Genomics and Speciation: The New World Mallard Complex

The New World (NW) mallard group includes the dichromatic mallard (Anas platyrhynchos), and four monochromatic taxa; American black duck, (A. rubripes), Mexican duck (A [p.] diazi), and two subspecies of mottled ducks (Florida, A. fulvigula fulvigula; and West Gulf Coast. A. f. maculata). Although all NW taxa are phenotypically diagnosable, resolving their taxonomic relationships has been challenging due to genomic similarities attributable to their recent ancestry and/or hybridization. Using ddRAD-seq methods, we sequenced 3,029 autosomal and 198 Z-chromosome markers from a total of 166 samples (24–43 per taxon). For both marker-types, the monochromatic taxa each clustered into independent groups; however, American black ducks were largely indistinguishable from mallards. Under a neutral scenario in which genetic divergence is driven by genetic drift, the expected ratio for Z:autosomal differentiation is < 1.33, because Z loci have 0.75 the effective population size of autosomal loci. Comparing mallards to each monochromatic taxa recovered elevated Z divergence, with Z:autosomal ratios ranging between 4 and 6.5, and evidence of divergent selection acting on 2-4% of Z-linked markers, but < 0.5% of autosomal markers. Furthermore, aligning markers along the Z chromosome revealed a region of elevated differentiation that was shared between all mallard-monochromatic comparisons; this region was less-differentiated or absent for pair-wise comparisons of monochromatic taxa. These results suggest that the Z-chromosome is at a later stage of divergence between mallards and monochromatic taxa and that this differentiation is likely driven by selection acting on traits that are Z-linked and derived in mallards. Overall, ddRAD-seq markers provided high resolution regarding the evolutionary history of the NW mallard clade. Furthermore, they revealed strong support for phylogenetic relationships within this group, suggesting that black ducks and mallards are sister species, this pair is sister to Mexican ducks, and the two mottled duck populations are a separate lineage.