This is part of a series on the evolution of human mating behavior, comparing evidence for promiscuity and pair-bonding in our species. Please see the Introduction here.

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Are humans naturally monogamous? Oprah Winfrey says ‘no.’That settles it, then. Maybe.

Oprah (she needs no last name) was a guest on a morning talk show, and the topic of discussion was two recent articles on the origins of monogamy in mammals (Lukas & Clutton-Brock, 2013) and another specifically on primates (Opie et al, 2013). Both articles are impressive for their large databases and attention to detail. The first looked at 2545 species of mammals while the Opie article examined 230 primate species.[1]

Both studies focused specifically on social, rather than sexual, monogamy. This distinction is important because sexual exclusivity was not what was being measured here. Rather, social monogamy was defined by both studies as simply living in breeding pairs. The Lukas & Clutton-Brock paper added that in social monogamy the pair shared a common territory, and “associate with each other for more than one breeding season” (p. 526).

After conducting their statistical analyses, the two came to different conclusions. Opie et al. found that primate males tended to become monogamous where infanticide was common, in order to protect young. By contrast, Lukas & Clutton-Brock concluded that monogamy evolved in mammals when competition for food among females forced them to live far away from one another and the best male strategy was to ‘mate-guard’ a specific female. All-in-all, not very romantic stuff.

The two articles were well-done and meticulous (the supplementary data provided in both articles are very rich). Still, it is a bit baffling as to why we should expect to find ‘the reason’ for social monogamy if only because this downplays the unique evolutionary histories of each species. For example, the Lukas article reported that social monogamy had evolved independently 61 times among mammals, and in very different lineages. While population densities or infanticide prevention may be more frequent precursors than other factors (such as biparental care), it seems unlikely that all of those transitions were qualitatively similar. I liked UPenn anthropologist Eduardo Fernandez-Duque’s take on this: “Many times we forget that this is not math…It’s unlikely that one size will fit all.” After all, how could it?

Monogamous species like prairie voles and owl monkeys may have arrived at similar mating patterns, but they likely took different paths to get there. The neurobiology reinforcing that behavior is almost assuredly different as well. But we use the same word – ‘monogamy’ – to describe them all. As an analogy, it’s true that hummingbirds, bats, dragonflies, and pterosaurs like Quetzalcoatlus, are all flying animals, but the properties of ‘flight’ among them – biomechanics, speed, efficiency, altitude – are idiosyncratic to each species. Yet we call them all the same thing: flight (or, more technically, aerial locomotion). This is simply a reminder of a lesson from Biology 101: the need to distinguish between homologous structures (when similarity results from common ancestry) and analogous ones (when similarity results from convergent evolution).

The point is that it can be easy to forget that all species are unique, with complex evolutionary histories. This seems relevant when looking at monogamy, especially if we are trying to understand human monogamy, which is what most people really care about. That’s understandable, given how central relationships are to our lives.

Back to Oprah.

Predictably, although species like dik-diks and owl monkeys are fascinating in their own right, what Oprah and the others really wanted to know was: “what about us!?” One of the hosts, Gail King, asked Dr. Stephen Snyder, a clinical professor of psychiatry who was invited to discuss the articles: “Can you just get to this question… We as human beings, are we naturally monogamous, or is promiscuity in the DNA?” Snyder replied: “I can answer that really quickly: we are not naturally monogamous.”

Many agree with Snyder (and Oprah). To pick a few, in a widely circulated essay on CNN Meghan Laslocky declared that “monogamy is not natural for many, or probably even most, humans.” Chris Ryan (also on CNN) came to a similar conclusion: “there is no reason to believe monogamy comes naturally to human beings.” Dan Savage has called the expectations of monogamy “ridiculous” and “unnatural.” David Barash was equally direct: “there can be no serious debate about whether monogamy is natural for human beings. It isn’t.” Barash added that there were evolutionary reasons for this:

“Right-wing pro-marriage advocates are correct: Monogamy is definitely under siege. But not from uncloseted polyamorists, adolescent “hook-up” advocates, radical feminists, Godless communists or some vast homosexual conspiracy. The culprit is our own biology.”

