Explosive Pleistocene range expansion leads to widespread Amazonian sympatry between robust and gracile capuchin monkeys

Aim Capuchin monkey species are widely distributed across Central and South America. Morphological studies consistently divide the clade into robust and gracile forms, which show extensive sympatry in the Amazon Basin. We use genetic data to test whether Miocene or Plio-Pleistocene processes may explain capuchin species present distributions, and consider three possible scenarios to explain widespread sympatry. Location The Neotropics, including the Amazon and Atlantic Coastal Forest. Methods We sequenced the 12S ribosomal RNA and cytochrome b genes from capuchin monkey specimens. The majority were sampled from US museum collections and were wild-caught individuals of known provenance across their distribution. We applied a Bayesian discrete-states diffusion model, which reconstructed the most probable history of invasion across nine subregions. We used comparative methods to test for phylogeographic association and dispersal rate variation. Results Capuchins contained two well supported monophyletic clades, the morphologically distinct ` gracile' and ` robust' groups. The time-tree analysis estimated a late Miocene divergence between Cebus and Sapajus and a subsequent Plio-Pleistocene diversification within each of the two clades. Bayesian analysis of phylogeographic diffusion history indicated that the current wide-ranging sympatry of Cebus and Sapajus across much of the Amazon Basin was the result of a single explosive late Pleistocene invasion of Sapajus from the Atlantic Forest into the Amazon, where Sapajus is now sympatric with gracile capuchins across much of their range. Main conclusions The biogeographic history of capuchins suggests late Miocene geographic isolation of the gracile and robust forms. Each form diversified independently, but during the Pleistocene, the robust Sapajus expanded its range from the Atlantic Forest to the Amazon, where it has now encroached substantially upon what was previously the exclusive range of gracile Cebus. The genus Cebus, as currently recognized, should be split into two genera to reflect the Miocene divergence and two subsequent independent Pliocene radiations: Cebus from the Amazon and Sapajus from the Atlantic Forest.