Paternal absence and increased caregiving independently and interactively shape the development of male prairie voles at subadult and adult life stages

Abstract

The influence of maternal caregiving is a powerful force on offspring development. The absence of a father during early life in biparental species also has profound implications for offspring development, although it is far less studied than maternal influences. Moreover, we have limited understanding of the interactive forces that maternal and paternal caregiving impart on offspring. We investigated if behaviorally upregulating maternal care compensates for paternal absence on prairie vole (Microtus ochrogaster) pup development. We used an established handling manipulation to increase levels of caregiving in father-absent and biparental families, and later measured male offspring behavioral outcomes at sub-adulthood and adulthood. Male offspring raised without fathers were more prosocial (or possibly less socially anxious) than those raised biparentally. Defensive behavior and responses to contextual novelty were also influenced by the absence of fathers, but only in adulthood. Offensive aggression and movement in the open field test changed as a function of life-stage but not parental exposure. Notably, adult pair bonding was not impacted by our manipulations. Boosting parental care produced males that moved more in the open field test. Parental handling also increased oxytocin immunoreactive cells within the supraoptic nucleus of the hypothalamus (SON), and in the paraventricular nucleus (PVN) of biparentally-reared males. We found no differences in vasopressinergic cell groups. We conclude that male prairie voles are contextually sensitive to the absence of fathers and caregiving intensity. Our study highlights the importance of considering the ways early experiences synergistically shape offspring behavioral and neural phenotypes across the lifespan.