A brief natural history of the orgasm

A brief natural history of the orgasm. Thierry Lodé. Frontiers in Life Science, Volume 13, 2019 - Issue 1, Pages 34-44. Sep 12 2019. https://doi.org/10.1080/21553769.2019.1664642

Abstract: Why the sexual climax, in humans, results in a pleasurable experience remains an important biological question. Analysis of evolutionary traits in numerous Vertebrates suggests that orgasm evolved through three phylogenetic stages during the transition from external to internal fertilization and viviparity. First, orgasm is directly dependent on ejaculation in males and the expulsion of fluids from the ovarian and urethral glands (Skene’s) in females. I propose that sexual orgasm could come from the primitive reflex of discharging gametes to ensure reproduction. Thus, the understanding of orgasm should not be reduced to a penis- or a clitoris-centred paradigm. Secondly, orgasm has evolved to stimulate sexual activity because the evolutionary transition from external fertilization to internal fertilization has been accompanied in numerous species 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 fertilization. Female 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.

KEYWORDS: Orgasm, ovarian fluids, mate choice, post-copulatory selection, sexual conflict, unrelated males

Introduction
Why the sexual climax, in humans, leads to the experience of pleasure remains an important biological question. While the male cannot transfer gametes without experiencing an orgasm, in the human species, the female orgasm seems completely decoupled from reproduction (Cabanac 1971 Cabanac M. 1971. Physiological role of pleasure. Science. 173:1103–1107. doi: 10.1126/science.173.4002.1103; Hrdy 1996 Hrdy SB. 1996. The evolution of female orgasms: logic please but no atavism. Anim Behav. 52:851–852. doi:10.1006/anbe.1996.0230; Wallen and Lloyd 2008 Wallen K, Lloyd E. 2008. Clitoral variability compared with penile variability supports non-adaptation of female orgasm. Evol Dev. 10:1e2.). Although orgasm could result from the point that individuals with an orgasm are more successful, Wheatley and Puts (2015 Wheatley JR, Puts DA. 2015. Evolutionary science of female orgasm. In: The evolution of sexuality, 123–148. Springer) argued that there is actually little evidence to suggest that female orgasm can promote a better reproduction. If orgasm had a selective role, then it is difficult to understand why females show such variability in their ability to reach a climax. Analysing the evolutionary history of the sexual climax from its phylogenetic origin, we can draw some new conclusions that can shed light on the function of orgasm.

Indeed, orgasm could only be regarded as a direct selective trait if individuals with this evolutionary trait have the best reproduction. Associated with ejaculation in males, orgasm is characterized by changes in blood pressure, increased heart rate, rhythmic respiratory pattern, involuntary body movements and, in females, by spontaneous colour changes of the labia minora which engorge to twice their size, and by vaginal and anal spasms (Masters and Johnson 1966 Masters WH, Johnson VE. 1966. Human sexual response. Boston: Little Brown. ; Berman et al. 1999 Berman JR, Berman L, Goldstein I. 1999. Female sexual dysfunction, incidence, pathophysiology, evaluation, and treatment options. Urology. 54:385–391. doi: 10.1016/S0090-4295(99)00230-7). The orgasm is directed by the autonomic nervous system and the spinal cord but activates numerous cortical zones through the vagus nerves mediation (Komisaruk et al. 2004 Komisaruk BR, Whipple B, Crawford A, Grimes S, Liu WC, Kalnin A, Mosier C. 2004. Brain activation during vaginocervical self-stimulation and orgasm in women with complete spinal cord injury: fMRI evidence of mediation by the vagus nerves. Brain Res. 1024:77–88. doi: 10.1016/j.brainres.2004.07.029).