These are not just cherry-picked quotations from evolutionary biologists or radical thinkers. Rabbi Shmuley Boteach made an astounding admission for a clergy member when he wrote: “Let’s be clear. Yes, monogamy is challenging and does not come naturally.” Though he also added, rightfully, that there are many things that do not come easily to us, but we do them anyway to try to behave more ethically. His example was that men no longer follow the natural inclination to bop women over the head with a club. This wasn’t a very helpful example – actually, it’s really, really terrible. But point taken: don’t hurt people, regardless of whether someone feels there is a ‘natural’ inclination to do so.

This is a really tricky topic, and as always, details matter. I think it’s telling that the Lukas & Clutton-Brock paper did not even include humans in its analysis of 2500+ species of mammals. And the two papers were focused on social monogamy, not long-term pair-bonding or sexual exclusivity, which is what Oprah and Gail King were really asking about. But that is a rather culturally specific version of monogamy. It is often hard to disentangle the idea of social monogamy in animal behavior from cultural notions of monogamy, intertwined with religious wedding ceremonies, domestic and economic partnerships, in-laws, inheritance rights, state recognition of marriages, and of course sexual exclusivity. As a reminder, Jon Marks warned that we need to be very careful with our vocabulary when comparing human and non-human animal mating patterns:

“Baboons should never be described as polygamous, since they do not have marriage.  They should be called polygynous instead… The gibbons are monogamous, because there is no such word as ‘monogynous.’ ” (Note: this is the funniest essay on primates you will ever read).

But if the question is whether sexual monogamy is ‘natural’ (which is also a slippery concept), then even species that were once thought to be paragons of fidelity and lifelong bonding seem fall short of being perfectly monogamous. Carl Zimmer referred to golden lion tamarins as “stunningly monogamous” monkeys that typically mate for life and have sex only with each other. But that’s not always true, and they may occasionally form polygynous groups. Similarly, owl monkeys do not seem to be as monogamous as once believed when observations were made primarily under captivity. Field observations reveal that bonds between males and females are pretty dynamic, and are sometimes interrupted by a third individual. In any case, it seems that for nearly all monogamous species – gibbons, swans, owl monkeys – we can find examples of sex outside the primary pair, at varying rates. However, none of this means that the concept of monogamy should be discarded from studies of animal behavior. If it did, most (all?) species would be disqualified. As Greg Laden wrote:

“I find that discussions of primate sexuality often break down the moment someone not versed in the subject learns that monogamy is often not as monogamous as they thought. The fact that monogamy is not what you thought does not mean that it does not exist.” 

Not only does monogamy exist in nature, it also appears to be more common than once thought, particularly among primates. The Lukas & Clutton-Brock study determined that 9% of mammals were socially monogamous, which is much higher than the typically cited rate of 3% (in fact, I used this figure in Part 2). Helpfully, Peter Gray pointed out that the 3% figure came from a 1977 paper, and this was simply outdated.

While earlier surveys cited similar rates of social monogamy for primates (about 3%), both the Lukas and Opie studies reported that it was much more common among primates than other orders of mammals. But here the studies diverged again, and this is why definitions and methodology are so important. Lukas & Clutton-Brock defined species’ social systems in three ways: solitary, socially monogamous, or group-living, and each species could belong to only one of the three, with no in between. By contrast, Opie and colleagues were more nuanced, allowing a species to belong to multiple categories. A species could be monogamous, while simultaneously also being polygynandrous, polygynous, or polyandrous. This seems more realistic, accounting for variation in behavior within a species. Here was their breakdown for primates:

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• Polygynandrous: 96 species (ex. rhesus macaques, chimpanzees, bonobos, ring-tailed lemur)
• Polygynous: 46 species (ex. gorillas, gelada baboons)
• Monogamous: 32 species (ex. pygmy marmoset, white-handed gibbon)
• Polygynous/Monogamous: 21 species (ex. humans, Philippine tarsier, golden lion tamarin)
• Polygynous/Polygynandrous: 10 species (ex. black howler monkey)
• Polygynandrous/Monogamous: 5 species (ex. red ruffed lemur)
• Polyandrous/Monogamous: 2 marmoset species
• Polgynous/Polyandrous/Monogamous: 2 tamarin species
• Not enough data: 16 species

Notes: polygynandrous (2+ males with 2+ females), polygynous (one male with 2+ females), polyandrous (one female with 2+ males).

