Repeated divergent selection on pigmentation genes in a rapid finch radiation driven by sexual selection

Abstract

The search for molecular targets of selection is leading to a better understanding of how evolution shapes biological diversity. Instances of recent and rapid speciation are suitable for associating phenotypes with their causal genotypes, because gene flow may homogenize areas of the genome that are not under divergent selection. Locating differentiated genomic regions among taxa allows us to test associations between the genes in these regions and their contributions to phenotypic diversity. Here we study a rapid radiation of nine sympatric bird species known as southern capuchino seedeaters, which are strikingly differentiated in sexually selected characters of male plumage and song. We sequenced the genomes of 72 individuals representing a diverse set of species and associated phenotypes to search for differentiated genomic regions. We asked what genes are harbored in divergent regions and to what extent has selection on the same targets shaped phenotypic diversity across different lineages. Capuchinos show differences in a small proportion of their genomes, yet selection has acted independently on the same targets during the groups’ radiation. Many divergence peaks contain genes involved in the melanogenesis pathway, with the strongest signal originating from a regulatory region upstream of the gene coding for the Agouti-signaling protein. Across all divergence peaks, the most differentiated areas are similarly likely regulatory. Our findings are consistent with selection acting on the same genomic regions in different lineages to shape the evolution of cis-regulatory elements, which control how more conserved genes are expressed and thereby generate diversity in sexually selected traits.

Admixture mapping in a hybrid zone reveals loci associated with avian feather coloration

“…For instance, several studies have consistently identified coding changes as well as putative regulatory differences in the gene agouti signalling protein (ASIP) between birds with melanic and non-melanic plumage patches [1,14,18,28]. Our assay identified 72 SNPs within 50 kb of the ASIP coding region, but none were highly differentiated between myrtle and Audubon's warblers (average F ST in this region ¼ 0.02, lower than the genome-wide average of 0.045).…”

“…Much recent progress has been made identifying putative genes involved in generating coloration differences between related species [4,5,14,28,29,52]. In birds, coloration differences are derived primarily from two molecules-melanins and carotenoids-that have different biochemical processing [4,5].…”

“…Our goal was to quantify the genomic substrate that leads to phenotypic divergence between these warblers, in this case by identifying regions of the genome significantly associated with plumage traits and possible candidate genes within these regions. Several recent anonymous genome scans have found differentiation peaks between closely related avian taxa disproportionately populated with pigmentation genes [18,28,29]. Yet, these studies have been focused on taxon comparisons with exceptionally low levels of genome-wide divergence.…”

“…Given that the plumage traits differing between myrtle and Audubon's warblers are most strongly expressed in males in the breeding season, and that sex chromosomes have been identified in previous research as often being involved in avian plumage traits [18,[30][31][32], we expected the Z chromosome to account for more of the plumage differences between myrtle and Audubon's warblers. Recent anonymous genome scans of phenotypically distinct birds that have also investigated pigmentation have identified both a large proportion of differentiation peaks on the Z chromosome and many that include pigmentation genes [18,28,52]. For example, among Vermivora warblers and Sporophila seedeaters, two of six (33%) and 10 of 25 divergent regions (40%) were associated with the Z chromosome, respectively [18,28].…”

“…Recent anonymous genome scans of phenotypically distinct birds that have also investigated pigmentation have identified both a large proportion of differentiation peaks on the Z chromosome and many that include pigmentation genes [18,28,52]. For example, among Vermivora warblers and Sporophila seedeaters, two of six (33%) and 10 of 25 divergent regions (40%) were associated with the Z chromosome, respectively [18,28]. This contrasts to the pattern between myrtle and Audubon's warblers, which have few divergent regions on the Z chromosome [25] and, of those, only two from the current study that show a plumage association.…”