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Human Sexuality

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H

Human Sexuality the design of the system – that is, what are the
evolutionary forces that have likely shaped the
Nicholas M. Grebe1 and Christine M. Drea1,2,3 constitution of human sexuality?
1
Department of Evolutionary Anthropology, The present chapter is focused on human sex-
Duke University, Durham, NC, USA uality from the perspective of the evolved nature
2
Department of Biology, Duke University, of mating systems. The main advantage of this
Durham, NC, USA focus is that it facilitates broad considerations
3
University Program in Ecology, Duke about the evolutionary biology and psychology
University, Durham, NC, USA of human mating. By the same token, a mating
systems approach leaves many aspects of human
sexuality unaddressed, namely, those that have
Synonyms less clear implications for reproduction. Omission
of a topic does not necessarily reflect a lack of
Primate Sexuality relevant evolutionary research; on the contrary,
evolutionary psychologists engage deeply with
all matters of human sexuality. For further reading
Definition on sexual diversity or nonreproductive sexuality,
please see entries in this volume such as “▶ Evo-
Human sexuality is most broadly defined as the lution of Homosexuality,” “▶ Same-Sex Sexual
totality of experiences, systems, attributes, and Behavior,” “▶ Human Copulation,” “▶ Sexual
behavior that characterize the sexual sensation, Identity,” and “▶ Sexual Pathology.”
reproduction, and intimacy of Homo sapiens.
Human Sexuality and the Comparative
Approach
Introduction Many aspects of human sexuality are unique
among species, but usually by a matter of degree
Human sexuality, a remarkably broad topic, is than of kind. This general observation has two
the purview of numerous academic fields and is implications. First, by using phylogenetic com-
a discipline unto itself. Scientific perspectives of parative methods (for instance, comparing fea-
human sexuality encompass, variously, its repro- tures of human mating to those of the other,
ductive, social, cultural, emotional, and biological extant great apes), one can attempt to draw general
aspects. Evolutionary psychologists frame these conclusions about the likely ancestral makeup of
facets by asking the following question: What is human sexuality. Second, a comparative approach
# Springer International Publishing AG 2018
T.K. Shackelford, V.A. Weekes-Shackelford (eds.), Encyclopedia of Evolutionary Psychological Science,
https://doi.org/10.1007/978-3-319-16999-6_3360-1
2 Human Sexuality

can also reveal instances in which human sexual- pressures that forged reproductive behavior. But
ity meets or violates expectations (for instance, mating systems also cause adaptations, as they
showing ways in which human sexual adaptations affect the reproductive strategies and tactics most
are compatible or incompatible with a given beneficial to males and females. Conceptually,
mating system). More generally, a comparative therefore, mating systems anchor the various
approach has value for informing an understand- facets of human sexuality discussed below (for
ing of the forces that have led to the current state an extended discussion of these issues, see
of human sexuality. A comparative perspective Gangestad and Grebe 2015).
is emphasized in Tinbergen’s (1963) “four ques-
tions” (about mechanism, ontogeny, adaptive
Traditional Mating Systems
value, and phylogeny) for explaining behavior.
Mating systems give rise to the nature and degree
Therefore, a recurring tool throughout this entry
of reproductive skew, namely, the partitioning of
will be comparisons with sexuality studies in
reproduction among members of a society. The
nonhumans.
following categories of vertebrate mating systems
are considered “traditional”:
A Note on Hormonal Mechanisms Underlying
Human Sexuality
Monogamy: Males and females have exclusive
Endocrine systems constitute an important class
sexual access to one another.
of proximate biological mechanisms underlying
Polygamy: Sexual exclusivity occurs, but is not
human sexuality. Hormones are chemical “mes-
monogamous. Three subtypes of polygamy
sengers” that allocate limited physiological and
can be discriminated: (a) polygyny, individual
psychological resources throughout an organism.
males have exclusive sexual access to two
As detailed below, hormones provide some of the
or more females; (b) polyandry, individual
physiological background for many of the hall-
females have exclusive sexual access to two
marks of human mating systems, including pair-
or more males; and (c) polygynandry, two or
bonding, parental care, and mutual mate choice.
more males have exclusive sexual access to
At a theoretical level, hormones – both indepen-
two or more females and vice versa.
dently and in concert with one another – are medi-
Promiscuity: Males within a group mate with
ators of an organism’s life history reproductive
any and potentially multiple females and vice
strategy, linking physiology, and behavior in the
versa. A subtype of promiscuity is dispersed
partitioning of energy between mating, parenting,
promiscuity, in which largely asocial individ-
and nonreproductive activities (e.g., Del Giudice
uals with overlapping home ranges mate with
et al. 2015). For these reasons, hormonal systems
multiple partners during brief periods of social
are frequently discussed below within the context
grouping (typically, a female’s fertile period;
of human mating adaptations.
see Dixson 2012).

