sign in sign up
<<
Home , Anomalepididae, Gerrhopilidae, Gerrhopilus, Leptotyphlops conjunctus, Mitophis, Myriopholis

Downloaded from rsbl.royalsocietypublishing.org on July 12, 2010

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 and S. Blair Hedges

Biol. Lett. 2010 6, 558-561 first published online 31 March 2010 doi: 10.1098/rsbl.2010.0220

Supplementary data "Data Supplement" http://rsbl.royalsocietypublishing.org/content/suppl/2010/03/25/rsbl.2010.0220.DC1.ht ml References This article cites 13 articles, 2 of which can be accessed free http://rsbl.royalsocietypublishing.org/content/6/4/558.full.html#ref-list-1 Subject collections Articles on similar topics can be found in the following collections

molecular biology (265 articles) and systematics (246 articles) evolution (1811 articles) Receive free email alerts when new articles cite this article - sign up in the box at the top Email alerting service right-hand corner of the article or click here

To subscribe to Biol. Lett. go to: http://rsbl.royalsocietypublishing.org/subscriptions

This journal is © 2010 The Royal Society Downloaded from rsbl.royalsocietypublishing.org on July 12, 2010

Biol. Lett. (2010) 6, 558–561 They feed on small social insects (, and doi:10.1098/rsbl.2010.0220 their larvae), and do so on a frequent basis (Cundall & Published online 31 March 2010 Greene 2000). They include the smallest Phylogeny and rarely exceed 30 cm in length (Hedges 2008). Most have greatly reduced eyes and head scalation, a pinkish or brownish, tubular-shaped body Blindsnake evolutionary with smooth scales, and are frequently mistaken for by non-scientists. Scolecophidians are tree reveals long history distributed on all continents except Antarctica, but most species inhabit the southern continents and on Gondwana tropical islands (Uetz et al. 2010). Nicolas Vidal1,*, Julie Marin1, Marina Morini1, Scolecophidians include approximately 400 species Steve Donnellan2,3, William R. Branch4, divided into three families: (anomale- Richard Thomas5, Miguel Vences6, pidids, approx. 17 species), Addison Wynn7, Corinne Cruaud8 (threadsnakes, approx. 120 species) and (blindsnakes, approx. 260 species) (Adalsteinsson and S. Blair Hedges9,* et al. 2009; Uetz et al. 2010). All three occur in the 1 De´partement Syste´matique et Evolution, UMR 7138, C.P. 26, New World tropics, with the anomalepidids restricted Muse´um National d’Histoire Naturelle, 57 rue Cuvier, F-75231 Paris cedex 05, France to that region. Threadsnakes also occur in , 2South Australian Museum, North Terrace, Adelaide 5000, Australia Arabia and southwest Asia, whereas blindsnakes are 3Australian Centre for Evolutionary Biology and Biodiversity, University even more broadly distributed, occurring in Africa, of Adelaide 5005, Australia 4Bayworld, PO Box 13147, Humewood 6013, South Africa Madagascar, southeastern Europe, southern Asia and 5Department of Biology, University of Puerto Rico, San Juan, Australia (Adalsteinsson et al. 2009). Puerto Rico 00931-3360, USA Remarkably, for a lineage of terrestrial vertebrates, 6 Zoological Institute, Technical University of Braunschweig, only two higher level scolecophidian phylogenies are Spielmannstr. 