Species differences in the effect of oxytocin on maternal behavior: A model incorporating the potential for allomaternal contributions

Oxytocin has historically been connected to processes involved with the physiology of motherhood. One of its earliest known functional roles, reported over 100 years ago, is to induce the uterine muscle contractions necessary for parturition (Dale, 1906). Indeed, this ability of oxytocin to induce parturition is where the name oxytocin is derived, Greek for oxys and toketos, meaning “quick birth” (Kamm et al., 1928). Given oxytocin’s essential role in the physiology of mothering, and similar to other hormones that simultaneously act peripherally and centrally across pregnancy and postpartum, it is not surprising that oxytocin also generally enhances maternal caregiving (Olazábal, 2018, Yoshihara et al., 2017). However, the significance of oxytocin for expressing maternal behavior varies widely among species, from indispensable to apparently nonessential. The purpose of this review is to first expand on recent reviews describing the role of oxytocin in maternal caregiving (Olazábal, 2018, Yoshihara et al., 2017) by specifically examining the role of oxytocin in mothering for a number of species, including some better-studied ungulates, laboratory rodents, humans, and non-human primates. Through this analysis, it becomes clear that oxytocin plays a more important role in inducing caregiving in species that are unresponsive to offspring as virgins, while in allomaternal species that are generally spontaneously maternal even before mating, oxytocin plays a lesser role in inducing caregiving. We postulate that this relationship is driven by an evolutionary pressure related to the likelihood of another conspecific providing quality offspring care, which we term allomaternal potential, which in turn drives species differences in the importance of oxytocin in mothering (Figure 1). More specifically, in species in which allomaternal potential is high (i.e., quality caregivers are likely present), we propose that oxytocin is decoupled from the onset of maternal behavior. We posit that this relationship between oxytocin and maternal behavior is a form of kin selection, whereby social structure, behavior, and oxytocin interact to compel mothers to preferentially dispense resources to their own young when quality helpers are improbable. Indeed, this model is an extension and refinement of parental expenditure/parental investment models of the evolution of parental care (Clutton-Brock, 2019, Kölliker et al., 2012, Trivers, 2017), whereby caregiving is related to the balance between the effort and resources to raise those offspring versus the benefits of future mating and raising more offspring. Finally, we will discuss limits of the current literature and critical tests of our ideas to help the overall understanding of the role of oxytocin in maternal behaviors.

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