AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 57:94–118 (2013)

Evolution and Human Sexuality Peter B. Gray* Department of Anthropology, University of Nevada, Las Vegas, Las Vegas, NV 89154-5003 KEY WORDS evolution; sexual behavior; sexual function; sexual selection; hominin; Homo; life course; life history; genetics; neuroendocrine; polygyny ABSTRACT The aim of this review is to put core features of human sexuality in an evolutionary light. Toward that end, I address five topics concerning the evolution of human sexuality. First, I address theoretical foundations, including recent critiques and developments. While much traces back to Darwin and his view of sexual selection, more recent work helps refine the theoretical bases to sex differences and life history allocations to mating effort. Second, I consider central models attempting to specify the phylogenetic details regarding how hominin sexuality might have changed, with most of those models honing in on transitions from a possible chimpanzee-like ancestor to the slightly polygynous and long-term bonded sociosexual partnerships observed among most recently studied hunter-gatherers. Third, I address recent genetic and physiological data contributing to a refined understanding of human sex-

uality. As examples, the availability of rapidly increasing genomic information aids comparative approaches to discern signals of selection in sexuality-related phenotypes, and neuroendocrine studies of human responses to sexual stimuli provide insight into homologous and derived mechanisms. Fourth, I consider some of the most recent, large, and rigorous studies of human sexuality. These provide insights into sexual behavior across other national samples and on the Internet. Fifth, I discuss the relevance of a life course perspective to understanding the evolution of human sexuality. Most research on the evolution of human sexuality focuses on young adults. Yet humans are sexual beings from gestation to death, albeit in different ways across the life course, and in ways that can be theoretically couched within life history theory. Am J Phys Anthropol 57:94–118, 2013. VC 2013 Wiley Periodicals, Inc.

The aim of this review is to put core features of human sexuality in an integrative, evolutionary light. Given the central importance of sexuality to the evolutionary imperative—reproductive success—there is strong theoretical impetus for understanding how evolution has shaped human sexuality in the past, and for how the influence of past selective forces continue to manifest in the present. For biological anthropologists, interdisciplinary social and biomedical scientists, and even wider audiences, questions about human sexuality can be among the most compelling and meaningful, another reason to try informing answers to fundamental questions of human sexuality with the most scientifically supported and current views. An understanding of human sexuality is central to topics as diverse as predicting the dynamics of a sexually transmitted infection (STI) outbreak to the reasons why people pour so much of their time and resources into mating effort. Human sexuality, as much as any other topical focus within biological anthropology, warrants ongoing evolutionary scrutiny. For several reasons, this is arguably an opportune time for providing a current overview of the evolution of human sexuality. For one, many of the foundational theoretical and empirical touchstones in biological anthropology that focus on the evolution of human sexuality are dated. Darwin’s (1871) seminal contributions continue to shape our thinking regarding sexual selection, sex differences, and evolutionary models of human mating. So too do important contributions from the 1970s and 1980s such as Symons (1979) Evolution of Human Sexuality and Hrdy’s (1981) The Woman that Never Evolved. Of more recent and prominent works focused on the evolution of human sexuality, however, many draw heavily from evolutionary psychology, such as

David Buss’ (2003) The Evolution of Desire. The field can benefit from a current overview of the evolution of human sexuality that integrates many of the disparate strands of work and that helps orient ongoing scholarship. If the field does not do this, others will fill that gap, leaving open the potential for best-selling but theoretically and empirically distorted works such as Ryan and Jetha’s (2010) Sex at Dawn to shape how people think human sexuality evolved. A second reason for a review is new theoretical and empirical work on the evolution of human sexuality. The theoretical foundations to sex differences in mating effort, for example, can also reflect demographic factors that had been less appreciated in previous theoretical formulations. New data from neuroimaging, hormonal studies, and genetics and genomics contribute to an enriched understanding of the mechanisms of human sexual behavior. The availability of more recent sex survey data drawing upon large, international, and even Internet-based content helps provide new insights into the patterning of human mating and interest in sexual stimuli. How these new lines of evidence fit with other lines of evidence and evolutionary theory is worthy of investigation. New theory and data could potentially transform, or slightly modify, or even affirm earlier perspectives regarding the evolutionary foundations of

Ó 2013 WILEY PERIODICALS, INC.

*Correspondence to: Peter B. Gray; Department of Anthropology, University of Nevada, Las Vegas, 4505 Maryland Parkway, Box 455003, Las Vegas, NV 89154-5003. E-mail: [email protected] DOI: 10.1002/ajpa.22394 Published online in Wiley Online Library (wileyonlinelibrary.com).

EVOLUTION AND HUMAN SEXUALITY human sexuality. As the lead author of a (2013) book— Evolution and Human Sexual Behavior—that was designed to be integrative, accessible, and current, I bring to this review insights from that work; a major reason why I coauthored that book was to fill a perceived need for a resource that pulled together all of these strands under one cover for teaching and wider scholarly purposes. In the following review, I address five topics concerning the evolution of human sexuality. These are theoretical foundations, models of hominin sexuality, recent genetic and physiological data, recent large and rigorous studies of human sexual behavior, and the relevance of a life course perspective to human sexuality. These topics do not exhaust the evolutionary-informed scope of human sexuality. However, these are areas in which there have been updated theoretical contributions and arguably considerable empirical advances, making this a good time to focus on them. The present review can also serve as a touchstone to continued interdisciplinary debates concerning evolution and human sexuality. In the course of this review, I also highlight hot areas for scholarly focus; to forecast two examples, the genetic basis to hominin shifts in sexuality remains poorly specified, and juvenile sexuality has been understudied relative to that of young nulliparous adults.

THEORETICAL FOUNDATIONS OF HUMAN SEXUALITY The classics: Darwin, Bateman, Trivers, and Clutton-Brock and Parker Like so many aspects of evolutionary theory, we begin the discussion of the evolutionary foundations of human sexuality with Charles Darwin. His (1871) The Descent of Man, and Selection in Relation to Sex advanced the concept of sexual selection, along with emphases on intrasexual (competition within members of the same sex) and intersexual selection (competition and coordination between the sexes). To account for traits such as the peacock’s train, Darwin suggested that even if a trait might have apparent survival costs, it could still be favored by selection if it enhanced mating success. Darwin catalogued many examples, and emphasized roles of male–male competition and female choice as the processes of sexual selection giving rise to many differences between the sexes (or sexual dimorphisms), such as the large antlers of many male deer. Angus Bateman (1948) conducted classic experiments with captive fruit flies. He ran a number of trials in which he mixed multiple females and males together in glass jars to determine patterns of mating and reproductive success. He found that males had higher variance in reproductive success than females. He also found that the number of mates appeared to mediate sex differences in reproductive output. For trials 5 and 6 in his experiments, females had similar reproductive success whether they had mated with one, two, or three males, whereas males had more offspring the more mates they had. Trials 1–4 also showed, however, that females appeared to have higher reproductive output if mating with two males, although that finding garnered less attention. Overall, Bateman’s observations were consistent with the idea that the ultimate constraint on female reproductive success tends to be access to sufficient resources like food, whereas for males the ultimate constraint on

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reproductive success tends to be access to reproductive females. Bateman suggested the sex differences in reproductive constraint originated with sex differences in gamete size, with females having the larger, more sessile gametes, and males more mobile and smaller gametes. Robert Trivers (1972) suggested that relative parental investment was a more meaningful factor than gamete size in accounting for sex differences in reproductive constraint. If females provide more parental investment than males, as during gestation and lactation among placental mammals, then females will be the reproductively limiting sex. Accordingly, females will be careful to exert choice, and males to compete among themselves for access to females. In sex role reversal species, by contrast, males providing more parental care can become the choosier sex over whom females compete. Among jacanas and phalaropes, for example, males provide more parental care, and females are larger and more colorful (see, e.g., Reynolds, 1987). However, Clutton-Brock and Parker (1991) pointed out exceptions to Trivers’ framework such as mouthbrooding frogs, in which males might provide more parental care than females, and yet females were nonetheless the reproductively limiting sex. They also pointed out the difficulties of measuring relative parental investment. Clutton-Brock and Parker (1991) thus advocated for basing sex differences with respect to potential reproductive rates: if females have slower reproductive rates than males within a species, then females will exert more choice, and males exhibit more intrasexual competition. Considerable bodies of empirical work on nonhuman animals (Andersson, 1994) and humans (Geary, 2010) lend support to general expectations of sexual selection theory. As an example, across mammals, male traits that seem to function to enhance intrasexual competition are more common than are such female traits, consistent with theoretical arguments that females tend to be the reproductive limiting sex over which males compete.

Challenges to the classics and greater appreciation for demographic influences These frameworks have been subject to critique, with most debate centering on the methods and interpretation of Bateman’s fruit fly experiments. Gowaty et al., (2012) critiqued Bateman’s methods on statistical grounds, stating that assumptions of the statistical tests used were not met; she also conducted an attempt at replicating his findings, but did not present the data (for related statistical reasons) to determine whether or not she found support for his work. In review of several recent human studies, Brown et al. (2009) found that, consistent with Bateman’s principle (that males will have higher variance in reproductive success than females in species where males exhibit greater mating competition), human males overall did have greater variance in reproductive success than females. However, Brown et al. (2009) also noted that this sex difference was observed in polygynous but not monogamous societies. An evolutionary-guided look at the specific cases also suggests that among hunter-gatherer societies (Aka, !Kung, Ache, Hadza), most of which have low rates of polygyny, males tend to have higher reproductive success than females. In a different review of human studies, which had partial overlap with Brown et al. in the American Journal of Physical Anthropology

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societies sampled, Betzig (2012) also found that males had higher variance in reproductive success than females. Betzig also showed that male reproductive skew was most pronounced in socially stratified intensive agricultural societies such as the Inka. Hanna Kokko and colleagues have also deepened our theoretical understanding of sexuality. She notes that actual, not potential, reproductive rates are what matters. That simple observation reminds us to consider the availability of potential mates (just because males may gain higher reproductive success than females if having more mates does not guarantee that mates are available). Males have lower parental certainty than females, and fewer males tend to reproduce than females, factors that result in males gaining fewer benefits and higher costs to parental care than females (Kokko and Jennions, 2003, 2008a). These processes may account for the origins of as well as positive reinforcement of sex differences in mating and parenting effort. Additionally, however, demographic factors play an important role in specifying the gradient of sexual selection (Kokko and Jennions, 2008b). As an example, if males are subject to greater mortality as a result of mating competition, then that lightens to some degree the mating competition the fewer, surviving males face. Such critiques have not overturned fundamental principles of sexual selection. Kokko’s work refines our theorizing (e.g., to push from sexual selection to parenting rather than from parenting to sexual selection), but ultimately anticipates sex differences in mating and parental care observed in the natural world. Additionally, these kinds of critiques and extensions point to the importance of socioecological context and demography in accounting for species and population differences in sexual selection pressures. In populations with more heavily biased sex ratios toward females, we might expect more female–female competition and enhanced male choice (e.g., Guttentag and Secord, 1983). Research shows that in many primate species, including humans, female reproductive success is highly attuned to variation in energetic factors such as food availability. Indeed, related theoretical models help situate socioecological and demographic considerations: Emlen and Oring (1977) pointed to the importance of resource distributions in accounting for variable mating dynamics, and Mitani et al. (1996) suggested that the operational sex ratio (ratio of breeding males:females) better represented the gradient of sexual selection than the actual adult sex ratio. All said, current sexual selection theory aims to account for the evolutionary past that shaped overarching patterns of sexual selection among species (including humans), as well as inform an understanding of population variation in sexual selection pressures.

Female promiscuity, mate choice, and female–female competition Part of the challenge to principles of sexual selection theory stems from data on female mating patterns. While Darwin and other theoreticians highlighted the relevance of female choice, how that played out in the natural world expanded theoretical imaginations. The advent of genetically based paternity testing among many avian field studies revealed that a sizable and variable fraction of offspring were sired by individuals other than a social partner (Birkhead, 2000). Even though over 90% of avian species tend to be socially American Journal of Physical Anthropology

monogamous (lekking species such as peacocks and turkeys among those exceptions), it became clear that social and sexual relationships were not identical. These observations may have helped raise more questions about the traits females sought in a prospective mate, including how this could give rise to mating with multiple partners (Clutton-Brock and McAuliffe, 2009; Geary, 2010). Across primates, current theorizing suggests female mate choice is oriented toward protection of herself and her offspring. Protection may be useful against would-be predators, but also against would-be harmful males. In species in which females mate with multiple males, such as chimpanzees and rhesus monkeys, Hrdy (1981) has suggested this represents paternity confusion, designed to make all males be kinder toward the female and her offspring. For some species with long-term sociosexual bonds and paternal care, including primarily smallbodied South American owl monkeys, tamarins, and marmosets, females may benefit from male support but evidence is lacking that females use cues of male investment (see Dixson, 2012). Females of various species may also seek to mate with males providing complementary (e.g., in MHC system) or “good” (e.g., beneficial alleles against local infectious disease ecology) genes. Since few primate species have males that provide food resources (some callitrichid monkeys of South America exceptions) or have a sexual division of labor, there are no strong nonhuman primate comparisons of females choosing males based on economic (e.g., food acquisition and provisioning) criteria. Although Darwin emphasized female choice and male– male competition, it is recognized that female–female competition and male choice occur (Low, 2000; Geary, 2010; Stockley and Bro-Jorgensen, 2011). Given that female reproductive success is often closely tied to resources such as food, models of female–female competition, and cooperation feature reproductively relevant resources such as ripe fruits among chimpanzees or resource-bearing males in human agricultural societies. Studies of nonhuman primates reveal that higherranking female social primates may benefit by having more surviving offspring and offspring whose reproductive careers are accelerated; this could be due to preferential food access often available to higher-ranking females (reviewed in Pusey, 2012). At the same time, potential female rank-related variance in female reproductive success should not be oversold; lower-ranking females may engage in alternative foraging strategies, resulting in no net differences in reproductive success, as is also frequently found in primate field studies (Pusey, 2012). In humans, much of the female–female competition literature has highlighted competition over acquiring and maintaining desirable mates (Campbell, 1999; Archer and Coyne, 2005; Geary, 2010). Further, reproductive competition can lead to attempts to channel limited resources toward one’s own rather than another women’s children, as observed with cowife competition (Jankowiak et al., 2005). As for male choice, even in multimale, multifemale species such as chimpanzees or rhesus monkeys, males may still attempt to channel their mating effort toward more desirable females, such as maximally fertile females; less fertile and experienced adolescent females may be relatively shunned as mates, for example (Manson, 2011; Muller et al., 2006). For human resource intensive strategies, males may seek to allocate their limited mating effort toward more desirable mates; that can include preferences for younger

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EVOLUTION AND HUMAN SEXUALITY females of high reproductive value, with whom a man might have multiple children in a long-standing sociosexual relationship, as well as other aspects of attractiveness indicative of health and relationship compatibility.

coercion occurs in part because animals can often fly away from would-be coercive efforts, helped lead to an underappreciation of the importance of sexual coercion to the evolution of human sexuality.

