Steven W. Gangestad1,*and Randy Thornhill2
1Department of Psychology, and2Department of Biology, University of New Mexico, Albuquerque, NM 87131, USA
For several decades, scholars of human sexuality have almost uniformly assumed that women
evolutionarily lost oestrus—a phase of female sexuality occurring near ovulation and distinct from other
phases of the ovarian cycle in terms of female sexual motivations and attractivity. In fact, we argue, this
long-standing assumption is wrong. We review evidence that women’s fertile-phase sexuality differs in a
variety of ways from their sexuality during infertile phases of their cycles. In particular, when fertile
in their cycles, women are particularly sexually attracted to a variety of features that likely are
(or, ancestrally, were) indicators of genetic quality. As women’s fertile-phase sexuality shares with other
vertebrate females’ fertile-phase sexuality a variety of functional and physiological features, we propose
that the term oestrus appropriately applies to this phase in women. We discuss the function of women’s
non-fertile or extended sexuality and, based on empirical findings, suggest ways that fertile-phase
sexuality in women has been shaped to partly function in the context of extra-pair mating. Men are
particularly attracted to some features of fertile-phase women, but probably based on by-products of
physiological changes males have been selected to detect, not because women signal their cycle-based
Keywords: oestrus; sexual selection; menstrual cycle; women’s sexuality; extended sexuality;
Scholars have long thought that the nature of human
sexuality provides key insights into hominin evolution, not
only of human mating adaptations but also, more broadly,
the importance of biparental care in human evolution,
human foraging patterns, prominent aspects of the human
life course, the general nature of human social organiz-
ation and even reasons for hominin encephalization—
indeed, virtually every core feature of adaptive complexes
arisen in hominins (e.g. Alexander & Noonan 1979;
Symons 1979; Alexander 1990; Miller 2000).
For close to half a century, evolution-minded theories
of human sexuality have typically been built around a
foundational ‘fact’: during the course of their evolution,
women lost a distinct phase of fertile sexuality in their
reproductive cycles, typically referred to as ‘oestrus’ in
non-human mammalian species (see Etkin 1964; Jolly
1972; Alexander & Noonan 1979; Burley 1979; Spuhler
1979; Symons 1979; Alexander 1990). Behaviourally,
oestrus has been thought to entail enhanced proceptivity
and receptivity to males when females are fertile. In its
stead, women evolved to exhibit ‘continuous’ sexuality—
a sexual nature that changes, if at all, in only minor ways
across the cycle, such that women are near-equally
sexually proceptive throughout it. Typically, scholars have
thought loss of oestrus functions to conceal ovulation.
Recent evidence and theory indicates that this fact is
fiction. Women have not lost oestrus. Although women are
continuously receptive, their sexuality is not accurately
characterized as continuous. Rather, women possess ‘dual
sexuality,’ consisting of a phase of oestrus and a phase of
extended (non-fertile) sexuality in their cycles. Loss of
oestrus in humans serves no function, as it simply has not
occurred, though there is an important sense in which
women have evolved to conceal cycle fertility (or, in our
terms, their oestrus).
In this review, we focus on evidence and theory
supporting these claims. We distinguish the oestrous
phase of women’s cycles from their phase of extended
sexuality. We also briefly comment on women’s concealed
oestrus. A forthcoming book expands upon these and
related arguments (Thornhill & Gangestad in press).
2. THE PHENOMENON OF OESTRUS
A dictionary definition of oestrus is ‘the periodic state of
excitement in the female of most mammals, excluding
humans, that immediately precedes ovulation and during
which the female is most receptive to mating; heat’
(American Stedman’s Medical Dictionary, 2002). The term
derives from the Greek word for a botfly that excites cows
when they lay eggs on their hide, and was first adopted to
refer to the sexual excitement during heat by 1890
(according to the Oxford English Dictionary, in Billings’
Medical Dictionary). This dictionary definition generally
reflects scientific usage, particularly of the concept of
behavioural oestrus (indeed, medical dictionaries seek to
distil scientific usage; see Nelson 2000). (Some usages of
the term, however, also include female attractivity to males
as a component of oestrus. Particularly in this regard,
some authors do not apply the term to all non-human
primates (see §7).) This characterization of behavioural
oestrus is, in our view, flawed or incomplete in three ways.
Proc. R. Soc. B (2008) 275, 991–1000
Published online 5 February 2008
*Author for correspondence (firstname.lastname@example.org).
Received 16 October 2007
Accepted 16 January 2008
This journal is q 2008 The Royal Society
(a) Behavioural oestrus is not typically
characterized by generalized sexual
excitement or motivation
It makes little sense that females possess special adaptation
benefits to female mates. Females should hence be choosy,
not indiscriminate, when making mate choices during the
fertile phase of their reproductive cycles. Empirically,
evidence suggests that, indeed, females are typically choosy
when fertile, often favouring males who, in theory, would
make good sires through delivery of intrinsic good genes or
compatible genes (e.g. house mouse: Potts et al. 1991,
Williams & Lenington 1993; pronghorn antelope: Byers
pygmy loris: Fisher et al. 2003; snow vole: Ludue-Larena
et al. 2003; guinea-pig: Hohoff et al. 2003; rhesus macaque:
Charlton et al. 2007). Recent evidence on a close relative of
humans, the common chimpanzee, illustrates this point.
Females are more sexually receptive and initiate sex with
more malesoutsideofthe period ofpeakfertilitythanduring
their most fertile period (Stumpf & Boesch 2005). Sex
during the period of infertile sex appears to function to
reduce male aggression towards offspring by confusing
paternity, which females do by having sex with most, any
resident male. At peak fertility, by contrast, females are
choosier—they both initiate less sex with other males and
are receptive to fewer males’ advances—and their prefer-
ences tend to converge on the same males, ones who may
offer the best genes for offspring.
Exceptions, in which females possess oestrous adap-
tations to assure conception per se, should be limited to
unusual circumstances in which females’ encounter rate
with males is severely limited or they are faced with strong
constraints on time to find sperm. For instance, gravid
accept sperm from lower quality males (but still prefer
whopossessadaptationtoseek out andfind fertile females.
in natural circumstances (see Thornhill & Gangestad
(in press) for a fuller discussion; see also Pagel 1994).
(b) A scientifically proper application does not
restrict oestrus to mammals
We argue that it makes little theoretical sense to restrict the
concept of oestrus to mammals. All vertebrates possess
receptors for oestrogen (itself named for being the ‘gen’
arily debuted in an ancestor common to all vertebrates
tion in the ancestor to jawed vertebrates (gnathosomes) ca
400 Myr ago (Thornton 2001). Moreover, oestrogen’s
effects on female sexuality may be homologous across
(Nonetheless, other reproductive hormones, such as
progesterone and testosterone (phylogenetically almost as
old as oestrogen; Thornton et al. 2003), also play important
roles in modulating female sexuality in these species. Also,
the precise roles played by different hormones may vary
across species.) For instance, females of many bird species
exhibit mating preferences during their fertile period
different from their preferences that characterize the period
preceding peak fertility, and this fertile phase possesses
homologies with mammalian fertile phases. Application of
the term oestrus to all vertebrate females who possess a
distinct fertile sexuality recognizes the homologies that they
use of this term (see Thornhill & Gangestad in press).
