PERSPECTIVE AND HYPOTHESIS

The Evolutionary Origin of Female

Orgasm
MIHAELA PAVLIČEV1,2∗
AND GÜNTER WAGNER
3,4,5,6
1
Center for Prevention of Preterm Birth, Perinatal Institute, Cincinnati Children’s Hospital Medical
Center, Cincinnati, Ohio
2
Department of Pediatrics, University of Cincinnati College of Medicine, Cincinnati, Ohio
3
Department of Ecology and Evolutionary Biology, Yale University, New Haven, Connecticut
4
Yale Systems Biology Institute, Yale University, West Haven, Connecticut
5
Department of Obstetrics, Gynecology and Reproductive Sciences, Yale Medical School, New
Haven, Connecticut
6
Department of Obstetrics and Gynecology, Wayne State University, Detroit, Michigan

ABSTRACT The evolutionary explanation of female orgasm has been difficult to come by. The orgasm in
women does not obviously contribute to the reproductive success, and surprisingly unreliably ac-
companies heterosexual intercourse. Two types of explanations have been proposed: one insisting
on extant adaptive roles in reproduction, another explaining female orgasm as a byproduct of se-
lection on male orgasm, which is crucial for sperm transfer. We emphasize that these explanations
tend to focus on evidence from human biology and thus address the modification of a trait rather
than its evolutionary origin. To trace the trait through evolution requires identifying its homologue
in other species, which may have limited similarity with the human trait. Human female orgasm
is associated with an endocrine surge similar to the copulatory surges in species with induced
ovulation. We suggest that the homolog of human orgasm is the reflex that, ancestrally, induced
ovulation. This reflex became superfluous with the evolution of spontaneous ovulation, potentially
freeing female orgasm for other roles. This is supported by phylogenetic evidence showing that
induced ovulation is ancestral, while spontaneous ovulation is derived within eutherians. In addi-
tion, the comparative anatomy of female reproductive tract shows that evolution of spontaneous
ovulation is correlated with increasing distance of clitoris from the copulatory canal. In summary,
we suggest that the female orgasm-like trait may have been adaptive, however for a different
role, namely for inducing ovulation. With the evolution of spontaneous ovulation, orgasm was
freed to gain secondary roles, which may explain its maintenance, but not its origin. J. Exp. Zool.
J. Exp. Zool. (Mol. Dev. Evol.) 00B:1–12, 2016.  C 2016 Wiley Periodicals, Inc.

(Mol. Dev. Evol.)

00B:1–12, How to cite this article: Pavličev M, Wagner G, 2016. The evolutionary origin of female
2016 orgasm. J. Exp. Zool. (Mol. Dev. Evol.) 00B:1–12.

Grant sponsor: March of Dimes Prematurity Research Center Ohio Collaborative; grant number: 22-FY14-470; grant sponsor: John Templeton Foundation;
grant number: 54860.
Conflicts of interest: None.
Additional Supporting Information may be found in the online version of this article.
∗ Correspondence to: Mihaela Pavličev, Center for Prevention of Preterm Birth, Perinatal Institute, Cincinnati Children’s Hospital Medical Center, Cincinnati,

Ohio 45229.
E-mail: mihaela.pavlicev@cchmc.org
Received 8 May 2016; Revised 20 June 2016; Accepted 23 June 2016
DOI: 10.1002/jez.b.22690
Published online in Wiley Online Library (wileyonlinelibrary.com).


C 2016 WILEY PERIODICALS, INC.
2 PAVLIČEV ET AL.
Human female orgasm has intrigued biologists for centuries,
trying to find its adaptive value, or any evolutionary explanation
at all. Already Aristotle noted the main obstacle in explaining
the role of female orgasm: human females can conceive without
it, so it does not appear to affect reproductive success (Aristo-
tle, after Leroi, 2014). In males, orgasm is invariably required for
ejaculation and transfer of sperm, but in females its function is
unclear. Equally suggestive is the statistics, showing that human
female orgasm during sexual intercourse is uncommon, in par-
ticular without additional clitoral stimulation (reviewed exten-
sively in Lloyd, 2005); the orgasm is in fact more common dur-
ing female masturbation or homosexual intercourse, than during
actual heterosexual intercourse (Garcia et al., 2014); or there is
no association between orgasm and number of offspring (Zietsch
and Santtila, 2013). So what is the female orgasm there for?
The field addressing the role of female orgasm is by no means
short of hypotheses. The evolutionary hypotheses align in two
groups: one group argues that it is not quite true that female or-
gasm has no effect on reproductive success (e.g., enabling female
choice, bonding, etc.), and the other group argues that it may
indeed have no reproductive value in the females, but rather its
existence is explained as a correlated effect of another selected
trait, or a different developmental stage. For example, one well
appreciated among the later hypotheses describes female orgasm
as a fortunate consequence of the shared developmental basis of
clitoris and penis, and therefore a consequence of reproductive
necessity of the male orgasm (by-product hypothesis, Symons,
’79). A critical review of the existing hypotheses has been pub-
lished in Lloyd (2005) and will not be attempted here.
Here, we note that most hypotheses are seeking an explanation
for the presence of female orgasm within the human or primate
lineage, whether due to direct or correlated effects of selection.
Yet we will argue below that female orgasm, as male orgasm,
predate the primate lineage, and the orgasm of human females
likely evolved from an ancestral and adaptive trait, which might
not have all the characteristics of human orgasm and may also
have had a different function. We propose that explanations fo-
cusing on primate mating system and behavior thus address the
primate-specific (or sometimes human-specific) modifications of
a previously existent trait rather than its origin (Amundson,
2008). Our focus here will be the question what that ancestral
trait may have been. As the lineage-specific modifications or
secondary cooption (“exaptation,” in terms of Gould and Vrba,
’82) can take extreme forms under different, internal, or external
selective forces, we therefore do not expect to find in animals a
female orgasm as we know it in human, but are rather seeking
its homologue in other species.
To address this question requires a description of the trait
and its occurrence across species. Human orgasm is often de-
scribed as a climax, followed by a sudden discharge of major
sexual arousal. Defined this way, the presence of female orgasm
is hard to establish with certainty beyond primates, and hence
J. Exp. Zool. (Mol. Dev. Evol.)
little has been found about its distribution. It is noteworthy that
the byproduct hypothesis (Symons, ’79; Lloyd, 2005) implies that
as the male orgasm is undisputed for most mammals, so must
be the female orgasm. Some indication for the existence of a
climax of sexual arousal in females is offered in the reports on
the work of reproductive zoologist Alfred C. Kinsey and col-
laborators. In the collection of Kinsey‘s unpublished research,
Pomeroy (’72) reports correspondence between Kinsey and sev-
eral animal breeders on the question of female orgasm in various
species. Indeed, Kinsey was able to collect evidence (including
film material), suggesting a climax in female ferret, cat, and rab-
bit, all of which are reflex ovulators, as will be explained next.
More thorough descriptions of orgasm include psychologi-
cal, endocrinological, and neurological aspects (list in Mah and
Binik, 2001). We will focus here on a specific physiological trait
that accompanies human female orgasm, namely the neuroen-
docrine discharge, and in particular the surge of prolactin (PRL),
and to a lesser extent, oxytocin. We suggest that the hormonal
surge that accompanies orgasm in humans may reveal its homo-
logue in other placental mammals. This surge serves a range of
important but variable reproductive functions across mammals,
and may have become modified to what we understand as fe-
male orgasm in humans, as its ancestral reproductive function
became less important or obsolete. It is crucial for this argument
to note that in humans the hormonal surge is not invariably as-
sociated with copulation, rather it is associated with the female
orgasm (e.g., Huynh et al., 2013). To build this argument, we will
first briefly review some aspects of the mammalian reproductive
evolution, discuss the role of endocrine surge, and finally also
review the anatomical aspects of copulation in eutherians (also
known as “placental” mammals) in the light of their ovarian
cyclicity.
ORGASM AND THE EVOLUTION OF MAMMALIAN
OVARIAN CYCLE
In spite of apparently enormous diversity of mammalian repro-
ductive biology, some core characteristics can be traced through-
out mammalian evolution. Female ovarian cycle is one such
characteristic. The essential condition for the success of internal
fertilization is the timely maturation and release of the oocytes
from the ovary into the female reproductive tract, that is, ovu-
lation, for the egg to be accessible to sperm. These events need
to be coordinated with the availability of males and favorable
environmental conditions for raising the young. The proximal
regulation of this process is dominated in mammals by pitu-
itary peptide hormones, mainly the follicle-stimulating hormone
(FSH) and luteinizing hormone (LH), which in turn are regulated
by gonadotropin releasing hormones.
In most mammals, the surges of FSH and LH trigger the cas-
cade of the ovarian cycle (Fig. 1), which consists of follicle
maturation, ovulation, the variable persistence of the hormone-
producing corpus luteum (CL), and its subsequent luteolysis,
EVOLUTION OF FEMALE ORGASM 3

