Sexual Selection and the Origins of Human Mating Systems

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An e-mail message challenging my previous blog post Monogamy Anchored in Our Genes? Human testicles are much larger than would be the case if there were not sperm competition. Compare to truly monogamous or harem holding species. I will not engage further on an email discussion of this, for it is very well known among behavioral ecologists.

At first, I was frustrated to see my carefully compiled account thus dismissed outright, with no mention of alternative evidence and blanket rejection of any discussion. But my dismay gave way to the realization that I had skimmed over the extensive comparative evidence regarding human mating adaptations yielded by studies of testes. My anonymous critic is surely not alone in accepting human sperm competition despite the complete absence of convincing indicators, and I owe it to my readers to set the record straight.

Like many other biological features, testis volume increases with body size across mammals. Comparisons between species of major very different body sizes must therefore allow for scaling effects. But the relationship between testis size and body size is non-linear, so a simple ratio is misleading. Because testis size increases less rapidly than body size, the ratio will tend to decrease as mammals become larger. In fact, the data clearly show an overall trend, with the testis-to-body size ratio decreasing at larger body sizes.

For instance, a two-pound owl monkey has a ratio of 0. Yet both species are monogamous and owl monkey testes actually turn out to be particularly small when appropriate adjustment is made for body size. And some striking points are obvious even without intricate calculations.

13. Sexual Selection

For instance, a twenty-pound adult male macaque has testes weighing close to three ounces, whereas testes of a seven-fold heavier adult man weigh under two ounces! Several decades elapsed before the connection between testis size and mating system was recognized. In , Roger Short started the ball rolling so to speak by considering differences among great apes in relation to their mating systems. Great apes do not differ greatly in body size, so explicit allowance for size effects was not essential. Short noted that male chimpanzees, which live in promiscuously mating multimale-multifemale groups containing several adults of both sexes, have notably large testes.

Their testes are three times bigger than in orangutans and four times bigger than in gorillas, both of which have single-male mating. In fact, male orangutans and, especially, male gorillas are considerably heavier than male chimpanzees, so relative to body size the difference is even more marked. To be fully informative, comparisons across species require appropriate allowance for body size effects. In , Alexander Harcourt and colleagues conducted a wide-ranging examination of relationships between testis weight, body weight and mating systems across monkeys and apes. Their results clearly confirmed that mating system is associated with testis size.

As expected, across species testis weight generally tends to increase with body size.

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As Alan Dixson emphasizes in his book Sexual Selection and the Origins of Human Mating Systems , men clearly have far smaller testes than male chimpanzees, despite our larger body size. Small testes conflict with any suggestion that humans are biologically adapted for promiscuous mating. Indeed, judged on size alone, human testes are apparently adapted for a one-male mating system without notable sperm competition between men.

Human testes are closely similar in size to those of orangutans, which live virtually solitary lives in a dispersed kind of harem system, with the home range of a fully adult male commonly overlapping with smaller ranges of two or more females. Evolutionary interpretations based on testis size and other dimensions of the male reproductive organs are based on a tacit assumption that these features are genetically determined and relatively unaffected by environmental conditions.

Yet it is known that in primate species with a restricted breeding season testis size typically varies greatly across the year. A paper by Jean Wickings and Eberhard Nieschlag reported a threefold annual variation in testis size in Rhesus macaques. Pronounced seasonal variation might explain why, in a plot of testis size against body size, the squirrel monkey, which lives in multimale-multifemale groups, lies close to the best-fit line rather than clearly above it.

Squirrel monkeys have a clearly defined breeding season, so it is crucial whether testis size was measured at an appropriate time. Matt Anderson and Alan Dixson neatly circumvented the issue of environmental influence on testis size by examining the sperms themselves. In all mammals, a sperm has a head containing the nucleus, a midpiece packed with mitochondria, and a whip-like propulsive tail. Midpiece mitochondria provide energy to power the tail.