Monogamy and polygamy assume forms

Defining Mating Systems
of sexual exclusivity, whereas promiscuity does
not. Whereas monogamous mating systems gen-
An understanding of mating systems is core to
erate variation in reproductive success that is
recreating how human sexuality might have
nearly equal across the sexes, polygynous mating
evolved. In brief, mating systems dictate who
systems generate greater male than female varia-
mates with whom, when, and how often. Mating
tion, and polyandrous mating systems generate
systems emerge from the cost and benefit male
greater female than male variation.
and female experience from mate choice and com-
petition for mating opportunities, which in turn
select for male and female adaptations. The details
of a mating system can thus suggest selection
Human Sexuality 3

Mixed Mating Systems from seeking multiple mates, females should

The traditional categories of mating systems do reap little, if any, benefit from mating multiply.
not exhaustively cover all possibilities; instead, Under many conditions, therefore, selection was
many animal populations exhibit mixed mating expected to favor multiple mating by males,
systems. In one case, different forms of sexual but only rarely by females, thereby driving an
exclusivity may exist simultaneously. For increase in polygynous mating systems.
instance, in avian species typically characterized Polygyny can take on different forms
as polygynous (such that some males mate with depending on male features that foster access to
two females), monogamous mating arrangements multiple females (e.g., Emlen and Oring 1977). In
can also occur in the same population. In other resource defense polygyny, males control the
cases, different forms of exclusivity may exist resources valued by females for fueling offspring
temporally or spatially within the same population production. In male dominance polygyny, which
or species. For instance, individuals of some involves leks (small territories where males con-
mockingbird species will mate both monoga- gregate to display and attract females), males are
mously and polygamously depending on avail- chosen by females for their ability to compete
able opportunities. Indeed, across the vertebrate with other males, but offer no material resources
species examined, humans included, there is more to females to be directed toward investment in
fluidity in mating system structure than has been offspring.
recognized historically: Human groups, large and In this “Darwin-Bateman” view, monogamy
small, have created and can create an array of typically evolves when males cannot defend
mixed mating systems. the resources that permit them to attract multiple
mates. Ecological constraints explain why,
for instance, most birds (over 90%) are socially
Selection Pressures Influencing monogamous: Resources are dispersed to a degree
Vertebrate Mating Systems that males cannot typically secure enough for
more than one female’s offspring (e.g., Emlen
Traditionally, sexual selection theorists had and Oring 1977). However, with the development
widely assumed that natural selection would of genetic tools in the late 1980s and early 1990s,
most likely give rise to mating systems character- researchers began testing some of the assumptions
ized by some degree of polygyny. The rationale about traditional mating systems, and avian
behind this assumption is known as the “Darwin- biologists discovered that many pair-bonding
Bateman effect”: the increase in offspring number birds actually exhibited high rates of extra-pair
as a function of the number of matings each male paternity – paternity by males other than the social
procures with different females, without a similar partner. This finding, which has now been
increase occurring as a function of the number of extended to primates also previously thought to
matings each female procures with different males be monogamous (e.g., in gibbons: Palombit
(see Drea 2005; Parker and Birkhead 2013). Ulti- 1994), prompted the recognition of an extra-pair
mately, the differential effect by sex of “multiply mating system. Although most of the sexual activ-
mating” was attributed to anisogamy – sexual ity occurs within structured units (e.g., individual
reproduction involving the union of “expensive” male-individual female units, individual male-
eggs and “cheap sperm” – and to differences multi-female units, and so on), some mating –
by sex in the initial investment in offspring. In “extra-pair” mating – occurs outside of these
placental mammals, internal fertilization and ges- units. In recognition of the social unit in which
tation delays the female’s production of new off- most mating occurs, systems with pair-bonding
spring until after birth, fetal or neonatal loss, and cuckoldry are said to reflect social monogamy
and/or some period of lactation; males, however, with EPC (extra-pair copulation). Some systems
do not experience these same delays. According entail little EPC, whereas others may entail
to this paradigm, whereas males should benefit
4 Human Sexuality

