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A brief natural history of the orgasm Thierry Lodé

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Thierry Lodé. A brief natural history of the orgasm. Frontiers in Life Science , Taylor and Francis, 2020, 13 (1), pp.34-44. ￿10.1080/21553769.2019.1664642￿. ￿hal-02285727￿

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A brief natural history of the orgasm

Thierry Lodé

To cite this article: Thierry Lodé (2020) A brief natural history of the orgasm, Frontiers in Life Science, 13:1, 34-44 To link to this article: https://doi.org/10.1080/21553769.2019.1664642

© 2019 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group

Published online: 12 Sep 2019.

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Full Terms & Conditions of access and use can be found at https://www.tandfonline.com/action/journalInformation?journalCode=tfls20 FRONTIERS IN LIFE SCIENCE 2019, VOL. 13, NO. 1, 34–44 https://doi.org/10.1080/21553769.2019.1664642

PERSPECTIVE A brief natural history of the orgasm

Thierry Lodé

Laboratoire d’Éthologie Animale et Humaine EthoS–UMR-CNRS 6552, Université de Rennes 1, Rennes, France

ABSTRACT ARTICLE HISTORY Why the sexual climax, in , results in a pleasurable experience remains an important biolog- Received 29 April 2019 ical question. Analysis of evolutionary traits in numerous Vertebrates suggests that orgasm evolved Accepted 27 August 2019 through three phylogenetic stages during the transition from external to internal fertilization and KEYWORDS . First, orgasm is directly dependent on ejaculation in males and the expulsion of fluids Orgasm; ovarian fluids; mate from the ovarian and urethral glands (Skene’s) in . I propose that sexual orgasm could come choice; post-copulatory from the primitive reflex of discharging to ensure reproduction. Thus, the understanding selection; sexual conflict; of orgasm should not be reduced to a - or a clitoris-centred paradigm. Secondly, orgasm has unrelated males evolved to stimulate sexual activity because the evolutionary transition from to internal fertilization has been accompanied in numerous with a lessening in reproductive rates. Because sexual activity encourages reproduction, it can be argued that orgasm has evolved to increase sexual activity, particularly in viviparous species with low reproductive rates. Third, internal fertilization in the genital tract of females weakens the visibility of the putative success of fertiliza- tion. sexual fluids and proteins can bias fertilization in favour of preferred males. Because orgasm could promote a better choice of partner, I argue that female orgasm may have evolved as a post-copulatory selection tactic by which females can increase their control of mates.

Introduction blood pressure, increased heart rate, rhythmic respi- Why the sexual climax, in humans, leads to the experi- ratory pattern, involuntary body movements and, in ence of pleasure remains an important biological ques- females, by spontaneous colour changes of the labia tion.Whilethemalecannottransfergameteswith- minora which engorge to twice their size, and by out experiencing an orgasm, in the species, vaginal and anal spasms (Masters and Johnson 1966; the female orgasm seems completely decoupled from Berman et al. 1999). The orgasm is directed by the reproduction (Cabanac 1971;Hrdy1996;Wallenand autonomic nervous system and the spinal cord but Lloyd 2008). Although orgasm could result from the activates numerous cortical zones through the vagus point that individuals with an orgasm are more suc- nerves mediation (Komisaruk et al. 2004). cessful, Wheatley and Puts (2015) argued that there is Although the definition of orgasm is rather uncer- actually little evidence to suggest that female orgasm tain, Bancroft (2005) described it as ‘a state motivated canpromoteabetterreproduction.Iforgasmhada toward the experience of sexual pleasure’. In males, selective role, then it is difficult to understand why it is associated with ejaculation and rhythmic muscle females show such variability in their ability to reach contractions of the perineal muscles, in females, with a climax. Analysing the evolutionary history of the clitoral retraction, rhythmic muscle contractions of the sexual climax from its phylogenetic origin, we can perineum and . Orgasm also releases some neu- draw some new conclusions that can shed light on the ropeptides, dopamine, oxytocin and prolactin, which function of orgasm. cause a deep sense of well-being. Here, orgasm is Indeed, orgasm could only be regarded as a direct defined as the culmination of sexual arousal activating selective trait if individuals with this evolutionary trait the reward circuit. The increase in dopamine, oxy- have the best reproduction. Associated with ejacula- tocin and prolactin concentration can, therefore, be tion in males, orgasm is characterized by changes in considered as a signal of sexual arousal. All

