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Dimensions US-BIOTA São Paulo: scales of biodiversity: integrated studies of snake venom evolution and function across multiple levels of diversity

Grant number: 16/50127-5
Support type:BIOTA-FAPESP Program - Thematic Grants
Duration: September 01, 2016 - August 31, 2023
Field of knowledge:Interdisciplinary Subjects
Cooperation agreement: NSF - Dimensions of Biodiversity and BIOTA
Principal researcher:Inácio de Loiola Meirelles Junqueira de Azevedo
Grantee:Inácio de Loiola Meirelles Junqueira de Azevedo
Principal researcher abroad: Christopher Parkinson
Institution abroad: University of Central Florida (UCF), United States
Principal researcher abroad: Harold Lisle Gibbs
Institution abroad: Ohio State University, Columbus, United States
Principal researcher abroad: Darin Rokita
Institution abroad: Florida State University, United States
Home Institution: Instituto Butantan. Secretaria da Saúde (São Paulo - Estado). São Paulo , SP, Brazil
Pesquisadores principais:
Ana Maria Moura da Silva ; Erika Hingst-Zaher ; Hussam El Dine Zaher
Associated scholarship(s):22/07935-4 - "Scales of biodiversity: Integrated studies of snake venom evolution and function across multiple levels of diversity"., BP.TT
22/05111-4 - Production of a digital exhibition about venoms and snakes, BP.TT
22/05063-0 - Training in techniques of generation and analysis of transcriptomes, BP.TT
+ associated scholarships 21/13671-7 - Fieldwork assistance for specimen collection, venom and glands - focused in extreme southern Brazil, BP.TT
21/09643-8 - Support and supervision for bioinformatic analysis in Scales of Biodiversity project, BP.TT
21/09929-9 - Production of a digital exhibit on venoms and snakes, BP.TT
21/10174-2 - Composition and evolution of venom in snakes from the tribe Hydropsini, BP.MS
20/15370-1 - Assistance and organization of expeditions to collect species of Brazilian snakes and assistance in curating the herpetological collection (specimens, tissue, glands and poisons) of the Butantan Institute: organization and management of animals in the vivarium, BP.TT
21/06270-6 - Support to the production of content to exhibitions and scientific dissemination, related to the evolution of snakes and their venom, BP.TT
20/02284-0 - Assistance for nucleic acid preparation and new generation sequencing, BP.TT
20/00235-1 - Support to the production of content for scientific dissemination, and activities related to the evolution of snakes and their venom, BP.TT
19/24505-0 - Support to the production of contents and material for scientific dissemination related to the scales of biodiversity project, BP.TT
19/21643-3 - Scales of biodiversity: integrated studies of snake venom and function across multiple levels of diversity, BP.TT
19/21121-7 - Fieldwork assistance for specimen, venom and gland collection: focusing on islands and coastal regions, BP.TT
19/21187-8 - Support for field work and management of specimens, venom, glands in the collection and live animals in captivity, BP.TT
19/02958-3 - Technical support for keeping snakes in captivity to the venom studies, BP.TT
19/03587-9 - Scales of biodiversity: integrated studies of snake venom evolution and function across multiple levels of diversity, BP.TT
18/25749-8 - Study on the variability of venom in snakes of the Bothrops jararaca complex and its correlation with the processes of speciation in continental islands, BP.PD