corpus luteum

luteolysis
CL

corpus albicans
ovulation
P4

pituitary

LH
FSH
Graafian follicle

ovary

folliculogenesis

Figure 1. The scheme of the ovarian cycle (CL, corpus luteum; see text).

leading to, in absence of fertilization, systemic progesterone
withdrawal. CL is a transient remnant of the burst egg follicle
after ovulation and the primary source of progesterone, which
plays essential roles in pregnancy. This relatively simple shared
process is at the core of female reproduction and has been mod-
ified multiple times independently to balance costs and benefits
of taxa-specific mating systems and environmental conditions.
One of the parts of the ovarian cycle that has undergone exten-
sive evolutionary changes is the upstream trigger of this process,
that is, which stimulus causes the release of pituitary hormones
leading to ovulation.
Regulation of Receptivity
In many mammalian species, the potential to reproduce is re-
stricted to a short season of the year, coinciding with either
suitable environmental conditions, or the availability of mates.
This restriction requires the coordination of reproduction using
external cues. The cues may be related to the season, such as
the length of the day or temperature. Environmentally induced
breeders are often polyestrous, that is, ovulating spontaneously
during a certain part of the year, likely corresponding to the
presence of an external cue (e.g., photoperiod or pheromones).
Species with seasonally restricted ovulation are common among
eutherians: Xenarthra (Knott et al., 2013), Laurasitheria (horses,
bats, hedgehogs, sheep), as well as basal primates (e.g., lemurs:
Van Horn, ’75, macaques: Lindburg, ’91).
Alternatively, the chances to encounter a sexual partner may
impose limitation on reproduction, in particular for species that
tend to live singly, such as rabbits, cats, or wolverines. In this
subset of induced ovulators, the external cue is either male
pheromones as in the short-tailed gray opossum, Monodelphis
domestica (Vandenbergh, ’83), or the copulation itself, as in rab-
bits or cats (Bakker and Baum, 2000). Laviriere and Ferguson
(2003) argued that not only partner-induced ovulation is adap-
tive because it ensures that ovulation coincides with the en-
counter of a mate, but it would also potentially enable the fe-
male to assess the quality of the partner in absence of direct
competition between males (assuming that the ability of a male
to induce ovulation in its mate reflects the quality of the male).
The authors have shown that the North American carnivores,
which are copulation-induced ovulators, indeed tend to have
large home ranges. Furthermore, monogamous species in which
partners would stay in proximity for extended period of time
are rare among these reflex ovulators. In contrast, a mating sys-
tem in which females mate with multiple males (polyandry), is
particularly common among these carnivores, supporting the as-
sociation between induced ovulation and female choice. Finally,
the spontaneous ovulators, such as primates including humans,
are at the extreme end of this continuum, with the autonomous
periodicity of LH surge, followed invariably by ovulation, and
in the case of fertilization, by implantation.
These three types of ovulatory induction, environmental,
male-induced, and spontaneous, are not fully separated. As men-
tioned above, many spontaneous ovulators also show seasonal-
ity, conditional on temperature or photoperiod. Degrees of mod-
ification of seasonality are well demonstrated in the animals

