Glance at the Terrain

'There is a gift of being able to see at a glance What prospects are offered by the terrain.'

Napoleon

'We see nothing till we truly understand it.'

John Constable

The purpose of these essays is to explore the evolutionary origins of human mating systems, the physical determinants of sexual attractiveness, mate choice, and patterns of copulatory behaviour. These are ambitious goals, given that sexual behaviour does not leave a fossil record.

We are all the products of an unbroken chain of sexual and reproductive events, extending back through time, to connect present generations with the ancestors of Homo sapiens and with human origins in Africa, more than 195,000 years ago. From such remote beginnings, and from small numbers, our populations have expanded across the globe, to exceed 6 billion people by the start of the present millennium. The most worrying graph ever drawn in biology may be that which depicts the growth of human numbers. I say this because, during my own lifetime, the population of the world has more than doubled. The overall biodiversity of the earth has, in consequence, declined, due to human activities which are now seriously fuelling global warming and climate change. It has been predicted that this catastrophic growth in human numbers may slow by 2050, to plateau at approximately 9.5 billion people. Even assuming that such demographic projections are accurate, and there is no assurance that they are, many of our descendents will find that life upon this population 'plateau' is far from pleasant. For, lacking access to clean water, adequate food, and medical care, let alone the benefits of a decent education, existence for billions of people will continue to be, in the words of Hobbs, 'nasty, brutish and short'.

The great geneticist Theodosius Dobzhansky famously commented that 'nothing in biology makes sense except in the light of evolution.' Thus, apart from its intrinsic interest, some attempt to understand the origins and nature of human sexuality is important, as it may provide a useful basis for consideration of current problems associated with human reproduction. Darwin's (1859; 1871) discoveries, concerning the laws of natural and sexual selection, by which evolution operates, paved the way for advances in every field of biology. His studies of intra-sexual and inter-sexual selection in animals led him to propose that these same processes had also shaped the evolution of various sexually dimorphic traits in human beings. He was intrigued by differences in the physique and facial and secondary sexual traits displayed by different human populations, and speculated as to whether sexual selection had influenced these variations. Both Charles Darwin and Thomas Henry Huxley (1863) also deduced that the great apes represent our closest relatives among the extant primates. For Darwin, the African apes were especially important in this context. He reasoned that humans had originated in Africa. These were remarkable insights since, at that time, there was no fossil evidence of human evolution in Africa and information about primate behaviour was largely anecdotal in nature. The only fossil hominids known to Darwin were a few Neanderthal specimens. Contrary to popular belief, fossil evidence played very little part in the pioneering work of Darwin and Huxley on human evolution. No formal science of genetics existed except for Mendel's pioneering work using pea plants, which remained largely unknown to his contemporaries. The scientific study of reproductive physiology and human sexuality was, likewise, still in its infancy. Indeed, Darwin's (1871) contributions regarding sexual selection and human evolution were largely neglected until many years after his death.

This book, in large measure, pays homage to Charles Darwin's early insights into the nature of sexual selection and its impact upon human evolution. However, for modern biologists who seek to understand the origins of human sexual behaviour, the intellectual 'terrain' now offers many advantages and a depth of understanding which was not available to Darwin.

1. A much more substantial fossil record of human evolution now exists, both as regards early hominids in Africa (such as the australopithecines) and the subsequent evolution of the genus Homo, in Africa and beyond. The fossil evidence of human evolution will be addressed below. Although these fossils cannot convey direct information concerning sexual behaviour, they provide an essential basis for understanding the origins of distinctive human traits such as bipedalism and large brain size. As we shall see in a moment, information about the degree of sexual dimorphism in fossil hominids is also potentially valuable for understanding their mating systems. For example, marked body size dimorphism is associated with effects of sexual selection via inter-male competition, and is characteristic of polygynous mammals, such as the gorilla. A controversial question concerns the existence and degree of such sexual dimorphism among the various fossil hominids.