8, 38106 Braunschweig, Germany 7Department of Vertebrate Zoology, National Museum of Natural History, available. The first one is an unpublished PhD disser- Smithsonian Institution, Washington, DC 20560-0162, USA tation based on an analysis of mostly internal anatomy 8Centre National de Se´quenc¸age, Genoscope, 2 rue (Wallach 1998). The second is a recent molecular Gaston-Cre´mieux, CP5706, 91057 Evry cedex, France study of threadsnakes using sequences of nine mito- 9Department of Biology, 208 Mueller Lab, Pennsylvania State University, University Park, PA 16802-5301, USA chondrial and nuclear genes (Adalsteinsson et al. 2009). *Authors for correspondence ([email protected]; [email protected]). Snakes in general and scolecophidians in particular Worm-like snakes (scolecophidians) are small, have a Gondwanan origin (Vidal et al. 2009). Thread- burrowing species with reduced vision. Although snakes originated on West Gondwana (Africa and largely neglected in vertebrate research, knowl- ), as did anomalepidids (Adalsteinsson edge of their biogeographical history is crucial et al. 2009). The wide distribution of blindsnakes on for evaluating hypotheses of origins. We Gondwana, and their fossorial (burrowing) habits, constructed a molecular dataset for scolecophi- suggests that continental drift influenced the early dians with detailed sampling within the largest evolutionary history of this family as well. However, family, Typhlopidae (blindsnakes). Our results they lack a significant fossil record and therefore details demonstrate that scolecophidians have had a are unclear. Did oceanic dispersals also occur? If long Gondwanan history, and that their initial so, which continents were occupied by blindsnakes diversification followed a vicariant event: the separation of East and West Gondwana approxi- ancestrally and which ones were colonized later by mately 150 Ma. We find that the earliest dispersal? These are questions that we address here blindsnake lineages, representing two new with a new molecular dataset. families described here, were distributed on the palaeolandmass of India1Madagascar named here as Indigascar. Their later evolution out of 2. MATERIAL AND METHODS Indigascar involved vicariance and several We constructed a molecular dataset for 96 scolecophidian species oceanic dispersal events, including a westward from the three recognized families, with detailed sampling of the lar- gest family, Typhlopidae. The dataset comprised of five nuclear transatlantic one, unexpected for burrowing protein-coding genes (recombination-activating gene 1: RAG1, ame- . The exceptional diversification of scole- logenin: AMEL, brain-derived neurotrophic factor: BDNF, cophidians in the Cenozoic was probably linked neurotrophin 3: NT3 and bone morphogenetic protein 2: BMP2) to a parallel radiation of prey (ants and termites) for 101 taxa (85% of the sequences were newly determined, i.e. as well as increased isolation of populations 402 sequences that have been deposited in GenBank under accession facilitated by their fossorial habits. numbers GU902304–GU902705). Phylogenies were built using probabilistic approaches (maximum-likelihood (ML) and Bayesian Keywords: biogeography; squamates; snakes; inferences) and dating analyses were performed according to the Bayesian relaxed molecular clock approach (figure 1; electronic dispersal; vicariance supplementary material).

