Human sexuality is most broadly defined as the totality of experiences, systems, attributes, and behavior that characterize the sexual sensation, reproduction, and intimacy of Homo sapiens.
Human sexuality, a remarkably broad topic, is the purview of numerous academic fields and is a discipline unto itself. Scientific perspectives of human sexuality encompass, variously, its reproductive, social, cultural, emotional, and biological aspects. Evolutionary psychologists frame these facets by asking the following question: What is the design of the system – that is, what are the evolutionary forces that have likely shaped the constitution of human sexuality?
The present chapter is focused on human sexuality from the perspective of the evolved nature of mating systems. The main advantage of this focus is that it facilitates broad considerations about the evolutionary biology and psychology of human mating. By the same token, a mating systems approach leaves many aspects of human sexuality unaddressed, namely, those that have less clear implications for reproduction. Omission of a topic does not necessarily reflect a lack of relevant evolutionary research; on the contrary, evolutionary psychologists engage deeply with all matters of human sexuality. For further reading on sexual diversity or nonreproductive sexuality, please see entries in this volume such as “Evolution of Homosexuality,” “Same-Sex Sexual Behavior,” “Human Copulation,” “Sexual Identity,” and “Sexual Pathology.”
Human Sexuality and the Comparative Approach
Many aspects of human sexuality are unique among species, but usually by a matter of degree than of kind. This general observation has two implications. First, by using phylogenetic comparative methods (for instance, comparing features of human mating to those of the other, extant great apes), one can attempt to draw general conclusions about the likely ancestral makeup of human sexuality. Second, a comparative approach can also reveal instances in which human sexuality meets or violates expectations (for instance, showing ways in which human sexual adaptations are compatible or incompatible with a given mating system). More generally, a comparative approach has value for informing an understanding of the forces that have led to the current state of human sexuality. A comparative perspective is emphasized in Tinbergen’s (1963) “four questions” (about mechanism, ontogeny, adaptive value, and phylogeny) for explaining behavior. Therefore, a recurring tool throughout this entry will be comparisons with sexuality studies in nonhumans.
A Note on Hormonal Mechanisms Underlying Human Sexuality
Endocrine systems constitute an important class of proximate biological mechanisms underlying human sexuality. Hormones are chemical “messengers” that allocate limited physiological and psychological resources throughout an organism. As detailed below, hormones provide some of the physiological background for many of the hallmarks of human mating systems, including pair-bonding, parental care, and mutual mate choice. At a theoretical level, hormones – both independently and in concert with one another – are mediators of an organism’s life history reproductive strategy, linking physiology, and behavior in the partitioning of energy between mating, parenting, and nonreproductive activities (e.g., Del Giudice et al. 2015). For these reasons, hormonal systems are frequently discussed below within the context of human mating adaptations.
Defining Mating Systems
An understanding of mating systems is core to recreating how human sexuality might have evolved. In brief, mating systems dictate who mates with whom, when, and how often. Mating systems emerge from the cost and benefit male and female experience from mate choice and competition for mating opportunities, which in turn select for male and female adaptations. The details of a mating system can thus suggest selection pressures that forged reproductive behavior. But mating systems also cause adaptations, as they affect the reproductive strategies and tactics most beneficial to males and females. Conceptually, therefore, mating systems anchor the various facets of human sexuality discussed below (for an extended discussion of these issues, see Gangestad and Grebe 2015).
Traditional Mating Systems
Monogamy: Males and females have exclusive sexual access to one another.
Polygamy: Sexual exclusivity occurs, but is not monogamous. Three subtypes of polygamy can be discriminated: (a) polygyny, individual males have exclusive sexual access to two or more females; (b) polyandry, individual females have exclusive sexual access to two or more males; and (c) polygynandry, two or more males have exclusive sexual access to two or more females and vice versa.
Promiscuity: Males within a group mate with any and potentially multiple females and vice versa. A subtype of promiscuity is dispersed promiscuity, in which largely asocial individuals with overlapping home ranges mate with multiple partners during brief periods of social grouping (typically, a female’s fertile period; see Dixson 2012).
Monogamy and polygamy assume forms of sexual exclusivity, whereas promiscuity does not. Whereas monogamous mating systems generate variation in reproductive success that is nearly equal across the sexes, polygynous mating systems generate greater male than female variation, and polyandrous mating systems generate greater female than male variation.
Mixed Mating Systems
The traditional categories of mating systems do not exhaustively cover all possibilities; instead, many animal populations exhibit mixed mating systems. In one case, different forms of sexual exclusivity may exist simultaneously. For instance, in avian species typically characterized as polygynous (such that some males mate with two females), monogamous mating arrangements can also occur in the same population. In other cases, different forms of exclusivity may exist temporally or spatially within the same population or species. For instance, individuals of some mockingbird species will mate both monogamously and polygamously depending on available opportunities. Indeed, across the vertebrate species examined, humans included, there is more fluidity in mating system structure than has been recognized historically: Human groups, large and small, have created and can create an array of mixed mating systems.