J. Exp. Zool. (Mol. Dev. Evol.)

4 PAVLIČEV ET AL.
kept under breeding conditions, either because of past selec-
tion for breeding efficiency during domestication, or because
the seasonally variable external factors are continuously present
in captivity. For example, while domestic pig is a spontaneous
ovulator throughout the year, its closely related European wild
boar undergoes ovarian inactivity (anestrus) over parts of the
year (Delcroix et al., 1990; Ahmad et al., 1995). Furthermore,
there is evidence that ovulation can be induced or accelerated
by copulation, or the presence of a male, even in several sponta-
neously ovulating species (see reports for mouse, rat, sow, sheep
in Zarrow and Clark, ’68; Zarrow et al., ’68; Signoret et al., ’72).
Potentially indicative of a role in inducing ovulation is an inter-
esting preference in rhesus macaques for masturbation before the
ovulation (Akers and Conaway, ’79). There are also reports to the
opposite, namely that spontaneous ovulation sometimes occurs
in induced ovulators (cats: Gudermuth et al., ’97). This over-
lap suggests that different signals are capable of triggering the
same pathway, and evolutionary transitions among these forms
are likely.
There has been much discussion about whether spontaneous
(or copulation) induced ovulation is the ancestral form (reviewed
in Bakker and Baum, 2000). This is in part due to our lim-
ited knowledge about the reproductive biology of many species,
and in part due to the presence of spontaneous and copulation-
induced ovulators in most therian clades. In addition, we think
that the attribution of species, which actually depend on envi-
ronmental cues (pheromones or photoperiod, rather than tactile
stimulation), to spontaneous ovulators (Weir and Rowlands, ’73)
may have been misleading. We will therefore distinguish three
principle classes of ovulatory cycle regulation: externally in-
duced, male-induced, and spontaneous. It should be noted here
that, in principle, the encounter of the traces of the ancestral
type of ovarian regulation in the derived type is not surprising.
The ancestral amniote state predating the placental mammals
on which we focus here, was likely that of external regulation
of the ovarian cycle. Indeed, seasonality of estrous is widespread
among eutherians of both spontaneous and male-induced ovula-
tory type. Ancestral status of external regulation of the ovarian
cycle is also supported by the widespread effect of photoperi-
odism on reproduction (Bradshaw and Holzapfel, 2007), and the
fact that environmental regulation of ovarian cycles predates in-
ternal fertilization: photoperiod and temperature regulate ovu-
lation in teleost fishes (Khan and Thomas in Knobil and Neill,
’88), ovarian cycles of amphibians (Norris and Jones, ’87), and
in lungfish (Kemp, ’84).
Within eutherian mammals, the question therefore concerns
the evolution of male-induced versus spontaneous ovulation,
based on the ancestral environmentally induced ovulation.
Bakker and Baum (2000) suggest that reflex ovulation may have
evolved as a special case of other type of male-induced ovula-
tion, for example, one in which a surge of gonadotropin is in-
duced by the behavioral or pheromonal stimuli. The phylogenetic
J. Exp. Zool. (Mol. Dev. Evol.)
distribution of the male-induced and spontaneous ovulation is
shown in Figure 2A. We included male pheromone induced ovu-
lation in opossum as male-induced ovulation. Additional tem-
perature/light effects on ovulation are not considered here for
simplicity, however we note that these conditions play a role in
many of the species shown. Even if environmental cues would
in some eutherian species be the sole trigger of ovulation, this
does not change the phylogenetic inference, as these cues are
likely ancestral (i.e., plesiomorphic).
It should be noted that the male-induced ovulation is hard
to establish with certainty in nature, and therefore its occur-
rence is likely underreported. For example, in addition to estab-
lished cases, male-induced ovulation has been suggested in ele-
phant seal, long-nosed kangaroo rat (marsupial), lump-nosed bat
(Norris and Carr, 2013), and further species of ground squirrels
(Landau and Holmes, ’88; Bouchie et al., 2006) and possibly
more, but a definite account is lacking for many species. This
complicates the reconstruction of character evolution.
It has been proposed early on that copulation-induced ovula-
tion predated spontaneous ovulation (Keverne in Vandenbergh,
’83). The supporting evidence is that the copulation-induced
ovulation is particularly common in the basal group of Eu-
lipotyphla (previously insectivores: shrews, hedgehogs, moles),
but also in carnivores (Felids, Mustelids, Ursids), Lagomorphs,
Rodentia, and Camelids, and further, that copulation has been
shown to induce ovulation in some of the spontaneous ovu-
lators, suggesting its ancestral primacy. According to mod-
ern eutherian phylogenetic hypotheses (dos Reis et al., 2012;
O’Leary et al., 2013), most clades include male-induced ovulators
(Fig. 2). Additional findings have been particularly informa-
tive, including the copulation-induced ovulation in marsu-
pials (koala: Johnston et al., 2000; Johnston et al., 2004),
Xenarthra (pichi: Superina and Jahn, 2009; Superina et al.,
2009), and Afrotheria (e.g., Eisenberg and Gould, ’70). This evi-
dence supports the notion that male-induced ovulation is ances-
tral in eutherians and spontaneous ovulation is a derived mode
of ovarian cyclicity, which likely evolved from some form of the
copulation-induced type of ovulation.
ENDOCRINE SURGES ASSOCIATED WITH HUMAN
ORGASM
Rather than looking for a neurological–behavioral description,
we focus on distinct hormonal signals that have been described
to accompany human orgasm, and importantly, are pronounced
in females by clitoral stimulation leading to female orgasm.
These are predominantly surges of PRL (Exton et al., ’99, 2001a,
2001b; Kruger et al., 2002; Huynh et al., 2013), LH (Exton et al.,
’99), and oxytocin (Carmichael et al., ’87; Carmichael et al., ’94;
Blaicher et al., ’99). Copulation-induced surges have been de-
tected in other spontaneous ovulators: PRL and LH surges are
known in rodents (Knobil and Neill, ’88). Interestingly, this pat-
tern of PRL increase was detected in both sexes in mice (Bronson
 B
A

C
Human
Human Human Chimpanzee
Chimpanzee Chimpanzee
Rhesus
Rhesus Rhesus
Marmoset
Marmoset Marmoset Tarsier
Tarsier Tarsier

black: no UGS
Ring-tailed lemur
Ring-tailed lemur Ring-tailed lemur
Mouse

grey: at the border

black: at the border
Mouse

black: spontaneous ov.

Mouse Rat

green: UGS (/cloaca)

green: clitoris outside

green: male-‐induced ov.
EVOLUTION OF FEMALE ORGASM

Rat Rat
Golden hamster
Golden hamster Golden hamster
Guinea pig
Guinea pig Guinea pig
Chinchilla
Chinchilla Chinchilla Mole rat
Mole rat Mole rat
Woodchuck
Woodchuck Woodchuck
Ground squirrel
Ground squirrel Ground squirrel Rabbit
Rabbit Rabbit
Goat
Goat Goat
Sheep
Sheep Sheep
Dolphin
Dolphin Dolphin Cow
Cow Cow
Pig
Pig Pig
Alpaca
Alpaca Alpaca Bactrian camel
Bactrian camel Bactrian camel
Horse
Horse Horse
Little mastif bat
Little mastif bat Little mastif bat
Ferret
Ferret Ferret Raccoon
Raccoon Raccoon
Dog
Dog Dog
Domestic cat
Domestic cat Domestic cat White-toothed shrew
White-toothed shrew White-toothed shrew
European hedgehog
European hedgehog European hedgehog
Brown-throated sloth
Brown-throated sloth Brown-throated sloth
Lesser anteater
Lesser anteater Lesser anteater Dwarf armadillo
Dwarf armadillo Dwarf armadillo
Nine-banded armadillo
Nine-banded armadillo Nine-banded armadillo
Dugong
Dugong Dugong Hyrax
Hyrax Hyrax
African elephant
African elephant African elephant
Tenrec
Tenrec Tenrec
Aardvark
Aardvark Aardvark Grey short-tailed opposum
Grey short-tailed opposum Grey short-tailed opposum
Koala
Koala Koala
5

