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Origin and evolution of snakes and their diversification in the Neotropics: a multidisciplinary approach

Grant number: 11/50206-9
Support type:BIOTA-FAPESP Program - Thematic Grants
Duration: December 01, 2011 - November 30, 2016
Field of knowledge:Biological Sciences - Zoology
Principal Investigator:Hussam El Dine Zaher
Grantee:
Home Institution: Museu de Zoologia (MZ). Universidade de São Paulo (USP). São Paulo, SP, Brazil
Co-Principal Investigators:Erika Hingst-Zaher ; Marcio Roberto Costa Martins ; Ricardo Jannini Sawaya
Associated grant(s):14/02805-9 - Anatomy and phylogenetic relationships of a new theropod dinosaur from the early Cretaceous of Brazil and the diversification of abelisaurid dinosaurs in the early Cretaceous of Gondwana, AV.EXT
Associated scholarship(s):15/05047-0 - Taxonomic revision and phylogeny of the genus Apostolepis cope, 1862 (snakes, Dipsadidae, Xenodontinae, Elapomorphini), BP.DR
14/14364-7 - Embryonic development of the venom-delivery system in snakes: a morphological and molecular approach with emphasis on its secondary loss or reduction, BP.PD
14/11855-0 - Ecology and natural history of snakes of Atlantic Forest at Sete Barras, south of São Paulo, BP.MS
+ associated scholarships 14/01733-4 - Morphological description and phylogeny of a lizard (Reptilia, Squamata) from the lower Miocene, Chichínales formation, general Roca, Rio Negro province, Argentina, BP.MS
13/04170-8 - Historical biogeography of the snakes from open landscapes in South America, BP.PD
12/24755-8 - Phylogenetic analysis and evolution of head forms of Amphisbaenia (Reptilia, Squamata), BP.DR
12/15273-0 - Evolutionary biology and conservation of vipers, BE.PQ
12/19858-2 - Conservation biogeography of Brazilian snakes, BP.PD
12/13327-5 - Phylogeny of the tribe Tachymenini Bailey, 1967 (Serpentes, Dipsadidae, Xenodontinae), BP.DR
12/11997-3 - Taxonomic revision of the tribe Dipsadini (Serpentes: Dipsadidae: Dipsadinae), BP.DR
12/12587-3 - Feeding behavior and mechanisms in goo-eaters snakes (Dipsadidae: Dipsadinae), and its infralabial gland secretion characterization, BP.PD - associated scholarships

Abstract

We aim to describe phylogenetic, biogeographic and ecological patterns of snakes while focusing mainly on the Neotropical fauna. Further, we will explore the evolutionary processes involved in the origin of these patterns. We will use a multidisciplinary approach to investigate the evolution of the species throughout a time interval that extends from the Cretaceous to the Recent. The project will synthesize several distinct and complimentary approaches including that will encompass palaeontology, molecular biology, biogeography, comparative ecology, geometrical morphometries, comparative anatomy and embryology. To assess the origin of snakes we will use a total evidence approach (Kluge, 1989) to infer their initial diversification. This will involve a study of key fossils that represent critical groups, such as the Pachyophiidae, Madtsoidae and North American "boo ids" and their affinities with extant groups. This analysis will be extended to the Colubroides, the most speciose group of extant snakes. For this group, we will produce a phylogeny that encompasses most species in the Neotropical irradiation of the Dipsadidae, which represents one of the most speciose lineages within the Colubroides. The phylogenies of the main groups, involving fossils and present forms, and the Colubroides and Neotropical Dipsadidae will provide the historical framework required for ecological and biogeographical studies. Finally, the origin, evolution and biology of snakes provide fascinating, high-profile topics for scientific knowledge and the dissemination of educational material. In terms of educational materials, we will prepare two main products: a series of short films introducing, explaining and exploring the most intriguing features of the evolution and biology of snakes, and books and related material to be used by teachers in primary and secondary schools. (AU)

Articles published in Agência FAPESP about the research grant
Research highlights diversification in vipers 
Articles published in Revista Pesquisa FAPESP about the project
Snakes in a bind 

Scientific publications (29)
(References retrieved automatically from Web of Science and SciELO through information on FAPESP grants and their corresponding numbers as mentioned in the publications by the authors)
FRANCO, FRANCISCO L.; TREVINE, VIVIAN C.; MONTINGELLI, GIOVANNA G.; ZAHER, HUSSAM. A new species of Thamnodynastes from the open areas of central and northeastern Brazil (Serpentes: Dipsadidae: Tachymenini). SALAMANDRA, v. 53, n. 3, p. 339-350, AUG 15 2017. Web of Science Citations: 0.
