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.
Highlights
The mechanisms and conditions facilitating species formation and the maintenance of species boundaries are central to our understanding the evolutionary process, wherein natural or sexual selection can often drive phenotypic differentiation and adaptive radiation
FST estimates were gen‐ erally low, there was a clear signal of geographic population struc‐ ture. Subsumed within this geographic variation, there was a signal of host‐related differentiation, with a small but significant sub‐ set of SNPs showing consistent allele frequency differences across sympatric sites. These results suggest that population structure in R. cerasi reflects both phylogeographic history and host‐related adaptation, and that host‐association may be restricting gene flow among local Prunus and Lonicera populations, a mechanism thought to contribute to ecological speciation
Our results demonstrate: (a) that R. cerasi populations appear to be genetically diverging based on their use of either Lonicera or Prunus host plants, and (b) that ddRAD‐ seq has increased resolution compared to microsatellites previously used in this system for inferring signatures of host‐associated ge‐ netic differentiation
Summary
The mechanisms and conditions facilitating species formation and the maintenance of species boundaries are central to our understanding the evolutionary process, wherein natural or sexual selection can often drive phenotypic differentiation and adaptive radiation. Theory predicts that under the ecological speciation hypothesis, regions of the genome subject to divergent environmental selection should show signifi‐ cant differentiation between populations, while those that are not should be homogenised by gene flow (Nosil, 2012) To adequately establish such a pattern requires genetically surveying not just one but multiple pairs of sympatric populations inhabiting alternative environments arrayed across the landscape (e.g., Soria‐Carrasco et al, 2014). Whether R. cer‐ asi is a panmictic generalist in Europe or whether it forms locally host‐adapted populations remains an open question To resolve these issues, we incorporated the repeated sampling of sympatric host‐associated populations and performed a genome‐wide survey of geographic and host‐related genetic differentiation for R. cerasi. Some of the specimens analysed here were genotyped for microsatellites in the study of Schuler et al (2016), allowing for comparisons between results obtained using different types of markers
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