The Build-Up of Population Genetic Divergence along the Speciation Continuum during a Recent Adaptive Radiation of Rhagoletis Flies.

Meredith M. Doellman,Stewart H. Berlocher,Thomas H. Q. Powell,Pheobe M. Deneen,Jeffrey L. Feder,James J. Smith,Glen Ray Hood

doi:10.3390/genes13020275

Abstract

New species form through the evolution of genetic barriers to gene flow between previously interbreeding populations. The understanding of how speciation proceeds is hampered by our inability to follow cases of incipient speciation through time. Comparative approaches examining different diverging taxa may offer limited inferences, unless they fulfill criteria that make the comparisons relevant. Here, we test for those criteria in a recent adaptive radiation of the Rhagoletis pomonella species group (RPSG) hypothesized to have diverged in sympatry via adaptation to different host fruits. We use a large-scale population genetic survey of 1568 flies across 33 populations to: (1) detect on-going hybridization, (2) determine whether the RPSG is derived from the same proximate ancestor, and (3) examine patterns of clustering and differentiation among sympatric populations. We find that divergence of each in-group RPSG taxon is occurring under current gene flow, that the derived members are nested within the large pool of genetic variation present in hawthorn-infesting populations of R. pomonella, and that sympatric population pairs differ markedly in their degree of genotypic clustering and differentiation across loci. We conclude that the RPSG provides a particularly robust opportunity to make direct comparisons to test hypotheses about how ecological speciation proceeds despite on-going gene flow.

Highlights

When speciation occurs in the face of documented, on-going gene flow, regions of the genome showing population genetic differentiation above neutral expectations of drift/migration balance may be inferred to contain genes under divergent selection contributing to reproductive isolation (RI)
Our results indicate that the Rhagoletis pomonella species group (RPSG) represents a nearly ideal system for testing hypotheses about how ecological and genomic divergence proceeds along the speciation continuum in the face of gene flow
Four factors set the stage for these flies providing a powerful window into the origin of biodiversity via ecological adaptation: (1) the primary axes of divergence and reproductive isolation for each case involve the same facets of host-plant adaptation [29,34,36,37], (2) each of the in-group taxa are diverging in the face of active gene flow with ancestral hawthorn R. pomonella populations (Tables S3–S5), (3) the taxa likely represent a nested radiation from the same proximate ancestral variation (Figure 2 and Figure S5), and (4) the taxa span a range of hypothesized stages along the speciation continuum (Figures 3–5)

Summary

Introduction

When speciation occurs in the face of documented, on-going gene flow, regions of the genome showing population genetic differentiation above neutral expectations of drift/migration balance may be inferred to contain genes under divergent selection contributing to RI. Analyses of how such patterns change as taxa move further along the speciation continuum can shed light on questions such as the roles that chromosome structure (i.e., chromosomal variants associated with reduced recombination), the genetic architecture of selected phenotypes (i.e., large effect mutations confined to small regions of particular chromosomes versus polygenic quantitative allelic variation distributed throughout the genome), and evolutionary coupling may play in facilitating or constraining speciation

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Results

Discussion

Conclusion