(c) Women possess oestrus
As we review, women possess a distinct fertile sexuality
that is, in fact, functionally homologous with as well as
functionally similar to oestrus observed in other vertebrate
species (see also Tarı ´n & Go ´mez-Piquer 2002).
3. CHANGES IN WOMEN’S SEXUAL PREFERENCES
ACROSS THE REPRODUCTIVE CYCLE
Similar to other mammal species, human females are
fertile during a brief window of their cycles, from several
days prior to the day of ovulation up until the day of
ovulation itself (e.g. Wilcox et al. 1995). If, in fact, women
possess a fertile-phase sexuality that is distinct from their
sexuality outside the fertile phase, female preferences
(e.g. features they find most sexually attractive) should
change across the cycle. If fertile-phase sexuality was
shaped by the benefits of obtaining sires who offer genetic
benefits to offspring, women should particularly prefer
male features indicative of genetic benefits to offspring
when fertile. Finally, cycle shifts should be particular to
women’s evaluations of men’s sexual attraction (e.g. their
‘sexiness’) rather than dimensions related to long-term
mateship compatibility (Penton-Voak et al. 1999).
(a) Preferences do shift
Over 20 studies, most in the past decade, show that female
preferences clearly do shift. We summarize findings on
purported fitness indicators in table 1. At mid-cycle,
normally ovulating, non-pill using women particularly
prefer a number of masculine male traits perceived through
a variety of sensory modalities: the scent of social
dominance; facial masculinity; bodily masculinity; mascu-
linevocal qualities;masculine behaviouraldisplays;and tall
height. They also prefer traits associated with body
body symmetry. Many of these effects appear to be robust,
even if some effects are of modest size and questions about
mediators remain. (For instance, what is the chemical(s)
responsible for women’s preference for the scents of
symmetry and social dominance mid-cycle? Women are
more attracted to certain androgen-related scents when
mid-cycle, but the one published study examining prefer-
ences for the scent associated with high testosterone levels
found no effect.) Masculine traits and traits associated with
symmetry may have been indicators of intrinsic good genes
ancestrally. (Intrinsic good genes have additive effects on
fitness and hence could benefit the offspring of any female;
see Jennions & Petrie 2000, Kokko et al. 2003.)
Evidence on whether symmetrical faces themselves
are more attractive to women when they are mid-cycle
is mixed. Possibly, facial symmetry itself is not a
cue that individuals use to assess intrinsic good genes
(Gangestad & Thornhill 2003). But Little et al. (2007b),
992S. W.Gangestad & R. Thornhill
Review. Human oestrus
Proc. R. Soc. B (2008)
who did find a preference shift in two studies, discussed
reasons why effects may not have been found in other
research. Evidence is mixed too with respect to purported
fitness indicators such as creative talent and intelligent
appearance, and the one study examining a feature of
compatible genes (major histocompatibility complex
(MHC) dissimilarity) found no effect (but see Garver-
Apgar et al. 2006). (See also DeBruine et al. (2005) who
found that, during the luteal phase, women are particularly
attracted to self-resembling faces of both men and women
and also discuss additional selection pressures that shaped
changes in preferences as a function of fertility and
the cycle in preferences for these measures is needed.
(b) Preference shifts are not general
Women do not find all positive traits sexier mid-cycle.
Traits particularly valued in long-term mates (e.g. promise
of material benefits) appear to be preferred as strongly by
infertile women as by fertile women (e.g. Thornhill et al.
2003). In one study (Gangestad et al. 2007), women rated
the attractiveness of men shown on videotapes. Indepen-
dent samples of women rated men on a variety of qualities
desirable in mates. Whereas fertile-phase women were
particularly sexually attracted to men perceived as
arrogant, intrasexually confrontative, muscular and phy-
sically attractive, no cycle shifts were observed in women’s
attraction to men seen to be successful financially,
intelligent or kind and warm. Men who appeared to be
sexually faithful were less sexually attractive to fertile-
phase women; put otherwise, fertile women are particu-
larly attracted to men who appear that they would not be
faithful (probably because they possess features women
find attractive in sex partners).
Women are also particularly attracted to healthy
looking faces during the infertile luteal phase and, more
Table 1. Demonstrated variation in female preferences for purported indicators of good genes across the cycle. (‘C’ indicates
that a significant effect (an overall preference or preference for a short-term mate at 0.05 level of statistical significance using a
directed test) was detected. ‘K’ indicates that no such effect was detected. (In no case was a significant effect in the unpredicted
direction detected. Hence, minuses connote null effects.) The interaction effect refers to finding a greater shift for ratings of
attractiveness in a short-term relationship (men’s sexiness) than long-term relationship. ‘0’ means that the effect was not
examined in the study. A few studies also examined differences in preferences as a function of whether women were in long-term
committed relationships or single. This table does not report these effects.)
trait study positive finding? interaction w relat. context
scent of social dominance
scent of androstenone
Havlicek et al. (2005)
Hummel et al. (1991)
Rantala et al. (2006)
Penton-Voak et al. (1999) study 1
Penton-Voak et al. (1999) study 2
Penton-Voak & Perrett (2000)
Johnston et al. (2001)
Scarbrough & Johnston (2005)
Jones et al. (2005a)
Roney & Simmons 2008
scent of testosterone
facial features associated with
masculine bodyLittle et al. (2007a)
Gangestad et al. (2007)
Feinberg et al. (2006)
Gangestad et al. (2004)
(see also Gangestad et al. 2007)
Pawlowski & Jasienska (2005)
dark (masculine) skin
correlates of symmetry
scent of symmetry Gangestad & Thornhill (1998)
Thornhill & Gangestad (1999)
Rikowski & Grammer (1999)
Thornhill et al. (2003)
Thornhill & Gangestad (2003)
0facial features associated with
facial symmetry Koehler et al. (2002)
Koehler et al. (2006)
Cardenas & Harris (2007)
Little et al. (2007b), study 1
Little et al. (2007b), study 2
purported mental fitness indicators
creative talent (versus wealth)
Haselton & Miller (2006)
Gangestad et al. (2007)
scent of MHC dissimilarity Thornhill et al. (2003)
Review. Human oestrus
S. W.Gangestad & R. Thornhill 993
Proc. R. Soc. B (2008)
generally, when women experience relatively high pro-
gesterone levels (Jones et al. 2005a,b). Possibly, this
preference shift is a by-product of selection favouring
avoidance of unhealthy persons during pregnancy.
(c) Preference shifts are particular to evaluations
of men’s sexiness
No study to date has detected fertile-phase shifts in
women’s evaluations of men as good long-term partners.
Rather, shifts in preferences are particular to women’s
ratings of men’s sex appeal (or, as it is sometimes phrased,
men’s attractiveness as a ‘short-term partner’; table 1).
Considered together, the findings are consistent with
the proposal that women’s oestrous preferences function
to enhance the genetic quality of offspring through sire
choice. Naturally, we cannot be certain that masculine
qualities and features associated with developmental
stability were associated with genetic quality ancestrally,
but we know of no adequate alternative explanation of
these preferences. The view that the preferences function
to acquire genes for offspring constitutes a defensible
‘inference to the best explanation’ (e.g. Sterelny &
(d) Women’s fertile-phase sexuality is appropriately
referred to as oestrus
Female vertebrate oestrus typically entails adaptations
that possess this same function (reviewed by Thornhil &
Gangestad in press). Moreover, components of the
physiological machinery (hormonal and neural) posses-
sing this function are broadly shared by vertebrates.