Selection Pressures Influencing Vertebrate Mating Systems
Traditionally, sexual selection theorists had widely assumed that natural selection would most likely give rise to mating systems characterized by some degree of polygyny. The rationale behind this assumption is known as the “Darwin-Bateman effect”: the increase in offspring number as a function of the number of matings each male procures with different females, without a similar increase occurring as a function of the number of matings each female procures with different males (see Drea 2005; Parker and Birkhead 2013). Ultimately, the differential effect by sex of “multiply mating” was attributed to anisogamy – sexual reproduction involving the union of “expensive” eggs and “cheap sperm” – and to differences by sex in the initial investment in offspring. In placental mammals, internal fertilization and gestation delays the female’s production of new offspring until after birth, fetal or neonatal loss, and/or some period of lactation; males, however, do not experience these same delays. According to this paradigm, whereas males should benefit from seeking multiple mates, females should reap little, if any, benefit from mating multiply. Under many conditions, therefore, selection was expected to favor multiple mating by males, but only rarely by females, thereby driving an increase in polygynous mating systems.
Polygyny can take on different forms depending on male features that foster access to multiple females (e.g., Emlen and Oring 1977). In resource defense polygyny, males control the resources valued by females for fueling offspring production. In male dominance polygyny, which involves leks (small territories where males congregate to display and attract females), males are chosen by females for their ability to compete with other males, but offer no material resources to females to be directed toward investment in offspring.
In this “Darwin-Bateman” view, monogamy typically evolves when males cannot defend the resources that permit them to attract multiple mates. Ecological constraints explain why, for instance, most birds (over 90%) are socially monogamous: Resources are dispersed to a degree that males cannot typically secure enough for more than one female’s offspring (e.g., Emlen and Oring 1977). However, with the development of genetic tools in the late 1980s and early 1990s, researchers began testing some of the assumptions about traditional mating systems, and avian biologists discovered that many pair-bonding birds actually exhibited high rates of extra-pair paternity – paternity by males other than the social partner. This finding, which has now been extended to primates also previously thought to be monogamous (e.g., in gibbons: Palombit 1994), prompted the recognition of an extra-pair mating system. Although most of the sexual activity occurs within structured units (e.g., individual male-individual female units, individual male-multi-female units, and so on), some mating – “extra-pair” mating – occurs outside of these units. In recognition of the social unit in which most mating occurs, systems with pair-bonding and cuckoldry are said to reflect social monogamy with EPC (extra-pair copulation). Some systems entail little EPC, whereas others may entail frequent EPC. Thus, social monogamy with EPC lies on a continuum of degree of sexual exclusivity.
The Polyandry “Revolution” Within Behavioral Biology
Over the past three decades, behavioral ecologists have increasingly recognized the benefits of female multiple mating, which includes EPC in addition to polyandrous mating more generally. Parker and Birkhead (2013) refer to the sea change as a “revolution.” By mating multiply, females could gain both direct benefits that increase reproductive success and indirect benefits that increase the genetic fitness of offspring. Direct benefits can include increased rates of fertilization, increased attainment of resources offered by males, and reduction in male aggression toward offspring via “paternity confusion.” Indirect benefits can include attaining a sire whose DNA is compatible with the mother’s (whereby selection occurs “cryptically” post copulation – within the reproductive tract of the female), diversification of offspring via multiple paternity (bet hedging), and, in the context of extra-pair mating, attaining a sire who potentially has greater genetic fitness (“intrinsic good genes”) than does an in-pair male. As a result of these benefits, female multiple mating is not a rare anomaly; it is commonplace (Parker and Birkhead 2013).
Benefits of Female Multiple Mating
The benefits of multiple mating can arise from multiple sources. To take the example of EPC, whereas many socially monogamous birds engage in extra-pair mating, it remains uncertain if females in particular derive any benefits from it. Males are assumed to benefit from multiple mating, in which case female engagement in EPC may simply reflect male assertion. In some instances, the costs of resisting copulation (e.g., physical harm) outweigh its benefits. Accordingly, EPC can commonly arise exclusively due to male sexual interests and female tolerance, under a scenario of “sexual conflict” (Parker and Birkhead 2013).
Nevertheless, in some avian species, females clearly solicit EPC (e.g., Parker and Birkhead 2013). In this case, the benefits that have the greatest empirical support are direct ones (e.g., parental care, food provisioning). The most controversial interpretation concerns “good gene” benefits. Some researchers conclude that support for genetic benefits of EPC is weak (Parker and Birkhead 2013), whereas others argue that inconclusive data do not necessarily counter a “good genes” interpretation (e.g., Eliassen and Kokko 2008). The jury is still out about whether or not avian EPC functions in a female to gain genetic benefits, and this same uncertainty extends to humans, as noted below in the section “Women’s Mating Adaptations.”