18/26520-4 - Characterization of the interrelationship between transcriptomes, miRNomes and proteomes from the venom glands of Bothrops fonsecai and Bothrops cotiara, BP.PD
18/26067-8 - Support to breeding and maintenance of captive snakes, BP.TT
18/19071-9 - Study of the adaptation of snakes to the specificity of their diet: comparative anatomy of the cephalic glands in three species of the Tachymenini tribe (Dipsadidae, Xenodontinae), BP.IC
18/15753-8 - Proteolytic enzymes and phospholipases in snake venoms: distribution and mechanisms of action related to venom toxicity and the digestion of prey, BP.DD
18/12126-2 - Fieldwork assistance to sample the target snake species for venom surveys - with special emphasis on the Atlantic Forest, BP.TT
18/06320-0 - Supervision for bioinformatic analysis in scales of biodiversity project, BP.TT
18/08995-5 - Production of educational material and support to scientific popularization through adaptation of the scientific results of the scales of biodiversity, BP.TT
18/07093-8 - Acquisition of high resolution computerized microtomography images and data processing through the use of segmentation softwares, BP.TT
18/04494-1 - Scales of biodiversity: integrated studies of snake venom evolution and function across multiple levels of diversity, BP.TT
17/24498-9 - Venomics analyses of Dipsadinae snakes focusing on adaptations to ophiophagy, BP.DD
17/24546-3 - Scales of biodiversity: integrated studies of snake evolution and venom function , BP.PD
17/24571-8 - Dimensions US-BIOTA São Paulo: scales of biodiversity: integrated studies of snake venom evolution and function across multiple levels of diversity, BP.TT
17/22059-8 - Scales of biodiversity: integrated studies of snake venom evolution and function, BP.TT - associated scholarships

Abstract

This project will determine how secondary key innovations within the venom system contribute to diversification patterns in the advanced snakes and test for biases in the genetic pathways underlying rapid phenotypie evolution in venoms as a means for understanding the mechanism underlying the process of diversification in this diverse group. In the first part, we will test for relationships between venom diversity and function and diversification rates using data from more than 100 species from the three families of venomous snakes collected from areas of exceptionally high biodiversity in the North and Central America and Brazil. Using data from venom-gland transcriptomics, quantitative mass spectrometry, and functional assays we will estimate phylogeny, quantify venom function and complexity and test for a link between clade diversification and venom composition. In the second part, we will evaluate the genetics of phenotypic divergence and mutational biases in the generation of venom as an adaptive trait by comprehensively investigating six species pairs (two from each of the three groups) that show recent divergence and significant differences in venom function. For these species, we will assess the importance of pre-transcriptional (e.g., cis- regulatory or copy-number) and post-transcriptional (e.g., translational efficiency or microRNA) mechanisms as determinants of venom protein diversity and test for prey-specific functional effects of venom. This will provide unprecedented detail about microevolutionary processes that underlie a key trait that influences macroevolutionary patterns providing an integrated perspective from the molecular to organismal level on the fundamental processes generating biodiversity. (AU)