CONTACT Thierry Lodé [email protected] Laboratoire d’Éthologie Animale et Humaine EthoS–UMR-CNRS 6552, Université de Rennes 1, 35042 Rennes, France © 2019 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. FRONTIERS IN LIFE SCIENCE 35 have the physiological capacity for orgasm (Fox and Puts 2015)sincefemaleorgasmsdonotappearto Fox 1971) and numerous vertebrates are known to have an active role in transport during coitus experience orgasm-like states such as primates i.e. (Levin 2011). Nonetheless, cervical excitations pro- bonobo, chimpanzee, gorilla, orangutan, proboscis duce contractions of the oviduct and fallopian tubes monkey, macaques (Chevalier-Skolnikoff 1974;Allen (Komisaruk et al. 2004), probably via prostaglandins and Lemon 1981; Troisi and Carosi 1998;Murai2006; and are essential for sperm transport and fertiliza- de Waal 2011; Grueter and Stoinski 2016), carnivores tion (Adler 1969;AdlerandZoloth1970; Wildt et al. and rodents (Adler 1969;HeebandYahr1996;Coolen 1998). et al. 1997;Kollack-WalkerandNewman1997;Tenk The second theory claims that female orgasm has et al. 2009;PavlicevandWagner2016), and rep- no selective role and must be understood as a simple tiles (Cabanac 1971; Winterbottom et al. 1999;Balland by-product of ontogenesis since the embryonic devel- Balthazart 2011)andfishes(PeterssonandJarvi2001). opmentofthemalepenisandfemaleclitorisremains It has even been demonstrated that ejaculation pro- very comparable (Symons 1979;Gould1987;Wallen voked by the activation of Crz-expressing neurons is and Lloyd 2008). rewarding to male flies (Zer-Krispil et al. 2018). Thus, orgasm seems a critical component of reproductive Phylogeny of the orgasm process for many species (Balcombe 2009). There are two main theories that provide an expla- Nevertheless,itseemsquiterelevanttoestimatethe nation for the manifestation of orgasm. It has been role of orgasm by analysing how orgasm phyloge- firstly hypothesized that orgasm would favour the per- netically developed during the evolution of sexual sistence of bonds to ensure the best care for the off- behaviour. Analysis of evolutionary traits suggests that spring (Alcock 1987) or serve as a secondary rein- orgasm evolved through three phylogenetic stages dur- forcement linking sexual behaviours and partner affil- ing the transition from external to internal fertilization iation (Prause 2011;Fleischman2016). However, in and viviparity. many species, the male provides virtually no care to First, because the orgasm is also associated with the young, which reduces the interest in this hypothe- ejaculation in males and with orgasmic expulsions sis. Moreover, the strengthening of the couple’s bonds from ovarian and urethral glands in females, I rea- is clearly refuted by the Coolidge effect (Brown 1974), soned that the sexual orgasm could originate from which leads many males, and to a lesser extent some the ancestral reflex of gametes release in both . females (Lester and Gorzalka 1988), to increase sexual has been found to be the most common repro- activity by adopting a greater diversity of partners. In ductivemodeamongeukaryotes.Originallybasedon monkeys, females that mated with high-ranking males , it has been hypothesized that sex could come showed the highest frequency of orgasms (Zumpe from very archaic interactions among ‘libertine bub- and Michael 1968; Chevalier-Skolnikoff 1974), sug- bles’, i.e. practising horizontal gene exchanges (see gesting a role in partner preference. Finally, among Lodé 2011). Eukaryotic lineages evolved from ances- thehypothesestendingtointerpretorgasmasarepro- tors that progressively developed male and female roles ductive enhancing effect, it has been assumed that (Crews 1982)insuchawaythatsexualityresulted female orgasm would have evolved for the selection from a series of small evolutionary changes since the ofapartner,thusenhancingthechanceofthebest primeval sexual interaction of gene transfers (Lodé fertilization (Thornhill et al. 1995). Thus, Fox et al. 2011, 2012a, 2013). Subsequently, the sexual chromo- (1970) hypothesized that the orgasmic spasms cause somes appeared independently and repeatedly, allow- contractions that may endorse sperm retention in the ing a chromosomic determination of the sexual gen- female genital tract, thus increasing the probability of der. Thus, initiated by the primitive genetic interac- fertilization. Fertilization of male gametes is stimu- tions of the very first protoeukaryotic organisms (Lodé lated by rhythmic contractions of the striated mus- 2011), the evolution of sexuality would be caused by a cles during orgasm (Levin 2002;Mestonetal.2004; succession of small events, more or less independent King et al. 2016). The allegation that female orgasms of each other, from genetic exchanges and recombi- may increase conception and progeny remains con- nation, from external fertilization, then from internal troversial (Zietsch and Santtila 2013;Wheatleyand to . 36 T. LODÉ