Sperm competition and cryptic female choice Sexual conflict One theme of the evolution of mating strategies is that female and male strategies variably conflict (Chapman et al., 2003). That degree of conflict may be minimized in species and contexts in which females and males form long-term reproductive relationships. If females and males depend upon each other to maximize their reproductive success, then they may exhibit less competition over allocation of resources to offspring or over competition with other possible mates. Conversely, when females and males have markedly different mating strategies, then conflicts between female and male priorities may be more likely. In this vein, an extreme example of sexual conflict is sexually selected infanticide, as observed in several species of one-male polygynous groups such as gorillas and langur monkeys (Hausfater and Hrdy, 1984; Van Schaik and Janson, 2000). A male with a limited social tenure in a polygynous group may seek to kill nursing infants of a mother to accelerate her return to fecundity and the possibility of having offspring with her; for her part, a female with an infant may actively attempt to avoid infanticide by a new male, but if unsuccessful may mate with the new, infanticidal male. Sexual conflicts of interest impact other aspects of sexual selection. Male sexual coercion can constrain female choice (Smuts, 1992; Muller and Wrangham, 2009). Whereas a female might seek to mate with a given male, a different male may benefit by preventing her exercising choice. The empirical data concerning nonhuman primate and human coercion have accumulated, revealing that coercive behavior is more common among male chimpanzees than bonobos, for example. Several phylogenetic and adaptive considerations may also be relevant to the context of human sexual coercion. Terrestrial primates may be more vulnerable to sexual coercion than arboreal primates or birds; the larger body sizes of many terrestrial primates may have been favored in contexts of male–male contest competition (i.e., fighting), but can incidentally or adaptively be used for coercive behavior of females too. In this vein, it has been noted that female assessments of human male secondary sexual characteristics such as muscle mass or voice pitch tend to favor less extreme phenotypes than are favored by males (Yang et al., 2005; Puts, 2010). These data are consistent with sexual conflicts of interest: males might favor more extremes of muscularity in contexts of male–male competition, but females prefer less extremes because male musculature could also be used for coercion. In this vein, it can be noted that whereas Miller (2000) has emphasized the relevance of ancestral female choice as the driver of human behavioral evolution, Puts (2010) contends that experimental and observational data are more compatible with male–male competition serving as the driver of male characteristics such as upper body musculature (males have approximately 60% more upper body lean muscle mass: Lassek and Gaulin, 2009), deepened voices, facial hair, and same-sex physical aggression. It could be that theoretical models of female choice borrowed from the avian world, where less sexual

One of the few areas of sexual science that Darwin apparently did not anticipate was postcopulatory selection. Whereas Darwin’s discussion of sexual selection concerned processes culminating in mating, we now recognize that semen within a female’s reproductive tract continue a dynamic process potentially leading to fertilization. Since Parker’s (1970) seminal studies on insects, theory and empirical research on sperm competition and cryptic female choice has progressed rapidly. From the standpoint of cryptic female choice, the idea is that a female’s anatomy and physiology can impact which sperm among those introduced into her reproductive tract successfully fertilizes her egg (Eberhard, 1996). From the standpoint of sperm competition, if a female mates with multiple males, then the sperm of those males may compete within her reproductive tract to fertilize her egg (Harcourt et al., 1981). Processes of cryptic female choice and/or sperm competition can be disentangled from those of precopulatory choice and competition; in practice, some primate species such as wooly monkeys have extreme sperm competition and minimal contest competition (Strier, 1990), whereas others such as chimpanzees exhibit high degrees of both male–male contest and sperm competition (Dixson, 2012). As we shall see, the physiological and genetic evidence regarding human cryptic female choice and/or sperm competition point toward low sperm competition pressures among our recent ancestors (Dixson, 2009).

Summary While theoretical foundations underlying the evolution of human sexuality trace to Darwin, more recent scholars such as Bateman, Trivers, Clutton-Brock and Parker, and Kokko have all elaborated on the basis of sex differences in mating and parenting effort. Contrary to some claims, the discovery of considerable female promiscuity does not undermine the accuracy or relevance of contemporary evolutionary theory. Demographic and socioecological variation are also inherently important. While male–male competition and female choice have garnered, for good reason, primary attention, theoretical and empirical work also focuses on female–female competition and male choice. Sexual conflict is of variable magnitude, but also of importance to mating systems. Competition can occur after copulation, giving rise to sperm competition and cryptic female choice.

EVOLUTIONARY SCENARIOS In speculating on the evolutionary origins of human sexual behavior, Charles Darwin noted, in Sexual Selection, and the Descent of Man, “Humans would probably have lived, as already stated, as polygamists or temporarily as monogamists. Their intercourse, judging from analogy, would not then have been promiscuous. They would, no doubt, have defended their females to the best of their power from enemies of all kinds, and would probably have hunted for their subsistence, as well as for that of their offspring. The most powerful and able males would have succeeded best in the struggle for life American Journal of Physical Anthropology

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and in obtaining attractive females.” Darwin’s observations are consistent with many aspects of contemporary theorizing concerning the evolution of male mating strategies; they leave out female strategies, which can be better elaborated, as we shall see below. In this section, I discuss evolutionary scenarios concerning hominin sexual behavior. Phylogenetic insights are drawn from great ape comparisons, specifics of the hominin fossil and archaeological record, and insights into recently studied human hunter-gatherer societies, with overarching theoretical guidance provided by sexual selection theory and socioecological principles. These scenarios will also later be connected with genetic and physiological data, contemporary international studies of human sexual behavior, and insights drawn from a life course perspective on human sexuality. While there is ongoing debate about specific evolutionary models of hominin sexuality, not surprisingly in light of the limitations of available data, it is also worth underscoring that the models are consistent with these latter bodies of evidence, an indication that there is a coherent and synthetic science here.

Early hominin and australopithecine sexuality Current genetic and fossil evidence suggests that the closest living relatives of humans are chimpanzees and bonobos (Goodman et al., 1998). Genetic data suggest that chimpanzees and bonobos themselves had a last common ancestor in Africa about 1 million years ago (Prufer et al., 2012). Humans had a last common ancestor with chimpanzees and bonobos in Africa around 6 million years ago. What was that ancestor like, and what can we infer about its sexual behavior? As we shall see, there are clues to help answer these questions, but there are also uncertainties. The earliest putative hominin fossils indicate body sizes comparable to today’s chimpanzees and bonobos (Senut et al. 2001; Brunet et al., 2005; Lovejoy, 2009). The finds are all in Africa. The locomotor anatomy suggests the earliest hominins, as well as later gracile and robust australopithecines, were semiterrestrial bipeds. They retained both adaptations for spending time moving in trees (e.g., long finger bones, relatively long arms, and mobile shoulder joint) and for moving bipedally. Most models suggest they moved bipedally on the ground (Lieberman, 2011), although it has also been suggested that bipedalism emerged on tree branches during foraging (Crompton et al., 2008). The environmental reconstructions of early and later pre-Homo hominins suggest they inhabited wooded environments. A few early hominins, such as a find at Chad dated to approximately 7 million years ago, appeared to have slightly larger canine teeth (compared with modern humans, but less than great apes), though generally among hominins canine teeth are reduced in size compared with extant and presumably ancestral great apes. The shift toward greater bipedalism may have relaxed selection on retention of larger canine teeth, particularly among males, for use in male–male contest competition; fighting may have relied, instead, on punching, grappling, or use of weapons. If early hominins were similar to extant great apes, these early hominins likely mated primarily diurnally (see Mitani et al., 2012). Among contemporary chimpanzees, most matings in the wild occur early morning or late afternoon when chimpanzee groups are more fused American Journal of Physical Anthropology

compared with other times across the day when they may be more fissioned (Martin Muller, personal communication). Most sexual behavior was likely in a type of ventral-dorsal position (e.g., males from behind), although bonobos and orangutans are recognized to use a wider array of sexual positions, especially compared with other primates and mammals (Dixson, 2012). Based on great ape comparisons, most matings likely took place on the ground. If early hominin sexuality resembled that of chimpanzees and bonobos, then it would have entailed mating in multimale, multifemale groups. Further, early hominin females might have mated with many males, while also showing preferential mating access to a dominant male around the time she was most fertile. Females might have mated during parts of their pregnancy, but exhibited profound reductions in sexual behavior when in a state of postpartum lactational amenorrhea (i.e., not cycling, but heavily lactating and caring for an infant). Males may have competed heavily through alliance formation and contest competition with other males for social rank, in turn translating higher rank into greater mating success. At this time, it is difficult to discern whether chimpanzees, some other ape such as gorilla, or no extant ape can serve as a strong referential model for early hominin sexuality. Reasons for the lack of clarity include questions whether the multimale, multifemale mating system of chimpanzees and bonobos (and related traits such as exaggerated sexual swellings and heightened evidence of sperm competition) is derived or shared with a common ancestor; over reconstructions of the degree of body size sexual dimorphism among early hominins and australopithecines; and a dearth of relevant genetic analyses that might be able to address the evolutionary polarity of potential shifts in hominin sexuality. Most researchers suggest that australopithecines were more polygynous than members of the genus Homo (McHenry, 1994). Debate continues on the number of gracile australopithecines and their phylogenetic relationship to earlier hominins and later members of Homo (Wood and Lonergan, 2008). However, most reconstructions of the postcranial remains of gracile australopithecines suggest they exhibited greater degrees of body size sexual dimorphism compared with modern humans and most other members of Homo, and possibly even more dimorphism compared with chimpanzees and bonobos (see Plavcan, 2012). The available postcranial remains are scanty, are scattered across time and locations, and entail inferences regarding sex in the first place. Such considerations have led other researchers to question whether australopithecine body size dimorphism estimates were exaggerated. It has been suggested the Aust. africanus might have been less dimorphic than Aust. afarensis (Harmon, 2009). It has also been suggested by Reno et al. (2003) that gracile forms were only mildly dimorphic—comparable with modern humans. If gracile australopithecines were highly dimorphic, the theoretical inference would suggest they mated in one-male polygynous groups, perhaps somewhat similarly to gorillas (Geary and Flinn, 2001). If they were only mildly dimorphic, that suggests, instead, they were mildly polygynous, and perhaps mating in somewhat human-like ways from this earlier time. The robust australopithecines, which most scholars suggest became evolutionary side branches rather than serving as human ancestors, appeared to be highly sexually dimorphic in body size. Aust. robustus, from southern Africa, may have had

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Fig. 1. Socioecological model of hominin sexuality. [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]

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Additionally, dental microstructure studies suggest that the pace of development was more apelike than humanlike (Dean et al., 2001), providing further impetus for seeing grade shifts in Homo as still showing considerable change over time rather than being established quickly with the earliest forms. Estimates of both Neandertal and modern human body size sexual dimorphism suggest about 15% differences in height and weight (see Plavcan, 2012). This would suggest modest degrees of male–male contest competition, consistent with slight polygyny/mostly monogamy. If this pattern held among the common ancestor of Neandertals and modern humans, then presumably similar aspects of sexual behavior held among archaic Homo/Homo heidelbergensis in Africa by about 600,000 years ago. Whether similar patterns can be pushed back to earlier Homo around 1.5 Ma then depends on the issues noted above regarding early Homo/Homo erectus skeletal material.

A socioecological approach to hominin sexuality pronounced sex differences in reproductive maturation, consistent with one-male polygyny (Lockwood et al., 2007), and appeared to exhibit sexually dimorphic craniofacial anatomy, also consistent with some degree of polygyny (Lockwood, 1999). Attempts to draw additional inferences concerning hominin sexuality have used the study of digit ratios (Nelson et al., 2011) and other aspects of craniofacial dimorphism (Schaefer et al., 2004), but without clear inferences. It can also be noted that the penis bone (baculum) and homologous clitoral bone were lost during hominin evolution, a difference consistent with evolutionary changes in our ancestors’ reproductive anatomy (Dixson, 2009).

Sexuality in the genus Homo Most evolutionary models of sexuality in the genus Homo suggest that grade shifts took place during early or middle Homo evolution. The transition from a presumed gracile australopithecine form to early Homo remains murky in phylogenetic and archaeological detail, in part because of a paucity of fossil material during this time frame. Scenarios regarding body size estimates and indices of sexual dimorphism are highly contingent upon availability of new and still-rare fossil specimens. For example, 1990s models suggested that Homo erectus/ ergaster exhibited increases in body size, had lower (human-like) body size sexual dimorphism, and humanlike limb proportions, with much of that inspiration drawn from the Nariokotome boy (KNM-WT-15000) (Walker and Leakey, 1993). More recently, a 1.5-Ma pelvis from Gona has been used to suggest that some females at that time were still small, and thus that body size dimorphism could have remained high, and similar to previous scenarios of highly dimorphic gracile australopithecines (Simpson et al., 2008). The shift toward human-like body proportions (e.g., relatively shorter arms), along with environmental reconstructions, suggests that Homo inhabited a wider array of environments than its woodlands-bound predecessors, and had also become a committed biped (giving up perhaps sleeping in trees at night). Beginning around 1.5 Ma, members of Homo began using new stone tool traditions, marked by the Acheulian (Foley and Gamble, 2009). Estimated brain sizes increased; however, the limited availability of postcranial remains makes adjustment for body size difficult, and probably thus leaves early and mid Homo as less encephalized as later forms.

To orient potential evolutionary models of sexuality in the genus Homo, we can draw upon socioecological principles. See Figure 1 for graphical illustration of a basic socioecological model. Such principles in turn begin with Bateman’s observations and additional layers concerning sex differences in reproductive constraint and reproductive strategy. As Wrangham (1979) noted, if females are ultimately constrained by access to resources such as food, then it makes sense in developing socioecological models of primate social behavior to ask about how females will distribute themselves in an environment with respect to available food resources. Van Schaik (1983) suggests that predation pressures may also serve as major selective forces operating on female distributions. Applied to the transition from a gracile australopithecine to early Homo, the shift toward committed, terrestrial bipedal lifeways might have exposed females to greater predation pressures (in terrestrial compared with arboreal environments). That could favor enhanced female group sizes. The formation of larger female group sizes could amplify female foraging competition. That could fuel intensified female extractive and processing foraging strategies, perhaps including tools used for digging roots (and tools that, incidentally, would not be regularly found in the fossil record, although some microwear studies of stone tools are also consistent with plant processing). If females are in larger groups, then they become more difficult for a single or several males to monopolize. From socioecological first principles, males are expected to map on to the availability of fertile females. With a larger number of males within groups, consequences could be diminished male reproductive skew, and perhaps male–male egalitarian relationships. The presence of multiple males in groups could foster lower-ranking males to attempt to mate guard fertile females, as is sometimes observed in chimpanzees, in which males attempt to coerce females into short-term liaisons removed from other group members. This kind of male mate guarding in Homo could give rise to long-term sociosexual relationships, but within multimale, multifemale groups. One aspect of such modeling is that evolutionary shifts in hominin sexuality are theorized from principles applied to other primates. This is different from emphasizing human-specific arguments. Another aspect of this approach is that it sees social behavioral changes rooted in female foraging and male mate-seeking as the American Journal of Physical Anthropology

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P.B. GRAY TABLE 1. Models of the evolution of sexuality in the genus Homo

Model

Female perspective

Male perspective

Mate guarding (Hawkes, 2004)

No benefit; constrained choice

Aids paternity certainty

Hired Gun (Mesnick, 1997)

Reduced predation and/or coercion by others of self and offspring

Benefit from sexual access in exchange for offering protection

Infanticide avoidance (van Schaik and Dunbar, 1990)

Reduced risk of infanticide if bonded to a protective male

May benefit from sexual access and higher offspring survival

Food-for-sex (Fisher, 1982)

Benefit from food

Benefit from sexual access

Male provisioning (Kaplan et al., 2000)

Gain from food resources in a sexual division of labor

Gain from mating access with a long-term partner within a sexual division of labor

Cooking hypothesis (Wrangham et al., 1999)

Benefit from reduced theft of cooked foods

Gain mating access in exchange for protection

Exchange of mates under parental control (Apostolou, 2007; Chapais, 2008)

Expands social ties and provides a mate, but with potential parent-offspring conflict

Gains expanded social ties and a mate, but with some potential for parent-offspring conflict

foundation, with subsequent layers of hominin economic and social behavior building on these. For example, a pronounced hunter-gatherer sexual division of labor is viewed as a more recent derivative of the preceding shifts in sexuality. Table 1 illustrates some leading models concerning the evolutionary foundations of Homo sexuality, featuring female perspectives, male perspectives, and commentary concerning the possible timing and relevance of each (see also Quinlan, 2008).