New Models of Sexual Selection Pressures on Males
In recent years, theorists have also questioned the traditional perspective on male interests. In the traditional view based on the Darwin-Bateman effect, males should possess promiscuous sexual motivations and, whenever ecological circumstances permit, compete for the resources or social standing that promote multiple mating. Yet, there are good reasons why males might not pursue this strategy. Males can instead benefit from providing care for their existing offspring. When the net benefits from providing care to offspring exceed the net benefits from competing for mates, males should be selected to care. These conditions are most likely to exist when (a) competing for mates is costly (e.g., males risk injury), relative to the costs of providing care, (b) the net benefits to competing are relatively weak (e.g., a male is not competitive or many males compete), and (c) the benefits to care are relatively great (e.g., males are able to discriminate their own offspring; offspring benefit from complementary care from males and females) (e.g., Kokko and Jennions 2008).
This framework offers a different perspective on why pair-bonding with biparental care is so common in birds. In the traditional view, the focus is on the male’s inability (e.g., due to resource dispersion) to defend resources supportive of multiple mates and their offspring. In the more recent view, the focus is instead on the relatively poor gain from competing and the substantial benefits to male care (see Kokko and Jennions 2008). In avian species especially, one parent may need to forage, while the other defends a nest of offspring that cannot yet fly. Thus, avian research has drawn attention to the importance of male care and its benefits in the evolution of mating systems – a framework that is broadly applicable to other pair-bonding species, including humans.
Hominoid Mating Systems
The Ancestral State
Applying a comparative perspective draws attention to selection pressures that can drive benefits of multiple mating and of male care – what mating systems characterized ancestral human groups that drove male and female mating adaptations? To address this question, one must consider some of the defining features of primates. Notably, within the primate order, females evolved from the “primitive” mammalian condition of strictly circumscribed sexual receptivity (limited to the 2–3-day peri-ovulatory or fertile period) to a more “advanced” state, evidenced by anthropoid primates, of situation-dependent receptivity. Thus, in female anthropoids, sexual behavior is decoupled from fertility, and females can engage in copulation at any stage of their cycle (Dixson 2012). In those primates that show “extended sexuality” (sexual activity outside of fertile phases), the social system can have significant influence over sexual behavior, despite the type of mating system. Such is likely to have been the case for our closest ancestors. But what mating system did this ancestral species possess?
Chimpanzee and Bonobo Mating Systems
Whatever mating systems evolved in humans, they originated from adaptations associated with the system(s) of the shared common ancestor with chimpanzees (Pan troglodytes) and bonobos (Pan paniscus) that existed about 5 million years ago. Chimpanzees and bonobos both live in mixed-sex groups and have promiscuous mating systems, in which females advertise their fertility and show extended sexuality. Females of both species possess hindquarter sexual swellings that serve as “graded signals” of fertility; yet, they are sexually active for a significant portion of their ~30-day cycle, mating with potentially all adult males in the group, typically multiple times. Despite these similarities, these species have highly divergent social organizations that likely impact their sexual strategies. Notably, chimpanzee societies are male dominant and despotic (in which males show female-directed aggression and infanticide), whereas bonobo societies are female dominant, peaceful, and more egalitarian.
In the better-studied chimpanzee, the favored hypothesis for the function of promiscuous mating in females is Hrdy’s (1979): Promiscuous mating confuses paternity. If no male can rule out his own paternity, each is less likely to aggress against the future offspring, thereby reducing the likelihood of infanticide. Nevertheless, there is recent evidence to suggest that the sexual interests of female chimpanzees change across the sexual period. During the non-fertile phase, females are most promiscuous, but during the fertile phase, they tend to prefer particular males (e.g., younger males whose status is rising; Stumpf and Boesch 2005). Perhaps females confuse paternity during non-conceptive portions of their cycle, but when they are fertile, they bias sireship toward males that can offer genetic benefits or certain forms of direct benefits (e.g., physical protection). Indeed, male reproductive success is highly skewed in chimpanzees, with one or two high-quality males typically siring many more offspring than the majority of other adult males, despite female promiscuity (e.g., Stumpf and Boesch 2005).
In bonobos, female coalitions are considerably more powerful than they are in chimpanzee societies. Female-female sociosexual exchanges regulate female social hierarchies and coalitional activity. It would seem that paternity confusion to protect against the threat of infanticide would be an unlikely explanation for female promiscuity in bonobos; it instead appears to be a mechanism for ensuring social harmony. In no study, however, have researchers yet tested for changes in female bonobo sexual activity or male preferences across the cycle. Despite promiscuity, male reproductive skew is strong, suggesting similar bias in mating with certain males at peak fertility (Gerloff et al. 1999).
Human Versus Pan Mating Systems
As Dixson (2012) notes, humans have diverged considerably from both chimpanzees and bonobos in a variety of respects. In chimpanzees, extreme sexual size dimorphism, rank relations in male androgen concentrations, relative testes size and ejaculate volume, structural features of semenogelin proteins (that coagulate sperm), and length of the female reproductive tract are consistent with the high degree of either male-male competition or sperm competition (multiple males’ sperm residing in the female reproductive tract vying for conception) evident in their social and mating systems, respectively. These features in humans are consistent with lower levels of male-male and sperm competition. Nonetheless, human mating adaptations may possess vestiges of Pan mating, as discussed below.
