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What is a paternal effect?

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Highlights

  • Paternal effects differ from maternal effects in fundamental ways.

  • Many paternal effects are mediated by maternal responses.

  • Maternal and paternal effects can have different evolutionary consequences.

Maternal effects are now universally recognised as a form of nongenetic parental influence on offspring but, until recently, paternal effects were regarded as an anomaly. Although it is now clear that paternal effects are both widespread and important, their proximate basis and evolutionary consequences have received little attention and remain poorly understood. In particular, because many paternal effects are mediated by maternal responses such as differential allocation, the boundary between paternal and maternal effects is sometimes blurred. We distinguish here three basic types of paternal effect and clarify the role of maternal responses in these effects. We also outline key questions that can serve as a road map for research on the proximate basis and evolutionary implications of paternal effects.

Section snippets

An unexpected source of heritable variation

Paternal effects (the influence of fathers on the features of their offspring via mechanisms other than the transmission of alleles) have long been regarded as a rare phenomenon confined to species exhibiting paternal care. However, a rapidly growing body of evidence now shows that such effects occur in a variety of organisms, can be mediated by cellular and physiological processes that characterise all sexually reproducing eukaryotic species, and affect a broad range of phenotypic traits in

The nature of paternal effects

Parents contribute in many ways to the development of their offspring but, by conventional definition, a paternal (or maternal) effect can be said to occur when variation in the paternal (or maternal) genotype or phenotype is causally associated with variation in offspring phenotype, and this effect cannot be accounted for by offspring genotype [14]. It has been recognised for a long time that the causal link between parents and offspring –that forms the basis of all forms of heredity – is the

Paternal or maternal?

When paternal influences on offspring are mediated by maternal responses (Box 1), we run into an obvious conundrum: should these effects be regarded as paternal effects or maternal effects? The logic of analysis of variance (ANOVA) suggests the most straightforward decision rule. Statistically, an effect occurs when variation in an independent variable is associated with variation in the response (dependent variable). Note that, although a key assumption of such analysis is that the

Questions to guide research on paternal effects

We outline below some key questions that can serve as a guide to research on the physiology, behavioural ecology, and evolutionary biology of paternal effects.

Concluding remarks and future directions

Mounting evidence from studies on a variety of organisms indicates that paternal effects are widespread and important. Indeed, because the paternal germline appears to be highly susceptible to environment-induced epigenetic reprogramming 55, 56, 72, 73, paternal effects could turn out to be as commonplace as maternal effects. However, the fundamental asymmetry between maternal and paternal influences on offspring, and the mediating role of maternal responses in many paternal effects, complicate

Acknowledgements

Funding for this work was provided by the Australian Research Council through a Discovery Early Career Researcher Award to A.J.C. and a Future Fellowship to R.B.

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