Recent speciation and elevated Z-chromosome differentiation between sexually monochromatic and dichromatic species of Australian teals

Abstract

Sex chromosomes potentially have an important role in speciation and often have elevated differentiation between closely related species. In birds, traits associated with male plumage, female mate preference, and hybrid fitness have been linked to the Z-chromosome (females are heterogametic, ZW). We tested for elevated Z-differentiation between two recently diverged species of Australian ducks, the sexually monochromatic grey teal Anas gracilis and the dichromatic chestnut teal A. castanea. Despite prominent morphological differences, these two species are genetically indistinguishable at both mitochondrial DNA (mean ST  0.0001) and 17 autosomal loci (mean ST  0.0056). However, we detected elevated Z-differentiation (mean ST  0.281) and tentative evidence of an island of differentiation on the Z-chromosome. is elevated differentiation was explained by a high frequency of derived alleles in chestnut teal that were absent in grey teal, which parallels independent evidence for a gain in dichromatism from a monochromatic ancestor. Coalescent estimates of demographic history and simulations indicated that the elevated Z-differentiation was unlikely to be explained by neutral processes, but instead supported a role of divergent selection. We discuss evidence for models of speciation with gene flow versus adaptive divergence in the absence of gene flow and find that both hypotheses are plausible explanations of the data. Overall, these teal have the weakest background differentiation documented to date for a species showing a large Z-effect, and they are an excellent model species for studying speciation genomics and the evolution of sexual dichromatism.