Mapping the past, present and future research landscape of paternal effects

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RESEARCH ARTICLE

Open Access

Mapping the past, present and future research landscape of paternal effects Joanna Rutkowska1,2* , Malgorzata Lagisz2 , Russell Bonduriansky2

and Shinichi Nakagawa2

Abstract Background: Although in all sexually reproducing organisms an individual has a mother and a father, non-genetic inheritance has been predominantly studied in mothers. Paternal effects have been far less frequently studied, until recently. In the last 5 years, research on environmentally induced paternal effects has grown rapidly in the number of publications and diversity of topics. Here, we provide an overview of this field using synthesis of evidence (systematic map) and influence (bibliometric analyses). Results: We find that motivations for studies into paternal effects are diverse. For example, from the ecological and evolutionary perspective, paternal effects are of interest as facilitators of response to environmental change and mediators of extended heredity. Medical researchers track how paternal pre-fertilization exposures to factors, such as diet or trauma, influence offspring health. Toxicologists look at the effects of toxins. We compare how these three research guilds design experiments in relation to objects of their studies: fathers, mothers and offspring. We highlight examples of research gaps, which, in turn, lead to future avenues of research. Conclusions: The literature on paternal effects is large and disparate. Our study helps in fostering connections between areas of knowledge that develop in parallel, but which could benefit from the lateral transfer of concepts and methods. Keywords: Research weaving, Systematic review, Meta-analysis, Parental effects, Transgenerational effects, Transgenerational plasticity

Background What does ocean acidification have in common with the Dutch famine? They both exert effects that can be nongenetically transmitted from the fathers to their offspring. Publications on such paternal effects (for definitions and nuances, see Table 1) are increasing in number and diversity, with research coming from evolutionary biology [22, 23], medicine [5, 11, 24] and toxicology [25]. Research on paternal effects carried out within those disciplines pursues different goals. For example, evolutionary ecologists seek to * Correspondence: [email protected] 1 Institute of Environmental Sciences, Faculty of Biology, Jagiellonian University, Kraków, Poland 2 Evolution & Ecology Research Centre, School of Biological, Earth and Environmental Sciences, BEES, The University of New South Wales, Sydney, Australia

understand how paternal effects contribute to heritable variation, how they are influenced by the ambient environment and what role they play in evolution. By contrast, medical and health researchers seek to understand how male health and lifestyle can influence the health of descendants. In each of these disciplines, research is carried out using somewhat different tools and approaches. Crossfertilization between these disciplines could be very valuable but has bee