Gene flow, divergent selection and resistance to introgression in two species of morning glories (Ipomoea)

Gene flow is thought to impede genetic divergence and speciation by homogenizing genomes. Recent theory and research suggest that sufficiently strong divergent selection can overpower gene flow, leading to loci that are highly differentiated compared to others. However, there are also alternative explanations for this pattern. Independent evidence that loci in highly differentiated regions are under divergent selection would allow these explanations to be distinguished, but such evidence is scarce. Here, we present multiple lines of evidence that many of the highly divergent SNPs in a pair of sister morning glory species, Ipomoea cordatotriloba and I. lacunosa, are the result of divergent selection in the face of gene flow. We analysed a SNP data set across the genome to assess the amount of gene flow, resistance to introgression and patterns of selection on loci resistant to introgression. We show that differentiation between the two species is much lower in sympatry than in allopatry, consistent with interspecific gene flow in sympatry. Gene flow appears to be substantially greater from I. lacunosa to I. cordatotriloba than in the reverse direction, resulting in sympatric and allopatric I. cordatotriloba being substantially more different than sympatric and allopatric I. lacunosa. Many SNPs highly differentiated in allopatry have experienced divergent selection, and, despite gene flow in sympatry, resist homogenization in sympatry. Finally, five out of eight floral and inflorescence characteristics measured exhibit asymmetric convergence in sympatry. Consistent with the pattern of gene flow, I. cordatotriloba traits become much more like those of I. lacunosa than the reverse. Our investigation reveals the complex interplay between selection and gene flow that can occur during the early stages of speciation. see also the Perspective by Field and Fraïsse