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.
Highlights
An ever-increasing number of genomic studies are revealing a history of gene flow between closely related lineages (Mallet et al 2016)
We found no evidence of greater gene flow before divergence of the allopatric and sympatric P. drummondii populations (Fig. 3), the fast evolution of flower colour under strong reinforcing selection would limit our ability to distinguish between gene flow that occurred during and after flower colour divergence
Introgression can be detected with a variety of methods (Payseur & Rieseberg 2016), but most of them cannot be applied to our data given the small number of samples and the use of transcriptomes composed of short contigs
Summary
An ever-increasing number of genomic studies are revealing a history of gene flow between closely related lineages (Mallet et al 2016). The prevalence of hybridization between taxa enlivens interest in how barriers to reproduction evolve in the presence of gene flow. Reinforcement is the process through which prezygotic reproductive isolation evolves in response to selection. Extensive theoretical research has investigated how gene flow can influence the successful evolution of reproductive isolation in sympatry (e.g. Barton & De Cara 2009; Felsenstein 1981; Kirkpatrick & Servedio 1999; Liou & Price 1994; Liou & Price 1994; Sanderson 1989; Servedio & Kirkpatrick 1997; Servedio & Noor 2003), but there are few empirical studies validating this theory (but see Matute 2010)
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