The reliability of environmental cues shape learning and selection against deleterious alleles in seed beetles

Abstract

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 adaptive behavioural plasticity could relax the strength of natural selection, but experimental evidence for this prediction remains scarce. Here, we first demonstrate that maternal care in the beetle Callosobruchus maculatus is dependent on environmental cues that allow females to reduce larval competition via learning and informed oviposition choices. We show that this facilitation of maternal care relaxes selection against deleterious alleles in offspring. We further find that mothers of low genetic quality generally provide poorer care. However, when receiving environmental cues providing accurate information about future host-quality, the increased opportunity for adaptive behavioural plasticity reduced genetic differences in maternal care, further relaxing selection against deleterious alleles. We use our data to illustrate how the identified link between adaptive behavioural plasticity in maternal care and the strength of natural selection can impact indirect genetic effects between mothers and offspring and the accumulation of cryptic genetic loads in populations inhabiting environments that differ in their predictability.