3. RESULTS AND DISCUSSION 1. INTRODUCTION The resulting ML and Bayesian phylogenetic trees Of the two major divisions of snakes, scolecophidians show remarkable consistency. Among , are the most poorly known in terms of species diversity, five main clades diverged in the Jurassic and Cretac- phylogeny, biogeography and ecology (Greene 1997). eous, between 159 (154–167) and 97 (112–81) Myr Electronic supplementary material is available at http://dx.doi.org/ ago: these are (i) anomalepidids; (ii) threadsnakes; 10.1098/rsbl.2010.0220 or via http://rsbl.royalsocietypublishing.org. (iii) hedraeus (Philippines) and Typhlops mirus

Received 3 March 2010 Accepted 8 March 2010 558 This journal is q 2010 The Royal Society Downloaded from rsbl.royalsocietypublishing.org on July 12, 2010

Blindsnake evolution N. Vidal et al. 559

Typhlops agoralionis Typhlops sylleptor Typhlops capitulatus Typhlops sulcatus Typhlops rostellatus Typhlops lumbricalis Typhlops schwartzi Typhlops eperopeus Typhlops syntherus 152 Ma Typhlops catapontus Typhlops naugus WG Typhlops richardii Typhlops platycephalus Typhlops hypomethes EG West Indies Typhlops granti (via dispersal) Typhlops geotomus Typhlops monastus Typhlops dominicanus Typhlops notorachius Typhlops anousius Asia Typhlops anchaurus NA Typhlops contorhinus Typhlops arator Typhlops caymanensis Typhlops brongersmianus 94Ma South America Typhlops reticulatus Af (via transatlantic dispersal) Typhlops punctatus SA Typhlops congestus Im Typhlops lineolatus Typhlops fornasinii Au Typhlops bibronii An mucruso Rhinotyphlops schlegelii Africa Typhlops angolensis Typhlops elegans Typhlops sp. NA Asia Typhlops obtusus Rhinotyphlops feae Rhinotyphlops newtonii Rhinotyphlops unitaeniatus 66Ma Typhlops sp. Af Typhlops arenarius SA Madagascar Typhlops andasibensis I Ramphotyphlops ligatus M Ramphotyphlops ganei Au Ramphotyphlops kimberleyensis Ramphotyphlops troglodytes An Ramphotyphlops unguirostris Ramphotyphlops guentheri Ramphotyphlops howi Ramphotyphlops diversus Ramphotyphlops bituberculatus Typhlopidae Australia Ramphotyphlops longissimus (via dispersal) Ramphotyphlops grypus Ramphotyphlops endoterus Ramphotyphlops hamatus Ramphotyphlops australis Ramphotyphlops pilbarensis Ramphotyphlops waitii Ramphotyphlops pinguis Ramphotyphlops splendidus Ramphotyphlops bicolor Ramphotyphlops polygrammicus Acutotyphlops subocularis Acutotyphlops kunuaensis Acutotyphlops sp. Ramphotyphlops acuticaudus Ramphotyphlops sp. Ramphotyphlops lineatus Typhlopoidea Eurasia Ramphotyphlops braminus Typhlops pammeces East Gondwana Ramphotyphlops albiceps Typhlops luzonensis Typhlops vermicularis Xenotyphlopidae (Madagascar) sp. Xenotyphlops grandidieri hedraeus Breakup of Gondwana Gerrhopilus mirus (out of India) Mitophis asbolepis Mitophis leptepileptus Mitophis pyrites Siagonodon septemstriatus Epictia columbi dulcis Scolecophidia Rhinoleptus koniagui Leptotyphlopidae Guinea bicolor Myriopholis adleri West Gondwana Myriopholis algeriensis Myriopholis longicauda nigroterminus Leptotyphlops conjunctus occidentalis Anomalepididae West Gondwana squamosus Boa constrictor Tropidophis sp. scytale J Early K Late K Pg Ng

165 150 125 100 75 5065 25 0 Ma Figure 1. (Caption opposite.)

Biol. Lett. (2010) Downloaded from rsbl.royalsocietypublishing.org on July 12, 2010

560 N. Vidal et al. Blindsnake evolution

Figure 1. (Opposite.) A timetree of scolecophidians based on the analysis of DNA sequences from five nuclear protein-coding genes. Inferred biogeographical events are indicated at nodes on the timetree (clades also defined by vertical bars next to taxon names). Nodes with black circles are supported by posterior probability . 95% and ML bootstrap probability . 70%. Inset in the upper left shows positions of the continents at three periods in the Earth’s history, after Scotese (2009): Late Jurassic (152 Ma), mid-Cretaceous (95 Ma) and Mesozoic–Cenozoic boundary (66 Ma). Labels on landmasses are: Af (Africa), An (Antarctica), Au (Australia), EG (East Gondwana), I (India), M (Madagascar), Im (Indigascar), NA (North America), SA (South America) and WG (West Gondwana). Labels on the time scale are K (Cretaceous), J (Jurassic), Ng (Neogene) and Pg (Palaeogene).

