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Origin and Hidden Diversity Within the Poorly Known Galápagos Snake Radiation (Serpentes: Dipsadidae)

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Origin and Hidden Diversity Within the Poorly Known Galápagos Snake Radiation (Serpentes: Dipsadidae) Systematics and Biodiversity ISSN: 1477-2000 (Print) 1478-0933 (Online) Journal homepage: http://www.tandfonline.com/loi/tsab20 Origin and hidden diversity within the poorly known Galápagos snake radiation (Serpentes: Dipsadidae) Hussam Zaher, Mario H. Yánez-Muñoz, Miguel T. Rodrigues, Roberta Graboski, Fabio A. Machado, Marco Altamirano-Benavides, Sandro L. Bonatto & Felipe G. Grazziotin To cite this article: Hussam Zaher, Mario H. Yánez-Muñoz, Miguel T. Rodrigues, Roberta Graboski, Fabio A. Machado, Marco Altamirano-Benavides, Sandro L. Bonatto & Felipe G. Grazziotin (2018): Origin and hidden diversity within the poorly known Galápagos snake radiation (Serpentes: Dipsadidae), Systematics and Biodiversity To link to this article: https://doi.org/10.1080/14772000.2018.1478910 View supplementary material Published online: 22 Aug 2018. Submit your article to this journal View Crossmark data Full Terms & Conditions of access and use can be found at http://www.tandfonline.com/action/journalInformation?journalCode=tsab20 Systematics and Biodiversity (2018), 0(0):1–29 Research Article Origin and hidden diversity within the poorly known Galapagos snake radiation (Serpentes: Dipsadidae) HUSSAM ZAHER1 , MARIO H. YANEZ-MU NOZ~ 2 , MIGUEL T. RODRIGUES3 , ROBERTA GRABOSKI1 , FABIO A. MACHADO4 , MARCO ALTAMIRANO-BENAVIDES5,6 , SANDRO L. BONATTO7 AND FELIPE G. GRAZZIOTIN8 1Museu de Zoologia, Universidade de S~ao Paulo, Avenida Nazare 481, Ipiranga, S~ao Paulo, SP, 04263-000, Brazil; 2Instituto Nacional de Biodiversidad, Av. De los Shyris y Rumipamba 341, Quito, Ecuador; 3Instituto de Bioci^encias, Universidade de S~ao Paulo, Rua do Mat~ao, Travessa 14, Cidade Universitaria, S~ao Paulo, SP, 05508-900, Brazil; 4Division de Mastozoologıa, Museo Argentino de Ciencias Naturales “Bernardino Rivadavia” CONICET, Av. Angel Gallardo 470, Buenos Aires (C1405DJR), Argentina; 5Instituto de Investigaciones Cientificas y Tecnologicas (INCYT), Universidad Iberoamericana del Ecuador, 9 de Octubre N25-12 y Colon, Quito, Ecuador; 6Estacion Cientıfica Amazonica Juri-Juri Kawsay, Universidad Central del Ecuador, Av. America N23-41 y Mercadillo, Quito, Ecuador; 7Laboratorio de Biologia Genomica^ e Molecular, Pontifıcia Universidade Catolica do Rio Grande do Sul, Av. Ipiranga 6681, 90619–900, Porto Alegre, RS, Brasil; 8Laboratorio de Colec¸oes~ Zoologicas, Instituto Butantan, Av. Vital Brasil, 1500, Butant~a, S~ao Paulo, SP, 05503-900, Brazil (Received 8 March 2018; Accepted 16 May 2018) Galapagos snakes are among the least studied terrestrial vertebrates of the Archipelago. Here, we provide a phylogenetic analysis and a time calibrated tree for the group, based on a sampling of the major populations known to occur in the Archipelago. Our study revealed the presence of two previously unknown species from Santiago and Rabida Islands, and one from Tortuga, Isabela, and Fernandina. We also recognize six additional species of Pseudalsophis in the Galapagos Archipelago (Pseudalsophis biserialis from San Cristobal, Floreana and adjacent islets; Pseudalsophis hoodensis from Espanola~ and adjacent islets; Pseudalsophis dorsalis from Santa Cruz, Baltra, Santa Fe, and adjacent islets; Pseudalsophis occidentalis from Fernandina, Isabela, and Tortuga; Pseudalsophis slevini from Pinzon, and Pseudalsophis steindachneri from Baltra, Santa Cruz and adjacent islets). Our time calibrated tree suggests that the genus Pseudalsophis colonized the Galapagos Archipelago through a single event of oceanic dispersion from the coast of South America that occurred at approximately between 6.9 Ma and 4.4 Ma, near the Miocene/Pliocene boundary. www.zoobank.org/urn:lsid:zoobank.org:pub:2679FD19-01E5-48FE-A0DA-A88FF145DE56 Key words: Dipsadidae; divergence time estimation; island speciation; molecular phylogeny; Pseudalsophis; Serpentes Introduction result, very little is known about their ecology, natural history, and conservation status. Despite more than 200 years of intensive research in the Snakes are very specific and unique predators within Galapagos islands, only a few systematic and ecological the reptile community of the Galapagos Islands, and it is studies, notably Van Denburgh (1912) and Thomas (1997), have been published on snakes, leading to only expected that their direct and indirect interactions can sig- preliminary taxonomic and biogeographic conclusions nificantly alter and model the community structure of ver- (Slevin, 1935; Thomas, 1997; Zaher, 1999) mostly tebrates and invertebrates of these islands. Known prey through the analysis of old museum specimens. As a include insects (grasshoppers, beetles, moths), intertidal rock marine