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 time. In variable environments where developing individuals cannot directly perceive future conditions, natural selection may favor the use of arbitrary but reliable cues by mothers to signal their progeny’s challenging environments, resulting in adaptation that otherwise could not be achieved. We performed evolution experiments with genetically-variable and predominantly selfing populations of the nematode Caenorhabditis elegans in a temporally uncorrelated anoxic selection environment, where during oogenesis and ovulation mothers received blue light pulses that either reliably or unreliably cued impending anoxic conditions in their progeny. After 60 non-overlapping generations of experimental evolution, populations reliably exposed to light evolved both a cue-dependent increase in offspring survival in anoxia following maternal light exposure, and a larger light-independent increase in survival that depended primarily on the maternal oxygen environment. Differentiation between reliable and unreliable populations in their ability to respond to light was most apparent after two generations of anoxia, with evidence of maladaptation in unreliable populations through decreased fecundity and survival in anoxia, although most fitness differentiation between reliable and unreliable populations was observed regardless of light variation, particularly when maternal generations were under normoxia. These results show that when maternal and offspring selection environments are uncorrelated, maternal traits evolve only if maternal environments provide cues predictive of offspring selection. They indicate that cue reliability can determine the evolution of adaptive plasticity in traits with maternal effects.