FORLANI, MAURICIO C.; TONINI, JOAO F. R.; CRUZ, CARLOS A. G.; ZAHER, HUSSAM; DE SA, RAFAEL O. Molecular and morphological data reveal three new cryptic species of Chiasmocleis (Mehely1904) (Anura, Microhylidae) endemic to the Atlantic Forest, Brazil. PeerJ, v. 5, FEB 21 2017. Web of Science Citations: 0.
DOS SANTOS, MARINA MEIRELES; DA SILVA, FERNANDA MAGALHAES; HINGST-ZAHER, ERIKA; MACHADO, FABIO ANDRADE; ZAHER, HUSSAM EL DINE; DA COSTA PRUDENTE, ANA LUCIA. Cranial adaptations for feeding on snails in species of Sibynomorphus (Dipsadidae: Dipsadinae). ZOOLOGY, v. 120, p. 24-30, FEB 2017. Web of Science Citations: 0.
DE OLIVEIRA, LEONARDO; GUERRA-FUENTES, RICARDO ARTURO; ZAHER, HUSSAM. Embryological evidence of a new type of seromucous labial gland in neotropical snail-eating snakes of the genus Sibynornorphus. ZOOLOGISCHER ANZEIGER, v. 266, p. 89-94, 2017. Web of Science Citations: 0.
ALENCAR, LAURA R. V.; QUENTAL, TIAGO B.; GRAZZIOTIN, FELIPE G.; ALFARO, MICHAEL L.; MARTINS, MARCIO; VENZON, MERICIEN; ZAHER, HUSSAM. Diversification in vipers: Phylogenetic relationships, time of divergence and shifts in speciation rates. Molecular Phylogenetics and Evolution, v. 105, p. 50-62, DEC 2016. Web of Science Citations: 4.
MARITZ, BRYAN; PENNER, JOHANNES; MARTINS, MARCIO; CRNOBRNJA-ISAILOVIC, JELKA; SPEAR, STEPHEN; ALENCAR, LAURA R. V.; SIGALA-RODRIGUEZ, JESUS; MESSENGER, KEVIN; CLARK, RULON W.; SOORAE, PRITPAL; LUISELLI, LUCA; JENKINS, CHRIS; GREENE, HARRY W. Identifying global priorities for the conservation of vipers. Biological Conservation, v. 204, n. A, SI, p. 94-102, DEC 2016. Web of Science Citations: 4.
WILSON, JEFFREY A.; POL, DIEGO; CARVALHO, ALBERTO B.; ZAHER, HUSSAM. The skull of the titanosaur Tapuiasaurus macedoi (Dinosauria: Sauropoda), a basal titanosaur from the Lower Cretaceous of Brazil. Zoological Journal of the Linnean Society, v. 178, n. 3, p. 611-662, NOV 2016. Web of Science Citations: 3.
BARBO, FAUSTO E.; GASPARINI, JOAO LUIZ; ALMEIDA, ANTONIO P.; ZAHER, HUSSAM; GRAZZIOTIN, FELIPE G.; GUSMAO, RODRIGO B.; FERRARINI, JOSE MARIO G.; SAWAYA, RICARDO J. Another new and threatened species of lancehead genus Bothrops (Serpentes, Viperidae) from Ilha dos Franceses, Southeastern Brazil. Zootaxa, v. 4097, n. 4, p. 511-529, APR 4 2016. Web of Science Citations: 2.
