The consequences of lifetime and evolutionary exposure to toxic prey: changes in avoidance behaviour through ontogeny

Responses to novel threats (e.g. invasive species) can involve genetic changes or plastic shifts in phenotype. There is controversy over the relative importance of these processes for species survival of such perturbations, but we are realizing they are not mutually exclusive. Native eastern fence lizards (Sceloporus undulatus) have adapted to top-down predation pressure imposed by the invasive red imported fire ant (Solenopsis invicta) via changes in adult (but not juvenile) lizard antipredator behaviour. Here, we examine the largely ignored, but potentially equally important, bottom-up effect of fire ants as toxic prey for lizards. We test how fire ant consumption (or avoidance) is affected by lifetime (via plasticity) and evolutionary (via natural selection) exposure to fire ants by comparing field-caught and laboratory-reared lizards, respectively, from fire ant-invaded and uninvaded populations. More naive juveniles from invaded populations ate fire ants than did adults, reflecting a natural ontogenetic dietary shift away from ants. Laboratory-reared lizards from the invaded site were less likely to eat fire ants than were those from the uninvaded site, suggesting a potential evolutionary shift in feeding behaviour. Lifetime and evolutionary exposure interacted across ontogeny, however, and field-caught lizards from the invaded site exhibited opposite ontogenetic trends; adults were more likely to eat fire ants than were juveniles. Our results suggest that plastic and evolutionary processes may both play important roles in permitting species survival of novel threats. We further reveal how complex interactions can shape adaptive responses to multimodal impacts imposed by invaders: in our system, fire ants impose stronger bottom-up selection than top-down selection, with each selection regime changing differently across lizard ontogeny.