Blindsnake evolutionary tree reveals long history on Gondwana

Nicolas Vidal ( Julie Marin Marina Morini Steve Donnellan William R. Branch Richard Thomas Miguel Vences Addison Wynn Corinne Cruaud S. Blair Hedges Articles on similar topics can be found in the following collections: evolution (794 articles) molecular biology (89 articles) taxonomy and systematics (81 articles) Receive free email alerts when new articles cite this article - sign up in the box at the top right-hand corner of the article or click here - Subject collections Email alerting service To subscribe to Biol. Lett., go to: http://rsbl.royalsocietypublishing.org/subscriptions Blindsnake evolutionary tree reveals long history on Gondwana Nicolas Vidal1,*, Julie Marin1, Marina Morini1, Steve Donnellan2,3, William R. Branch4, Richard Thomas5, Miguel Vences6, Addison Wynn7, Corinne Cruaud8 and S. Blair Hedges9,* Worm-like snakes (scolecophidians) are small, burrowing species with reduced vision. Although largely neglected in vertebrate research, knowledge of their biogeographical history is crucial for evaluating hypotheses of snake origins. We constructed a molecular dataset for scolecophidians with detailed sampling within the largest family, Typhlopidae (blindsnakes). Our results demonstrate that scolecophidians have had a long Gondwanan history, and that their initial diversification followed a vicariant event: the separation of East and West Gondwana approximately 150 Ma. We find that the earliest blindsnake lineages, representing two new families described here, were distributed on the palaeolandmass of India1Madagascar named here as Indigascar. Their later evolution out of Indigascar involved vicariance and several oceanic dispersal events, including a westward transatlantic one, unexpected for burrowing animals. The exceptional diversification of scolecophidians in the Cenozoic was probably linked to a parallel radiation of prey (ants and termites) as well as increased isolation of populations facilitated by their fossorial habits. 1. INTRODUCTION Of the two major divisions of snakes, scolecophidians are the most poorly known in terms of species diversity, phylogeny, biogeography and ecology (Greene 1997). Electronic supplementary material is available at http://dx.doi.org/ 10.1098/rsbl.2010.0220 or via http://rsbl.royalsocietypublishing.org. They feed on small social insects (ants, termites and their larvae), and do so on a frequent basis (Cundall & Greene 2000). They include the smallest snakes and rarely exceed 30 cm in length (Hedges 2008). Most species have greatly reduced eyes and head scalation, a pinkish or brownish, tubular-shaped body with smooth scales, and are frequently mistaken for earthworms by non-scientists. Scolecophidians are distributed on all continents except Antarctica, but most species inhabit the southern continents and tropical islands (Uetz et al. 2010). Scolecophidians include approximately 400 species divided into three families: Anomalepididae (anomalepidids, approx. 17 species), Leptotyphlopidae (threadsnakes, approx. 120 species) and Typhlopidae (blindsnakes, approx. 260 species) (Adalsteinsson et al. 2009; Uetz et al. 2010). All three occur in the New World tropics, with the anomalepidids restricted to that region. Threadsnakes also occur in Africa, Arabia and southwest Asia, whereas blindsnakes are even more broadly distributed, occurring in Africa, Madagascar, southeastern Europe, southern Asia and Australia (Adalsteinsson et al. 2009). Remarkably, for a lineage of terrestrial vertebrates, only two higher level scolecophidian phylogenies are available. The first one is an unpublished PhD dissertation based on an analysis of mostly internal anatomy (Wallach 1998). The second is a recent molecular study of threadsnakes using sequences of nine mitochondrial and nuclear genes (Adalsteinsson et al. 2009). Snakes in general and scolecophidians in particular have a Gondwanan origin (Vidal et al. 2009). Threadsnakes originated on West Gondwana (Africa and South America), as did anomalepidids (Adalsteinsson et al. 2009). The wide distribution of blindsnakes on Gondwana, and their fossorial (burrowing) habits, suggests that continental drift influenced the early evolutionary history of this family as well. However, they lack a significant fossil record and therefore details are unclear. Did oceanic dispersals also occur? If so, which continents were occupied by blindsnakes ancestrally and which ones were colonized later by dispersal? These are questions that we address here with a new molecular dataset. 2. MATERIAL AND METHODS We constructed a molecular dataset for 96 scolecophidian species from the three recognized families, with detailed sampling of the largest family, Typhlopidae. The dataset comprised of five nuclear protein-coding genes (recombination-activating gene 1: RAG1, amelogenin: AMEL, brain-derived neurotrophic factor: BDNF, neurotrophin 3: NT3 and bone morphogenetic protein 2: BMP2) for 101 taxa (85% of the sequences were newly determined, i.e. 402 sequences that have been deposited in GenBank under accession numbers GU902304GU902705). Phylogenies were built using probabilistic approaches (maximum-likelihood (ML) and Bayesian inferences) and dating analyses were performed according to the Bayesian relaxed molecular clock approach (figure 1; electronic supplementary material). 3. RESULTS AND DISCUSSION The resulting ML and Bayesian phylogenetic trees show remarkable consistency. Among Scolecophidia, five main clades diverged in the Jurassic and Cretaceous, between 159 (154 167) and 97 (112 81) Myr ago: these are (i) anomalepidids; (ii) threadsnakes; (iii) Typhlops hedraeus (Philippines) and Typhlops mirus Af Af South America (via transatlantic dispersal) Xenotyphlopidae (Madagascar) Gerrhopilidae (out of India) Blindsnake evolution N. Vidal et al. Typhlops agoralionis Typhlops sylleptor Typhlops jamaicensis Typhlops capitulatus Typhlops sulcatus Typhlops rostellatus Typhlops lumbricalis Typhlops schwartzi Typhlops eperopeus Typhlops syntherus Typhlops catapontus Typhlops naugus Typhlops richardii Typhlops platycephalus Typhlops hypomethes Typhlops granti Typhlops geotomus Typhlops monastus Typhlops dominicanus Typhlops notorachius Typhlops anousius Typhlops anchaurus Typhlops contorhinus Typhlops arator Typhlops caymanensis Typhlops brongersmianus Typhlops reticulatus Typhlops punctatus Typhlops congestus Typhlops lineolatus Typhlops fornasinii Typhlops bibronii Rhinotyphlops mucruso Rhinotyphlops schlegelii Typhlops angolensis Typhlops elegans Typhlops sp. Typhlops obtusus Rhinotyphlops feae Rhinotyphlops newtonii Rhinotyphlops lalandei Rhinotyphlops unitaeniatus Typhlops sp. Typhlops arenarius Typhlops andasibensis Ramphotyphlops ligatus Ramphotyphlops ganei Ramphotyphlops kimberleyensis Ramphotyphlops troglodytes Ramphotyphlops unguirostris Ramphotyphlops guentheri Ramphotyphlops howi Ramphotyphlops diversus Ramphotyphlops bituberculatus Ramphotyphlops longissimus Ramphotyphlops grypus Ramphoty (...truncated)