Shifting ecosystem connectivity during the Pleistocene drove diversification and gene-flow in a species complex of Neotropical birds (Tityridae: Pachyramphus)

Abstract

Aim: We aim to test the biogeographic drivers of diversification and gene-flow at the Isthmus of Panama using a species complex of suboscine birds as a case study. We specifically evaluate whether diversification in these birds is better explained by continuous parapatry or a Refuge Model of periodic isolation and gene-flow due glacial cycling. Location: The Isthmus of Panama (Neotropics). Taxon: Pachyramphus aglaiae and Pachyramphus homochrous (Aves: Tityridae). Methods: We develop an approach to distinguish among the two biogeographic hypotheses—parapatric ecological speciation versus climatically mediated speciation—by making explicit predictions for demographic history, niche evolution and change in geographic connectivity over time. We sequenced genome-wide markers (ultraconserved elements) to estimate the evolutionary and demographic history of this group. We applied both phylogenomic network analyses and demographic modelling using a supervised machine learning approach. These genetic analyses were combined with a novel distribution modelling method that estimates the probability of interspecies contact as a function of climatic conditions through time. Results: We found that both spatial and genetic analyses revealed concordant results. All speciation events occurred during the Pleistocene and were characterized by non-continuous gene-flow, supporting a scenario of climate-mediated diversification. Spatial connectivity was highest at present, consistent with our best demographic model of secondary contact. Main conclusions: This study exemplifies a mechanism by which speciation, dispersal and introgression unfold in an important region for Neotropical diversification—the Isthmus of Panama—where periods of both isolation and introgression probably drive diversification. Overall, our results are consistent with the Refuge Model of biotic diversification, but suggest that introgression may be a crucial yet underappreciated component of this classic paradigm.