Evolution of Same Sex Behaviour

Function and Phylogeny:
The Evolution of Same-Sex Sexual Behavior

in Primates
Paul L. Vasey, PhD
SUMMARY. Evolutionary explanations come in two basic forms.

Functional explanations focus on elucidating the adaptive (i.e., repro-
ductive) value of a particular behavior. Phylogenetic explanations fo-
cus on understanding the evolutionary history of a behavior: that is,
how it originated and changed in a step-by-step manner over time.
Cross-species comparisons indicate that same-sex sexuality is not an
evolutionarily uniform phenomenon. Multiple analogous forms of ho-
mosexual behavior have evolved. I argue that our understanding of why
same-sex sexualities evolved is contingent on the implementation of
both types of evolutionary analysis. I describe research on female
bonobos (Pan paniscus) to illustrate how functional investigations can
help explain why some forms of primate homosexual behavior
evolved, such as those that are sociosexual in nature. I then describe
my research on female Japanese macaques (Macaca fuscata) to illus-
trate how phylogenetic investigations can help account for how other
forms of homosexual behavior evolved, such as those that are strictly
sexual in nature. I conclude by discussing how both functional and
phylogenetic perspectives need to be fully integrated to account for
Paul L. Vasey is Professor of Psychology, University of Lethbridge, Alberta, Can-

ada (E-mail: paul.vasey@uleth.ca).
[Haworth co-indexing entry note]: “Function and Phylogeny: The Evolution of Same-Sex Sexual Behav-
ior in Primates.” Vasey, Paul L. Co-published simultaneously in Journal of Psychology & Human Sexuality
(The Haworth Press, Inc.) Vol. 18, No. 2/3, 2006, pp. 215-244; and: Handbook of the Evolution of Human
Sexuality (ed: Michael R. Kauth) The Haworth Press, Inc., 2006, pp. 215-244. Single or multiple copies of
this article are available for a fee from The Haworth Document Delivery Service [1-800-HAWORTH, 9:00
a.m. - 5:00 p.m. (EST). E-mail address: docdelivery@haworthpress.com].
Available online at http://jphs.haworthpress.com
© 2006 by The Haworth Press, Inc. All rights reserved.
doi:10.1300/J056v18n02_07 215
216 HANDBOOK OF THE EVOLUTION OF HUMAN SEXUALITY
these data and, by extension, the evolution of male homosexuality in

humans. doi:10.1300/J056v18n02_07 [Article copies available for a fee from
The Haworth Document Delivery Service: 1-800-HAWORTH. E-mail address:
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KEYWORDS. Primates, Japanese macaques, female-female sexual be-

havior
FUNCTIONAL AND PHYLOGENETIC PERSPECTIVES

IN EVOLUTIONARY THEORY
Evolutionary explanations come in two basic forms (Tinbergen,
1963; Alcock, 1989). Functional explanations focus on elucidating the
adaptive (i.e., reproductive) value of a particular behavior: that is, how a
particular behavior facilitates reproductive success in its bearer. Phylo-
genetic explanations, on the other hand, focus on understanding the
evolutionary history of a behavior: that is, how a particular behavior
came into being and then changed in a step-by-step manner over time.
The information derived from each of these two levels of evolutionary
theory differs, but this information is not mutually exclusive. Insights
derived from one level of evolutionary explanation do not negate the in-
sights derived from the other. Despite the complementary nature of
these two evolutionary perspectives, most research on the evolution of
sexual behavior has taken place from a functionalist perspective, with
far less consideration being given to a phylogenetic perspective.
In this text, I explore how functional and phylogenetic explanations
can help account for same-sex sexual behavior and partner preference in
non-human primates. Cross-species comparisons indicate that same-
sex sexuality is not an evolutionarily uniform phenomenon. I argue here
that our understanding of why same-sex sexualities evolved is contin-
gent on the implementation of both types of evolutionary analysis. I be-
gin by discussing how same-sex sexual behavior and sexual partner
preference can be studied from an ethological perspective. I then de-
scribe research on female bonobos (Pan paniscus) to illustrate how
functional investigations can help to explain why some forms of pri-
mate same-sex sexual behavior evolved. Following this, I describe my
own research on female Japanese macaques (Macaca fuscata) to illus-
trate how phylogenetic investigations can help account for how other
forms of primate same-sex sexuality evolved, such as those that are
Paul L. Vasey 217
strictly sexual in nature. I conclude by outlining recent empirical evi-

dence for maternally inherited factors favoring the evolution of male
homosexuality in humans. In so doing, I show how both functional and
phylogenetic perspectives need to be integrated to account for these
data and, by extension, the evolution of male homosexuality in humans.
Defining Sexual Behavior
Any useful discussion of the evolution of same-sex sexuality in ani-

mals requires an explicit statement concerning what counts as “sexual
behavior.” For this review, an ethological definition of sexual behavior
is needed that can be easily operationalized. As such, sexual behavior is
defined as including courtship displays (or sexual solicitations), mount-
ing, and any interaction involving genital contact between one individ-
ual and another. Although stimulation of the genitals or other erogenous
zones can result in orgasm, orgasmic response is not a necessary
criterion for labeling a behavior as sexual.
Other definitions of sexual behavior are much broader than the one I
employ in this text. For example, Bagemihl (1999) characterizes sexual
behavior in terms of five sweeping categories that include courtship, af-
fection, interactions involving mounting and genital contact, pair-bond-
ing and parenting activities. My concern with such an approach is that
by casting the net too widely, there is a risk of including social interac-
tions under the rubric of sexual behavior. This, in turn, could result in
preferences for particular social partners being labeled as sexual partner
preferences. This is not to say that relationships such as pair-bonding or
affectionate behaviors such as kissing cannot be sexual. However, la-
beling them as sexual typically occurs because they exist in close tem-
poral association with courtship displays, mounting, or genital contact.
In the absence of such sexual markers, the sexual or social character of a
particular behavior is open for debate.
It deserves to be stressed that a sexual act or interaction (e.g., sexual
behavior) is not, and should not, be taken as synonymous with sexual
orientation (e.g., heterosexuality, homosexuality, and bisexuality, in
addition to various paraphilic sexualities such as zoophilia, pedophilia,
autogynephilia, etc.). Sexual orientation refers to an individual’s overall
pattern of sexual attraction/arousal as measured by multiple parameters
such as behavior, fantasy, courtship, and genital blood flow. Further,
sexual behavior should not be equated with sexual orientation identity
(i.e., the sexuality that one feels themselves to be, such as gay, straight,
bisexual, queer, boidyke, etc.) (for a theoretical discussion, see Cass,
1983/1984). With the exception of the great apes, evidence for self-rec-
ognition in animals is weak (reviewed in Tomasello & Call, 1997). As
such, there is no reason to expect that animals would develop personal
identities based on an introspective sense of sexual orientation. In addi-
tion, some cultures, but not others, have created systems for classifying
people based on their sexual behaviors and/or sexual orientations. The
deployment of such classification schemes typically involves the im-
plicit presupposition that particular types of sexual behavior and sexual
orientations encapsulate the very essence of an individual. Classifying
individuals in this manner results in culturally constructed categories of
sexual being (e.g., the homosexual, the heterosexual, the bisexual, the
gay man, the lesbian, etc.) (Foucault, 1990; Katz, 1995; for non-West-
ern examples, see Nanda, 2000). Sexual behavior in animals should not
be taken as evidence for membership in one of these culturally con-
structed categories. There is no evidence that animals classify their
conspecifics in this manner nor is there a particular reason to expect that
they would do so. In addition, the execution of a homosexual behavior
does not imply any sort of a temporally stable pattern of activity. There-
fore, both a homosexual and a bisexual individual who engage in homo-
sexual behavior will have different sexual histories. The homosexual
individual may exhibit a temporally stable pattern of same-sex sexual
behavior and exclusive same-sex sexual partner preference over the life-
span, whereas the bisexual individual may exhibit a variety of sexual
histories including punctuated periods of same-sex sexual behavior
throughout his or her lifetime, coupled with facultative same-sex sexual
partner preference in the context of less sexually desirable other-sex
alternatives that might be available at a particular point in time.
Care must be taken not to make semantic leaps from “sexual behav-
ior” to language that denotes sexual orientation, sexual orientation iden-
tity, categories of sexual beings, or temporally stable patterns of sexual
activity and sexual preference. Some authors fail to make these concep-
tual distinctions (e.g., Dixson, 1998; Wallen & Parsons, 1997), which
can lead to unnecessary disagreements over interpretation of the behav-
ioral data. Clearly, my conservative definition of sexual behavior risks
excluding potential episodes of sexual activity, and some researchers
will find it decidedly narrow. Nevertheless, a much stronger case can be
made that those behaviors that are consistent with my definition are
indeed sexual.
A large body of observational evidence exists indicating that interac-
tions involving same-sex courtship, mounting, and genital contact are
phylogenetically widespread (Bagemihl, 1999; Vasey, 1995; Wallen &
Paul L. Vasey 219
Parsons, 1997). The frequency with which such behaviors are mani-
fested varies greatly both inter-specifically and intra-specifically, but
the existence of such interactions seems to be relatively uncon-
tested by the scientific community. Although scientists have recog-
nized that manipulation of steroid hormones (Adkins-Regans,
1998), lesions to the medial preoptic-anterior hypothalamus
(Paredes & Baum, 1995), and rearing in unisexual social groups
(Adkins-Regan & Krakauer, 2000; Price, Katz, Wallach & Zenchak,
1988; Price & Smith, 1984/1985; Zenchak, Anderson & Schein, 1981)
promote the expression of same-sex interactions in certain species, they
have commonly acknowledged that such behaviors also occur in
hormonally and neurologically unmanipulated animals raised in spe-
cies-typical social environments.
Criteria for Determining Same-Sex Sexual Partner Preference

