Why have animals evolved to have sex? The obvious answer, "for reproduction", is at odds with the diversity of non-reproductive sexual behavior. Some non-reproductive sexual behavior may exist merely by accident, but there's a variety of ways non-reproductive sexual behavior may otherwise benefit animals. There's no ready answer to the general question of why animals have sex.
Why has natural selection allowed sexual affect and sexual behavior to flourish, particularly in humans? The obvious answer is that sexual affect motivates sexual behavior, and sexual behavior is necessary for reproduction. But only a small subset of sexual behavior is actually capable of producing offspring. Why has evolution preserved such things as masturbation, oral sex, homosexuality, and sex after menopause?
I should first of all point out that we can't blame any one weird culture or historical accident, since non-reproductive sexual behavior can be found throughout world history. Pederasty was practiced in medieval Japan (Childs, 1980) as well as in ancient Greece (Percy, 2005), the Florentine Codex mentions gay sex among the Aztecs (Kimball, 1993), the Kama Sutra discusses fellatio in detail, and in ancient Egyptian mythology, Ra created Shu and Nefnut through masturbation (Armour, 2001). (And on the flipside, if you took the popular claim that masturbation is universal at face value, you might be surprised to learn of peoples in the Central African Republic and the Democratic Republic of the Congo who aren't even aware that masturbation exists; Hewlett & Hewlett, 2010.) Non-reproductive sex isn't even unique to humans: see the Wikipedia article "Non-reproductive sexual behavior in animals" for an impressive laundry list.1
Unfortunately, the extant research doesn't clearly support any one explanation of all these behaviors across all these species. Perhaps this shouldn't be a surprise. In this chapter, I enumerate some of the available explanations and the evidence for them. They aren't mutually exclusive, but nor are there any proposals of how to integrate them into a coherent theory of non-reproductive sexual behavior. Therefore, the adaptive value of sexuality—the one domain of life that evolutionary psychology would presumably most easily explain—is in fact an open question.
The most parsimonious explanation is that non-reproductive sexual behavior is a spandrel. That is, natural selection created a motivation to seek genital stimulation because this motivation makes animals more likely to reproduce, and it is merely an accident of evolution that this motivation also gets animals to do useless things like masturbate.
Lloyd (2006), for example, argues that orgasm in women is a spandrel of orgasm in men, the idea being that female orgasm is of little consequence for fitness but male orgasm is strongly selected for. By contrast, Lloyd doesn't doubt that the clitoris has an adaptive function of encouraging coitus (Smith, 2005), although I would think this a more likely candidate for spandrelism. Consider that the clitoris is a homologue of the penis with no direct reproductive function, just like men's breasts are (usually) nonfunctional equivalents of women's breasts. Consider also that contrary to both (a) the natural a priori expectation that women would only orgasm from something like coitus and (b) the idea that there is no vaginal orgasm, just vaginal stimulation that also happens to stimulate part of the clitoris (Kinsey, Pomeroy, Martin, & Gebhard, 1953, p. 582; Koedt, 1970), women are capable of distinct clitoral and vaginal orgasms: clitoral stimulation alone can produce orgasm in most women, and Komisaruk, Gerdes, and Whipple (1997) showed that orgasm can be induced from vaginal stimulation in women with complete spinal cord injury, whose clitorises must therefore be numb. Vaginal orgasm has obvious utility for fitness; with that taken for granted, the clitoris and its orgasm are the seeming oddballs. Things only get odder, though, given (what I believe to be) the common belief by sex therapists that clitoral orgasm is easier to achieve than vaginal orgasm. This idea has some support in the observation of Kinsey et al. (1953) that women orgasm from 95% of masturbation events (p. 132) but only 70–77% of coitus events (p. 393). If masturbation is more reliably reinforced than reproductive sex, a spandrel argument becomes more difficult to believe.