J. Exp. Zool. (Mol. Dev. Evol.)

6 PAVLIČEV ET AL.

and Desjardins, ’82) as well as humans (Exton et al., 2001aa). In
the case of LH, postcoital surge has been detected in rats (Taleis-
nik et al., ’66; Moss and Cooper, ’73) and its presence is associ-
ated with lordosis behavior, that is, indicating copulatory readi-
ness in female rodents (Broitman and Donoso, ’75).
Most of the research on copulation-associated surges of pitu-
itary hormones has been conducted in species in which an envi-
ronmental stimulus is required for an aspect of the female ovar-
ian cycle. Specifically, PRL is found to be a mediating hormone
involved in three processes: environmentally induced ovulation,
copulation-induced ovulation, and regulation of implantation,
as will be explained next.
Interestingly, PRL is involved in induction of ovulation both
in environmentally induced and copulation-induced ovulators.
Furthermore, PRL peak precedes ovulation in spontaneous ovu-
lators as well, as is known from rats and to a lesser extent
humans (Freeman et al., 2000). PRL mediates pheromonal ef-
fects on sexual behavior in lemurs (lemurs: Perret and Schilling,
’87; Freeman et al., 2000; mice: Mak et al., 2007; Larsen et al.,
2008), and likely mediates the effects of light period on repro-
ductive seasonality (Curlewis, ’92). The environmental induction
of the PRL surge has been co-opted also in regulation of the im-
plantation after diapause (e.g., in mink), further synchronizing
the embryonal development with the season (Papke et al., ’80;
Renfree and Shaw, 2000).
In reflex ovulators, it is the copulation that induces a neu-
roendocrine response and elicits a surge of PRL, LH, and FSH,
the pro-ovulatory hormones whose dynamic is autonomous in
most spontaneous ovulators. The main mechanism is thought
to be physical stimulation (although there is evidence that bio-
chemical signals in seminal plasma play a role in camelids), and
its pro-ovulatory effect may be conserved even in some spon-
taneous ovulators (Bogle et al., 2011). Tactile stimulation dur-
ing coitus is mediated to central nervous system by the nora-
drenergic system (Terkel, ’88). The function of the PRL surge is
potentiating the effects of LH by regulating the expression of
LH (as well as estrogen) receptors in the follicle and later in the
CL, and inhibiting progesterone metabolizing enzymes, therefore
promoting the progesterone secretion (Freeman et al., 2000).
Interestingly, copulation has a related but distinct func-
tion in many rodents (mouse, rat, hamster). These species
exhibit regular LH surges and spontaneous ovulation, yet
in the absence of a blastocyst their estrous cycle is short,
with almost nonexistent CL. If sperm is deposited in female
reproductive tract without the physical stimulation of the coitus,
the blastocyst cannot implant due to the lack of progesterone
from CL. The hormone maintaining the CL until implantation
and even through the first part of pregnancy is PRL. Copulation-
associated PRL surge in these species is thus not pro-ovulatory,
but it is luteotroph. Luteotrophic function of PRL is also nec-
essary for implantation in ferret, an induced ovulator (Murphy,
’79). This suggests that either the rodents maintained only the lu-
teotroph aspect of PRL surge, or the pro-ovulatory function has
been co-opted into the signal for prolonged luteal activity en-
abling implantation. Albeit not a requirement as in rodents, there
are indications that intercourse affects implantation in human
as well. In their controlled study of in vitro fertilized patients,
Tremellen et al. (2000) found significantly increased proportion
of viable embryos at 6–8 weeks in the group that was asked to
engage in intercourse shortly before embryo transfer, relative to
a second group that was instructed to abstain from sex. It is not
clear from this study to what extent orgasm accompanied in-
tercourse, however the study does show a correlation between
intercourse and successful implantation. This could suggest that
at least some aspects of the female arousal response are still un-
der selection even in humans, even though not strictly necessary
for the initiation of pregnancy.
It is important to note that PRL has diverse functions in re-
production, and they may differ greatly between stages of the
ovarian cycle (Freeman et al., 2000), including possible lute-
olytic and other inhibitory effects (e.g., inhibition of ovulation
during lactation; McNeilly et al., ’94). In humans, the inhibitory
effect of pathological hyperprolactinemia on folliculogenesis has
been invoked to interpret the copulatory PRL surge as an adap-
tive signal inhibiting further copulatory behavior (Kruger et al.,
2002). It is likely, however, that the inhibitory effect on ovula-
tion is restricted to persistent pathologically high levels of PRL
(>100 ng/mL, while the copulatory PRL surge has peak serum
concentrations of up to 40 ng/mL), or specific times in the ovar-
ian cycle. It seems more likely that the copulatory PRL surge
is a remnant of the evolutionarily older pregnancy-supportive
role in induced ovulators. Supportive of this suggestion is also
the fact that in women decreased physiological levels of PRL are
also associated with shortened luteal phase of the ovarian cycle
(Kauppila et al., ’88), consistent with the luteotrophic effect of
PRL in mice and rats.
Although we focus here on female orgasm, it is important to
note that PRL plays a gonadotrophic role in both sexes, and the

Figure 2. Phylogenetic distribution of (A) modes of ovulation, (B) the presence of the urogenital sinus (UGS; in basal species: cloaca),
and (C) the position of clitoris relative to the vaginal orifice (in, border, out). Note the phylogenetic correlation between spontaneous
ovulation with the reduction of the urogenital sinus, and the external position of the clitoris. This correlation is suggestive of an ancestral
role of clitoral stimulation for the initiation of pregnancy in induced ovulators and the loss of this function in spontaneous ovulators. The
phylogenetic relationships are according to dos Reis et al. (2012) and O’Leary et al. (2013).

