Who listens to mother? A whole-family perspective on the evolution of maternal hormone allocation

Abstract

Maternal effects, or the influence of maternal environment and phenotype on offspring phenotype, may allow mothers to fine-tune their offspring's developmental trajectory and resulting phenotype sometimes long after the offspring has reached independence. However, maternal effects on offspring phenotype do not evolve in isolation, but rather within the context of a family unit, where the separate and often conflicting evolutionary interests of mothers, fathers and offspring are all at play. While intrafamilial conflicts are routinely invoked to explain other components of reproductive strategy, remarkably little is known about how intrafamilial conflicts influence maternal effects. We argue that much of the considerable variation in the relationship between maternally derived hormones, nutrients and other compounds and the resulting offspring phenotype might be explained by the presence of conflicting selection pressures on different family members. In this review, we examine the existing literature on maternal hormone allocation as a case study for maternal effects more broadly, and explore new hypotheses that arise when we consider current findings within a framework that explicitly incorporates the different evolutionary interests of the mother, her offspring and other family members. Specifically, we hypothesise that the relationship between maternal hormone allocation and offspring phenotype depends on a mother's ability to manipulate the signals she sends to offspring, the ability of family members to be plastic in their response to those signals and the capacity for the phenotypes and strategies of various family members to interact and influence one another on both behavioural and evolutionary timescales. We also provide suggestions for experimental, comparative and theoretical work that may be instrumental in testing these hypotheses. In particular, we highlight that manipulating the level of information available to different family members may reveal important insights into when and to what extent maternal hormones influence offspring development. We conclude that the evolution of maternal hormone allocation is likely to be shaped by the conflicting fitness optima of mothers, fathers and offspring, and that the outcome of this conflict depends on the relative balance of power between family members. Extending our hypotheses to incorporate interactions between family members, as well as more complex social groups and a wider range of taxa, may provide exciting new developments in the fields of endocrinology and maternal effects.

Keywords: honest signalling; interacting phenotypes; intrafamilial conflict; maternal effects; maternal hormones; offspring competition; parent-offspring conflict; plasticity; sexual conflict.

Fig 1

Overview of maternal hormone allocation under intrafamilial conflict. At each point along the timeline between oogenesis until offspring independence or dispersal, various family members have the opportunity to express strategies that aim to skew offspring phenotype towards their personal optimum. The success and evolutionary stability of such strategies is determined by various factors regarding costs, information or power asymmetries, and social context (‘determining factors’), and also the actions of other family members (denoted by grey arrows). We argue that understanding the link between maternal hormone allocation and offspring phenotype requires understanding which family member strategies have evolved under intrafamilial conflict, which in turn depends on the ecological and social context.