Plastic and evolved responses to host fruit in apple maggot flies

Phil Huntley-Franck

The apple maggot fly, Rhagoletis pomonella, which is so much prettier than its name implies! Photo by Phil Huntley-Franck,

The apple maggot fly, Rhagoletis pomonella, is a prominent system for the study of sympatric speciation. Sister taxa in the R. pomonella species complex, the apple-infesting race of R. pomonella and the snowberry-infesting R. zephyria, have sympatric distributions and the fruiting time of their preferred hosts widely overlaps. However, apple trees and snowberry fruits contain distinct secondary metabolites that have toxic effects on herbivorous insects and may facilitate adaptive divergence in Rhagoletis.
In their new Molecular Ecology paper, Ragland et al. performed reciprocal transplants and measured variation in performance (larval survivorship, larval development time, and pupal mass) and gene expression in fly larvae of the apple-infesting R. pomonella and R. zephyria raised on different host fruit. The aim of the study was to examine the plastic and evolved performance differences between R. pomonella and R. zephyria, which hybridize with low frequency in the field but remain genetically and morphologically distinct.  

The rapidity with which new host races can form in the Rhagoletis species complex suggests that larvae are able to respond to different and potentially toxic host fruit environments with sufficient plasticity to exploit the new host, even if performance is initially poor.

Ragland et al. found that larval survival in R. pomonella was significantly higher when flies were raised on apples, their native host fruit. While there was a decrease in larval survival in R. zephyria raised on apples (their non-native fruit), it was not significant. Rhagoletis zephyria larvae took longer to develop, but were larger, when reared on apple versus snowberry hosts. However, previous studies have shown negative consequences for longer development time because fruit is often parasitized and/or rots a faster rate in the field compared to lab conditions, leading to larval mortality. Taken together, these results suggest host-related fitness trade-offs in R. zephyria.
Because only 10% of R. pomonella raised on snowberries survived, Ragland et al. focused their transcriptomic analyses on the plastic response of R. zephyria raised in snowberry vs. apple hosts and the evolved differences between R. zephyria and R. pomonella raised on apples. 20% of transcripts were significantly differentially expressed between R. zephyria raised on snowberries (native host) versus apples (non-native host). These differences represent plastic responses in gene expression in R. zephyria larvae associated with feeding in the novel apple host. An even higher number of genes (30%) was differentially expressed between R. pomonella and R. zephyria when both species were raised on apples, representing evolved differences between species.
In terms of function, many differentially expressed genes with expression patterns consistent with selection to maintain the plastic response of R. zephyria raised on the non-native apple were candidates for detoxification responses:

Detoxification-related genes are strong candidates likely to underlie the ability of the flies to initially colonize (through plastic expression) and subsequently adapt (through evolution of expression levels) to host fruits with different suites of chemical defenses.

Ragland, G. J., Almskaar, K., Vertacnik, K. L., Gough, H. M., Feder, J. L., Hahn, D. A., & Schwarz, D. (2015). Differences in performance and transcriptome‐wide gene expression associated with Rhagoletis (Diptera: Tephritidae) larvae feeding in alternate host fruit environments. Molecular Ecology. DOI: 10.1111/mec.13191

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