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 accompanies 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 selection 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 addition, 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.
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 (Aristotle, 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 particular without additional clitoral stimulation (reviewed extensively in Lloyd, 2005); the orgasm is in fact more common during 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 orgasm 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, 1979). A critical review of the existing hypotheses has been published in Lloyd (2005) and will not be attempted here.
Here, we note that most hypotheses are seeking an explanation for the presence of female orgasmwithin 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 focusing 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, 1982) 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 described 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 little has been found about its distribution. It is noteworthy that the byproduct hypothesis (Symons, 1979; 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 collaborators. In the collection of Kinsey`s unpublished research, Pomeroy (1972) reports correspondence between Kinsey and several 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 rabbit, all of which are reflex ovulators, as will be explained next.
More thorough descriptions of orgasm include psychological, 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 neuroendocrine 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 homologue 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 female 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 associated 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 reproductive biology, some core characteristics can be traced throughout 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, ovulation, 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 pituitary 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 cascade 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, 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 modified 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 extensive evolutionary changes is the upstream trigger of this process, that is, which stimulus causes the release of pituitary hormones leading to ovulation.
Figure 1.
The scheme of the ovarian cycle (CL, corpus luteum; see text).
Regulation of Receptivity
In many mammalian species, the potential to reproduce is restricted 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, 1975, macaques: Lindburg, 1991).
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, 1983), or the copulation itself, as in rabbits or cats (Bakker and Baum, 2000). Laviriere and Ferguson (2003) argued that not only partner-induced ovulation is adaptive because it ensures that ovulation coincides with the encounter of a mate, but it would also potentially enable the female 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 system in which females mate with multiple males (polyandry), is particularly common among these carnivores, supporting the association 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 mentioned above, many spontaneous ovulators also show seasonality, conditional on temperature or photoperiod. Degrees of modification of seasonality are well demonstrated in the animals kept under breeding conditions, either because of past selection 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 spontaneously ovulating species (see reports for mouse, rat, sow, sheep in Zarrow and Clark, 1968; Zarrow et al., 1968; Signoret et al., 1972). Potentially indicative of a role in inducing ovulation is an interesting preference in rhesus macaques for masturbation before the ovulation (Akers and Conaway, 1979). There are also reports to the opposite, namely that spontaneous ovulation sometimes occurs in induced ovulators (cats: Gudermuth et al., 1997). This overlap 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 limited 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 environmental cues (pheromones or photoperiod, rather than tactile stimulation), to spontaneous ovulators (Weir and Rowlands, 1973) may have been misleading. We will therefore distinguish three principle classes of ovulatory cycle regulation: externally induced, 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 ovulatory type. Ancestral status of external regulation of the ovarian cycle is also supported by the widespread effect of photoperiodism on reproduction (Bradshaw and Holzapfel, 2007), and the fact that environmental regulation of ovarian cycles predates internal fertilization: photoperiod and temperature regulate ovulation in teleost fishes (Khan and Thomas in Knobil and Neill, 1988), ovarian cycles of amphibians (Norris and Jones, 1987), and in lungfish (Kemp, 1984).
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 ovulation, for example, one in which a surge of gonadotropin is induced by the behavioral or pheromonal stimuli. The phylogenetic distribution of the male-induced and spontaneous ovulation is shown in Figure 2A. We included male pheromone induced ovulation in opossum as male-induced ovulation. Additional temperature/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).
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).
It should be noted that the male-induced ovulation is hard to establish with certainty in nature, and therefore its occurrence is likely underreported. For example, in addition to established cases, male-induced ovulation has been suggested in elephant seal, long-nosed kangaroo rat (marsupial), lump-nosed bat (Norris and Carr, 2013), and further species of ground squirrels (Landau and Holmes, 1988; 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 ovulation predated spontaneous ovulation (Keverne in Vandenbergh, 1983). The supporting evidence is that the copulation-induced ovulation is particularly common in the basal group of Eulipotyphla (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 ovulators, suggesting its ancestral primacy. According to modern 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 informative, including the copulation-induced ovulation in marsupials (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, 1970). This evidence supports the notion that male-induced ovulation is ancestral 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., 1999, 2001a, 2001b; Kruger et al., 2002; Huynh et al., 2013), LH (Exton et al., 1999), and oxytocin (Carmichael et al., 1987; Carmichael et al., 1994; Blaicher et al., 1999). Copulation-induced surges have been detected in other spontaneous ovulators: PRL and LH surges are known in rodents (Knobil and Neill, 1988). Interestingly, this pattern of PRL increase was detected in both sexes in mice (Bronson and Desjardins, 1982) as well as humans (Exton et al., 2001aa). In the case of LH, postcoital surge has been detected in rats (Taleisnik et al., 1966; Moss and Cooper, 1973) and its presence is associated with lordosis behavior, that is, indicating copulatory readiness in female rodents (Broitman and Donoso, 1975).
