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 the exchange of alleles, impacting speciation and adaptation. In western Panama, lekking golden-collared and white-collared manakins (Manacus vitellinus and M. candei, respectively) interbreed in a narrow hybrid zone across which males' brilliant yellow collar plumage, principally controlled by the carotenoid metabolism gene BCO2, has introgressed from vitellinus into candei under sexual selection. Plumage introgression is sharply limited across the lower reaches of the widest river in the region, but both color morphs occur on both riverbanks at its headwaters. Previous authors have speculated that the river may be a strong barrier to gene flow, preventing further plumage color introgression, but this hypothesis has never been tested. In this study, we used between ∼10,000 and 14,000 single nucleotide polymorphisms (SNPs) to test this hypothesis by assessing genetic differentiation and estimating gene flow across the river. We found that, while the river did show a clear effect of structuring genetic variation, particularly along its wide lower reaches, it was not sufficient to prevent extensive gene flow at its narrow headwaters. This result mirrors observed patterns at some of the world's larges rivers, albeit on a much smaller scale. It also implicates several possible alternatives to the strong barrier hypothesis, including that introgression is still ongoing or that selection for plumage color varies across the river. Either scenario is rare to capture in nature, and we recommend behavioral studies to further untangle this intriguing case of evolution in action.