Hunter-gatherer sexuality As another source of insight into the evolution of human sexuality, we can draw upon patterns observed among recently studied hunter-gatherers (Berndt and American Journal of Physical Anthropology

Timing and relevance Some relevance across Homo; may have been the original basis of long-term Homo sociosexual partnerships, since in a wider phylogenetic scope male mate guarding is one of the best predictors of social monogamy (Lukas and Clutton-Brock, 2013); female hunter-gatherers favor specific mates and often seek to maintain a bond Some relevance across Homo; while male partners tend to be the most coercive of female partners, those same male partners may also deter additional coercion by other males and have helped reduce predation upon females and their offspring Some relevance if early hominins or Australopithecus lived in one-male groups, in which infanticide risk tends to be higher; little evidence of infanticide risk by unrelated males among huntergatherers May be part of the sex-specific resource exchange within long-term unions and within a sexual division of labor Relevance to recently studied hunter-gatherers, but unlikely to be the starting point of Homo shifts to long-term sociosexual bonds Evidence of regular use of fire/ cooking aligns best with archaic Homo/Homo heidelbergensis; evidence for huntergatherer concern over food theft is lacking; could be consistent with other protective services Relevant to recently studied hunter-gatherers; unlikely to project beyond modern humans given cognitive and demographic constraints underlying mate exchange

Berndt, 1951; Shoskak, 1981; Hewlett and Hewlett, 2010; Marlowe 2010; Walker et al., 2011). Because the socioecology of hunter-gatherers is thought to resemble in some respects (e.g., small group sizes, family relationships) that in which earlier forms of Homo sexuality evolved, hunter-gatherers can serve as analogies for more distant patterns. Of course, recently studied hunter-gatherers are not living fossils; they have different foraging tools than more distant ancestors (e.g., Marlowe, 2005), among other differences. Yet observations and patterns among foragers offer insights that otherwise are not accessible. From recently studied hunter-gatherers, the most common marital system is slight polygyny (Marlowe, 2005; Walker et al., 2011). That is, among foragers, most

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EVOLUTION AND HUMAN SEXUALITY societies allow polygyny, but typically only a few men are married polygynously, with the vast majority of men monogamously partnered. The regional exception is among Australian aborigines, where higher rates of polygynous marriage were observed, but that may be in part due to cultural transmission from New Guinea (see O’Connell and James 2007). Across hunter-gatherers, the men most likely to have two wives tend to have higher status, achieved through hunting success or from shamanic activities (Smith, 2004). Divorce is variably common, especially among younger couples (Blurton Jones et al., 2000; Winking et al., 2007). Marriages, especially first marriages, are often arranged by older family members, although the married partners may have influence on whether those arrangements proceed (Apostolou, 2007). While polyandrous mating systems tend to be rare in mammals generally, including humans, it is occasionally observed among huntergatherers, and typically when there is a shortage of men (Starkweather and Hames, 2012). Affairs also occur, with love triangles (e.g., men competing over a woman) a regular context of competition among foraging societies such as the !Kung and Hadza (Gat, 2006). What other aspects of hunter-gatherer sexuality stand out? A sexual division of labor is observed, whereby females tend to undertake subsistence activities yielding reliable food availability and in ways compatible with having young children (Bliege Bird, 1999; Marlowe, 2007). Males tend to undertake riskier subsistence activities, including foraging for more difficult-to-acquire but highly relished foods such as larger game animals and honey. Foods may be shared between partners, with a female’s provision of reliable resources helping make possible a male’s riskier undertakings. Resources males acquire appear designed to serve multiple ends: partly as provisioning family members, but with the acquisition and sharing of large game also enhancing male status in ways that may yield political benefits or mating opportunities (Marlowe, 2010). It has also been suggested that male resources are most useful during a “critical period” of provisioning a partner who has a young nursling (Marlowe, 2003). Also among hunter-gatherers, females spend the bulk of their reproductive years pregnant or in a state of lactational amenorrhea, meaning that they are nursing but not cycling (Short, 1976; Ellison, 2001). This latter observation has dramatic impacts on the evolutionary foundations of human sexuality: it is comparatively rare for a woman to be cycling, and the true female baseline is one of fluctuations in sexuality across reproductive states. Among foragers, there are also few unattached and fertile females. Individuals are familiar, and frequently off-limits as potential mates because they are close family members or circumscribed for other reasons that may be designed to extend coalitions (e.g., wife exchange). One of the distinguishing features of huntergatherer sexuality (and among humans more generally) compared with other primates is that sex is typically covert. While in some other primates surreptitious matings may take place to reduce same-sex conflict or coercion (e.g., baboons: Smuts 1985), this is a much greater human concern. Ethnographic descriptions include cases of couples having sex at night near a fire, within short distance of children and other campmates (but the poor light providing some cover); in other cases, a couple may seek to have sex during the day away from camp. One interpretation of the pattern of seeking to shield sexual

behavior from the eyes of others is that it may reduce sexual jealousy and mating competition. The unusual human mating pattern of forming long-term sociosexual bonds within multimale, multifemale groups is vulnerable to such competition. This privacy-seeking also contrasts with the sexual behavior of other apes, in which group members often have abilities to witness the sexual behavior of group-mates. Additionally, same-sex sexual behavior has been observed among some, but not all, hunter-gatherer societies (Hewlett and Hewlett, 2010). Few details of forager sexuality across the life course are available: sex play has been reported in several foraging societies, including the !Kung, Hadza, and Aka, while among the Aka older couples have sex less frequently (Hewlett and Hewlett, 2010).

Summary Evidence from other primates, the hominin fossil and archaeological record, and studies of human huntergatherers can be combined with socioecological principles to depict the evolution of hominin sexuality. There are a range of theoretical models to draw upon in this effort, such as models emphasizing the benefits of male protection or care to long-term bond formation. Some reconstructions of early hominin sexuality draw upon comparisons with chimpanzees because they and bonobos are our closest living relatives and the body sizes of early hominins are chimpanzee-sized. However, debate continues whether features of the multimale, multifemale mating system of chimpanzees are derived or shared with an early hominin. Many reconstructions of gracile australopithecine sexuality feature pronounced body size sexual dimorphism, which could be consistent with gorilla-like one-male polygyny; other reconstructions emphasize more modest dimorphism. Most scenarios suggest that body size dimorphism decreased in early or mid Homo evolution, with the inference that these hominins experienced lower male–male contest competition and more socially monogamous long-term bonds. The transition toward slightly polygynous/more monogamous Homo may have originated with changes in female foraging and possibly increased group sizes, attended by male mate guarding. During later Homo, male care, in particularly provisioning, may have arisen, reinforcing benefits such as higher female lifetime reproductive success and male sexual access to forming long-term bonds. Among modern humans, older adults may have taken on greater and evolutionarily novel roles in mate exchange. Across the existence of long-term hominin sociosexual bonds, male protection against harassment by other males may have been relevant, although aspects of the infanticide and cooking models are less supported. Key features of human sexuality thus arose in a mosaic fashion during hominin evolution, with different selective scenarios having relevance at different times.

RECENT GENETIC, GENOMIC AND PHYSIOLOGICAL DATA An explosion of recent data from genetics, genomics, and physiology can inform an understanding of human sexuality. These sources of data can provide tests of evolutionary-based understandings of human sexuality. For example, human and chimpanzee Y chromosomes have diverged rapidly, likely in part due to species differences in mating systems (Hughes et al., 2010). Equally important, an evolutionary perspective can help account American Journal of Physical Anthropology

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for the patterning of genetic data and how proximate mechanisms underpinning romantic and sexual behavior are expressed. Many of the recent physiological data on human sexuality have been generated without explicit evolutionary theorizing and interpretation, even though an understanding of proximate mechanisms and adaptive function are complementary ways to investigate the system (Tinbergen, 1963).

Recent genetic and genomic data related to the evolution of human sexuality From the standpoint of genetics and genomics, several approaches guide the application of new data to evolutionary questions. One is a candidate gene approach, in which tests for signatures of selection are undertaken to determine whether a specific gene thought to be implicated in some aspect of human sexuality shows evidence of this. As an example, the vasopressin 1a receptor (AVPR1a) has been implicated in vertebrate male species- and individual differences in mating and paternal behavior; one report noted that humans and bonobos had a distinct AVPR1a compared with chimpanzees, raising the prospect of this genetic difference serving as a possible contributor to species differences in male social behavior (Hammock and Young, 2005). However, subsequent comparative genomic work has not implicated selection upon this gene during hominin or hominid evolution. Another approach is to study genetic information from other forms, such as herpes or HIV, to infer possible evolutionary-related scenarios regarding sexually transmitted disease. Still another is to draw comparisons of genomic sequences (or even entire genomes rather than a single or several genes) between humans and other species, between human populations, or within individuals of a human population in order to identify genetic differences that might be related to sexually relevant phenotypic differences. In a related vein, quantification of sex-specific genetic contributions to a population can inform an understanding of mating dynamics (e.g., specifying the relative variance in male and female reproductive success: Heyer et al., 2012). As an example, relatively less male genetic variation was found among the Yoruba in Nigeria compared with a Chinese sample, consistent with recognized differences in marital behavior (Labuda et al., 2010). The availability of a draft human genome in 2003, and of the chimpanzee in 2005, has helped fuel interest in the growing field of comparative genomics (Chimpanzee Sequencing and Analysis Consortium, 2005). The availability of orangutan, gorilla, and bonobo genomes now means that the genomes of all great ape species can be compared to discern similarities and differences, and in turn raise questions about the genetic bases to species differences in sexuality. The publication of draft genomes from Neandertal and Denisova extends the comparisons to two extinct and closely related hominins (Disotell, 2012). Given that Neandertals and Denisovans are apparently sister groups, and that modern humans, apart from a small degree of population-specific interbreeding with them, last shared common ancestry with Neandertals and Denisovans around 600,000 years ago, comparisons with these extinct hominins can help shed light on the phylogenetic structure of hominin sexuality. What insights have emerged thus far in such comparisons (O’Bleness et al., 2012)? American Journal of Physical Anthropology

Genetically based insights into the evolution of human sexuality One of the most rapidly evolving regions of the human and these other hominids’ genomes involves male reproductive genes (Clark and Swanson, 2005). Given that the bottom line of evolution is reproductive success, it is not surprising that genes involved in spermatogenesis or semen parameters might be rapidly evolving. As an example, the SEMG1 and SEMG2 genes, thought to aid the coagulation of semen, appear to have undergone a loss of function in gorillas and gibbons (which have low sperm competition pressures), while being subject to adaptive evolution in chimpanzees (which have high sperm competition pressures); “Interestingly, the observation that humans are in a sense intermediate in their rates of seminal protein evolution between chimpanzees and gorillas parallels that of anatomical and physiological correlates of mating systems.” (Carnahan and Jensen-Seamen 2008: 946). However, a wider comparison of the ejaculate components across humans, chimpanzees, bonobos, and gorillas found that effective population size rather than sperm competition pressure appeared to best explain overall species differences in genes expressed in ejaculate (Good et al., 2013). When related analyses compared subsets of genes involved in different ejaculate functions, there was some evidence of enhanced selection on genes involved in immune responses and protease, suggesting different components of the semen may evolve at different rates. Good et al. (2013) also note that the genetic bases underlying species differences in human and African ape male reproductive function may rely more on gene expression than protein differences and that gamete differences may be more important than semen components. Differences between human androgen receptor and that of primates have also been noted (Mubiru et al., 2012). Humans have more CAG repeats in the androgen receptor promoter region than other primates although it is not clear whether the pattern represents phylogenetic inertia or lineage-specific selective effects. A 2011 paper noted a deletion upstream of the human androgen receptor after comparison with other primates including chimpanzee (McLean et al., 2011). In vivo work suggests that the genetic deletion results in loss of penile spines situated on the glans penis. Further, Neandertal has the same version as humans (Hawks, 2011), suggesting this deletion may have occurred among a common ancestor, possibly in association with some derived aspect of hominin mating. As to other genetic insights into hominin sexuality, Gentry et al. (1988) note that oral and genital herpes strains have separated long ago and remained that way, suggesting that oral sex may not have occurred regularly among our ancestors (since those strains of herpes would have merged rather than remained distinct). From a candidate gene approach, some work has investigated potential human between- and withinpopulation genetic differences related to sexually relevant phenotypic differences. Population differences in dopamine receptor (DRD4) genetic polymorphisms exist, with possible explanations advanced to account for those differences including genetic drift, adaptive migration, and mating behavior (Harpending and Cochran, 2002). A U.S. study found that polymorphisms in this same system were associated with differences in sexual promiscuity in a university sample (Garcia et al., 2010).

EVOLUTION AND HUMAN SEXUALITY Individual differences in the oxytocin system, including the oxytocin receptor, have been observed (Prichard et al., 2007). However, these have not been clearly linked with sexuality related phenotypic differences. A Swedish study of AVPR1a polymorphisms identified small differences in male partnering behavior (Walum et al., 2008). Overall, the cases suggesting genetic polymorphisms associated with differences in partnering or sexual behavior have small effect sizes, and as of yet have failed to identify candidate genes playing large potential roles in accounting for the hominin evolutionary shifts in sexuality reconstructed from comparative, fossil, archaeological, and other lines of evidence. Although human mating is expected to entail the expression of many genes, it remains a puzzle why so few genes of even small effect sizes have not been identified as contributing to such behavior.

Neuroendocrine bases of human partnering and sexual behavior How do scholars gain insight into potential physiological contributions to an evolutionary understanding of human sexuality? Much of the inspiration stems from a rapidly growing body of research on the neuroendocrine bases of human partnering and sexual behavior. This body of work, in turn, represents a cross-fertilization with comparative and animal model research. Through recent developments in brain imaging, identification of increased brain activity associated with specific mating stimuli helps reveal brain processes involved in human sociosexuality. The measurement of baseline or reactive hormone concentrations in relation to partnering or sexual behavior also sheds light on the endocrine bases to human sociosexuality. The neuroendocrine system takes in, integrates, and puts out information that helps orient an individual’s anatomy, physiology, and behavior. The way its mechanisms work both constrain and reflect age, sex-, individual-, and context-specific variation in ways that may enhance reproductive success. As an example, pubertal increases in male testosterone levels are bound by tissue-specific androgen receptor in ways that may enhance an individual’s motivation to engage in samesex competition and courtship behavior.

Imaging romance and sex With respect to brain imaging, foundational studies on partnering have been conducted by Bartels and Zeki (2000) and Aron et al. (2005) using fMRI. These kinds of studies typically rely on assessing brain activity in response to subjects looking at photos of, for example, a romantic partner, subtracting out brain activity from control stimuli in order to reveal brain areas of heightened activity. Bartels and Zeki’s (2000) study revealed increased activity in the hypothalamus and ventral tegmental area. Activation of the hypothalamus is of note because of the linkage to potential peripheral hormone release (e.g., release of hormones to reach the pituitary, and in turn throughout the body). These are areas known to be rich in oxytocin and vasopressin receptors and involved in reward pathways, suggesting linkages with these other systems and the positively reinforcing experience of reflecting upon a romantic partner. Furthermore, decreases in brain activity associated with social judgment and negative emotion were also noted. Aron et al.’s (2005) study of romantic love showed both similarities and differences with Bartels and Zeki’s find-

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ings, with differences potentially due to Aron et al.’s subjects reporting higher levels of passionate love for their partners and overall shorter relationship durations compared with the earlier study. The ventral tegmental area also showed heightened activity. Among subjects in longer-term relationships, some areas such as the anterior cingulate cortex were more highly activated. This could suggest development of connections between more emotional and higher cognitive associations with longerterm relationships. In a related study of the brain activity of rejected participants, many of the same brain areas such as the ventral tegmental area were activated as in those subjects in love. However, a few areas were differentially activated too, including parts of the forebrain that have been implicated in drug-use addiction (Fisher et al., 2006). Additionally, Zeki and Romaya (2010) found that patterns of brain activity of subjects in love did not differ depending on sexual orientation, either for males or females. Brain imaging studies relying upon fMRI or PET scanning have also been conducted on women and men engaged in sexual behavior. Such studies typically situate an individual inside of a brain scanner, asking the individual or a partner to stimulate to orgasm. As an example, Beverly Whipple and colleagues have investigated the responses of women with spinal cord injuries to cervical self-stimulation, showing both brain activity associated with the behavior while also implicating the vagus nerve in transmitting genital information to the brain (see Komisaruk and Whipple, 2005). In a PET study enabling direct comparisons between women and men’s brain responses to genital stimulation (by masturbation) and orgasm, Georgiadis et al. (2009) found distinct sex differences during the stimulation phase of the sexual response but similarities between the sexes during the experience of orgasm. As examples, during genital stimulation, men experienced greater deactivation of the right amygdala, greater activation of the right middle temporal gyrus, and women experienced greater activation of the right inferior parietal lobe. During orgasm, by contrast, men and women shared an array of deactivated brain areas such as the left inferior frontal gyrus, while among the few differences women showed more pronounced activity in the right insula. The observation that many brain areas were deactivated during orgasm is itself notable, marking an experience in which individuals are less aware of their wider surroundings. Another observation from such imaging studies is that the brain mechanisms of sexual behavior are distinct from those activated while imagining a romantic partner. This distinction is consistent with other findings that romantic love and sexual behavior can be behaviorally separated too; while someone may both experience romantic passion and sex with the same individual, ethnographic reports note that these can be separated (e.g., when having sex without love, or loving someone without having a sexual relationship: Jankowiak, 2008).