Many vertebrates seem to experience numerous mely comparable between teleostei, , rep- characteristic manifestations of an orgasm during their tiles, birds and mammals. Moreover, notable dopamin- copulatory activity (Fox and Fox 1971;Gould1987; ergic and mesolimbic neuronal circuits regulating sex- Balcombe 2009). Females Macaca mulatta have been ual behaviour exist in early vertebrates (O’Connell and found to reach orgasms after artificial vaginal stim- Hofmann 2011). ulations (Burton 1971). Zumpe and Michael (1968) There is no reason to suppose that the intromission also noted pelvic movements in female (Macaca rhe- organsarenecessarytoobtainasexualclimax.Inbirds, sus) and some mammals such as dogs, cats, guinea for instance, the muscular contractions of the pigs, hamsters, gerbils, ferrets and rats are known to drive into the reproductive tract. In most verte- be stimulated by frictional means (Heeb and Yahr brates with external fertilization, basic reflex contrac- 1996; Troisi and Carosi 1998;Pfausetal.2016). In tions accelerate release, promoting the velocity mammals, orgasm is accompanied by prostate dis- of spermatozoids and expelling ova into water (Cooke charge in males and release of the para-urethral glands et al. 2001).Malesoftenbuildnestsandcompeteto [Guérin/Skene’s] in females, suggesting a similar role attract females to lay their in the nests (Gross and ingametereleaseinbothsexes.Infemales,coitus Charnov 1980;Ridgwayetal.1989). In females, the causes a hormonal discharge and climax is accompa- musclesoftheoviductandthoseofthebodywallcon- nied by vaginal spasms and contractions of the uterus tract causing the ova to move through the oviduct until (Zumpe and Michael 1968; Fox and Fox 1971;Health total expulsion onto the substrate. In males, sperm is 1984;Erskineetal.1989; Bancroft 2005;BallandBalt- expelled onto the ova by repeated muscular contrac- hazart 2011). tions but survive only a few minutes, during which In fact, most species of vertebrates have devel- the fertilization occurs, may be stimulated by chemi- oped sensitive organs and organic receptors linked to cals. A large amount of fluid is secreted by numerous the ‘nervous circuit of reward’ (Figure 1). Many ani- glands and this reflex implies concomitant rhythmic mals have nuclear habenulae, which control reward contractions of the pelvi-perineal muscles in the two improvement mechanisms, usually associated with sexes. pleasure (Loonen and Ivanova 2015). Similarly, the Although stimulation of the sexual organs trig- neurochemicalprofilesofventralpallidumareextre gersit,orgasmischaracterizedbyasuddenrelease