Unique Features of Human Systems
Limits on Reproductive Skew
Hominoids – and humans in particular – have extremely slow life histories, which severely constrains female fertility. Because of the energetic demands of producing highly encephalized infants (and usually only one per pregnancy), hominoid mothers are heavily invested in their young, assuming costs associated with lengthy gestation and lactation, as well as extended infant and juvenile dependency. Women are especially reproductively inefficient, even “infertile”. Beyond the constraints imposed by the concealed release and short-term survival of generally one egg per fertile period, approximately 50% of human cycles are anovulatory or too short to allow implantation. Women also suffer relatively high rates of conception failure, low embryo viability, miscarriage, premature delivery, and perinatal death (reviewed in Drea 2005).
Coupling women’s extended sexuality with the various physiological constraints on her reproduction, there is enhanced potential in humans for non-fertile mating (Drea 2005; Thornhill and Gangestad 2008). The low probability of conception associated with each copulatory act challenges predictions arising from the Darwin-Bateman paradigm about the almost limitless potential for fatherhood as a function of increasing the number of sexual partners. Brown et al. (2009) examined variance in reproductive success across 18 traditional or preindustrial societies. On average, male variance exceeded female variance (median ratio ≈ 1.70); yet, this ratio varies widely (ranging from <1 to nearly 5).
Mating Arrangements and Sexual Exclusivity
One feature entirely unique to modern humans is the influence of cultural evolution on mating systems. Notably, marriage is a near-universal institution in human societies; despite this ubiquity, marriage does not imply near-universal monogamy (or even serial monogamy) in humans. Ethnographic evidence from the standard cross-cultural sample (SCCS) shows that over 80% of present-day, human societies possess some degree of polygyny. Fewer than 20% are completely monogamous, and 1% are characterized by a nonzero level of polyandry. Agriculture, herding, and other relatively recent means of resource production may alter mating arrangements; Western religious traditions promoting marriage do so as well. Marlowe (2003) examined mating arrangements in the SCCS’s 36 foraging groups and found that about 90% exhibit a nonzero level of polygyny. Monogamy is, however, still the most typical, socially sanctioned mating arrangement in human societies. In about two-thirds of foraging societies, for instance, the percentage of polygynously married women is 12% or less (Marlowe 2003); in only 13% of these societies does the rate reach 50%.
Nevertheless, marital systems may or may not imply sexual exclusivity. Although most offspring may be produced by in-pair partners, some may be produced through extra-pair matings. Questions of interest, then, are how common is extra-pair sex and how often does it result in extra-pair paternity (EPP). Anderson (2006) reviewed studies estimating nonpaternity, largely in developed countries. Nearly all samples give biased estimates, depending on how they were selected. High paternity confidence samples estimate an EPP rate averaging just 2%. Samples of men who suspicion about their partner’s fidelity estimate it to be, on average, about 30%. Once again, tremendous variation exists, ranging from <1% in high paternity confidence samples (in Switzerland and Germany) to about 12% (in Monterrey, Mexico). For some other traditional societies, ethnographies report very frequent EPC, but systematic data on EPP rates are scant (Anderson 2006). Within developed countries, extra-pair paternity rates have declined in the past century; the advent of effective birth control may reduce incidence of conceptive EPC, suppressing the EPP rate. In traditional settings, then, EPP rates may have been low on average (5% or less) but variable (in some societies >10%).
As with females of other species, the benefits that give rise to women’s extra-pair mating are debated. Some scholars argue that benefits lie largely (or even exclusively) with male extra-pair partners, while others stress the possibility that women too, in many circumstances, benefit (for a review, see Thornhill and Gangestad 2008).
Consistent with slow life histories, human offspring are, in many respects, remarkably altricial at birth. Compared to other hominoids, humans are born with extreme motor immaturity and brains that represent a relatively small proportion of adult size. As in other primates, human mothers harvest the overwhelming majority of calories consumed by offspring during pregnancy and lactation. For periods longer than in any other primate (i.e., including postweaning), however, human infants continue to be dependent on mothers and others for food, protection, and social development. Because of their extended dependency and juvenility, evolutionary theorists argue that early humans developed a system for rearing their young (and, thus, ensuring their own reproductive success) in which mothers, along with various helpers, cooperate in raising infants (Hrdy 2009). These adaptations for care stem from the nature of human mating systems and life history that inform the likely structure of ancestral human sexuality.
Mothers and Allomothers
The maternal bond or mother-infant relationship is one of the strongest across mammalian species. Its development, which begins in pregnancy, is influenced by the hormone oxytocin (OT). Most generally, OT (along with related homologs in nonmammalian taxa) is a smooth muscle contractor that plays a highly conserved role in orgasm and sexual functioning, as well as in parturition and lactation. OT also functions as a neurotransmitter involved in establishing and maintaining maternal behavior (see Gangestad and Grebe 2017). It is thought that OT’s role in maternity constitutes the “biological prototype” for its functions in facilitating other kinds of social bonds so critical to human society (see section on “Pair-Bonding and Oxytocin”).