Dixson and Anderson reasoned that in promiscuously mating species the sperm midpiece should be bigger, equivalent to a larger fuel tank. As expected, a plot of midpiece size against relative testis size in various primate species reveals a clear correlation. Promiscuously mating species such as baboons, macaques and plains baboons lie in the upper right sector of the graph because they have large sperm midpieces as well as relatively large testes. By contrast, the lower left sector of the plot contains various primates with single-male mating systems, such as marmosets, gibbons and orangutans.

These species have small sperm midpieces as well as relatively small testes. Importantly, humans fall into that lower sector and are actually quite similar to orangutans. Geoffrey Miller rated it really liked it Jun 19, Bogdan Cihodariu-ionita rated it it was amazing Jun 10, Zvr added it May 17, Stark marked it as to-read Aug 16, Keith marked it as to-read Dec 14, Isaiah marked it as to-read Mar 10, Besha marked it as to-read Apr 09, Xynnia marked it as to-read Jun 21, Stefano marked it as to-read Jul 14, Denae marked it as to-read Oct 09, Sir marked it as to-read Nov 18, Constantin Minov marked it as to-read Jan 28, Dinh marked it as to-read Mar 21, Jen marked it as to-read Apr 16, Late Night Novice marked it as to-read May 28, Samra marked it as to-read Dec 14, Kelli marked it as to-read Jan 06, Rachel Raphael kapler marked it as to-read Jan 13, Lily May added it Feb 18, Rebecca is currently reading it Mar 03, Tigran Ghardashyan marked it as to-read Jan 08, Abi added it Mar 27, Juliusz Gonera marked it as to-read Sep 15, Pranon marked it as to-read Sep 24, Jurgen Dhaese marked it as to-read Sep 26, Jeyashree Krishnan marked it as to-read Dec 05, Sara Walker marked it as to-read Jan 30, While a simple classification would be useful for cross-species comparisons, monogamous, polyandrous, and polygynous marriage systems exist across contemporary human societies.

Moreover, sexual relationships occur outside of or in tandem with marriage, resulting in most societies exhibiting multiple kinds of marriage and mating relationships. Further complicating a straightforward classification of mating system are the multiple possible interpretations of biological traits typical of humans used to indicate ancestral mating patterns. While challenging to characterize, our review of the literature offers several key insights. Thus, we conclude that while there are many ethnographic examples of variation across human societies in terms of marriage patterns, extramarital affairs, the stability of relationships, and the ways in which fathers invest, the pair-bond is a ubiquitous feature of human mating relationships.

How best to characterize the human mating system is a subject of intense and polarized debate. On the one hand, sex differences in reproductive investment, and resultant differing potential reproductive rates, are argued to favor elevated mating effort behavior in males i. However, on the other hand, an evolved sexual division of labor, with offspring dependence on paternal care, is argued to generate overlapping interests in long-term, monogamous relationships for both men and women Washburn and Lancaster, ; Lancaster and Lancaster, ; Kaplan et al.

Given the varied sources of support for both approaches, disagreement exists on how best to describe mating patterns in humans.

Sexual Selection and the Evolution of Brain Size in Primates

Particularly challenging is to generate an agreed upon definition of a species-typical strategy often used in comparative studies. This review is focused on an attempt to offer resolution regarding the current debate. After reviewing the literature on marriage and mating systems in humans, we present a cross-cultural examination as well as comparative and evolutionary evidence for and against particular lines of inquiry. Confusion and debate describing a human-typical mating pattern are warranted given the diversity of strategies both across and within cultures.

This figure is often used to support claims of the mating effort intensive nature of males given that most societies allow men to have multiple wives.

However, upon closer inspection, within a small-scale polygynous society, the majority of marriages are monogamous Murdock and White, ; Flinn and Low, ; Binford, Figure 1. Adapted from Marlowe Although most marriages are monogamous at any one point in time, over the life course individuals may reenter the marriage market more than once.

Mating Systems in Sexual Animals

Nonetheless, while individuals may have more than one partner across their life, sexual fidelity within a marriage is generally expected. Marriage is common to all human societies and publicly acknowledges who has sexual access to whom, with divorce often resulting from extramarital relationships Irons, ; Marlowe, ; Kramer and Greaves, However, typical of the range of behavioral variation expressed by humans, many exceptions exist, and sex is found outside of marriage both cross-culturally and among individuals in any one society Box 1 : Sex outside of the pairbond across human societies.