Figure 1. Simplified scheme of neural circuits of reward in the rat brain. Reward and pleasure are generated by a set of hedonic hotspots within mesocortilimbic dopamine circuit, especially from nucleus accumbens, which controls the release of dopamine from the ventral tegmental area. Beta-endorphins are released by pituitary glands. Orgasm is experienced when genitalia provokes nervous excitations towards spinal cord and brain (from Berridge and Kringelbach 2015 adapted). FRONTIERS IN LIFE SCIENCE 37 of genital fluids. Ejaculation is the most rewarding in required two exaptations, the evolution of component of male sexual behaviour in rats, Syrian internal fertilization and a process of retention (see hamsters and gerbils (Heeb and Yahr 1996;Kollack- Kalinka 2015 for a detailed analysis). Internal fertiliza- Walker and Newman 1997;Tenketal.2009). The tion in the genital track of females developed in the argument that the orgasm comes from the ances- Late Ordovician from the retention of ova. tral reflex of gamete release is all the more plausi- The evolutionary interest of the internal fertiliza- blebecausetheorgasmisaccompaniedbyejacula- tion mode is to facilitate a terrestrial way of life while tion in males and by fluids from ovaries and from maintaining gametes in a liquid medium. On the other para-urethral glands in females. A discharge of the hand, internal fertilization requires either indirect prostate typifies male orgasm, but in females, orgasm insemination, through a or by cloacal is associated by a release of homologous para-urethral orvaginalcoupling.Themoveofspermatozoidsinto glands, the Guérin–Skene’s glands, when stimulated the ejaculatory ducts results from the smooth mus- from inside the vagina, evoking an identical func- cle contractions associated with abundant secretions of tion in both sexes (Tepper et al. 1984). Fluid secre- fluids which product a pressure propelling the sperm tion by the female glands reveals ejaculatory function forward. Similarly, the release of ova is assisted by equivalent to that of the male (Health 1984;Korda the secretion of ovarian fluids. The luteinizing hor- et al. 2010). Skene’s glands produce the same type mone has an important role for the release of gametes. of fluid, including enzymes and proteins, as prostate Pituitary activation produces higher plasma concen- fluid with lower levels of creatinine, but they have high trations of oxytocin and prolactin (Huyunh et al. 2013) levels of prostate specific antigen, prostatic acid phos- and luteotrophic factor stimulates the vacated folli- phatase and glucose, and it is believed that both work cle to secrete progesterone. These hormones can have inthesameway.Orgasmtriggersmanyneurohormone a role in inducing vaginal and uterus movements, secretions such as oxytocin, dopamine, prolactin and ovulation and improving sperm and egg transport endorphins. Dopamine is at the heart of the mesolim- (Wildt et al. 1998). An increase in prolactin levels bic reward system and the contribution of dopamine has been demonstrated during orgasm (Krüger et al. to the accumbens nucleus is decisive for reward associ- 2002;Haakeetal.2003; Huyunh et al. 2013). Similarly, ated behaviour (Yamamoto and Vernier 2011; Berridge testosterone, estradiol and progesterone are known to and Kringelbach 2015; Loonen and Ivanova 2015). In modulate reward processing. fact, there is no objective reason why sexuality Thus, the behaviour of the male and the female should be disconnected from a positive experience and helps to synchronize the maturation and release of no physiological element contradicts the hypothesis sperm and eggs for fertilization to occur. Precisely, that stimulation of the genitals can lead to an orgasm the evolutionary development of many intromittent in many vertebrates, including mammals, birds and organs in males (Figure 2) – such as gonopodium, (Cabanac 1971; Balcombe 2009;BallandBalt- phallodeum, hemipenis, pseudo-penis and penis – hazart 2011). allowing internal fertilization and directly involved in Thus, far from being limited to sexual organs, the orgasm, finds a homologue in the development orgasm may be directly related to the strong expul- of grooved tubercle in females as a rudimentary cli- sion of prostate fluids and para-urethral glands in toral structure also implicated in the orgasm (Cibrian- both males and females, suggesting an ancestral role Llandera et al. 2010)aswellinfish,asinreptiles, of orgasm in gamete emission. birdsormammals.Thus,themalesofBuffaloweavers (Bubalornis sp.) possess a phalloid organ that gener- ates an orgasm-like state (Winterbottom et al. 1999). Evolution of sexual behaviour and fertilization Such a development of specialized organic structures, Secondly, the evolutionary passage from external fer- therefore, supports my hypothesis of a primitive origin tilization (ovuliparity and external fertilization) to of orgasm linked to the basic reflex of gamete expul- the retention of the ova (internal fertilization) con- sion,bothinmalesandfemales,thuscouldconstitute tinued with egg retention and internal embryonic a convergent evolution. development (, histotrophic and hemotrophic In recent work, Pavlicev and Wagner (2016)devel- viviparity, see Lodé 2012b). The evolution of viviparity oped an analysis of induced ovulation and clitoral 38 T. LODÉ

