Change in sexual signaling traits outruns morphological divergence in a recent avian radiation across an ecological gradient

Abstract

The relative roles of natural and sexual selection in promoting evolutionary lineage divergence remains controversial and difficult to assess in natural systems. Local adaptation through natural selection is known to play a central role in adaptive radiations, yet secondary sexual traits can vary widely among species in recent radiations, suggesting that sexual selection may also be important in the early stages of speciation. Here we compare rates of divergence in ecologically relevant traits (morphology) and sexually selected signaling traits (coloration) relative to neutral structure in genome-wide molecular markers, and examine patterns of variation in sexual dichromatism to understand the roles of natural and sexual selection in the diversification of the songbird genus Junco (Aves: Passerellidae). Juncos include divergent lineages in Central America and several dark-eyed junco (J. hyemalis) lineages that diversified recently as the group recolonized North America following the last glacial maximum (c.a. 18,000 years ago). We found an accelerated rate of divergence in sexually selected characters relative to ecologically relevant traits. Moreover, a synthetic index of sexual dichromatism comparable across lineages revealed a positive relationship between the degree of color divergence and the strength of sexual selection, especially when controlling for neutral genetic distance. We also found a positive correlation between dichromatism and latitude, which coincides with the latitudinal pattern of decreasing lineage age but also with a steep ecological gradient. Finally, we detected an association between outlier loci potentially under selection and both sexual dichromatism and latitude of breeding range. These results suggest that the joint effects of sexual and ecological selection have played a role in the junco radiation and can be important in the early stages of lineage formation.