Interplay between paternal germline and maternal effects in shaping development: The overlooked importance of behavioural ecology

Abstract

Abstract Environmental conditions can have a lasting epigenetic impact on development, and there is increasing evidence that these effects can be transmitted across generations. Evidence for parental transmission of epigenetic variation to offspring has been primarily focused on paternal epigenetic influences induced by a male's experience of nutritional, social and toxicological exposures. There is an assumption in the literature that paternal influence on offspring in non‐biparental species is mediated exclusively through epigenetic transmission via the germline. However, integration of concepts from behavioural ecology into the study of parental transmission of environmental effects reveals the importance of mating tactics and maternal–paternal interplay in shaping resource allocation towards offspring in considering the mechanism(s) of epigenetic transmission. This paper describes the current state of knowledge regarding paternal epigenetic germline effects, the interplay between maternal and paternal influences and the importance of considering the complex nature of reproduction when predicting the transmission of phenotype across generations. Further, this paper highlights how incorporating concepts from behavioural ecology into the study of epigenetic transmission can refine predictions of phenotypes that emerge and create a more integrated notion of development and inheritance. It is proposed that theoretical and methodological approaches that consider the impact of reproductive context, which include mating dynamics, fertility, variation in parental life history and assessment of maternal effects, could improve the predictions made within studies of paternal epigenetic effects on offspring development. A free Plain Language Summary can be found within the Supporting Information of this article.