Hormonal bases of partnering and sexual behavior The hormonal bases of partnering have been explored in the U.S., but also a growing number of international settings (van Anders and Gray, 2007; Gray and Campbell, 2009). Drawing upon comparative research, much of the focus has been on oxytocin and male testosterone with respect to partnering, although relations between American Journal of Physical Anthropology

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partnering and other hormones such as cortisol have also been investigated. In one oxytocin study of 38 couples, Grewen et al. (2005) found that blood oxytocin levels were higher throughout a 10 min behavioral session among both women and men reporting greater partner support. In an experimental study in which women and men were either administered intranasal oxytocin (which is known to exert effects in the brain) or intranasal placebo spray, those given oxytocin showed relatively higher ratios of positive to negative partnerdirected behavior during a behavioral interaction session (Ditzen et al., 2009). Studies of both young and older couples’ blood cortisol levels have been conducted in relation to marital discussion, a paradigm in which couples report to a lab and are asked to talk about topics known to elicit conflict (such as sex or finances) (KiecoltGlaser et al., 2003). As one of the main findings from these studies, women in more positive marital relationships had rapidly reduced cortisol profiles during the discussion compared with women in less positive marital relationships (Robles et al., 2006). Among studies investigating male testosterone levels and partnering, nearly all conducted in North America have found that men involved in committed, romantic relationships have lower testosterone levels than their unpartnered counterparts (Gray and Campbell, 2009). A longitudinal study of U.S. military veterans showed that men’s testosterone levels increased after divorce, providing evidence that changes in relationships can precede changes in men’s testosterone levels (Mazur and Michalek, 1998). However, international studies have been less consistent in findings linking men’s testosterone and relationship status. In most international studies, becoming a father in a social context in which men provide paternal care is associated with lower testosterone levels, but a number of studies found no difference in the testosterone levels between partnered and unpartnered childless men. As an example, in a sample of 126 men aged 21–38 in Beijing, fathers had lower testosterone levels than both partnered childless men and single men, with the testosterone levels of partnered men with and without children similar (Gray et al., 2006). A longitudinal study of several hundred men in Cebu City, Philippines, revealed that becoming a father, particularly of infants and associated with greater paternal care, caused men’s testosterone levels to decrease (Gettler et al., 2011). Four studies have also investigated men’s testosterone levels with respect to polygynous marriage. In the first of these, conducted among Swahili men in Kenya, men married to two wives had higher testosterone levels than other men, whether monogamously married or unmarried (Gray, 2003). The interpretation of these and the several other studies suggest that age and social context matter, and it is also difficult to disentangle potential confounding influences such as developmental impacts of diet and physical activity. A growing number of studies have investigated hormonal responses to sexual behavior, with emphasis upon intercourse or solitary masturbation culminating in orgasm. Some of these studies have become more technically feasible with the use of minimally invasive measurement of hormone concentrations from saliva, whereas assessments of peptides typically rely upon blood draws. Some of the effects appear sex-specific, whereas others, involving peptide release, appear similar between females and males. Among males, a considerable literature has tested whether men’s testosterone American Journal of Physical Anthropology

levels acutely increase in response to sexual stimuli (reviewed in Archer, 2006; Van Anders and Watson, 2006). In studies of solitary masturbation, men’s testosterone levels do not consistently change, whereas exposure of men to audiovisual sexual stimuli more reliably increases testosterone levels. In a naturalistic study of men’s testosterone responses conducted at an adult club, men’s testosterone levels increased more when engaging in rather than observing sexual behavior (Escasa et al., 2011). In other studies, among men who masturbated, prolactin levels did not change (Kruger et al., 2003), whereas in men and women who engaged in partnered intercourse their prolactin levels showed acute increases (reviewed in Bancroft, 2005). In both men and women, oxytocin levels tend to increase during sexual behavior; it may be that oxytocin is involved in smooth muscle contraction associated with orgasm as well as the rewarding experience of sexual behavior (Carmichael et al., 1987). Studies have typically found no changes in women’s estradiol, but in some cases increases in women’s testosterone levels during sexual behavior (see Van Anders et al., 2009). Summarizing much of this literature on hormonal responses to sexual behavior, major features of the system are homologous across a wide phylogenetic scope, and both sex similarities and differences have been recognized.

Human reproductive physiology and anatomy in comparative context Closing out this section on physiological data, several recent syntheses warrant attention. One is Alan Dixson’s (2009) compilation of human reproductive physiology and anatomy placed within an explicitly comparative perspective, and the conclusion from multiple lines of evidence that humans bear signatures of low sperm competition pressures. While classic comparative research on relative primate testis size reached a similar conclusion (Harcourt et al., 1981), the earlier work had a human sample size of four individuals from which testicle size was measured in contrast to over 7,000 men in more recent analyses. Dixson summarizes data indicating humans have low sperm quality, ejaculate volume, sperm reserves, modestly sized seminal vesicles, and prostate gland, and relatively small sperm midpiece volume. Human females also have relatively short oviduct length (i.e., Fallopian tube), consistent with relatively low sperm competition pressures. This conclusion is at odds with views espoused in Baker and Bellis (1994) or Ryan and Jetha (2010). The evolutionary significance of population and individual human variation in these and related reproductive physiological and anatomical parameters, however, remains unclear. As examples, differences in human sperm counts (Dixson, 2009) and female vaginal flora (Ravel et al., 2011) have been noted. That variation helps provide a basis on which selection can act, but it is not clear if observed population differences in, for example, testis size can be traced to population-specific selective pressures rather than other evolutionary or developmental processes. The way in which genital responses align (or not) with subjective sexual arousal tends to differ between males and females. Through measurement of vaginal blood flow or penile tumescence in response to exposure to audiovisual stimuli, meta-analysis reveals that women’s responses less consistently align (r 5.26) with subjective reports of arousal compared with men’s responses

EVOLUTION AND HUMAN SEXUALITY (r 5.66) (Chivers et al., 2010). As one extreme illustration, women showed vaginal blood flow responses when watching video of bonobos having sex, even though women reported not being aroused. How can these patterns be situated within larger evolutionary concepts? One interpretation is that a low threshold of female sexual response, particularly vaginal lubrication, can be adaptive because it avoids injuries during coerced or unarousing sex. Another interpretation recognizes that female sexual desire is highly contextualized, helping inform how subjective and objective measures of response can be separated. Still another interpretation could recognize that males tend to have a more proceptive, and females a more receptive sexuality, with the result that it makes more sense for male subjective and objective responses to align to best facilitate the motivation and capacity to engage in sexual behavior, while females can respond sexually even to a sexual encounter in which they have little motivation to initiate. As such interpretations indicate, new physiological data continue to call for interpretation in light of an overarching evolutionary perspective. There are also potential prospects to expand the comparative and human socioecological scope (e.g., investigating brain activity in polygynous contexts) of such work.

Summary New genetic, genomic, and physiological data concerning human sexuality are available and need to be integrated with contemporary evolutionary theory and models depicting the evolution of hominin sexuality. The heritable basis underlying shifts toward human longterm slightly polygynous bonding can be investigated from candidate gene or comparative genomic approaches, but to date has been unsuccessful. While multiple lines of evidence converge in indicating that humans are adapted for low sperm competition pressures, the genetically based attempts (e.g., SEMG1 and other genes expressed in semen) to specify the evolutionary origins and trajectory of this pattern in hominins also remain murky. Evolutionary theory tells us that reproductively relevant genes should be hotspots of selective action; that expectation is partly born out, although subject to caveats such as whether gene regulation or protein coding is more important. Brain imaging and hormonal studies help elucidate the shared and derived mechanisms by which long-term human bonding and sexual behavior occur. The brain imaging data, in particular, derive from a very narrow cultural scope. Nonetheless, various brain processes in humans show homology with mechanisms from other long-term bonded species such as prairie voles. There are some distinct brain processes implicated in romantic bonding from sexual behavior, as would be expected from other lines of evidence (e.g., in other species that engage in sexual behavior without long-term bonds, or in humans the ability to separate sex from love). Brain imaging and hormonal studies of romantic bonding show evidence of sex-similarities (e.g., in involvement of oxytocin in both sexes); that is expected since the mechanisms of long-term sociosexual bonds may in part piggyback on those related to mammalian maternal behavior. At the same time, evidence of lower male testosterone levels within contexts of long-term intimate family relationships speaks to processes that appear more sex-specific (i.e., males decreasing the hormonally based investment

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in mating effort). The data on sex differences in the coincidence of objective and subjective measures of sexual arousal indicates that—as Darwin and other theorists would anticipate—sex differences exist. One overarching interpretation is that males have been equipped with a more proceptive sexuality and females a more receptive sexuality.

RECENT AND LARGE DATA SETS ON AMERICAN AND INTERNATIONAL HUMAN SEXUALITY Alfred Kinsey’s interview-based studies of U.S. human sexuality were foundational contributions. The data he and collaborators collected and published in the mid20th century provided quantitative insight into the sex lives of approximately 12,000 Americans (Kinsey et al., 1948, 1953). He found, for example, that premarital and extramarital sex was common, and that more men than women reported same-sex sexual behaviors. As important as these works were, however, others criticized the findings on methodological grounds. The sample was nonrandom, including an inordinate number of men in prisons, and short on members of groups (e.g., from churches) who less often agreed to participate in the research (factors that could have overestimated the frequency of certain sexual behaviors). It was not until the 1990s that a nationally representative probability sample of U.S. adult sexual behavior was conducted (Laumann et al., 1994). In the first part of this section, we consider what this 1994 publication, along with several other large and rigorous, U.S. data sets on sexuality have found, effectively updating Kinsey’s insights with more current and arguably better-designed studies. These studies are important to an evolutionary perspective on human sexuality for several reasons. One is that they enable rigorous tests of expectations derived from relevant theory, such as whether males report higher sexual desire than females, as would be expected if females are the reproductively limiting sex. These data can serve as the basis for productive, empirically grounded discussions concerning the patterning of human sexuality, a contrast to choosing a single study suiting one’s preferred interpretation or ignoring altogether data on the subject. Another reason is that an evolutionary perspective can be brought to bear on such rich data sets, something which is lacking in the majority of the original publications describing these large human sexuality studies. Before presenting findings from U.S. and international sexuality data, it is important to comment on methodological constraints inherent to the study of human sexual behavior. The study of human sexual behavior is one of the most emotionally, politically, and socially charged domains of human experience, complicating its study. Direct observations of human sexual behavior are rarely possible. While a primatologist can observe nonhuman primates in the wild or captivity engaging in various sexual behaviors (Dixson, 2012), few humans will tolerate the same intrusions into their sex lives. Accordingly, the vast amount of information on human sexual behavior derives from questionnaire responses and interviews. Individuals may be asked to complete a survey, sometimes anonymously and confidentially, on a paper-andpencil version, or perhaps via a computer interface. Collecting data by these means raises questions of validity. How do we know whether individuals are accurately describing their sexual behavior, especially when there American Journal of Physical Anthropology

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may be temptations to downplay (e.g., affairs) or exaggerate (in the attempt to impress others) claims? Some cross-checks are feasible, such as aligning data between partners or the sexes (e.g., regarding coital frequency within partnerships) or other sources of clinical or commercial information (e.g., patterns of STIs and knowledge of contraception use should be consistent with reports of sexual behaviors). The appropriate caution is thus warranted when evaluating data on human sexual behavior.

Sex in large U.S. surveys From Ed Laumann and colleagues’ (1994) study of U.S. sexuality, approximately 5,000 individuals aged 18– 59 years participated in in-person interviews. Outcomes included frequency and types of various sexual behaviors, and were provided with respect to sociodemographic variables including age group, sex, sexual orientation, ethnicity, and educational attainment. Data on the frequency of sexual behavior the past year are presented with respect to age group and sex in Table 2. As shown in this table, the percentage of women and men reporting having sex four or more times the past year tends to diminish with age, while the percentage of women and men not having sex the past year is highest among young and old age groups. This same U.S. survey provided a quantitative snapshop of other features of adult sexuality. Across all age groups, men engage in more frequent masturbation than do women. As an example, at ages 18–24, 29% of men and 9% of women reported masturbating at least once a week. Masturbation rates also declined with age, with 10% of men and 2% of women aged 55–59 reporting weekly masturbation. Men reported more often thinking about sex and using autoerotic material such as watching erotic videos; for example, 54% of men and 19% of women reported thinking about sex at least daily. Extramarital affairs were noted among a minority of respondents: “Over 90 percent of the women and over 75 percent of the men in every cohort report fidelity within their marriage, over its entirety.” (Laumann et al., 1994: 214). Men reported a higher frequency over various time frames engaging in same-sex sexual behavior than did women with, for example, 2.0% of men and 0.8% of women specifying having sex with same-sex partners over the past five years. With respect to sexual identity, 2.8% of men and 1.4% of women reported either bisexual or homosexual identity. Women (22%) were much more likely to report being forced to have sex than were men (1%), with most of women’s forced sex occurring with known individuals such as someone with whom the woman was in love or someone she knew well. More recently, a nationally representative probability sample of U.S. sexuality was conducted in 2009 by scholars based at Indiana University, thus continuing Kinsey’s legacy of work there. This study relied upon computer-aided survey. A sample of 5,865 men and women aged 14–94 participated. Findings from the survey were published in a special edition of the Journal of Sexual Medicine in 2010. The study presented data on various sexual practices such as intercourse, masturbation, and oral sex with respect to age, sex, and a host of social variables including sexual orientation, ethnicity, education, income, and geographical region. Among some of the take-home findings from the study, males engaged in higher rates of masturbation than females American Journal of Physical Anthropology

TABLE 2. Frequency of sex in the past year from early 1990s U.S. national sex survey Age group Men 18–24 25–29 30–39 40–49 50–59 Women 18–24 25–29 30–39 40–49 50–59

Not at all

A few times per year

A few times per month

2–3 times per week

4 or more times a week

15 7 8 9 11

21 15 15 18 22

24 31 37 40 43

28 36 23 27 20

12 10 6 5 2

11 5 9 15 30

16 10 16 16 22

32 38 36 44 35

9 37 33 20 12

12 10 6 5 2

across the sample; age-related patterning in sexual behaviors showed that masturbation was relatively more common early and late in adult life, while vaginal sex relatively more common during the prime reproductive years; and for both men and women partnered sexual behaviors declined in frequency in the 50s onward, showing even steeper declines around the 70s.

A quantitative cross-cultural approach to human sexuality Apart from U.S. studies, we also want to know about the wider cultural record of human sexuality. What can be said about the sexual behavior of people around the world? Charles Darwin himself tried to collect as much information on mate preferences and other features of sexuality as he could by compiling the observations of travelers and others with international experience. Those cross-cultural anecdotes are included in his 1871 book. As far as more rigorous cross-cultural study of human sexuality, the standard bearer has been Ford and Beach’s (1951) Patterns of Sexual Behavior. This is a compilation of cross-cultural accounts drawn from the human relations area files (HRAF). In Ford and Beach’s book, sections are devoted to a variety of sexual practices, from subadult sexuality to adolescence, and adult sexual behaviors ranging from intercourse positions to extramarital affairs. Variation is recognized and in some cases patterned; for example, longer taboos against postpartum female sexual behavior are found in polygynous societies, consistent with the idea that a wife with cowives can abstain longer from sex after having had a baby when there is another sexual partner available to her husband. Additionally, Ford and Beach concluded that cross-cultural standards of attractiveness varied, although female appearance garnered more attention than male appearance, and male social success often mattered more than attractiveness in determining male marital and reproductive success. In this section, we move beyond Ford and Beach’s book to present more recent international studies of human sexual behavior. Some of these more recently published studies are derivatives of the HRAF data set, while others rely on nationally representative probability samples of sexual behavior from various countries around the world. The most widely used quantitative measures of crosscultural sexuality tend to rely upon marital patterns. Societies are variously described as monogamous, with

EVOLUTION AND HUMAN SEXUALITY mild polygyny, generalized polygyny, and occasionally polyandry based on the most prevalent patterns of marriage. As noted in the more than 1,200 societies comprising the HRAF, approximately 85% have some degree of polygyny (Murdock, 1949). A related sample, restricted to the so-called standard cross-cultural sample (Murdock and White, 1969), viewed as a more representative (with respect to linguistic and geographic distribution) crosscultural sample of 186 societies, shows similarly that mild polygyny is the most common marital pattern, with around 15% of societies classified as monogamous. The use of marital patterns as a proxy for aspects of sexuality has its pluses and minuses. On the favorable side, this measure is more readily available in the literature, most of partnered human sexual behavior occurs within longterm relationships such as marriage, and the relations between marital and other quantifiable variables such as paternal involvement enables testing for links between sexuality and other factors. On the downside, use of societal-level marital patterns ignores premarital and extramarital sex, reliance upon prostitution, and ignores within-societal variation in sexuality as well as that arising in other contexts such as across the full life course. Evolutionary psychologists led by David Buss and David Schmitt have conducted some of the largest international surveys related to human sexuality. These efforts relied upon survey administration to samples in various countries of the world, frequently relying upon international university student samples but in other cases also including community samples. These samples thus lack the small-scale hunter-gatherer, horticultural, agricultural and pastoralist emphases of the crosscultural anthropological surveys drawing upon the HRAF or SCCS. That said, these studies have yielded rich findings that speak to sex, age-related, and other aspects of human sexuality. From the effort led by David Buss (1989, 2003), mate preferences were surveyed among 37 societies around the world. Among his findings, love, emotional stability or maturity, and a dependable character were ranked the highest among traits preferred in a mate by both men and women around the globe. These preferred traits accord with what one would expect for maintenance of a successful long-term sexual and reproductive relationship. Buss also found sex differences in mate choice. Men valued female attractiveness more than women did, whereas women valued status and resources in a partner more than did men. Men preferred younger partners, whereas women preferred older partners. Variation across societies also emerged. Chastity in a mate was highly valued in some countries such as India and Indonesia, but not in other countries such as the Netherlands and France. David Schmitt spearheaded an international project focused on questionnaire-based investigation of human sociosexuality through the International Sexuality Description Project (Schmitt, 2003, 2005). This sample drew upon approximately 16,000 participants from 52 countries. Among the central findings were that men consistently expressed more interest in having multiple sexual partners than women, and across variable lengths of time (e.g., over the next month to next 30 years). Similarly, men consistently had higher sociosexuality scores (e.g., expressing more open rather than restricted sexual views) than did women across the sample. Yet in both desired number of sexual partners and sociosexuality there was considerable international vari-

