Monogamy Anchored in Our Genes?
Examining the case for exclusive pair-bonding as a human adaptation
Posted Apr 30, 2018
Biological anthropologists and evolutionary psychologists commonly take it for granted that human monogamy has a biological basis. Desmond Morris was an influential early advocate. His 1967 swashbuckling best-seller The Naked Ape proposed long-term monogamous human mating as an extreme expression of natural pair-bonding. Morris dismissed alternative mating arrangements in other cultures as relics of “obscure, backward tribal units”.
Yet any biologically based human behaviour should surely be universal across cultures. As it happened, 1967 was also the original publication date for George Murdock’s Ethnographic Atlas, a magisterial global compilation of baseline anthropological data. Murdock’s survey of 849 human societies revealed polygyny (cohabitation of a man with more than one woman) to be four times more common than monogamy.
Seeking evidence for ancestral mating patterns
Oftentimes, comparison with our closest zoological relatives, the apes, yields useful guidelines. But ape mating systems are so diverse that this does not take us far. The distantly related gibbons are in fact monogamous, but both orangutans and gorillas typically have single-male, polygynous mating arrangements. By contrast, social units in our closest relatives — chimpanzees (including bonobos) — contain multiple adult males that mate promiscuously with several females. Note, however, that single-male mating does predominate among apes, characterizing all except chimpanzees. This is hence the most likely condition in the common ancestor of apes and humans.
Strangely, the notion of biologically anchored human monogamy coexists with another, similarly widespread tenet: adaptation for sperm competition. Bluntly stated, natural selection supposedly favored adaptations for women having coitus with two or more men in sufficiently rapid succession for direct interaction between their ejaculates. Without much evidence, various authors have simply extended sperm competition theory to humans.
Multiple males versus single males
Comparisons with chimpanzees are particularly instructive. In every relevant feature examined, chimpanzees (like other promiscuously mating primates such as macaques) clearly show adaptations for sperm competition, whereas humans (like many primates living in single-male groups) do not. Male chimpanzees have conspicuously large testes with short muscular ducts that quickly disgorge ejaculates with strikingly high sperm counts. Each sperm has a large mid-piece containing many mitochondria supplying abundant propulsion energy. Moreover, fluid secreted by a large prostate gland and seminal vesicles coagulates to form a plug hindering insemination by other males. Chimpanzee semen also contains very few visibly malformed sperms. Subtle adaptations for sperm competition are also found in female chimpanzees, notably elongated oviducts.
For every single feature indicating adaptation for sperm competition in chimpanzees humans show a contrasting condition. Most strikingly, human semen — just like that of gorillas — contains many defective sperms. In sum, humans possess multiple features corresponding to a single-male mating system.
Susceptibility to sexually transmitted diseases (STDs) yields further evidence. Charlie Nunn and colleagues predicted that primates with promiscuous mating habits would be more exposed to STDs and would hence show adaptations to combat higher infection risks. Sure enough, promiscuously mating primates have distinctly higher white blood cell counts than species with single-male mating. Humans have naturally low white blood cell counts like primates with single-male mating. (See my blog piece Sexually Transmitted Diseases: An Evolutionary View, posted October 12, 2015.) This may explain why we are so vulnerable to STDs. The latest report from the Centers for Disease Control and Prevention estimates for the USA that in 2015 the total number of STD infections reached 110 million.
Monogamy or polygyny?
Available evidence overwhelmingly indicates that humans are biologically equipped for a single-male mating system. But this leaves open the question of whether that system is monogamous or polygynous.
With truly monogamous primates such as gibbons, exclusive pair-bonds and lifetime mating are typical. Even in these species, however, extra-pair paternity does occur at low frequency (just a few percent). In fact, well-documented studies have indicated a comparably low level of extra-pair paternity for humans. But low levels of extra-group paternity seemingly also occur with polygynous primates. DNA studies have, for instance, revealed within-group paternity to be the norm in mountain gorillas. So extra-group paternity is apparently limited with single-male groups generally, both monogamous and polygynous.
Kavita Isvaran and Tim Clutton-Brock conducted a comparative study of extra-group paternity in 26 mammal species. Almost half of those species showed levels of 10% or less, while only a seventh showed 50% or more. Extra-group paternity was most common in species with a restricted mating season and also increased with number of females per breeding group, indicating that levels are higher where males are less able to monopolize females. On balance, these findings indicate that a low level of extra-group paternity should be expected for the human species.