frequent EPC. Thus, social monogamy with EPC 2013). In this case, the benefits that have the
lies on a continuum of degree of sexual greatest empirical support are direct ones (e.g.,
exclusivity. parental care, food provisioning). The most con-
troversial interpretation concerns “good gene”
The Polyandry “Revolution” Within Behavioral benefits. Some researchers conclude that support
Biology for genetic benefits of EPC is weak (Parker and
Over the past three decades, behavioral ecologists Birkhead 2013), whereas others argue that incon-
have increasingly recognized the benefits of clusive data do not necessarily counter a “good
female multiple mating, which includes EPC genes” interpretation (e.g., Eliassen and Kokko
in addition to polyandrous mating more generally. 2008). The jury is still out about whether or not
Parker and Birkhead (2013) refer to the sea avian EPC functions in a female to gain genetic
change as a “revolution.” By mating multiply, benefits, and this same uncertainty extends to
females could gain both direct benefits that humans, as noted below in the section “Women’s
increase reproductive success and indirect bene- Mating Adaptations.”
fits that increase the genetic fitness of offspring.
Direct benefits can include increased rates of New Models of Sexual Selection Pressures on
fertilization, increased attainment of resources Males
offered by males, and reduction in male aggres- In recent years, theorists have also questioned the
sion toward offspring via “paternity confusion.” traditional perspective on male interests. In the
Indirect benefits can include attaining a sire whose traditional view based on the Darwin-Bateman
DNA is compatible with the mother’s (whereby effect, males should possess promiscuous sexual
selection occurs “cryptically” post copulation – motivations and, whenever ecological circum-
within the reproductive tract of the female), diver- stances permit, compete for the resources or social
sification of offspring via multiple paternity (bet standing that promote multiple mating. Yet, there
hedging), and, in the context of extra-pair mating, are good reasons why males might not pursue this
attaining a sire who potentially has greater genetic strategy. Males can instead benefit from providing
fitness (“intrinsic good genes”) than does an care for their existing offspring. When the net
in-pair male. As a result of these benefits, female benefits from providing care to offspring exceed
multiple mating is not a rare anomaly; it is com- the net benefits from competing for mates, males
monplace (Parker and Birkhead 2013). should be selected to care. These conditions are
most likely to exist when (a) competing for mates
Benefits of Female Multiple Mating is costly (e.g., males risk injury), relative to the
The benefits of multiple mating can arise from costs of providing care, (b) the net benefits to
multiple sources. To take the example of EPC, competing are relatively weak (e.g., a male is not
whereas many socially monogamous birds engage competitive or many males compete), and (c) the
in extra-pair mating, it remains uncertain if benefits to care are relatively great (e.g., males are
females in particular derive any benefits from able to discriminate their own offspring; offspring
it. Males are assumed to benefit from multiple benefit from complementary care from males and
mating, in which case female engagement in females) (e.g., Kokko and Jennions 2008).
EPC may simply reflect male assertion. In some This framework offers a different perspective
instances, the costs of resisting copulation (e.g., on why pair-bonding with biparental care is so
physical harm) outweigh its benefits. Accord- common in birds. In the traditional view, the
ingly, EPC can commonly arise exclusively due focus is on the male’s inability (e.g., due to
to male sexual interests and female tolerance, resource dispersion) to defend resources support-
under a scenario of “sexual conflict” (Parker and ive of multiple mates and their offspring. In the
Birkhead 2013). more recent view, the focus is instead on the
Nevertheless, in some avian species, females relatively poor gain from competing and the sub-
clearly solicit EPC (e.g., Parker and Birkhead stantial benefits to male care (see Kokko and
Human Sexuality 5

Jennions 2008). In avian species especially, one active for a significant portion of their ~30-day
parent may need to forage, while the other defends cycle, mating with potentially all adult males
a nest of offspring that cannot yet fly. Thus, avian in the group, typically multiple times. Despite
research has drawn attention to the importance of these similarities, these species have highly diver-
male care and its benefits in the evolution of gent social organizations that likely impact their
mating systems – a framework that is broadly sexual strategies. Notably, chimpanzee societies
applicable to other pair-bonding species, includ- are male dominant and despotic (in which males
ing humans. show female-directed aggression and infanticide),
whereas bonobo societies are female dominant,
peaceful, and more egalitarian.
Hominoid Mating Systems In the better-studied chimpanzee, the favored
hypothesis for the function of promiscuous mat-
The Ancestral State ing in females is Hrdy’s (1979): Promiscuous
Applying a comparative perspective draws atten- mating confuses paternity. If no male can rule
tion to selection pressures that can drive benefits out his own paternity, each is less likely to aggress
of multiple mating and of male care – what mating against the future offspring, thereby reducing the
systems characterized ancestral human groups likelihood of infanticide. Nevertheless, there is
that drove male and female mating adaptations? recent evidence to suggest that the sexual interests
To address this question, one must consider some of female chimpanzees change across the sexual
of the defining features of primates. Notably, period. During the non-fertile phase, females are
within the primate order, females evolved from most promiscuous, but during the fertile phase,
the “primitive” mammalian condition of strictly they tend to prefer particular males (e.g., younger
circumscribed sexual receptivity (limited to the males whose status is rising; Stumpf and Boesch
2–3-day peri-ovulatory or fertile period) to 2005). Perhaps females confuse paternity during
a more “advanced” state, evidenced by anthropoid non-conceptive portions of their cycle, but when
primates, of situation-dependent receptivity. they are fertile, they bias sireship toward males
Thus, in female anthropoids, sexual behavior is that can offer genetic benefits or certain forms of
decoupled from fertility, and females can engage direct benefits (e.g., physical protection). Indeed,
in copulation at any stage of their cycle (Dixson male reproductive success is highly skewed in
2012). In those primates that show “extended chimpanzees, with one or two high-quality males
sexuality” (sexual activity outside of fertile typically siring many more offspring than the
phases), the social system can have significant majority of other adult males, despite female pro-
influence over sexual behavior, despite the type miscuity (e.g., Stumpf and Boesch 2005).
of mating system. Such is likely to have been the In bonobos, female coalitions are considerably
case for our closest ancestors. But what mating more powerful than they are in chimpanzee soci-
system did this ancestral species possess? eties. Female-female sociosexual exchanges reg-
ulate female social hierarchies and coalitional
Chimpanzee and Bonobo Mating Systems activity. It would seem that paternity confusion
Whatever mating systems evolved in humans, to protect against the threat of infanticide would
they originated from adaptations associated with be an unlikely explanation for female promiscuity
the system(s) of the shared common ancestor with in bonobos; it instead appears to be a mechanism
chimpanzees (Pan troglodytes) and bonobos (Pan for ensuring social harmony. In no study, how-
paniscus) that existed about 5 million years ago. ever, have researchers yet tested for changes in
Chimpanzees and bonobos both live in mixed-sex female bonobo sexual activity or male preferences
groups and have promiscuous mating systems, in across the cycle. Despite promiscuity, male repro-
which females advertise their fertility and show ductive skew is strong, suggesting similar bias in
extended sexuality. Females of both species pos- mating with certain males at peak fertility (Gerloff
sess hindquarter sexual swellings that serve as et al. 1999).
“graded signals” of fertility; yet, they are sexually
6 Human Sexuality