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ation observed. In East Asian samples, 17.9% of men and 2.6% of women said they wanted more than one sexual partner over the next month, whereas in South America 35.0% of men and 6.1% of women wanted more than one sexual partner over the next month. Across countries, several variables were correlated with sociosexuality scores. The operational sex ratio (OSR) was correlated with sociosexuality scores, whereby societies with a relatively higher proportion of women tended to have less restricted sociosexuality. Fertility rates were inversely related to sociosexuality, such that societies with higher rates of fertility had more restricted sociosexuality. Further, scores on the Human Development Index (a measure of societal quality of life) were positively associated with more open sociosexuality. An increasing number of countries, apart from the U.S., have conducted nationally representative probability samples of sexual behavior. To illustrate, the first probability sample of sexual behavior in China was conducted in 1999–2000 (Parish et al., 2007). This Chinese study included more than 3,700 adults aged 20–64 who reported to a secure neighborhood location to complete an interview and items on a laptop computer. As an illustration of the findings, approximately 70% of men and 30% of women under the age of 30 reported masturbating, rates that were higher than previous reports in China based on smaller samples, and consistent with recent changes in sexual behavior. Additionally, approximately 50% of men and 30% of women in the late 1990s reported engaging in premarital sex, rates that were markedly higher than data from previous decades, especially the 1950s. Rates of same-sex sexual behavior were higher for men than women, a pattern also found crossculturally (Kirkpatrick, 2000; Poiani, 2010). The largest compilation of international sexual behavior data yet was published by Kaye Wellings and colleagues in 2006. They drew upon data from 59 countries, from Kenya to Ghana, Bangladesh to Turkey. All studies were published between 1995 and 2005, included some longitudinal analyses, and featured nationally representative samples. The compilation was facilitated by the availability of Demographic and Health Surveys from many developing countries, conducted in order to provide baseline data informing reproductive health agendas but also providing an unprecedented availability of quantitative, international data. A number of take-home points emerge from the analysis, showing both patterns observed across all samples as well as variation that itself invites explanation. In all countries, married men and women report a higher likelihood of engaging in sexual behavior in the past four weeks compared with unmarried respondents. This pattern reinforces the context of most human sexual behavior, occurring within the context of a long-term relationship such as marriage. Across samples, men typically report more often having had multiple sex partners the past year than do women. This sex difference appears across an array of contexts, including premarital, extramarital or marital (as in polygynous marriages) sexual behavior. The countries in which a higher prevalence of women report multiple sex partners the past year tend to be in Europe or North America, and largely reflect premarital behavior. Age discrepancies in marriages reveal that husbands tend to be older than wives, although the age difference is lowest in countries such as the U.S. (2.2 years) and Australia (1.9 years), and highest in African countries such as Burkina Faso (14.7 American Journal of Physical Anthropology

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years) and Mali (13.2 years). The age of first intercourse varies globally. In some countries, women have an earlier sexual debut and higher intercourse rates compared with men; examples include a number of west African countries and Bangladesh, in which women marry at younger ages and the pattern reflects having sex within marriages. The prevalence of premarital sex among women is highest among countries such as the U.S. and in Europe, but quite low in other countries such as Mali, Nepal, and Indonesia. In the latter cases, less than 25% of women report engaging in intercourse before marriage. In other countries, such as Brazil, men tend to have younger ages of sexual debut than women, with this reflecting higher rates of male premarital sex, including in some cases with prostitutes. Data compiled by Wellings and colleagues only tabulate use of prostitutes by men, a recognition that prostitution is largely an industry servicing men; most male prostitutes service other men rather than women. Yet the percentage of men who say they paid for sex in the past year—a measure of use of prostitutes—varies around the globe. Higher rates are found in China and East and West Africa (around 10%) than in Latin America, North America, Europe, and North Africa (less than 3%).

Sex on the Internet New sources of data on human sexuality continue to arise. The Internet is one opening novel avenues by which measures of human sexuality can be obtained and interpreted. This is reflected in multiple ways, including the diversification of websites catering to all kinds of sexual and romantic interest groups. Online dating has become a burgeoning industry and an increasingly common means by which partners in countries such as the U.S. meet. The quantitative analysis of search contents has also opened up fresh ways to explore human sexual expression. The most ambitious and current account to quantitatively explore sexuality related Internet search contents was published in Ogas and Gaddam’s (2011) A Billion Wicked Thoughts. They report the results of over 400 million web searches from more than 2 million users, primarily from the U.S., but also other countries such as the U.K., India, Nigeria, and Canada. They analyzed search data from 2009–2010 as well as a supplementary AOL search database on more than 650,000 users. Much of their effort honed in on potential differences in search content according to sex and sexual orientation. Summarizing what they found, “On the Web, men prefer images. Women prefer stories. Men prefer graphic sex. Women prefer relationships and romance. This is also reflected in the divergent responses of men and women when asked about what sexual activities they perform on the Internet.” (p. 19) Men were much more likely (37%) than women (6%) to list viewing erotic images and movies as preferred Internet sex-related activities. Conversely, women (21%) were more likely than men (8%) to report sex-related activities on the Internet involving attempts to maintain contact with love or sex partners. Of other patterns in Internet sex searches, younger women (age 16–18) draw the most interest, consistent with male orientation toward cues of high reproductive value and pursuit of a long-term mate.

Summary A variety of large U.S. and international quantitative sexuality data are available. These data reveal patterns American Journal of Physical Anthropology

with respect to sex (male/female), sexual orientation and age, among other factors, while also providing a window into cross-cultural variation. Sex differences in behavioral measures of desire such as masturbation or use of prostitution are quite robust across these samples, consistent with theory that males have evolved a more proceptive sexuality. Males engage in higher rates of samesex sexual behavior than females in these large U.S. and international data sets. Age-related declines in various measures of sexual behavior, such as coital frequency, also conform to waning selective pressures to maintain sexual function, a topic we will also turn to in the next section on human life course variation in sexuality. Most sexual behavior occurs within the context of long-term bonds, even when humans today face an unprecedented array of novel potential mating partners compared to hunter-gatherer forebears. Yet the international data also indicate that, at the societal level, slight polygyny is a better descriptor of human marital patterns than monogamy. The international data also underscore the importance of contextual variables such as fertility rate and OSR. As an example, the societies with higher fertility rates tend to have more restrictive attitudes toward female sexuality. The Internet provides a new window into human sexuality, showing that some of the longstanding patterns such as sex differences in sexual desire manifest in this new arena. The collective weight of this body of evidence argues for the continued relevance of evolutionary theory to understanding human sexuality today, and presents a standard against which competing explanations are challenged to explain.

LIFE COURSE PERSPECTIVE ON HUMAN SEXUALITY The vast amount of theoretical and empirical attention to human sexuality from an evolutionary perspective has focused on prime adult years. A large literature investigating and adaptively interpreting sex differences in mating strategies has, for example, tended to emphasize young adults who do not have children. In this section, a life course perspective is applied to human sexuality. This is important for a number of reasons: sex differentiation of brains and genitals begins before birth; juveniles learn and practice sociosexual behaviors (in addition to economic and social skills emphasized by evolutionary thinkers) that may be suited to their context and future reproductive success; puberty and adolescence transition individuals into the raised stakes of potential reproduction; features of human sexuality fluctuate across the prime adult years, including across peripartum transitions; and features of human sexuality change with age in ways that can be understood with respect to evolutionary-based models of reproductive senescence. Life history theory provides a theoretical and empirical toolkit to make sense of the patterning of human sexuality across the life course (Stearns, 1992; Geary, 2002; Hawkes and Paine, 2006; Muehlenbein, 2010). Individuals have limited time and energy to devote to competing allocations of growth, maintenance, and reproduction. The specific allocations to these agendas can exhibit age, sex-, and context-specific variation in ways that may make adaptive sense. There may also be tradeoffs across these allocations, meaning that allocation to one outcome comes at expense to another. To illustrate, based on the theory reviewed above, female mammals tend to

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EVOLUTION AND HUMAN SEXUALITY TABLE 3. Life course perspective on human sexuality Life course stage

Key adaptive and physiological processes

Perinatal

Early organizing effects on brain and differentiation of primary reproductive characteristics

Early Childhood

Dependency on mothers and other caregivers for social and energetic support

Middle Childhood

Greater independence and interaction with other adults and juveniles

Puberty and Adolescence

A second phase of organizing effects of steroid hormones on the brain, and development of secondary sexual characteristics

Adulthood

Age-related changes in reproductive physiology Subtle physiological changes across the ovulatory cycle and dramatic changes across the reproductive cycle

Senescence

Age-related declines in reproductive function, including decreases in sex steroids

devote more of their reproductive effort to parenting effort, whereas male mammals tend to devote more of their reproductive effort to mating effort. The shifts from growth to reproductive effort at puberty entail development of secondary sexual characteristics; by waiting until puberty to develop these characteristics, organisms delay the potential social and energetic costs of their maintenance. Peripartum shifts in female sociosexuality, which can also impact the sexuality of a longterm partner, can be viewed from the standpoint of life history tradeoffs between investment in current and future reproduction.

The early development of human sexuality As an unusual anecdotal insight into the development of human sexuality, an ultrasound taken of a male fetus appeared to show him engaging in autostimulation (masturbation), an indication that sexuality can precede birth (Meizner, 1987). Female infants are capable of vaginal lubrication, and male infants of erections. Infants of both sexes are capable of orgasm, though without ejaculation. These observations indicate that even young

Key patterns of sexuality Sex-specific developmental trajectories begin to unfold Sex-specific and plastic mechanisms orient toward social stimuli to enhance survival Interest in own and others’ genitals, including auto-stimulation Some degree of sex differentiation in social behavior Expanded distinctions in sex differentiation, with females more oriented toward caregiving contexts and males more oriented toward physical play Increasing frequency of sex play, especially for males, in same-sex and between-sex pair-bonding contexts Shift into potential reproductive realm Females tend to be 1–2 years ahead of males Marking transition toward social, economic, and political activities conducive to reproductive success, with female transitions highlighting aspects of fertility and male transitions highlight social achievement Increased frequency of intercourse, but also quite variable by individual, sex, population Age-related changes in sexuality during adulthood can be related to reproductive partnerships Cyclical female shifts across the ovarian cycle have at best subtle influences on sexuality, whereas shifts across pregnancy and postpartum phases have pronounced impacts on female sexuality Male sexuality is typically intertwined with that of a long-term partner, although sex differences in desire are amplified during late pregnancy and early postpartum The menopausal transition in women is associated with some declines in sexual function Measures of sexual behavior decline with advancing age in both women and men, although in sex- and context-specific ways

children have a limited sexual capacity, but a capacity that can foster engaging in the kinds of sociosexual play that may eventually attune their sex- and contextspecific reproductive investment. To help capture some of the key processes and patterns of human sexuality across the life course, from the perinatal period onwards, these are summarized in Table 3. I consider some of these major processes and patterns from early to late in the life course, touching on some of the most common changes in sociosexual behavior, underlying physiological processes, and with some reference to life history theory. Rigorous, quantitative studies of childhood sexuality are fraught with ethical and methodological challenges, even more than research on adults. Thus, the available data are quite limited, and the studies conducted by Alfred Kinsey and colleagues in the mid-20th century still stand as pillars in the field. What Kinsey et al. learned, primarily through interviews conducted with adults who recalled their childhood sexual experiences, was that children’s sexual behavior was patterned with respect to age and sex. By around age 5, approximately 10% of girls and boys reported having engaged in any American Journal of Physical Anthropology

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sex play. Across aged 5 through 13, however, that frequency remained comparable for girls, but increased steadily to around 35% for boys aged 11–13. A fraction of these experiences were same-sex: while 8% of girls aged 5–7 and 3% of girls aged 11 reported engaging in homosexual play, 5% of boys aged 5–7 and about 30% of boys aged 11 reported in homosexual play. More recent quantitative studies of children’s sexuality have been conducted in the U.S. and Europe, but typically rely on parent or doctor reports rather than reports by children or adult retrospective reports. These latter studies underestimate frequencies of childhood sexual behaviors that children intentionally shield from adult view, but nonetheless can offer some useful insights. For example, one study found that masturbation frequencies in the U.S. increased from around 10% by age 7 to around 80% by age 13 (Mallants and Casteels, 2008). As a complement to quantitative studies, ethnographic reports of childhood sociosexuality provide insight into age-, sex-, and context-specific patterns. Eleanor Maccoby (1998) summarizes research on U.S. children’s sexuality, noting that by around ages 7–9 children begin to conceptualize cross-sex interactions with romantic or sexual overtones. Herdt and McClintock (2000) suggest that the timing in the U.S., New Guinea, and elsewhere of children developing sexual attractions to same- and other-sex partners around age 10 may be related to rising concentrations of adrenal androgens as part of adrenarche. Ford and Beach (1951) parse cross-cultural variation in childhood sexuality into three broad categories: restrictive, semirestrictive, and permissive societies. They note that the varied degree of proscriptions guiding childhood sexuality tend to be aligned with adult sexuality; in other words, children are variably granted sexual latitude or constraint in ways consistent with the adult sex lives they will later have. Several hunter-gatherer ethnographic anecdotes recognize that sex play also occurs, as among the Hadza of Tanzania in which Frank Marlowe (2010) noted boys and girls “playing house” and engaging in sex play by around age 7–8.

Puberty and adolescence As childhood wanes, puberty and adolescence begin (Bogin, 1999; Weisfeld, 1999). This is a time of shifting life history priorities. Investment in growth wanes and maintenance efforts can be compromised as allocations to reproductive effort increase. Females typically undertake the pubertal transition 1–2 years before males, a sex difference consistent with slight polygyny (Dixson, 2012). Sex steroids exert a second stage of organizational effects on the brain, serving as physiological mechanisms shaping these shifting priorities. Sex steroids also regulate the expression of secondary sexual characteristics. Effectively, the increased estrogen released by the ovary and androgen by the testis shape various anatomical and physiological characteristics in ways that enhance reproductive success in sex-specific ways. As examples, females develop greater gluteofemoral fat, which can serve as a metabolic reservoir on which to draw during gestation and lactation, and males put on more upper body musculature, thought to aid ancestral male success in mating competition. The impacts of the pubertal transition on human sexuality are context-specific. Returning to Ford and Beach (1951), their scheme recognized restrictive, semirestrictive, and permissive societies. Among permissive American Journal of Physical Anthropology

societies, women and men had similar regulations governing sexual behavior, whereas among more restrictive societies men’s sexual activities were sometimes less constrained than women’s. This yields a sexual double standard among some societies. A variety of factors underlie cross-cultural differences in these aspects of adolescent sexuality (Schlegel and Barry, 1991). Some of the most important factors are residence (matrilocality associated with more permissiveness, patrilocality with less) and inheritance and descent (greater permissiveness associated with bilateral descent and little inheritance, but more restriction in patrilineal descent). Schlegel and Barry (1991) also discuss cross-cultural patterns of same-sex adolescent sexual behavior. If restrictions govern same-sex sexual behavior of one sex, those are often found in the other sex too. If adolescent males are subject to same-sex sexual restriction, they are often subject to similar restrictions through adulthood. While a fraction of men hold lifelong same-sex primary attractions, adolescent male same-sex sexual behavior is often a life history phase resulting from a lack of mating access to females. Quantitative studies of adolescent sexuality are available for the U.S. and many other countries, complementing the qualitative cross-cultural compilations. In the U.S., about 50% of secondary school students report having engaged in intercourse, with no notable sex differences, although frequencies vary across reported ethnicity. Approximately 25% of these students also report more than one sexual partner. To gain insight into quantitative international adolescent sexual behavior, we can return to the Wellings et al. (2006) review previously noted. From this review, one of the central findings is that in countries with young age of female marriage, females typically engage in earlier sexual intercourse than males, often within marriage. As another pattern, in developing countries the duration between sexual initiation and marriage is shorter among females than in males, meaning that female sexual debuts tend to be more closely tied to marriage than are male sexual debuts. However, this is not the case in developed countries such as the U.S. or Australia, in which both males and females tend to engage in premarital sex that is not closely tied to marriage. From an evolutionary perspective, some of the most profound impacts on adolescent sexuality entail a lengthened duration of adolescence, especially for females. Among hunter-gatherer societies, females tend to experience menarche around age 15–16, with marriage and reproduction following a few years later (Kelly, 1995; Ellison, 2001; Howell, 2010). The brief phase of adolescence among female foragers entails infertility or subfecundity as ovarian cycles are less regular and often nonovulatory, helping make possible sexual experimentation (if not socially proscribed) (Montague, 1946). For hunter-gatherer males, pubertal milestones are more difficult to measure (such as “nocturnal emissions” or changes in testis and penis size), although male pubertal transitions (like in other societies) typically begin later and extend considerably longer. Males must demonstrate their social and foraging prowess, perhaps through bride service, to show they are worthy of marriage. A consequence is that in foraging societies males are commonly in their mid-20s before marrying and becoming fathers. Against a hunter-gatherer backdrop, however, in many contemporary contexts females and males are undergoing earlier puberty and postponing the

EVOLUTION AND HUMAN SEXUALITY formation of long-term partnerships (such as marriage) and having children. In some countries, such as Singapore and China (Parrish et al., 2007), a majority of women and men are postponing having intercourse into the 20s despite earlier ages of puberty and later ages of reproduction. In other countries, such as the U.S., premarital sex at younger ages is the norm. The spawning of a “hook up” culture, in which adolescents deliberately seek to engage in sex but avoid long-term commitment, has also fallen into this growing adolescent gap (Garcia et al., 2012). In university samples, female-biased sex ratios may also be contributing to hook up culture by granting more political leverage to male mating preferences. For females, the duration of adolescence can now thus extend for decades rather than a few years among ancestors, and the social contexts during adolescence often include many similarly aged females, creating evolutionarily novel contexts for female–female competition and cooperation. For females and males alike, contemporary social contexts (like on a university campus) offer a number and variety of fellow adolescent prospective mates that has no evolutionary precursor.

