Idiosyncratic evolution of maternal effects in response to juvenile malnutrition in Drosophila

Abstract

Maternal effects often affect fitness traits, but there is little experimental evidence pertaining to their contribution to response to selection imposed by novel environments. We studied the evolution of maternal effects in Drosophila populations selected for tolerance to chronic larval malnutrition. To this end, we performed pairwise reciprocal F 1 crosses between six selected (malnutrition tolerant) populations and six unselected control populations and assessed the effect of cross direction on larval growth and developmental rate, adult weight and egg-to-adult viability expressed under the malnutrition regime. Each pair of reciprocal crosses revealed large maternal effects (possibly including cytoplasmic genetic effects) on at least one trait, but the magnitude, sign and which traits were affected varied among populations. Thus, maternal effects contributed significantly to the response to selection imposed by the malnutrition regime, but these changes were idiosyncratic, suggesting a rugged adaptive landscape. Furthermore, although the selected populations evolved both faster growth and higher viability, the maternal effects on growth rate and viability were negatively correlated across populations. Thus, genes mediating maternal effects can evolve to partially counteract the response to selection mediated by the effects of alleles on their own carriers' phenotype, and maternal effects may contribute to evolutionary trade-offs between components of offspring fitness.

Offspring development and life‐history variation in a water flea depends upon clone‐specific integration of genetic, non‐genetic and environmental cues

“…Thus, dynamic cue integration during development allows phenotypes that are facing similar problems (such as minimising age at maturity) to develop multiple solutions (either increasing growth rate or reducing the size at which maturation is initiated). This finding supports the ideas that phenotypes are evolving in a rugged adaptive landscape, rather than converging on a single 'adaptive peak' (West-Eberhard 2003;Pfennig et al 2010;Vijendravarma & Kawecki 2015). Variation in cue integration during ontogeny is likely to be facilitated by the modular nature of development (West-Eberhard 2003), especially if different developmental or life stages face dissimilar selective pressures.…”

“…S5A), and maternal effects canalised offspring age and size at maturity in clone Ness1 irrespective of the offspring environment (Figs S4C and S5C). Thus, cue integration is not only dependent on environmental influences but is also genetically variable (this study; Vijendravarma & Kawecki ). Variation in cue integration suggests that the reliability of genetic, environmental and maternal environmental signals with respect to food availability differs between the clones, and is likely to reflect the environments in which these clones evolved.…”

“…This finding supports the ideas that phenotypes are evolving in a rugged adaptive landscape, rather than converging on a single ‘adaptive peak’ (West‐Eberhard ; Pfennig et al . ; Vijendravarma & Kawecki ). Variation in cue integration during ontogeny is likely to be facilitated by the modular nature of development (West‐Eberhard ), especially if different developmental or life stages face dissimilar selective pressures.…”

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

“…Theoretical evidence suggests that 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. Maternal effects can potentially produce time lags, which other forces like selection and maternal inheritance can then act upon to influence the rate of evolution.…”

“…It is currently believed that maternal effects are the result of interaction of mother's gene products (maternal RNAs and proteins) in the zygote's cytoplasm (Vaiserman et al 2013). 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).…”