Articles published in Agência FAPESP Newsletter about the research grant:
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VEICULO: TITULO (DATA)
VEICULO: TITULO (DATA)

Scientific publications (26)
(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)
FREITAS-DE-SOUSA, LUCIANA APARECIDA; COLOMBINI, MONICA; LOPES-FERREIRA, MONICA; SERRANO, SOLANGE M. T.; MOURA-DA-SILVA, ANA MARIA. Insights into the Mechanisms Involved in Strong Hemorrhage and Dermonecrosis Induced by Atroxlysin-Ia, a PI-Class Snake Venom Metalloproteinase. TOXINS, v. 9, n. 8, . (14/26058-8, 16/50127-5, 13/07467-1)
BAYONA-SERRANO, JUAN DAVID; VIALA, VINCENT LOUIS; RAUTSAW, RHETT M.; SCHRAMER, TRISTAN D.; BARROS-CARVALHO, GESIELE A.; NISHIYAMA, JR., MILTON YUTAKA; FREITAS-DE-SOUSA, LUCIANA A.; MOURA-DA-SILVA, ANA MARIA; PARKINSON, CHRISTOPHER L.; GRAZZIOTIN, FELIPE GOBBI; et al. Replacement and Parallel Simplification of Nonhomologous Proteinases Maintain Venom Phenotypes in Rear-Fanged Snakes. Molecular Biology and Evolution, v. 37, n. 12, p. 3563-3575, . (17/24546-3, 17/24498-9, 16/50127-5, 13/07467-1)
GIMENES, SARAH N. C.; SACHETT, JACQUELINE A. G.; COLOMBINI, MONICA; FREITAS-DE-SOUSA, LUCIANA A.; IBIAPINA, HIOCHELSON N. S.; COSTA, ALLYSON G.; SANTANA, MONIQUE F.; PARK, JEONG-JIN; SHERMAN, NICHOLAS E.; FERREIRA, LUIZ C. L.; et al. Observation of Bothrops atrox Snake Envenoming Blister Formation from Five Patients: Pathophysiological Insights. TOXINS, v. 13, n. 11, . (17/24546-3, 18/13108-8, 19/08208-6, 16/50127-5)
SOUSA, LEIJANE F.; HOLDING, MATTHEW L.; DEL-REI, TIAGO H. M.; ROCHA, MARISA M. T.; MOURAO, V, ROSA H.; CHALKIDIS, HIPOCRATES M.; PREZOTO, BENEDITO; GIBBS, H. LISLE; MOURA-DA-SILVA, ANA M.. Individual Variability in Bothrops atrox Snakes Collected from Different Habitats in the Brazilian Amazon: New Findings on Venom Composition and Functionality. TOXINS, v. 13, n. 11, . (17/15170-0, 16/50127-5, 14/13124-2)
NACHTIGALL, PEDRO G.; RAUTSAW, RHETT M.; ELLSWORTH, SCHYLER A.; MASON, ANDREW J.; ROKYTA, DARIN R.; PARKINSON, CHRISTOPHER L.; JUNQUEIRA-DE-AZEVEDO, INACIO L. M.. ToxCodAn: a new toxin annotator and guide to venom gland transcriptomics. BRIEFINGS IN BIOINFORMATICS, v. 22, n. 5, . (16/50127-5, 18/26520-4)
NACHTIGALL, PEDRO G.; GRAZZIOTIN, FELIPE G.; JUNQUEIRA-DE-AZEVEDO, INACIO L. M.. MITGARD: an automated pipeline for mitochondrial genome assembly in eukaryotic species using RNA-seq data. BRIEFINGS IN BIOINFORMATICS, v. 22, n. 5, . (13/07467-1, 16/50127-5, 18/26520-4)
ALMEIDA, MICHELLE TEIXEIRA DE; FREITAS-DE-SOUSA, LUCIANA APARECIDA; COLOMBINI, MONICA; GIMENES, SARAH N. C.; KITANO, EDUARDO S.; FAQUIM-MAURO, ELIANA L.; SERRANO, SOLANGE M. T.; MOURA-DA-SILVA, ANA MARIA. Inflammatory Reaction Induced by Two Metalloproteinases Isolated from Bothrops atrox Venom and by Fragments Generated from the Hydrolysis of Basement Membrane Components. TOXINS, v. 12, n. 2, . (14/26058-8, 16/50127-5, 13/07467-1)
SILVA, FERNANDA MAGALHAES; DA COSTA PRUDENTE, ANA LUCIA; MACHADO, FABIO ANDRADE; SANTOS, MARINA MEIRELES; ZAHER, HUSSAM; HINGST-ZAHER, ERIKA. Aquatic adaptations in a Neotropical coral snake: A study of morphological convergence. JOURNAL OF ZOOLOGICAL SYSTEMATICS AND EVOLUTIONARY RESEARCH, v. 56, n. 3, p. 382-394, . (11/21674-4, 16/50127-5, 11/50206-9)