J. Exp. Zool. (Mol. Dev. Evol.)

EVOLUTION OF FEMALE ORGASM
orgasm-associated PRL peak has been observed also in males
(Bronson and Desjardins, ’82). This indicates a perhaps even
older function of synchronizing reproductive behavior with en-
vironmental conditions, which is not limited to one sex. PRL
may have been co-opted in this reproductive role, because its
expression is sensitive to photoperiod. Effect of PRL on ovula-
tion may thus itself have a precedent in a general gonadotropic
effect, which might have become co-opted for the ovulatory
impulse in females.
Oxytocin is another pituitary hormone whose expression has
been reported to be associated with human orgasm (Carmichael
et al., ’87; Blaicher et al., ’99), and vaginal stimulation in gen-
eral (Komisaruk and Steinman, ’86). The orgasm peak in periph-
eral plasma is quite low and its detection somewhat inconsistent
(Krueger et al., 2003), however the role of oxytocin in the reg-
ulation of ovarian cycle has been detected across species. The
ancestral role of oxytocin may have to do with ovulation and
associated oviducal contractions involved in propulsion of the
egg through the female reproductive tract (Guillette et al., ’91).
It is plausible that this pathway is related to the extant function
of oxytocin in emptying of the uterus at parturition, while be-
ing suppressed during pregnancy. Apart from well-documented
roles of oxytocin in eliciting myometrial contractions in labor
and lactation, the oxytocin signaling is involved in inducing
prostaglandin PGF2 α at ovulation (Viggiano et al., ’89). Oxy-
tocin signals via G-protein coupled oxytocin receptor, with dif-
ferent second messengers in different tissues. Indeed, oxytocin
receptor is expressed in ovarian granulosa cells during all stages
of follicular development (Saller et al., 2010), and oxytocin in-
jections during mouse estrous increased the volume of corpora
lutea 48 hr later (Roshangar et al., 2009). The experiments of
Copland et al. (2002) on human granulosa cell line suggest that
oxytocin augments the effect of luteotropins. Thus, also oxytocin
peak detected at orgasm may have been originally involved in
inducing ovulation and supporting the luteal phase.
Finally, an indirect indication of the endocrine role of cop-
ulation is a recommendation for several species to use addi-
tional stimulation during artificial insemination (e.g., for pigs:
https://www.daf.qld.gov.au). Thus, even in species in which ovu-
lation does not depend on copulation, stimulation still appears
to increase efficiency of insemination. Whether this is due to the
endocrine effects akin to luteotrophic PRL surge as is necessary
in rodents, or has other causes, is not known to us.
Overall, the evidence summarized above shows considerable
similarities between the orgasm induced hormonal changes in
women and the hormonal signals causing ovulation, in particu-
lar in copulation-induced ovulation. We interpret this evidence
to suggest that the physiological changes caused by human fe-
male orgasm are homologous to those that cause ovulation in
other species, likely going back to the most recent common an-
cestor of therian mammals (i.e., the ancestor of marsupials and
placental mammals).
7
FEMALE GENITAL ANATOMY IN INDUCED AND
SPONTANEOUS OVULATORS
In humans, the female orgasm often requires additional, non-
penile, clitoral stimulation, because the position of the clitoris
does not allow adequate stimulation during penetration. Vari-
ation in human female genital anatomy has been suggested
previously to be associated with the likelihood of reaching or-
gasm during intercourse. Wallen and Lloyd (2008) argued that
clitoral size variation is greater than penile size variation, in-
dicating that selection on female orgasm is weaker in compar-
ison to selection on male orgasm. This reasoning has been dis-
puted with an argument that clitoral volume rather than length
is an appropriate metric, however volume does not show the
same sexual dimorphism of variation as length (Lynch, 2008).
We maintain, however, that variation in the clitoral length may
in fact be more informative in the case of female orgasm. This
is because the longer clitoris reduces the distance to the vagi-
nal orifice (this distance is increased in primates), and thereby
influences the potential for stimulation during the intercourse
(see next). This is very different from the male phallus, which
is invariably stimulated during the intercourse and the length
may be less important. Indeed, the data collected by Bonaparte
(1924) and Landis (1940), and reanalyzed by Wallen and Lloyd
(2011), show that the distance between urethral orifice and cli-
toris is negatively correlated with the likelihood of reaching
orgasm during the intercourse. This is indicative of the im-
portance of clitoral position for the human female orgasm. It
should be noted that the size of the clitoris in mammals is
very sensitive to the androgen exposure during fetal develop-
ment (Cunha et al., 2014), which in its extreme form can man-
ifest as masculinized external (and internal) female genitalia—
as occurs occasionally in multiple species (“freemartins”; Smith
and Dunn, ’81; Braun et al., ’83; Padula, 2005; Drea and Weil,
2008), and are even the normal characteristics in some, as is best
known of hyena and fossa (Neaves et al., ’80; Hawkins et al.,
2002) and to some extent spider monkey (Dixson, 2012). As an-
drogen level may be affected by selection on its other func-
tions (for instance, aggression; French et al., 2013), the varia-
tion in clitoral length could certainly be affected indirectly as
well.
To examine the association of genital anatomy with differ-
ent types of ovarian cyclicity, we compared the female genital
anatomy across eutherians. If female orgasm is vestigial in spon-
taneous ovulators, but crucial in reflex ovulators, we expect to
see a signature in genital anatomical differences. We assume in
the following that the clitoris is the main source of the orgasm-
induced endocrine surge in all mammals, as it is in women, and
examine the clitoral position relative to genital orifice, to in-
fer the potential for clitoral stimulation during the intercourse
in various eutherian mammals. We note that there is a surpris-
ing scarcity of detailed comparative anatomical/developmental
descriptions of female genital anatomy across vertebrates (the
J. Exp. Zool. (Mol. Dev. Evol.)
8 PAVLIČEV ET AL.
information collected here can be found listed by species in Sup-
plementary Table S1).
The developmental origin of the clitoris is the same as that of
the penis, and thus suggesting a common evolutionary origin.
Phallus (penis or clitoris) is suggested to have a single origin
in amniotes and arises as an anlage on the ventral side of the
cloaca, which in males then evolved into the copulatory organ
and enabled internal fertilization (Gredler et al., 2015; Sanger
et al., 2015).
The evolution of female urogenital tract in mammals shows a
general trend toward increasing compartmentalization (Gegen-
baur, 1864; Starck, ’78). In basal lineages of mammals
(monotremes, Tasmanian devil, tenrec), genital, urethral, and
rectal canals are still united in a multifunctional cloaca with
a single opening, as is also the case in birds and reptiles. In most
other eutherian species, the separation of rectum from urogen-
ital channels prevails, however urethra still opens into either
the vagina itself, or into a common canal distally of the vagina
proper, the urogenital sinus—in both cases resulting in a sin-
gle urogenital orifice. For our question, both of these situations
are equivalent, as in both cases the clitoris, which is vaguely
associated with urethral opening, will be located more or less
inside of the copulatory canal, sometimes reaching out through
the orifice. Figure 2B shows the distribution of common (uro-
genital sinus or cloaca) orifices across placental mammals. In
relatively few species, including primates and some rodents, the
shortening of urogenital sinus proceeds to the effect that the
urethra becomes separated from the vagina, resulting in a sepa-
rate urethral orifice to the ventral side of the vaginal orifice. In
many primates, both openings are still part of a common slit, the
vestibulum vaginosis. This trend from common tract to the sepa-
ration of vaginal and urethral orifices is shown schematically in
Figure 3. Note that, in spite of the common developmental ori-
gin of male and female urogenital organs, the male and female
genitalia have diverged strongly, as male urethral and genital
canals are unified in a common canal in the penis, the urethra,
whereas such is only very rarely the case for female clitoris (e.g.,
hyaena).
As the genital and urethral orifices separate in primates and
rodents, the distance of the clitoris from the vaginal orifice in-
creases. This is because the clitoris is located anterioventrally to
the urethra and hence is associated with the urethra rather than
the vaginal orifice. Figure 2C shows the phylogenetic distribu-
tion of the position of clitoris relative to the vaginal orifice, being
inside of the copulatory canal, on the border, or at some distance,
outside. Note that the position of the clitoris and the type of
ovulation are roughly associated on the phylogenetic tree. The
outside position of the clitoris at a distance from vaginal ori-
fice is rare in eutherians and specifically derived within the pri-
mates. Its position on the outside in rodents appears surprising,
as rodents need copulatory PRL surge to establish pregnancy.
However, the rodent clitoris appears more similar to the penis in
J. Exp. Zool. (Mol. Dev. Evol.)
A R
U c CC
UGS
gc
B
B R
U c V
UGS
B gc
C R
U c
V
B
gc
D dorsal
R
anterior posterior
U c
V
B
ventral
gc
Figure 3. Schematic of the types of female genital anatomy,
showing the trend from common anal and urogenital opening in
the form of cloaca in (A); to separation of rectal opening and short-
ening of urogenital sinus in (B); to increasingly separated vaginal
and urethral orifices in (C) and (D). R, rectum; CC, cloaca; UGS,
urogenital sinus; U, uterus; V, vagina; B, bladder; gc, glans clitoris;
c, cervix.
size and while separated from vagina (Weiss et al., 2012), it is
likely stimulated during copulation. In contrast, in humans and
in particular other apes, the clitoris is small and removed from
the vagina. This situation is consistent with a vestigial func-
tion of clitoral stimulation during reproductive intercourse in
human and primates in general, and thus likely is the anatom-
ical basis for the inconsistent association between intercourse
and female orgasm, the so-called orgasm/intercourse discrep-
ancy (Lloyd, 2005).
To summarize, there is phylogenetic support that induced ovu-
lation in any form is ancestral to spontaneous ovulation. We
propose, in addition, that copulation-induced ovulation is an-
cestral to spontaneous ovulation and female orgasm in any
shape or form is homologous to the neuroendocrine reflex un-
derlying copulation-induced ovulation, and furthermore, that
copulation-induced ovulation is triggered by clitoral stimula-
tion (Fig. 4). In spontaneous ovulators, the role of clitoral stim-
ulation for ovulation became vestigial but maintained traces of
the ancestral neuroendocrine reflex even in humans. With the
evolution of spontaneous ovulation, clitoral stimulation lost its
EVOLUTION OF FEMALE ORGASM 9

