Maternal effects likely coevolve with plasticity in male care: a comment on Paquet and Smiseth

Parental care is in many ways the quintessential example of conflict between the sexes. Paquet and Smiseth (2016) suggest that maternal effects may affect this conflict by allowing females to induce males to provide more care. This represents a promising generalization of the more specific hypothesis that females adjust the androgens in their eggs to increase male care. The strength of this review is that it not only examines the empirical evidence for this specific hypothesis but it also gives concrete suggestions for future research. Here, I highlight some promising insights this research could provide, but question whether it is useful to frame these maternal effects as female manipulation of male care. One research direction I find particularly intriguing is their suggestion that conflict over parental care might shape female life histories, including the classic trade-off between offspring size and number. Is it possible that some of the variation we see both within and between species can be explained by how males adjust paternal effort in response to egg size (or number)? We already know total maternal investment in the current brood (Kempenaers and Sheldon 1997) as well as maternal allocation between egg size and number (Kindsvater et al. 2013; Kindsvater and Alonzo 2014) can be influenced by paternal effects. Studying the connection between maternal effects and male parental effort would represent a useful extension of our existing understanding of female differential allocation in response to mates. Another interesting implication—though they do not present it this way—is that a between-generation form of plasticity in females (i.e., maternal effects) evolves in response to a within-generation form of plasticity in males (e.g., male plasticity in parental care). A link between withinand between-generation phenotypic plasticity in response to predators has recently been demonstrated empirically (Walsh et al. 2015), but to date these ideas have not been applied to interactions between the sexes. It is interesting to consider when selection will favor plasticity in maternal allocation and male care and how this interaction will affect observed patterns of reproduction. It is precisely this link, however, between female and male plasticity that makes me question whether framing this interaction as female manipulation is productive. For females to manipulate males, males must first exhibit a behavioral reaction norm in parental care that responds to the maternal effect. And for the maternal effect to represent a manipulation, this adjustment must also decrease male fitness (compared with no change in male care). In essence, the females must cause the male to adjust in a way that is not in the male’s interests. Paquet and Smiseth (2016) suggest that this will be detected as the maternal effect moving the male away from his optimal level of paternal care (thus representing manipulation, sensu Dawkins 1999). Although I find the suggestion that maternal effects may evolve in response to male parental care rules exciting, I find this part of the argument flawed. The argument that females can adjust their allocation to manipulate male care only works if we focus on short-term behavioral adjustments. For example, males might have evolved to increase paternal care if females produce smaller eggs (perhaps because this is a general cue of food limitation). If females make smaller eggs (even in the absence of food limitation) then this maternal effect may cause males to provide more care to the offspring even at a net cost to male fitness in the short term. However, not only is parental care plastic but plasticity in care evolves in response to selection (Royle et al. 2014). If we take a long-term evolutionary view, we would expect the male’s parental care reaction norm to evolve in response to female manipulation. Assuming the male’s parental care reaction norm is adaptive, the male response to the female’s adjustment (i.e., the maternal effect) should increase not decrease the male’s lifetime reproductive success (otherwise no plastic adjustment in male care would be expected to evolve). Thus, one cannot detect the interesting dynamics they suggest by asking whether the male adjustment moves the male away from an abstract and unmeasurable male optimum. This not only poses a problem for our ability to demonstrate whether maternal effects allow females to manipulate males but also questions whether it is productive to frame this interaction as manipulation. I would argue that the interesting piece of this interaction and the ideas contained in this review are not whether one sex manipulates the other. Instead, the proposed general interaction between maternal effects and male care suggests an even more fascinating question for future research. First, how do plastic parental effects in one sex coevolve with plasticity in paternal care in the opposite sex? And second, can these coevolutionary dynamics help explain any of the striking but to date puzzling patterns of male and female behavior we see in nature?