One of the weirdest examples of non-reproductive sex is mounting among desert-grasslands whiptail lizards, Aspidoscelis uniparens.2 A. uniparens is all-female and reproduces exclusively by parthenogenesis, that is, development from unfertilized egg cells. However, during part of the ovarian cycle (after ovulation), individuals will mount other individuals, like the males of the sexually reproducing ancestor species Aspidoscelis inornata,3 and during follicular development, A. uniparens individuals are receptive to mounting, just like A. inornata females (Woolley, Sakata, & Crews, 2004). This "pseudosexual" behavior is consequential insofar as mounting seems to increase the number of eggs laid by the receptive animal (Crews, Grassman, & Lindzey, 1986). Crews et al. reason that this dependency is a consequence of A. uniparens's unusual history, which includes hybridization. I imagine that it will disappear from the species eventually, so long as A. uniparens never regains males.
There are some species in which certain sexual behaviors have been observed at least once but only rarely. For example, Starin (2004) observed just five instances of masturbation by males in a five-and-a-half–year field study of western red colobus, a type of monkey. Behavior so rare and with no obvious consequences presumably has no function, and is under little selective pressure to disappear.
(No, not that kind of social function.)
Bonobos, one of the two species of chimpanzee, are famous for their sociosexuality (Manson, Perry, & Parish, 1997), particularly tribadism (usually called "genitogenital rubbing" in writing about bonobos). Observation of the circumstances in which tribadism most frequently occurs has suggested that tribadism can be a means of reconciliation after conflict (Hohmann & Fruth, 2000), integration of new females into a group (Idani, 1991, who also points out that males frequently copulate with immigrant females and suggests that coitus thus serves a similarly relationship-solidifying function), or regulation of social tension that arises during eating (Hohmann & Fruth, 2000; Kano, 1980). Li, Yin, and Zhou (2007) observed Tibetan macaques, which can only conceive during their mating season, copulating many times outside of the mating season. As Hohmann and Fruth say of bonobos, Li et al. suggests that this non-reproductive sexual behavior could have a function of reducing conflict ("approximately 20% of the matings during the birth season took place in aggressive situations, which is a higher percentage than in the mating season"). Li et al. also suggests that females copulate outside the mating season in exchange for resources such as food or "favorable places".4
Intuitively, I think the idea that sexuality has been co-opted by evolution to serve social in addition to reproductive functions makes sense. Since reproduction was already an important reason for conspecifics to interact with each other, it would've been a natural choice for a parsimonious designer to extend into a general mechanism for navigating and shaping the social world. This idea also provides a possible explanation for why human sexual behavior is so frequently and thickly intertwined with social relationships, despite the appeal of spontaneous anonymous sex.
I feel obliged to point out that these ideas don't imply that sex is a good way for modern humans to communicate. As Apfelbaum (1984) argues convincingly, sex isn't even an effective form of communication about simple sexual matters.
Disposal of suboptimal sperm
A man who's trying to impregnate a woman needs to strike a balance as to the number of sperm he ejaculates. For, a high concentration of sperm in a woman's reproductive tract increases the chance of successful conception only up to a point. This is best demonstrated by the findings that (1) in vitro, as the sperm-to-egg ratio increases past some point, the chance of conception decreases (e.g., Tsunoda & Chang, 1975) and (2) men with polyzoospermia, who emit very high numbers of sperm per ejaculate, are less fertile although in-vitro fertilization with their sperm is unimpaired (Tournaye et al., 1997). Baker and Bellis (1993) offer two possible explanations: enzymes released by large numbers of sperm can destroy an egg, and fertilization of a single egg by multiple sperm yields a non-viable zygote. At any rate, this need for balance explains Baker and Bellis's observation that men emit more sperm per copulation the longer the intervals between copulations, effectively "topping up" the woman to an optimum level.
An additional complication to this balancing act, Baker and Bellis postulate, is that sperm grow less effective as they age. If sperm are emitted in first-in-first-out order, this raises the danger of a man who's only emitting a limited number of sperm failing to emit the best sperm available. Non-reproductive ejaculation, especially masturbation and nocturnal emission, provide a solution by disposing of sperm in large quantities. Levan, Fedina, and Lewis (2009) concluded that male–male anal copulation among flour beetles serves a similar function.
When non-reproductive sex is more accessible than reproductive sex, animals might pursue it for practice. Li et al. (2007) noticed that during the mating season, some male macaques wouldn't tolerate other males copulating with females, particularly if the copulating male was adolescent or ranked below the other male. The lower stakes outside of the mating season would probably be a better time for males to practice sex.
