Amazonian Amphibian Diversity Is Primarily Derived from Late Miocene Andean Lineages

Abstract

The Neotropics contains half of remaining rainforests and Earth's largest reservoir of amphibian biodiversity. However, determinants of Neotropical biodiversity (i.e., vicariance, dispersals, extinctions, and radiations) earlier than the Quaternary are largely unstudied. Using a novel method of ancestral area reconstruction and relaxed Bayesian clock analyses, we reconstructed the biogeography of the poison frog clade (Dendrobatidae). We rejected an Amazonian center-of-origin in favor of a complex connectivity model expanding over the Neotropics. We inferred 14 dispersals into and 18 out of Amazonia to adjacent regions; the Andes were the major source of dispersals into Amazonia. We found three episodes of lineage dispersal with two interleaved periods of vicariant events between South and Central America. During the late Miocene, Amazonian, and Central American-Chocoan lineages significantly increased their diversity compared to the Andean and Guianan-Venezuelan-Brazilian Shield counterparts. Significant percentage of dendrobatid diversity in Amazonia and Chocó resulted from repeated immigrations, with radiations at <10.0 million years ago (MYA), rather than in situ diversification. In contrast, the Andes, Venezuelan Highlands, and Guiana Shield have undergone extended in situ diversification at near constant rate since the Oligocene. The effects of Miocene paleogeographic events on Neotropical diversification dynamics provided the framework under which Quaternary patterns of endemism evolved.

Author Summary

The Neotropics, which includes South and Central America, contains half of remaining rainforests and the largest reservoir of amphibian diversity. Why there are so many species in certain areas and how such diversity arose before the Quaternary (i.e., more that 1.8 million years ago [MYA]) are largely unstudied. One hypothesis is that the Amazon Basin was the key source of diversity, and species dispersed from there to other areas. Here, we reconstruct a time-calibrated phylogeny and track, in space and time, the distribution of the endemic and species-rich clade of poison frogs (Dendrobatidae) during the Cenozoic (more than 65 MYA) across the continental Neotropics. Our results indicate a far more complex pattern of lineage dispersals and radiations during the past 10 MY. Rather than the Amazon Basin being the center of origin, our results show that the diversity stemmed from repeated dispersals from adjacent areas, especially from the Andes. We also found a recurrent pattern of colonization of Central America from the Chocó at 4–5 MY earlier than the formation of the Panamanian Land Bridge at 1.5 MYA. Thus, the major patterns of dispersals and radiations in the Neotropics were already set by ∼5–6 MYA (the Miocene–Pliocene boundary), but the ongoing process of Neotropical radiation is still happening now, especially in the Chocó–Central America region and Amazonian rainforest.

Abstract

Phylogenetic analysis and ancestral range modeling of the poison-frog clade (Dendrobatidae) indicates that Amazonian species richness derives from repeated dispersals from adjacent regions, especially the Andes.