Most of the research on copulation-associated surges of pituitary hormones has been conducted in species in which an environmental stimulus is required for an aspect of the female ovarian 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.
In reflex ovulators, it is the copulation that induces a neuroendocrine 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 biochemical signals in seminal plasma play a role in camelids), and its pro-ovulatory effect may be conserved even in some spontaneous ovulators (Bogle et al., 2011). Tactile stimulation during coitus is mediated to central nervous system by the noradrenergic system (Terkel, 1988). 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 function 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 necessary for implantation in ferret, an induced ovulator (Murphy, 1979). This suggests that either the rodents maintained only the luteotroph aspect of PRL surge, or the pro-ovulatory function has been co-opted into the signal for prolonged luteal activity enabling 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 intercourse, 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 under 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 reproduction, and they may differ greatly between stages of the ovarian cycle (Freeman et al., 2000), including possible luteolytic and other inhibitory effects (e.g., inhibition of ovulation during lactation; McNeilly et al., 1994). In humans, the inhibitory effect of pathological hyperprolactinemia on folliculogenesis has been invoked to interpret the copulatory PRL surge as an adaptive signal inhibiting further copulatory behavior (Kruger et al., 2002). It is likely, however, that the inhibitory effect on ovulation 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 ovarian 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 ofPRL are also associated with shortened luteal phase of the ovarian cycle (Kauppila et al., 1988), 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 orgasm-associated PRL peak has been observed also in males (Bronson and Desjardins, 1982). This indicates a perhaps even older function of synchronizing reproductive behavior with environmental 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 ovulation 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., 1987; Blaicher et al., 1999), and vaginal stimulation in general (Komisaruk and Steinman, 1986). The orgasm peak in peripheral plasma is quite low and its detection somewhat inconsistent (Krueger et al., 2003), however the role of oxytocin in the regulation 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., 1991). It is plausible that this pathway is related to the extant function of oxytocin in emptying of the uterus at parturition, while being 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 PGF2α at ovulation (Viggiano et al., 1989). Oxytocin signals via G-protein coupled oxytocin receptor, with different 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 injections 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 copulation is a recommendation for several species to use additional stimulation during artificial insemination (e.g., for pigs:https://www.daf.qld.gov.au). Thus, even in species in which ovulation 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 particular in copulation-induced ovulation. We interpret this evidence to suggest that the physiological changes caused by human female orgasm are homologous to those that cause ovulation in other species, likely going back to the most recent common ancestor of therian mammals (i.e., the ancestor of marsupials and placental mammals).
FEMALE GENITAL ANATOMY IN INDUCED AND SPONTANEOUS OVULATORS
In humans, the female orgasm often requires additional, nonpenile, clitoral stimulation, because the position of the clitoris does not allow adequate stimulation during penetration. Variation in human female genital anatomy has been suggested previously to be associated with the likelihood of reaching orgasm during intercourse. Wallen and Lloyd (2008) argued that clitoral size variation is greater than penile size variation, indicating that selection on female orgasm is weaker in comparison to selection on male orgasm. This reasoning has been disputed 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 vaginal 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 clitoris is negatively correlated with the likelihood of reaching orgasm during the intercourse. This is indicative of the importance 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 development (Cunha et al., 2014), which in its extreme form can manifest as masculinized external (and internal) female genitalia—as occurs occasionally in multiple species (“freemartins”; Smith and Dunn, 1981; Braun et al., 1983; 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., 1980; Hawkins et al., 2002) and to some extent spider monkey (Dixson, 2012). As androgen level may be affected by selection on its other functions (for instance, aggression; French et al., 2013), the variation in clitoral length could certainly be affected indirectly as well.