in Animals
Sexual partner preference refers to an individual’s predilection for

sexual partners of one sex or the other, or both, when given a choice.
Bagemihl (1999) has argued persuasively that at least some individu-
als in over fifty bird and mammal species exhibit a sexual preference
for members of the same-sex. He describes five different types of in-
teractions among animals as evidence for this conclusion. First are
exchanges in which individuals compete with other-sex rivals (i.e.,
inter-sexual competition) for same-sex sexual partners. Second are
interactions in which the objects of inter-sexual (i.e., male-female)
competition go on to engage in sexual behavior with the same-sex com-
petitor. Third are occasions when animals repeatedly form pair-bonds
with same-sex individuals or repeatedly select same-sex sexual part-
ners. Fourth are interactions in which animals reunite with same-sex
partners following prolonged separations from other-sex individuals.
Fifth are situations in which animals engage in same-sex sexual behav-
ior in the presence of other-sex individuals. Although such examples
are certainly suggestive of a preference for same-sex sexual partners
and deserve more complete investigation, they are by no means defini-
tive proof of such a preference. In fact, for most cases presented by
Bagemihl (1999), alternative explanations can be generated to account
for why individuals are engaging in the same-sex courtship, mounting,
and genital contact observed.
Evolutionists operate with the assumption that animals behave in
ways to maximize their reproductive success. For this reason, evolu-
tionists do not tend to question whether sexual activity between males

and females reflects a preference on the part of the participants for the
other sex. However, claims that some animals exhibit same-sex sexual
partner preference are likely to be met with a healthy dose of skepti-
cism. Consequently, if such claims are to be taken seriously and to have
any important impact on the manner in which evolutionists conceptual-
ize sexuality, then rigorous criteria for the existence of same-sex sexual
partner preference in animals need to be developed and applied (Vasey,
2002a).
More definitive proof as to whether animals ever exhibit an exclusive
or facultative preference for same-sex sexual partners over other-sex
ones requires observing a male or female individual (the subject) in a
choice situation where they have the opportunity to select between a
same-sex or other-sex sexual partner (the stimulus animals). Several ad-
ditional criteria must be met before concluding that choice of a
same-sex sexual partner reflects a sexual preference on the part of the
subject animal: (a) the subject should be able to simultaneously
choose between a male or female; (b) the two stimulus animals
should ideally be sexually proceptive vis-à-vis the subject; (c) these
interactions must culminate in actual sexual behavior between the
subject and the same-sex stimulus animal; (d) the subject must be
uncoerced; and (e) the behaviors used to measure sexual partner pref-
erence must be sexual, at least in part.
The condition of simultaneous choice is key because without such a
situation, it is impossible to determine whether the choice of a same-sex
sexual partner reflects the subject’s true sexual partner preference, or
simply one that occurred because an other-sex alternative was unavail-
able. Sexual proceptivity on the part of the stimulus animals is impor-
tant because in the absence of such motivation the possibility cannot be
eliminated that a same-sex sexual partner, if chosen, was selected sim-
ply because an other-sex sexual partner, although physically present,
was not motivated to engage in sexual activity. The condition that the
interaction must culminate in actual sexual behavior is a necessary one
because in the absence of such a behavioral endpoint it is impossible to
determine which stimulus animal, if any, is the preferred sexual partner.
Some researchers have used spatial proximity to a male or female stim-
ulus animal as a measure of sexual partner preference (e.g., Hetta &
Meyerson, 1978; Meyerson & Lindström, 1973). This type of informa-
tion might tell us something about social partner preferences, but it tells
us nothing definitive about sexual partner preference. Sexual coercion
involves the use or threat of aggression to obtain sexual contact with an
Paul L. Vasey 221
individual against their will. It is unclear how common coercion of

same-sex sexual partners is in the animal kingdom. It has, however,
been observed in a number of animal species (reviewed in Bagemihl,
1999) and studied systematically in some, such as elephant seals (e.g.,
Rose, Deutsch, & LeBoeuf, 1991). As such, the confounding effects of
same-sex sexual coercion should not be dismissed as unimportant.
Rather, when determining same-sex sexual partner preference, the con-
dition of uncoerced choice is essential because in the absence of
uncoerced choice, it is impossible to determine whether any resulting
sexual behavior between the subject and a same-sex stimulus animal
reflects the subject’s true sexual partner preference or one that has been
over-ridden through coercive means.
Again, researchers should also demonstrate that the behaviors used to
measure sexual partner preference are sexual, if only in part. There are
at least three means by which the sexual nature of same-sex courtship,
mounting, and genital contact might be established using non-invasive
observational techniques. First, the same-sex behaviors under investi-
gation are patterned in similar ways to male-female courtship and copu-
lation. Although male-female courtship and copulation should not be
the yardsticks by which all other types of sexual behaviors are mea-
sured, many researchers consider these behaviors to be sexual a priori
(for discussion, see Bagemihl, 1999). Consequently, demonstrating that
same-sex courtship, mounting, and genital contact parallel their male-
female counterparts in terms of their expression represents strong evi-
dence for many researchers that the former are indeed sexual behaviors.
Second, in determining sexual motivation, patterns of same-sex court-
ship, mounting, and genital contact should differ in their expression
from more generalized patterns of social affiliation. If we subscribe to
the idea that sexual behaviors are related to but ultimately distinct from
ordinary social behaviors, then presumably patterns of sexual affiliation
should not completely mimic patterns of affiliation that are widely rec-
ognized as social. Third, prolonged and directed genital stimulation, or
orgasm, or both during same-sex interactions represent definitive proof
for many researchers that the behaviors are sexually motivated. Again,
the failure to provide clarity with regards to the sexual nature of the be-
haviors in question results in confusion over whether individuals are
choosing purely social partners, or ones that are at least in part sexual.
Of course, a behavior can be simultaneously social and sexual. For ex-
amples, animals and humans may derive intense sexual gratification
from sexual interactions that occur as part of a reconciliation process
(see information on bonobos below). As such, a behavior may well have
a social function, but this does not in and of itself demonstrate an

