Comparative population genomics reveals convergent adaptation across independent origins of avian obligate brood parasitism

Abstract

Parental care evolved as a strategy to enhance offspring survival at the cost of reduced fecundity. While most birds provide parental care, obligate brood parasites circumvent this tradeoff by exploiting the parental behavior of other species. This radical life history shift has occurred independently seven times in birds, offering an outstanding opportunity to test for convergent patterns of adaptation in the genome. To investigate genomic adaptations underlying this transition, we analyzed population resequencing data from five brood-parasitic species across three independent origins of brood parasitism -- three parasitic finches (family Viduidae), a honeyguide, and a cowbird -- alongside related non-parasitic (parental) outgroups. Using the McDonald-Kreitman framework, we found evidence for repeated adaptation in genes involved in spermatogenesis and sperm function in multiple parasitic clades, but not in the matched outgroup parental species. This is consistent with evidence for increased male-male competition in parasitic lineages as a result of the loss of parental care. In addition, we detected selective sweeps near genes associated with nervous system development in parasitic lineages, perhaps associated with improved spatial cognition that aids brood parasites in locating, monitoring, and laying eggs in host nests. Finally, we found more selective sweeps in host-specific brood parasites as compared to parental outgroups, perhaps reflecting ongoing host-parasite coevolutionary arms races.