environmental environmental environmental

signal signal signal

ovulation ovulation ovulation

copulation copulation copulation

fertilization fertilization fertilization

pregnancy pregnancy pregnancy

Figure 4. The model of the evolutionary change in the upstream mechanism inducing ovulation in mammals, starting with environmental
induction, copulatory induction, and finally spontaneous ovulation. Note that the potential for the effect of ancestral signal may be
maintained in some species.

role in ensuring fertilization simultaneously with the removal of extant induced ovulators are also associated with human or-
clitoris from the copulatory canal, likely causing a variable asso- gasm, and that of other spontaneous ovulators; (3) the morphol-
ciation between copulation and orgasms for the female. Clitoral ogy of the female genitalia suggests that the copulation in the
stimulation and female orgasm then possibly acquired secondary majority of clades induces clitoral stimulation, with the excep-
roles that are different from the ancestral ovulatory function. tion of primates, where clitoris is located at some distance from
vaginal orifice.
One may argue that the fact that the hormonal surges are still
CONCLUSION
detectable in spontaneous ovulators such as humans, may not
The model presented here offers a plausible explanation for
itself be sufficient to prove that they are the signature of the
the evolutionary origin of female orgasm, which is increasing
female (primate) orgasm. They could simply be a part of copu-
the likelihood of mating success in many nonhuman mammals.
lation itself. And this may in part be true, because in induced
Female orgasm did not evolve in the human lineage but may
ovulation, the copulation is consistently associated with stim-
have acquired additional roles after it became dispensable for
ulation of the clitoris. However, the fact that these surges are
ovulation, such as bonding or contractions, that are specific to
enhanced by the female orgasm, rather than general arousal, in-
the primate lineage (for discussion of hormonal exaptations,
dicates that the orgasmic peak is an important part of the mech-
see Ketterson and Nolan, ’99). However, its evolutionary origin
anism. The disconnect of copulation from clitoral stimulation,
is likely not explained by its current role in humans. Thus, we
which appears to coincide with anatomical changes in the pri-
note that the hypothesis that female orgasm may have evolved
mate lineage, is only possible when the ovarian cycle becomes
as an adaptation for a direct reproductive role, and the fact that
autonomous. This likely opened the potential to coopt the clitoris
it is not necessary in humans to conceive, are not contradictory
into new, primate- or human-specific roles.
at all. The effects of female orgasm in humans may not be
Finally, it is important to note that the extant species, both in-
clear, however if present, the extant effects of the trait are
duced and spontaneous ovulators, are themselves derived, and
not necessarily the functions for which the traits originated in
hence copulation-associated endocrine discharge might have ac-
the first place. Instead they can be new functions (as is well
quired additional characteristics and functions in these species
established for feathers, hair, or swim bladder, etc.), evolved as
as well, as the female orgasm likely did in our lineage. These
the traits have been co-opted into secondary adaptations (i.e.,
novel characteristics thus distinguish the extant traits and limit
exaptations; Gould and Vrba, ’82).
the comparability, and may also be what maintains the female
We suggest that the ancestral trait that evolved into human
orgasm presently.
female orgasm had an ancestral function in inducing ovulation:
the neuroendocrine reflex present in species in which ovulation
is dependent on physical stimulation during copulation, such as ACKNOWLEDGMENTS
rabbits or cats. Three main observations lead us to this conclu- The authors thank Drs. Elizabeth Lloyd, Marty Cohn, and Ron
sion: (1) induced ovulation evolved prior to spontaneous ovu- Amundson for helpful comments on a previous version of this
lation; (2) the pathways by which ovulation is induced in the paper. Research in the Pavlicev lab is funded by March of

