Patterns of lineage-specific genome evolution in the brood parasitic black-headed duck (Heteronetta atricapilla)

Abstract

Occurring independently at seven separate origins across the avian tree of life, obligate brood parasitism is a unique suite of traits observed in only approximately 1% of all bird species. Obligate brood parasites exhibit varied physiological, morphological, and behavioural traits across lineages, but common among all obligate brood parasites is that the females lay their eggs in the nest of other species. Unique among these species is the black-headed duck (Heteronetta atricapilla), a generalist brood parasite that is the only obligate brood parasite among waterfowl. This provides an opportunity to assess evolutionary changes in traits associated with brood parasitism, notably the loss of parental care behaviours, with an unspecialized brood parasite. We generated new high-quality genome assemblies and genome annotations of the black-headed duck and three related non-parasitic species (freckled duck, African pygmy-goose, and ruddy duck). With these assemblies and existing public genome assemblies, we produced a whole genome alignment across Galloanserae to identify conserved non-coding regions with atypical accelerations in the black-headed duck and coding genes with evidence of positive selection, as well as to resolve uncertainties in the duck phylogeny. To complement these data, we sequenced a population sample of black-headed ducks, allowing us to conduct McDonald-Kreitman tests of lineage-specific selection. We resolve the existing polytomy between our focal taxa with concordance from coding and non-coding sequences, and we observe stronger signals of evolution in non-coding regions of the genome than in coding regions. Collectively, the new high-quality genomes, comparative genome alignment, and population genomics provide a detailed picture of genome evolution in the only brood parasitic duck.