The impact of maternal effects on adaptive evolution: Combining quantitative genetics and phenotypic selection in a natural plant population

When a mother influences the phenotypic expression of traits in her offspring, the direction, rate, and duration of adaptive evolution can be modified from standard Mendelian models. To explore the evolutionary implications of trans-generational maternal effects, I quantified two aspects of evolutionary response: the quantitative genetic basis of maternal inheritance and the magnitude of phenotypic selection at the individual and maternal family level for ten traits expressed at four stages in the life cycle in a winter annual plant, Collinsia verna. In a hierarchical quantitative genetic analysis of Mendelian and maternal inheritance, I estimated six additive and environmental causal components of variance: direct (i.e. Mendelian) additive and environmental, maternal additive and environmental and the direct-maternal additive and environmental covariances. The structure of maternal inheritance changed through the life cycle. Early traits were influenced more by maternal additive than by direct effects, direct and maternal additive effects covaried negatively, and direct-maternal environmental covariance was positive. At subsequent stages, some traits displayed strictly Mendelian inheritance, while others displayed direct and maternal additive genetic effects of the same magnitude and negative direct-maternal covariances. Maternal environmental components were negligible beyond emergence. The negative direct-maternal covariances for all maternally inherited traits resulted in near zero or negative realized heritabilities indicating no or reversed response to selection, respectively. In nature, the magnitude of selection on maternally inherited traits will also determine evolutionary response. I examined phenotypic selection at two levels: individual and maternal. An episodic analysis of individual selection across four stages in the life cycle demonstrated that large fall size and later emergence were directly favored across all episodes, although the magnitude and direction of selection varied among episodes. As a result of positive phenotypic correlations among size traits, selection also indirectly favored heavier seeds and larger initial size. Maternal selection may also affect selection response because substantial among maternal family variance in fitness indicated the opportunity for maternal selection. Maternal effects are likely to have dramatic short-term evolutionary consequences by constraining the selection response, influencing correlated response to selection via the phenotypic variance-covariance matrix, and affecting offspring fitness directly via maternal selection.