absence of sexual motivation on the part of the participants.
Same-sex sexual partner preference can be exercised in relation to
other-sex sexual partners or to other-sex reproductive partners. These
two distinct forms of same-sex sexual partner preference should not be
treated as synonymous. Moreover, evidence for or against one should
not be taken as evidence for or against the other. One can imagine, for
example, a situation in which individuals invariably prefer reproductive
partners to same-sex sexual partners. However, when the issue of repro-
duction is moot, these same individuals might on occasion, or even reg-
ularly, prefer same-sex sexual partners to other-sex ones. Preference for
a same-sex sexual partner over an other-sex reproductive partner can
only be demonstrated if all of the criteria outlined above are met. In ad-
dition, researchers must also demonstrate that the subject animal es-
chewed sex with an other-sex stimulus animal that was potentially
reproductive, in favor of sexual activity with a same-sex stimulus
animal.
Although same-sex courtship, mounting, and genital contact are
phylogenetically widespread and occur quite frequently in some spe-
cies, the expression of these behaviors does not necessarily reflect some
underlying preference for same-sex sexual partners. Alternative expla-
nations exist for the occurrence of such behavior, and these alternatives
need to be carefully considered before they can be rejected. Indeed, ex-
clusive and even facultative same-sex sex sexual partner preference ap-
pears to be extremely rare in the animal kingdom (Vasey, 2002a). Apart
from domestic rams (Ovis aries), there exist no conclusive examples of
exclusive, same-sex sexual partner preference in animals (e.g., Perkins &
Fitzgerald, 1997; Resko, Perkins, Roselli, Fitzgerald, & Stormshak,
1999; Roselli, Resko, & Stormshak, 2002), although anecdotal evi-
dence suggests that this phenomenon may occur in certain bird species,
such as gulls (reviewed in Bagemihl, 1999). At this time, conclusive ev-
idence of facultative same-sex sexual partner preference in animals ex-
ists only for female Japanese macaques (Vasey, 1998, 2002a; see
below). Anecdotal evidence for facultative same-sex sexual partner
preference in females exists for a number of additional species, includ-
ing cattle (Bos taurus), a type of African ungulate known as the Uganda
kob (Kobus kob tomasi), and a type of New Zealand swamp bird, the
pukeko (Porphyrio porphyrio melanotus) (reviewed in Vasey, 2002a).
Clearly our knowledge concerning same-sex sexualities in animals is
very limited at present, so this area is wide open for future research.
Paul L. Vasey 223
EVOLUTIONARY THEORY AND SAME-SEX SEXUALITY
From an ultimate evolutionary perspective, sexual selection and pa-

rental investment theories are the key theoretical frameworks for inter-
preting the evolution of sexual behavior (Darwin, 1871; Trivers, 1972).
Darwin (1871) described sexual selection as a process of differential re-
production among males that occurs because males vary in their ability
to acquire female mates (i.e., reproductive partners). He identified two
key mechanisms that influence mate acquisition. Mate competition oc-
curs intra-sexually among males for females and encompasses various
interactions from physical fights and threats (e.g., contest competition)
to ritualized displays aimed at attracting discriminating females (e.g.,
courtship competition). Mate choice occurs inter-sexually and involves
females selecting the most attractive male competitor (i.e., the one that
is the most genetically superior or who contributes the most in terms of
parental care). More recently, Smuts and Smuts (1993) proposed that
sexual coercion is an additional mate acquisition mechanism that males
can employ if they are unsuccessful at competing for or attracting
female reproductive partners.
Sex differences in patterns of mate choice and competition have been
explained in terms of Trivers’ (1972) parental investment theory. In
“typical” species, females provide more parental investment than
males. This difference limits their potential reproductive rate so that at
any one time there will be fewer receptive females than there are repro-
ductively active males in a population. Thus, theoretically speaking,
males should compete intra-sexually for reproductive access to females,
coerce females if necessary, and copulate relatively indiscriminately.
Females, on the other hand, should carefully discriminate among poten-
tial male mates in favor of those that contribute the most to offspring
quality and survival. In “atypical” species, the roles are reversed; males
provide the bulk of parental investment and are choosy about the fe-
males with which they copulate, while females compete among
themselves for male mates (Gywnne, 1991).
From the perspective of sexual selection and parental investment the-
ories, one might assume that sex is synonymous with reproduction. In
reality, of course, many species engage in non-reproductive sexual be-
haviors as well (Bagemihl 1999). Parental investment theory clearly
predicts that individuals should choose, compete for, and coerce sexual
partners that confer the greatest reproductive advantage (Smuts & Smuts,
1993; Trivers, 1972). And when given a choice, potentially reproductive
sex should be preferred over non-conceptive sex. Of course humans and
other animals engage in many different kinds of non-conceptive sex, but

basic evolutionary theory predicts that other-sex reproductive partners
should be preferred to same-sex sexual partners, sexual coercion should
occur inter-sexually, and mate competition should occur intra-sexually.
Because non-conceptive sexual behaviors would appear to under-
mine reproduction, it is appropriate to ask why animals would engage in
these behaviors at all. This question has been most closely examined in
relation to one type of non-reproductive sex: same-sex sexual behavior.
At an evolutionary (functional) level, scientists have widely argued that
same-sex sexual behavior is “socio-sexual” in character: that is, sexual
in terms of its outward form and enacted to facilitate some sort of adap-
tive social goal, such as dominance demonstration (Wickler, 1967).
Same-sex sexual interactions in bonobos provide excellent examples of
how such interactions can function to mediate adaptive social goals,
which help the participants to survive within complex social networks
and ultimately to reproduce.
Same-Sex Sexual Behavior in Bonobos: Functional Perspectives
Bonobos are well known for their sexual behavior, particularly sex-
ual interactions among members of the same sex (de Waal, 1987; de
Waal & Lanting, 1997). For example, bonobo females rub their genita-
lia together in lateral movements known as genito-genital rubbing
(“gg-rubbing”; Kuroda, 1980). Same-sex encounters between males in-
clude “french kissing,” fellatio, manual genital massage, and “penis
fencing” (de Waal & Lanting, 1997).
Numerous authors have described same-sex sexual behavior in
bonobos as sociosexual in nature. Sociosexual behaviors are those that
are sexual in terms of their outward form, but are enacted principally to
mediate some sort of fitness-enhancing social goal. Although sexual
arousal can be a component of sociosexual interactions, the social func-
tions that they mediate are typically characterized as being their primary
raison d’être. Many researchers have noted a relationship between so-
cial tension and same-sex sexual behavior in bonobos, particularly
around feeding activity. Same-sex sexual behavior frequently occurs
between bonobo individuals feeding at the same food site, where signs
of tension over food are apparent (Kano, 1980; Kuroda, 1980, 1984;
Thompson-Handler, Malenky & Badrain, 1984; de Waal, 1987; Furuichi,
1989; White & Thompson-Handler, 1989). Kuroda (1980) has inter-
preted same-sex sexual behavior among bonbos as a mechanism to re-
duce tension during periods of close proximity in the same food patch.
Paul L. Vasey 225
He argued that same-sex sexual behavior “works to calm anxiety or ex-