Aspects of women’s oestrus, then, are homologous with
oestrus in other vertebrates. From a broad comparative
and phylogenetic perspective, then, women’s fertile-phase
sexuality constitutes oestrus.
4. WOMEN’S EXTENDED SEXUALITY
(a) The function of extended sexuality
In addition to possessing oestrus, some vertebrate species
are also sexually receptive or proceptive outside of their
fertile phase (e.g. Rodriguez-Girones & Enquist 2001);
they possess ‘extended sexuality,’ motivation or interest in
sex that is not directly conceptive (though, in theory, it
typically evolved owing to its reproductive benefits, i.e. it
reflects adaptation, not by-product). The explanation of
extended sexuality most conceptually coherent while also
receiving empirical support argues that it reflects adap-
tation to obtain material benefits, typically male delivered
(e.g. Rodriguez-Girones & Enquist 2001; Wakano & Ihara
2005; see also Stacy 1982).
This functionisillustratedbymany Old World primates.
Hrdy (1981) proposed that females may protect offspring
from infanticide (or more mild forms of harm) imposed by
female has sex with all adult males in a troop during a
reproductive cycle, not allowing any one to exclude
possibility of paternity, it may benefit no male to harm her
offspring. A female can simultaneously maintain control
if most promiscuous outside of the fertile phase (i.e. during
extended sexuality) while maintaining choosiness at peak
fertility. (This assumes that males themselves cannot
perfectly discriminate a female’s fertile phase from her
infertile phases.) As noted earlier, Stumpf & Boesch (2005)
observed precisely this pattern in common chimpanzees.
The purported function of extended sexuality in these
species is, ultimately, to obtain material benefits from
males. In the logic of evolutionary economics, actions that
reduce male-imposed harm yield male-delivered benefits.
(b) Women exhibit extreme extended sexuality
Few, if any females, match the degree to which women’s
sexuality is extended into infertile phases of the reproduc-
tive cycle. A recent study of over 20 000 women of
reproductive age in 13 developing countries detected no
systematic changes in frequency of sexual intercourse with
regular partners across the cycle, aside from a drop during
menses (Brewis & Meyer 2005; cf. Wilcox et al. 2004).
These women had sex with partners as frequently during
the luteal phase as during their fertile phases. Women are
sexually receptive and proceptive during other non-fertile
periods of life as well: across anovulatory cycles; during
adolescence; when pregnant; and when lactating.
Women’s extended sexuality too appears to function to
obtain male-delivered benefits. Unlike close primate
relatives, however, extended sexuality in human females
appears to function to enhance the flow of material
benefits delivered by primary partners within pair bonds.
Whether men’s subsidization of women’s and offspring
diet serves a function of parental effort or mating effort has
been widely debated (e.g. Kaplan et al. 2000; Hawkes
2004). Although an argument is beyond the scope of this
review, recent evidence points to a role for parental effort
(e.g. Marlowe 2003). Extended sexuality may enhance the
flow of material benefits from partners in two different
ways. First, receptivity during extended sexuality may
enhance a partner’s assessment of paternity (assuming,
again, that male ascertainment of female fertility status is
imperfect). Second, males may deliver benefits as a
function of sexual access (Symons 1979; Hill 1982; Buss
2003). Females in manybiparentally investing bird species
appear to have a fertile sexuality as well as extended
sexuality (e.g. Birkhead & Møller 1992). As in humans,
these two periods are partially characterized by adap-
tations that have different functions. Indeed, the effects
summarized in table 1 constitute evidence that sexuality
during the two phases have been shaped, in part, by
different costs and benefits (see also below and Thornhill &
Gangestad in press). The phases are not discrete; rather,
changes in women’s preferences are graded shifts probably
5. THE ROLE OF EXTRA-PAIR COPULATION
(a) Oestrus in species with biparental care
As distant vertebrate ancestors of women possessed
oestrus (see above), women’s oestrus did not evolve in
the context of biparental care. Nonetheless, components
of women’s oestrus may have been altered by selection
subsequent to the evolution of biparental investment in
hominins. In biparentally investing species, reproductive
benefits achieved through oestrus can be, in principle,
partly garnered through extra-pair copulations (EPCs).
Reproducing females possess primary investing partners,
which vary in the extent towhich they possess indicators of
genetic fitness. When females paired with mates not
possessing these indicators are sexually attracted to and
994 S. W.Gangestad & R. Thornhill
Review. Human oestrus
Proc. R. Soc. B (2008)
mate with other males during oestrus, they may receive
genetic benefits to offspring through EPC. In these
species, then, several additional predictions about oestrus
follow. First, females on average should be more attracted
to males other than primary partners during oestrus than
infertile phases. Second, shifts in attraction to extra-pair
males should be moderated by the qualities of the male
primary partner: females with partners lacking indicators
of genetic fitness should be most attracted to extra-pair
males during oestrus. Females whose primary partners
possess these indicators should evidence little or no shift.
In some biparental species of birds, these predictions
have been confirmed: western bluebirds (Dickinson
1997, 2001); hooded warblers (Neudorf et al. 1997);
wheatears (Currie et al. 1999); collared flycatchers
(Sheldon et al. 1999, Michl et al. 2002); superb fairy
wrens (Double & Cockburn 2000); raptors (Mougeot
2004); and common yellowthroats (Pedersen et al.
2006). Akc ¸ay & Roughgarden (2007) recently meta-
analysed 121 studies testing claims that female birds EPC
to obtain genetic benefits. Over 40% of the studies
yielded support, whether assessing benefits of intrinsic
good or compatible genes. As some null results occur
even when true effects exist, these results are consistent
with the possibility that female EPC in birds often, even if
not always, functions to obtain genetic benefits.
(b) Women’s extra-pair sexual interests during
In women, too, these predictions receive support. Two
studies that had women report sexual attraction in the past
2 days twice in a month—once when fertile and once
during the luteal phase—revealed substantial increases
in women’s attraction to extra-pair men during oestrus,
but detected no change in women’s attraction to their
primary partners (Gangestad et al. 2002, 2005). (Using a
different design, Pillsworth et al. (2004) did not replicate
this pattern. Bellis & Baker (1990), however, found that
women’s rates of EPC increased mid-cycle, whereas
in-pair copulation rates did not. Perhaps relatedly,
Jones et al. (2005a) found that women reported
themselves to be less committed to their partners when
fertile in their cycles, when compared with during the
Several studies have documented moderators of these
effects. (i) Gangestad et al. (2005) found that male primary
partners’ fluctuating asymmetry (FA) moderated the effect:
compared with women paired with relatively symmetrical
men. By contrast, women paired with symmetrical men
experienced greater shifts towards attraction to their own
partners than women paired with asymmetrical men. (ii)
Two studies found that women mated with sexually
unattractive men (as rated by these women themselves)
experienced greater increases in attraction to extra-pair
men, compared with women mated with sexually attractive
men (Haselton & Gangestad 2006; Pillsworth & Haselton
2006). (iii) Although most studies have focused on
purported indicators of intrinsic good genes, one study
examined the effects of the purported compatibility of male
genes with female genes to produce fit offspring. MHC
alleles code for cell surface markers used by the immune
system to detect foreign pathogens. Purportedly, offspring
benefit from being heterozygotic and hence obtaining two
who do not share alleles at MHC loci hence possess
compatible genes. Garver-Apgar et al. (2006) found that
MHC sharing (proportion of alleles at three loci also
possessed by the primary partner) predicted cycle shifts in
women’s attraction to extra-pair men. Women paired with
men with whom they shared relatively many alleles were
more attracted to extra-pair men when fertile. By contrast,
women paired with men with whom they shared no alleles
showed notendencytobecome moreattracted toextra-pair
men when fertile. Moreover, men’s FA and MHC sharing
have independent effects on cycle shifts in women’s
6. MEN’S COUNTER-ADAPTATIONS
(a) Sexually antagonistic coevolution
As women’s attraction to men other than primary partners
during oestrus conflicts with the reproductive interests of
primary partners, sexually antagonistic coevolution of
male adaptations in response tofemale adaptations maybe
expected. In many bird species, primary partners engage
in paternity assurance tactics, such as mate guarding and
frequent copulation. For some species, investigators have
documented increases in the intensity of these tactics
when female partners are fertile (e.g. house martins: Riley
et al. 1995; kestrels: Korpimaki et al. 1996; Montagu’s
harrier: Arroyo 1999; bearded vultures: Bertran &
Margalida 1999; Seychelles warblers: Komdeur et al.
