Genomic evidence for convergent evolution of a key trait underlying divergence in island birds

Reproductive isolation can be initiated by changes in one or a few key traits that prevent random mating among individuals in a population. During the early stages of speciation, when isolation is often incomplete, there will be a heterogeneous pattern of differentiation across regions of the genome between diverging populations, with loci controlling these key traits appearing the most distinct as a result of strong diversifying selection. In this study, we used Illumina-sequenced ddRAD tags to identify genomewide patterns of differentiation in three recently diverged island populations of the Monarcha castaneiventris flycatcher of the Solomon Islands. Populations of this species have diverged in plumage colour, and these differences in plumage colour, in turn, are used in conspecific recognition and likely important in reproductive isolation. Previous candidate gene sequencing identified point mutations in MC1R and ASIP, both known pigmentation genes, to be associated with the difference in plumage colour between islands. Here, we show that background levels of genomic differentiation based on over 70,000 SNPs are extremely low between populations of distinct plumage colour, with no loci reaching the level of differentiation found in either candidate gene. Further, we found that a phylogenetic analysis based on these SNPs produced a taxonomy wherein the two melanic populations appear to have evolved convergently, rather than from a single common ancestor, in contrast to their original classification as a single subspecies. Finally, we found evidence that the pattern of low genomic differentiation is the result of both incomplete lineage sorting and gene flow between populations.