Environmental predictability favours adaptive behavioural plasticity and relaxes selection against deleterious alleles

Behavioural plasticity can play a key role in evolution by either facilitating or impeding genetic adaptation. The latter occurs when behaviours mitigate selection pressures that otherwise would target associated traits. Therefore, environments that facilitate the evolution of adaptive behavioural plasticity are predicted to relax natural selection overall, but experimental evidence for this prediction remains scarce. Here, we first demonstrate that adaptive behavioural plasticity in maternal care in the beetle Callosobruchus maculatus is dependent on reliable environmental cues that allow females to reduce larval competition via learning and informed oviposition choices. By comparing survival of larvae of low and high genetic quality in competition with the conspecific C. phaseoli , we show that predictable maternal environments relax selection on deleterious alleles in offspring. We further find that females of low genetic quality generally provide poorer care. However, in the predictable environment, the increased opportunity for learning reduced genetic differences in female care, further relaxing selection against deleterious alleles. We illustrate how the identified link between adaptive behavioural plasticity and the strength of natural selection can have important implications for the build-up of cryptic genetic loads and outcomes of interspecific competition across variable environments that differ in their predictability.