citement, to dissolve inter-individual tension” and “thus to increase tol-
erance, which makes food sharing smooth” (Kuroda, 1980, p. 190). In
support of this hypothesis, individuals entering an occupied patch are
more likely to acquire food after engaging in same-sex sexual interactions
(Kuroda, 1984; de Waal, 1987; Furuichi, 1989). Moreover, genito-genital
rubbing between female bonobos is positively correlated with food patch
size, which presumably reflects the amount of time individuals spend in
close proximity competing for resources (White & Thompson-Handler,
1989). Sexual behavior between females also promotes alliance forma-
tion between the participants, which allows partners to monopolize food
sources and deter male harassment (Kano, 1980; Parish, 1994) or gain en-
try into a new group (Furuichi, 1989; Idani, 1991).
When mechanisms for regulating aggression fail, bonobos also
use same-sex sexual behavior to re-establish social bonds. Research
demonstrates that same-sex sexual interactions increase signifi-
cantly following agonistic conflicts (including those unrelated to
food), compared to pre-conflict control periods (de Waal, 1987; Hoh-
mann & Fruth, 2000; Kano, 1980). Researchers have interpreted this
distinct temporal pattern as evidence that same-sex sexual activity in
bonobos mediates reconciliation (de Waal, 1987; Hohmann & Fruth,
2000). De Waal (1987) found that aggressors were more likely to initi-
ate same-sex sexual contact with their victims than vice versa, which he
interpreted as reconciliation attempts by the aggressors.
Taken together, this body of research suggests that same-sex sexual
interactions in bonobos evolved because it functions to facilitate a
number of adaptive sociosexual goals, including (a) the regulation of
social tension and (b) alliance formation, particularly in the context of
food competition, and (c) reconciliation following the outbreak of ag-
gression.
Same-Sex Sexuality in Japanese Macaques:

A Phylogenetic Perspective
Female Japanese macaques, in certain populations, routinely en-

gage in both other-sex and same-sex sexual behavior over the course
of their life spans. Sexual behavior is only loosely linked to ovulation
and females engage in sexual activity before and after their ovulatory
periods (Fedigan & Gouzoules, 1978; Gouzoules & Goy, 1983; O’Neill,
Fedigan, & Zeigler, 2004). Female same-sex sexual behavior occurs
in both captive (Chapais & Mignault, 1991; Chapais, Gauthier, Prud’
homme, & Vasey, 1997; Lunardini, 1989; Rendall & Taylor, 1991;
Vasey, 1996, 1998; Vasey & Gauthier 2000; Vasey, Chapais & Gauthier,
1998) and free-ranging (Eaton, 1978; Enomoto, 1974; Fedigan &
Gouzoules, 1978; Gouzoules & Goy, 1983; Takahata, 1982; Wolfe,
1984) populations of this species. Consequently, these types of same-
sex interactions cannot be dismissed as abnormal products of captivity.
Female-female sexual behavior in Japanese macaques takes place
during temporary but exclusive associations termed “consortships.”
These relationships can be brief, lasting less than one hour, or they can
continue for over a week (Wolfe, 1984). During same-sex consortships,
females solicit each other to mount and to be mounted, using vocaliza-
tions and a variety of postural and facial gestures. Sexual solicitations
include pushing, hitting, grabbing, slapping the ground, head bobbing,
screaming, lip quivering, body spasms, and intense gazing. A female
can specifically request to be mounted by presenting her inclined back
or her hindquarters to a potential mounter. Conversely, a female can
specifically request to mount another female by placing her hands on
the other’s hindquarters (Vasey et al., 1998). Single mounts between fe-
males are rarely observed. Instead, multiple mounts or a series of
mountings between consort partners is the norm. During these interac-
tions, females mount each other in a bi-directional manner and routinely
employ up to eight different types of mounting postures (Vasey et al.,
1998). During mounts, mounters often thrust against mountees who in
turn commonly reach back to grasp the mounter and gaze intently into
her eyes.
Mounting between consort partners and the accompanying sexual so-
licitations can continue uninterrupted for well over an hour. Thus, sex-
ual behavior is clearly the defining feature of same-sex consortships.
Between bouts of sexual activity, partners exhibit highly synchronized
activity, such as huddling and sleeping together, as well as grooming,
following, and defending each other for prolonged periods of time
(Gouzoules & Goy, 1983; Vasey, 1996; Wolfe, 1984). Partners will
also forage side-by-side during same-sex consortships, although this
form of co-feeding is not a prominent feature of these relationships.
The frequency of female-female sexual behavior varies both within
and between Japanese macaque populations. In some populations, the
behavior has never been reported and appears to be non-existent. In
other populations, some females engage in same-sex sexual behavior,
while others do not, and the proportion of females engaging in the be-
havior varies from year to year. In the Arashiyama West (Texas) popu-
lation, for example, the proportion of females engaging in same-sex
Paul L. Vasey 227
consortship activity has been reported to vary from 61% (Fedigan &
Gouzoules, 1978) to 51% (Gouzoules & Goy, 1983) and 78% (Wolfe,
1984). Similarly, in the Arashiyama (Japan) troop of Japanese ma-
caques, the proportion of females engaging in same-sex consortship ac-
tivity has been reported to vary from 47% (Takahata, 1982) to 23%
(Wolfe, 1984). In still other populations, every sexually mature female
engages in same-sex consortship activity, and they do so frequently. For
example, Vasey (2002b) reported that during a typical mating season
(October 1993-February 1994) every sexually mature female in the
University of Montreal colony (14 sexually active females and five sex-
ually active males) engaged in female-female sexual behavior. During
consortships, females mounted each other on average 31 times per hour
of observation (N = 129 observation hours). The population-specific
nature of this behavior has led some researchers to suggest that these be-
haviors represent group-specific social “traditions” (Stephenson,
1973). If this is true, we have no empirical information at present as to
how such sexual traditions might be socially transmitted.
A number of convergent lines of evidence indicate that female
same-sex sexual behavior in Japanese macaques is a sexual behavior
(Fedigan & Gouzoules, 1978; Gouzoules & Goy, 1983; Wolfe, 1984;
Vasey, 1996; Vasey et al., 1998). To begin with, same-sex sexual inter-
actions follow many of the same patterns as male-female copulation.
For example, female same-sex sexual behavior is never observed out-
side of the species’ fall-winter mating season and females that engage in
same-sex sexual behavior exhibit a reddening of the face and perineum
that is indicative of increased sexual receptivity. Like heterosexual in-
teractions, female-female sexual behavior occurs within the context of
temporary but exclusive sexual relationships called consortships. Fe-
male same-sex sexual behavior is temporally linked to the bi-directional
exchange of sexual solicitations between partners, and these sexual so-
licitations appear to be identical to those exchanged in the context of
male-female sexual interactions. Moreover, females employ certain
mounting postures in a same-sex context (e.g., double-foot clasp
mounts with thrusting) that appear to be indistinguishable from the ones
that males employ during copulation. Finally, female mountees do not
try to push or shake off the mounter; instead, they typically brace their
bodies to support the mounters. Often, the mountees will facilitate
mounts-in-progress by reaching back and clasping the mounters while
gazing into the mounters’ eyes. The same pattern occurs during
male-female mounts.
When considering the issue of sexual motivation, it is worth noting