(Sri Lanka); (iv) the Malagasy Xenotyphlops; and species, an African clade, a second Malagasy clade (v) all the remaining blindsnakes (Eurasia, Australasia, (separate from Xenotyphlopidae) and a South Ameri- Africa, Madagascar, South America, West Indies). The can clade spawning the West Indian radiation. These deep splits between the three main blindsnake clades clades diverged between 63 (78–49) and 59 (74–46) ((iii)–(v) above) are strongly supported (bootstrap Myr ago, just after the end-Cretaceous extinctions, as probability values, 91–100%; posterior probability was the case with microhylid and ranoid frogs (Van values, 100%) and are older than divergences among der Meijden et al. 2007). This corresponded to a all other families of living snakes (Vidal et al. 2009). time when sea levels were lower and continental con- For this reason, we erect the two newly discovered nections were forming (Smith et al. 1994; Miller clades ((iii)–(iv) above) to familial rank and redefine et al. 2005), facilitating land or flotsam dispersal the Superfamily Typhlopoidea to include only the among continents and islands. Subsequent diversifica- three blindsnake families. tion of clades during the Cenozoic was parallel to that Gerrhopilidae Vidal, Wynn, Donnellan and Hedges, of primary food sources—ants and termites (Thorne new family, with the genus Gerrhopilus Fitzinger, 1843 et al. 2000; Brady et al. 2006). The fossorial habits of as genus. Included genus: Gerrhopilus. Gerrhopilus these snakes also makes them more prone to isolation. comprises the former Typhlops ater species group Recent studies have indicated that scolecophidians (McDowell 1974), diagnosable by the presence of harbour a large hidden diversity of species (Thomas & gland-like structures ‘peppered’ over the scales of the Hedges 2007; Adalsteinsson et al. 2009). head (minimally the rostral and nasals, but often The large Eurasian/Australasian group must have other scales on the head and chin). A divided preocular originated by dispersal northwards from Gondwana— and/or ocular is common and all species have overlap as did afrophidian snakes—either out of Africa through of the preocular (or subpreocular when present) by the Europe and Asia (Laurasia) or out of India second supralabial (except G. tindalli ). Included (Gheerbrant & Rage 2006; Ali & Aitchison 2008; species are: G. andamanensis, G. ater, G. beddomii, Vidal et al. 2009). Within this group, the Australian G. bisubocularis, G. ceylonicus, G. depressiceps, G. floweri, radiation is relatively recent, 28 (19–39) Myr ago, G. fredparkeri, G. hades, G. hedraeus, G. inornatus, and apparently reached Australia by oceanic (flotsam) G. mirus, G. mcdowelli, G. oligolepis and G. tindalli. dispersal from Southeast Asia or Indonesia. Another Xenotyphlopidae Vidal, Vences, Branch and insular radiation occurred in the West Indies, Hedges, new family, with the genus Xenotyphlops originating by dispersal from South America during Wallach and Ineich, 1996 as type genus. Included the mid-Cenozoic, 33 (44–23) Myr ago, as did the genus: Xenotyphlops. Xenotyphlops is distinguishable vast majority of West Indian terrestrial vertebrates externally by its greatly enlarged and nearly circular (Hedges 2006). Finally, because all major splits rostral shield that is nearly vertical in the lateral among typhlopids are more recent than 63 (49– aspect and a single enlarged anal shield. Internally 78) Myr ago, and because Africa broke from South Xenotyphlops is unique among blindsnakes in lacking America 100 Ma, only westward—not eastward— a tracheal lung and possessing an unexpanded tracheal transatlantic dispersal can explain the presence of membrane, type G tracheal foramina and a long blindsnakes in South America. Until now, only six or heart–liver gap (Wallach et al. 2007). Included species seven transatlantic events were known in terrestrial are X. grandidieri and X. mocquardi. vertebrates, all following the prevailing westward water Threadsnakes and typhlopoids are closest relatives currents (Vidal et al.2008; Adalsteinsson et al.2009). and their divergence has been dated back to 154 Transatlantic journeys during the Cenozoic would (163–136) Myr ago (Vidal et al. 2009)and155(182– have taken at most six months (Houle 1999), not an 129) Myr ago (this study). Because West Gondwana insurmountable task for vertebrates with a low food drifted from East Gondwana (Antarctica, Madagascar, requirement and most likely travelling along with their India and Australia) 166–116 Myr ago (Ali & Aitchison invertebrate prey. Our molecular timing results support 2008) and the basal typhlopoid lineages are present on the conclusion that oceanic dispersal should not be dis- the palaeolandmass of Indigascar, it can be inferred missed as a possible biogeographical mechanism for that typhlopoids have an East Gondwanan origin. In organisms that otherwise appear to be poorly adapted turn, this infers that the split between typhlopoids and for an overseas journey (Vidal et al.2008). Thus, threadsnakes is the result of a vicariant event: the separ- blindsnakes—and scolecophidians in general—have ation of East and West Gondwana. The subsequent split had a long evolutionary history that has been influenced of Indigascar into India and Madagascar may explain by both continental drift and ancient ocean currents. the earliest divergence in the typhlopoid tree (figure 1). The Typhlopidae includes four major clades: a Eur- This work was funded by grants from the Service de asian one spawning the Australasian radiation of Syste´matique mole´culaire du Muse´um National d’Histoire

