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. 2019 Oct;28(20):4648-4666.
doi: 10.1111/mec.15239. Epub 2019 Oct 13.

Host Plant-Related Genomic Differentiation in the European Cherry Fruit Fly, Rhagoletis Cerasi

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Free PMC article

Host Plant-Related Genomic Differentiation in the European Cherry Fruit Fly, Rhagoletis Cerasi

Vid Bakovic et al. Mol Ecol. .
Free PMC article

Abstract

Elucidating the mechanisms and conditions facilitating the formation of biodiversity are central topics in evolutionary biology. A growing number of studies imply that divergent ecological selection may often play a critical role in speciation by counteracting the homogenising effects of gene flow. Several examples involve phytophagous insects, where divergent selection pressures associated with host plant shifts may generate reproductive isolation, promoting speciation. Here, we use ddRADseq to assess the population structure and to test for host-related genomic differentiation in the European cherry fruit fly, Rhagoletis cerasi (L., 1758) (Diptera: Tephritidae). This tephritid is distributed throughout Europe and western Asia, and has adapted to two different genera of host plants, Prunus spp. (cherries) and Lonicera spp. (honeysuckle). Our data imply that geographic distance and geomorphic barriers serve as the primary factors shaping genetic population structure across the species range. Locally, however, flies genetically cluster according to host plant, with consistent allele frequency differences displayed by a subset of loci between Prunus and Lonicera flies across four sites surveyed in Germany and Norway. These 17 loci display significantly higher FST values between host plants than others. They also showed high levels of linkage disequilibrium within and between Prunus and Lonicera flies, supporting host-related selection and reduced gene flow. Our findings support the existence of sympatric host races in R. cerasi embedded within broader patterns of geographic variation in the fly, similar to the related apple maggot, Rhagoletis pomonella, in North America.

Keywords: RADSeq,Tephritidae; ecological speciation; host plant races.

Figures

Figure 1
Figure 1
Map of study area including 15 Rhagoletis cerasi sampling locations throughout Europe and Iran. Coloured pie charts represent sampling sites included in this study with colours corresponding to Structure analysis. Table within figure includes locations of sampling sites, population IDs used throughout this study, numbers of individuals sampled (n) and host plant from which fly samples were collected. Dark green surface represents the geographic range of the host plant Prunus avium [Colour figure can be viewed at http://wileyonlinelibrary.com]
Figure 2
Figure 2
Population structure of Rhagoletis cerasi samples across geography inferred using called genotypes at 2,494 SNPs. (a) structure plot depicting individual membership probabilities at a K = 5. Individuals are ordered according to geographic site. (b) Clustering relationships among geographic sites based on PCs calculated from the same SNP data set, using PC 1 and PC 3, which explain 8.27% and 3.23%, of the variance, respectively. (c) Bootstrapped maximum likelihood tree with individual samples at its tips. For collection site abbreviations, see Figure 1 [Colour figure can be viewed at http://wileyonlinelibrary.com]
Figure 3
Figure 3
Unrooted neighbour‐joining network of four pairs of PrunusLonicera sympatric Rhagoletis cerasi flies based on (a) 2,336 called SNPs and (b) 17 outlier SNPs. The network was generated using Nei's genetic distances and 1,000 bootstrap replicates (squares). The last letter of population labels indicates host plant of origin; P, Prunus; L, Lonicera [Colour figure can be viewed at http://wileyonlinelibrary.com]
Figure 4
Figure 4
Discriminant analysis of principal components plot of scores of individual Rhagoletis cerasi flies for discriminant functions 1 (85.24% variation explained) vs. 2 (10.33% variation explained) for individual Prunus and Lonicera flies from one sympatric site in Norway (NO) and three sympatric sites in Germany (DE). All population labels ending with a letter “L”, represent Lonicera flies and population labels ending with a letter “P”, represent Prunus flies. For additional clarity, Prunus flies are represented by squares, while Lonicera flies by circles. The inset plot shows a histogram of DA eigenvalues, providing a relative measure of the ratio of geography vs. host plant variation explained by discriminant functions 1 and 2 for the PCs retained (13) in the DAPC analysis [Colour figure can be viewed at http://wileyonlinelibrary.com]
Figure 5
Figure 5
Discriminant analysis of principal components partially discriminates Prunus‐ and Lonicera‐associated Rhagoletis cerasi flies. The first column (a, c, e, g) displays kernel density plots illustrating the distribution of individual discriminant function 1 scores for flies sampled from Prunus (red) and Lonicera (grey) hosts. The second column (b, d, f, h) displays assignment probabilities to Prunus and Lonicera (again, red and grey, respectively). The rows represent different geographic sites. Number of retained principal components (PCs), mean assignment probabilities to the correct host (AP), and p‐value testing whether assignment probabilities were greater than expected by chance (P) were as follows: (a,b) Norway, Grimstadt (NO‐G), PCs = 1, AP = 0.634 ± 0.056 SE, p = .005; (c,d) Germany, Ober‐Ramstadt (DE‐O), PCs = 1, AP = 0.791 ± 0.056 SE, p < 1e−4; (e,f) Germany, Dossenheim (DE‐D), PCs = 3, AP = 0.771 ± 0.088 SE, p = .018; (g,h) Germany, Witzenhausen (DE‐W), PCs = 1, AP = 0.638 ± 0.056 SE, p = .003 [Colour figure can be viewed at http://wileyonlinelibrary.com]
Figure 6
Figure 6
Pie chart and violin plots representing shared and nonshared host adaptation in four sympatric Prunus‐Lonicera Rhagoletis cerasi flies. (a) comparison of number of differentiated SNPs found only within one site with number of differentiated SNPs shared by more than one site. (b) Nevertheless, within this minority, a significant amount of shared differentiation is found by looking at comparisons of observed numbers of shared SNPs (red stars) with simulated distributions (violins) of differentiated SNPs that are found in any two, three and all four population pairs. Horizontal lines within the violins are the 0.025 and 0.975 quantiles [Colour figure can be viewed at http://wileyonlinelibrary.com]
Figure 7
Figure 7
Venn diagram showing overlap of SNPs differentiating the host races found using three different analyses; bayenv2 (n = 24), SNPs showing significant allele frequency differences in at least three of the four sympatric PrunusLonicera sites (n = 134), highest contributing SNPs to discriminant function 2 of the host race DAPC analysis (n = 24). SNPs identified with at least two different analyses (n = 17) are considered putative candidate SNPs under host‐related divergent selection

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