1999; European barn swallows: Saino et al. 1999;
Australian magpie-larks: Hall & Magrath 2000; northern
mockingbirds: Bodily & Neudorf 2004; New Zealand
stitchbirds: Low 2005).
Similar effects have been documented in humans.
of proprietary or related behaviours (e.g. vigilance of
partners’ whereabouts) when they are fertile (Gangestad
et al. 2002; Haselton & Gangestad 2006), and reports from
male partners yield similar effects (Garver-Apgar et al.
in preparation). Moreover, men whose proprietary
behaviours increase most dramatically during partners’
attraction increases most emphatically during oestrus
(Gangestad et al. 2002; Haselton & Gangestad 2006;
Garver-Apgar et al. in preparation; see also Pillsworth &
women’s attention to extra-pair men during oestrus drives
men’s increased attention to partners during oestrus. Other
work indicates that men’s perceptions of other men may
change across the cycle as a function of their partners’
fertility. Burriss & Little (2006) found that men tend to
perceive dominant men as even more dominant when their
partners are mid-cycle, an effect that may reflect adaptation
to enhance awareness of threats from potential competitors
when partners are fertile.
(b) Extra-pair paternity rates
In human populations, extra-pair paternity (EPP) rates
are typically low (less than 5%) but variable (in places,
more than 10%; Anderson 2006; see also Simmons et al.
2004). These rates do not imply a lack of sexually
antagonistic coevolution surrounding females’ EPC.
When males invest heavily in offspring, strong selection
Review. Human oestrus
S. W.Gangestad & R. Thornhill995
Proc. R. Soc. B (2008)
may lead to the evolution of costly counter-adaptations
relatively effective at maintaining low EPP rates. By
contrast, when the costs of EPP to male partners are
relatively low, male counter-adaptations that evolve may
be both less costly and less effective, leading to higher
rates of EPP (see also Møller 2000). Because sexually
antagonistic adaptations pertaining to female EPC can
occur despite persistently low rates of female EPC, the
question of whether these adaptations exist in any species
is distinct from the question of whether sperm competition
has been an important selective force in that species (cf.
Simmons et al. 2004).
This point is illustrated by many raptor species, in
which paternal investment importantly affects offspring
success. Males hunt across wide ranges, taking them far
from nests when foraging. EPP rates are typically low (less
than 5%, and often less than 2%), but by no means imply a
lack of sexually antagonistic selection. Males engage in
costly anti-cuckoldry tactics, returning to the nest to
copulate with female partners up to a dozen times a day,
on average (see Mougeot 2004). In Montagu harriers,
these rates have been observed to increase when females
are fertile (Arroyo 1999; see also Mougeot 2004).
In some species, loss of paternal investment due to male
detection of non-paternity (in conjunction with low
genetic diversity, e.g. Møller 2003) may be sufficient to
keep EPP rates low, despite a lack of costly male paternity
assurance behaviours (e.g. some island birds such as
purple sandpipers: Pierce & Lifjeld 1998; great spotted
and middle spotted woodpeckers: Michalek & Winkler
2001; Capricorn silvereye: Robertson et al. 2001;
Monteiro’s hornbill: Stanback et al. 2002). In such
species, females may evolve to lose a distinctive period of
oestrus. As documented in our review, humans do not
appear to be one of these species.
7. CUES TO OESTRUS
Men apparently detect cues of women’s oestrus, whether
physiological or behavioural. Women’s scent appears to be
more attractive to men during their fertile phase than the
luteal phase (Doty et al. 1975; Poran 1994; Singh &
Bronstad 2001; Thornhill et al. 2003; Kuukasja ¨rvi et al.
2004; Havlicek et al. 2006; for a negative finding, see
Thornhill & Gangestad 1999). Their faces may become
more attractive when they are fertile (Roberts et al. 2004).
or provocatively (Grammer et al. 2004). In one study, the
tips received by women working as lap dancers increased
nearly $100 per shift when they were fertile, compared with
the luteal phase (Miller et al. 2007).
A signal is a perceptible cue that has evolved owing to
benefits achieved through communication to other
individuals (conspecifics or members of other species). If
the cues men use to detect women’s oestrus are signals,
then women benefit(ed) from men’s (or others’) detection
of them, leading to their evolution. It is highly unlikely that
ancestral women benefited from men’s detection of
oestrous cues. First, in general, females should not pay
large costs to signal fertility status, except in rare cases
(e.g. Pagel 1994). Selection strongly operates on males to
detect fertile phases, which they typically achieve by
detecting by-products of the physiological changes in
females associated with fertility (e.g. by-products of
changing levels of oestrogen; Nelson 2000), for which
females pay no costs of signalling. Second, in humans in
particular, it makes little sense that females would benefit
through male detection of fertility status, in the light of
mounting evidence for sexually antagonistic coevolution
of adaptations leading to conflicts during oestrus. (We
note, in this context, that a variety of psychological
features associated with oestrus may also be by-products
of adaptations rather than directly selected; see Jones
et al. 2005a.)
In fact, women have probably evolved to conceal their
oestrus. Concealment need not imply a complete lack of
fertility cues. Females’ bodies change during oestrus, and
the by-products of these changes ‘leak’ information about
their fertility status. Concealment instead implies a
reduction in the intensity of these cues selected owing to
the valueof suppressing information about fertility status to
conspecifics (notably, male partners). Concealment is
unlikely to be perfect, as a coevolutionary race between
females and males leads men to be increasingly sensitive to
itself (e.g. fertility depends on changes in oestrogen; see
Ellison 2001). Males of virtually any non-human primate
species can probably detect the fertility status of females
through use of scent cues (e.g. Dixson 1998) much better
than men can detect the women’s fertility status. (Hence,
female primates that lack sexual swellings do not typically
possess ‘concealed ovulation’; cf. Sille ´n-Tullberg & Møller
1993; see Thornhill & Gangestad in press.) That men can
do so at all, we suggest, persists due to positive selection on
men for detection, and despite selection on females to
conceal reliable cues of oestrus.