AMAZONAS, DIANA R.; FREITAS-DE-SOUSA, LUCIANA A.; OREFICE, DANIELE P.; DE SOUSA, LEIJIANE F.; MARTINEZ, MELISSA G.; MOURAO, ROSA H. V.; CHALKIDIS, HIPOCRATES M.; CAMARGO, PLINIO B.; MOURA-DA-SILVA, ANA M.. Evidence for Snake Venom Plasticity in a Long-Term Study with Individual Captive Bothrops atrox. TOXINS, v. 11, n. 5, . (16/50127-5, 14/13124-2)
GIBBS, H. LISLE; SOVIC, MICHAEL; AMAZONAS, DIANA; CHALKIDIS, HIPPOCRATES; SALAZAR-VALENZUELA, DAVID; MOURA-DA-SILVA, ANA M.. Recent lineage diversification in a venomous snake through dispersal across the Amazon River. Biological Journal of the Linnean Society, v. 123, n. 3, p. 651-665, . (16/50127-5)
MENDOZA-ROLDAN, JAIRO; RIBEIRO, STEPHANY ROCHA; CASTILHO-ONOFRIO, VALERIA; GRAZZIOTIN, FELIPE GOBBI; ROCHA, BRUNO; FERRETO-FIORILLO, BRUNO; PEREIRA, JOSIVANIA SOARES; BENELLI, GIOVANNI; OTRANTO, DOMENICO; BARROS-BATTESTI, DARCI MORAES. Mites and ticks of reptiles and amphibians in Brazil. Acta Tropica, v. 208, . (17/12910-2, 16/50127-5, 15/21259-8)
AZEVEDO, WEVERTON DOS SANTOS; FRANCO, FRANCISCO LUIS; THOMASSEN, HANS; DE CASTRO, THIAGO MARCIAL; ABEGG, ARTHUR DIESEL; LEITE, FELIPE SA FORTES; BATTILANA, JAQUELINE; GRAZZIOTIN, FELIPE GOBBI. Reassessment of Tantilla boipiranga (Serpentes: Colubrinae) and a preliminary approach to the phylogenetic affinities within Tantilla. SALAMANDRA, v. 57, n. 3, p. 400-412, . (16/50127-5, 19/03587-9)
SCHRAMER, TRISTAN D.; RAUTSAW, RHETT M.; BAYONA-SERRANO, JUAN DAVID; NYSTROM, GUNNAR S.; WEST, TAYLOR R.; ORTIZ-MEDINA, JAVIER A.; SABIDO-ALPUCHE, BIANCA; MENESES-MILLAN, MARCOS; BORJA, MIGUEL; JUNQUEIRA-DE-AZEVEDO, INACIO L. M.; et al. n integrative view of the toxic potential of Conophis lineatus (Dipsadidae: Xenodontinae), a medically relevant rear-fanged snak. Toxicon, v. 205, p. 38-52, . (16/50127-5, 18/26520-4)
ALMEIDA, DIEGO DANTAS; VIALA, VINCENT LOUIS; NACHTIGALL, PEDRO GABRIEL; BROE, MICHAEL; GIBBS, H. LISLE; SERRANO, SOLANGE MARIA DE TOLEDO; MOURA-DA-SILVA, ANA MARIA; HO, PAULO LEE; NISHIYAMA-JR, MILTON YUTAKA; JUNQUEIRA-DE-AZEVEDO, INACIO L. M.. Tracking the recruitment and evolution of snake toxins using the evolutionary context provided by the Bothrops jararaca genome. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, v. 118, n. 20, . (16/50127-5, 13/07467-1, 15/03509-7, 12/00177-5, 18/26520-4)
FREITAS-DE-SOUSA, LUCIANA A.; NACHTIGALL, PEDRO G.; FORTES-JUNIOR, JOSE A.; HOLDING, MATTHEW L.; NYSTROM, GUNNAR S.; ELLSWORTH, SCHYLER A.; GUIMARIES, NORANATHAN C.; TIOYAMA, EMILLY; ORTIZ, FLORA; SILVA, BRUNO R.; et al. Size Matters: An Evaluation of the Molecular Basis of Ontogenetic Modifications in the Composition of Bothrops jararacussu Snake Venom. TOXINS, v. 12, n. 12, . (18/25749-8, 18/08589-7, 18/15753-8, 18/26520-4, 16/50127-5, 17/24546-3)
DRABECK, DANIELLE H.; RUCAVADO, ALEXANDRA; HINGST-ZAHER, ERIKA; CRUZ, YOLANDA P.; DEAN, ANTONY M.; JANSA, SHARON A.. Resistance of South American opossums to vWF-binding venom C-type lectins. Toxicon, v. 178, p. 92-99, . (16/50127-5)
ZAHER, HUSSAM; MURPHY, ROBERT W.; ARREDONDO, JUAN CAMILO; GRABOSKI, ROBERTA; MACHADO-FILHO, PAULO ROBERTO; MAHLOW, KRISTIN; MONTINGELLIL, GIOVANNA G.; QUADROS, ANA BOTTALLO; ORLOV, NIKOLAI L.; WILKINSON, MARK; et al. Large-scale molecular phylogeny, morphology, divergence-time estimation, and the fossil record of advanced caenophidian snakes (Squamata: Serpentes). PLoS One, v. 14, n. 5, . (02/13602-4, 07/52144-5, 11/50206-9, 12/24755-8, 16/50127-5)