Human Versus Pan Mating Systems challenges predictions arising from the Darwin-
As Dixson (2012) notes, humans have diverged Bateman paradigm about the almost limitless
considerably from both chimpanzees and bonobos potential for fatherhood as a function of increas-
in a variety of respects. In chimpanzees, extreme ing the number of sexual partners. Brown et al.
sexual size dimorphism, rank relations in male (2009) examined variance in reproductive success
androgen concentrations, relative testes size across 18 traditional or preindustrial societies. On
and ejaculate volume, structural features of average, male variance exceeded female variance
semenogelin proteins (that coagulate sperm), and (median ratio  1.70); yet, this ratio varies widely
length of the female reproductive tract are consis- (ranging from <1 to nearly 5).
tent with the high degree of either male-male
competition or sperm competition (multiple Mating Arrangements and Sexual Exclusivity
males’ sperm residing in the female reproductive One feature entirely unique to modern humans
tract vying for conception) evident in their social is the influence of cultural evolution on mating
and mating systems, respectively. These features systems. Notably, marriage is a near-universal
in humans are consistent with lower levels of institution in human societies; despite this ubiq-
male-male and sperm competition. Nonetheless, uity, marriage does not imply near-universal
human mating adaptations may possess vestiges monogamy (or even serial monogamy) in
of Pan mating, as discussed below. humans. Ethnographic evidence from the standard
cross-cultural sample (SCCS) shows that over
80% of present-day, human societies possess
Unique Features of Human Systems some degree of polygyny. Fewer than 20% are
completely monogamous, and 1% are character-
Limits on Reproductive Skew ized by a nonzero level of polyandry. Agriculture,
Hominoids – and humans in particular – have herding, and other relatively recent means of
extremely slow life histories, which severely resource production may alter mating arrange-
constrains female fertility. Because of the ener- ments; Western religious traditions promoting
getic demands of producing highly encephalized marriage do so as well. Marlowe (2003) examined
infants (and usually only one per pregnancy), mating arrangements in the SCCS’s 36 foraging
hominoid mothers are heavily invested in their groups and found that about 90% exhibit a non-
young, assuming costs associated with lengthy zero level of polygyny. Monogamy is, however,
gestation and lactation, as well as extended infant still the most typical, socially sanctioned mating
and juvenile dependency. Women are especially arrangement in human societies. In about two-
reproductively inefficient, even “infertile”. thirds of foraging societies, for instance, the per-
Beyond the constraints imposed by the concealed centage of polygynously married women is 12%
release and short-term survival of generally one or less (Marlowe 2003); in only 13% of these
egg per fertile period, approximately 50% of societies does the rate reach 50%.
human cycles are anovulatory or too short to Nevertheless, marital systems may or may not
allow implantation. Women also suffer relatively imply sexual exclusivity. Although most offspring
high rates of conception failure, low embryo may be produced by in-pair partners, some may be
viability, miscarriage, premature delivery, and produced through extra-pair matings. Questions
perinatal death (reviewed in Drea 2005). of interest, then, are how common is extra-pair sex
Coupling women’s extended sexuality with the and how often does it result in extra-pair paternity
various physiological constraints on her reproduc- (EPP). Anderson (2006) reviewed studies estimat-
tion, there is enhanced potential in humans for ing nonpaternity, largely in developed countries.
non-fertile mating (Drea 2005; Thornhill and Nearly all samples give biased estimates,
Gangestad 2008). The low probability of concep- depending on how they were selected. High pater-
tion associated with each copulatory act nity confidence samples estimate an EPP rate
Human Sexuality 7

