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

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.

Keywords: Rhagoletis zephyria; Washington state; insect pest; introgression; microsatellites; snowberries.

Figure 1

Map of the nine paired collection sites in Washington (WA) state genetically analyzed in the study. 1 = Bellingham; 2 = Vancouver, Washington State University campus; 3 = Vancouver; Burnt Bridge Creek Greenway; 4 = St. Cloud Park; 5 = Beacon Rock State Park; 6 = Home Valley; 7 = Klickitat; 8B = Burbank black hawthorn; 8W = Walla Walla snowberry; 9 = Tampico near Yakima. See Table S1 for site descriptions. Arrows denote spread of R. pomonella north and south along the western side of the Cascade Mountains and eastward into the Columbia River gorge following its putative introduction into Portland, OR. Black hawthorn-infesting populations of the fly have now encroached on the commercial apple-growing region of central WA centered in Yakima.

Figure 2

Neighbor-joining network for the nine paired black hawthorn-infesting R. pomonella (unfilled circles) and snowberry-infesting R. zephyria populations (dark triangles) in WA based on Nei's overall genetic distances for 19 microsatellite loci. See Fig. 1 legend and Table S1 for descriptions of the nine paired sites designated. Bootstrap support values based on 10 000 replicates are given for the node separating R. pomonella and R. zephyria populations.

Figure 3

STRUCTURE bar plots for four paired sites at (A) St. Cloud Park; (B) Beacon Rock State Park; (C) Home Valley; and (D) Burbank/Walla Walla, WA, depicting posterior probabilities of individual R. pomonella black hawthorn fly genotypes (on left) and R. zephyria snowberry fly genotypes (on right) belonging to one of four genotypic classes: pure R. pomonella origin (black), pure R. zephyria (light gray), F1 hybrid (red), or backcross (blue), based on genotypes at 19 microsatellite loci. Bars along the x-axis represent individual flies.

Figure 4

Association between mean allele frequency difference for 19 microsatellite loci between R. zephyria and R. pomonella populations at each of the nine paired sites plotted against each pairs geographic distance to the Tampico unincorporated community near Yakima, WA. Best fit line added to illustrate association. Note: the mean allele frequency difference at the Klickitat site was based on only 17 loci.