that patterns of affiliation during same-sex consortships do not mimic
generalized patterns of social affiliation that occur outside of these
associations. Rather, patterns of affiliation between females during
same-sex consortships represent radical departures from normal pat-
terns of affiliation that are widely recognized as social. This suggests
that same-sex consortships are not social relationships but rather are
sexual ones. Consistent with male-female sexual relationships, female
Japanese macaques exercise incest avoidance with close female kin (r =
0.25) (for more details, see Chapais et al., 1997). Mounting, sexual so-
licitations, and consortships are never observed between mothers and
daughters, between sisters, or between grandmothers and grand-
daughters (Chapais & Mignault, 1991; Chapais et al., 1997; Wolfe,
1984). In contrast, close female kin commonly engage in other types
of affiliative behavior with each other, such as grooming, huddling,
and supporting each other during conflicts with third-party individuals
that are more distantly related (Chapais, 1992; Koyama, 1991; Kurland,
1977). Female consort partners intervene in conflicts to support each
other at consistently high rates during same-sex consortships. Outside
the consortship period, these same females rarely support each other
(Vasey, 1996). In addition, normal dominance relationships are tempo-
rarily destabilized during same-sex consortships because subordinate
consort partners receive support from their dominant partners against
targets that normally rank above them or with whom they share ambigu-
ous dominance relationships (Vasey, 1996). Also, dominant consort
partners groom their subordinate counterparts significantly more often
than the reverse (Vasey, 1996). Outside of same-sex consortships, the
opposite pattern holds true; female Japanese macaques overwhelmingly
direct grooming up the hierarchy, not down (Chapais, Gauthier, &
Prud’homme, 1995; Koyama, 1991). Finally, females are almost exclu-
sively in proximity with their non-kin consort partners during same-sex
consortships (Gouzoules & Goy, 1983; Vasey, 1996, 1998; Wolfe,
1984). Outside the consortship period, however, female Japanese ma-
caques spend most of their time in proximity with close kin (Kurland,
1977; Singh, D’Souza, & Singh, 1992).
Finally, repetitive vulvar contact and stimulation occur during most
female-female mounts (Vasey & Duckworth, in press). Two forms of
vulvar stimulation by female mounters have been observed and these
can occur separatively, simultaneously, or sequentially. While sitting in
a jockey-style position on the mountee, a female mounter will rub her
vulva against the mountee’s back. In addition, female mounters stimu-
Paul L. Vasey 229
late their vulvas with their tails during same-sex mounts. During
mounts, mounters move their tails in a directed, voluntary, sex-specific
manner and are never observed to do so in non-sexual contexts (e.g.,
grooming interactions). Given the vulva’s and more specifically the cli-
toris’ primary role in mediating sexual response, the results of this re-
search provide direct evidence bearing on the sexual nature of female-
female mounting in Japanese macaques.
Taken together, these various lines of evidence suggest that female-
female courtship, mounting, and genital contact among Japanese ma-
caques are sexual behaviors. Moreover, the overwhelmingly bi-direc-
tional flow of sexual solicitations, mounts, clasping, approaches, and
conflict interventions within consortships (Chapais & Mignault, 1991;
Vasey, 1996; Vasey et al., 1998) suggests that these relationships are
based on a mutual sexual attraction between the partners.
Sexual Partner Preference Among Female Japanese Macaques
Having marshaled support for the conclusion that female same-sex

sexual behavior in Japanese macaques is a sexual behavior, I now turn
to the issue of sexual partner preference. Vasey (1998) analyzed pat-
terns of sexual partner preference in anovulatory female Japanese ma-
caques that were the focus of inter-sexual competition. His study
subjects lived in a captive, mixed-sex group of 37 individuals: 18 sexu-
ally active females, ages 3.5-23 years; 5 sexually active males, 4.5-9.5
years; and 14 sexually immature individuals. These individuals were
members of three unrelated families named A, B, and C in accordance
with their overall dominance relationships (A > B > C). The size, adult
sex ratio, kinship composition, and organization of this study group fell
well within the normal ranges and patterns reported for free ranging
populations of Japanese macaques (Kawai, 1958; Yamagiwa & Hill,
1998). Consequently, Vasey’s (1998) study subjects lived in a species-
typical social environment.
Inter-sexual competition for female sexual partners occurred when a
sexually motivated male and female (competitors) simultaneously
sought access to the same anovulatory female sexual partner (focus of
competition). Competitors were considered to be sexually motivated,
vis-à-vis the focus of competition, if they solicited her for sex while
competing inter-sexually for her, or if they solicited her for sex at some
point during the same day. Inter-sexual competition for female sexual
partners was manifested during intrusions and counter-challenges. In-
trusions occurred when a male competitor attempted to acquire exclu-
sive access to an infertile or post-conception female engaged in a

same-sex consortship by targeting that female as the focus of competi-
tion and her partner as his competitor (N = 120 intrusions). Intrusions
took the form of approaches and sexual solicitations directed at the fo-
cus of competition, as well as displacements and aggression directed at
the female competitor. As such, intrusions functioned to increase the
male’s access to an anovulatory female sexual partner (i.e., the focus of
competition), while decreasing or preventing her same-sex consort
partner from doing the same.
Intrusions on same-sex consortships did not reflect a generalized mo-
tivation among males to disrupt any type of affiliation between non-kin
females. Males intruded on same-sex consortships for female sexual
partners 4.3 times more often (0.6 intrusions/hr; x = 0.15) than they in-
terfered with non-kin female grooming dyads observed outside the mat-
ing season (0.14 grooming interferences/hr; x = 0.04). The tendency to
disrupt females engaged in sexual affiliation but not to disrupt those en-
gaged in social affiliation strongly suggests that intrusions are correctly
identified as sexual, not social, competition.
Following 62% of intrusions, inter-sexual competition for female
sexual partners terminated. In such cases, the consorting females exhib-
ited a range of reactions. They might ignore the male who would even-
tually leave, move away from the male altogether, separate and then
rejoin to continue their consortship, or terminate their consortship alto-
gether. Inter-sexual competition for female sexual partners could, how-
ever, escalate with the female competitor posing a counter-challenge
against the intruding male. Counter-challenges occurred following an
intrusion when a female competitor attempted to maintain exclusive ac-
cess to her consort partner, the focus of competition, while preventing
the male competitor from doing the same. Counter-challenges took the
form of approaches and sexual solicitations directed at the focus of
competition, as well as displacements and aggression directed at the in-
truding male competitor. During some counter-challenges, female com-
petitors would also interpose themselves between the male competitor
and the focus of competition. Overall, 38% of intrusions by male
competitors provoked counter challenges by female competitors (N =
45 counter-challenges observed).
Proceptive females did not perform counter-challenges simply be-
cause they were in a heightened state of arousal and, thus, more asser-
tive. They retaliated in kind against males that aggressed or displaced
them significantly more often when they were engaged in same-sex
consortships (x = 17.4%) compared to when they were not (x = 0.01%;
Paul L. Vasey 231
p < 0.05). Further, females were never seen to retaliate against males
that disrupted their grooming interactions with non-kin females outside
the mating season. The females’ tendency to challenge males that dis-
rupted their sexual but not their social affiliations strongly suggests that
counter-challenges are correctly identified as sexual competition and
are not part of a more generalized pattern of social competition.
Following episodes of inter-sexual competition, females that were
the foci of competition could choose between two sexually motivated
competitors–one male and the other female–that were simultaneously
available. In only one instance of inter-sexual competition for female
sexual partners (N = 120) was a female focus of competition sexually
coerced by a female competitor. Consequently, these interactions repre-
sented an excellent natural experiment for testing whether females pre-
ferred certain female sexual partners relative to male alternatives when
given a choice. By examining sexual partner choice in anovulatory fe-
males, Vasey (1998) was able to ensure that subjects were choosing be-
tween two sexual partners, one male and one female. In contrast, had
sexual partner preference been examined in females that were ovulat-
ing, then the subjects would have had to choose between a female sex-
ual partner and a male reproductive partner. Obviously, this would have
introduced the confounding effect of reproductive preference. In the
overwhelming majority of cases (92.5%; N = 120), the foci of competi-
tion chose to continue mounting with their female sexual partners sig-
nificantly more often (p < 0.01) than they chose to begin mounting with
the male competitor, or to cease mounting altogether. Taken together,
this research suggests that in some populations female Japanese ma-
caques sometimes prefer female sexual partners even when they are si-
multaneously presented with sexually motivated male partners.
Many animal species, such as bonobos, appear to engage in same-sex
sexual activity to facilitate adaptive, sociosexual functions (e.g.,
Bagemihl, 1999; Dixson, 1998; Wallen & Parsons, 1997). In contrast,
no study has demonstrated any sort of sociosexual function for female-
female sexual activity in Japanese macaques despite over 40 years of in-
tensive research on populations such as Arashiyama (Japan), where fe-
males regularly engage in same-sex mounting and courtship (Takahata,
1982; Wolfe, 1984). All of the available evidence indicates that fe-
male-female mounting and courtship are not sociosexual behaviors in
this species. Female Japanese macaques do not use same-sex mounting
and courtship to attract male sexual partners, impede reproduction by
same-sex competitors (Gouzoules & Goy, 1983; Vasey, 1995), form al-
liances, foster social relationships outside consortships (Vasey, 1996),
communicate about dominance relationships, reduce social tension as-

