or monogamy, and a relative absence of sperm competition. This does not mean that sperm competition never occurs, or that it is impossible for it to occur in modern-day human populations. The anatomical and physiological evidence does indicate, however, that sperm competition is unlikely to have played any significant role in human evolution. Some evolutionary psychologists adopt a contrary view, and propose that human sexual behaviour and mating strategies have been affected by sperm competition pressures (Baker and Bel-lis 1995; Gallup et al. 2003; Shackelford et al. 2005; Platek and Shackelford 2006). However, the absence of anatomical and physiological specializations for sperm competition in H. sapiens argues very strongly against the validity of such conclusions.

Comparative studies also offer useful insights concerning the origins of human copulatory behaviour. Copulatory postures and patterns among the non-human primates present some interesting phylogenetic variations. These have been subject to the effects of both natural and sexual selection, as was discussed in Chapter 5. Among the lorisines, for example, the African potto, and slender and slow lorises of Asia all exhibit distinctive inverted copulatory postures, with the female clinging underneath a branch as the male mounts in a dorso-ventral position. This probably represents a phylo-genetically ancient trait in this group of prosimians. Similarly, among the New World primates, most of the ateline monkeys exhibit a peculiar leg-lock variation of the dorso-ventral mounting posture, in which the male places his legs over, and medial to those of the female partner (see Figure 5.3). Such postural specializations are interesting from a phy-logenetic perspective, but all of them are variations of the typical dorso-ventral mounting postures which occur throughout the Order Primates, and in mammals in general. However, among the apes as well as in human beings, ventro-ventral and female superior copulatory postures have also been recorded. Face-to-face mating postures, such as the 'missionary position' are thus not unique to human beings, and probably represent phylogenetically primitive traits. In Chapter 5, it was argued that the evolution of brachiation and the postural flexibility conferred by specializations of the shoulder joint and shoulder musculature allowed apes to adopt more variable postures during arboreal copulation. Orangutans, despite their great size, copulate using a variety of suspensory postures, or with the male reclining upon his back whilst the female mounts him. Although the African apes are largely terrestrial, face-to-face matings occur quite commonly among wild bonobos, and have occasionally been reported in captive and free-ranging gorillas. Thus, it is likely that ventro-ventral or female superior copulatory positions in the apes and human beings derive from postures used by their common ancestors, and would have been present also in the earliest hominids. These observations provide no support for the view that ventro-ventral copula-tory postures represent uniquely human specializations, serving to increase clitoral stimulation and enhance orgasmic responses in women (Ford and Beach 1951). Rather, the three basic human copula-tory positions (ventro-ventral, female superior, and dorso-ventral) all derive from patterns homologous with those which occur in extant apes.

Copulatory durations also vary considerably among mammals, lasting only for a few seconds, or for hours depending upon the species considered. Among the primates, examples of these two extremes are provided by the common marmoset, which reaches ejaculation in 5 s, and the greater galago which may intromit for 2 h or more, and probably exhibits multiple ejaculations during that time. The evolution of intromission durations, patterns of pelvic thrusting, and occurrences of a genital lock between the sexes and other features were also addressed in some detail in Chapter 5. There, the conclusion was reached that the evolution of complex patterns, involving single prolonged, or multiple brief, intromissions with pelvic thrusting has occurred due to sexual selection. Such patterns are found almost exclusively in those primates where the females engage in multiple-partner mat-ings. The behavioural specializations exhibited by such males during mating thus correlate with their genital specializations. These are due to sexual selection by sperm competition, cryptic female choice, or a combination of both processes.

Human beings sometimes prolong periods of copulation. However, it is noteworthy that large-scale surveys of human sexual behaviour such as those conducted by Kinsey and his colleagues (1948) have reported that the average time taken by men to reach ejaculation is relatively brief. Likewise, consideration of the anthropological literature leads to the conclusion that techniques for extending the duration of intercourse and delaying ejaculation have to be practised and learned by men and women. Although the acquisition of such techniques may be encouraged in some cultures, they appear not to represent fundamental patterns of human behaviour. On the contrary, men are most likely to reach ejaculation relatively quickly once intromission is attained and pelvic thrusting has been initiated. The phenomenon of premature ejaculation, whereby the male is over-responsive and reaches orgasm quickly, is relatively common, and may have its origin in the evolutionary history of H. sapiens.