Patterns of adult sexuality As the life course proceeds, humans move from adolescence into adulthood, a time during which females and males are at their reproductive prime (Hrdy, 1999, 2009; Gray and Anderson, 2010). From a life history perspective, sex differences across the adult years can be anticipated in features of sexuality, including subtle effects across the ovulatory cycle and more pronounced effects across the reproductive cycle (cycle of pregnancy, postpartum, and eventually resumption of cycling). Because most of human sexual behavior takes place within the context of long-term bonds, adult male sexuality is often hitched in its patterning to that of females. Still, the variable social context of adult sexuality allows for different degrees of acceptance of partner numbers, samesex sexuality, and other features. Given that sexual desire is a primary motivator to engage in sexual behavior, even if desire can serve other ends such as bonding, a response to boredom, or for pleasure itself, it makes life history sense that various features of adult sexuality appear to favor reproductive success in sex-, condition-, and context-specific ways. In the earlier section addressing large quantitative studies of human sexuality, we saw some of the key patterns with respect to adult sexual behavior. These patterns include sex differences in some measures of sexual behavior such as males engaging in higher rates of masturbation and same-sex sexual behavior than females. These patterns also include cross-cultural and international variation in sexuality, such as the variable degree to which polygynous marriages are allowed, even if these are generally much more common than polyandrous partnerships. Here, we consider some of the primary patterns of sexuality during the primary adult years. One of the primary aspects of adult sexuality is age itself. For women, fecundability (likelihood of conceiving for a given act of intercourse) is at its peak during the early to mid 20s to mid 30s (Ellison, 2001; Vitzhum, 2009). This is true across populations, including in the U.S. Associated with declining fecundability in women are age-related decreases in fertility: in hunter-gatherer societies, women’s last age of reproduction tends to be in the late 30s to early 40s, well in advance of the complete

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cessation of cycling. For men, various measures of reproductive function begin to decline as early as the 30s, although as we shall see more pronounced effects tend to be observed in the 50s, 60s, and later. To the degree sexual behavior motivates reproduction, life history theory suggests that adults will be highly motivated to have sex, more than during juvenile ages or in later life. As one quantitative contribution to this point, Herbenick et al.’s (2010) probability-based survey of U.S. sexuality showed age- and sex-related patterns of sexual behavior among individuals aged 14–94. Among the relevant findings, rates at which males masturbated alone the previous month were higher among males aged 18–39 than younger or older males, and rates of vaginal intercourse the previous month were highest among males aged 25– 39. Additionally, among women, rates of masturbation alone and rates of vaginal intercourse the past month were both at their highest among women aged 25–29 years.

Concealed ovulation? From an evolutionary perspective, one of the topics that has garnered considerable attention is whether humans have concealed ovulation, or a lack of overt indication of the fertile phase of the ovulatory cycle. Some theorists have suggested that humans evolved concealed ovulation to adaptively retain a male partner across the cycle, also facilitating maintenance of a long-term sociosexual relationship and paternal care (e.g., Strassman, 1981). More recently, some scholars have sought to challenge such a view by investigating cycle-related shifts in female proceptivity (actively seeking sex), receptivity (accepting another’s sexual advance), and attractiveness (stimulus value to potential partners) (Beach, 1976). In a review of many of these studies, Gangestad and Thornhill (2008) found that female facial attractiveness is often more highly rated during the fertile phase of the cycle. Moreover, women during their fertile phase tend to express higher preferences for masculine traits such as broad shoulders or robust jaws. Several other studies found cycle-related differences in behaviors such as how revealing women’s clothes are, women’s gait, and women’s acceptances of men’s courtship invitations (e.g., Durante et al., 2008; Gueguen, 2009), findings compatible with enhanced female sociosexuality during the fertile phase. Some of these psychological and behavioral differences disappeared among women on monthly based hormonal contraception (e.g., the Pill), implicating a role of fluctuating (or not) sex steroids in any such effects (Alvergne and Lumma, 2010). Appropriate caveats are warranted, however. One is that these effects tend to be subtle rather than pronounced; human females do not exhibit cyclical traits akin to a chimpanzee or bonobo female’s sexual swelling (Dixson, 2009, 2012). These psychological and behavioral fluctuations across women’s cycles do not have dramatic impacts on sexual behavior either. In some of the best designed studies, slight increases in sexual behavior during the fertile phase among partnered women have been found (e.g., Wilcox et al., 2004). However, a large study from 13 countries of partnered women’s sexuality during the previous month did not show any differences in sexual behavior during the fertile phase (Brewis and Meyer, 2005a). The one phase of the cycle in which female sexual behavior is commonly and dramatically lower is during menstruation, a finding that has been American Journal of Physical Anthropology

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documented cross-culturally (e.g., Ford and Beach, 1951) and in many other studies. A parsimonious comparative interpretation of these cycle-related patterns in human female sexuality is that they are consistent with the lack of selection on female multimale mating (unlike chimpanzees, for example: Nunn, 1999), while also providing support for subtle increases in female proceptivity, receptivity and attractivity when fertilization is most likely.

Peripartum fluctuations in human sexuality Any ovulatory cycle-related changes in female sexuality pale in comparison to those occurring across the reproductive cycle, or transition from life history states of cycling to pregnancy to postpartum amenorrhea (not menstruating) and eventually cycling. From the standpoint of life history theory, women’s changes in sexuality across the reproductive cycle can be viewed as tradeoffs between current and future reproduction (Escasa-Dorne et al., 2013). Sexual behavior may be high during times cycling, possibly leading to conception and successful reproduction. Sexual behavior may occur at variable rates across pregnancy, and for functions such as relationship maintenance (to recruit an investing partner such as a child’s father) or as a byproduct of physiological shifts arising during pregnancy (such as elevated estrogen concentrations). Sexual behavior tends to diminish after having had a child, as a mother focuses her reproductive investment on keeping alive and aiding the current reproductive product (baby) rather than attempts to beget the next one. Because of the typical links between male and female sexuality in long-term partnerships, many of the shifts in female sociosexuality across the reproductive cycle impact male sexuality too. Cross-cultural attitudinal and international quantitative studies reveal that many women report being sexually active during pregnancy, but with additional patterns across pregnancy and social context. In Ford and Beach’s (1951) cross-cultural survey, they found that among small-scale societies 70% approved of female sexual behavior during early pregnancy, but that those rates of approval diminished across gestation. A primary reason for disapproving of pregnant women’s engaging in sex, especially during late gestation, was concern over the well-being of the fetus. Among more polygynous societies, sex during pregnancy was disapproved of earlier in gestation; this is consistent with the sexual availability of an alternative sexual outlet (cowife) to a husband and would-be father, also lessening any pressures for pregnant women to engage in sex for a relationship maintenance function. In Brewis and Meyer’s (2005b) compilation of recent sexual data from more than 90,000 women from 19 countries such as Bolivia and Cameroon, they found that pregnancy impacted sexuality: “Pregnancy has a negative effect for the most part on sexual frequencies. . .[G]enerally, coital frequencies are significantly lower in pregnancy compared with the nonpregnant state. . .[O]verall. . .sexual frequencies decline in the first trimester, decrease further in the second, and still further in the third.” (p. 508) Similar patterns were observed in a meta-analysis of 59 sexuality studies largely conducted in North America or Europe, with measures of sexual frequency initially little different the first trimester from a nonpregnant state, but decreasing across gestation (von Sydow, 1999). Many studies find that measures of women’s postpartum sexuality are diminished. Cross-cultural taboos govAmerican Journal of Physical Anthropology

erning women’s sexual behavior vary in length; in one compilation, taboos lasting 1–5 months were typical in Eurasia and the Mediterranean region, but taboos around 2 years in length more common across many sub-Saharan African societies. A key factor in variable postpartum female sexual taboo lengths is whether a mother’s partner—typically the infant’s father—has another sexual outlet. In polygynous societies, the father of an infant may have another partner (e.g. a mother’s cowife), allowing for longer taboos. In the same kinds of demographic reports on women’s recent sexual behavior, Brewis and Meyer (2005b) summarized the data across 19 countries such as the Philippines and Kenya, showing dramatically lower frequencies of female intercourse during the early postpartum phase. Similarly, Von Sydow (1999) observed, in the same review as noted above for gestational sex, that, “Compared with the prepregnancy period, coital frequency is reduced in most couples during the first year after birth.” (p. 36) In this same review, a fraction of men’s sexual desire remained lower during the postpartum period, though postpartum paternal sexuality has been poorly studied relative to that of postpartum women. From an evolutionary and life history perspective, it is during late pregnancy and the early postpartum phase when sex differences in sexual desire are at their maximum during the reproductive years. That is an important consideration because it is rarely considered in discussions of sex differences in sexuality, including sexual desire (see Baumeister et al., 2001). It is also an important contributor to potential sexual conflicts of interest, whereby mothers may be adaptively shifting life history investments toward a current reproductive bout (infant), but fathers’ investments represent a greater mixture of parenting and mating effort. Other considerations can be at play too during this postpartum period: the duration of female lactational amenorrhea varies considerably across and within populations, and in relation to central energetic influences; that variation can impact a women’s physiology in relation to orienting toward investment in current or future reproduction (e.g., shorter durations of amenorrhea and more rapid resumption of ultimately functional cycles can promote female sexuality). The availability of a partner and other allocaregivers can also be important; mothers without a desirable partner may be motivated to more rapidly shift toward enhanced mating effort. Above all, from an evolutionary perspective, studies of nonhuman primates and human hunter-gatherers recognize that the bulk of female reproductive years were spent pregnant or in a state of lactational amenorrhea. The reproductive cycle shifts in female (and male) sexuality summarized here can be viewed as central to ancestral adult sexuality in addition to being of relevance to society today. In other words, the sexual lives of our recent ancestors were likely characterized by shifts across pregnancy and postpartum phases throughout the primary adult reproductive years.

Aging and human sexuality Human reproductive senescence proceeds, marking the last major stage from a life course perspective in which to situate human sexuality. While considerable attention has been given to the evolution of human senescence (loss of function with age) (e.g., Williams, 1957), with discussions regarding grandmothering

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EVOLUTION AND HUMAN SEXUALITY frequently featured (Hawkes et al., 1998), it is striking how rarely those evolutionary-informed discussions of senescence explicitly address changes in sexual behavior with age. Yet many of the same insights from the evolutionary literature on senescence inform expectations regarding past and present aspects of sexuality among individuals of advancing age. The evolutionary puzzle remains why humans live beyond reproductive capacities. That extended discussion lies outside the scope of the present review. Of more immediate relevance, however, is the fact that the existence of older and often postreproductive humans enables evolutionary- and life history theory-informed insight into their sexuality. In this vein, theory would suggest that postreproductive individuals should exhibit age-related declines in the physiological support of sexual behavior as well as of sexual behaviors themselves (Gray and Garcia, 2013). With older ages, selection on the maintenance of reproductive function diminishes. Any age-related decreases in mating effort can also allow life history reallocation toward parenting (and grandparenting) effort. A postreproductive woman who has reduced investment in an ongoing sexual partnership has more time and effort that can be devoted to descendant kin. Indeed, the cross-cultural literature highlights both expanded social freedoms of postreproductive women and their prominent roles in providing resources to offspring and grandoffspring (Frayser, 1985; Kerns and Brown, 1992). Additionally, patterns of age-related sexuality can unfold in sex- and context-specific ways. As examples, the fact that women tend to outlive men results in demographic skew whereby fewer older females have potential mates of similar ages, although they can also take as mates considerably younger men (Winn and Newton, 1982). Age-related declines in measures of human sexual behavior such as intercourse or masturbation frequency have been found in large, quantitative sexuality surveys, including in the U.S. The findings of these studies are generally consistent with life history expectations of reduced maintenance of reproductive function with advancing age. As an example, Lindau et al. (2007) conducted a nationally representative probability U.S. study of sexuality based on interviews with approximately 3000 adults aged 57–84 years of age. Both women and men reported declining frequency of sex with advancing age, with those frequencies lower at all ages for women than men. Masturbation rates, which can serve as a behavioral measure of sexual desire, also showed agerelated declines, and were also lower among women at all ages than among men. As frequency of sexual behaviors decreases, the prevalence of sexual problems increases. A higher percentage of women reported low sexual desire than men. Men reported increased agerelated problems maintaining erections, and women with vaginal lubrication. Age-related decreases in erectile function have been found in various contexts, including among Ariaal agropastoralists of northern Kenya (Gray and Campbell, 2005). Returning to a different probability sample of U.S. sexuality, Herbenick et al. (2010) found (across a sample aged 14–94 years) declines in sexual behaviors and increases in sexual problems with advancing ages. As an example, during the past 12 months, 51% of women age 55–59 and 22% of women aged 70 and older reported engaging in vaginal intercourse. Further, 54% of women in their 50s and 33% of women in their 70s reported masturbating alone during

the past 12 months, whereas 72% of men in their 50s and 46% of men in their 70s reported masturbating alone, a sex difference consistent with findings from earlier in the life course and with the broader point that males tend to have higher sexual desire than females. One of the best-studied aspects of aging and human sexuality has been across the menopausal transition. While aging along may negatively impact sexual capacities (e.g., increased frailty, regardless of sexual desire), a relevant question is whether the physiological transition of menopause itself influences female sexuality. Reviewing approximately 15 studies, both cross-sectional and longitudinal designs, Dennerstein et al. (2003) found that the best of these (studies of longer duration, those measuring hormones) consistently documented an influence of the menopausal transition on measures of sexuality such as elevated dyspareunia (pain during intercourse) and reduced sexual desire, with effects linked to declining estrogen. As an example, in one of the best U.S. studies of this type, the Study of Women’s Health across the Nation study, involving more than 3,000 women aged 42–52 years of age, increases in dyspareunia and decreases in sexual desire were observed among women, although there were no effects on intercourse frequency (Avis et al., 2009).

Summary Human sexuality shows age-, sex-, and socioecologically contextualized patterns, with those patterns interpretable in light of life history theory. One take home lesson is that human sexuality begins before puberty, a point that receives less attention than it should in the literature. Sex differences occur not just during adolescence or adult reproductive years, but across the entire life course, with even juvenile boys and postreproductive males showing, for example, higher masturbation rates than females. A major life history mismatch today is an extended adolescent gap, especially for females. While evolutionary scholars have long appreciated that ovarian cycling is relatively rare in ancestral environments, that insight has not been prominently applied to models of sexuality. When put in direct focus, peripartum shifts in female sexuality are dramatic, more so than those occurring across the ovarian cycle, and should be viewed as evolutionarily normative. Declines in various aspects of sexuality, including coital and masturbation frequency as well as erectile function or vaginal lubrication, can be viewed as a consequence of diminished selective pressures on maintenance of reproductive function.