sociated with incipient aggression (Vasey, Chapais, & Gauthier, 1998),
obtain alloparental care (Vasey, 1998), practice for heterosexual activ-
ity (i.e., female-male mounting), or reconcile conflicts (Vasey, 2004). If
female-female sexual activity in some populations of Japanese mac-
aques is not functional as the data suggest, then how might we account
for this phenomenon?
I have argued previously that female Japanese macaques engage in
same-sex sexual interactions because in doing so they obtain immediate
sexual reward (Vasey & Duckworth, in press; Vasey, Foroud,
Duckworth, & Kovacovsky, 2006). Females frequently engage in pro-
longed and directed clitoral stimulation during same-sex mounting
(Vasey & Duckworth, in press), and they employ a variety of mount
postures and pelvic movements aimed at stimulating their genitals
(Vasey, Foroud, Duckworth, & Kovacovsky, 2006). However, my ac-
count of same-sex sexual behavior between female Japanese macaques
in terms of proximate sexual reward does not address why the behavior
evolved in the first place. In this regard, I have suggested that female-fe-
male sexual activity is not an adaptation, but is the functionless
by-product of an adaptation (Vasey, 1996, 1998, 2002a, 2002b, 2004;
Vasey et al., 1998). Functionless by-products of adaptations are charac-
teristics that do not evolve to solve adaptive problems and, thus, do not
have a function and are not products of natural selection. Instead, func-
tionless by-products evolve in association with particular adaptations
because they happened to be coupled with those adaptations (Buss,
Haselton, Shackelford, Bleske, & Wakefield, 1998). Functionless
by-products of adaptations cannot be explained in adaptive terms and,
instead, phylogenetic history must be invoked to account for their exis-
tence. Explanations that invoke phylogenetic history focus on recon-
structing the evolutionary steps that lead to a current behavior. This
process involves understanding the origin of the behavior and how it
has changed over time (Alcock, 1989).
I have speculated previously that female-female sexual behavior as
expressed in some populations of Japanese macaques is a functionless
by-product of an adaptation: namely, female-male mounting (Vasey,
2002a). Female-male mounting is routinely observed in certain popula-
tions of this species (Gouzoules & Goy, 1983), and I have suggested
that this behavior is an adaptation that females employ to prompt sexu-
ally disinterested or sluggish males to copulate with them (Vasey,
2002a). In line with this hypothesis is the observation that proceptive fe-
males routinely perform mount prompting and mounts in response to
Paul L. Vasey 233
movement by desired males away from their immediate vicinity

(Vasey, personal observation). Once females evolved the capacity to
mount and the capacity to derive sexual gratification during mounts
through clitoral stimulation, they could do so just as easily by mounting
females as mounting males. Indeed, at that point in the species’ evolu-
tion, some same-sex sexual partners might be preferred over certain
other-sex alternatives (see Vasey, 1998, 2002a, 2002b; Vasey &
Gauthier, 2000) simply because females derive more sexual gratifica-
tion during interactions with them. Within the context of this evolution-
ary scenario, female-male mounting can be explained in terms of
function and phylogenetic history, but female-female mounting can
only be explained in terms of the latter.
IMPLICATIONS FOR THE EVOLUTION

OF SAME-SEX SEXUAL BEHAVIOR IN HUMAN MALES
The foregoing discussion has been intended to illustrate how evolu-

tionary explanations at both the functional and phylogenetic level can
contribute towards a more comprehensive understanding of same-sex
sexuality. I have attempted to take lessons learned from cross-species
research and apply them toward rethinking how we might study and
reconceptualize the evolution of human same-sex sexual behavior. I do
not offer any definitive explanations as to how human same-sex sexual
behavior evolved. Rather, my goal here is to highlight how an expanded
concept of what counts as an “evolutionary” explanation (i.e., func-
tional and phylogenetic analyses) might contribute toward a better un-
derstanding as to the ultimate basis for same-sex sexual behavior in
humans. My focus here is on male homosexuality in humans because
very little, if any, evolutionary research has been conducted on female
homosexuality (see Diamond, this volume).
To date, functional attempts to understand same-sex sexuality in hu-
man males have not been particularly fruitful. Wilson (1975) proposed
that if androphilic males (i.e., adult males that are sexually attracted to
adult males) sufficiently increase the reproductive success of kin then
the shared genetic material transmitted to the next generation via kin
may offset the individual’s lack of offspring. In other words, if
same-sex oriented individuals function as “helpers” promoting their
kins’ reproductive success, then kin selection could maintain genes for
homosexuality. Literature reviews have generated little evidence in
support of the hypothesis that lineages gain reproductive advantage
through offspring-care by same-sex oriented members (Kirkpatrick,