averaging just 2%. Samples of men who suspicion Mothers and Allomothers
about their partner’s fidelity estimate it to be, The maternal bond or mother-infant relationship
on average, about 30%. Once again, tremendous is one of the strongest across mammalian species.
variation exists, ranging from <1% in high pater- Its development, which begins in pregnancy, is
nity confidence samples (in Switzerland and influenced by the hormone oxytocin (OT). Most
Germany) to about 12% (in Monterrey, Mexico). generally, OT (along with related homologs in
For some other traditional societies, ethnogra- nonmammalian taxa) is a smooth muscle contrac-
phies report very frequent EPC, but systematic tor that plays a highly conserved role in orgasm
data on EPP rates are scant (Anderson 2006). and sexual functioning, as well as in parturition
Within developed countries, extra-pair paternity and lactation. OT also functions as a neurotrans-
rates have declined in the past century; the advent mitter involved in establishing and maintaining
of effective birth control may reduce incidence maternal behavior (see Gangestad and Grebe
of conceptive EPC, suppressing the EPP rate. In 2017). It is thought that OT’s role in maternity
traditional settings, then, EPP rates may have been constitutes the “biological prototype” for its func-
low on average (5% or less) but variable (in some tions in facilitating other kinds of social bonds so
societies >10%). critical to human society (see section on “Pair-
As with females of other species, the benefits Bonding and Oxytocin”).
that give rise to women’s extra-pair mating are Many have argued that the extended period of
debated. Some scholars argue that benefits lie infant care is intricately linked to the early termi-
largely (or even exclusively) with male extra- nation of fertility in women – that the distinct
pair partners, while others stress the possibility post-reproductive period (i.e., menopause) that
that women too, in many circumstances, benefit characterizes human females allowed reproduc-
(for a review, see Thornhill and Gangestad 2008). tively senescent mothers to better ensure their
latest progeny’s survival and overall reproductive
success, relative to aged mothers who continued
Offspring Care
to engage in risky pregnancies. This “stopping
Consistent with slow life histories, human off-
early” hypothesis has been contrasted with the
spring are, in many respects, remarkably altricial
“grandmother hypothesis” that instead proposes
at birth. Compared to other hominoids, humans
that senior women contribute best to their own
are born with extreme motor immaturity and
inclusive fitness by investing in the reproductive
brains that represent a relatively small proportion
success of their childbearing daughters. Accord-
of adult size. As in other primates, human mothers
ingly, the diets of women of reproductive age and
harvest the overwhelming majority of calories
their children are subsidized, not primarily by the
consumed by offspring during pregnancy and lac-
women’s mates, but through the efforts of mater-
tation. For periods longer than in any other pri-
nal kin – most importantly, the mothers’ mothers
mate (i.e., including postweaning), however,
(Hawkes 2003).
human infants continue to be dependent on
mothers and others for food, protection, and social
Paternal Care
development. Because of their extended depen-
Questions intensely debated within evolutionary
dency and juvenility, evolutionary theorists argue
anthropology over the past two decades include
that early humans developed a system for rearing
whether human pair-bonding is central to the mat-
their young (and, thus, ensuring their own repro-
ing system and whether males possess adaptations
ductive success) in which mothers, along with
for providing care for offspring. Did ancestral
various helpers, cooperate in raising infants
conditions that favored male care, at least contin-
(Hrdy 2009). These adaptations for care stem
gently, exist recurrently in human groups, leading
from the nature of human mating systems and
natural selection to shape male features that pro-
life history that inform the likely structure of
moted care? Although pair-bonding need not
ancestral human sexuality.
8 Human Sexuality

imply biparental care, the two are strongly asso- about 95% of their calories from collected foods
ciated in the animal world. Male care potentially requiring no manual extraction (e.g., fruits,
comes in many forms: Protection, direct care (e.g., leaves), only about 8% of calories consumed by
supervision), and provisioning are three promi- modern hunter-gatherers are from foods requiring
nent categories. In the anthropological literature, no manual extraction, with a large proportion
two research areas have received significant atten- (30–80%) derived from vertebrate meat. The
tion: the role of testosterone (T) in men’s parent- level of male contribution to the diet varies con-
ing effort and the importance of men’s hunting in siderably across foraging societies (~40–90+%).
provisioning mates and offspring. Women reproductively benefit from the male-
generated surplus. Women’s offspring production
Parenting Effort and Testosterone or, specifically, their inter-birth interval – the
Across vertebrate taxa, T is a crucial component delay between the birth of one offspring and the
of a system that functions to facilitate male mating same woman’s next offspring – is aided by male
effort by channeling energetic resources to fea- contribution to subsistence (Marlowe 2001).
tures particularly useful in male-male competition Thus, a traditional anthropological view is that
(e.g., muscles, sensitivity to dominance ranks, and male surplus food production evolved as paternal
cues of social hierarchy) and, due to necessary care. According to this view, the nuclear family is
trade-offs, away from other targets of allocation a key economic unit in the evolution of human
(e.g., repair, immune function; see Bribiescas mating relations. For subsidies generated by male
2001). In species in which males exert parental hunting to function as parental effort, nutrients
effort, a modification may have evolved: T may that men generate must flow to their mates (and
also modulate allocations of effort to mating then to offspring) or directly to offspring. Addi-
versus parenting (in shorthand, competing tionally, if one adopts the perspective of T as
vs. caring). In some species in which males invest a mediator of mating versus parenting effort, this
in offspring (e.g., marmosets, some birds), male view of hunting as an instantiation of paternal care
T concentrations drop after the birth/hatching of suggests it should be associated with T decreases.
the mates’ offspring (discussed in Bribiescas An alternative view of hunting – in that it primar-
2001; also see section on “Mating (Versus Parent- ily functions as an activity to gain new mates – is
ing) Effort and Testosterone”). discussed below in the section “Views About
Hunting as “Mating Effort”.”
Views About Hunting as “Parental Effort”
In most primate species, individuals of both sexes
are largely responsible for their own subsistence Adaptations for Mating
after at most a few years after birth. In most human
foraging populations, however, the average adult In general, patterns of human mating and repro-
male generates more calories than he consumes, duction are consistent with human pair-bonding
with the surplus being distributed among kin and, and biparental investment, albeit with modest
in some cases, non-kin group members. The pri- levels of polygyny, nonzero rates of EPC, and
mary activity through which men generate surplus notable variability. How do these patterns inform
calories in foraging societies is hunting (broadly male and female adaptations for mating? These
defined to include any activity, including fishing, features, in some instances, serve as telltale sig-
aimed at harvesting animal meat). Although natures of the mating system that led them to
women forage and extract roots (and, in a mean- evolve. The subsections below address evolution-
ingful minority of societies, produce more calo- ary forces and mechanisms that (a) contribute
ries than do men), only rarely do they hunt to somewhat equally to mating adaptations in both
a substantial degree. Human foragers appear to sexes, (b) are most directly relevant to men’s
be adapted to a diet consisting of high-quality, mating adaptations, and (c) are most directly rel-
calorie-rich foods. Whereas chimpanzees obtain evant to women’s mating adaptations.
Human Sexuality 9