Copulatory frequencies vary in primates depending upon their mating systems and the likely occurrence of sperm competition. Thus, ejaculatory frequencies are greatest in males of those species which have multi-male/multi-female mating systems, such as macaques, baboons, and chimpanzees. Polygynous or monogamous species such as gorillas or marmosets copulate much less often. Again, the comparative data indicate that frequencies of human copulation are similar to those of polygy-nous or monogamous non-human primates (see Table 5.4). Moreover, men's sperm counts decline rapidly as a result of repeated ejaculations, a further indication of the limited human capacity to produce and store sperm.

It has been proposed that despite these limited capacities, men might engage in prudent allocation of sperm numbers in the ejaculate, and that this might be adaptive in terms of human sperm competition (Pound et al. 2006). Prudent allocation of sperm has been demonstrated in domestic fowl, for example, in which cockerels ejaculate greater numbers of sperm if paired with a new hen (the 'Coolidge effect') or one with a larger comb on the head (females with larger combs have greater reproductive success: Pizzari et al. 2003). Some experiments have shown that men also ejaculate larger numbers of sperm under particular circumstances. This occurs, for example, if men are separated from their partners for long periods (Baker and Bellis 1989), or if stimulation is heightened during prolonged bouts of masturbation (Pound et al. 2002). It is not the experimental results which I find problematic in these studies, so much as the interpretation that these effects must necessarily reflect adaptations for sperm competition in human beings. As an alternative, I suggest that male vertebrates may share a fundamental physiological capacity to increase sperm numbers in the ejaculate in response to situations which heighten sexual arousal (e.g. the presence of a highly attractive female, or the sight of other conspecifics mating). It may be these very capacities which sexual selection acts upon in species, such as the domestic fowl, where males commonly mate with multiple partners and prudent sperm allocation becomes adaptive in order to maximize fertility.

Taken as a whole, the results of research on comparative reproductive anatomy, physiology, and copulatory patterns indicate that H. sapiens was originally polygynous or monogamous (or both), and did not arise from forms which had a multi-male/multi-female mating system. Current knowledge of reproductive anatomy and physiology does not allow a distinction to be drawn between the relative contributions made by polygyny or monogamy to the remote origins of human mating systems. It is possible that further fine-grained analyses of sperm biology, the functions of the accessory reproductive organs, and penile morphology might reveal differences between polygynous and monogamous primate species. However, it is much more productive, when seeking a solution to this problem, to consider comparative studies of sexually dimorphic traits in physique and secondary sexual adornments. These topics were covered in Chapters 7 and 8, which revisit some of the ground covered by Darwin (1871), in order to reassess matters in the light of modern advances in the fields of anthropology and evolutionary psychology.

In a wide range of human populations, men are, on average, heavier and taller than women. Although sexual dimorphism is not as pronounced in Homo sapiens as in polygynous non-human primate species, its significance becomes clearer when sex differences in body composition, as well as body size are taken into account. Women have much larger reserves of body fat than men (Clarys et al. 1984; Pond 1998).These play essential roles in fuelling reproductive processes, and especially the enormous energetic demands posed by pregnancy and lactation. Men, by contrast, are considerably more muscular and physically stronger than women, traits which were probably favoured by both natural and sexual selection from the earliest phases of the evolution of the genus Homo in Africa. The ratio of adult male/female muscle mass is 1.5 in modern human beings, and this is similar to the sexual dimorphism in overall body mass exhibited among non-human primates which have polygy-nous mating systems. The occurrence of sexual bi-maturism in human beings, with earlier growth and reproductive development taking place at puberty in the female sex, also resembles the situation found in those anthropoid primates which display significant sexual (body size) dimorphism in adulthood.

