What is it that makes some of us true to our mates while others just can’t resist the appeal of a new sexual partner? We don’t know the answer to this complex question, but in recent years some interesting ideas have emerged from the study of wild rodents (no, “wild rodent” is not being used here as a zoological pejorative term like “philandering toad” or “two-timin’ snake”). Voles, also known as field mice, are found around the world in a number of temperate habitats. Some species of vole like the prairie and pine voles live in social groups and have a monogamous mating system: after a pair mates, neither the male or the female is likely to mate with any other vole. In fact, if one partner dies, the remaining partner will typically never mate again. As is common with monogamous mating systems, both the mother and the father are involved in parental care. By contrast, montane voles and meadow voles are asocial, living mostly in isolated burrows, and are sexually promiscuous. In these species the father makes no contribution to rearing the offspring and the mother does the bare minimum, abandoning the nest about 2.5 weeks after birth.
What makes some voles monogamous and others promiscuous? A clue comes from the distribution of a receptor for the hormone vasopressin: the V1a subtype of vasopressin receptor shows strikingly different distribution patterns in the brains of monogamous voles, like the prairie vole, as opposed to promiscuous voles, like the montane vole. Among other differences, the promiscuous voles had high expression in a region called the lateral septum and low expression in a different region called the diagonal band, while the monogamous voles showed the opposite expression pattern. Importantly, the molecular structure of the receptors in the two types of vole is nearly identical; it’s just the distribution pattern that’s different, as determined by the promoter region of the V1a receptor gene.
There are several reasons to believe that vasopressin signaling is important in determining the sexual behavior of male rodents. In the male prairie vole, mating with a female stimulates a surge of vasopressin release in the brain. Tom Insel and his laboratory, now at the National Institutes of Health, showed that if a drug is used to block the effects of vasopressin on V1a receptors, the male will not form a pair bond with the female or become engaged in parental care. Furthermore, if vasopressin is injected into the brains of male prairie voles, but not montane voles, it causes an increase in so-called affiliative behavior towards a nearby females (in a vole, this means sniffing the rear end). Most impressively, this group used a molecular genetic trick to express V1a receptors in mice in a pattern similar to that found in monogamous voles. Normal male mice, which mate promiscuously, showed no increase in affiliative behavior towards females after receiving a brain injection of vasopressin. However, the mutant mice with monogamous vole V1a receptor distribution, showed a significant increase in amorous butt-sniffing. This appeared to be a genuine expression of attachment rather than just greater curiosity about new odors as vasopressin had no effect on the time mutant mice spent investigating control odor (a lemon-scented tissue).
In monogamous female voles, pair bonding appears to be triggered by a surge of a hormone related to vasopressin called oxytocin, and this can be inhibited by drugs which block oxytocin receptors, particularly in a region called the medial amygdala. Oxytocin may also have a role in males as well: both male and female mice in which the oxytocin gene has been deleted do not appear to form social memories of other mice they have encountered previously (they sniff their butts just as assiduously as they would a newly introduced mouse).
What does this tell us about our own sexual behavior? Human sexual behavior shares some similarities to that of rodents, but has some important differences as well. It shows much greater variability and is probably less closely tied to the olfactory system. At present, it is tempting to speculate that those of us with cheatin’ hearts might have differences in brain vasopressin or oxytocin signaling when compared to our more faithful friends of the “prairie vole persuasion.”