Quantitative species delimitation, tests for gene flow, and migration models uncover complex, recent speciation in tree squirrels

Accurate estimates of species diversity are essential for all biodiversity research. Delimiting species and understanding the underlaying processes of speciation are also central components of systematic biology that outline our comprehension of the evolutionary mechanisms generating biodiversity. We obtained genomic data (Ultraconserved Elements and single nucleotide polymorphisms) for a widespread genus of South American tree squirrels (genus Guerlinguetus) to explore alternative hypotheses on species limits and to clarify recent and rapid speciation on continental-scale and dynamically evolving landscapes. Using a multilayered genomic approach that integrates fine-scale population genetic analyses with quantitative molecular species delimitation methods, we observed that (i) the most likely number of species within Guerlinguetus is six, contrasting with both classic morphological revision and mitochondrial species delimitation; (ii) incongruencies in species relationships still persist, which might be a response to population migration and gene flow taking place in lowlands of eastern Amazonia; and (iii) effective migration surfaces detected important geographic barriers associated with the major Amazonian riverine systems and the mountain ranges of the Guiana shield. In conclusion, we uncovered unexpected species diversity of keystone mammals that are critical in tree-seed predation and dispersal in one of the most fragile and threated ecosystems of the world, the tropical rainforests of South America. Our results corroborate recent findings suggesting that much of the extant species-level diversity in Amazonia is young, dating back to the Quaternary, while also reinforcing long-established hypotheses on the role of rivers and climate-driven forest dynamics triggering Amazonian speciation.