Biol. Lett. (2010) Downloaded from rsbl.royalsocietypublishing.org on July 12, 2010

Blindsnake evolution N. Vidal et al. 561

Naturelle to N.V., the NASA Astrobiology Institute and US Houle, A. 1999 The origin of platyrrhines: an evaluation of National Science Foundation to S.B.H., the Australian the Antarctic scenario and the floating island model. Department for the Environment, Water, Heritage and the Am. J. Phys. Anthropol. 109, 541–559. (doi:10.1002/ Arts’ CERF programme to S.C.D. and by the Consortium (SICI)1096-8644(199908)109:4,541::AID-AJPA9.3. National de Recherche en Ge´nomique, Genoscope. We 0.CO;2-N) thank E. Rochel for laboratory assistance and those persons McDowell, S. B. 1974 A catalogue of the snakes of New and institutions who contributed some of the tissue and Guinea and the Solomons, with special reference to DNA samples used in this study, or assisted us in the field: those in the Bernice P. Bishop Museum. K. Aplin, A. Bauer, C. Austin, L. Chirio, C. Cicero Part I. Scolecophidia. J. Herpetol. 8, 1–57. (doi:10. (MVZ), K. Coate, R. Crombie, K. Daoues, D. Dittmann 2307/1563076) (LSUMZ), P. Doughty, J. Feinstein (AMNH, Ambrose- Miller, K. G. et al. 2005 The Phanerozoic record of global Monnell), E. Greenbaum, C. Hass, T. Heger, J. Lazell, sea-level change. Science 310, 1293–1298. (doi:10. C. Marty, G. Mayer, R. Murphy (ROM), R. Platenberg, N. Puillandre, S. Richards, C. Ross, S. Thomson, 1126/science.1116412) S. Trape, USNM, J. Vindum (CAS), L. Vitt, L. Whitsed Scotese, C. R. 2009 Paleomap project. TX, USA: Paleomap and E. Wikramanayake. K. P. Schliep helped with Project. See www.scotese.com (accessed 5 February Multidivtime and J. S. Keogh commented on the 2010). manuscript. Smith, A. G., Smith, D. G. & Funnell, B. M. 1994 Atlas of Mesozoic and Cenozoic coastlines. Cambridge, UK: Cam- bridge University Press. Thomas, R. & Hedges, S. B. 2007 Eleven new species of Adalsteinsson, S. A., Branch, W. R., Trape, S., Vitt, L. J. & snakes of the genus Typhlops (Serpentes: Typhlopidae) Hedges, S. B. 2009 Molecular phylogeny, classification, from and Cuba. Zootaxa 1400, 1–26. and biogeography of snakes of the family Leptotyphlopi- Thorne, B. L., Grimaldi, D. A. & Krishna, K. 2000 Early dae (Reptilia, ). Zootaxa 2244, 1–50. fossil history of the termites. In Termites: evolution, social- Ali, J. R. & Aitchison, J. C. 2008 Gondwana to Asia: plate ity, symbioses, and ecology (eds T. Abe, D. E. Bignell & tectonics, paleogeography and the biological connectivity M. Higashi), pp. 