Genomic evidence of gene flow during reinforcement in Texas Phlox

Abstract

Gene flow can impede the evolution of reproductive isolating barriers between species. Reinforcement is the process by which prezygotic reproductive isolation evolves in sympatry due to selection to decrease costly hybridization. It is known that reinforcement can be prevented by too much gene flow, but we still do not know how often have prezygotic barriers evolved in the presence of gene flow or how much gene flow can occur during reinforcement. Flower colour divergence in the native Texas wildflower, Phlox drummondii, is one of the best-studied cases of reinforcement. Here we use genomic analyses to infer gene flow between P. drummondii and a closely related sympatric species, Phlox cuspidata. We de novo assemble transcriptomes of four Phlox species to determine the phylogenetic relationships between these species and find extensive discordance among gene tree topologies across genes. We find evidence of introgression between sympatric P. drummondii and P. cuspidata using the D-statistic, and use phylogenetic analyses to infer the predominant direction of introgression. We investigate geographic variation in gene flow by comparing the relative divergence of genes displaying discordant gene trees between an allopatric and sympatric sample. These analyses support the hypothesis that sympatric P. drummondii has experienced gene flow with P. cuspidata. We find that gene flow between these species is asymmetrical, which could explain why reinforcement caused divergence in only one of the sympatric species. Given the previous research in this system, we suggest strong selection can explain how reinforcement successfully evolved in this system despite gene flow in sympatry.

The relationship between postmating reproductive isolation and reinforcement inPhlox

“…Taken together, the genomic evidence of asymmetric gene flow (Roda et al. ) and our evidence of strong reproductive barriers to gene flow into both species, support the hypothesis that the higher frequency of hybrid introgression experienced by P. drummondii relative to P. cuspidata can explain why phenotypic divergence evolved in P. drummondii .…”

“…Genome wide patterns of genetic variation indicate there is asymmetric gene flow from P. cuspidata into P. drummondii , which could result in stronger reinforcing selection for P. drummondii than P. cuspidata (Roda et al. ). While our RI data suggest it should be easier for more hybrids to be mothered by P. cuspidata than by P. drummondii , in the field most hybrids are mothered by P. drummondii (Ferguson ), and backcrossing likely occurs more frequently into P. drummondii than into P. cuspidata .…”

“…The genetic basis of RI in Phlox is currently unknown, but the lack of an association between RI and phylogenetic distance may suggest that a few genes of large effect, or changes in chromosomal structure (Edmands ) underlie RI, or that incomplete lineage sorting or introgression within this clade (Roda et al. ) is obscuring the relationship between phylogenetic distance and RI. It is worth noting that we used three species pairs in this study, and studies incorporating many more species pairs would be useful to test the general hypothesis that stronger postmating RI is associated with a higher occurrence of reinforcement across taxa.…”

“…The species diverged about two million years ago and, although there is extensive discordance across gene trees, P. drummondii and P. roemeriana are sister taxa while P. cuspidata is sister to that pair (Roda et al. ). All three species have light‐blue flowers throughout most of their ranges.…”

Correlated evolution of self and interspecific incompatibility across the range of a Texas wildflower

“…Phlox drummondii pollen is completely compatible on P. cuspidata stigmas but the reciprocal cross is usually less successful (Suni & Hopkins, ). Phlox drummondii and P. cuspidata hybridize in areas where they grow sympatrically (Levin, ; Ferguson et al ., ; Roda et al ., ). Both species have similar light‐blue flowers in allopatry, but in sympatry, P. drummondii has dark‐red flowers (Levin, ).…”