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

Abstract

Host race formation, the establishment of new populations using novel resources, is a major hypothesized mechanism of ecological speciation, especially in plant-feeding insects. The initial stages of host race formation will often involve phenotypic plasticity on the novel resource, with subsequent genetically based adaptations enhancing host-associated fitness differences. Several studies have explored the physiology of the plastic responses of insects to novel host environments. However, the mechanisms underlying evolved differences among host races and species remain poorly understood. Here, we demonstrate a reciprocal larval performance difference between two closely related species of Rhagoletis flies, R. pomonella and R. zephyria, specialized for feeding in apple and snowberry fruit, respectively. Microarray analysis of fly larvae feeding in apples versus snowberries revealed patterns of transcriptome-wide differential gene expression consistent with both plastic and evolved responses to the different fruit resources, most notably for detoxification-related genes such as cytochrome p450s. Transcripts exhibiting evolved expression differences between species tended to also demonstrate plastic responses to fruit environment. The observed pattern suggests that Rhagoletis larvae exhibit extensive plasticity in gene expression in response to novel fruit that may potentiate shifts to new hosts. Subsequent selection, particularly selection to suppress initially costly plastic responses, could account for the evolved expression differences observed between R. pomonella and R. zephyria, creating specialized races and new fly species. Thus, genetically based ecological adaptations generating new biodiversity may often evolve from initial plastic responses in gene expression to the challenges posed by novel environments.

Sequential divergence and the multiplicative origin of community diversity

“…Reciprocal fruit transplant studies of apple-and hawthorn-infesting R. pomonella have failed to detect host-related differences in larval feeding performance with respect to survivorship to pupariation (46). However, tradeoffs in larval performance have been documented for R. pomonella sibling species (33,34) that may distinguish species from the apple and hawthorn host races. If the same is true for wasps, experiments investigating performance tradeoffs may help establish the taxonomic status of D. alloeum, D. mellea, and U. canaliculatus.…”

“…Lastly, to link host-associated genetic differentiation to divergence in life history timing (criterion 7), we tested for associations between microsatellite genotypes and the timing of eclosion for U. canalicualtus and D. mellea. Although host-associated fitness tradeoffs (criterion 8) have been inferred for several species of Rhagoletis feeding in natal versus nonnatal fruit (33,34), difficulty in reciprocally transplanting wasps precludes these experiments at this time but remain an area for future study.…”

Gene expression plasticity across hosts of an invasive scale insect species

“…What genetic systems enable host-use promiscuity in plant eating insects? Some key host-use genes and proteins have been identified [6], and in the last few years there has been a number of studies examining how gene expression varies across hosts [7, 8]. Nevertheless, at this stage, few plant-eating insect species and host interactions have been studied, and we still know little with confidence about the genetic architecture of generalism in plant-eating insects.…”

“…The recent spate of comparative transcriptomics studies indicates that broad diets are, in fact, facilitated by differential expression of detoxification genes [8, 16, 17]. However, those studies also indicate that detoxification genes are only a small part of the picture.…”

“…Most of the significant host-induced changes in gene expression do not appear to be related to detoxification. For example, researchers have found consistent host-dependent expression of many genes involved in primary metabolism [8, 18]. Furthermore, some studies have recovered evidence of a trade-off between expression of genes for detoxification and primary metabolism [7, 18]; for some plant-eating insects, increased investment in the expression of detoxification genes may come at the cost of reduced investment in growth and reproduction.…”