Success in hunting, and especially in endurance running and persistence hunting, as well as intermale competition may have favoured the evolution of masculine physical traits required for survival (Bramble and Lieberman 2004). In all probability, these developments took place relatively early in the evolution of the genus Homo, for instance, in H. ergaster and H. erectus which lacked the degree of cerebral development and hunting technology achieved by H. sapiens. Then, as now, it is surmised that males provided resources as well as protection for their female partners and offspring. It is interesting, therefore, that women in a variety of cultures rate images of men with muscular (mesomorphic) or average somatotypes as most attractive. The ideal form may lie somewhere between the average and the mesomorphic male physique. A muscular male torso, with broad shoulders and a narrow waist and hips, is often preferred. Images of very slim men (ectomorphs) tend to be assessed as somewhat less attractive, whilst heavily built (endomorphic) males receive consistently low ratings in cross-cultural studies (see Figure 7.7).

Fat deposition during puberty and adolescence is markedly sexually dimorphic in human beings. It is during this time that young women develop larger fat deposits than young men in their buttocks, thighs, and breasts. Fat deposition and distribution is under oestrogenic control, and it is indicative of female health and reproductive potential. Evidence leading to these conclusions was reviewed in Chapter 7, in relation to Singh's theory concerning evolution of the hourglass figure and female sexual attractiveness. Cross-cultural evidence indicates that a low female waist-to-hip ratio (WHR) is perceived as attractive by men, who prefer female images in which the WHR falls somewhere in the range between 0.6 and 0.8, depending upon the population considered (see Figures 7.9 and 7.10). Women with narrow waists and large breasts have significantly higher levels of oestrogen during their menstrual cycles (Jasienska et al. 2004). By contrast, women with high WHRs and more obese physiques are at greater risk of diabetic and other health problems (Singh 2002; 2006). Although female body mass index (BMI) has been suggested to play a more important role than WHR in men's judgements of women's attractiveness, it appears that female shape is the crucial cue (see Figure 7.12). Female WHR may provide males with a first pass filter when assessing a prospective partner.

A word of caution is required about defining any single trait as being decisive in judgements of sexual attractiveness, as they impact human mate choice. Meston and Buss (2007) record that men and women express no less than 237 possible reasons for having sex. Factors which influence mating decisions are clearly complex, and attractiveness is likely to involve an amalgam of traits, some of them physical and others linked to behaviour and personality. Buss (1989) has made this point comprehensively in his reports concerning cross-cultural norms of mate choice. He stresses both the similarities and differences in mate preference displayed by men and women around the world:

Both sexes wanted mates who were kind, understanding, intelligent, healthy and dependable.

However

Women more than men in all 37 cultures valued potential mates with good financial prospects. Men more than women across the globe placed a premium on youth and physical attractiveness, two hypothesized correlates of fertility and reproductive value.

When we consider the remote origins of human mating preferences, including the effects of selection prior to the evolution of language, and of sophisticated cognitive assessments concerning personality, then judgements of physical traits indicative of female reproductive potential and of masculine status and health were probably of paramount importance. This is the case in the non-human primates, as well as in other animals. Human beings are the descendents of non-human primate ancestors. Deeply implanted in the human psyche, therefore, is the tendency to respond to physical traits displayed by the opposite sex when making initial decisions about attractiveness. Although such initial filtering may not always dictate ultimate decisions about mate choice, it is probable that even in modern societies it continues to exert important effects. Further, such filtering of first impressions concerning members of the opposite sex may be very subtle indeed, and involve subliminal processing, which is not necessarily verbalized in discussions (or when answering questionnaire surveys). Hence the reference to the significance of love at first sight, not love at first discussion at the beginning of Chapter 7.

