Major Caribbean and Central American frog faunas originated by ancient oceanic dispersal

Abstract

Approximately one-half of all species of amphibians occur in the New World tropics, which includes South America, Middle America, and the West Indies. Of those, 27% (801 species) belong to a large assemblage, the eleutherodactyline frogs, which breed out of water and lay eggs that undergo direct development on land. Their wide distribution and mode of reproduction offer potential for resolving questions in evolution, ecology, and conservation. However, progress in all of these fields has been hindered by a poor understanding of their evolutionary relationships. As a result, most of the species have been placed in a single genus, Eleutherodactylus, which is the largest among vertebrates. Our DNA sequence analysis of a major fraction of eleutherodactyline diversity revealed three large radiations of species with unexpected geographic isolation: a South American Clade (393 sp.), a Caribbean Clade (171 sp.), and a Middle American Clade (111 sp.). Molecular clock analyses reject the prevailing hypothesis that these frogs arose from land connections with North and South America and their subsequent fragmentation in the Late Cretaceous (80-70 Mya). Origin by dispersal, probably over water from South America in the early Cenozoic (47-29 million years ago, Mya), is more likely.

Fig. 1.

Composite distribution of eleutherodactyline frogs and Brachycephalus (812 sp.). “Middle America” refers to Central America and Mexico. No evolutionary groupings are implied.

Fig. 2.

Major clades of eleutherodactyline frogs. (a) ML phylogeny of 280 species of frogs including eleutherodactylines, Brachycephalus, and three out-group species. Species are numbered according to SI Table 4. Major groups with support values (ML bootstrap/ME bootstrap/Bayesian posterior probability), number of species sampled, and total number of described species per clade are indicated. ML, ME, and Bayesian trees including taxon names and all confidence values are available (SI Figs. 5–7). (b) Distribution of Caribbean, Middle American, and South American clades.

Fig. 3.

A time tree of eleutherodactyline frogs. The tree topology is derived from a ML analysis of 61 eleutherodactylines, Brachycephalus, and three out-group species. Support values for groups mentioned in the text are indicated at nodes (ML/ME/Bayesian posterior probability). Calibration nodes are indicated by open circle (minimum constraint), filled circles (maximum constraint), or filled square (minimum and maximum constraints). The two proposed oceanic dispersal events are on the branches leading to the Caribbean Clade (CC) and the Middle American Clade (MAC). [The South American Clade (SAC) and Southeast Brazil Clade (SBC) are indicated.] Times and credibility intervals for numbered nodes are shown in Table 1. Geologic epochs are abbreviated as follows: Paleocene (Pa), Eocene (E), Oligocene (O), Miocene (M), Pliocene (P), Pleistocene (Pl), Holocene (H).

Fig. 4.

Biogeographic model showing the origin of the Middle American and Caribbean clades of eleutherodactyline frogs. Location of exposed land is conjectural and based on a synthesis of models (24, 25, 50). Landmasses are abbreviated as follows: North America (NA), Middle America (MA), South America (SA), Proto-Antilles (PA), Cuba (Cu), Hispaniola (H), Puerto Rico (PR), Lesser Antilles (LA), Jamaica (Ja), Bahama Bank (BB). (a) Middle Eocene (49–37 Mya), when dispersal over water from South America probably occurred, leading to the origin of the Middle American Clade (MAC) and Caribbean Clade (CC). (b) Early Oligocene (≈30 Mya), when land subsidence and higher sea levels led to isolation of a western Caribbean (WCC) lineage on Cuba and an eastern Caribbean (ECC) lineage on Hispaniola and Puerto Rico. (c) Early Miocene (≈20 Mya), when dispersal from Cuba to the mainland led to a radiation of the subgenus Syrrhopus in southern North America and northern Middle America and when the Lesser Antilles were colonized by members of the ECC and South American Clade (SAC). (d) Pliocene (≈3 Mya), when closing of the Isthmus of Panama allowed overland dispersal of species of the MAC to South America and species of the SAC to Middle America.