NOBREGA, ROMULO PANTOJA; MONTINGELLI, GIOVANNA GONDIM; TREVINE, VIVIAN; FRANCO, FRANCISCO LUIS; VIEIRA, GUSTAVO H. C.; COSTA, GABRIEL C.; MESQUITA, DANIEL OLIVEIRA. Morphological variation within Thamnodynastes pallidus (Linnaeus, 1758) (Serpentes: Dipsadidae: Xenodontinae: Tachymenini). HERPETOLOGICAL JOURNAL, v. 26, n. 2, p. 165-174, APR 2016. Web of Science Citations: 1.
STENDER-OLIVEIRA, FERNANDA; MARTINS, MARCIO; MARQUES, OTAVIO A. V. Food Habits and Reproductive Biology of Tail-Luring Snakes of the Genus Tropidodryas (Dipsadidae, Xenodontinae) from Brazil. Herpetologica, v. 72, n. 1, p. 73-79, MAR 2016. Web of Science Citations: 0.
DAL VECHIO, FRANCISCO; TEIXEIRA, JR., MAURO; RECODER, RENATO SOUSA; RODRIGUES, MIGUEL TREFAULT; ZAHER, HUSSAM. The herpetofauna of Parque Nacional da Serra das Confusoes, state of Piaui, Brazil, with a regional species list from an ecotonal area of Cerrado and Caatinga. Biota Neotropica, v. 16, n. 3 2016. Web of Science Citations: 0.
RIBEIRO, SIRIA; SANTOS-, JR., ALFREDO P.; ZAHER, HUSSAM. A new species of Leposternon Wagler, 1824 (Squamata, Amphisbaenia) from northeastern Argentina. Zootaxa, v. 4034, n. 2, p. 309-324, OCT 29 2015. Web of Science Citations: 1.
FEITOSA, DARLAN TAVARES; DA SILVA, JR., NELSON JORGE; PIRES, MATHEUS GODOY; ZAHER, HUSSAM; DA COSTA PRUDENTE, ANA LUCIA. A new species of monadal coral snake of the genus Micrurus (Serpentes, Elapidae) from western Amazon. Zootaxa, v. 3974, n. 4, p. 538-554, JUN 24 2015. Web of Science Citations: 1.
GRABOSKI, ROBERTA; PEREIRA FILHO, GENTIL ALVES; ARAUJO DA SILVA, ARIANE AUXILIADORA; DA COSTA PRUDENTE, ANA LUCIA; ZAHER, HUSSAM. A new species of Amerotyphlops from Northeastern Brazil, with comments on distribution of related species. Zootaxa, v. 3920, n. 3, p. 443-452, FEB 23 2015. Web of Science Citations: 1.
GUEDES, THAIS B.; NOGUEIRA, CRISTIANO; MARQUES, OTAVIO A. V. Diversity, natural history, and geographic distribution of snakes in the Caatinga, Northeastern Brazil. Zootaxa, v. 3863, n. 1, p. 1-93, SEP 19 2014. Web of Science Citations: 6.
KLACZKO, JULIA; MONTINGELLI, GIOVANNA G.; ZAHER, HUSSAM. A combined morphological and molecular phylogeny of the genus ChironiusFitzinger, 1826 (Serpentes: Colubridae). Zoological Journal of the Linnean Society, v. 171, n. 3, p. 656-667, JUL 2014. Web of Science Citations: 4.
PIRES, MATHEUS GODOY; DA SILVA, JR., NELSON JORGE; FEITOSA, DARLAN TAVARES; DA COSTA PRUDENTE, ANA LUCIA; PEREIRA FILHO, GENTIL ALVES; ZAHER, HUSSAM. A new species of triadal coral snake of the genus Micrurus Wagler, 1824 (Serpentes: Elapidae) from northeastern Brazil. Zootaxa, v. 3811, n. 4, p. 569-584, JUN 5 2014. Web of Science Citations: 4.
GUEDES, THAIS B.; SAWAYA, RICARDO J.; NOGUEIRA, CRISTIANO DE C. Biogeography, vicariance and conservation of snakes of the neglected and endangered Caatinga region, north-eastern Brazil. Journal of Biogeography, v. 41, n. 5, p. 919-931, MAY 2014. Web of Science Citations: 12.
POL, DIEGO; NASCIMENTO, PAULO M.; CARVALHO, ALBERTO B.; RICCOMINI, CLAUDIO; PIRES-DOMINGUES, RICARDO A.; ZAHER, HUSSAM. A New Notosuchian from the Late Cretaceous of Brazil and the Phylogeny of Advanced Notosuchians. PLoS One, v. 9, n. 4 APR 2 2014. Web of Science Citations: 28.
