Impact of a putative riverine barrier on genomic population structure and gene flow in the presence of sexual selection.

Abstract

Gene flow connects populations and facilitates exchanging alleles, impacting speciation and adaptation. In Panama, lekking golden-collared and white-collared manakins (Manacus vitellinus and M. candei) interbreed in a narrow hybrid zone. Males' brilliant yellow plumage, principally controlled by the carotenoid metabolism gene BCO2, has introgressed from vitellinus into candei under sexual selection as far as the largest river in the region. Introgression is sharply limited across its lower reaches, but both color forms occur on both banks at its headwaters. Previous authors have therefore speculated that the river is a strong barrier to gene flow. In this study, we used ∼14,000 single nucleotide polymorphisms to test this hypothesis by assessing cross-river genetic differentiation and estimating gene flow. We found that, while the river clearly structured genetic variation, particularly downriver, it did not prevent extensive gene flow upriver. This result mirrors patterns observed at some of the world's largest rivers, albeit on a much smaller scale. It also implicates several alternatives to the barrier hypothesis, including that introgression is still ongoing or that selection for plumage color varies across the river-both rare phenomena to capture in nature. We recommend behavioral studies to further untangle this intriguing case of evolution in action.