A wide range of cues involving the body, face, skin and hair, as well patterns of movement, vocal and olfactory stimuli, combine in ways which are still not fully understood, to produce individual variations in attractiveness. Many of these traits relate to underlying qualities of physiology, and may provide men and women with clues about the likely health, endocrine status, and developmental history of prospective partners. It is remarkable, for example, that women who have higher levels of oestrogen during the follicular phases of their menstrual cycles are consistently rated as being facially more attractive (Law-Smith et al. 2006). The quality of the skin and the female complexion may be relevant here, as well as differences in other facial traits which are affected by hormones (see Figure 7.17). The reduction of hair on the body and face, which occurred during human evolution, for reasons that are still debated (Jablonski 2006; Rantala 2007), provided further avenues for sexual selection to operate, as the exposed areas of skin vary with age, sex, health, and reproductive status. The significance of sex differences in skin colour, noted originally by Darwin (1871), still remains enigmatic, although there is a little evidence that lighter feminine skin tones are rated as more attractive by men in some cultures (see Figure 7.15). This question is still unresolved, however, as is the significance of sex differences in other cutaneous features. Men, for example, have more body hair than women, although the expression of this trait varies tremendously between populations, as does the development of facial hair. It is interesting that masculine trunk hair is rated as being unattractive by women in some countries (Figure 7.21) although most of the available information concerns the preferences of younger subjects, and it would be important to obtain data from older age groups.

Darwin considered that the origin of the human beard might reside in its attractiveness to women.

However, there has been relatively little detailed experimental or cross-cultural work conducted on the significance of masculine facial hair. The origins of the human beard, whether via inter-sexual selection (via attractiveness) or intra-sexual selection in relation to status and dominance, are still unclear. It may be significant that beard growth accentuates the appearance of another masculine trait: the larger size and length of the lower face and jaw (Barber 1995). Because beard growth is stimulated by testosterone, it could provide yet another potential cue concerning physical maturity and reproductive condition. It may be a very ancient trait indeed, representing part of a suite of specializations inherited from australopithecines, or the earliest members of the genus Homo. Although Darwin drew attention to the occurrence of beards in some non-human primates, the degree of homology is questionable. This is because growth of human facial hair, like pubic hair, is stimulated by testosterone, and the hair is morphologically distinct from that which occurs elsewhere on the head or body. The beards of non-human primates such as orangutans or mandrills are not morphologically differentiated to the same degree as the human beard and, to the best of my knowledge, there is no experimental evidence that their growth is stimulated by testosterone. The peculiar nature of the human beard and pubic hair may relate to their evolution as conspicuous visual signals in ancestral forms where hair was lost on adjacent areas of the face and body. Thus, these traits may have arisen very early in the genus Homo, and may have accompanied the overall reduction of body hair in H. ergaster and H. erectus.

Whatever the functions of these cutaneous specializations in human beings may be, it is clear that the degree of expression of such secondary sexual traits in human males (beard, male pattern baldness, and body hair) is commensurate with that which occurs in polygynous non-human primates. Comparative studies of visually striking, secondary sexual traits in male monkeys, apes, and humans (see Figure 7.19) strengthen the view that polygyny has played a significant role during the origins of human sexuality.

This conclusion is also reinforced when sex differences in the structure of the larynx and vocalizations are compared among the anthropoid primates. This topic was addressed in Chapter 8. Men have larger larnyges, longer vocal cords, and deeper voices than women. Further, there is evidence that women rate the lower pitch of the male voice as pleasant and attractive, and that men may lower the pitch of the voice in situations involving social dominance (Bruckert et al. 2006; Puts et al. 2006). Testosterone stimulates laryngeal growth in boys when they reach puberty, and there is a positive relationship between masculine testosterone levels and vocal pitch in adulthood (Dabbs and Malinger 1999). Comparisons of sexual dimorphism of the larynx and its associated structures in the non-human primates show that such differences are greatest in polygynous species, less marked in forms with multi-male/multi-female mating systems, and minimal or absent in monogamous species (see Figure 8.9). It is among the polygynous non-human primates that the most sexually dimorphic and low-pitched calls are given by adult males, especially in those species that inhabit rainforest. The enlargement of the larynx and deep voice of the human male is also likely to represent another ancient trait, derived from early ancestral forms among australo-pithecines which were polygynous in their mating behaviour.

All these observations lead to the prediction that, as further fossil evidence accumulates regarding the question of body size in early hominids, it may confirm that the direct ancestors of the genus Homo were indeed markedly sexually dimorphic, as is consistent with sexual selection via inter-male competition within polygynous mating systems.

