Climate explains recent population divergence, introgression and persistence in tropical mountains: phylogenomic evidence from Atlantic Forest warbling finches

Abstract

Taxa with disjunct distributions are common in montane biotas and offer excellent opportunities to investigate historical processes underlying genetic and phenotypic divergence. In this context, subgenomic datasets offer novel opportunities to explore historical demography in detail, which is key to better understand the origins and maintenance of diversity in montane regions. Here we used a large ultraconserved elements dataset to get insights into the main biogeographic processes driving the evolution of the Montane Atlantic Forest biota. Specifically, we studied two species of warbling finches disjunctly distributed across a region of complex geological and environmental history. We found that a scenario of three genetically differentiated populations is best supported by genomic clustering methods. Also, demographic simulations support simultaneous isolation of these populations at ~10 kya, relatively stable population sizes over recent time, and recent gene flow. Our results suggest a dual role of climate: population divergence, mediated by isolation in mountain tops during warm periods, as well as population maintenance - allowing persistence mediated by shifts in elevation distribution during periods of climate change, with episodic bouts contact and gene flow. Additional support for the role of climate comes from evidence of their contact in a recent past. We propose that two major gaps, which we call Sao Paulo and Caparao subtropical gaps, have been historically important in the divergence of cold adapted organisms in the Atlantic Forest, and could be associated to cryptic diversity. Finally, our results suggest that shallow divergence and past gene flow may be common in montane organisms, but complex demographic histories may be detectable only when using subgenomic or genomic datasets.