Is Monogamy Natural? Our Anatomy Suggests Perhaps Not

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It is tempting to assume that mating arrangements directly match the typical social pattern. For instance, in a pair-living species it might seem obvious that the adult male sires any offspring of the pair. In other words, pair-living social organization and strictly monogamous mating may appear to be two sides of the same coin. Take, for example, the thousands of pair-living bird species that have traditionally been regarded as strictly monogamous. Countless hours of observation by dedicated bird-watchers failed to reveal any deviation from strict limitation of mating to the partners in a pair. However, the advent of DNA-based paternity tests changed all that. Surprisingly, for nine out of every ten bird species studied, it was discovered that the pair male did not consistently sire all offspring in a nest; about half of them resulted from extrapair copulations. How, we may ask, did such extrapair mating escape detection through the binoculars of all those eager bird-watchers? The answer is that “sneaky” copulations are rapid and discreet. The pair male may be as unaware of them as the peeping ornithologist.

Theorists have leapt in to explain these exciting new findings, incautiously borrowing loaded terms from the human arena. Ironically, the Middle English “cuckold,” used to describe human infidelity, was originally derived from an old French word for cuckoo. Coming full circle, it is now widely applied to animals to refer to pair-living males tending offspring that may not be their own. The customary explanation for this occurrence is that it is in a female’s genetic interest for different males to father her offspring. She may pair up with one male to ensure paternal care while also engaging in extrapair copulations that will boost genetic variability in her offspring. It is in a female’s interest to conceal from her pair mate any sneaky copulations with other males. If the female’s partner were to become aware of the threat to paternity, he might abandon the nest. Or so the argument goes.

This explanation assumes that a male’s overriding interest is to strive for exclusive paternity of any offspring in his nest. Hence strong selection would be expected for any mechanism that reduces the likelihood of extra-pair copulation. Yet chances are that any pair-living male will himself seek mating opportunities with females of nearby pairs. As is the case for females, it is surely in a male’s genetic interest to father offspring in nests of females paired with other males. Perhaps there is a trade-off between a male’s interest in defending paternity of offspring in his own nest and benefits from contributing to paternity of offspring in other nests. Males, too, can spread their options. In any event, the mating arrangements of pair-living birds have turned out to be considerably more tangled than originally believed.Thus patterns of social organization and mating systems are not simply two sides of the same coin; they can vary independently, at least to some extent. This variation also applies to mammals, including primates. DNA-based tests have been used to assess paternity in a few mammal species, and similar results have emerged. Compared to the wide array of studies conducted with birds, there have been few genetic studies of paternity in pair-living mammals, but evidence for frequent extrapair copulations will doubtless emerge. To take one example, in 2007 behavioral biologist Jason Munshi-South conducted a DNA-based study of a pair-living treeshrew species in Sabah (Borneo) and found a high level of extrapair paternity. Similar evidence has also been reported for certain pair-living primates—for example, for fork-crowned lemurs and fat-tailed dwarf lemurs, both night-active inhabitants of Madagascar. Even gibbons, the prime example of monogamy in primates, have been observed engaging in sneaky extrapair matings in the wild.