J. Exp. Zool. (Mol. Dev. Evol.)

10
Dimes Prematurity Research Center Ohio Collaborative (grant
#22-FY14-470) and in the Wagner lab by the John Templeton
Foundation (grant #54860).
LITERATURE CITED
Ahmad E, Brooks JE, Hussain I, Khan MH. 1995. Reproduction in
Eurasian wild boar in central Punjab, Pakistan. Acta Theriologica
40:163–173.
Akers JS, Conaway CH. 1979. Female homosexual behavior in Macaca
mulatta. Arch Sex Behav 8:63–80.
Amundson R. 2008. Why don’t you write about something more in-
teresting, Lisa? Biol Philos 23:439–446.
Bakker J, Baum MJ. 2000. Neuroendocrine regulation of GnRH release
in induced ovulators. Front Neuroendocrinol 21:220–262.
Blaicher W, Gruber D, Bieglmayer C, Blaicher AM, Knogler W, Huber
JC. 1999. The role of oxytocin in relation to female sexual arousal.
Gynecol Obstet Invest 47:125–126.
Bogle OA, Ratto MH, Adams GP. 2011. Evidence for the conserva-
tion of biological activity of ovulation-inducing factor in seminal
plasma. Reproduction 142:277–283.
Bonaparte M. 1993. Les deux frigidités de la femme. Bulletin de la
Société de Sexologie 5:161–170.
Bouchie L, Bennett NC, Jackson T, Waterman JM. 2006. Are cape
ground squirrels (Xerus inauris) induced or spontaneous ovulators?
J Mammol 87:60–66.
Bradshaw WE, Holzapfel CM. 2007. Evolution of animal photoperi-
odism. Annu Rev Ecol Evol Syst 38:1–25.
Braun U, Forster M, Schams D. 1983. Freemartin syndrome in sheep.
Morphological, hormone-analytical and cytogenetic studies. Tier-
arztl Prax 11:293–302.
Broitman ST, Donoso AO. 1975. Modifications of post-coital LH se-
cretion and oestrous behaviour induced by drugs in ovariectomized
rats. J Reprod Fertil 44:309–312.
Bronson FH, Desjardins C. 1982. Endocrine responses to sexual arousal
in male mice. Endocrinology 111:1286–1291.
Carmichael MS, Humbert R, Dixen J, et al. 1987. Plasma oxytocin
increases in the human sexual response. J Clin Endocrinol Metab
64:27–31.
Carmichael MS, Warburton VL, Dixen J, Davidson JM. 1994. Relation-
ships among cardiovascular, muscular, and oxytocin responses dur-
ing human sexual activity. Arch Sex Behav 23:59–79.
Copland JA, Zlatnik MG, Ives KL, Soloff MS. 2002. Oxytocin receptor
regulation and action in a human granulosa-lutein cell line. Biol
Reprod 66:1230–1236.
Cunha GR, Risbridger G, Wang H, et al. 2014. Development of the
external genitalia: perspectives from the spotted hyena (Crocuta
crocuta). Differentiation 87:4–22.
Curlewis JD. 1992. Seasonal prolactin secretion and its role in sea-
sonal reproduction: a review. Reprod Fertil Dev 4:1–23.
Delcroix I, Mauget R, Signoret JP. 1990. Existence of synchronization
of reproduction at the level of the social group of the European
wild boar (Sus scrofa). J Reprod Fertil 89:613–617.
J. Exp. Zool. (Mol. Dev. Evol.)
PAVLIČEV ET AL.
Dixson AF. 2012. Primate sexuality: comparative studies of the
prosimians, monkeys, apes, and humans. Oxford: Oxford University
Press.
dos Reis M, Inoue J, Hasegawa M, et al. 2012. Phylogenomic datasets
provide both precision and accuracy in estimating the timescale of
placental mammal phylogeny. Proc Biol Sci R Soc 279:3491–3500.
Drea CM, Weil A. 2008. External genital morphology of the ring-tailed
lemur (Lemur catta): females are naturally "masculinized". J Mor-
phol 269:451–463.
Eisenberg JF, Gould E. 1970. The tenrecs: a study in mammalian be-
haviour and evolution. Smithsonian Contrib Zool 1–152.
Exton MS, Bindert A, Kruger T, et al. 1999. Cardiovascular and en-
docrine alterations after masturbation-induced orgasm in women.
Psychosom Med 61:280–289.
Exton MS, Kruger TH, Bursch N, et al. 2001a. Endocrine response to
masturbation-induced orgasm in healthy men following a 3-week
sexual abstinence. World J Urol 19:377–382.
Exton MS, Kruger TH, Koch M, et al. 2001b. Coitus-induced orgasm
stimulates prolactin secretion in healthy subjects. Psychoneuroen-
docrinology 26:287–294.
Freeman ME, Kanyicska B, Lerant A, Nagy G. 2000. Prolactin: struc-
ture, function, and regulation of secretion. Physiol Rev 80:1523–
1631.
French JA, Mustoe AC, Cavanaugh J, Birnie AK. 2013. The influence
of androgenic steroid hormones on female aggression in ’atypical’
mammals. Philos Trans R Soc Lond Ser B 368:20130084 (1–10).
Garcia JR, Lloyd EA, Wallen K, Fisher HE. 2014. Variation in orgasm
occurrence by sexual orientation in a sample of U.S. singles. J Sex
Med 11:2645–2652.
Gegenbaur C. 1864. Untersuchungen zur vergleichenden anatomie
der wirbelthiere. Leipzig: W. Engelmann.
Gould SJ, Vrba ES. 1982. Exaptation—a missing term in the science of
form. Paleobiology 8:4–15.
Gredler ML, Sanger TJ, Cohn MJ. 2015. Development of the cloaca,
hemipenes, and hemiclitores in the green anole, Anolis carolinensis.
Sex Dev 9:21–33.
Gudermuth DF, Newton L, Daels P, Concannon P. 1997. Incidence
of spontaneous ovulation in young, group-housed cats based on
serum and faecal concentrations of progesterone. J Reprod Fertil
Suppl 51:177–184.
Guillette LJ, Jr., Dubois DH, Cree A. 1991. Prostaglandins, oviducal
function, and parturient behavior in nonmammalian vertebrates.
Am J Physiol 260:R854–R861.
Hawkins CE, Dallas JF, Fowler PA, Woodroffe R, Racey PA. 2002. Tran-
sient masculinization in the fossa, Cryptoprocta ferox (Carnivora,
Viverridae). Biol Reprod 66:610–615.
Huynh HK, Willemsen AT, Holstege G. 2013. Female orgasm but
not male ejaculation activates the pituitary. A PET-neuro-imaging
study. Neuroimage 76:178–182.
Johnston SD, McGowan MR, O’Callaghan P, Cox R, Nicolson V. 2000.
Studies of the oestrous cycle, oestrus and pregnancy in the koala
(Phascolarctos cinereus). J Reprod Fertil 120:49–57.
EVOLUTION OF FEMALE ORGASM
Johnston SD, O’Callaghan P, Nilsson K, Tzipori G, Curlewis JD. 2004.
Semen-induced luteal phase and identification of a LH surge in the
koala (Phascolarctos cinereus). Reproduction 128:629–634.
Kauppila A, Martikainen H, Puistola U, Reinila M, Ronnberg L. 1988.
Hypoprolactinemia and ovarian function. Fertil Steril 49:437–441.
Kemp A. 1984. Spawning of the Australian lungfish, Neoceratodus
forsteri (Krefft) in the Brisbane River and in Enoggera Reservoir,
Queensland. Mem Qd Mus 391–399.
Ketterson ED, Nolan V. 1999. Adaptation, exaptation, and constraint:
a hormonal perspective. Am Nat 154:S4–S25.
Knobil E, Neill JD. 1988. The physiology of reproduction. New York:
Raven Press.
Knott KK, Roberts BM, Maly MA, et al. 2013. Fecal estrogen, pro-
gestagen and glucocorticoid metabolites during the estrous cycle
and pregnancy in the giant anteater (Myrmecophaga tridactyla):
