Hybridization and the spread of the apple maggot fly, Rhagoletis pomonella (Diptera: Tephritidae), in the northwestern United States.

James J Smith,Jeffrey L Feder,Thomas H Q Powell,Robert B Goughnour,Tracy Arcella,Scott P Egan,Wee L Yee,Dietmar Schwarz,Sheina B Sim,Glen R Hood

doi:10.1111/eva.12298

Abstract

Hybridization may be an important process interjecting variation into insect populations enabling host plant shifts and the origin of new economic pests. Here, we examine whether hybridization between the native snowberry-infesting fruit fly Rhagoletis zephyria (Snow) and the introduced quarantine pest R. pomonella (Walsh) is occurring and may aid the spread of the latter into more arid commercial apple-growing regions of central Washington state, USA. Results for 19 microsatellites implied hybridization occurring at a rate of 1.44% per generation between the species. However, there was no evidence for increased hybridization in central Washington. Allele frequencies for seven microsatellites in R. pomonella were more ‘R. zephyria-like’ in central Washington, suggesting that genes conferring resistance to desiccation may be adaptively introgressing from R. zephyria. However, in only one case was the putatively introgressing allele from R. zephyria not found in R. pomonella in the eastern USA. Thus, many of the alleles changing in frequency may have been prestanding in the introduced R. pomonella population. The dynamics of hybridization are therefore complex and nuanced for R. pomonella, with various causes and factors, including introgression for a portion, but not all of the genome, potentially contributing to the pest insect's spread.

Highlights

Hybridization between closely related species can provide insights into the nature of species boundaries and the speciation process (Barton and Hewitt 1985; Arnold 1992; Harrison 1993; Mallet 2005)
Species differences None of the 19 microsatellites scored displayed a diagnostic difference between R. pomonella and R. zephyria
The difference could be explained by larger effective population sizes and/or higher microsatellite mutation rates in R. pomonella, but given the history of recent introduction and generally lower densities of the apple maggot in the Pacific Northwest (PNW), these two hypotheses seem less likely

Summary

Introduction

Hybridization between closely related species can provide insights into the nature of species boundaries and the speciation process (Barton and Hewitt 1985; Arnold 1992; Harrison 1993; Mallet 2005). Hybrids themselves may not have higher fitness, but certain genes may be favored, Apple maggot hybridization resulting in the adaptive introgression of a subset of favorable alleles into the genetic background of the alternate parental population (Seehausen 2004; Mallet 2005). The process may be detrimental to ecosystems when one species involved is invasive In this case, hybridization can contribute to the genetic extirpation of native species (Echelle and Connor 1989; Rhymer and Simberloff 1996; Huxel 1999) or help facilitate the spread of a modified form of the invader into previously unpopulated habitats (Ellstrand and Schierenbeck 2000; Perry et al 2001; Arcella et al 2013). If hybrids alter the local ecology or experience an escape from biotic factors normally constraining population densities, they can cause the loss of endemic biodiversity and ecosystem functions (Lodge et al 2012)

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Results

Conclusion