Fitness consequences of maternal and grandmaternal effects

Abstract

Transgenerational effects are broader than only parental relationships. Despite mounting evidence that multigenerational effects alter phenotypic and life-history traits, our understanding of how they combine to determine fitness is not well developed because of the added complexity necessary to study them. Here, we derive a quantitative genetic model of adaptation to an extraordinary new environment by an additive genetic component, phenotypic plasticity, maternal and grandmaternal effects. We show how, at equilibrium, negative maternal and negative grandmaternal effects maximize expected population mean fitness. We define negative transgenerational effects as those that have a negative effect on trait expression in the subsequent generation, that is, they slow, or potentially reverse, the expected evolutionary dynamic. When maternal effects are positive, negative grandmaternal effects are preferred. As expected under Mendelian inheritance, the grandmaternal effects have a lower impact on fitness than the maternal effects, but this dual inheritance model predicts a more complex relationship between maternal and grandmaternal effects to constrain phenotypic variance and so maximize expected population mean fitness in the offspring.

Adaptation to temporally fluctuating environments by the evolution of maternal effects

“…Directly showing these long-term fitness components is beyond the scope of the present study, since increasing the number of generations considered results in a geometric increase in the number of assays required. Theory has shown, however, that multigeneration carryover effects can be selected in fluctuating environments [16][17][18][88][89][90], and in C. elegans, transgenerational effects over more than two generations have been described [91][92][93]. In our experiments, there was room for the evolution of these transgenerational effects, since the unpredictable populations faced environmental variation that was moderately correlated at multigeneration intervals (S2 Fig).…”

Maternal Effects in a Wild Songbird Are Environmentally Plastic but Only Marginally Alter the Rate of Adaptation

“…Had we included a realistic adult survival rate (for great tits circa 0.5) in the model, the effect of the maternal effect on the evolutionary response would have been even more reduced due to increased generation time, indicating even more strongly that the evolutionary consequences of the maternal effect on clutch size in our population are negligible. Indeed, had we used extreme parameter values used in theoretical model exercises (e.g., Hoyle and Ezard 2012;Ezard et al 2014;Prizak et al 2014), the effects would have been more profound ( fig. S5).…”

“…Theoretical studies of maternal inheritance effects on fitness and rates of adaptation are ample (Kirkpatrick and Lande 1989;Bijma 2011;Hoyle and Ezard 2012;Prizak et al 2014;Kuijper and Hoyle 2015). Empirical work mainly comes from short-term studies testing the effect of experimentally manipulated maternal trait values on offspring performance (e.g., Schluter and Gustafsson 1993;Beckerman et al 2006;Rechavi et al 2011; but for studies with more generations, see, e.g., Plaistow and Benton 2009;Dey et al 2016), and some have identified a role for epigenetic effects as an important driver of phenotypic variation in offspring (e.g., Cubas et al 1999;Champagne 2008).…”

“…Different scenarios can then be explored, varying m and predicting its role in adaptation and fitness in combination with other adaptive mechanisms such as phenotypic plasticity and grand-maternal effects (Hoyle and Ezard 2012;Ezard et al 2014;Prizak et al 2014). In reality, however, maternal effects may not be fixed but plastic in response to environmental conditions and hence may change from season to season.…”

Maternal effect and speciation: maternal effect contributes to the evolution of hybrid inviability betweenDrosophila simulansandDrosophila mauritiana

“…The provisioning of nutrients, transcripts, hormones and signaling molecules by the mother in the developing egg's cytoplasm during oogenesis, allows the zygote to survive through the early stages of development before its own genes can be activated (Vijendravarma and Kawecki 2015). In addition to affecting the offspring's phenotypes, maternal effects may also enable or hinder adaptive evolution based on specific genotypic expressions in the offspring (Kirkpatrick and Lande 1989;McGlothlin and Galloway 2014;Prizak et al 2014;Vijendravarma and Kawecki 2015).…”