Environmental interactions during host race formation: host fruit environment moderates a seasonal shift in phenology in host races of Rhagoletis pomonella

Abstract

Summary1. Host race formation is a common form of ecological speciation during which new populations that exploit a novel host (e.g. nutritional resource) experience divergent natural selection, causing adaptive divergence from the ancestral population. Typically, multiple selection pressures drive this divergence, suggesting that interactions among environmental effects may be critical during the speciation process.2. Host‐race‐forming phytophagous insects often experience divergent natural selection imposed by seasonality and nutritional environment, two factors likely to interact through their effects on growth and life‐history timing. We tested for the presence of such an interaction in the apple maggot fly, Rhagoletis pomonella, asking whether nutritional effects interact with seasonality to determine overwintering success.3. We find evidence for such an interaction, wherein feeding on a novel host fruit actually mitigates the negative effects of novel seasonality. Feeding on apple (novel) compared to hawthorn (ancestral) fruit conferred greater fly lipid reserves the overwintering, diapause stage. Earlier, seasonal emergence characteristic of the apple host race imposes an overwintering survival cost. But feeding on apples offsets this cost, which confers greater pupal lipid reserves and consequently larger adult body size post‐winter. Seasonality and host fruit interact to determine fly lipid reserves, and host race differences in lipid content are maximized under the most stressful conditions typically experienced by the apple host race. F1 rearing and genetic association tests revealed no evidence for genetically based divergence in lipid content, suggesting that differences in lipid storage among the fly host races are driven primarily by the host fruit environment.4. Our results suggest that interactions between seasonality and host plant environment shape natural selection and therefore influence adaptive divergence during host race formation.