Male Cape ground squirrels masturbate to ejaculation frequently, on the order of once a day, sometimes several times a day. Waterman (2010) observed instances of masturbation in a wild population to test several different hypotheses as to its function. She found that (1) the males masturbated more frequently on days during which a female was in estrous, (2) masturbation increased with number of partners, and (3) masturbation was more common after than before or between coitus events. She concluded that the best supported hypothesis is that masturbation is a means of flushing the penis of sexually transmitted pathogens.
One might wonder why Cape ground squirrels don't just urinate to accomplish this function. People are sometimes advised to urinate after sex for this reason (Donovan, 2000). "As a desert-adapted species, however," Waterman writes, "Cape ground squirrels produce very concentrated urine and rarely urinate". The squirrels minimize waste of moisture through masturbation by swallowing their ejaculate (apparently, they find autofellatio much less difficult than humans do).
Tan et al. (2009) observed female greater short-nosed fruit bats (Cynopterus sphinx) licking the shaft and base of their mate's penis during coitus. (So unlike the other non-reproductive sexual behaviors discussed in this chapter, this behavior occurs only in an apparently reproductive context.) Tan et al. make a similar suggestion: saliva may kill pathogens and thus reduce the spread of disease.
Tan et al. noticed that the longer the coitus event, the more time the female spent licking. This might be just because a longer coitus event means the females have more time to do this, but it could also be that the licking prolongs the coitus, which in turn might have benefits such as increasing the chance of conception.5
The award for originality goes to Cox (1995). Cox draws an analogy between the human foreskin and hymen. Each serves as a barrier, however slight, to coitus: the foreskin needs to be retracted and the hymen needs to be burst. (Cox also points out several parallels in how cultures regard the foreskin and the hymen.) But the foreskin also facilitates masturbation. Cox reasons that the purpose of the foreskin and hymen is to discourage early reproduction, the idea being that humans are best off establishing themselves socially and economically before investing resources in raising children. Masturbation, at least in men, exists as a substitute for coitus and therefore a disincentive. (But see the previous chapter for surveys that are unsupportive of this last assertion.)
Apfelbaum, B. (1984, November). Sexual reality and how we dismiss it. Paper presented at the meeting of the American Association of the Advancement of Science, San Francisco State University, San Francisco, CA. Retrieved from https://web.archive.org/web/20010627190317/http://www.bapfelbaumphd.com/Sexual_Reality.html
Armour, R. A. (2001). Gods and myths of ancient Egypt. Cairo, Egypt: American University in Cairo Press.
Baker, R. R., & Bellis, M. A. (1993). Human sperm competition: Ejaculate adjustment by males and the function of masturbation. Animal Behaviour, 46(5), 861–885. doi:10.1006/anbe.1993.1271
Bruce, H. M. (1959). An exteroceptive block to pregnancy in the mouse. Nature, 184, 105. doi:10.1038/184105a0
Childs, M. (1980). Chigo monogatari: Love stories or Buddhist sermons? Monumenta Nipponica, 35, 127–151.
Cox, G. (1995). De virginibus puerisque: The function of the human foreskin considered from an evolutionary perspective. Medical Hypotheses, 45(6), 617–621. doi:10.1016/0306-9877(95)90248-1
Crews, D., Grassman, M., & Lindzey, J. (1986). Behavioral facilitation of reproduction in sexual and unisexual whiptail lizards. Proceedings of the National Academy of Sciences, 83(24), 9547–9550. doi:10.1073/pnas.83.24.9547
Donovan, B. (2000). The repertoire of human efforts to avoid sexually transmissible diseases: past and present. Part 2: Strategies used during or after sex. Sexually Transmitted Infections, 76(2), 88–93. doi:10.1136/sti.76.2.88
Grindal, S. D., Collard, T. S., Brigham, R. M., & Barclay, R. M. R. (1992). The influence of precipitation on reproduction by Myotis bats in British Columbia. American Midland Naturalist, 128(2), 339–344. Retrieved from http://www.jstor.org.proxy.library.stonybrook.edu/stable/2426468
Hewlett, B. S., & Hewlett, B. L. (2010). Sex and searching for children among Aka foragers and Ngandu farmers of central Africa. African Study Monographs, 31(3), 107–125. doi:10.14989/128939
Hohmann, G., & Fruth, B. (2000). Use and function of genital contacts among female bonobos. Animal Behaviour, 60(1), 107–120. doi:10.1006/anbe.2000.1451
Hunter, F. M., & Davis, L. S. (1998). Female Adélie Penguins acquire nest material from extrapair males after engaging in extrapair copulations. The Auk, 115(2), 526–528. Retrieved from http://elibrary.unm.edu/sora/Auk/v115n02/p0526-p0528.pdf
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Kinsey, A. C., Pomeroy, W. B., Martin, C. E., & Gebhard, P. H. (1953). Sexual behavior in the human female. Philadelphia, PA: Saunders.
