Late Pleistocene landscape changes and habitat specialization as promoters of population genomic divergence in Amazonian floodplain birds

Abstract

Although vicariant processes are expected to leave similar genomic signatures among codistributed taxa, ecological traits such as habitat and stratum can influence genetic divergence within species. Here, we combined landscape history and habitat specialization to understand the historical and ecological factors responsible for current levels of genetic divergence in three species of birds specialized in seasonally flooded habitats in muddy rivers and which are widespread in the Amazon basin but have isolated populations in the Rio Branco. Populations of the white-bellied spinetail (Mazaria propinqua), lesser wagtail-tyrant (Stigmatura napensis) and bicolored conebill (Conirostrum bicolor) are currently isolated in the Rio Branco by the black-waters of the lower Rio Negro, offering a unique opportunity to test the effect of river colour as a barrier to gene flow. We used ultraconserved elements (UCEs) to test alternative hypotheses of population history in a comparative phylogeographical approach by modelling genetic structure, demographic history and testing for shared divergence time among codistributed taxa. Our analyses revealed that (i) all three populations from the Rio Branco floodplains are genetically distinct from other populations along the Amazon River floodplains; (ii) these divergences are the result of at least two distinct events, consistent with species habitat specialization; and (iii) the most likely model of population evolution includes lower population connectivity during the Late Pleistocene transition (~250,000 years ago), with gene flow being completely disrupted after the Last Glacial Maximum (~21,000 years ago). Our findings highlight how landscape evolution modulates population connectivity in habitat specialist species and how organisms can have different responses to the same historical processes of environmental change, depending on their habitat affinity.

Keywords: Rio Branco; biogeographical barrier; comparative phylogeography; ecological traits; geogenomics; population structure.