Mutual Mate Choice (of which MHC complement is only one feature;
In species in which male and female pairs bond, see Thornhill and Gangestad 2008).
“mutual mate choice” typically evolves. Members
of both sexes are advantaged through preference
Pair-Bonding and Oxytocin
of some mates over others (e.g., Kokko and
As discussed above (see section on “Offspring
Jennions 2008). Studies of mate preferences
Care”), OT plays a major role in the formation
strongly point to mutual mate choice in modern
of social bonds; its role in pair-bonds has become
human societies. In many instances, choice for
a hot topic within social psychology. Classic com-
mates that exhibit good parenting qualities should
parative studies in voles were the first to implicate
be preferred. In seeking a long-term mate, both
OT in sexual pair-bonding, showing that brain
men and women, on average, rate “kindness and
neuroanatomy and central nervous activity of the
understanding” as the top preference. Many other
OT system underlie the development of monoga-
mate preferences for personality traits, however,
mous partner preferences. From this foundation,
are characterized by large sex differences (see
psychologists have recently begun to examine
Conroy-Beam et al. 2015).
how OT plays a role in human sexual pair-
Specific forms of mate preference offer partic-
bonding. Some evidence is consistent with a pro-
ularly compelling examples of adaptation for
social role for OT in romantic bonding in both
mutual choice. The human leukocyte antigen
sexes. OT administration leads to more engaged,
(HLA) system, for example, which controls the
constructive communication about relationship
immune response and pathogen resistance, has
conflicts and more intense orgasms and greater
been correlated with both odor preferences and,
contentment after intercourse with a pair-bond
to a lesser extent, facial preferences in potential
partner. Success of relationship interventions
mates (Winternitz et al. 2017). The HLA is
and overall relationship satisfaction are related to
a highly variable gene complex encoding the
OT concentrations, and both men and women
major histocompatibility complex (MHC) pro-
in newly involved couples exhibited high
teins in humans. MHC genes code for cell surface
serum concentrations of OT (see Gangestad and
markers that function to “declare” that a cell is
Grebe 2017).
uninfected (when the MHC molecule presents
In other studies, OT has been linked to distress
only self-peptides) or infected (when the MHC
and attachment anxiety in romantic relationships.
molecule binds a non-self-peptide structure
These conflicting results reflect a more general
that is “visible” to the immune system). All else
uncertainty regarding the overarching function
being equal, it pays to mate with someone who
of OT in social behavior (see Gangestad and
possesses alleles optimally different from one’s
Grebe 2017). As one possible resolution, it may
own, either to avoid inbreeding or to produce
be that threats to valuable, vulnerable relation-
advantaged heterozygotic offspring. MHC
ships are key triggers of the OT system. This
appears to be detectable through signatures in
hormonal increase, in turn, then functions to
scent (or facial attractiveness). In a variety of
reorient psychological resources toward these
species, females prefer the scent of males that
relationships. Preliminary evidence from both
possess MHC genes different from their own.
men and women in romantic bonds is in line
Studies strongly suggest that humans too are
with such an interpretation, further suggesting
most sexually attracted to scents of others who
that the role of OT in pair-bonding is central for
possess non-shared MHC alleles. Consistent with
both sexes. A focus on relationship vulnerability
mutual mate choice, preferences typically exist in
may also generalize to other social bonds regu-
both sexes (reviewed and meta-analyzed in
lated by OT – in particular, the mother-infant
Winternitz et al. 2017). Evidence for mutual
relationship (see Gangestad and Grebe 2017).
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
10 Human Sexuality