Until recently, women have been thought to possess no
distinctive sexuality during the fertile phase of their
menstrual cycle. Abundant evidence now indicates that
they do. This sexuality is appropriately referred to as
oestrus. The function of oestrous sexual proceptivity is not
to obtain sperm from any male. Rather, oestrous females
should be discriminating and prefer to mate with good
sires for offspring. Women’s sexual preferences for certain
male traits probably connoting male genetic quality (or
ones that did so ancestrally) appear to be enhanced when
women are fertile in their cycles. Women’s oestrus shares
functional and physiological homologies with the oestrus
of not only other mammals but also female vertebrates in
general. Oestrus, we propose, debuted ca 400 Myr ago.
That women’s preferences change across their cycles
is the claim that, similar to some bird species in which both
sexes exert substantial efforts to enhance offspring quality,
obtaining reproductive benefits in the context of EPC. On
average, women experience greater sexual attraction to
particular extra-pair men, but not their own partners,
primary partners lack purported indicators of intrinsic or
compatible good genes. Some of the best evidence that
sexually antagonistic coevolution pertaining to women’s
EPC has led to fertility-dependent adaptations are
provided by the examination of male counter-adaptations
996 S. W.Gangestad & R. Thornhill
Review. Human oestrus
Proc. R. Soc. B (2008)
to enhance paternity as primary partners. Men engage in
mate-retention tactics more frequently during oestrus, and
particularly when their partners experience increased
attraction to men other than their primary partners during
oestrus. Women may engage in actual EPC very infre-
quently, despite oestrous changes in their sexuality,
precisely because men have evolved counter-adaptations
The fact that women possess oestrus raises important
unanswered questions. Although many changes across the
cycle in women and their partners have been documented,
many more may await uncovering. The precise endocrine
mechanisms that regulate these changes remain largely
unknown. Research to date implicates oestrogen, pro-
gesterone and testosterone (e.g. Puts 2006; Welling et al.
2007; Garver-Apgar et al. in press; Roney & Simmons
2008). Lancaster & Kaplan (in press) raised the possibility
that prolactin and oxytocin, whose levels are heightened
when women lactate, suppress or alter oestrous sexuality
in women, thereby reducing its effects (e.g. on extra-pair
sexual interest) in women with young offspring (on one
possible effect of prolactin, see Puts 2006; cf. Garver-
Apgar et al. in press). As research to date has largely
examined oestrous effects in nulliparous young women,
studies investigating the nature of oestrus in other
populations are especially needed.
Most fundamentally, the discovery of women’s oestrus
has penetrating and potentially revolutionary implications
for a proper conceptualization of human mating. New
theoretical frameworks that recognize this discovery are
needed; we have sketched the outlines of some conjectures
here (see also Thornhill & Gangestad in press). The field
can look forward to new, exciting avenues of research on
human mating that will surely follow.
Akc ¸ay, E. & Roughgarden, J. 2007 Extra-pair paternity in
birds: review of the genetic benefits. Evol. Ecol. Res. 9,
Alexander, R. D. 1990 How did humans evolve? Reflections
on the uniquely unique species. Ann Arbor, MI: Museum
of Zoology, The University of Michigan. Special publi-
cation no. 1.
Alexander, R. D. & Noonan, K. M. 1979 Concealment of
ovulation, parental care, and human social evolution. In
Evolutionary biology and human social behavior: an anthro-
pological perspective (eds N. A. Chagnon & W. G. Irons),
pp. 436–453. Scituate, MA: North Duxbury Press.
Anderson, K. G. 2006 How well does paternity confidence
match actual paternity? Evidence from worldwide non-
paternity rates. Curr. Anthropol. 47, 513–520. (doi:10.
Arroyo, B. E. 1999 Copulatory behavior of semi-colonial
Montagu’s Harriers. Condor 101, 340–346. (doi:10.2307/
Bellis, M. A. & Baker, R. R. 1990 Do females promote sperm
competition? Anim. Behav. 40, 997–999. (doi:10.1016/
Bertran, J. & Margalida, A. 1999 Copulatory behavior of the
bearded vulture. Condor 101, 164–168. (doi:10.2307/
Birkhead, T. R. & Møller, A. P. 1992 Sperm competition in
birds: evolutionary causes and consequences. New York, NY:
Bodily, R. Y. & Neudorf, D. L. H. 2004 Mate guarding in
northern mockingbirds (Mimus polyglottos). Texas J. Sci.
Brewis, A. & Meyer, M. 2005 Demographic evidence that
human ovulation is undetectable (at least in pair bonds).
Curr. Anthropol. 46, 465–471. (doi:10.1086/430016)
Burley, N. 1979 The evolution of concealed ovulation. Am.
Nat. 114, 835–858. (doi:10.1086/283532)
Burriss, R. P. & Little, A. C. 2006 Effects of partner
conception risk phase on male perception of dominance
in faces. Evol. Hum. Behav. 27, 297–305. (doi:10.1016/
Buss, D. M. 2003 The evolution of desire: strategies of human
mating. New York, NY: Basic Books.
Byers, J. A., Moodie, J. D. & Hall, N. 1994 Pronghorn
females choose vigorous mates. Anim. Behav. 47, 33–43.
Cardenas, R. A. & Harris, L. J. 2007 Do women’s preferences
for symmetry change across the cycle? Evol. Hum. Behav.
28, 96–105. (doi:10.1016/j.evolhumbehav.2006.08.003)
Charlton, B. D., Reby, D. & McComb, K. 2007 Female red
deer prefer the roars of larger males.Biol. Lett. 3, 382–385.
Currie, D., Krupa, A. P., Burke, T. & Thompson, D. B. A.
1999 The effect of experimental male removals on extra-
pair paternity in the wheatear, Oenanthe oenanthe. Anim.
Behav. 57, 145–152. (doi:10.1006/anbe.1998.0960)
DeBruine, L. M., Jones, B. C. & Perrett, D. I. 2005 Women’s
attractiveness judgments of self-resembling faces change
across the menstrual cycle. Horm. Behav. 47, 379–383.
Dickinson, J. L. 1997 Male detention affects extra-pair
copulation frequency and pair behaviour in western
bluebirds. Anim. Behav. 53, 561–571. (doi:10.1006/
Dickinson, J. L. 2001 Extrapair copulations in western
bluebirds (Sialia mexicana): female receptivity favors
older males. Behav. Ecol. Sociobiol. 50, 423–429. (doi:10.
Dixson, A. F. 1998 Primate sexuality: comparative studies of the
prosimians, monkeys, apes, and humans. Oxford, UK:
Oxford University Press.
Doty, R. L., Ford, M., Preti, G. & Huggins, G. R. 1975
Changes in the intensity and pleasantness of human
vaginal odors during the menstrual cycle. Science 190,
Double, M.& Cockburn,A. 2000Pre-dawn infidelity: females
control extra-pair mating in superb fairy-wrens. Proc. R.
Soc. B 267, 465–470. (doi:10.1098/rspb.2000.1023)
Ellison, P. T. 2001 On fertile ground: a natural history of
reproduction. Cambridge, MA: Harvard University Press.
Etkin, W. 1964 Types of social organization in birds and
mammals. In Social behavior and organization among
vertebrates (ed. W. Etkin), pp. 256–298. Chicago, IL:
University of Chicago Press.
Feinberg, D. R., Jones,B. C., LawSmith, M. J., Moore, F. R.,
DeBruine, L. M., Cornwell, R. E., Hillier, S. G. & Perrett,
D. I. 2006 Effects of menstrual cycle and trait estrogen
level on masculinity preferences in the human voice.