Many have argued that the extended period of infant care is intricately linked to the early termination of fertility in women – that the distinct post-reproductive period (i.e., menopause) that characterizes human females allowed reproductively senescent mothers to better ensure their latest progeny’s survival and overall reproductive success, relative to aged mothers who continued to engage in risky pregnancies. This “stopping early” hypothesis has been contrasted with the “grandmother hypothesis” that instead proposes that senior women contribute best to their own inclusive fitness by investing in the reproductive success of their childbearing daughters. Accordingly, the diets of women of reproductive age and their children are subsidized, not primarily by the women’s mates, but through the efforts of maternal kin – most importantly, the mothers’ mothers (Hawkes 2003).
Questions intensely debated within evolutionary anthropology over the past two decades include whether human pair-bonding is central to the mating system and whether males possess adaptations for providing care for offspring. Did ancestral conditions that favored male care, at least contingently, exist recurrently in human groups, leading natural selection to shape male features that promoted care? Although pair-bonding need not imply biparental care, the two are strongly associated in the animal world. Male care potentially comes in many forms: Protection, direct care (e.g., supervision), and provisioning are three prominent categories. In the anthropological literature, two research areas have received significant attention: the role of testosterone (T) in men’s parenting effort and the importance of men’s hunting in provisioning mates and offspring.
Parenting Effort and Testosterone
Across vertebrate taxa, T is a crucial component of a system that functions to facilitate male mating effort by channeling energetic resources to features particularly useful in male-male competition (e.g., muscles, sensitivity to dominance ranks, and cues of social hierarchy) and, due to necessary trade-offs, away from other targets of allocation (e.g., repair, immune function; see Bribiescas 2001). In species in which males exert parental effort, a modification may have evolved: T may also modulate allocations of effort to mating versus parenting (in shorthand, competing vs. caring). In some species in which males invest in offspring (e.g., marmosets, some birds), male T concentrations drop after the birth/hatching of the mates’ offspring (discussed in Bribiescas 2001; also see section on “Mating (Versus Parenting) Effort and Testosterone”).
Views About Hunting as “Parental Effort”
In most primate species, individuals of both sexes are largely responsible for their own subsistence after at most a few years after birth. In most human foraging populations, however, the average adult male generates more calories than he consumes, with the surplus being distributed among kin and, in some cases, non-kin group members. The primary activity through which men generate surplus calories in foraging societies is hunting (broadly defined to include any activity, including fishing, aimed at harvesting animal meat). Although women forage and extract roots (and, in a meaningful minority of societies, produce more calories than do men), only rarely do they hunt to a substantial degree. Human foragers appear to be adapted to a diet consisting of high-quality, calorie-rich foods. Whereas chimpanzees obtain about 95% of their calories from collected foods requiring no manual extraction (e.g., fruits, leaves), only about 8% of calories consumed by modern hunter-gatherers are from foods requiring no manual extraction, with a large proportion (30–80%) derived from vertebrate meat. The level of male contribution to the diet varies considerably across foraging societies (~40–90+%). Women reproductively benefit from the male-generated surplus. Women’s offspring production or, specifically, their inter-birth interval – the delay between the birth of one offspring and the same woman’s next offspring – is aided by male contribution to subsistence (Marlowe 2001).
Thus, a traditional anthropological view is that male surplus food production evolved as paternal care. According to this view, the nuclear family is a key economic unit in the evolution of human mating relations. For subsidies generated by male hunting to function as parental effort, nutrients that men generate must flow to their mates (and then to offspring) or directly to offspring. Additionally, if one adopts the perspective of T as a mediator of mating versus parenting effort, this view of hunting as an instantiation of paternal care suggests it should be associated with T decreases. An alternative view of hunting – in that it primarily functions as an activity to gain new mates – is discussed below in the section “Views About Hunting as “Mating Effort”.”
Adaptations for Mating
In general, patterns of human mating and reproduction are consistent with human pair-bonding and biparental investment, albeit with modest levels of polygyny, nonzero rates of EPC, and notable variability. How do these patterns inform male and female adaptations for mating? These features, in some instances, serve as telltale signatures of the mating system that led them to evolve. The subsections below address evolutionary forces and mechanisms that (a) contribute somewhat equally to mating adaptations in both sexes, (b) are most directly relevant to men’s mating adaptations, and (c) are most directly relevant to women’s mating adaptations.
Mutual Mate Choice
In species in which male and female pairs bond, “mutual mate choice” typically evolves. Members of both sexes are advantaged through preference of some mates over others (e.g., Kokko and Jennions 2008). Studies of mate preferences strongly point to mutual mate choice in modern human societies. In many instances, choice for mates that exhibit good parenting qualities should be preferred. In seeking a long-term mate, both men and women, on average, rate “kindness and understanding” as the top preference. Many other mate preferences for personality traits, however, are characterized by large sex differences (see Conroy-Beam et al. 2015).