Men’s Mating Adaptations participant’s own face or, alternatively, that of

another participant is digitally combined with the
Mating (Versus Parenting) Effort and Testosterone face of a small child to create two composite
Evidence from nonhuman studies are consistent images of child faces – one “self-resembling”
with a T-mediated hormonal system that is sensi- and one not. Participants then choose between
tive to the relative value of exerting mating versus the children based on their likelihood of investing
parental effort. There is increasing evidence to in (e.g., spending time with, adopting) each child.
suggest men’s T mediates a similar trade-off. Men consistently prefer the self-resembling one,
Men with higher T concentrations exhibit greater an effect not due to conscious recognition of
frequency and intensity of male-male competi- self-resemblance (reviewed in Thornhill and
tion, dominance behavior, and mate seeking; in Gangestad 2008).
contrast, men who are mated or have offspring
typically have lower T concentrations than do
Views About Hunting as “Mating Effort”
single, childless men (reviewed in Gray and
The theory of male-hunting-as-parental-effort,
Campbell 2009). Some evidence indicates that
discussed above, faces a fundamental difficulty:
the association depends partly on changes in
Nuclear families are not, in fact, potent economic
T concentrations following changes in mating or
units in foraging societies. In the Hadza of Tanza-
paternal status. Additionally, among fathers, those
nia and the Ache of Paraguay, for instance,
with lower concentrations of T and smaller testes
hunters have little control over the distribution of
show a pattern of brain activation when looking at
the meat they generate. Instead, meat (particularly
photos of their own children, indicative of greater
from large game) is shared widely across commu-
paternal involvement.
nity members. A Hadza hunter’s own family
The effect of mating status on men’s
receives no more meat from his large game kills
T concentrations is moderated by men’s interest
than what it receives from the same-sized animal
in pursuing extra-pair relationships with women
a neighbor killed. In one analysis, offspring nutri-
other than their primary partners. Men who have
tional status covaried with Hadza women’s forag-
little interest in or history of extra-pair relation-
ing returns, but not with men’s returns. Thus,
ships reveal the typical drop in T concentrations
perhaps men’s hunting functions as (i.e., is
when mated, as compared to their concentrations
adapted for) mating effort – effort to compete for
while single. Men who have interest in extra-pair
access to mates through “showing off” – rather
relationships, by contrast, showed no difference:
than as parental effort. Men garner prestige
Their T concentrations were just as high when
through successful hunting exploits, particularly
in relationships as when single (see Gray and
big-game hunting, and this prestige translates into
Campbell 2009).
mating opportunities.
Of course, male hunting subsidizes the diets of
Paternity Certainty and Male Care women and their offspring. But these subsidies, in
Because male confidence in paternity is variable, the male-hunting-as-mating-effort view, are not
men’s parental efforts may be contingent on cues generated directly by the women’s own mates or
of paternity, such as self-resemblance. In a large by the children’s own fathers. Rather, they are
Western sample, men assisted offspring they generated through the efforts of men in general
report as likely to be their own genetic offspring to gain mates. The surplus calories generated by
more so than those they suspect reflect EPP male hunting that benefit women and offspring are
(Anderson et al. 2007). Behavioral researchers by-products of men’s showing off – windfalls they
have examined possible psychological underpin- enjoy, not benefits men’s efforts were designed to
nings of discriminative parenting. In one design, achieve.
a digital photograph is taken of a participant. The
Human Sexuality 11

A Blended View on Hunting in Relation to Human physiologically exhausting. Periodicities in sexu-

Sexuality ality are regulated by a concert of hormonal
Historically, men may have benefited from hunt- changes, involving luteinizing hormone, follicle-
ing in currencies of enhanced viability of off- stimulating hormone, estradiol (E2), and proges-
spring and mating opportunities (e.g., Gurven terone (P4). Together, these hormones function to
and Hill 2009). Patterns of Hadza foraging rates ensure successful conception, gestation, and par-
and activities support this relationship (Marlowe turition (reviewed in Dixson 2012). E2 and P4
2003). Overall, married Hadza women produce as have received substantial attention for their roles
many calories as do married Hadza men. Women in the psychology of women’s mating as well (for
with young children, however, do not, because a review, see Roney 2015).
their childcare interferes with effective foraging.
In such circumstances, their husbands forage Mating Effort and Estradiol
more than they do; in couples with an infant less In line with other phenotypically integrated hor-
than 1 year of age, men produce almost 70% of the monal systems, E2’s psychological effects “go
total calories generated within the family unit. along” with its physiological roles to regulate
Hadza men’s work efforts (and prey items energy allocation – in this case, toward females’
targeted) adjust in response to the direct food mating effort, perhaps at the expense of other
production of wives and the presence or absence activities, such as feeding (see Roney 2015). His-
of young children. The view that men’s work torically, some sexuality researchers have argued
functions solely as mating effort cannot readily that E2 has little, if any, impact on women’s sexual
explain this pattern. behavior, noting, for instance, that the effect
Other data also support this blended view. of ovariectomy on women’s sexual behavior is
Across societies of the standard cross-cultural less than the effect on comparable sexual behavior
sample, pair-bond stability (low divorce rate) in other female primates (Dixson 2012). In
associates with children being weaned at older the most robustly designed study to date, how-
ages. Because lactation interferes with women’s ever, researchers sampled women continuously
ability to collect food, male subsidy purportedly throughout multiple cycles and found that E2
permits women to invest in young offspring does, in fact, predict overall levels of female sex-
through nursing. Additionally, if men contribute ual desire (reviewed in Roney 2015).
to the household’s consumables, male total con-
tribution to calorie production should predict Social Bonding and Progesterone
greater levels of monogamy across societies. The role of P4 in human sexual behavior has
This prediction is supported by the available received relatively less attention. Dixson (2012)
anthropological evidence (see Marlowe 2003; reviewed studies involving the administration of
Thornhill and Gangestad 2008). P4 to female nonhuman primates, in which the
general finding was that P4 diminishes sexual
Women’s Mating Adaptations receptivity and proceptivity. Roney (2015) argues
that because women’s P4 concentrations associate
The Ovulatory Cycle negatively with subjective sexual desire, P4 is
Women, like the vast majority of other mamma- a “stop signal” for sexual motivation that facili-
lian females, undergo regular cycles that restrict tates a shift toward other activities. An alternative
the window in which successful conception from viewpoint is that P4 modifies the nature of sexual
sexual intercourse is possible. It is thought that motivation. P4 is most consistently elevated at two
these cycles arise, at least in part, because (1) sub- times: during the luteal phase and during preg-
stantial time is required to prepare the uterus nancy. During these non-conceptive phases, in
for implantation and (2) the production of germ which women still initiate and accept sexual
cells and behavioral adaptations essential to advances, P4 may have been selected because it
ensure conception from sexual intercourse are shifted sexual interests to allow focus on pair-
12 Human Sexuality