Although the definition of orgasm is rather uncertain, Bancroft (2005 Bancroft J. 2005. The endocrinology of sexual arousal. J End. 186:411–427. doi: 10.1677/joe.1.06233) described it as ‘a state motivated toward the experience of sexual pleasure’. In males, it is associated with ejaculation and rhythmic muscle contractions of the perineal muscles, in females, with clitoral retraction, rhythmic muscle contractions of the perineum and vagina. Orgasm also releases some neuropeptides, dopamine, oxytocin and prolactin, which cause a deep sense of well-being. Here, orgasm is defined as the culmination of sexual arousal activating the reward circuit. The increase in dopamine, oxytocin and prolactin concentration can, therefore, be considered as a signal of sexual arousal. All mammals have the physiological capacity for orgasm (Fox and Fox 1971 Fox CA, Fox BA. 1971. A comparative study of coital physiology, with special reference to the sexual climax. J Rep Fert. 24:319–336. doi: 10.1530/jrf.0.0240319) and numerous vertebrates are known to experience orgasm-like states such as primates i.e. bonobo, chimpanzee, gorilla, orangutan, proboscis monkey, macaques (Chevalier-Skolnikoff 1974 Chevalier-Skolnikoff S. 1974. Male–female, female–female, and male–male sexual behavior in the stumptail monkey, with special attention to the female orgasm. Archiv Sex Behav. 3:95. doi:101007/BF01540994; Allen and Lemon 1981 Allen ML, Lemon WB. 1981. Orgasm in female primates. Am J Primatol. 1:15–34. doi: 10.1002/ajp.1350010104; Troisi and Carosi 1998 Troisi A, Carosi M. 1998. Female orgasm rate increases with male dominance in Japanese macaques. Anim Behav. 56:1261–1266. doi:101006/anbe19980898; Murai 2006 Murai T. 2006. Mating behaviors of the proboscis monkey (Nasalis larvatus). Am J Primatol. 68:832–837. PMID: 16847976. doi: 10.1002/ajp.20266; de Waal 2011 de Waal F. 2011. Le singe en nous, Fayard/Pluriel, Paris. ; Grueter and Stoinski 2016 Grueter CC, Stoinski TS. 2016. Homosexual behavior in female mountain gorillas: reflection of dominance, affiliation, reconciliation or arousal? PLoS ONE. 11(5):e0154185. doi: 10.1371/journal.pone.0154185), carnivores and rodents (Adler 1969 Adler NT. 1969. The effect of males’ copulatory behaviour on successful pregnancy of the female rat. J Comp Phys. 69:613; Heeb and Yahr 1996 Heeb MM, Yahr P. 1996. . c-Fos immunoreactivity in the sexually dimorphic area of the hypothalamus and related brain regions of male gerbils after exposure to sex-related stimuli or performance of specific sexual behaviors. Neuroscience. 72:1049–1071 doi: 10.1016/0306-4522(95)00602-8; Coolen et al. 1997 Coolen LM, Olivier B, Peters HJ, Veening JG. 1997. Demonstration of ejaculation-induced neural activity in the male rat brain using 5-HT1A agonist 8-OH-DPAT. Physiol Behav. 62:881–891. doi: 10.1016/S0031-9384(97)00258-8; Kollack-Walker and Newman 1997 Kollack-Walker S, Newman SW. 1997. Mating-induced expression of c-fos in the male Syrian hamster brain: role of experience, pheromones, and ejaculations. J Neurobiol. 1997(32):481–501.doi: 10.1002/(SICI)1097-4695(199705)32:5<481::AID-NEU4>3.0.CO;2-1; Tenk et al. 2009 Tenk CM, Wilson H, Zhang Q, Pitchers KK, Coolen LM. 2009. Sexual reward in male rats: effects of sexual experience on conditioned place preferences associated with ejaculation and intromissions. Horm Behav. 55:93–97. doi: 10.1016/j.yhbeh.2008.08.012; Pavlicev and Wagner 2016 Pavlicev M, Wagner G. 2016. The evolutionary origin of female orgasm. J Exp Zool B Mol Dev Evol. 326B:326–337. doi:101002/jezb22690, birds and reptiles (Cabanac 1971 Cabanac M. 1971. Physiological role of pleasure. Science. 173:1103–1107. doi: 10.1126/science.173.4002.1103; Winterbottom et al. 1999 Winterbottom M, Burke T, Birkhead TR. 1999. A stimulatory phalloid organ in a weaver bird. Nature. 399:28. doi: 10.1038/19884; Ball and Balthazart 2011 Ball GF, Balthazart J. 2011. Sexual arousal, is it for mammals only? Horm Behav. 59:645–655. doi: 10.1016/j.yhbeh.2010.11.001) and fishes (Petersson and Jarvi 2001 Petersson E, Jarvi T. 2001. ‘False orgasm’ in female brown trout: trick or treat? Anim Behav. 61:497–501. doi: 10.1006/anbe.2000.1585). It has even been demonstrated that ejaculation provoked by the activation of Crz-expressing neurons is rewarding to male flies (Zer-Krispil et al. 2018 Zer-Krispil S, Zak H, Shao L, Ben-Shaanan S, Tordjman L, Bentzur A, Shmueli A, Shohat-Ophir G. 2018. Ejaculation induced by the activation of Crz neurons is rewarding to Drosophila males. Curr Biol. 28:1445–1452.e3. doi: 10.1016/j.cub.2018.03.039). Thus, orgasm seems a critical component of reproductive process for many species (Balcombe 2009 Balcombe J. 2009. Animal pleasure and its moral significance. App Anim Behav Sci. 118:212. doi:101016/japplanim200902012).