Yet, while engaging in sex outside of marriage likely occurs to some extent in all societies, because men and women typically live in long-term pairbonds within the same residential unit, they have been described as practicing social monogamy Reichard, ; Strassmann, While human patterns are distinct from genetic monogamy, defined as two individuals who only reproduce with one another, levels of extra pair paternity are relatively low compared to other socially monogamous species.

Box 1. Sex outside of the pairbond across human societies. While humans form long-term pair bonds that are recognized as marriages in all societies, sexual relations also occur outside of marriage. In some societies and incidences these relations are clandestine and considered transgressions with punishments that range in severity. But in other cases, uncommitted sexual liaisons are socially permissible, and generally fall under two well-documented ethnographic contexts.

The first occurs prior to first marriage when adolescent girls are in a life stage when they have a low probability of conceiving and are given freedom to explore different premarital relationships Mead, ; Irons, ; Parker, ; Gregor, For example, among the Makushi of Guyana, recently sexual mature individuals receive parental support to engage in pre-marital sex Schacht, The stated purpose of this mating behavior is to allow for mutual mate choice and the identification of a possible long-term mate.

However, once married, copulation outside of the pair-bond is expected to cease. A second socially sanctioned form of sex outside marriage occurs in the context of either partible paternity or wife sharing during prescribed situations. For example, among some lowland South American groups, women regularly have several sexual partners in addition to their husband Beckerman and Valentine, ; Walker et al. This practice is common where the contribution of multiple men is thought to be required for fetal development.

References and Recommended Reading

While women do not formalize additional relationships through marriage i. In other societies, wife sharing may occur during publicly acknowledged situations. This exchange was reportedly agreed upon by all parties, and often, though not always, resulted in long-term social and sexual relationships. Other extrapair relationships are more clandestine, likely because of penalties that may follow e. Nonetheless, there are many examples of men offering food and other resources in exchange for extramarital sex Holmberg, ; Gregor, ; Hill and Hurtado, ; Pollock, In sum, a simple classification of a human-typical mating system is challenging given the variety of pairing strategies observed.

Monogamous, polyandrous, polygynous, and short-term mating patterns are found across contemporary human societies, with most societies exhibiting multiple kinds of marriages and mating relationships Marlowe, ; Fortunato, What can be most simply distilled from this is that humans form long-term pairbonds. However, while polygynous and polyandrous marriages are found in many societies, ethnographic evidence indicates that most individuals within a society live in monogamous marriages that are generally, but not always, sexually exclusive.

It is important also to emphasize that these unions are commonly serially monogamous, and that regardless of divorce rates, this likely would have been the case in the past due to high rates of spousal mortality under premodern mortality schedules Gurven and Kaplan, Although cross-cultural information may illuminate contemporary variation in mating patterns, it tells us less about their antiquity. To seek additional support to characterize the human mating system, we turn to indicators of ancestral mating patterns. Sexual selection is a widely recognized force influencing behavioral and physical traits across animal taxa Andersson, Differences between males and females within and across species can offer insight into both historical and contemporary selection pressures.

Mating systems are amazingly diverse across mammals generally, and primates in particular Dixson, ; Kappeler and van Schaik, Given human placement in the primate order, here we approach human mating from a comparative perspective to better understand behavioral and physical traits that either are shared or distinguish us from our closest living relatives. We target three commonly examined traits in reference to predicting primate breeding systems: sexual dimorphism, testis size, and concealed ovulation Dixson, We review each of these and discuss whether the evidence supports a human monogamous past that may serve to explain the mating system's current prevalence.

Sexual dimorphism exists within a species when, in addition to differences between the sexual organs themselves, males and females differ in size or appearance Andersson, Across primates, minimal levels of sexual dimorphism in body weight and canine size are generally associated with monogamy and low rates of male antagonistic competition e. Unsurprisingly, gorillas exhibit high levels of reproductive skew and males are nearly twice the size of females Leigh and Shea, Given these patterns, what evidence of sexual dimorphism do we see in our hominin line i.