Specific forms of mate preference offer particularly compelling examples of adaptation for mutual choice. The human leukocyte antigen (HLA) system, for example, which controls the immune response and pathogen resistance, has been correlated with both odor preferences and, to a lesser extent, facial preferences in potential mates (Winternitz et al. 2017). The HLA is a highly variable gene complex encoding the major histocompatibility complex (MHC) proteins in humans. MHC genes code for cell surface markers that function to “declare” that a cell is uninfected (when the MHC molecule presents only self-peptides) or infected (when the MHC molecule binds a non-self-peptide structure that is “visible” to the immune system). All else being equal, it pays to mate with someone who possesses alleles optimally different from one’s own, either to avoid inbreeding or to produce advantaged heterozygotic offspring. MHC appears to be detectable through signatures in scent (or facial attractiveness). In a variety of species, females prefer the scent of males that possess MHC genes different from their own. Studies strongly suggest that humans too are most sexually attracted to scents of others who possess non-shared MHC alleles. Consistent with mutual mate choice, preferences typically exist in both sexes (reviewed and meta-analyzed in Winternitz et al. 2017). Evidence for mutual mate choice also exists in the domains of voice pitch and facial symmetry, perhaps because these traits too are cues of the bearer’s condition (of which MHC complement is only one feature; see Thornhill and Gangestad 2008).
Pair-Bonding and Oxytocin
As discussed above (see section on “Offspring Care”), OT plays a major role in the formation of social bonds; its role in pair-bonds has become a hot topic within social psychology. Classic comparative studies in voles were the first to implicate OT in sexual pair-bonding, showing that brain neuroanatomy and central nervous activity of the OT system underlie the development of monogamous partner preferences. From this foundation, psychologists have recently begun to examine how OT plays a role in human sexual pair-bonding. Some evidence is consistent with a prosocial role for OT in romantic bonding in both sexes. OT administration leads to more engaged, constructive communication about relationship conflicts and more intense orgasms and greater contentment after intercourse with a pair-bond partner. Success of relationship interventions and overall relationship satisfaction are related to OT concentrations, and both men and women in newly involved couples exhibited high serum concentrations of OT (see Gangestad and Grebe 2017).
In other studies, OT has been linked to distress and attachment anxiety in romantic relationships. These conflicting results reflect a more general uncertainty regarding the overarching function of OT in social behavior (see Gangestad and Grebe 2017). As one possible resolution, it may be that threats to valuable, vulnerable relationships are key triggers of the OT system. This hormonal increase, in turn, then functions to reorient psychological resources toward these relationships. Preliminary evidence from both men and women in romantic bonds is in line with such an interpretation, further suggesting that the role of OT in pair-bonding is central for both sexes. A focus on relationship vulnerability may also generalize to other social bonds regulated by OT – in particular, the mother-infant relationship (see Gangestad and Grebe 2017).
Men’s Mating Adaptations
Mating (Versus Parenting) Effort and Testosterone
Evidence from nonhuman studies are consistent with a T-mediated hormonal system that is sensitive to the relative value of exerting mating versus parental effort. There is increasing evidence to suggest men’s T mediates a similar trade-off. Men with higher T concentrations exhibit greater frequency and intensity of male-male competition, dominance behavior, and mate seeking; in contrast, men who are mated or have offspring typically have lower T concentrations than do single, childless men (reviewed in Gray and Campbell 2009). Some evidence indicates that the association depends partly on changes in T concentrations following changes in mating or paternal status. Additionally, among fathers, those with lower concentrations of T and smaller testes show a pattern of brain activation when looking at photos of their own children, indicative of greater paternal involvement.
The effect of mating status on men’s T concentrations is moderated by men’s interest in pursuing extra-pair relationships with women other than their primary partners. Men who have little interest in or history of extra-pair relationships reveal the typical drop in T concentrations when mated, as compared to their concentrations while single. Men who have interest in extra-pair relationships, by contrast, showed no difference: Their T concentrations were just as high when in relationships as when single (see Gray and Campbell 2009).
Paternity Certainty and Male Care
Because male confidence in paternity is variable, men’s parental efforts may be contingent on cues of paternity, such as self-resemblance. In a large Western sample, men assisted offspring they report as likely to be their own genetic offspring more so than those they suspect reflect EPP (Anderson et al. 2007). Behavioral researchers have examined possible psychological underpinnings of discriminative parenting. In one design, a digital photograph is taken of a participant. The participant’s own face or, alternatively, that of another participant is digitally combined with the face of a small child to create two composite images of child faces – one “self-resembling” and one not. Participants then choose between the children based on their likelihood of investing in (e.g., spending time with, adopting) each child. Men consistently prefer the self-resembling one, an effect not due to conscious recognition of self-resemblance (reviewed in Thornhill and Gangestad 2008).