Horm. Behav. 46, 215–222. (doi:10.1016/j.yhbeh.2005.
Fisher, H. S., Swaisgood, R. R. & Fitch-Snyder, H. 2003
Countermarking by male pygmy lorises (Nycticebus
pygmaeus): do females use odor cues to select mates with
high competitive ability? Behav. Ecol. Sociobiol. 53,
Frost, P. 1994 Preference for darker faces in photographs at
different phases of the menstrual cycle: preliminary
assessment of evidence for a hormonal relationship.
Percept. Mot. Skills 79, 507–514.
Review. Human oestrus
S. W.Gangestad & R. Thornhill 997
Proc. R. Soc. B (2008)
Gangestad, S. W. & Thornhill, R. 1998 Menstrual cycle
variation in women’s preferences for the scent of
symmetrical men. Proc. R. Soc. B 265, 927–933. (doi:10.
Gangestad, S. W. & Thornhill, R. 2003 Fluctuating
asymmetry, developmental instability, and fitness: toward
model-based interpretation. In Developmental instability:
causes and consequences (ed. M. Polak), pp. 62–80.
Cambridge, UK: Cambridge University Press.
Gangestad, S. W., Thornhill, R. & Garver, C. E. 2002
Changes in women’s sexual interests and their partners’
mate-retention tactics across themenstrual cycle: evidence
for shifting conflicts of interest. Proc. R. Soc. B 269,
Gangestad, S. W., Simpson, J. A., Cousins, A. J., Garver-
Apgar, C. E. & Christensen, P. N. 2004 Women’s
preferences for male behavioral displays shift across the
menstrual cycle. Psychol. Sci. 15, 203–207. (doi:10.1111/
Gangestad, S. W., Thornhill, R. & Garver-Apgar, C. E. 2005
Women’s sexual interests across the ovulatory cycle
depend on primary partner developmental instability.
Proc. R. Soc. B 272, 2023–2027. (doi:10.1098/rspb.
Gangestad, S. W., Garver-Apgar, C. E., Simpson, J. A. &
Cousins, A. J. 2007 Changes in women’s mate preferences
across the ovulatory cycle. J. Pers. Soc. Psychol. 92,
Garver-Apgar, C. E., Gangestad, S. W., Thornhill, R., Miller,
R. D. & Olp, J. J. 2006 MHC alleles, sexually responsivity,
and unfaithfulness in romantic couples. Psychol. Sci. 17,
Garver-Apgar, C. E., Cousins, A. J., Thornhill, R. &
Gangestad, S. W. In preparation. Intersexual conflict
across women’s ovulatory cycle.
Garver-Apgar, C. E., Gangestad, S. W. & Thornhill, R. In
press. Hormonal correlates of women’s mid-cycle pre-
ference for the scent of symmetry. Evol. Hum. Behav.
Grammer, K. 1993 5-a-androst-16-en-3a-on: a male phero-
mone? A brief report. Ethol. Sociobiol. 14, 201–207.
Grammer, K., Renninger, L. & Fischer, B. 2004 Disco
clothing, female sexual motivation, and relationship
status: is she dressed to impress? J. Sex Res. 41, 66–74.
Hall, M. L. & Magrath, R. D. 2000 Duetting and mate-
guarding in Australian magpie-larks (Grallina cyanoleuca).
Behav. Ecol. Sociobiol.
Haselton, M. G. & Gangestad, S. W. 2006 Conditional
expression of women’s desires and male mate retention
efforts across the ovulatory cycle. Horm. Behav. 49,
Haselton, M. & Miller, G. F. 2006 Women’s fertility across
the cycle increases the short-term attractiveness of creative
intelligence compared to wealth. Hum. Nat. 17, 50–73.
Haselton, M. G., Mortezaie, M., Pillsworth, E. G., Bleske-
Recheck, A. M. & Frederick, D. A. 2007 Ovulation and
human female ornamentation: near ovulation, women
dress to impress. Horm. Behav. 51, 40–45. (doi:10.1016/
Havlicek, J., Roberts, S. C. & Flegr, J. 2005 Women’s
preference for dominant male odour: effects of menstrual
cycle and relationship status. Biol. Lett. 1, 256–259.
Havlicek, J., Dvorakova, R., Bartos, L. & Flegr, J. 2006 Non-
advertized does not mean concealed: body odour change
across the human menstrual cycle. Ethology 112, 81–90.
Hawkes, K. 2004 Mating, parenting, and the evolution of
human pairbonds. In Kinship and behavior in primates (eds
B. Chapais & C. M. Berman), pp. 443–473. Oxford, UK:
Oxford University Press.
Hill, K. 1982 Hunting and human evolution. J. Hum. Evol.
11, 521–544. (doi:10.1016/S0047-2484(82)80107-3)
Hohoff, C., Franzin, K. & Sachser, N. 2003 Female choice in
a promiscuous wild guinea pig, the yellow-toothed cavy
(Galea musteloides). Behav. Ecol. Sociobiol. 53, 341–349.
Hrdy, S. B. 1981 The woman that never evolved. Cambridge,
MA: Harvard University Press.
Hummel, T., Gollisch, R., Wildt, G. & Kobal, G. 1991
Experientia 47, 712–715. (doi:10.1007/BF01958823)
Jennions, M. D. & Petrie, M. 2000 Why do females mate
multiply? A review of the genetic benefits. Biol. Rev. 75,
Johnston, V. S., Hagel, R., Franklin, M., Fink, B. &
Grammer, K. 2001 Male facial attractiveness: evidence
for hormone-mediated adaptivedesign. Evol. Hum. Behav.
22, 251–267. (doi:10.1016/S1090-5138(01)00066-6)
Jolly, A. 1972 The evolution of primate behavior. New York,
Jones, B. C., Little, A. C., Boothroyd, L., DeBruine, L. M.,
Feinberg, D. R., Law Smith, M. J., Cornwell, R. E.,
Moore, F. R. & Perrett, D. I. 2005a Commitment to
relationships and preferences for femininity and apparent
health in faces are strongest on days of the menstrual cycle
when progesterone level is high. Horm. Behav. 48,
Jones, B. C. et al. 2005b Menstrual cycle, pregnancy and oral
contraceptive use alter attraction to apparent health in
faces. Proc. R. Soc. B 272, 347–354. (doi:10.1098/rspb.
Kaplan, H., Hill, K., Lancaster, J. & Hurtado, A. M. 2000 A
theory of human life history evolution: diet, intelligence,
and longevity. Evol. Anthropol. 9, 156–185. (doi:10.1002/
Koehler, N., Rhodes, G. & Simmons, L. W. 2002 Are human
female preferences for symmetrical male faces enhanced
when conception is likely? Anim. Behav. 64, 233–238.
Koehler, N., Rhodes, G., Simmons, L. W. & Zebrowitz, L. A.
2006 Do cyclic changes in women’s face preferences target
cues to long-term health. Soc. Cogn. 24, 641–656. (doi:10.
Kokko, H., Brooks, R., Jennions, M. D. & Morley, J. 2003
The evolution of mate choice and mating biases. Proc. R.
