Intergenerational transmission of sociality: the role of parents in shaping social behavior in monogamous and non-monogamous species

Abstract

Social bonds are necessary for many mammals to survive and reproduce successfully. These bonds (i.e. pair-bonds, friendships, filial bonds) are characterized by different periods of development, longevity and strength. Socially monogamous species display certain behaviors not seen in many other mammals, such as adult pair-bonding and male parenting. In our studies of prairie voles (Microtus ochrogaster) and titi monkeys (Callicebus cupreus), we have examined the neurohormonal basis of these bonds. Here, we discuss the evidence from voles that aspects of adolescent and adult social behavior are shaped by early experience, including changes to sensory systems and connections, neuropeptide systems such as oxytocin and vasopressin, and alterations in stress responses. We will compare this with what is known about these processes during development and adulthood in other mammalian species, both monogamous and non-monogamous, and how our current knowledge in voles can be used to understand the development of and variation in social bonds. Humans are endlessly fascinated by the variety of social relationships and family types displayed by animal species, including our own. Social relationships can be characterized by directionality (either uni- or bi-directional), longevity, developmental epoch (infant, juvenile or adult) and strength. Research on the neurobiology of social bonds in animals has focused primarily on 'socially monogamous' species, because of their long-term, strong adult affiliative bonds. In this Review, we attempt to understand how the ability and propensity to form these bonds (or lack thereof), as well as the display of social behaviors more generally, are transmitted both genomically and non-genomically via variation in parenting in monogamous and non-monogamous species.

Keywords: Monogamy; Oxytocin; Parental care; Vasopressin; Vole.

Fig. 1.

Potential pathways for intergenerational transmission of social bonds. AVP, arginine vasopressin; DA, dopamine; LS, lateral septum; NAcc, nucleus accumbens; OT, oxytocin.