Views About Hunting as “Mating Effort”
The theory of male-hunting-as-parental-effort, discussed above, faces a fundamental difficulty: Nuclear families are not, in fact, potent economic units in foraging societies. In the Hadza of Tanzania and the Ache of Paraguay, for instance, hunters have little control over the distribution of the meat they generate. Instead, meat (particularly from large game) is shared widely across community members. A Hadza hunter’s own family receives no more meat from his large game kills than what it receives from the same-sized animal a neighbor killed. In one analysis, offspring nutritional status covaried with Hadza women’s foraging returns, but not with men’s returns. Thus, perhaps men’s hunting functions as (i.e., is adapted for) mating effort – effort to compete for access to mates through “showing off” – rather than as parental effort. Men garner prestige through successful hunting exploits, particularly big-game hunting, and this prestige translates into mating opportunities.
Of course, male hunting subsidizes the diets of women and their offspring. But these subsidies, in the male-hunting-as-mating-effort view, are not generated directly by the women’s own mates or by the children’s own fathers. Rather, they are generated through the efforts of men in general to gain mates. The surplus calories generated by male hunting that benefit women and offspring are by-products of men’s showing off – windfalls they enjoy, not benefits men’s efforts were designed to achieve.
A Blended View on Hunting in Relation to Human Sexuality
Historically, men may have benefited from hunting in currencies of enhanced viability of offspring and mating opportunities (e.g., Gurven and Hill 2009). Patterns of Hadza foraging rates and activities support this relationship (Marlowe 2003). Overall, married Hadza women produce as many calories as do married Hadza men. Women with young children, however, do not, because their childcare interferes with effective foraging. In such circumstances, their husbands forage more than they do; in couples with an infant less than 1 year of age, men produce almost 70% of the total calories generated within the family unit. Hadza men’s work efforts (and prey items targeted) adjust in response to the direct food production of wives and the presence or absence of young children. The view that men’s work functions solely as mating effort cannot readily explain this pattern.
Other data also support this blended view. Across societies of the standard cross-cultural sample, pair-bond stability (low divorce rate) associates with children being weaned at older ages. Because lactation interferes with women’s ability to collect food, male subsidy purportedly permits women to invest in young offspring through nursing. Additionally, if men contribute to the household’s consumables, male total contribution to calorie production should predict greater levels of monogamy across societies. This prediction is supported by the available anthropological evidence (see Marlowe 2003; Thornhill and Gangestad 2008).
Women’s Mating Adaptations
The Ovulatory Cycle
Women, like the vast majority of other mammalian females, undergo regular cycles that restrict the window in which successful conception from sexual intercourse is possible. It is thought that these cycles arise, at least in part, because (1) substantial time is required to prepare the uterus for implantation and (2) the production of germ cells and behavioral adaptations essential to ensure conception from sexual intercourse are physiologically exhausting. Periodicities in sexuality are regulated by a concert of hormonal changes, involving luteinizing hormone, follicle-stimulating hormone, estradiol (E2), and progesterone (P4). Together, these hormones function to ensure successful conception, gestation, and parturition (reviewed in Dixson 2012). E2 and P4 have received substantial attention for their roles in the psychology of women’s mating as well (for a review, see Roney 2015).
Mating Effort and Estradiol
In line with other phenotypically integrated hormonal systems, E2’s psychological effects “go along” with its physiological roles to regulate energy allocation – in this case, toward females’ mating effort, perhaps at the expense of other activities, such as feeding (see Roney 2015). Historically, some sexuality researchers have argued that E2 has little, if any, impact on women’s sexual behavior, noting, for instance, that the effect of ovariectomy on women’s sexual behavior is less than the effect on comparable sexual behavior in other female primates (Dixson 2012). In the most robustly designed study to date, however, researchers sampled women continuously throughout multiple cycles and found that E2 does, in fact, predict overall levels of female sexual desire (reviewed in Roney 2015).
Social Bonding and Progesterone
The role of P4 in human sexual behavior has received relatively less attention. Dixson (2012) reviewed studies involving the administration of P4 to female nonhuman primates, in which the general finding was that P4 diminishes sexual receptivity and proceptivity. Roney (2015) argues that because women’s P4 concentrations associate negatively with subjective sexual desire, P4 is a “stop signal” for sexual motivation that facilitates a shift toward other activities. An alternative viewpoint is that P4 modifies the nature of sexual motivation. P4 is most consistently elevated at two times: during the luteal phase and during pregnancy. During these non-conceptive phases, in which women still initiate and accept sexual advances, P4 may have been selected because it shifted sexual interests to allow focus on pair-bond relationships, perhaps especially when the male partner’s interest in the relationship lags behind that of the woman (Gangestad and Grebe 2017). During pregnancy, women may have particularly benefited from consolidating social support from a pair-bond partner, kin, or trusted friends. Preliminary evidence is consistent with an interpretation of P4 facilitating bonding in a targeted manner, rather than it contributing to generalized affiliative motives (see Gangestad and Grebe 2017).