CONCLUSIONS Having reached the end of the life course, we also wrap up this overview of human sexuality within evolutionary perspective. Multiple lines of evidence recognize human sex differences in sexuality, such as in sexual desire, masturbation rates, and accessing services of prostitutes. Those sex differences are consistent with theory noting that females tend to be the reproductively limiting sex over which males compete. Multiple lines of evidence also point to the importance of long-term slightly polygynous sociosexual bonds as the typical context in which humans have sex. These lines of evidence include cross-cultural marital data, including among recent hunter-gatherers, as well as neuroendocrine mechanisms of romantic love and anatomical and physiological data indicating low sperm competition American Journal of Physical Anthropology

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pressures. The phylogenetic origins of these long-term bonds, by most accounts, appear to trace to the genus Homo, with ongoing debate about the most likely timing of shifts with earlier Homo vs. Homo heidelbergensis vs. Homo sapiens. At the same time, the expression of human sexuality exhibits considerable within- and between-population variation. Rates of polygynous marriage, affairs, masturbation and other features of sexuality vary, which underscores the point that sexuality needs to be placed within its social context. Such an observation argues against any simplistic and deterministic view of the interaction between the heritable basis of sexuality and socioecological context. Furthermore, a life course perspective recognizes that age-related aspects of human sexuality have a structure to them that can be understood with respect to life history theory. Human sexuality has a course ranging from juvenile sex play to diminished rates of sexual behavior with advanced age. The world of human sexuality continues to spawn new questions and new insights. Although an evolutionary perspective has previously been brought to bear on human sexuality, in both past and present contexts, the scholarship on this subject itself has been evolving. As we saw in theoretical discussions, some foundational concepts have been subject to scrutiny, even as a refined understanding emerges. Important features of demography and social context influence the details of sexual behavior in humans, just as in other species. New genetic, genomic, and physiological data have added to our understanding of human sexuality in a variety of ways, and will continue to enrich some of the most cutting-edge of understandings in the field. One of the most exciting areas will be to clarify the timing of evolutionary shifts in hominin sexual behavior through genetic research. Another exciting avenue will be to specify the heritable basis to human long-term sociosexual bonds. New fossil and archaeological finds will provide greater comparative, functional, and phylogenetic insight into the evolution of human sexual behavior too. Neuroendocrine mechanisms constraining and regulating human sexuality represent a growing avenue of research, with new findings regularly revealed from brain imaging and hormonal studies. However, the cultural scope of this work, especially brain imaging studies, has been quite narrow. The availability of large, quantitative studies offers unprecedented insights into patterns of human sexuality in the U.S. and internationally. Many of these studies rely upon randomized, probability studies of populations from various countries. Differences in human sexuality have been noted with respect to sex, sexual orientation, and age, among other central variables. The Internet also serves as a growing resource into the evolutionaryinspired investigation into human sexuality, revealing that patterns of accessing sexual content in this technologically new domain draw upon long-evolved mechanisms. Additionally, claims regarding sex differences or societal-specific patterns of sexuality can ideally be situated within a life course perspective and life history theory. Patterns of human sexuality exhibit sex-, age-, and context-specific differences that contribute to the richest and most integrative understanding of human sexuality. That said, there is a decided shortage of welldesigned studies investigating specific features of human sexuality in particular small-scale socioecological contexts. That is one reason why much older data on, for American Journal of Physical Anthropology

example, postpartum women’s sex taboos, may still be drawn upon. Biological anthropologists are well-suited to conceptualizing specific facets or cases of human sexuality within evolutionary and life history theory. Just as Charles Darwin long-ago showed us, the most integrative and robust understanding of human sexuality is rooted in an evolutionary perspective.

ACKNOWLEDGMENTS For comments on an earlier draft, I thank Kali Bertelsen, Bill Jankowiak, Matthew Martinez, Timothy McHale, Michael Moncrieff, David Puts, Shelly Volsche, and Sharon Young.

LITERATURE CITED Alvergne A, Lummaa V. 2010. Does the contraceptive pill alter mate choice in humans? TREE 25:171–179. Andersson M. 1994. Sexual selection. Princeton, NJ: Princeton University Press. Apostolou M. 2007. Sexual selection under parental choice: The role of parents in the evolution of human mating. Evol Hum Behav 28:403–409. Archer J. 2006. Testosterone and human aggression: an evaluation of the Challenge Hypothesis. Neurosci Biobehav Rev 30: 319–345. Archer J, Coyne SM. 2005. An integrated review of indirect, relational, and social aggression. Pers Soc Psychol Rev 9:212– 230. Avis NE, Brockwell S, Randolph JF Jr, Shen S, Cain VS, Ory M, Greendale GA. 2009. Longitudinal changes in sexual functioning as women transition through menopause: results from the study of women’s health across the nation (SWAN). Menopause 16:442–452. Aron A, Fisher H, Mashek DJ, Strong G, Li H, Brown LL. 2005. Reward, motivation, and emotion systems associated with early-stage intense romantic love. J Neurophysiol 94: 327–337. Baker RR, Bellis MA. 1994. Human sperm competition: copulation, masturbation and infidelity. New York: Springer. Bancroft J. 2005. The endocrinology of sexual arousal. J Endocrinol 186:411–427. Bateman A J. 1948. Intra-sexual selection in drosophila. Heredity 2:349–368. Bartels A, Zeki S. 2000. The neural basis of romantic love. Neuroreport 11:3829–3834. Baumeister RF, Catanese KR, Vohs KD. 2001. Is there a gender difference in strength of sex drive? Theoretical views, conceptual distinctions, and a review of relevant evidence. Pers Soc Psychol Rev 5:242–273. Beach FA. 1976. Sexual attractivity, proceptivity, and receptivity. Horm Behav 7:105–138. Berndt R, Berndt C. 1951. Sexual behavior in Arnhem land. New York: Viking Fund. Betzig L. 2012. Means, variances, and ranges in reproductive success: comparative evidence. Evol Human Behav 33:309– 317. Birkhead T. 2000. Promiscuity. Cambridge: Harvard University Press. Bliege Bird R. 1999. Cooperation and conflict: The behavioral ecology of the sexual division of labor. Evol Anthropol 8:65– 75. Blurton Jones NG, Marlowe F, Hawkes K, O’Connell JF. 2000. Hunter-gatherer divorce rates and the paternal provisioning theory of human monogamy. In: Cronk L, Chagnon N, Irons W, editors. Adaptation and human behavior: an anthropological perspective. New York: Aldine. p 65–84. Bogin B 1999. Patterns of human growth, 2nd ed. New York: Cambridge University Press. Brewis A, Meyer M. 2005a. Demographic evidence that human ovulation is undetectable (at least in pair bonds). Curr Anthropol 46:465–471.

EVOLUTION AND HUMAN SEXUALITY Brewis A, Meyer M. 2005b. Marital coitus across the life course. J Biosoc Sci 37:499–518. Brown GR, Laland KN, Borgerhoff Mulder M. 2009. Bateman’s principles and human sex roles. TREE 24:297–304. Brunet M, Guy F, Pilbeam D, Lieberman DE, Likius A, Mackaye HT, Ponce de Leon MS, Zollikofer CPE, Vignaud P 2005. New material of the earliest hominid from the Upper Miocene of Chad. Nature 434:752–755. Buss DM. 1989. Sex differences in human mate preferences: evolutionary hypotheses tested in 37 cultures. Behav Brain Sci 12:1–49. Buss DM. 2003. The evolution of desire: strategies of human mating. New York: Basic Books. Campbell A. 1999. Staying alive: evolution, culture and women’s intra-sexual selection. Behav Brain Sci 22:203–252. Carmichael MS, Humbert R, Dixen J, Palmisano G, Greenleaf W, Davidson JM. 1987. Plasma oxytocin increases in the human sexual response. J Clin Endocrinol Metab 64:27–31. Carnahan SJ, Jensen-Seaman MI. 2008. Hominoid seminal protein evolution and ancestral mating behavior. Am J Primatol 70:939–948. Chapais B. 2008. Primeval kinship: how pair-bonding gave birth to human society. Cambridge, MA: Harvard University Press. Chapman T, Arnqvist G, Bangham J, Rowe L. 2003. Sexual conflict. TREE 18:41–47. Chimpanzee Sequencing and Analysis Consortium. 2005. Initial sequence of the chimpanzee genome and comparison with the human genome. Nature 437:69–87. Chivers ML, Seto MC, Lalumeire ML, Laan E, Grimbos T. 2010. Agreement of self-reported and genital measures of sexual arousal in men and women: a meta-analysis. Arch Sex Behav 39:5–56. Clark NL, Swanson WJ. 2005. Pervasive adaptive evolution in primate seminal proteins. PLoS Genet 1(3):e35. Clutton-Brock T, McAuliffe K. 2009. Female mate choice in mammals. Q Rev Biol 84:3–27. Clutton-Brock TH, Vincent ACJ. 1991. Sexual selection and the potential reproductive rates of males and females. Science 351:58–60. Crompton RH, Vereecke EE, Thorpe SKS. 2008. Locomotion and posture from the common hominoid ancestor to fully modern humans, with special reference to the last common panin/hominin ancestor. J Anat 212:501–543. Darwin C. 1871. The descent of man, and selection in relation to sex. Princeton, NJ: Princeton University Press. Dean C, Leakey MG, Reid D, Schrenk F, Schwartz GT, Stringer C, Walker A. 2001. Growth processes in teeth distinguish modern humans from Homo erectus and earlier hominins. Nature 414:628–631. Dennerstein L, Alexander JL, Kotz K. 2003. The menopause and sexual functioning: a review of the population-based studies. Annu Rev Sex Res 14:64–82. Disotell TR. 2012. Archaic human genomics. Yearb Phys Anthropol 55:24–39. Ditzen B, Schaer M, Gabriel B, Bodenmann G, Ehlert U, Heinrichs M. 2009. Intranasal oxytocin increases positive communication and reduces cortisol levels during couple conflict. Biol Psychiatry 65:728–731. Dixson AF. 2009. Sexual selection and the origins of human mating systems. New York: Oxford University Press. Dixson AF. 2012. Primate sexuality, 2nd ed. New York: Oxford University Press. Durante KM, Li NP, Haselton MG. 2008. Changes in women’s choice of dress across the ovulatory cycle: naturalistic and laboratory task-based evidence. Pers Soc Psychol Bull 34: 1451–1460. Eberhard WG. 1996. Female control: sexual selection by cryptic female choice. Princeton: Princeton University Press. Ellison PT. 2001. On fertile ground. Cambridge, MA: Harvard University Press. Emlen ST, Oring LW. 1977. Ecology, sexual selection, and the evolution of mating systems. Science 197:215–223.

115

Escasa MJ, Casey J, Gray PB. 2011. Salivary testosterone levels in men at a U.S. sex club. Arch Sex Behav 40:921–926. Escasa-Dorne MJ, Young SM, Gray PB. 2013. Now or later: peripartum shifts in female sociosexuality. In: Fisher ML, Garcia JR, Sokol Chang R, editors. Evolution’s empress. New York: Cambridge University Press. p 260–277. Fisher HE. 1982. The sex contract. New York: Quill. Fisher HE, Aron A, Brown LL. 2006. Romantic love: a mammalian brain system for mate choice. Philos Trans R Soc Lond B Biol Sci 361:2173–2186. Foley R, Gamble C. 2009. The ecology of social transitions in human evolution. Philos Trans Roy Soc B 364:3267–3279. Ford CS, Beach FA 1951. Patterns of sexual behavior. New York: Ace Books. Frayser S. 1985. Varieties of sexual experience. New Haven, CT: HRAF Press. Gangestad SW, Thornhill R. 2008. Human oestrus. Proc Roy Soc B 275:991–1000. Gat A. 2006. War in human civilization. New York: Oxford University Press. Garcia JR, MacKillop J, Aller EL, Merriwether AM, Wilson DS, Lum JK. 2010. Associations between dopamine D4 receptor gene variation with both infidelity and sexual promiscuity. PLoS ONE 5:e14162. Garcia JR, Reiber C, Massey SG, Merriwether AM. 2012. Hookup culture: a review. Rev Gen Psychol 16:161–176. Geary DC. 2010. Male, female: the evolution of human sex differences, 2nd ed. Washington, D.C.: American Psychological Association. Geary DC. 2002. Sexual selection and human life history. Adv Child Behav Devel 30:41–101. Geary DC, Flinn MV. 2001. Evolution of human parental behavior and the human family. Parenting 1:5–61. Gentry GA, Lowe M, Alford G, Nevins R. 1988. Sequence analyses of herpesviral enzymes suggest an ancient origin for human sexual behavior. Proc Natl Acad Sci 85:2658–2661. Georgiadis JR, Reinders AA, Paans AM, Renken R, Kortekaas R. 2009. Men versus women on sexual brain function: prominent differences during tactile genital stimulation, but not during orgasm. Hum Brain Mapp 30:3089–3101. Gettler LT, McDade TW, Feranil AB, Kuzawa CW. 2011. Longitudinal evidence that fatherhood decreases testosterone in human males. Proc Natl Acad Sci 108:16194–16199. Good JM, Wiebe V, Albert FW, Burbano HA, Kircher M, Green RE, Halbwax M, Andre C, Atencia R, Fischer A, Paabo S. 2013. Comparative population genomics of the ejaculate in humans and the great apes. Mol Biol Evol 30:964–976. Goodman M, Porter CA, Czelusniak J, Page SL, Schneider H, Shoshani J, Gunnell G, Groves CP. 1998. Toward a phylogenetic classification of primates based on DNA evidence complemented by fossil evidence. Mol Phylogenet Evol 9:585–598. Gowaty P, Kim Y-K, Anderson WW. 2012. No evidence of sexual selection in a repetition of Bateman’s classic study of Drosophila melanogaster. Proc Natl Acad Sci 109:11740–11745. Gray P, Campbell B. 2005. Erectile dysfunction and its correlates among the Ariaal of northern Kenya. Intl J Impot Res 17:445–449. Gray PB. 2003. Marriage, parenting, and testosterone variation among Kenyan Swahili men. Am J Phys Anthropol 122:279– 286. Gray PB, Anderson KG. 2010. Fatherhood: evolution and human paternal behavior. Cambridge: Harvard University Press. Gray PB, Campbell BC. 2009. Human male testosterone, pair bonding and fatherhood. In: Ellison PT, Gray PB, editors. Endocrinology of social relationships. Cambridge, MA: Harvard University Press. Gray PB, Garcia JR. 2012. Aging and human sexual behavior. Gerontol 58:446–452. Gray PB, Garcia JR. 2013. Evolution and human sexual behavior. Cambridge, MA: Harvard University Press. Gray PB, Yang CF, Pope HG Jr. 2006. Fathers have lower salivary testosterone levels than unmarried men and married non-fathers in Beijing, China. Proc Biol Sci 273:333–339.

American Journal of Physical Anthropology

116

P.B. GRAY

Grewen KM, Girdler SS, Amico J, Light KC. 2005. Effects of partner support on resting oxytocin, cortisol, norepinephrine, and blood pressure before and after warm partner contact. Psychosom Med 67:531–538. Gueguen N. 2009. Menstrual cycle phases and female receptivity to a courtship solicitation: an evaluation in a nightclub. Evol Hum Behav 30:351–355. Guttentag M, Secord PF. 1983. Too many women? The sex ratio question. Beverly Hills, CA: Sage. Hammock EAD, Young LJ. 2005. Microsatellite instability generates diversity in brain and sociobehavioral traits. Science 308:1630–1634. Harcourt AH, Harvey PH, Larson SG, Short RV. 1981. Testis weight, body weight and breeding system in primates. Nature 293:55–57. Harmon E. 2009. Size and shape variation in the proximal femur of Australopithecus. J Hum Evol 56:551–559. Harpending H, Cochran G. 2002. In our genes. Proc Natl Acad Sci 99:10–2. Hausfater G, Hrdy SB. 1984. Infanticide: comparative and evolutionary perspectives. New York: Aldine. Hawkes K. 2004. Mating, parenting, and the evolution of human pair bonds. In: Chapais B, Berman CM, editors. Kinship and behavior in primates. New York: Oxford University Press. p 443–473. Hawkes K, O’Connell JF, Blurton Jones NG, Charnov EL, Alvarez H. 1998. Grandmothering, menopause, and the evolution of human life histories. Proc Natl Acad Sci 95:1336– 1339. Hawkes K, Paine R, editors. 2006. The evolution of human life history. New Mexico: School of American Research. Hawks, 2011. http://johnhawks.net/weblog/reviews/neandertals/ neandertal_dna/penis-spines-mclean-2011.html. Herbenick D, Reece M, Schick V, Sanders SA, Dodge B, Fortenberry JD. 2010. Sexual behavior in the United States: results from a national probability sample of men and women ages 14–94. J Sex Med 7:255–265. Herdt G, McClintock M. 2000. The magical age of 10. Arch Sex Behav 29:587–606. Hewlett BS, Hewlett BL. 2010. Sex and searching for children among Aka foragers and Ngandu farmers of Central Africa. Afr Study Monographs 31:107–125. Heyer ER, Chaix R, Pavard S, Austerlitz F. 2012. Sex-specific demographic behaviours that shape human genomic variation. Mol Ecol 21:597–612. Howell N. 2010. Life histories of the Dobe !Kung. Berkeley: University of California Press. Hrdy SB. 1981. The woman that never evolved. Cambridge, MA: Harvard University Press. Hrdy SB. 1999. Mother nature: a natural history of mothers, infants, and natural selection. New York: Pantheon. Hrdy SB. 2009. Mothers and others: the evolutionary origins of mutual understanding. Cambridge, MA: Belknap Press of Harvard University Press. Hughes JF, Skaletsky H, Pyntikova T, Graves TA, van Daalen SKM, et al. 2010. Chimpanzee and human Y chromosomes are remarkably divergent in structure and gene content. Nature 463:536–539. Jankowiak W, editor. 2008. Intimacies: love and sex across cultures. New York: Columbia University Press. Jankowiak W, Sudakov M, Wilreker BC. 2005. Co-wife conflict and co-operation. Ethnology 44:81–98. Kaplan H, Hill K, Lancaster J, Hurtado AM. 2000. A theory of human life history evolution: diet, intelligence, and longevity. Evol Anthropol 9:156–185. Kelly R. 1995. The foraging spectrum. Washington, D.C.: Smithsonian Press. Kerns V, Brown JK, editors. 1992. In her prime: new views of middle-aged women, 2nd ed. Urbana and Chicago: University of Illinois Press. Kiecolt-Glaser JK, Bane C, Glaser M, Malarkey WB. 2003. Love, marriage, and divorce: newlyweds’ stress hormones foreshadow relationship changes. J Consult Clin Psychol 71: 176–188.

