Rain forest shifts through time and riverine barriers shaped the diversification of South American terrestrial pit vipers (Bothrops jararacussu species group)

Abstract

Aim To investigate (a) historical biogeographical connections and species interchange among rain forest habitats and (b) the role of riverine barriers on population divergence and speciation in the Neotropical region. Location Amazonia and Atlantic Forest in South America. Taxon Bothrops jararacussu species group (Serpentes: Viperidae). Methods We inferred phylogenetic relationships within Bothrops with an emphasis on the jararacussu species group under a Bayesian framework based on six molecular loci. We also used genetic coalescent simulations and approximate Bayesian computation to infer historical demography within the jararacussu group based on tests of alternative scenarios. Results We found the jararacussu species group to be monophyletic. The Atlantic Forest species B. pirajai and B. muriciensis were inferred nested within this group, closely related to B. jararacussu, confirming that Atlantic Forest species form a clade. The historical demographic analyses support vicariant separation between populations of B. brazili north and south of the Amazon River during the Miocene–Pliocene border, as well as colonization of the Atlantic Forest by a northern Amazonian ancestor in the Pleistocene. Main Conclusion The evolutionary history of the jararacussu species group sheds light on the dynamism of Neotropical rain forests over time, with at least one event of forest expansion leading to faunal interchange between Amazonian and Atlantic forests in the Pleistocene. Moreover, tests of alternative demographic scenarios suggest that the populations of B. brazili from north and south of the Amazon River originated from a vicariant event during the Miocene–Pliocene border, in agreement with the proposed age of establishment of the modern Amazon River drainage. Our results also have taxonomic implications for these medically important venomous snakes, supporting unrecognized diversity at the species level.