2000; Muscarella, 2000). Two studies, one conducted in the United
States (Bobrow & Bailey, 2001) and the other in the United Kingdom
(Rahman & Hull, 2005), found that homosexual males were no more
likely than heterosexual males to channel financial and emotional re-
sources to close relatives. On the basis of these results, male homosexu-
ality in humans is unlikely to have evolved by kin selection.
Another line of theoretical inquiry suggests that same-sex attraction
and sexual behavior are adaptative mechanisms that facilitate alliance
formation among males. Based on his review of the anthropological lit-
erature, Kirkpatrick (2000) argued that male same-sex sexual behavior
and erotic attraction are adaptations that functions to reinforce fitness
enhancing same-sex alliances among individuals who are facultatively
bisexual. In a similar vein, Kauth (2000) argued that females may prefer
male mates who form same-sex erotic alliances because such males
would be better able to acquire resources and would enjoy larger social
networks and increased status. As such, erotic attraction for males could
be selectively favored over evolutionary time owing to its adaptive
value as a mechanism promoting alliance formation among males.
My empirical research on Japanese macaques indicates, however,
that these conclusions may be premature because same-sex sexual inter-
actions and alliance formation may be correlated without the former be-
ing an adaptation for the latter (Vasey, 2000). In Japanese macaques,
females that engage in same-sex sexual behavior frequently form alli-
ances. They do not, however, engage in same-sex sexual activity for the
express purpose of alliance formation (Vasey, 1996). If the primary rea-
son for engaging in same-sex consortships is to mediate alliance forma-
tion, then two key behavioral patterns should be expected to occur.
First, higher ranking females should be preferred as consort partners be-
cause they represent more powerful allies and, as such, are able to chal-
lenge targets that they dominate but that their subordinate consort
partners do not. By providing support against targets that rank above
their subordinate partners but below themselves, dominant consort part-
ners can help their partners increase in dominance temporarily, at little
risk to themselves (Chapais, 1992; Vasey, 1996). Females should, thus,
prefer to consort with dominant partners and competition for such part-
ners should ensue. The most successful competitors should also be the
most dominant ones. Given the constraint that incest avoidance places
against the formation of consortships with close kin (Chapais &
Mignault, 1991; Chapais et al., 1997; Wolfe, 1984), this should have re-
sulted in a concentration of consortships between members of the two
Paul L. Vasey 235
highest ranking families in my study group (i.e., A-B consortships ver-

sus A-C or B-C consortships where A family is dominant over B family
and C family, and B family is dominant over C family). Keeping in
mind that consortships between females were possible only if two indi-
viduals were receptive on the same days, a possible 42 A-B consort-
ships could have potentially been formed, of which 42.9% actually
occurred (Vasey, 1996). Of a possible 12 A-C consortships, 41.7% ac-
tually occurred. Of a possible 13 B-C consortships, 38.5% actually oc-
curred. Thus, non-kin individuals of higher rank (A-B) did not form
consortships together significantly more often, than other types of
consortships (i.e., A-C, B-C). Moreover, there was also no significant
difference in the number of days over which each of the three different
types of consortships took place (x for A-B dyads = 5 days; x, A-C
dyads = 4.4 days; x, B-C dyads = 5.8 days).
Second, in light of the dominance-related benefits they derive from
same-sex consortships, subordinate partners should be more responsi-
ble for showing the affiliative behaviors that maintain these associa-
tions. This prediction was not supported, however. During same-sex
consortships, the overwhelming majority of affiliation flowed in a re-
markably bi-directional manner with no statistically significant differ-
ences between dominant and subordinate consort partners (Chapais &
Mignault, 1991; Vasey, 1996; Vasey et al., 1998). For example, 49% of
approaches (N = 2386) were performed by dominant members of the
consortships, and 51% by their subordinate partners (Vasey, 1996).
Similarly, 45.2% of sexual solicitations (N = 3,649), were performed by
dominant consort partners and 54.8% by subordinate partners. In addi-
tion, dominant females intervened in support of their subordinate con-
sort partners during 29.2% of the opportunities to do so (N = 411),
whereas subordinate females intervened for their dominant consort
partners during 8.7% of available opportunities (N = 601) (p = 0.16).
The sole difference in affiliative behavior involved grooming, which
the dominant consort partners performed significantly more often than
their subordinate counterparts. Out of 1,328 instantaneous scan samples
during which grooming was recorded dominant females groomed their
subordinate consort partners 86.2% of the time, and subordinate part-
ners groomed 13.8% of the time (p = 0.001). Thus, dominant consort
partners were actually more responsible for maintaining same-sex
consortships than their subordinate partners.
In sum, although female Japanese macaques that form homosexual
consortships tend to form alliances with each other against third-party
individuals, the patterns of partner choice and affiliation between con-
sort partners suggest that females were not engaging in these rela-
tionships for the express purpose of alliance formation. As such,
associations with useful allies during same-sex consortships, let alone
powerful ones, would be variable at best. This suggests that same-sex
sexual behavior was not specially designed by natural selection as a
sociosexual adaptation for alliance formation. The Japanese macaque
research indicates that we have to be cautious about concluding that
same-sex sexual behavior is an adaptation for alliance formation in hu-
mans simply because same-sex sexual partners engage in alliance-re-
lated activities with each other.
Mutual sexual attraction and gratification appear to be the basis on
which female Japanese macaques acquire and maintain same-sex sex-
ual partners (Vasey, 1996; Vasey, Chapais, & Gauthier, 1998; Vasey &
Duckworth, in press). If humans, like female Japanese macaques, typi-
cally choose same-sex sexual partners on the basis of “sexual emotion,”
as Kirkpatrick (2000) implies, then associations with useful allies, let
alone powerful ones, would occur only as often as mutual sexual at-
traction existed between such individuals. The variability inherent in
such a system of ally choice would seem to indicate that same-sex sex-
ual attraction and behavior were not designed by natural selection as
adaptations for alliance formation. In contrast, among bonobos, young
females immigrating into a new community appear to target dominant
resident females (i.e., potentially powerful allies) for sexual interac-
tions (Idani, 1991). The specificity of this partner choice suggests that
female-female sexual activity, as manifested by immigrant female
bonobos, may have been modified by natural selection to act as an adap-
tation for alliance formation.
Recently, Camperio-Ciani, Corna, and Capiluppi (2004) reported
that female maternal relatives of homosexual men have a higher fecun-
dity than female maternal relatives of heterosexual men. These results
suggest that there is a genetic advantage associated with male homosex-
uality: namely, the female maternal relatives of homosexual men expe-
rience increased reproductive success. Why would male homosexuality
be correlated with increased fecundity among female kin? LeVay
(1996) has speculated that an X-linked gene, such as the famous “gay
gene” Xq28 (Hamer, Hu, Magnuson, Hu, & Pattatucci, 1993; Hamer &
Copland, 1994) could predispose individuals towards androphilic sex-
ual attraction (i.e., sexual attraction towards males). The existence of
such a gene in males would predispose them towards bisexuality and
exclusive homosexuality. However, the same gene(s) in females would
enhance a woman’s already existing attraction to males. Thus, such a
Paul L. Vasey 237
gene would result in a phenotypic expression of homosexuality in male