2. Genetic studies have confirmed the close phylogenetic relationship between H. sapiens and the African apes. The pioneering work of Allan Wilson and his colleagues, carried out at Berkeley during the 1960s (Sarich and Wilson 1967; Wilson and Sarich 1969), employed calculations of DNA

mutation rates to calibrate a 'molecular clock', which was used to time the evolutionary divergence between human and chimpanzee ancestors at some point between 5 and 4 million years ago (MYa). Forms which were ancestral to the gorilla diverged somewhat earlier. Modern research places the time of divergence between chimpanzee and human ancestors at around 8 million years, whilst fossil evidence of a possible ancestor of the gorilla has been discovered in Ethiopia, and dated at 10 million years (Suwa et al. 2007). Human population genetics has also clarified that anatomically modern H. sapiens most likely originated in Africa, and that all of us are the descendents of African ancestors, rather than representing the products of 'multiregional' evolution from H. erectus populations in different parts of the world (Stringer 2002; Manica et al. 2007; Behar et al. 2008).

3. A huge amount is now known about the sexual and social lives of the nonhuman primates (Smuts et al. 1987; Dixson 1998a; Jones 2003; Kappeler and Van Schaik 2004; Campbell et al. 2007), so that a rich source of comparative information is available to help place human sexual behaviour and mating systems in an evolutionary perspective.

4. Darwin considered that sexual selection operates primarily at the pre-copulatory level, via intermale competition, for greater access to females, and via inter-sexual selection to enhance attractiveness to the opposite sex. However, it is now appreciated that sexual selection also occurs at copulatory and post-copulatory levels. Females of many species mate with multiple partners, resulting in the potential for sperm competition (Parker 1970) and cryptic female choice (Eberhard 1985, 1996) to profoundly influence reproductive success. Sexual selection has affected the structure and functions of the genitalia in both sexes. Comparative studies of the anatomy and physiology of the reproductive organs as well as detailed analyses of copulatory behaviour have much to tell us about the evolution of human reproduction.

5. To this array of evolutionary tools, we may add insights gained from cross-cultural, anthropological studies of sexual behaviour and reproduction (Ford and Beach 1951; Betzig, Borgerhoff Mulder, and Turke 1988; Betzig 1997; Ellison 2001), from research in evolutionary psychology, as it relates to human sexuality (Symons 1979; Daly and Wilson 1983; Buss 1994; 2005; Barrett, Dunbar, and Lycett 2002; Kauth 2006), and from the vast medical literature on human sexuality and reproduction (Johnson and Everitt 1988; Bancroft 1989; Knobil and Neill 1994; Le Vay and Valente 2002; Piñón 2002).

Given all these potential sources of information, and the huge scope offered by the subject of human sexuality, it will be helpful to define not only the goals, but also the limits of the current exercise. As Darwin correctly deduced, humans evolved from non-human primate ancestors, ape-like creatures which Foley (1995) has aptly called 'Humans before Humanity'. Darwin (1871) noted that, despite all his exalted powers 'Man still bears in his bodily frame the indelible stamp of his lowly origin.' Therefore, any serious attempt to understand the 'origins' of human sexuality must take account of traits that derive from earlier periods of evolution, as well as those traits which are more distinctively 'human'. Thus, in what follows, the goal is to examine how in ancestral hominids, lacking language and having smaller brains and less developed intellectual capacities than ourselves, the conditions were created for the emergence of human patterns of mate choice and copulatory behaviour. In order to attain this goal, I shall rely heavily upon insights gained from comparative studies of the anatomy and reproductive biology of extant primates. Effects of sexual selection upon the evolution of the primary genitalia and patterns of copulatory behaviour in both sexes are explored in Chapters 2-5. The evolution of sexual behaviour in relation to the menstrual cycle is considered in Chapter 6. Chapters 7 and 8 deal with the origins of sexually dimorphic traits in H. sapiens, and the role played by sexual dimorphism in bodily and facial cues in relation to sexual attractiveness and mate choice. The origins of human kinship systems, incest avoidance, and pair bonding have recently been analysed by Chapais (2008). His findings are incorporated into Chapter 9, which presents an overview, and conclusions, based upon the previous eight chapters.

Before entering upon this task, however, some introductory remarks are essential, concerning hominid palaeontology and the fossil evidence of human evolution.

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