The phylogenetic position of ridley's worm lizard reveals the complex biogeographic history of New World insular amphisbaenids

Abstract

The archipelago of Fernando de Noronha (FN) is located in the Equatorial South Atlantic Ocean, at 375 km off the northeastern coast of Brazil. Its endemic vertebrate land fauna is restricted to only six species, and three main hypotheses have been proposed to explain their presence in the archipelago. These hypotheses suggest FN had alternative biogeographic connections with: 1) the West Indies; 2) the South America mainland; or 3) Africa. Here, we evaluate for the first time the phylogenetic position of Amphisbaena ridleyi within the diversity of Amphisbaenia, and we infer the biogeographic processes that explain its presence in FN and its relationship with amphisbaenids from the West Indies. We analyzed a comprehensive multilocus dataset for Amphisbaenidae using maximum likelihood and time-calibrated Bayesian phylogenetic approaches. Based on our time-calibrated tree, we tested different biogeographic scenarios through historical biogeographic analyses. Our phylogenetic results for the high-level relationships of Amphisbaenia can be parenthetically summarized as (Rhineuridae, (Blanidae, (Bipedidae, (Cadeidae, (Trogonophidae, (Amphisbaenidae))))). Nine highly supported groups of species were recovered among the mainland South American amphisbaenids (SAA), whereas two phylogenetically distant groups of species were inferred for the West Indies: 1) WIC01, an Oligocene lineage present in Cuba and Hispaniola, which is the sister group of all other SAA groups; and 2) WIC02, a Miocene lineage that is restricted to southern Hispaniola and is closely related to Am. ridleyi. We estimated two events of transatlantic dispersal of amphisbaenians from Africa to West Indies: the dispersal of Cadeidae during the Middle Eocene, and the dispersal of the ancestor of Amphisbaena during the transition Eocene/Oligocene. These events were likely affected by the North Equatorial and South Equatorial currents, respectively, which have been flowing westwards since the Paleocene. The ancestral cladogenesis of Amphisbaena during the Late Oligocene is likely related to overwater dispersal events, or alternatively can be associated with the fragmentation of GAARlandia, when WIC01 was isolated in the West Indies, while the remaining groups of Amphisbaena diversified throughout the South American continent. During the Late Miocene, the ancestor of WIC02 dispersed from northern South America to the West Indies, while Am. ridleyi dispersed from the same region to FN. The overwater dispersal of WIC02 was driven by the North Brazilian Current and the dispersal of Am. ridleyi was likely influenced by the periodic shifts in direction and strength estimated for the North Equatorial Counter-Current during the Late Miocene.

Keywords: Amphisbaena ridleyi; Amphisbaenidae; Caribbean biogeography; GAARlandia; North Brazilian Current; North Equatorial Counter-Current; North Equatorial Current; South Equatorial Current.