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

Abstract

Summary 1.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.

Differences in performance and transcriptome‐wide gene expression associated with Rhagoletis (Diptera: Tephritidae) larvae feeding in alternate host fruit environments

“…; Hahn & Denlinger ; Ragland et al . ). Moreover, larval host use can affect multiple metrics of adult mating and reproductive performance, and incorporating these added selective dimensions should clarify the true nature of fitness differences among populations exploiting different resource environments.…”

Adaptation to a Novel Host by a Seed Beetle (Coleoptera: Chrysomelidae: Bruchinae): Effect of Source Population

“…Some host-range expansions appear to require relatively little change in the genetic composition of an insect population because the insect is already well adapted to the newly encountered, novel host (Agosta 2006, Singer et al 2008, Gillespie and Wratten 2011. In other cases, shifting to even a closely related host plant can be accompanied by a substantial modiÞcation of behavior, physiology, morphology, phenology, and other Þtness-related traits on the new host (e.g., Dworkin and Jones 2009, Linn et al 2012, Nielsen 2012, Ragland et al 2012.…”

Divergence of the diapause transcriptome in apple maggot flies: winter regulation and post-winter transcriptional repression

“…host to track the earlier fruiting time of apples compared with hawthorns (Bush, 1969;Feder and Filchak, 1999;Feder et al, 1993;Smith, 1988). Though hawthorn-and apple-infesting populations eat different fruits as larvae, apples and hawthorns are nutritionally similar, with the larger apples generally yielding larger-bodied adults with greater lipid reserves because of greater resource quantity (Ragland et al, 2012). However, common garden experiments rearing both populations through apple clearly demonstrate that differences in diet do not contribute to the pronounced population difference in eclosion time observed in the field or the laboratory (Dambroski and Feder, 2007;Feder and Filchak, 1999;Smith, 1988).…”