77–93. London, UK: Kluwer Academic to the Indian sub-continent from the Middle Jurassic Publishers. through latest Eocene (166–35 Ma). Earth Sci. Rev. 88, Uetz, P., Goll, J. & Hallerman, J. 2010 The TIGR data- 145–166. (doi:10.1016/j.earscirev.2008.01.007) base.MD,USA:JCVI.Seehttp://www.reptiles-database. Brady, S. G., Schultz, T. R., Fisher, B. L. & Ward, P. S. org (accessed 25 January 2010). 2006 Evaluating alternative hypotheses for the early evol- Van der Meijden, A., Vences, M., Hoegg, S., Boistel, R., ution and diversification of ants. Proc. Natl Acad. Sci. Channing, A. & Meyer, A. 2007 Nuclear gene phylogeny USA 103, 18 172–18 177. (doi:10.1073/pnas. of narrow-mouthed toads (Family: Microhylidae) and a 0605858103) discussion of competing hypotheses concerning their Cundall, D. & Greene, H. W. 2000 Feeding in snakes. In biogeographical origins. Mol. Phylogenet. Evol. 44, Feeding, form, function, and evolution in tetrapod vertebrates 1017–1030. (doi:10.1016/j.ympev.2007.02.008) (ed. K. Schwenk), pp. 293–333. San Diego, CA: Vidal, N., Azvolinsky, A., Cruaud, C. & Hedges, S. B. 2008 Academic Press. Origin of tropical American burrowing by trans- Gheerbrant, E. & Rage, C. 2006 Paleobiogeography of atlantic rafting. Biol. Lett. 4, 115–118. (doi:10.1098/ Africa: how distinct from Gondwana and Laurasia? rsbl.2007.0531) Palaeogeogr. Palaeoclimatol. Palaeoecol. 241, 224–246. Vidal, N., Rage, J.-C., Couloux, A. & Hedges, S. B. 2009 (doi:10.1016/j.palaeo.2006.03.016) Snakes (Serpentes). In The timetree of life (eds S. B. Greene, H. W. 1997 Snakes: the evolution of mystery in nature. Hedges & S. Kumar), pp. 390–397. New York, NY: Berkeley, CA: University of California Press. Oxford University Press. Hedges, S. B. 2006 Paleogeography of the Antilles and Wallach, V. 1998 The visceral anatomy of blindsnakes and origin of West Indian terrestrial vertebrates. Ann. Missouri wormsnakes and its systematic implications (Serpentes: Bot. Garden 93, 231–244. (doi:10.3417/0026- Anomalepididae, Typhlopidae, Leptotyphlopidae). PhD 6493(2006)93[231:POTAAO]2.0.CO;2) dissertation, Northeastern University, Boston, MA. Hedges, S. B. 2008 At the lower limit of size in snakes: two Wallach, V., Mercurio, V. & Andreone, F. 2007 Rediscovery new species of threadsnakes (Squamata: Leptotyphlopi- of the enigmatic blind snake genus Xenotyphlops in north- dae: Leptotyphlops) from the Lesser Antilles. Zootaxa ern Madagascar, with description of a new species 1841, 1–30. (Serpentes: Typhlopidae). Zootaxa 1402, 59–68.

Biol. Lett. (2010)