Figure 2. Occurrences and types of intromittent organs in males according to phylogenetic relationships. orgasm development. These authors present a new rodents, ejaculation was found to have greater reward- phylogenetic scenario in eutherian mammals based ing properties than intromissions (Heeb and Yahr on the distance from the clitoris to the vaginal ori- 1996;Kollack-WalkerandNewman1997;Tenketal. fice, which increases with the evolution of spontaneous 2009). Moreover, even in that perform exter- ovulation. This is because the longer clitoris reduces nal fertilization, the use of a muscle reflex to expel the distance to the vaginal orifice, and thereby influ- fluidsandgametesisrequiredinbothmalesand ences the potential for stimulation. Genital organs are females (Gross and Charnov 1980). Internal fertiliza- formed from the same undifferentiated embryonic tis- tion does not depend on intromittent organs and could sues, resulting in the clitoris and penis (Wallen and be achieved through a strong expulsion of sperm, Lloyd 2008), and leading to the conceptual dominance which suggests that the evolutionary significance of of a kind of a ‘penis or clitoris-centred paradigm’. orgasm should not be limited to a ‘penis-centred’ or By influencing the time between orgasm and ovula- a ‘clitoris-centred’ paradigm. The orgasmic response tion, due to egg retention, the evolution of internal is characterized by a strong prostate flow in men and, fertilization would have favoured the appearance of in women, Skene glands and ovarian fluids are known orgasm in eutherian mammals. In developing this new to participate in the sperm nutrition process and to clitoris-centred theory, Pavlicev and Wagner (2016) accelerate sperm velocity (Urbach et al. 2005;Santos suggest that female orgasm may come from the reflex and Taboga 2006;Gasparinietal.2010). Antimicro- which, ancestrally, induces spontaneous ovulation in bial compounds and many other secretion products eutherian mammals. from ovarian fluids and para-urethral glands promote Nonetheless, by emphasizing clitoral arousal, this greater receptivity of females to coitus at a higher theory is based stimuli of the sexual organs alone. frequency (Moalem and Reidenberg 2009). These penis- or clitoris-centred theories, therefore, Indeed, during the evolution towards internal fertil- tend to consider that the clitoris functions as a reduced ization, many species have seen their reproduction rate penis, suggesting that vertebrates without intromis- decrease in favour of protecting embryonic develop- sion organs could not experience a sexual climax. In ment. Over the course of evolution, many species have females, Kraus’ corpuscles innervate both the clitoris associated internal fertilization with a range of organic andthevagina,sothatitisdisputabletodifferenti- procedures that protect the intrauterine development ate clitoral orgasm from vaginal orgasm (Pfaus et al. of their offspring. But species that have developed a 2016) although most women experience positive cli- reproduction by internal fertilization have seen a sig- toralexcitations.Thepenisisaspecializedstructure nificant decrease in their offspring. These species have that is involved in gamete transfer and micturition then compensated for this lessening in their progeny butitcanalsobecomeerectforotherreasons.In by promoting greater ease in multiplying copulations. FRONTIERS IN LIFE SCIENCE 39

