The Evolution of Multivariate Maternal Effects

There is a growing interest in predicting the social and ecological contexts that favor the evolution of maternal effects. Most predictions focus, however, on maternal effects that affect only a single character, whereas the evolution of maternal effects is poorly understood in the presence of suites of interacting traits. To overcome this, we simulate the evolution of multivariate maternal effects (captured by the matrix M) in a fluctuating environment. We find that the rate of environmental fluctuations has a substantial effect on the properties of M: in slowly changing environments, offspring are selected to have a multivariate phenotype roughly similar to the maternal phenotype, so that M is characterized by positive dominant eigenvalues; by contrast, rapidly changing environments favor Ms with dominant eigenvalues that are negative, as offspring favor a phenotype which substantially differs from the maternal phenotype. Moreover, when fluctuating selection on one maternal character is temporally delayed relative to selection on other traits, we find a striking pattern of cross-trait maternal effects in which maternal characters influence not only the same character in offspring, but also other offspring characters. Additionally, when selection on one character contains more stochastic noise relative to selection on other traits, large cross-trait maternal effects evolve from those maternal traits that experience the smallest amounts of noise. The presence of these cross-trait maternal effects shows that individual maternal effects cannot be studied in isolation, and that their study in a multivariate context may provide important insights about the nature of past selection. Our results call for more studies that measure multivariate maternal effects in wild populations.Author Summary: In numerous organisms, mothers influence the phenotype of their offspring by transmitting hormones, antibodies and nutrients to the embryo. Evolutionary studies that make predictions about the evolution of these maternal effects typically focus, however, on single maternal characters only, in isolation of other traits. This contrasts with insights from quantitative genetics where reliable predictions about evolutionary change can only be made when measuring multiple traits simultaneously. The current study is therefore the first to make formal predictions about the evolutionary properties of multiple maternal effects. We show that maternal phenotypic characters generally give rise to developmental interactions in which one maternal character affects multiple offspring characters. In turn, such interactions can give rise to correlations between different traits in parent and offspring, which constrain evolutionary responses to sudden change. In addition, we find that the rate of environmental change directly affects some of the measurable properties of maternal effects: in rapidly changing environments, multivariate maternal effects are negative, so that offspring attain phenotypes that are different from their mothers, whereas positive maternal effects where offspring are more similar to their mothers occur in slowly changing environments. Hence, multivariate maternal effects provide a clear signature of the past selective environment experienced by organisms.