Soc. B 270, 653–664. (doi:10.1098/rspb.2002.2235)
Komdeur, J., Kraaijeveld-Smit, F., Kraaijeveld, K. & Edelaar,
P. 1999 Explicit experimental evidence for the role of mate
guarding in minimizing loss of paternity in the Seychelles
warbler. Proc. R. Soc. B 266, 2075–2081. (doi:10.1098/
Korpimaki, E., Lahti, K., May, C. A., Parkin, D. T., Powell,
G. B., Tolonen, P. & Wetton, J. H. 1996 Copulatory
behaviour and paternity determined by DNA fingerprint-
ing in kestrels: effects of cyclic food abundance. Anim.
Behav. 51, 945–955. (doi:10.1006/anbe.1996.0098)
Kuukasja ¨rvi, S., Eriksson, C. J. P., Koskela, E., Mappes, T.,
Nissinen, K. & Rantala, M. J. 2004 Attractiveness of
women’s body odors over the menstrual cycle: the role of
oral contraception and received sex. Behav. Ecol. 15,
Lancaster, J. B. & Kaplan, H. S. In press. The endocrinology
of the human adaptive complex. In Endocrinology of social
relationships (eds P. G. Gray & P. T. Ellison). Cambridge,
MA: Harvard University Press.
998 S. W.Gangestad & R. Thornhill
Review. Human oestrus
Proc. R. Soc. B (2008)
Little, A. C., Jones, B. C. & Burriss, R. P. 2007a Preferences
for masculinity in male bodies change acrossthe menstrual
cycle. Horm. Behav. 31, 633–639. (doi:10.1016/j.yhbeh.
Little, A. C., Jones, B. C., Burt, D. M. & Perrett, D. I. 2007b
Preferences for symmetry in faces change across the
menstrual cycle. Biol. Psychol. 76, 209–216. (doi:10.1016/
Low, M. 2005 Factors influencing mate guarding and
territory defence in the stitchbird (hihi) Notiomystis cincta.
New Zeal. J. Ecol. 29, 231–242.
Ludue-Larena, J. J., Lo ´pez, P. & Gosa ´lbez, J. 2003 Male
dominance and female chemosensory preferences in the
Lynch, K. S., Rand, A. S., Ryan, M. J. & Wilczynski, W. 2005
Plasticity in female mate choice associated with changing
reproductive states. Anim. Behav. 69, 689–699. (doi:10.
Lynch, K. S., Crews, D., Ryan, M. J. & Wilczynski, W. 2006
Hormonal state influences aspects of female mate choice
in the Tu ´ngara Frog (Physalaemus pustulosus). Horm.
Behav. 49, 450–457. (doi:10.1016/j.yhbeh.2005.10.001)
Marlowe, F. W. 2003 A critical period for provisioning
by Hadza men: implications for pair bonding. Evol.
Hum. Behav. 24, 217–229. (doi:10.1016/S1090-5138
Michalek, K. G. & Winkler, H. 2001 Parental care and
parentage in monogamous great spotted woodpeckers
(Picoides major) andmiddle
(Picoides medius). Behav. 138, 1259–1285. (doi:10.1163/
Michl, G., Torok, T., Griffith, S. C. & Sheldon, B. C. 2002
Experimental analysis of sperm competition mechanisms
in a wild bird population. Proc. Natl Acad. Sci. USA 99,
Miller, G. F. 2000 The mating mind: how sexual choice shaped
the evolution of human nature. New York, NY: Anchor
Miller, G. F., Tybur, J. & Jordan, B. 2007 Ovulatory cycle
effects on tip earnings by lap dancers: economic evidence
for human estrus? Evol. Hum. Behav. 28, 375–381.
Møller, A. P. 2000 Male paternal care, female reproductive
success, and extrapair paternity. Behav. Ecol. 11, 161–168.
Møller, A. P. 2003 The evolution of monogamy: mating
relationships, paternal care and sexual selection. In
Monogamy: mating strategies and partnerships in birds,
humans and other mammals (eds U. H. Reichard &
C. Boesch), pp. 29–41. Cambridge, UK: Cambridge
Mougeot, F. S. 2004 Breeding density, cuckoldry risk and
copulation behaviour during the fertile period in raptors: a
comparative analysis. Anim. Behav. 67, 1067–1076.
Nelson, R. J. 2000 An introduction to behavioral endocrinology,
2nd edn. Sunderland, MA: Sinauer Associates, Inc.
Neudorf, D. L., Stutchbury, B. J. M. & Piper, W. H. 1997
Covert extraterritorial behavior of female hooded warblers.
Behav. Ecol. 8, 595–600. (doi:10.1093/beheco/8.6.595)
Pagel, M. 1994 Evolution of conspicuous estrous advertise-
ment in old-world monkeys. Anim. Behav. 47, 1333–1341.
Pawlowski, B. & Jasienska, G. 2005 Women’s preferences for
sexual dimorphism in height depend on menstrual cycle
phase and expected duration of relationship. Biol. Psychol.
70, 38–43. (doi:10.1016/j.biopsycho.2005.02.002)
Pedersen, M. C., Dunn, P. O. & Whittingham, L. A. 2006
Extraterritorial forays are related to a male ornamental
trait in the common yellowthroat. Anim. Behav. 72,
Penton-Voak, I. S. & Perrett, D. I. 2000 Female preference
for male faces changes cyclically—further evidence. Evol.
Hum. Behav. 21, 39–48. (doi:10.1016/S1090-5138(99)
Penton-Voak, I. S., Perrett, D. I., Castles, D. L., Kobayashi,
T., Burt, D. M., Murray, L. K. & Minamisawa, R. 1999
Female preference for male faces changes cyclically.
Nature 399, 741–742. (doi:10.1038/21557)
Pierce, E. P. & Lifjeld, J. T. 1998 High paternity without
paternity–assurance behavior in the purple sandpiper, a
species with high paternal investment. Auk 115, 602–612.
Pillsworth, E. G. & Haselton, M. G. 2006 Male sexual
attractiveness predicts differential ovulatory shifts in female
extra-pair attraction and male mate retention. Evol. Hum.
Behav. 27, 247–258. (doi:10.1016/j.evolhumbehav.2005.
Pillsworth, E. G., Haselton, M. G. & Buss, D. M. 2004
Ovulatory shifts in female sexual desire. J. Sex Res. 41,
Poran, N. S. 1994 Cycle attractivity of human female odors.
Adv. Biosci. 93, 555–560.
Potts, W. K., Manning, C. J. & Wakeland, E. K. 1991 Mating
patterns in seminatural populations of mice influenced by
MHC genotype. Nature 352, 619–621. (doi:10.1038/
Puts, D. A. 2005 Mating context and menstrual phase affect
women’s preferences for male voice pitch. Evol. Hum.
Behav. 26, 388–397. (doi:10.1016/j.evolhumbehav.2005.
Puts, D. A. 2006 Cyclic variation in women’s preferences for
masculine traits: potential hormonal causes. Hum. Nat.
17, 114–127. (doi:10.1007/s12110-006-1023-x)
Radford, S. L., Croft, D. B. & Moss, G. L. 1998 Mate choice
in female red-necked pademelons, Thylogale thetis (Mar-
supialia: Macropodidae). Ethology 104, 217–231.
Rantala, M. J., Eriksson, C. J. P., Vainikka, A. & Kortet, R.
2006 Male steroid hormones and female preference for
male body odor. Evol. Hum. Behav. 27, 259–269. (doi:10.
Rikowski, A. & Grammer, K. 1999 Human body odour,
symmetry and attractiveness. Proc. R. Soc. B 266,
Riley, H. T., Bryant, D. M., Carter, P. E. &Parkin, D. T. 1995
Extrapair fertilizations and paternity defense in house
martins, Delichon urbica. Anim. Behav. 49, 495–509.