At the same time, the sexual climax has evolved to pro- of sperm in the female spermatheca, as in salaman- mote reproductive performance in low reproductive ders, also facilitated post-copulatory rate species because they need to have high frequency to occur (Houck and Schwenk 1984). It is difficult to . Non penetrative sexual behaviour, determine the evolutionary response of males to such masturbation or same-sex sexual behaviour are com- cryptic behaviours, but, over the course of mon in a wide range of species, including mammals, evolution, it could be hypothesized that males should birds, reptiles and amphibians (Balcombe 2009;Ball have developed contact behaviours such as amplexus and Balthazart 2011). Further in humans, most homo- or cloacal kiss as a response to these false orgasms sexual men could also reach orgasm by stimulating delivering no or too few eggs to fertilize, leading to the the prostate during anal sex, demonstrating the role of evolutionary development of internal fertilization. fluid discharge in achieving orgasm. It is likely that the Male and female orgasms may originate from the achievement of non-genital orgasms is derived from evolution of fertilization modes but have hence fol- genital orgasms. The sexual climax being accompanied lowed different evolutionary pathways. It could be sus- by a sense of pleasure provides sufficient gratification pected that the evolutionary pathway from external to to engage in non-reproductive actions such as anal internal fertilization, which presupposes retention of or oral sex, masturbation and homosexual behaviour ovainthefemalegenitaltract,mayhaveledtoachange (Dagg 1984;MacFarlaneetal.2010). In any case, it that dissociates the signal from the reflex expulsion of seems that the sexual climax has evolved by promoting gametes. Indeed, pre-existing traits are known to pro- the multiplication and intensity of sexual activity. duce new effects without any apparent change affecting them, constituting what Gould and Vrba (1982)called an exaptation. In species with internal fertilization, the A mechanism of post-copulatory selection disconnection between ovulation and the sexual sig- Third, internal fertilization in the genital tract of nal may allow the female to defer her mate choice so females makes ovulation invisible, masking the poten- that it results in a selective runaway. The drift of the tial success of fecundation. The assumption that sexual signal could, therefore, give the sexual climax a orgasm promotes a better reproduction is arguable, new meaning for its evolutionary maintenance, at least especially given that orgasms are not necessary for in spontaneous ovulators (see Pavlicev and Wagner fecundation to take place. Nevertheless, because it 2016), since the female orgasmic signal is dissociated could promote better mate choice, it could be argued from the gamete release. Sexual selection can drive thatfemaleorgasmhasevolvedasapost-copulatory important evolutionary changes and could influence selection tactic by which females can increase their spermatozoid morphology (Rowe et al. 2015), devel- control of mates. opment of baculum (Brindle and Opie 2016)orpenis Mate preferences may be due to active female choice morphology for instance (Bertin and Fairbairn 2005; andmale-malecompetition,andmaybeduetopost- Mautz et al. 2013). Post-copulatory sexual selection copulatory mate choice, with cryptic female choice occurs after successful and insemination and sperm competition. In most species using exter- via two main processes: sperm competition and cryp- nal fertilization, often depends on the female’s tic female choice (Olsson et al. 1996;Arnqvist1998). willingnesstomate,whileinmanyspeciesusinginter- Both of these processes require that a female have nal fertilization, male coercive behaviours were widely multiple mates. demonstrated. Spawning is an external gamete release Post-copulatory sexual selection promotes a rapid method that easily allows post-copulatory selection to evolutionary diversification of sexual signals. In fact, occur (Alonzo et al. 2016).Femalesofteleostfishescan phenotypic differences in males and females often control the numbers of eggs laid (Alonzo et al. 2016). resulted in sexually antagonistic coevolution (Rice They also present a ‘false orgasm’, demonstrating all 2000). Sexual conflicts over mating lead to an antago- the patterns of the spawning behaviour, without lay- nistic coevolution, in which one sex develops a benefi- ing in the nest where the male spills out his sperm cial trait that is compensated by an opposite trait in the (Ridgway et al. 1989; Petersson and Jarvi 2001). Such other sex. Models of coevolution by sexual selection misleading behaviours reveal that orgasm can be a sig- can broadly be classified into those where the female nalusedtomanipulatemales.Asexpected,thestorage preference is favoured indirectly and those where it 40 T. LODÉ is favoured directly (Chapman et al. 2003). Over the optional in many species, including humans, its role course of the evolutionary history of some groups, it in choosing a better mating and avoiding inbreed- couldbearguedthat,whenthemaleshadintromission ing has yet to be determined. Nonetheless, in the organs, the females began to be subjected to more coer- absence of visible competition between males, it would