To examine the association of genital anatomy with different types of ovarian cyclicity, we compared the female genital anatomy across eutherians. If female orgasm is vestigial in spontaneous 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 infer the potential for clitoral stimulation during the intercourse in various eutherian mammals. We note that there is a surprising scarcity of detailed comparative anatomical/developmental descriptions of female genital anatomy across vertebrates (the information collected here can be found listed by species in Supplementary 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 (Gegenbaur, 1864; Starck, 1978). 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 urogenital 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 single 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 (urogenital 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 separate 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 separation of vaginal and urethral orifices is shown schematically in Figure 3. Note that, in spite of the common developmental origin 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).
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 shortening 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.
As the genital and urethral orifices separate in primates and rodents, the distance of the clitoris from the vaginal orifice increases. 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 distribution 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 orifice is rare in eutherians and specifically derived within the primates. 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 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 function of clitoral stimulation during reproductive intercourse in human and primates in general, and thus likely is the anatomical basis for the inconsistent association between intercourse and female orgasm, the so-called orgasm/intercourse discrepancy (Lloyd, 2005).
To summarize, there is phylogenetic support that induced ovulation in any form is ancestral to spontaneous ovulation. We propose, in addition, that copulation-induced ovulation is ancestral to spontaneous ovulation and female orgasm in any shape or form is homologous to the neuroendocrine reflex underlying copulation-induced ovulation, and furthermore, that copulation-induced ovulation is triggered by clitoral stimulation (Fig. 4). In spontaneous ovulators, the role of clitoral stimulation 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 role in ensuring fertilization simultaneously with the removal of clitoris from the copulatory canal, likely causing a variable association between copulation and orgasms for the female. Clitoral stimulation and female orgasm then possibly acquired secondary roles that are different from the ancestral ovulatory function.
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.
CONCLUSION
The model presented here offers a plausible explanation for the evolutionary origin of female orgasm, which is increasing the likelihood of mating success in many nonhuman mammals. Female orgasm did not evolve in the human lineage but may have acquired additional roles after it became dispensable for ovulation, such as bonding or contractions, that are specific to the primate lineage (for discussion of hormonal exaptations, see Ketterson and Nolan, 1999). However, its evolutionary origin is likely not explained by its current role in humans. Thus, we note that the hypothesis that female orgasm may have evolved as an adaptation for a direct reproductive role, and the fact that it is not necessary in humans to conceive, are not contradictory at all. The effects of female orgasm in humans may not be clear, however if present, the extant effects of the trait are not necessarily the functions for which the traits originated in the first place. Instead they can be new functions (as is well established for feathers, hair, or swim bladder, etc.), evolved as the traits have been co-opted into secondary adaptations (i.e., exaptations; Gould and Vrba, 1982).
We suggest that the ancestral trait that evolved into human 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 rabbits or cats. Three main observations lead us to this conclusion: (1) induced ovulation evolved prior to spontaneous ovulation; (2) the pathways by which ovulation is induced in the extant induced ovulators are also associated with human orgasm, and that of other spontaneous ovulators; (3) the morphology of the female genitalia suggests that the copulation in the majority of clades induces clitoral stimulation, with the exception of primates, where clitoris is located at some distance from vaginal orifice.
One may argue that the fact that the hormonal surges are still detectable in spontaneous ovulators such as humans, may not itself be sufficient to prove that they are the signature of the female (primate) orgasm. They could simply be a part of copulation itself. And this may in part be true, because in induced ovulation, the copulation is consistently associated with stimulation of the clitoris. However, the fact that these surges are enhanced by the female orgasm, rather than general arousal, indicates that the orgasmic peak is an important part of the mechanism. The disconnect of copulation from clitoral stimulation, which appears to coincide with anatomical changes in the primate lineage, is only possible when the ovarian cycle becomes autonomous. This likely opened the potential to coopt the clitoris into new, primate- or human-specific roles.
Finally, it is important to note that the extant species, both induced and spontaneous ovulators, are themselves derived, and hence copulation-associated endocrine discharge might have acquired additional characteristics and functions in these species as well, as the female orgasm likely did in our lineage. These novel characteristics thus distinguish the extant traits and limit the comparability, and may also be what maintains the female orgasm presently.
ACKNOWLEDGMENTS
The authors thank Drs. Elizabeth Lloyd, Marty Cohn, and Ron Amundson for helpful comments on a previous version of this paper. Research in the Pavlicev lab is funded by March of Dimes Prematurity Research Center Ohio Collaborative (grant #22-FY14-470) and in the Wagner lab by the John Templeton Foundation (grant #54860).
