Spatiotemporal diversification of a low-vagility Neotropical vertebrate clade (short-tailed opossums, Didelphidae: Monodelphis)

Aim: To infer historical-biogeographical patterns and processes in South America based on estimated divergence times and ancestral distributions for a diverse clade of small marsupials (Monodelphis). Location: South America. Methods: We estimated a time-scaled phylogeny using sequence data from four nuclear genes and one mitochondrial gene for most currently recognized species, which we also scored for biome occupancy. We used maximum-likelihood methods that explicitly model historical-biogeographical processes to estimate ancestral distributions. Results: The earliest cladogenetic events in the genus occurred in the late Miocene, with subsequent diversification from the early Pliocene to the late Pleistocene. Model selection suggests an important role for founder-event speciation, a process seldom accounted for in previous biogeographical analyses of continental clades. Two equivalently optimal models that incorporate this process each reconstruct the most recent common ancestor of Monodelphis as occurring in both Amazonia and the Atlantic Forest, from which the Andes, the Arid Diagonal (Caatinga, Cerrado, Chaco) and other neighbouring biomes were colonized during the Pliocene and Pleistocene. Main Conclusions: The diversification of Monodelphis was not restricted to a narrow time interval, suggesting that speciation cannot be attributed to a single leading factor such as tectonism or Pleistocene climatic fluctuations. In particular, speciation within the Atlantic Forest biome appears to have occurred in the Neogene, whereas most Amazonian speciation events are substantially younger. Amazonia and/or the Atlantic Forest hosted most diversification events within Monodelphis and were the historical sources of lineages that subsequently colonized other areas. Founder-event speciation, a concept traditionally associated with long-distance dispersal among islands, must sustain other interpretations in historical-biogeographical analyses of non-vagile organisms in continental contexts. Possible mechanisms for founder-event speciation in Monodelphis include historically transient connections between currently disjunct biomes and rapid reproductive isolation of populations colonizing adjacent but ecologically disparate biomes.