Sexual dimorphism and mating system
Broad comparisons of primates are once again informative. Take, for instance, sexual dimorphism: difference between males and females in features not directly connected with reproduction. A long-recognized principle is that body size typically shows little sexual dimorphism in monogamous primates. In pair-living gibbons, for example, males and females have similar body sizes, whereas in polygynous gorillas males weigh almost twice as much as females. Tantalizingly, globally speaking men are on average about 18% heavier than women, slightly but not emphatically exceeding the upper boundary of 15% for monogamous primates.
Alan Dixson has, however, noted an additional indicator: In polygynous primate species, males tend to have distinctive facial adornment of various kinds, and men score unusually highly, notably because of beards. On balance, then, any biological basis for human mating systems is likely to be a mild tendency towards polygyny.
Explanations for malformed sperms
Robin Baker and Mark Bellis claimed that physically abnormal sperms in human ejaculates are not defective but actually adapted to compete in different ways, including killing rival sperms. (See my blog post Kamikaze Sperms or Flawed Products?, posted October 16, 2013.) They tested their hypothesis by mixing ejaculates from two men in experiments in which some sperms reportedly stuck together. But even that ambiguous result was not confirmed in an independent investigation by Harry Moore and colleagues.
In stark contrast, Gerhard van der Horst, Liana Maree and colleagues have reported striking new evidence showing that visibly aberrant sperms in mammals are truly defective and not adapted for warfare. They studied naked mole-rats, ugly-looking East African rodents that live in underground societies that are the closest thing to ant colonies among mammals. Each naked mole-rat colony is effectively monogamous, with a single breeding female usually mated by a single male. Other adults are “workers”. Regardless of status, all males had mostly degenerate sperms of abnormal appearance with an unusually tiny mid-piece containing only half a dozen mitochondria. Less than one in ten sperms were motile, and even those swam exceptionally slowly.
The extreme case of the naked mole-rat shows that a high frequency of defective sperms is associated with minimal sperm competition. In a nutshell, if selection pressure from sperm competition is weak or absent, male mammals can seemingly get by with low ejaculate quality. So abundant defective sperms in human ejaculates clearly indicate that adaptation for single-male mating was a key feature of our evolution.
Adaptation for Mild Polygyny
Hogamus, higamus, men are polygamous;
Higamus, hogamus, women are monogamous.
Mrs. Amos Pinchot reputedly penned this couplet after a dream, although it is unknown whether she wrote this before or after obtaining a virtually uncontested divorce from her spouse. Regardless, her doggerel neatly expresses the notion that men may be less monogamously inclined than women.
Overall, the biological evidence suggests that humans are adapted for mild polygyny, with some men having two or more wives. Perhaps the average condition might be one man with one-and-a-half wives? Note, however, that — even in societies that permit polygyny — many men are monogamous by default, lacking the resources for more than one spouse. Accordingly, in a mildly polygynous society monogamy is not uncommon. Contractual marriage is perhaps needed for a general limitation to monogamy in a human society.
Baker, R.R. (1997) Sperm Wars: The Science of Sex. New York: Basic Books.
Baker, R.R. & Bellis, M.A. (1995) Human Sperm Competition: Copulation, Masturbation and Infidelity. London: Chapman & Hall.
Dixson, A.F. (2012) Primate Sexuality: Comparative Studies of the Prosimians, Monkeys, Apes and Human Beings (Second Edition). Oxford: Oxford University Press.
Dixson, A.F. (2009) Sexual Selection and the Origins of Human Mating Systems. Oxford: Oxford University Press.
Isvaran, K. & Clutton-Brock, T. (2007) Ecological correlates of extra-group paternity in mammals. Proceedings of the Royal Society of London B 274:219-224.
Martin, R.D. (2013) How We Do It: The Evolution of Sex, Childbirth and Parenting. New York: Basic Books.
Moore, H.D.M., Martin, M. & Birkhead, T.R. (1999) No evidence for killer sperm or other selective interactions between human spermatozoa in ejaculates of different males in vitro. Proceedings of the Royal Society of London B 266:2343-2350.
Morris, D. (1967) The Naked Ape: A Zoologist's Study of the Human Animal. London: Jonathan Cape.
Murdock, G.P. (1967) Ethnographic Atlas. Pittsburgh, PA: University of Pittsburgh Press.
Nunn, C.L., Gittleman, J.L. & Antonovics, J. (2000) Promiscuity and the primate immune system. Science 290:1168-1170.
van der Horst, G., Maree, L., Kotzé, S.H. & O’Riain, M.J. (2011) Sperm structure and motility in the eusocial naked mole-rat, Heterocephalus glaber: a case of degenerative orthogenesis in the absence of sperm competition? BMC Evolutionary Biology 11,351:1-11.
Wlasiuk, G. & Nachman, M.W. (2010) Promiscuity and the rate of molecular evolution at primate immunity genes. Evolution 64:2204-2220.
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