bearers, but “hyper-heterosexuality” in female bearers. Theoretically
speaking, hyper-heterosexuality might predispose women to having
more offspring than they might otherwise have had, and the reproduc-
tive benefits they accrue might offset the reproductive costs associated
with androphilia in their male kin. The reproductive benefit of such an
X-linked gene to females would be more important in terms of the
gene’s evolutionary survival than its benefit to males, because females
have two X chromosomes and males only have one. As a consequence,
over evolutionary time, the X chromosome is acted on by natural
selection twice as often in females than in males (Hamer & Copland,
1994; LeVay, 1996; Trivers, 1974).
The Camperio-Ciani et al. (2004) study is interesting because it un-
derscores how the integration of functional and phylogenetic perspec-
tives can contribute toward a better understanding of the evolution of
same-sex sexuality. In line with the logic of the Camperio-Ciani et al.
study, male homosexuality might be conceptualized as an evolutionary
by-product of positive selection for increased female fecundity. More
research remains to be done before any definitive conclusions can be
drawn, but if this is indeed the case, then male homosexuality per se
would not be adaptive–rather, increased female fecundity would be.
Thus, within the context of this evolutionary hypothesis, female fecun-
dity in humans could be explained in functional (adaptive) terms, but
male homosexuality could not. To reiterate a previous point, by-prod-
ucts of adaptations do not evolve to solve adaptive problems and, thus,
do not have a function(s). If male homosexuality in humans is indeed a
by-product of an adaptation as the Camperio-Ciani et al. data suggest,
then evolutionists who seek to explain this trait will need to abandon at-
tempts to identify a direct adaptive function that male homosexuality in
humans might subserve and focus instead on elucidating the trait’s
phylogenetic history. Instead, it might be more productive to think in
terms of how natural selection is constrained in terms of the design of
certain adaptive traits, resulting in the evolution of concomitant by-
products.
By-products of adaptations are not the result of direct selection in the
evolutionary past. They can, however, come under direct selection pres-
sure if they are co-opted to serve an adaptive function in the present,
which augments the participants’ reproductive success. By-products of
adaptations that are co-opted in this manner are referred to as
exaptations (Gould & Vrba, 1982) or co-opted spandrels (Buss et al.,
1998). Of the two terms, co-opted spandrels may be more precise, be-
cause the word spandrel is a clear reference to a trait’s status as a

by-product. Spandrel is an architectural term that refers to the triangular
space that results when two arches meet and are framed by horizontal
cornice above them. Spandrels exist not because they are inherently
functional. Rather, they exist as incidental by-products of a particular
architectural design that is functional. Despite their status as incidental
design constraints, spandrels are routinely used as surfaces for painted
or sculpted decoration. In this way these incidental by-products are
co-opted to fulfill a decorative function (see Gould & Lewontin, 1979,
for an extended discussion of this point). At present, it is unclear
whether the same-sex sociosexual behaviors that we see in many animal
species, such as bonobos, are best characterized as adaptations (i.e.,
traits that originate due to directional selection owing to their fitness-en-
hancing effects) or as co-opted spandrels (i.e., by-products of adapta-
tions that are co-opted to serve adaptive sociosexual functions).
Likewise, more research is needed before definitive statements can be
made with regard to whether same-sex sexual behavior in humans is an
adaptation, a by-product of an adaptation, or a co-opted spandrel.
CONCLUSION
Cross-species studies suggest that different kinds of homosexualities
have evolved. Same-sex sexual behavior is not a uniform phenomenon
across species. Instead, multiple motivations, developmental pathways,
functions, and phylogenetic histories underlie same-sex sexual behav-
ior, and these vary both within and between species (Bagemihl, 1999;
Vasey, 1995). Some forms of homosexuality may serve no evolutionary
function whatsoever, while others may be non-sexual acts that are exe-
cuted to mediate adaptive social goals. As such, we should not expect
any one evolutionary explanation for same-sex sexual behavior to ac-
count for the diversity of this phenomenon. Indeed, attempts to make
unifying interspecies generalizations about the evolution of same-sex
sexual behavior may be misguided and misleading.
Attempts to explain human homosexuality as an adaptation have
been ongoing for over a quarter of a century (Wilson, 1975). This
adaptationist approach has not been particularly productive. Although it
is important to continue to test plausible adaptive hypotheses for human
homosexuality, it might also be time to diversify our theoretical ap-
proaches on the issue. As such, we need to be open to the possibility that
homosexuality in humans is not adaptive in and of itself, but rather is an
Paul L. Vasey 239
evolutionary by-product of some adaptation that remains to be identi-

fied. If so, then a complete understanding of how human homosexuality
evolved will require the implementation of both functional and
phylogenetic levels of evolutionary analysis.
ISSUES FOR FURTHER CONSIDERATION

How many forms does animal same-sex sexual behavior take and what
are the relationships among these behaviors, if any?
Why do some species exhibit same-sex sexual behavior relatively fre-
quently, while others do not? Why is exclusive same-sex sexual part-
ner preference so rare in the animal kingdom?
Do individuals invariably prefer other-sex reproductive partners to
same-sex sexual partners?
Do males and females compete with each other for sexual partners?
If homosexuality in humans is an evolutionary by-product of an adapta-
tion, to which adaptation is it linked, and what sort of design con-
straints would have necessitated such a linkage?
FURTHER READING
Alcock, J. (1989). Animal Behavior, 4th Edition. Sunderland, MA: Sinauer Associates,
Inc. (Chapter 7, The Evolution of Behavior: Historical Pathways, contains an excel-
lent discussion of phylogenetic analyses of behavior.)
Bagemihl, B. (1999). Biological exuberance: Animal homosexual and natural diver-
sity. New York: St. Martin’s Press. (An exhaustive treatment of same-sex sexual be-
havior in animals and an excellent reference source.)
Buss, D., Haselton, M. G., Shackelford, T. K., Bleske, A. L., & Wakefield, J. C.,
(1998). Adaptations, exaptations, and spandrels. American Psychologist, 53,
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doi:10.1300/J056v18n02_07

Evolution of Same Sex Behaviour

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Evolution of Same Sex Behaviour

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Function and Phylogeny:

The Evolution of Same-Sex Sexual Behavior

SUMMARY. Evolutionary explanations come in two basic forms.

Paul L. Vasey is Professor of Psychology, University of Lethbridge, Alberta, Can-

these data and, by extension, the evolution of male homosexuality in

KEYWORDS. Primates, Japanese macaques, female-female sexual be-

FUNCTIONAL AND PHYLOGENETIC PERSPECTIVES

strictly sexual in nature. I conclude by outlining recent empirical evi-

Defining Sexual Behavior

Any useful discussion of the evolution of same-sex sexuality in ani-

Criteria for Determining Same-Sex Sexual Partner Preference

Sexual partner preference refers to an individual’s predilection for

tionists do not tend to question whether sexual activity between males

individual against their will. It is unclear how common coercion of

a social function, but this does not in and of itself demonstrate an

EVOLUTIONARY THEORY AND SAME-SEX SEXUALITY

From an ultimate evolutionary perspective, sexual selection and pa-

other animals engage in many different kinds of non-conceptive sex, but

Same-Sex Sexual Behavior in Bonobos: Functional Perspectives

He argued that same-sex sexual behavior “works to calm anxiety or ex-

Same-Sex Sexuality in Japanese Macaques:

Female Japanese macaques, in certain populations, routinely en-

When considering the issue of sexual motivation, it is worth noting

Sexual Partner Preference Among Female Japanese Macaques

Having marshaled support for the conclusion that female same-sex

sive access to an infertile or post-conception female engaged in a

communicate about dominance relationships, reduce social tension as-

movement by desired males away from their immediate vicinity

IMPLICATIONS FOR THE EVOLUTION

The foregoing discussion has been intended to illustrate how evolu-

through offspring-care by same-sex oriented members (Kirkpatrick,

highest ranking families in my study group (i.e., A-B consortships ver-

gene would result in a phenotypic expression of homosexuality in male

cause the word spandrel is a clear reference to a trait’s status as a

evolutionary by-product of some adaptation that remains to be identi-

ISSUES FOR FURTHER CONSIDERATION

Alcock, A. (1989). Animal behavior (4th ed.). Sunderland, MA: Sinauer.

Muscarella, F. (2000). The evolution of homoerotic behavior in humans. Journal of

Tinbergen, N. (1963). On aims and methods of ethology. Zeitschrift fürTier-

Wolfe, L. D. (1984). Japanese macaque female sexual behavior: A comparison of

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