Cue reliability and the evolution of adaptive plasticity in maternal traits

Natural populations face challenges from multiple environmental factors, and adaptive phenotypic plasticity is expected to evolve only when these factors are strongly correlated across space and/or time. In situations where individuals rely on signals from their mothers to inform them about selection, maternal trait responses to environmental factors that provide reliable cues may evolve to enable adaptation to selective but unreliable environments. We performed evolution experiments with the hermaphroditic nematode Caenorhabditis elegans in a temporally uncorrelated anoxic selective environment, where, prior to reproduction, maternal generations received innocuous blue-light pulses that either reliably or unreliably cued their progeny for anoxia. After 60 non-overlapping generations of experimental evolution, populations that were reliably exposed to blue light during their history evolved plasticity in two maternal effect traits: one involved in the sensing of blue light and signal transduction to the germline, which was expressed only when grandmothers and mothers developed under anoxia; the other in oocyte deposition and embryo provisioning of essential energetic resources for survival in anoxia. We further found that reliably cued populations adapted to their temporally uncorrelated anoxic selective environment, while there was evidence of maladaptation in populations that were unreliably exposed to blue light, partly because they did not evolve maternal bet-hedging strategies of embryo resource provisioning. These findings demonstrate that environmental cue reliability can determine adaptive phenotypic plasticity in maternal traits.