cion. So, the development of sexual conflict would have potentially allow the female to assess the quality of allowed females to dissociate the orgasmic signal asso- the partner. It is likely that genetic elements indi- ciated with ovulation, thus promoting the possibility of cating the quality of the partner could be sought in post-copulatory sexual choice. theunrelatedandinthedifferenceorcomplemen- Ovarian fluids influence sperm behaviour and play tarity of their MHC/HLA system (Bruford and Jor- an important role in sperm selection by females dan 1998; Eklund 1998;Penn2002). Indeed, ovar- (Alonzo et al. 2016). In many species, ovarian fluids ian fluids are capable to bias fertilizations for unre- released with eggs provide gamete-recognition pro- lated males in some (Swanson and Vacquier teins (Vacquier 1998;SwansonandVacquier2002). 2002; Gasparini and Pilastro 2011)andinhensGallus Recent evidences show that fluids and proteins can gallus, phenotypic indices help females to discrimi- bias fertilization in favour of preferred males in species nate among unrelated males, but post-mating cryptic with external fertilization (Urbach et al. 2005;Rosen- choice strategies are mainly based on MHC dissimi- grave et al. 2008;Gasparinietal.2010;Alonzoetal. larity (Gillingham et al. 2009;Løvlieetal.2013). In 2016) so that these fluids allow opportunities for cryp- duck, Anas platyrhynchos, female sperm selection acts tic female choice. In mammals, such as in otters, as a mechanism of inbreeding avoidance (Denk et al. badgers or rodents, the probability of superfoetation 2005)andSetchell et al. (2011)pointedoutthatthe makespossibletomultiplypairings(Yamaguchietal. olfactory profile is related to MHC dissimilarity and 2006;Annavietal.2014), hence allowing the female pedigree relatedness in mandrill, Mandrillus sphinx, to use orgasm as a selective choice of the partner. Fur- providing a potential mechanism for selective mate thermore, in all mammalian species, spermatozoa are choice. Dissimilarities in MHC are also involved in stopped in the caudal isthmus before ovulation to form sexual choice in numerous animals, from tunicates to anoviductalspermreservoir.Thefactthatovarian salmonids for instance (Scofield et al. 1982;Skarstein fluids can influence the sperm velocity of unrelated et al. 2005). males (Rosengrave et al. 2008; Gasparini and Pilastro One could, therefore, consider that the expression 2011;FitzpatrickandEvans2014)supportsthethe- of a false orgasm in females is used as a diversion, sis that such post-copulatory mechanisms are capable suggesting that copulation is going well. Many male of biasing fertilization by favouring unrelated males. primates exhibit significant sexual coercion (Goetz The release of fluids involved in sexual orgasm could, et al. 2007;Knottetal.2010). Although these are therefore, reduce the cost of mating with relatives common and known strategies in many primates, (see Fitzpatrick and Evans 2014). It could be inferred post-copulatory cryptic choice and confusion of pater- that, in the course of evolution, orgasm evolved to nity are poorly documented in humans (Knott et al. increase sexual activity and favour partner selection, 2010). Such diversionary behaviour could be impor- as species increasingly exhibited a lower reproduc- tant strategies to reduce sexual coercion. It is even pos- tive rate. Cervical stimulation is vital to successful sible that sperm-sensitive receptors may be involved sperm transport and fertilization (Adler 1969). The in the oviduct or uterus and that sperm recognition intensity of the sexual orgasm suggests to the partners proteins may allow sperm selection (Swanson and Vac- that this sexual activity, and especially the copulation, quier 2002;Berlinetal.2008). probably ended in potential fertilization, providing Numerous primate females show their receptivity the protagonists with sufficient diversion that attracts with phenotypic cues as excessive sexual swellings the male’s attention to wait for a putative favourable (Deschner et al. 2004) in contrast with concealed ovu- outcome. lation in humans (Schoroder 1993)orinlangurs(Heis- Linking orgasm and reproduction, the female termann et al. 2001). Moderate swellings were also orgasm has been assumed to be dependent on fac- found in some mustelids with multiple mating, such tors related to male traits indicating paternal invest- as mink (Neovison vison, Mustela lutreola), martens ment (Sherlock et al. 2016). Since orgasm is completely (Martes foina)(Lodé1991), ferret or polecat (Mustela FRONTIERS IN LIFE SCIENCE 41 putorius)(Lodé2001)andinatleastonebirdspecies Acknowledgements (Prunella collaris) (Nakamura 1998). In polecat, for Thanks are due to two anonymous reviewers who improved instance, the strong congestion of the vulva is asso- the manuscript and to Dominique Le Jacques and Marie-Loup ciated with the follicular maturation, so that ovu- Lélias for their assistance in the study. lation is generally induced by long copulation, but spontaneous ovulation may also occur. In fact, in pri- Disclosure statement mates, excessive swelling is a morphological signal No potential conflict of interest was reported by the author. that indicates ovulation in females according to the graduated signal hypothesis (Nunn 1999). 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