The Monogamy Paradox: What Do Love and Sex Have to Do With It?

Abstract

Genetic monogamy is rare–at least at the level of a species–and monogamy can exist in the absence of sexual fidelity. Rather than focusing on mating exclusivity, it has become common to use the term “social monogamy” to describe a cluster of social features, including the capacity for selective and lasting social bonds, central to what humans call “love.” Socially monogamous mammals often exhibit selective aggression toward strangers and form extended families. These features of social monogamy in mammals are supported by patterns of hormonal function originating in the neurobiology of maternity, including oxytocin, as well as a more primitive vasopressin pathway. Another key feature of social monogamy is reduced sexual dimorphism. Processes associated with sexual differentiation offer clues to the mysteries surrounding the evolution of monogamy. Although there is consistency in the necessary ingredients, it is likely that there is no single recipe for social monogamy. As reviewed here, genes for steroids and peptides and their receptors are variable and are subject to epigenetic regulation across the lifespan permitting individual, gender and species variations and providing substrates for evolution. Reduced sensitivity to gonadal androgens, and a concurrent increased reliance on vasopressin (for selective defense) and oxytocin (for selective affiliation) may have offered pathways to the emergence of social monogamy.

Genetic ancestry predicts male-female affiliation in a natural baboon hybrid zone

“…Strong evidence for genetic effects comes from interspecific comparisons between pair-bonded and multiply mating species. For example, comparisons between the monogamous prairie vole and other, closely related promiscuous voles have identified genetic divergence in the pathways that regulate arginine vasopressin, oxytocin, and dopamine signaling, which in turn influences pair-bonding behavior (Young et al, 1996; Young et al, 1999; Young et al, 1997a; Young et al, 1997b; reviewed in Carter & Perkeybile, 2018; Johnson & Young, 2015; Sadino & Donaldson, 2018; Young et al, 2011). These pathway differences may in part be due to differences in the distribution and densities of hormone receptors in the brain, suggesting one important mechanism through which variation in opposite-sex social relationships evolves (Insel & Shapiro, 1992; Insel et al, 1994; Smeltzer et al, 2006).…”

The evolution of pair‐living, sexual monogamy, and cooperative infant care: Insights from research on wild owl monkeys, titis, sakis, and tamarins

“…Approaches have ranged from cross‐cultural studies of human behavior (Quinlan & Quinlan, ), to mathematical models of behavior (Gavrilets, ; Schacht & Bell, ), to sociobiological and psychological attempts to find an adaptive value for currently observed patterns (Borgerhoff Mulder, ; Fletcher et al, ; Quinlan, ; Schacht & Bell, ). There are several recent reviews on the topic that offer a comprehensive point of entry to this literature (Carter & Perkeybile, ; French et al, ; Rooker & Gavrilets, ; Schacht, Davis, & Kramer, ; Schacht & Kramer, ). Thus, we will set aside the literature on humans, and instead focus our attention on the contributions that the investigation of nonhuman primates has made to our knowledge of the evolution, behavioral correlates, and biological underpinnings of pair‐living, pair‐bonding, sexual monogamy, genetic monogamy, biparental care, and cooperative infant care.…”

“…The study of pair‐living, pair‐bonding, sexual monogamy, and genetic monogamy in extant primates continues to be an exciting research endeavor that contributes to our knowledge of evolutionary biology and human evolution. In fact, decades after the publication of several early and influential considerations of human “monogamy” and pair‐bonding in an evolutionary framework (Alexander & Noonan, ; Kleiman, ; Lancaster & Lancaster, ), biological anthropologists and evolutionary biologists continue to search for satisfying explanations for the “paradox of monogamy" (Carter & Perkeybile, ). While, historically, few people questioned why females should mate only with a single partner, it was seen as paradoxically that males should restrict their mating to a single partner (Klug, ).…”

Pair bonding slows epigenetic aging and alters methylation in brains of prairie voles

“…We expect that the availability of these epigenetic clocks will provide a significant boost to the attractiveness of the prairie vole as a biological model in aging research. Prairie voles are perhaps best known for their propensity to form human-like socially monogamous pair bonds 12,13 . The human literature has demonstrated overwhelming evidence that there are a suite of positive health and longevity benefits associated with healthy supportive marriage partnerships.…”

“…However, most rodents lack the propensity to form pair bonds, a key feature that is so definitive of humans 10 and relatively rare among mammals in general 11 . Prairie voles (Microtus ochrogaster), on the other hand, are an excellent model species for investigating the neurobiology of complex social behaviors because they form long-term socially monogamous bonds with their mates 12,13 , and both parents exert significant and relatively equal effort to raise their young 14,15 . In laboratory settings, prairie voles that cohabitate and mate with an opposite-sex partner for an extended period (>24 hours) exhibit a robust preference for their partner over a stranger and develop selective aggression toward unfamiliar intruders, whereas sex naïve individuals do not demonstrate these behaviors, which are consistent with a pair bond 16 .…”