Cyclic Shifts in Women’s Mating Behavior and Preferences
Whereas ovarian hormones may be the proximate biological factors thought to underlie changes in women’s sexuality, cycle phase (i.e., fertile vs. non-fertile windows) provides a relevant functional distinction for understanding adaptations in women’s sexual behavior. Changes in concentrations of E2 and P4 that result from the physiology of the ovarian cycle convey information, via the neuromodulatory effects of these hormones, related to fecundity (i.e., the probability of successful conception and gestation). Presumably, because the costs and benefits of sexual activity differ depending on whether or not conception is possible, women’s mating adaptations should shift accordingly. A substantial literature has accumulated addressing if and how women’s sexual preferences and behavior shift as a function of where they are in their cycle.
In most vertebrate species, females are only sexually receptive during their fertile reproductive phase. Consistent with early views about the minimal influence of E2 on women’s sexuality, initial accounts on the evolution of human sexuality minimized or entirely discarded the idea of a distinct fertile-phase sexuality in women, proposing that it was lost and replaced by continuous, unchanging sexual receptivity across the ovarian cycle. Decades of empirical research have since shown that while sexual frequency may not always vary across the ovulatory cycle, women’s sexual behavior, preferences, and interests clearly do change (see Thornhill and Gangestad 2008). In an impressive longitudinal study following over 400 naturally cycling women, Arslan et al. (2017) found that women in the peri-ovulatory period, compared to during non-fertile phases, reported increased extra-pair sexual desire and behavior, in-pair sexual desire, and self-perceived desirability. Additionally, when fertile, women may be more attracted to certain male features, such as masculine bodies and behavioral dominance. And, should the women’s primary partners lack those desired features, fertile women (only) report greater attraction to men other than their partners (findings reviewed and meta-analyzed in Gildersleeve et al. 2014). Thus, one possibility is that women’s fertile-phase sexuality is attuned to certain male features when fertile – namely, those that represent “good genes” that could be transmitted to offspring (Thornhill and Gangestad 2008). In cases in which primary partners lack these features, women’s mating adaptations could facilitate EPCs. Nonetheless, other possibilities cannot be ruled out: First, these preferences may reflect adaptive mate choice without any selection for EPCs per se; second, women may have retained a vestigial form of estrous-related sexual interests that carry little adaptive significance (e.g., Thornhill and Gangestad 2008).
Women also exhibit extended sexuality to an extreme degree: In addition to potential receptivity and proceptivity throughout the cycle, women’s frequency of sexual intercourse changes little depending on where they are in their cycle (Thornhill and Gangestad 2008). In chimpanzees, the prevailing explanation of extended sexuality is that non-conceptive sexual behavior functions to confuse paternity and prevent infanticide by males (see above; Hrdy 1979); however, women’s extended sexuality does not function in this way. Rather, emerging evidence suggests that sexual interests during the non-conceptive phase function, at least in part, to elicit investment and benefits from male pair-bond partners (see Gangestad and Grebe 2017). This account perhaps provides another example of an adaptation for pair-bonding in the human lineage.
What can be concluded about the evolved nature of human sexuality, as it has shaped human adaptations for reproduction?
First, humans likely evolved systems in which pair-bonding has been important and in which men often exert considerable effort to invest in offspring (e.g., Dixson 2012; Thornhill and Gangestad 2008). Monogamy or serial monogamy is the most frequent mating arrangement, especially when male contribution to subsistence is great, but most human societies possess some degree of polygyny. Both men and women possess adaptations that serve as telltale signs of selection in favor of pair-bonding and paternal investment, but both also exhibit features that suggest some degree of adaptation for short-term mating bonds. Indeed, although typically occurring at low frequencies, nonzero rates of EPP characterize most human groups. Female benefits to EPC are not fully understood and may or may not include genetic benefits.
Second, despite these general patterns, wide variations across human groups exist in degrees of monogamy, sex differences in reproductive skew, and EPP rates. Some variation derives from flexibility in which group members invest heavily in offspring: Reliance on paternal contributions fosters monogamy and relatively low EPP rates; heavy reliance on maternal kin (arrangements of communal breeding) likely leads to increased EPP rates.
Third, human mating systems possess some similarities to the mating systems of several of our close ancestors, including chimpanzees and bonobos, but the differences also cannot be denied. Evolutionary biologists have intensely debated the order in which humans proceeded through specific primate-like mating systems, as well as the events and adaptations which eventually spurred a transition to the contemporary systems displayed by humans. There is no clear consensus on this issue, although further research may lead to future insights.
Finally, biological mechanisms (and hormonal systems in particular) are central to the development and expression of human sexuality. Sexual behavior in humans, compared to that of most other primates, appears to be less tightly regulated by hormonal mechanisms. Indeed, human sexuality is characterized by its remarkable flexibility and diversity, much of which cannot be parsimoniously explained by biological forces. Nevertheless, there exists some hormonal influence on women’s sexual behavior and preferences, which is modulated by partner characteristics, cultural norms, and environmental circumstances.
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