Roberts, S. C., Havlicek, J., Flegr, J., Hruskova, M., Little,
A.C., Jones, B. C.,Perrett, D. I. &Petrie, M.2004 Female
facial attractiveness increases during the fertile phase of
the menstrual cycle. Proc. R. Soc. B 271, S270–S272.
Robertson, B. C., Degnan, S. M., Kikkawa, J. & Moritz,
C. C. 2001 Genetic monogamy in the absence of paternity
guards: the Capricorn silvereye, Zosterops lateralis chlor-
ocephalus, on Heron Island. Behav. Ecol. 12, 666–673.
Rodriguez-Girones, M. A. & Enquist, M. 2001 The evolution
of female sexuality. Anim. Behav. 61, 695–704. (doi:10.
preference for facial cues of men’s testosterone. Horm.
Behav. 53, 14–19. (doi:10.1016/j.yhbeh.2007.09.008)
Saino, N., Primmer, C. R., Ellegren, H. & Moller, A. P. 1999
Breeding synchrony and paternity in the barn swallow
(Hirundo rustica). Behav. Ecol. Sociobiol. 45, 211–218.
Review. Human oestrus
S. W.Gangestad & R. Thornhill999
Proc. R. Soc. B (2008)
Scarbrough, P. S. & Johnston, V. S. 2005 Individual Download full-text
differences in women’s facial preferences as a function
of digit ratio and mental rotation ability. Evol. Hum.
Behav. 26, 509–526. (doi:10.1016/j.evolhumbehav.2005.
Schulte, B. A. & Rasmussen, L. E. L. 1999 Signal receiver
interplay in the communication of male condition by
Asian elephants. Anim. Behav. 57, 1265–1274. (doi:10.
Sheldon, B. C., Davidson, P. & Lindgren, G. 1999
Mate replacement in experimentally widowed collared
flycatchers (Ficedula albicollis): determinants and out-
comes. Behav. Ecol. Sociobiol. 46, 141–148. (doi:10.1007/
Sille ´n-Tullberg, B. & Møller, A. P. 1993 The relationship
between concealed ovulation and mating systems in
anthropoid primates—a phylogenetic analysis. Am. Nat.
141, 1–25. (doi:10.1086/285458)
Simmons, L. W., Firman, R. C., Rhodes, G. & Peters, M.
2004 Human sperm competition: testis size, sperm
production, and rates of extra-pair copulations. Anim.
Behav. 68, 297–302. (doi:10.1016/j.anbehav.2003.11.013)
Singh, D. & Bronstad, P. M. 2001 Female body odour is a
potential cue to ovulation. Proc. R. Soc. B 268, 797–801.
Spritzer, M. D., Meikle, D. B. & Solomon, N. G. 2005
Female choice based on male spatial ability and aggres-
Spuhler, J. N. 1979 Continuities and discontinuities in
anthropoid-hominid behavioral evolution: bipedal loco-
motion and sexual receptivity. In Evolutionary biology and
human social behavior: an anthropological perspective (eds
N. A. Chagnon & W. Irons), pp. 454–461. North Scituate,
MA: Duxbury Press.
Stacy, P. B. 1982 Female promiscuity and male reproductive
success in social birds and mammals. Am. Nat. 120,
Stanback, M., Richardson, D. S., Boix-Hinzen, C. &
Mendelsohn, J. 2002 Genetic monogamy in Monteiro’s
hornbill, Tockus monteiri. Anim. Behav. 63, 787–793.
Sterelny, K. & Griffiths, P. E. 1999 Sex and death: an
introduction to the philosophy of biology. Chicago, IL:
University of Chicago Press.
Stumpf, R. M. & Boesch, C. 2005 Does promiscuous mating
preclude female choice? Female sexual strategies in
chimpanzees (Pan troglodytes verus) of the Taı ¨ National
Park, Co ˆte d’Ivoire. Behav. Ecol. Sociobiol. 57, 511–524.
Symons, D. 1979 The evolution of human sexuality. Oxford,
UK: Oxford University Press.
Tarı ´n, J. J. & Go ´mez-Piquer, V. 2002 Do women have a
hidden heat period? Hum. Reprod. 17, 2243–2248.
Thornhill, R. & Gangestad, S. W. 1999 The scent of
symmetry: a human sex pheromone that signals fitness?
Evol. Hum. Behav. 20, 175–201. (doi:10.1016/S1090-
Thornhill, R. & Gangestad, S. W. 2003 Do women have
Evolutionary aesthetics (eds E. Voland & K. Grammer),
pp. 341–368. Heidelberg, Germany: Springer.
Thornhill, R. & Gangestad, S. W. In press. The evolutionary
biology of human female sexuality. New York, NY: Oxford
Thornhill, R., Gangestad, S. W., Miller, R., Scheyd, G.,
Knight, J. & Franklin, M. 2003 MHC, symmetry, and
body scent attractiveness in men and women. Behav. Ecol.
14, 668–678. (doi:10.1093/beheco/arg043)
Thornton, J. W. 2001 Evolution of vertebrate steroid
receptors from an ancestral estrogen receptor by ligand
exploitation and serial genome expansions. Proc. Natl
Acad. Sci. USA 98, 5671–5676. (doi:10.1073/pnas.
Thornton, J. W., Need, E. & Crews, D. 2003 Resurrecting the
ancestral steroid receptor: ancient origin of estrogen
signaling. Science 301, 1714–1717. (doi:10.1126/science.
Wakano, J. Y. & Ihara, Y. 2005 Evolution of male parental
care and female multiple mating: game–theoretical and
two-locus diploid models. Am. Nat. 166, E32–E44.
Waitt, C., Little, A. C., Wolfensohn, S., Honess, P., Brown,
A. P., Buchanan-Smith, H. M. & Perrett, D. I. 2003
Evidence from rhesus macaques suggests that male
coloration plays a role in female primate mate choice.
Proc. R. Soc. B 270, S144–S146. (doi:10.1098/rsbl.2003.
Welling, L. L. M., Jones, B. C., DeBruine, L. M., Conway,
C. A., Law Smith, M. J., Little, A. C., Feinberg, D. R.,
Sharp, M. A. & Al-Dujaili, E. A. S. 2007 Raised salivary
testosterone in women is associated with increased
Wilcox, A. J., Weinberg, C. R. & Baird, D. D. 1995 Timing of
sexual intercourse in relation to ovulation: effects on the
probability of conception, survival of the pregnancy, and
sex of the baby. New Engl. J. Med. 333, 1517–1521.
Wilcox, A. J., Baird, D. D., Dunson, D. B., McConnaughey,
D. R., Kesner, J. S. & Weinberg, C. R. 2004 On the
frequency of intercourse around ovulation: evidence for
biological influences. Hum. Reprod. 19, 1539–1543.
Williams, R. J. & Lenington, S. 1993 Factors modulating
preferences of female house mice for males differing in
genetic background, and estrous condition of females.
Behav. Genet. 23, 51–58. (doi:10.1007/BF01067553)
Wolff, J. O. 1998 Breeding strategies, mate choice, and
reproductive success in American bison. Oikos 83,
of T-complex genotype,
1000S. W.Gangestad & R. Thornhill
Review. Human oestrus
Proc. R. Soc. B (2008)