A major question concerns the nature of social organization and group composition in ancestral hominids. Recently Chapais (2008) has produced a most scholarly review and analysis of the origins of kinship and pair bonding in human evolution. He points out that kinship is important in many nonhuman primates, and that homologues of these processes would have existed also in early hominids. Thus, monkeys such as the macaques and baboons exhibit strong matrilineal social bonds. Mating between mothers and offspring, or between brothers and sisters is very rare, as in Barbary macaques (Kuester, Paul, and Arnemann 1994), or chimpanzees (Goodall 1986). This is the non-human primate equivalent of what is called an incest taboo and

Gorilla

Chimpanzee

Bonobo

Human

Gorilla

Chimpanzee

Bonobo

Human

Figure 9.1 Hypothetical stages In the evolution of the mating systems of humans and the African apes. ■ = multi-male/multi-female mating system (males are philopatric). □ = Polygynous, one-male unit. In the gorilla, individual units are spatially separate. In australopithecines ancestral to Homo, groups consisted of a number of polygynous units. □ = monogamy. Ancestral human groups were made up of monogamous pairs, together with smaller numbers of polygynous units.

Figure 9.1 Hypothetical stages In the evolution of the mating systems of humans and the African apes. ■ = multi-male/multi-female mating system (males are philopatric). □ = Polygynous, one-male unit. In the gorilla, individual units are spatially separate. In australopithecines ancestral to Homo, groups consisted of a number of polygynous units. □ = monogamy. Ancestral human groups were made up of monogamous pairs, together with smaller numbers of polygynous units.

probably preceded its cultural elaboration in human beings. Long-term familiarity between female apes or monkeys and their offspring ('uterine kin' as defined by Chapais) reduces sexual attractiveness and discourages the likelihood of copulation. These observations of non-human primates provide parallels with Westermarck's hypothesis, by which he sought to explain lack of sexual attraction due to familiarity between close relatives in humans (as reviewed in Dixson 1998a). Among most non-human primates, however, there is no evidence that fathers recognize their offspring, or vice versa, so that the likelihood of incestuous matings cannot be inhibited by social familiarity in these cases. Chapais (2008) stresses that the chimpanzee and the bonobo are unusual among extant anthropoids in that their multi-male/multi-female social groups exhibit male philopatry. Thus, unlike most Old World monkeys, male chimpanzees and bonobos remain in their natal groups, whilst females emigrate as they mature and join neighbouring communities in order to reproduce. Wrangham (1987) has proposed that this form of male philopatry is a primitive trait among African apes, and would likely have occurred also in the earliest hominids. Indeed, even in the gorilla, females transfer out of their natal groups at maturity, whilst males may either leave and become lone silverbacks, or remain in their natal groups until they achieve alpha breeding status (Harcourt and Stewart 2007).

These arguments lead Chapais to propose that the common ancestor of Pan and Homo probably formed large multi-male/multi-female groups, in which males were philopatric, and females emigrated at sexual maturity. Polygyny emerged later, in the hominid line, and in forms which were ancestral to human beings. Chimpanzees, by contrast, retained a multi-male/multi-female social organization and mating system, in which sperm competition has been a major driving force (Figure 9.1). It is important to consider the mechanism by which polgyny might have developed in those australop-ithecines which gave rise to the genus Homo. Here Chapais posits (and I concur) that spatially separate one male units (as in gorillas) were much less likely to have been involved. It is more parsimonious to suggest that a group structure containing numbers of adults of both sexes would have been retained. In various African and Asian monkeys, polygynous one-male units are nested within much larger social groups, which probably derive from multi-male/ multi-female social groups in evolutionary terms (e.g. Papio hamadryas, Theropithecus gelada, Nasalis larvatus, Rhinopithecus roxellana). Thus, in the homi-nid case, polygyny may have developed due to enhanced male mate guarding of a small number of partners within multi-male/multi-female social groups. This development would have been present in the australopithecine precursors of the genus Homo. Under these conditions, intra-sexual selection would have favoured the evolution of sexual size dimorphism, as is posited to have occurred (on the basis of limited fossil evidence) in various australopithecine species. From this condition, as Chapais points out, the transition to mixed monogamy/polygyny in bands of early Homo would have required only a reduction in numbers of females associated with each male. Monogamous pair bonds gradually replaced polygyny as the prevalent mating system (Figure 9.1).

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