American Journal of Physical Anthropology

Kinsey A, Pomeroy WB, Martin CE. 1948. Sexual behavior in the human male. Philadelphia: Saunders. Kinsey A, Pomeroy W, Martin C, Gebhard P. 1953. Sexual behavior in the human female. Philadelphia: Saunders. Kirkpatrick RC. 2000. The evolution of human homosexual behavior. Curr Anthropol 41:385–413. Kokko H, Jennions M. 2003. It takes two to tango. Trends Ecol Evol 18:103–104. Kokko H, Jennions MD. 2008a. Parental investment, sexual selection and sex ratios. J Evol Biol 21:919–948. Kokko H, Jennions MD. 2008b. Sexual conflict: battle of the sexes reversed. Curr Biol 18:R121–R123. Komisaruk BR, Whipple B. 2005. Functional MRI of the brain during orgasm in women. Annu Rev Sex Res 16:62–86. Kruger THC, Haake P, Chereath D, Knapp W, Janssen OE, Exton MS, Schedlowski M, Hartmann U. 2003. Specificity of the neuroendocrine response to orgasm during sexual arousal in men. J Endocrinol 177:57–64. Labuda D, Lefebre J-F, Nadeau P, Roy-Gagnon M-H. 2010. Female-to-male breeding ratio in modern humans—an analysis based on historical recombinations. Am J Hum Genet 86: 353–363. Lassek WD, Gaulin JC. 2009. Costs and benefits of fat-free muscle mass in men: relationship to mating success, dietary requirements, and native immunity. Evol Hum Behav 30: 322–328. Laumann EO, Gagnon JH, Michael RT, Michaels S. 1994. The social organization of sexuality: sexual practices in the United States. Chicago: University of Chicago Press. Lieberman DE. 2011. The evolution of the human head. Cambridge, MA: Harvard University Press. Lindau ST, Schumm LP, Laumann EO et al. 2007. A study of sexuality and health among older adults in the United States. N Engl J Med 357:762–774. Lockwood CA. 1999. Sexual dimorphism in the face of Australopithecus africanus. Am J Phys Anthropol 108:97–127. Lockwood CA, Menter CG, Moggi-Cecchi J, Keyser AW. 2007. Extended male growth in a fossil hominin species. Science 318:1443–1446. Lovejoy CO. 2009. Reexamining human origins in light of Ardipithecus. Science 326:74e1–7. Low BS. 2000. Why sex matters. Princeton: Princeton University Press. Lukas D, Clutton-Brock TH. 2013. The evolution of social monogamy in mammals. Science 341:526–530. Maccoby EE. 1998. The two sexes: growing up apart, coming together. Cambridge: Harvard University Press. Mallants C, Casteels K. 2008. Practical approach to childhood masturbation—a review. Eur J Pediatr 167:1111–1117. Manson JH. 2011. Mate choice. In: Campbell CJ, Fuentes A, MacKinnon KC, Bearder SK, Stumpf R, editors. Primates in perspective, 2nd ed. New York: Oxford University Press. Marlowe FW. 2003. A critical period for provisioning by Hadza men: implications for pair bonding. Evol Hum Behav 24:217– 229. Marlowe FW. 2005. Hunter-gatherers and human evolution. Evol Anthropol 14:54–67. Marlowe FW. 2007. Hunting and gathering: the human sexual division of foraging labor. Cross-Cultural Res 41:170–195. Marlowe FW. 2010. The Hadza: hunter-gatherers of Tanzania. Berkeley and Los Angeles: University of California. Mazur A, Michalek J. 1998. Marriage, divorce and male testosterone. Soc Forces 77:315–330. McHenry HM. 1994. Behavioral ecological implications of early hominin body size. J Hum Evol 27:77–87. McLean CY, Reno PL, Pollen AA, Bassan AI, Capellini TD, Guenther C, Indjeian VB, Lim X, Menke DB, Schaar BT, Wenger AM, Bejerano G, Kinsley DM. 2011. Human-specific loss of regulatory DNA and the evolution of human-specific traits. Nature 471:216–219. Meizner I. 1987. Sonographic observation of in utero fetal ‘masturbation’. J Ultrasound 6:111. Mesnick SL. 1997. Sexual alliances: evidence and evolutionary implications. In: Gowaty PA, editor. Feminism and

EVOLUTION AND HUMAN SEXUALITY evolutionary biology: boundaries, intersections and frontiers. New York: Chapman and Hall. Miller G. 2000. The mating mind. London: Heineman. Mitani JC, Call J, Kappeler PM, Palombit RA, Silk JB, Editors. 2012. The evolution of primate societies. Chicago: University of Chicago Press. Mitani JC, Gros-Louis G, Richards AF. 1996. Sexual dimorphism, the operational sex ratio, and the intensity of male competition in polygynous primates. Am Nat 147:966–980. Montagu MFA. 1946. Adolescent sterility. Springfield, IL: CC Thomas. Mubiru JN, Cavazos N, Hemmat P, Garcia-Forey M, Shade RE, Rogers J. 2012. Androgen receptor CAG repeat polymorphism in males of six non-human primate species. J Med Primatol 41:67–70. Muehlenbein, M, ed. 2010. Human evolutionary biology. New York: Cambridge University Press. Muller MN, Emery Thompson ME, Wrangham RW. 2006. Male chimpanzees prefer mating with older females. Curr Biol 16: 2234–2238. Muller MN, Wrangham RW, editors. 2009. Sexual coercion in primates and humans. Cambridge, MA: Harvard University Press. Murdock GP. 1949. Social structure. New York: Free Press. Murdock GP, White DR. 1969. Standard cross-cultural sample. Ethnology 8:329–369. Nelson E, Rolian C, Cashmore L, Shultz S. 2011. Digit ratios predict polygyny in early apes, Ardipithecus, Neanderthals and early modern humans but not in Australopithecus. Proc Roy Soc Lond B 278:1556–1563. Nunn CL. 1999. The evolution of exaggerated sexual swellings in primates and the graded-signal hypothesis. Anim Behav 58:229–246. O’Bleness M, Searles VB, Varki A, Gagneux P, Sikela JM. 2012. Evolution of genetic and genomic features unique to the human lineage. Nat Rev Genet 13:853–866. O’Connell JF, Allen J. 2007. Pre-LGM Sahul (Pleistocene Australia-New Guinea) and the archaeology of early modern humans. In: Mellars P, Boyle K, Bar-Yosef O, Stringer C, editors. Rethinking the human revolution. Cambridge: McDonald Institute for Archaelogical Research. p 395–410. Ogas O, Gaddam S. 2011. A billion wicked thoughts. New York: Dutton. Parish WL, Laumann EO, Mojola SA. 2007. Sexual behavior in China: trends and comparisons. Popul Dev Rev 33:729–756. Parker GA. 1970. Sperm competition and its evolutionary consequences in the insects. Biol Rev 45:525–567. Plavcan JM. 2012. Sexual size dimorphism, canine dimorphism, and male-male competition in primates: where do humans fit in? Hum Nat 23: 45–67. Poiani A. 2010. Animal homosexuality. New York: Cambridge University Press. Prichard ZM, Mackinnon AJ, Jorm AF, Easteal S. 2007. AVPR1A and OXTR polymorphisms are associated with sexual and reproductive behavioral phenotypes in humans. Hum Mutat 28:1150. Prufer K, et al. 2012. The bonobo genome compared with the chimpanzee and human genomes. Nature 486:527–531. Pusey AE. 2012. The magnitude and sources of variation in female reproductive performance. In: Mitani J, Call J, Kappeler P, Palombit R, Silk J, editors. Evolution of primate societies, Chicago: University of Chicago Press. Puts D. 2010. Beauty and the beast: mechanisms of sexual selection in humans. Evol Hum Behav 31:157–175. Quinlan RJ. 2008. Human pair-bonds: evolutionary functions, ecological variation, and adaptive development. Evol Anthropol 17:227–238. Ravel J, Gajer P, Abdo Z, Schneider GM, Koenig SSK, McCulle SL, Karlebach S, Gorle R, Russell G, Tacket CO, Brotman RM, Davis CC, Ault K, Peralta L, Forney LJ. 2011. Vaginal microbiome of reproductive-age women. Proc Natl Acad Sci 108:4680–4687. Reno PL, Meindl RS, McCollum MA, Lovejoy CO. 2003. Sexual dimorphism in Australopithecus afarensis was similar

117

to that of modern humans. Proc Natl Acad Sci 100:9404– 9409. Reynolds JD. 1987. Mating systems and nesting biology of the red-necked phalarope Phaloropus lobatus: what constrains polyandry? Ibis 129:225–242. Robles TF, Shaffer VA, Malarkey WB, Kiecolt-Glaser JK. 2006. Positive behaviors during marital conflict: influences on stress hormones. J Soc Pers Rel 23:305–325. Ryan C, Jetha C. 2010. Sex at dawn: how we mate, how we stray, and what it means for modern relationships. New York: Harper Perennial. Schaefer K, Mitteroecker P, Gunz P, Bernhard M, Bookstein FL. 2004. Craniofacial sexual dimorphism patterns and allometry among extant hominids. Ann Anat 186:471–478. Schlegel A, Barry H III. 1991. Adolescence: an anthropologicaliInquiry. New York: The Free Press. Schmitt DP. 2003. Universal sex differences in the desire for sexual variety: tests from 52 nations, 6 continents, and 13 islands.” J Pers Soc Psychol 85:85–104. Schmitt DP. 2005. Sociosexuality from Argentina to Zimbabwe: a 48-nation study of sex, culture, and strategies of human mating.” Behav Brain Sci 28:247–311. Senut B, et al. 2001. First hominid from the Miocene (Lukeino Formation, Kenya). CR Acad Sci Paris 332:137–144. Shoskak M. 1981. Nisa, the life and words of a !Kung woman. Cambridge, MA: Harvard University Press. Short RV. 1976. The evolution of human reproduction. Proc Roy Soc Lond B 195:3–24. Simpson SW, Quade J, Levin NE, Butler R, Dupont-Nivet G, Everett M, Semaw S. 2008. A female Homo erectus pelvis from Gona, Ethiopia. Science 322:1089–1092. Smith EA. 2004. Why do good hunters have higher reproductive success? Hum Nat 15:343–364. Smuts BB. 1985. Sex and friendship in baboons. New York: Aldine. Smuts BB. 1992. Male aggression against women: An evolutionary perspective. Hum Nat 3:1–44. Starkweather KE, Hames R. 2012. A survey of non-classical polyandry. Hum Nat 23:149–172. Stearns SC. 1992. The evolution of life histories. New York: Oxford University Press. Stockley P, Bro-Jorgensen J. 2011. Female competition and its evolutionary consequences in mammals. Biol Rev Camb Philos Soc 86:341–366. Strassman BI. 1981. Sexual selection, paternal care, and concealed ovulation in humans. Ethol Sociobiol 2:31–40. Strier KB. 1990. New world primates, new frontiers: Insights from the woolly spider monkey, or muriqui (Brachyteles arachnoides). Int J Primatol 11:7–19. Symons D. 1979. The evolution of human sexuality. New York: Oxford University Press. Tinbergen N. 1963. On aims and methods in ethology. Zeitschrift fur Tierpsychologie 20:410–433. Trivers R. 1972. Parental investment and sexual selection. In Sexual Selection and the Descent of Man, ed. BC Campbell, 136-179. Chicago: Aldine. Van Schaik CP, Dunbar RIM. 1990. The evolution of monogamy in large primates: A new hypothesis and some crucial tests. Behaviour 115:30–62. Vitzhum V. 2009. The ecology and evolutionary endocrinology of reproduction in the human female. Ybk Phys Anthropol 49: 95–136. Van Anders SM, Brotto L, Farrell J, Yule M. 2009. Associations between physiological and subjective sexual responses, sexual desire, and salivary steroid hormones in healthy premenopausal women. J Sex Res 6:739–751. Van Anders SM, Gray PB. 2007. Hormones and human partnering. Ann Rev Sex Res 18:60–93. Van Anders SM, Watson NV. 2006. Social neuroendocrinology: effects of social contexts and behaviors on sex steroids in humans. Hum Nat 17:212–237. Van Schaik CP. 1983. Why are diurnal primates living in groups? Behav 87:120–144. Van Schaik CP, Janson CH, Eds. 2000. Infanicide by males and its implications. Cambridge: Cambridge University Press.

American Journal of Physical Anthropology

118

P.B. GRAY

Von Sydow K. 1999. Sexuality during pregnancy and after childbirth: a metacontent analysis of 59 studies. J Psychosom Res 47:27–49. Walker AC, Leakey RE, Eds. 1993. The Nariokotome Homo erectus skeleton. Cambridge: Cambridge University Press. Walker RS, Hill KR, Flinn MV, Ellsworth RM. 2011. Evolutionary history of hunter-gatherer marriage practices. PLoS ONE 6:e19066. Walum H, Westberg L, Henningsson S, Neiderhiser JM, Reiss D, Igl W, Ganiban JM, Spotts EL, Pedersen NL, Eriksson E, Lichtenstein P. 2008. Genetic variation in the vasopressin receptor 1a gene (AVPR1A) associates with pair-bonding behavior in humans. Proc Natl Acad Sci 105: 14153–14156. Weisfeld GE. 1999. Evolutionary principles of human adolescence. New York: Basic Books. Wellings K, Collumbien M, Slaymaker E, Singh S, Hodges Z, Patel D, Bajos N. 2006. Sexual behavior in context: a global perspective. Lancet 368:1706–1728. Wilcox AJ, Baird DD, Dunson DB, McConnaughey DR, Kesner JS, Weinberg CR. 2004. On the frequency of intercourse

American Journal of Physical Anthropology

around ovulation: Evidence for biological influences. Hum Reprod 19:1539–1543. Williams GC. 1957. Pleiotropy, natural selection, and the evolution of senescence. Evolution 11:398–411. Winking J, Kaplan H, Gurven M, Rucas S. 2007. Why do men marry and why do they stray? Proc Roy Soc B: Biol Sci 274: 1643–1649. Winn RL, Newton N. 1982. Sexuality in aging: a study of 106 cultures. Arch Sex Behav 11:283–298. Wood B, Lonergan N. 2008. The hominin fossil record: taxa, grades and clades. J Anat 212:354–376. Wrangham RW. 1979. On the evolution of ape social systems. Soc Sci Info 18:335–368. Wrangham RW, Jones JH, Laden G, Pilbeam D, ConklinBritain N. 1999. The raw and the stolen: cooking and the ecology of human origins. Curr Anthropol 40:567–594. Yang CF, Gray P, Pope HG Jr. 2005. Male body image in Taiwan versus the West: Yanggang Zhiqi meets the Adonis complex. Am J Psychiatry 162:263–269. Zeki S, Romaya JP. 2010. The brain reaction to viewing faces of opposite- and same-sex romantic partners. PLoS ONE 5(12): e15802.