fish (e.g., four-eyed blenny), lizards (lava-liz- ards, geckos, hatchling marine iguanas), birds (hatchling Correspondence to: Hussam Zaher. E-mail: hussam. cucuves), and small mammals (endemic rice rats) (Beebe, [email protected] 1924; Merlen & Thomas, 2013; Van Denburgh, 1912). ISSN 1477-2000 print / 1478-0933 online # The Trustees of the Natural History Museum, London, 2018. All Rights Reserved. http://dx.doi.org/10.1080/14772000.2018.1478910 Published online 22 Aug 2018 2 H. Zaher et al. In general, endemic snakes from oceanic or island eco- Materials and methods systems are particularly vulnerable/endangered, but before Specimens examined, meristic counts, and any monitoring, conservation, or management programmes can be developed, it is critical to determine the taxonomic measurements status of the Galapagos snakes, the phylogeographic struc- We examined and compared 322 specimens of ture of their recognizable populations, and their phylogen- Pseudalsophis (Table S1, see supplemental material etic affinities within the New World dipsadid radiation of online) deposited in the following institutions (acronyms snakes (Grazziotin et al., 2012;Zaheretal.,2009). used in the text are given in parentheses): Museu de The lack of previous thorough systematic treatment of Zoologia da Universidade de S~ao Paulo (MZUSP); Galapagos snakes is understandable given that most National Museum of Natural History, Washington specimens in scientific collections are unsuitable for (USNM); American Museum of Natural History, New anatomical studies or DNA extraction due to their rarity York (AMNH); Instituto Nacional de Biodiversidad, or their preservation. As such, the Galapagos snake radi- Quito (DHMECN); Museum of Vertebrate Zoology at ation remains one of the poorest known groups of ter- Berkeley (MVZ); Natural History Museum, London restrial vertebrates in the Archipelago. In order to obtain (BMNH); California Academy of Sciences, San ’ new samples that would allow a more detailed phylo- Francisco (CAS); Museum National d Histoire Naturelle genetic and taxonomic analysis of the group, we con- de Paris (MNHN); Field Museum of Natural History, ducted in June 2008 a joint expedition of the Museum Chicago (FMNH); Academy of Natural Sciences, Philadelphia (ANSP); San Diego Natural History of Zoology of the University of S~ao Paulo (MZUSP) Museum (SDNHM); Museo de Vertebrados, Fundacion and Instituto Nacional de Biodiversidad (INABIO) (for- Charler Darwin, Puerto Ayora (CDRS and MVECCD); mer Museo Ecuatoriano de Ciencias Naturales, MECN) Peabody Museum of Natural History, Yale University, that visited 14 islands and islets of the Archipelago in New Haven (YPM); Senckenberg Forschungsinstitut und 15 days (Fig. S1, see online supplemental material, Naturmuseum, Frankfurt am Main (SMF). Total length which is available from the article’s Taylor & Francis (TTL), snout–vent length (SVL), and tail length (TL) were Online page at https://doi.org/10.1080/14772000.2018. measured to the nearest 1 mm by carefully stretching the 1478910). Our new sampling represents an important specimens along a ruler. Snout length (SL), head length addition to the limited number of specimens of (HL) and head scale length were measured to the nearest 0. Galapagos snakes already preserved in museums world- 1 mm with a digital calliper. HL was measured from the tip wide and helps to fill a significant gap in our knowledge of the rostral to the retroarticular process of the lower jaw. of the group. SL was measured from the tip of the rostral to the anterior According to Zaher (1999), the Galapagos snakes are edge of the eye. Head scales were measured only on the a monophyletic group that is most closely related to the right side of the specimen. Most measures were converted ‘ ’ mainland South American Alsophis elegans and to proportions for purposes of description. Images were Saphenophis, without any special affinities to any of the taken with a digital camera and mounted in plates with the West Indian genera (Thomas, 1997). Subsequently, aid of Adobe Photoshop. Ventral scales were counted Zaher et al. (2009) erected the new genus Pseudalsophis beginning from the first preventral scale. However, preven- to accommodate the mainland Alsophis elegans and the tral numbers are given in parentheses to facilitate compari- Galapagos species, allocating both genera Pseudalsophis sons with counts from other authors that begin from the first and Saphenophis in the tribe Saphenophiini. However, ventral scale distinctly wider than long (Dowling, 1951; the phylogenetic affinities and taxonomic status of the Myers, 2003). Dorsal scales were counted in three distinct Galapagos snakes remain unsolved. Additionally, the places in the body, at the level of the first ventral scales, at phylogeographic structure of their populations along all mid-body, and five to eight dorsal scale rows prior to the 13 major
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