TREVINE, VIVIAN; FORLANIL, MAURICIO C.; HADDAD, CELLO F. B.; ZAHER, HUSSAM. Herpetofauna of Paranapiacaba: expanding our knowledge on a historical region in the Atlantic forest of southeastern Brazil. Zoologia, v. 31, n. 2, p. 126-146, APR 2014. Web of Science Citations: 3.
ZAHER, HUSSAM; DE OLIVEIRA, LEONARDO; GRAZZIOTIN, FELIPE G.; CAMPAGNER, MICHELLE; JARED, CARLOS; ANTONIAZZI, MARTA M.; PRUDENTE, ANA L. Consuming viscous prey: a novel protein-secreting delivery system in neotropical snail-eating snakes. BMC Evolutionary Biology, v. 14, MAR 25 2014. Web of Science Citations: 4.
DE OLIVEIRA, LEONARDO; DA COSTA PRUDENTE, ANA LUCIA; ZAHER, HUSSAM. Unusual Labial Glands in Snakes of the Genus Geophis Wagler, 1830 ( Serpentes: Dipsadinae). Journal of Morphology, v. 275, n. 1, p. 87-99, JAN 2014. Web of Science Citations: 4.
DAMASCENO, E. M.; HINGST-ZAHER, E.; ASTUA, D. Bite force and encephalization in the Canidae (Mammalia: Carnivora). JOURNAL OF ZOOLOGY, v. 290, n. 4, p. 246-254, AUG 2013. Web of Science Citations: 7.
SCANFERLA, AGUSTIN; ZAHER, HUSSAM; NOVAS, FERNANDO E.; DE MUIZON, CHRISTIAN; CESPEDES, RICARDO. A New Snake Skull from the Paleocene of Bolivia Sheds Light on the Evolution of Macrostomatans. PLoS One, v. 8, n. 3 MAR 1 2013. Web of Science Citations: 5.
MARTINS, ITAMAR A.; ZAHER, HUSSAM. A new species of the highland frog genus Holoaden (Amphibia, Strabomantidae) from cloud forests of southeastern Brazil. Zootaxa, v. 3599, n. 2, p. 178-188, JAN 4 2013. Web of Science Citations: 2.
MOLINA, FLAVIO B.; MACHADO, FABIO A.; ZAHER, HUSSAM. Taxonomic validity of Mesoclemmys heliostemma (McCord, Joseph-Ouni & Lamar, 2001) (Testudines, Chelidae) inferred from morphological analysis. Zootaxa, n. 3575, p. 63-77, DEC 7 2012. Web of Science Citations: 2.
GRAZZIOTIN, FELIPE G.; ZAHER, HUSSAM; MURPHY, ROBERT W.; SCROCCHI, GUSTAVO; BENAVIDES, MARCO A.; ZHANG, YA-PING; BONATTO, SANDRO L. Molecular phylogeny of the New World Dipsadidae (Serpentes: Colubroidea): a reappraisal. CLADISTICS, v. 28, n. 5, p. 437-459, OCT 2012. Web of Science Citations: 36.
BARBO, FAUSTO E.; GRAZZIOTIN, FELIPE G.; SAZIMA, IVAN; MARTINS, MARCIO; SAWAYA, RICARDO J. A NEW AND THREATENED INSULAR SPECIES OF LANCEHEAD FROM SOUTHEASTERN BRAZIL. Herpetologica, v. 68, n. 3, p. 418-429, SEP 2012. Web of Science Citations: 3.
HUSSAM ZAHER; FELIPE G. GRAZZIOTIN; ROBERTA GRABOSKI; RICARDO G. FUENTES; PAOLA SÁNCHEZ-MARTINEZ; GIOVANNA G. MONTINGELLI; YA-PING ZHANG; ROBERT W. MURPHY. Phylogenetic relationships of the genus Sibynophis (Serpentes: Colubroidea). Papéis Avulsos de Zoologia (São Paulo), v. 52, n. 12, p. 141-149, 2012.

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