There are two main theories that provide an explanation for the manifestation of orgasm. It has been firstly hypothesized that orgasm would favour the persistence of bonds to ensure the best care for the offspring (Alcock 1987 Alcock J. 1987. Ardent adaptation. Nat Hist. 96:4. ) or serve as a secondary reinforcement linking sexual behaviours and partner affiliation (Prause 2011 Prause N. 2011. The human female orgasm: critical evaluations of proposed psychological sequelae. Sex Relat Ther. 26:315–328. doi: 10.1080/14681994.2011.651452; Fleischman 2016 Fleischman DS. 2016. An evolutionary behaviorist perspective on orgasm. Socioaffect Neurosci Psychol. 6:32130. doi:103402/snpv632130). However, in many species, the male provides virtually no care to the young, which reduces the interest in this hypothesis. Moreover, the strengthening of the couple’s bonds is clearly refuted by the Coolidge effect (Brown 1974 Brown RE. 1974. Sexual arousal, the Coolidge effect and dominance in the rat Rattus norvegicus. Anim Behav. 22:634–637. doi:101016/S0003–34727480009–6), which leads many males, and to a lesser extent some females (Lester and Gorzalka 1988 Lester GL, Gorzalka BB. 1988. Effect of novel and familiar mating partners on the duration of sexual receptivity in the female hamster. Behav Neural Biol. 49:398–405. doi:101016/s0163–10478890418–9), to increase sexual activity by adopting a greater diversity of partners. In monkeys, females that mated with high-ranking males showed the highest frequency of orgasms (Zumpe and Michael 1968 Zumpe D, Michael RP. 1968. The clutching reaction and orgasm in the female rhesus monkey (Macaca mulatta). J End. 40:117. doi: 10.1677/joe.0.0400117; Chevalier-Skolnikoff 1974 Chevalier-Skolnikoff S. 1974. Male–female, female–female, and male–male sexual behavior in the stumptail monkey, with special attention to the female orgasm. Archiv Sex Behav. 3:95. doi:101007/BF01540994), suggesting a role in partner preference. Finally, among the hypotheses tending to interpret orgasm as a reproductive enhancing effect, it has been assumed that female orgasm would have evolved for the selection of a partner, thus enhancing the chance of the best fertilization (Thornhill et al. 1995 Thornhill R, Gangestad SX, Comer R. 1995. Human female orgasm and mate fluctuating asymmetry. Anim Behav. 50:1601–1615. doi:101016/0003–34729580014–X). Thus, Fox et al. (1970 Fox CA, Wolff HS, Baker JA. 1970. Measurement of intra-vaginal and intra-uterine pressures during human coitus by radio-telemetry. J Rep Fert. 22:243–251. doi:101530/jrf00220243) hypothesized that the orgasmic spasms cause contractions that may endorse sperm retention in the female genital tract, thus increasing the probability of fertilization. Fertilization of male gametes is stimulated by rhythmic contractions of the striated muscles during orgasm. The allegation that female orgasms may increase conception and progeny remains controversial (Zietsch and Santtila 2013 Zietsch BP, Santtila P. 2013. No direct relationship between human female orgasm rate and number of offspring. Anim Behav. 86:253–255; Wheatley and Puts 2015 Wheatley JR, Puts DA. 2015. Evolutionary science of female orgasm. In: The evolution of sexuality, 123–148. Springer) since female orgasms do not appear to have an active role in sperm transport during coitus (Levin 2011 Levin RJ. 2011. Can the controversy about the putative role of the human female orgasm in sperm transport be settled with our current physiological knowledge of coitus? J Sex Med. 8:1566–1578. doi: 10.1111/j.1743-6109.2010.02162.x). Nonetheless, cervical excitations produce contractions of the oviduct and fallopian tubes (Komisaruk et al. 2004 Komisaruk BR, Whipple B, Crawford A, Grimes S, Liu WC, Kalnin A, Mosier C. 2004. Brain activation during vaginocervical self-stimulation and orgasm in women with complete spinal cord injury: fMRI evidence of mediation by the vagus nerves. Brain Res. 1024:77–88. doi: 10.1016/j.brainres.2004.07.029), probably via prostaglandins and are essential for sperm transport and fertilization (Adler 1969 Adler NT. 1969. The effect of males’ copulatory behaviour on successful pregnancy of the female rat. J Comp Phys. 69:613. ; Adler and Zoloth 1970 Adler NT, Zoloth SR. 1970. Copulatory behaviour can inhibit pregnancy in female rats? Science. 168:1480–1482. doi: 10.1126/science.168.3938.1480Wildt et al. 1998 Wildt L, Kissler S, Licht P, Becker B. 1998. Sperm transport in the human female genital tract and its modulation by oxytocin as assessed by hysterosalpingoscintigraphy, hysterotonography, electrohysterography and Doppler sonography. Hum Reprod Update. 4:655–666. doi: 10.1093/humupd/4.5.655

The second theory claims that female orgasm has no selective role and must be understood as a simple by-product of ontogenesis since the embryonic development of the male penis and female clitoris remains very comparable (Symons 1979 Symons D. 1979. The evolution of human sexuality. Oxford: Oxford University Press; Gould 1987 Gould SJ. 1987. Freudian slip. Nat Hist. 96:14–21; Wallen and Lloyd 2008 Wallen K, Lloyd E. 2008. Clitoral variability compared with penile variability supports non-adaptation of female orgasm. Evol Dev. 10:1e2).