evidence for delayed implantation. Reprod Biol Endocrinol 11:83–
96.
Komisaruk BR, Steinman JL. 1986. Genital stimulation as a trigger
for neuroendocrine and behavioral control of reproduction. Ann NY
Acad Sci 474:64–75.
Kruger TH, Haake P, Hartmann U, Schedlowski M, Exton MS. 2002.
Orgasm-induced prolactin secretion: feedback control of sexual
drive? Neurosci Biobehav Rev 26:31–44.
Kruger TH, Haake P, Chereath D, Knapp W, Janssen OE, Exton MS,
Schedlowski M, Hartmann U. 2003. Specificity of the neuroen-
docrine response to orgasm during sexual arousal in men. J En-
docrinol 177:57–64.
Landau IT, Holmes WG. 1988. Mating of captive thirteen-lined ground
squirrels and the annual timing of estrus. Horm Behav 22:474–487.
Landis C, Landis A, Bowles M. 1940. Sex in Development. New York:
P.B. Hoeber Inc.
Larsen CM, Kokay IC, Grattan DR. 2008. Male pheromones initiate
prolactin-induced neurogenesis and advance maternal behavior in
female mice. Horm Behav 53:509–517.
Laviriere S, Ferguson SH. 2003. Evolution of induced ovulation in
North American carnivores. J Mammal 84:937–947.
Leroi AM. 2014. The lagoon. How Aristotle invented science. New
York: Viking.
Lindburg DG. 1991. Ecological requirements of macaques. Lab Anim
Sci 41:315–322.
Lloyd EA. 2005. The case of female orgasm: bias in the science of
evolution. Cambridge: Harvard University Press.
Lynch VJ. 2008. Clitoral and penile size variability are not significantly
different: lack of evidence for the byproduct theory of the female
orgasm. Evol Dev 10:396–397.
Mah K, Binik YM. 2001. The nature of human orgasm: a critical review
of major trends. Clin Psychol Rev 21:823–856.
Mak GK, Enwere EK, Gregg C, et al. 2007. Male pheromone-stimulated
neurogenesis in the adult female brain: possible role in mating be-
havior. Nat Neurosci 10:1003–1011.
McNeilly AS, Tay CC, Glasier A. 1994. Physiological mechanisms un-
derlying lactational amenorrhea. Ann NY Acad Sci 709:145–155.
11
Moss RL, Cooper KJ. 1973. Temporal relationship of spontaneous and
coitus-induced release of luteinizing hormone in the normal cyclic
rat. Endocrinology 92:1748–1753.
Murphy BD. 1979. The role of prolactin in implantation and luteal
maintenance in the ferret. Biol Reprod 21:517–521.
Neaves WB, Griffin JE, Wilson JD. 1980. Sexual dimorphism of
the phallus in spotted hyaena (Crocuta crocuta). J Reprod Fertil
59:509–513.
Norris DO, Carr JA. 2013. Vertebrate endocrinology. Amsterdam: Aca-
demic Press, Elsevier.
Norris DO, Jones RE. 1987. Hormones and reproduction in fishes, am-
phibians, and reptiles. New York: Plenum Press.
O’Leary MA, Bloch JI, Flynn JJ, et al. 2013. The placental mammal an-
cestor and the post-K-Pg radiation of placentals. Science 339:662–
667.
Padula AM. 2005. The freemartin syndrome: an update. Anim Reprod
Sci 87:93–109.
Papke RL, Concannon PW, Travis HF, Hansel W. 1980. Control of luteal
function and implantation in the mink by prolactin. J Anim Sci
50:1102–1107.
Perret M, Schilling A. 1987. Role of prolactin in a pheromone-like
sexual inhibition in the male lesser mouse lemur. J Endocrinol
114:279–287.
Pomeroy WB. 1972. Dr. Kinsey and the Institute of Sex Research. New
York: Harper & Row.
Renfree MB, Shaw G. 2000. Diapause. Annu Rev Physiol 62:353–
375.
Roshangar L, Rad JS, Nikpoo P, Melli MS. 2009. Effect of oxytocin
injection on folliculogenesis, ovulation and endometrial growth in
mice. Iran J Reprod Med 7:91–95.
Saller S, Kunz L, Dissen GA, et al. 2010. Oxytocin receptors in the
primate ovary: molecular identity and link to apoptosis in human
granulosa cells. Hum Reprod 25:969–976.
Sanger TJ, Gredler ML, Cohn MJ. 2015. Resurrecting embryos of the
tuatara, Sphenodon punctatus, to resolve vertebrate phallus evo-
lution. Biol Lett 11:20150694.
Signoret JP, Du Mesnil du Buisson F, Mauleon P. 1972. Effect of mat-
ing on the onset and duration of ovulation in the sow. J Reprod
Fertil 31:327–330.
Smith MC, Dunn HO. 1981. Freemartin condition in a goat. J Am Vet
Med Assoc 178:735–737.
Starck D. 1978. Vergleichende Anatomie der Wirbeltiere auf evolu-
tionsbiologischer Grundlage. Berlin: Springer-Verlag.
Superina M, Jahn GA. 2009. Seasonal reproduction in male pichis Za-
edyus pichiy (Xenarthra:Dasypodidae) estimated by fecal androgen
metabolites and testicular histology. Anim Reprod Sci 112:283–
292.
Superina M, Carreno N, Jahn GA. 2009. Characterization of
seasonal reproduction patterns in female pichis Zaedyus
pichiy (Xenarthra:Dasypodidae) estimated by fecal sex steroid
metabolites and ovarian histology. Anim Reprod Sci 116:358–
369.
J. Exp. Zool. (Mol. Dev. Evol.)
12
Symons D. 1979. The evolution of human sexuality. Oxford: Oxford
University Press.
Taleisnik S, Caligaris L, Astrada JJ. 1966. Effect of copulation on the
release of pituitary gonadotropins in male and female rats. En-
docrinology 79:49–54.
Terkel J. 1988. Neuroendocrine processes in the establishment of
pregnancy and pseudopregnancy in rats. Psychoneuroendocrinol-
ogy 13:5–28.
Tremellen KP, Valbuena D, Landeras J, et al. 2000. The effect of in-
tercourse on pregnancy rates during assisted human reproduction.
Hum Reprod 15:2653–2658.
Van Horn RN. 1975. Primate breeding season: photoperiodic regula-
tion in captive Lemur catta. Folia Primatol (Basel) 24:203–220.
Vandenbergh JG. 1983. Pheromones and reproduction in mammals.
New York: Academic Press.
Viggiano M, Franchi AM, Zicari JL, et al. 1989. The involvement of
oxytocin in ovulation and in the outputs of cyclo-oxygenase and
5-lipoxygenase products from isolated rat ovaries. Prostaglandins
37:367–378.
J. Exp. Zool. (Mol. Dev. Evol.)
PAVLIČEV ET AL.
Wallen K, Lloyd EA. 2008. Clitoral variability compared with pe-
nile variability supports nonadaptation of female orgasm. Evol Dev
10:1–2.
Wallen K, Lloyd EA. 2011. Female sexual arousal: genital anatomy and
orgasm in intercourse. Horm Behav 59:780–792.
Weir BJ, Rowlands IW. 1973. Reproductive strategies of mammals.
Annu Rev Ecol Syst 4:139–163.
Weiss DA, Rodriguez E, Jr., Cunha T, et al. 2012. Morphology of the
external genitalia of the adult male and female mice as an endpoint
of sex differentiation. Mol Cell Endocrinol 354:94–102.
Zarrow MX, Clark JH. 1968. Ovulation following vaginal stimulation in
a spontaneous ovulator and its implications. J Endocrinol 40:343–
352.
Zarrow MX, Campbell PS, Clark JH. 1968. Pregnancy following coital-
induced ovulation in a spontaneous ovulator. Science 159:329–
330.
Zietsch BP, Santtila P. 2013. No direct relationship between human
female orgasm rate and number of offspring. Anim Behav 86:253–
255.