MASON, ANDREW J.; GRAZZIOTIN, FELIPE G.; ZAHER, HUSSAM; LEMMON, ALAN R.; LEMMON, EMILY MORIARTY; PARKINSON, CHRISTOPHER L.. Reticulate evolution in nuclear Middle America causes discordance in the phylogeny of palm-pitvipers (Viperidae: Bothriechis). Journal of Biogeography, v. 46, n. 5, p. 833-844, . (16/50127-5, 11/50206-9)
GRABOSKI, ROBERTA; ARREDONDO, JUAN C.; GRAZZIOTIN, FELIPE G.; DA SILVA, ARIANE A. A.; PRUDENTE, ANA L. C.; RODRIGUES, MIGUEL T.; BONATTO, SANDRO L.; ZAHER, HUSSAM. Molecular phylogeny and hemipenial diversity of South American species of Amerotyphlops (Typhlopidae, Scolecophidia). ZOOLOGICA SCRIPTA, v. 48, n. 2, p. 139-156, . (03/10335-8, 16/50127-5, 11/50206-9)
VALENTE, RICHARD HEMMI; LUNA, MILENE SCHMIDT; DE OLIVEIRA, URSULA CASTRO; NISHIYAMA-JUNIOR, MILTON YUTAKA; JUNQUEIRA-DE-AZEVEDO, INACIO DE LOIOLA; PORTES-JUNIOR, JOSE ANTONIO; CLISSA, PATRICIA BIANCA; VIANA, LUCIANA GODOY; SANCHES, LEONARDO; MOURA-DA-SILVA, ANA MARIA; et al. Bothrops jararaca accessory venom gland is an ancillary source of toxins to the snake. JOURNAL OF PROTEOMICS, v. 177, p. 137-147, . (13/07467-1, 14/26058-8, 16/50127-5)
AMAZONAS, DIANA R.; PORTES-JUNIOR, JOSE A.; NISHIYAMA-JR, MILTON Y.; NICOLAU, CAROLINA A.; CHALKIDIS, HIPOCRATES M.; MOURAO, V, ROSA H.; GRAZZIOTIN, FELIPE G.; ROKYTA, DARIN R.; LISLE GIBBS, H.; VALENTE, RICHARD H.; et al. Molecular mechanisms underlying intraspecific variation in snake venom. JOURNAL OF PROTEOMICS, v. 181, p. 60-72, . (12/16277-9, 14/26058-8, 16/50127-5)
CARRASCO, PAOLA A.; GRAZZIOTIN, FELIPE G.; CRUZ FARFAN, ROY SANTA; KOCH, CLAUDIA; ANTONIO OCHOA, JOSE; SCROCCHI, GUSTAVO J.; LEYNAUD, GERARDO C.; CHAPARRO, JUAN C.. A new species of Bothrops (Serpentes: Viperidae: Crotalinae) from Pampas del Heath, southeastern Peru, with comments on the systematics of the Bothrops neuwiedi species group. Zootaxa, v. 4565, n. 3, p. 301-344, . (16/50127-5)
JUAN CAMILO ARREDONDO; FELIPE G. GRAZZIOTIN; GUSTAVO J. SCROCCHI; MIGUEL TREFAUT RODRIGUES; SANDRO LUÍS BONATTO; HUSSAM ZAHER. Molecular phylogeny of the tribe Philodryadini Cope, 1886 (Dipsadidae: Xenodontinae): Rediscovering the diversity of the South American Racers. Papéis Avulsos de Zoologia (São Paulo), v. 60, . (16/50127-5, 11/50206-9, 11/50146-6, 03/10335-8)
BERNARDE, PAULO SERGIO; PUCCA, MANUELA BERTO; MOTA-DA-SILVA, AGEANE; DA FONSECA, WIRVEN LIMA; DE ALMEIDA, MARLLUS RAFAEL NEGREIROS; DE OLIVEIRA, ISADORA SOUSA; CERNI, FELIPE AUGUSTO; GOBBI GRAZZIOTIN, FELIPE; SARTIM, MARCO A.; SACHETT, JACQUELINE; et al. Bothrops bilineatus: An Arboreal Pitviper in the Amazon and Atlantic Forest. FRONTIERS IN IMMUNOLOGY, v. 12, . (20/13176-3, 16/50127-5)
BARBO, FAUSTO E.; BOOKER, WILLIAM W.; DUARTE, MARCELO R.; CHALUPPE, BETINA; PORTES-JUNIOR, JOSE A.; FRANCO, FRANCISCO L.; GRAZZIOTIN, FELIPE G.. peciation process on Brazilian continental islands, with the description of a new insular lancehead of the genus Bothrops (Serpentes, Viperidae. SYSTEMATICS AND BIODIVERSITY, v. 20, n. 1, p. 1-25, . (18/25749-8, 16/50127-5, 12/09156-0)
BARBO, FAUSTO E.; GRAZZIOTIN, FELIPE G.; PEREIRA-FILHO, GENTIL A.; FREITAS, MARCO A.; ABRANTES, STEPHENSON H. F.; KOKUBUM, MARCELO N. DE C.. solated by dry lands: integrative analyses unveil the existence of a new species and a previously unknown evolutionary lineage of Brazilian Lanceheads (Serpentes: Viperidae: Bothrops) from a Caatinga moist-forest enclav. CANADIAN JOURNAL OF ZOOLOGY, v. 100, n. 1, p. 147-159, . (16/50127-5)

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