Koedt, A. (1970). The myth of the vaginal orgasm. Retrieved from http://www.cwluherstory.org/myth-of-the-vaginal-orgasm.html
Komisaruk, B. R., Gerdes, C. A., & Whipple, B. (1997). "Complete" spinal cord injury does not block perceptual responses to genital self-stimulation in women. Archives of Neurology, 54(12), 1513–1520. doi:10.1001/archneur.1997.00550240063014
Levan, K. E., Fedina, T. Y., & Lewis, S. M. (2009). Testing multiple hypotheses for the maintenance of male homosexual copulatory behaviour in flour beetles. Journal of Evolutionary Biology, 22(1), 60–70. doi:10.1111/j.1420-9101.2008.01616.x
Li, J., Yin, H., & Zhou, L. (2007). Non-reproductive copulation behavior among Tibetan macaques (Macaca thibetana) at Huangshan, China. Primates, 48(1), 64–72. doi:10.1007/s10329-006-0002-5
Lloyd, E. A. (2006). The case of the female orgasm: Bias in the science of evolution. Cambridge, MA: Harvard University Press. ISBN 0674022467.
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Percy, W. A., III. (2005). Reconsiderations about Greek homosexualities. Journal of Homosexuality, 49(3, 4), 13–61. doi:10.1300/J082v49n03_02
Smith, D. (2005, May 17). A critic takes on the logic of female orgasm. The New York Times. Retrieved from http://www.nytimes.com/2005/05/17/science/17orga.html
Starin, E. D. (2004). Masturbation observations in Temmnick's red colobus. Folia Primatologica, 75(2), 114–117. doi:10.1159/000076273
Tan, M., Jones, G., Zhu, G., Ye, J., Hong, T., Zhou, S., … Zhang, L. (2009). Fellatio by fruit bats prolongs copulation time. PLOS ONE. doi:10.1371/journal.pone.0007595
Tournaye, H., Staessen, C., Camus, M., Verheyen, G., Devroey, P., & Van Steirteghem, A. (1997). No evidence for a decreased fertilizing potential after in-vitro fertilization using spermatozoa from polyzoospermic men. Human Reproduction, 12(10), 2183–2185. doi:10.1093/humrep/12.10.2183
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Waterman, J. M. (2010). The adaptive function of masturbation in a promiscuous African ground squirrel. PLOS ONE. doi:10.1371/journal.pone.0013060
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Surprisingly, in at least one species, male–male anal sex can be ultimately reproductive. Levan et al. (2009) had virgin male flour beetles copulate anally once, then had each member of these pairs copulate with a female once. 7% of the females produced offspring who were apparently fathered by the male partner of their mate. Apparently, in these cases, a spermatophore was emitted by the partner, stuck to the mate, and impregnated the female during mating.
Formerly Cnemidophorus uniparens.
Formerly Cnemidophorus inornatus.
A more widely known example of "prostitution" in animals is Hunter and Davis's (1998) observation of mated female Adélie penguins copulating with males other than their mate in exchange for rocks on which to lay their eggs. But in this case, the harlotry could conceive, so it isn't a clear example of non-reproductive sex.
Yet another hypothesis Tan et al. suggest is that the licking helps with mate choice by helping the female identify a feature of the male's genotype. But by the time coitus is occurring, it's too late for the female to exercise mate choice—unless greater short-nosed fruit bats can abort pregnancies in response to environmental cues, as in the Bruce effect (Bruce, 1959). At least some bats can abort or reabsorb an embryo if food is scarce (Grindal, Collard, Brigham, & Barclay, 1992).