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. 2018:6:202.
doi: 10.3389/fevo.2018.00202. Epub 2018 Nov 29.

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

C Sue Carter  1 , Allison M Perkeybile  1
Affiliations

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

C Sue Carter et al. Front Ecol Evol. 2018.

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.

Keywords: androgens; estrogen; monogamy; oxytocin; prairie vole; testosterone; vasopressin.

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Conflict of interest statement

Conflict of Interest Statement: The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

FIGURE 1 ∣
FIGURE 1 ∣
Sexual differentiation into masculinized and feminized physical phenotypes. (A) This classical model characterizes the differential development of the primordial gonad into testes or ovaries, depending on the presence of the SRY gene found on the Y chromosome. As testes develop, high levels of androgens, including testosterone and dihydrotestosterone (DHT), act on highly sensitive androgen receptors to developmasculinized internal (Wolffian duct) and external genitalia. Anti-Müllerian hormone is also produced, causing the Müllerian ducts to degenerate. In the absence of the SRY gene (in an XX genotype), the ovaries produce very low amounts of androgens, causing the Wolffian ducts to degenerate and allowing for feminization of external genitalia. In typical females anti-Müllerian hormone is also not produced, allowing the Müllerian ducts to develop into feminized internal genitalia. (B) In a social monogamy behavioral phenotype, we hypothesize that changes in the response to androgens produced by the testes during prenatal development may lead to changes in the masculinization of the external genitalia in XY genotype individuals. While testosterone production remains high to allow for the masculinization of the internal genitalia, decreases either in the production of DHT or in the sensitivity of the androgen receptor to either testosterone or DHT decrease the extent of masculinization of the external genitalia, a common physical feature of males of socially monogamous species.
FIGURE 2 ∣
FIGURE 2 ∣
Functional differences in the effects of steroids and peptides may contribute to non-monogamous vs. socially monogamous behavioral phenotypes in males. This hypothesis is based primarily on data from laboratory rodents including prairie voles. (A) Males of non-monogamous species often display a suite of behaviors that include low levels of paternal investment, non-selective social and sexual behavior, and non-selective aggression that typically occurs when competing for a mate or territory. These behaviors are facilitated by high levels of androgens and a high sensitivity of the androgen receptor. High levels of testosterone, some of which is aromatized locally to an estrogen, may contribute to low levels of paternal behavior and lead to non-selective social behavior and mating. In addition, vasopressin, facilitated by androgens, is involved in mating- and territory-related aggression in these males. (B) In socially monogamous males, we hypothesize that decreased sensitivity of the androgen receptor, or possibly lower levels of DHT, with a concurrent increase in vasopressin, could contribute to high levels of paternal investment, selective social preferences, and selective mate guarding aggression. Testosterone can be aromatized locally to estrogen and also facilitate the release of oxytocin and vasopressin.
FIGURE 3 ∣
FIGURE 3 ∣
In comparison to non-monogamous montane voles, the socially monogamous prairie vole shows higher unstimulated levels of hormones of the hypothalamic-pituitary-adrenal axis. Adapted from Taymans et al. (1997).
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