Effects of paternal predation risk and rearing environment on maternal investment and development of defensive responses in the offspring

Abstract

Detecting past experiences with predators of a potential mate informs a female about prevailing ecological threats, in addition to stress-induced phenotypes that may be disseminated to offspring. We examined whether a male rat’s prior exposure to predator (cat) odor influences a female’s attraction towards a male, subsequent mother-infant interactions and the development of defensive (emotional) responses in the offspring. Females displayed less interest in males that had experienced predator odor. Mothers that reared young in larger, semi-naturalistic housing provided more licking and grooming and active arched-back-nursing behavior toward their offspring compared to dams housed in standard housing, although some effects interacted with paternal experience. Paternal predation risk and maternal rearing environment revealed sex-dependent differences in offspring wean weight, juvenile social interactions and anxiety-like behavior in adolescence. Additionally, paternal predator experience and maternal housing independently affected variations in crf gene promoter acetylation and crf gene expression in response to an acute stressor in offspring. Our results show for the first time in mammals that variation among males in their predator encounters may contribute to stable behavioral variation among females in preference for mates and maternal care, even when the females are not directly exposed to predator threat. Furthermore, when offspring were exposed to the same threat experienced by the father, hypothalamic crf gene regulation was influenced by paternal olfactory experience and early housing. These results, together with our previous findings, suggest that paternal stress exposure and maternal rearing conditions can influence maternal behavior and development of defensive responses of offspring.

Significance Statement: The differential allocation hypothesis implies that animals can detect prior experiences of potential mates through variation in that animal’s behavior and then vary their own reproductive investment accordingly, yet little is known about its role in offspring development. The authors examine the effects of predator odor exposure in male rats on female partner preference and maternal care, and show sex-specific changes in juvenile play and anxiety-related behavior. Epigenetic regulation of hypothalamic crf in response to stress is also influenced by paternal experience, which is contextually-dependent on the rearing environment. This argues that preconception paternal stress and housing can influence maternal care and the development of defensive behaviors of offspring.