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 Crunching the numbers, Lukas & Clutton-Brock defined 29% of primates as monogamous (far more than the rate of 9% in mammals generally, and much higher than the old 3% figure). In the Opie et al. study, 14% of primates were defined as monogamous, while 27% were at least partly monogamous in combination with some other mating system. Almost overnight, social monogamy just became more common among primates and mammals than it used to be. But there are still questions. Questions that need answering.

Part of the problem is it is hard to define something as fluid as behavior. Rigid definitions usually mean that some complexity must be shaved off in order to fit into a discrete category more cleanly. Broad patterns are instructive, but there is lots of value in thinking species-first, rather than behavior-first. There is no reason to expect all species listed under the same type of mating system to behave identically.

It is telling that many primate species in the Opie study were placed into multiple categories. Two primates, the Saddleback tamarin and Emperor tamarin, were labeled as “polgynous/polyandrous/monogamous,” highlighting these species’ behavioral plasticity (or is it indecisiveness?). Humans were not labeled as strictly monogamous, but rather as “polygynous/monogamous,” reflecting the common cross-cultural marriage practice of allowing men to have multiple wives. However, Starkweather and Hames (2012) noted that the frequency of polyandry (one woman having multiple husbands) has been underestimated in the ethnographic record. How much polyandry is necessary to consider it a part of the human repertoire? At some point, someone has to make a gut-level call. 

If polyandry were considered not just one of those rare, exotic practices from the ethnographic record, but as part of a continuum of marital/social/sexual arrangements, would this change our perception of what is ‘natural’ when it comes to human female sexuality? I think the reason this is often overlooked is the presumption that males have more to gain from having multiple partners because the potential reproductive payoff is higher (at least for heterosexual encounters between individuals within a certain age range). But for humans, sex is about much more than reproduction, which changes the model substantially. A few weeks ago, the BBC reported that a woman in Kenya agreed to marry two men when she could not choose between the two. The men agreed that this was the best arrangement for them, and that they would share and play nice. Flexibility is one of the hallmarks of being human, as is true of all organisms. It’s not too hard to imagine a monogamous gibbon female adjusting to polyandry if the situation presented itself. Is there a good reason to expect her to protest? Sarah Hrdy argued that:

“The existence of one-male mating systems does not prove that females “naturally” gravitate to them. Typically monandrous (copulating with just one partner) mating systems are maintained by one male excluding rivals or by other circumstances that distort female options. As with many other animals, primate females (including women) can benefit reproductively from polyandrous matings. Understanding this takes us beyond narrow research programs intent on demonstrating “universal” differences between the sexes, and allows us to study females as flexible and opportunistic individuals who confront recurring reproductive dilemmas and tradeoffs within a world of shifting options.” (2000: 75)

 In other words, primate females are just as complex as males.

So What?

What this all comes down to is how the question is framed. It is one thing to ask: “Is lifelong, sexual exclusivity within a single pair, from sexual maturation until death something that humans do with ease?” From what we know of break-ups and rates of infidelity and divorce, this is obviously not the case (see Parts 2-4 of this series). If long-term relationships were that easy, there would be less need for advice columnists, or marital counselors. Television and literature would be much less interesting too.

But this is not that same question as: “Are humans naturally monogamous?” There is pretty good support for the argument that we have some strong monogamous tendencies. Evidence for the neurobiology of romantic love is solid, as is the nearly ubiquitous concept of romantic love across cultures (see Part 5). I don’t think we’d find those things unless there was some innate tendency for our species to form pair-bonds and be monogamous. Justin Garcia has used the phrase “the biological centrality of the pair-bond” to describe human mating behavior, indicating how important this type of relationship is for our species (Garcia et al. 2012; Gray and Garcia 2013).

At the same time, where there is a center there is also a periphery. Perhaps the question is not whether humans are ‘naturally’ monogamous. Instead, we should ask what are the relative sizes of the center and the periphery, and how much variation there is around them, and what factors affect these?