bond relationships, perhaps especially when the found that women in the peri-ovulatory period,
male partner’s interest in the relationship lags compared to during non-fertile phases, reported
behind that of the woman (Gangestad and Grebe increased extra-pair sexual desire and behavior,
2017). During pregnancy, women may have par- in-pair sexual desire, and self-perceived desirabil-
ticularly benefited from consolidating social sup- ity. Additionally, when fertile, women may be
port from a pair-bond partner, kin, or trusted more attracted to certain male features, such
friends. Preliminary evidence is consistent with as masculine bodies and behavioral dominance.
an interpretation of P4 facilitating bonding in And, should the women’s primary partners
a targeted manner, rather than it contributing to lack those desired features, fertile women (only)
generalized affiliative motives (see Gangestad and report greater attraction to men other than their
Grebe 2017). partners (findings reviewed and meta-analyzed in
Gildersleeve et al. 2014). Thus, one possibility is
Cyclic Shifts in Women’s Mating Behavior and that women’s fertile-phase sexuality is attuned to
Preferences certain male features when fertile – namely, those
Whereas ovarian hormones may be the proximate that represent “good genes” that could be trans-
biological factors thought to underlie changes mitted to offspring (Thornhill and Gangestad
in women’s sexuality, cycle phase (i.e., fertile 2008). In cases in which primary partners lack
vs. non-fertile windows) provides a relevant func- these features, women’s mating adaptations
tional distinction for understanding adaptations in could facilitate EPCs. Nonetheless, other possibil-
women’s sexual behavior. Changes in concentra- ities cannot be ruled out: First, these preferences
tions of E2 and P4 that result from the physiology may reflect adaptive mate choice without any
of the ovarian cycle convey information, via selection for EPCs per se; second, women may
the neuromodulatory effects of these hormones, have retained a vestigial form of estrous-related
related to fecundity (i.e., the probability of suc- sexual interests that carry little adaptive signifi-
cessful conception and gestation). Presumably, cance (e.g., Thornhill and Gangestad 2008).
because the costs and benefits of sexual activity Women also exhibit extended sexuality to
differ depending on whether or not conception an extreme degree: In addition to potential recep-
is possible, women’s mating adaptations should tivity and proceptivity throughout the cycle,
shift accordingly. A substantial literature has women’s frequency of sexual intercourse changes
accumulated addressing if and how women’s little depending on where they are in their cycle
sexual preferences and behavior shift as a function (Thornhill and Gangestad 2008). In chimpanzees,
of where they are in their cycle. the prevailing explanation of extended sexuality is
In most vertebrate species, females are only that non-conceptive sexual behavior functions to
sexually receptive during their fertile reproductive confuse paternity and prevent infanticide by
phase. Consistent with early views about the min- males (see above; Hrdy 1979); however, women’s
imal influence of E2 on women’s sexuality, initial extended sexuality does not function in this way.
accounts on the evolution of human sexuality Rather, emerging evidence suggests that sexual
minimized or entirely discarded the idea of interests during the non-conceptive phase func-
a distinct fertile-phase sexuality in women, pro- tion, at least in part, to elicit investment and ben-
posing that it was lost and replaced by continuous, efits from male pair-bond partners (see Gangestad
unchanging sexual receptivity across the ovarian and Grebe 2017). This account perhaps provides
cycle. Decades of empirical research have since another example of an adaptation for pair-bonding
shown that while sexual frequency may not in the human lineage.
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)
Human Sexuality 13

Conclusion Finally, biological mechanisms (and hormonal

systems in particular) are central to the develop-
What can be concluded about the evolved nature ment and expression of human sexuality. Sexual
of human sexuality, as it has shaped human adap- behavior in humans, compared to that of most
tations for reproduction? other primates, appears to be less tightly regulated
First, humans likely evolved systems in which by hormonal mechanisms. Indeed, human sexual-
pair-bonding has been important and in which ity is characterized by its remarkable flexibility
men often exert considerable effort to invest in and diversity, much of which cannot be parsimo-
offspring (e.g., Dixson 2012; Thornhill and niously explained by biological forces. Neverthe-
Gangestad 2008). Monogamy or serial monog- less, there exists some hormonal influence on
amy is the most frequent mating arrangement, women’s sexual behavior and preferences, which
especially when male contribution to subsistence is modulated by partner characteristics, cultural
is great, but most human societies possess some norms, and environmental circumstances.
degree of polygyny. Both men and women pos-
sess adaptations that serve as telltale signs of
selection in favor of pair-bonding and paternal
Cross-Reference
investment, but both also exhibit features that
suggest some degree of adaptation for short-term
▶ Bonobo Sexuality
mating bonds. Indeed, although typically occur-
▶ Chimpanzee Sexuality
ring at low frequencies, nonzero rates of EPP
▶ Mating Systems
characterize most human groups. Female benefits
▶ Sexual Behavior
to EPC are not fully understood and may or may
not include genetic benefits.
Second, despite these general patterns, wide
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