Our understanding of monogamy draws heavily on birds rather than mammals. Birds are more likely than not to practice monogamy whereas there are very few monogamous mammals. Birds do cheat, however, as do humans (see post Did Stoneage men and women sleep around?). The explanation may be chemical.
Many birds are socially monogamous, which is to say that the male and female form an exclusive bond and spend a great deal of their time together. Yet, they are not sexually exclusive. When the male departs, his mate is known to entertain rival males who sire some of the chicks.
For his part, the absent male does a certain amount of philandering. Among barn swallows, that have been extensively studied, about a quarter of the nestlings were sired by a male other than the mate, according to genetic tests. So birds are monogamous but they cheat as well, within limits.
In recent decades, researchers have turned to rodents, specifically voles, in their efforts to understand the biology of monogamy. Prairie voles live in family groups consisting of a monogamous mated pair and their offspring. Meadow voles do not form pair bonds.
When they first get together, prairie vole couples copulate often and this "honeymoon" experience plays a major role in getting them hooked on each other in much the same way that people get addicted to drugs (1,2).
So why do meadow voles not get addicted to each other? Extensive tests have demonstrated that this is due to fewer receptors for oxytocin (the cuddling hormone) and angiotensin in key regions of their brains. In an ingenious experiment it was found that experimentally increasing the number of receptors made meadow voles form pair bonds even without copulating (3).
What if anything do voles tell us about human monogamy?
The fact that the capacity to form lasting pair bonds is a function of brain biology in voles allowed researchers to speculate that differing levels of interest in monogamy for our own species are also partly a matter of biology. Is there a human gene affecting our propensity to bond with a single mate?
In 2008, Swedish researcher Hasse Walum and others (4) reported that variation in a gene known as RS3 affected men's capacity to form an emotional bond with a woman. Men with a double dose of the gene were twice as likely to have troubled marriages. This gene affects the angiotensin receptor system that plays a critical role in social monogamy for male prairie voles.
So we are faced with the uncanny possibility that monogamy in humans is affected by essentially the same brain mechanisms as monogamy in voles. Monogamy in voles takes the form of a deep social attachment combined with a willingness to care for offspring.
Prairie voles are generally sexually faithful to each other because females mate exclusively with the resident male so there are minimal opportunities for philandering males. This is not so very far from most human societies.
Some societies are very different. In the South Seas, wives have relationships with so many extramarital partners that husbands pay little attention to children of the marriage, concentrating their affection on their sisters' children, a phenomenon known as "the avunculate."
Social monogamy is more tightly linked to sexual fidelity for female prairie voles than for males and the same is likely true of humans based on the fact that prostitution and pornography cater mostly to male clients.
People who travel for a living have more opportunities for sexual cheating. If the movie Up In the Air is to be credited, they take advantage of these opportunities sometimes whether they are male or female.
Among humans, it is possible that the social attachment aspect of marriage is sometimes independent of sexual fidelity, particularly for men. We are mostly unaware of this because married couples are addicted to each other's company and spend so much time together that it limits their opportunities for relationships with other people that they find sexually attractive. We are so vole!
1. Young, L. J., Murphy Young, A. Z., & Hammock, E. A. (2005). Anatomy and neurochemistry of the pair bond. Journal of Comparative Neurology, 493, 51-57.
2. Vacek, M. (2002). High on fidelity. American Scientist, 90(3), 225-226.
3. Insel, R., and Hulihan, T. (1995). A gender-specific mechanism for pair bonding: Oxytocin and partner preference formation in monogamous voles. Behavioral Neuroscience, 109, 782-789
4. Walum, H., Westberg, L., Henningsson, S., Neiderhiser, J. M., Reiss, D., Igl, W., et al. (2008). Genetic variation in the vasopressin receptor 1a gene (AVPR1A) associates with pair-bonding behavior in humans. Proceedings of the National Academy of Sciences, 105, 14153-14156.