Lifelong commitment can be done, as my grandparents did. But the ebbs and flows behind the curtains of any relationship are usually private matters. To many people mentioned above, the reason we often have difficulties with lifelong, or even long-term, relationships is because of our biology and an evolutionary history of promiscuity. To the Apostle Paul, it was Satan tempting married people due to their their “lack of self-control” (1 Corinthians 7: 3-5). To Frida Ghitis, it’s because men are stupid (this is not helpful). To marriage counselors, it may just be that difficulties are inevitable over the course of any long-term relationship. Do any two people always get along? Some of us have trouble getting along with ourselves. Or, it could be any number of things: genuine incompatibility between mates, habituation to each other over time, or a desire for novelty. Another possibility is that people can form many meaningful types of bonds, whether simultaneously or sequentially. Augustin Fuentes wrote that: 

 “the need to form multiple physiological and psychological close bonds with other humans is core to who we are. It is part of our nature. If Walter Goldschmidt is right, and this is what we call love, then the need for love via social pair bonds is a hallmark of our evolutionary history and current biology. Humans are rarely sexually monogamous over their lifetimes. Rather we can form multiple sexual pair bonds of differing durations over the course of our lives, which may or may not also be social pair bonds” (2012: 192-3). 

It could just come down to this: if perfect monogamy is the ideal standard, then there are innumerable ways to deviate from that (though the evidence for the Satan hypothesis is lacking. And isn’t that just like him?). As Richard Dawkins said about death being a hair away from life: “however many ways there may be of being alive, it is certain that there are vastly more ways of being dead, or rather not alive” (Dawkins 1986:9).

Perhaps we are, as Dan Savage has said ‘monogam-ish.’ Or we could say we are ‘pair-bonded-plus’ or mostly monogamous. I have this line from Billy Crystal in The Princess Bride ringing in my ears:

“It just so happens that your friend here is only mostly dead. There’s a big difference between mostly dead and all dead… Mostly dead is slightly alive.”

We may not be perfectly monogamous, but nature doesn’t do ‘perfect.’ Our mating patterns have been called tragically confused (Robert Sapolsky), wondrously complex, a funny puzzle (Laurie Santos), a drama (Stephen Snyder), or just conflicted. Nature is messy, and so are we. But for us somewhere in that mess, perhaps even near the core, is monogamy.

Series

1. Part 1. Introduction Link
2. Part 2. Promiscuity Link
3. Part 3. Promiscuity (Genetics) Link
4. Part 4. Promiscuity (Anatomy/Physiology) Link
5. Part 5. Pair-Bonding and Romantic Love Link
6. Part 6. Many Intimate Relationships Link
7. Part 7. Is It Possible to Love Two People? Link
8. Part 8. Love and Suffering Link
9. Part 9. Love Is an Evolutionary Compromise  Link
10. Part 10. Wondrously Complex Paleo-Sex Link
11. Part 11. Sexaptation: The Many Functions of Sex Link
12. Part 12. A Tripartite Conundrum Link
13. Part 13. Is Monogamy ‘Natural?’ Link

 

References

Dawkins R. 1986. The Blind Watchmaker. Norton. Link

Dixson A. 2009. Sexual Selection and the Origins of Human Mating Systems. Oxford. Link

Fuentes A. 2012. Race, Monogamy, and Other Lies They Told You: Busting Myths about Human Nature. University of California Press. Link

Garcia JR, Reiber C, Massey SG, Merriwether AM. 2012. Sexual hookup culture: A review. Review of General Psychology. 16(2):161-176. Link

Gray PB, Garcia JR. 2013. Evolution and Human Sexual Behavior Hardcover.  Link

Hrdy SB. 2000. The optimal number of fathers: Evolution, demography, and history in the shaping of female mate preferences. Annals of the New York Academy of Sciences. 907: 75–96. Link

Lukas D, Clutton-Brock TH. 2013. The evolution of social monogamy in mammals. Science Vol. 341 no. 6145: 526-530. Link

Opie C, Atkinson QD, Dunbar RIM, Shultz S. 2013. Male infanticide leads to social monogamy in primates. PNAS PNAS 2013 110 (33) 13229-13230. Link

Starkweather, KE Hames R. 2012.  A survey of non-classical polyandry. Human Nature 23(2): 149-72. Link