Consuming viscous prey: a novel protein-secreting delivery system in neotropical snail-eating snakes

Detalhes bibliográficos
Autor(a) principal: Zaher, Hussam
Data de Publicação: 2014
Outros Autores: Oliveira, Leonardo de [UNESP], Grazziotin, Felipe G., Campagner, Michelle, Jared, Carlos, Antoniazzi, Marta M., Prudente, Ana L.
Tipo de documento: Artigo
Idioma: eng
Título da fonte: Repositório Institucional da UNESP
Texto Completo: http://dx.doi.org/10.1186/1471-2148-14-58
http://hdl.handle.net/11449/112812
Resumo: Background: Efficient venom delivery systems are known to occur only in varanoid lizards and advanced colubroidean snakes among squamate reptiles. Although components of these venomous systems might have been present in a common ancestor, the two lineages independently evolved strikingly different venom gland systems. In snakes, venom is produced exclusively by serous glands in the upper jaw. Within the colubroidean radiation, lower jaw seromucous infralabial glands are known only in two distinct lineages-the basal pareatids and the more advanced Neotropical dipsadines known as goo-eating snakes. Goo-eaters are a highly diversified, ecologically specialized clade that feeds exclusively on invertebrates (e. g., gastropod molluscs and annelids). Their evolutionary success has been attributed to their peculiar feeding strategies, which remain surprisingly poorly understood. More specifically, it has long been thought that the more derived Dipsadini genera Dipsas and Sibynomorphus use glandular toxins secreted by their infralabial glands to extract snails from their shells.Results: Here, we report the presence in the tribe Dipsadini of a novel lower jaw protein-secreting delivery system effected by a gland that is not functionally related to adjacent teeth, but rather opens loosely on the oral epithelium near the tip of the mandible, suggesting that its secretion is not injected into the prey as a form of envenomation but rather helps control the mucus and assists in the ingestion of their highly viscous preys. A similar protein-secreting system is also present in the goo-eating genus Geophis and may share the same adaptive purpose as that hypothesized for Dipsadini. Our phylogenetic hypothesis suggests that the acquisition of a seromucous infralabial gland represents a uniquely derived trait of the goo-eating clade that evolved independently twice within the group as a functionally complex protein-secreting delivery system.Conclusions: The acquisition by snail-eating snakes of such a complex protein-secreting system suggests that the secretion from the hypertrophied infralabial glands of goo-eating snakes may have a fundamental role in mucus control and prey transport rather than envenomation of prey. Evolution of a functional secretory system that combines a solution for mucus control and transport of viscous preys is here thought to underlie the successful radiation of goo-eating snakes.
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spelling Consuming viscous prey: a novel protein-secreting delivery system in neotropical snail-eating snakesPhylogenyEvolutionDipsadinaeGlandsSecretionMusclesGoo-eatersBackground: Efficient venom delivery systems are known to occur only in varanoid lizards and advanced colubroidean snakes among squamate reptiles. Although components of these venomous systems might have been present in a common ancestor, the two lineages independently evolved strikingly different venom gland systems. In snakes, venom is produced exclusively by serous glands in the upper jaw. Within the colubroidean radiation, lower jaw seromucous infralabial glands are known only in two distinct lineages-the basal pareatids and the more advanced Neotropical dipsadines known as goo-eating snakes. Goo-eaters are a highly diversified, ecologically specialized clade that feeds exclusively on invertebrates (e. g., gastropod molluscs and annelids). Their evolutionary success has been attributed to their peculiar feeding strategies, which remain surprisingly poorly understood. More specifically, it has long been thought that the more derived Dipsadini genera Dipsas and Sibynomorphus use glandular toxins secreted by their infralabial glands to extract snails from their shells.Results: Here, we report the presence in the tribe Dipsadini of a novel lower jaw protein-secreting delivery system effected by a gland that is not functionally related to adjacent teeth, but rather opens loosely on the oral epithelium near the tip of the mandible, suggesting that its secretion is not injected into the prey as a form of envenomation but rather helps control the mucus and assists in the ingestion of their highly viscous preys. A similar protein-secreting system is also present in the goo-eating genus Geophis and may share the same adaptive purpose as that hypothesized for Dipsadini. Our phylogenetic hypothesis suggests that the acquisition of a seromucous infralabial gland represents a uniquely derived trait of the goo-eating clade that evolved independently twice within the group as a functionally complex protein-secreting delivery system.Conclusions: The acquisition by snail-eating snakes of such a complex protein-secreting system suggests that the secretion from the hypertrophied infralabial glands of goo-eating snakes may have a fundamental role in mucus control and prey transport rather than envenomation of prey. Evolution of a functional secretory system that combines a solution for mucus control and transport of viscous preys is here thought to underlie the successful radiation of goo-eating snakes.Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP)Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq)Univ Sao Paulo, Museu Zool, BR-04263000 Sao Paulo, SP, BrazilUniv Estadual Paulista, Programa Pos Grad Zool, BR-13506900 Rio Claro, SP, BrazilInst Butantan, Museu Biol, BR-05503900 Sao Paulo, SP, BrazilInst Butantan, Lab Biol Celular, BR-05503900 Sao Paulo, BrazilMuseu Paraense Emilio Goeldi, BR-66040170 Belem, Para, BrazilUniv Estadual Paulista, Programa Pos Grad Zool, BR-13506900 Rio Claro, SP, BrazilFAPESP: 11/50206-9CNPq: 565046/2010-1CNPq: 303545/2010-0CNPq: 308950/2011-9CNPq: PROTAXA 562171/2010-0FAPESP: 08/57102-1FAPESP: 12/12587-3Biomed Central Ltd.Universidade de São Paulo (USP)Universidade Estadual Paulista (Unesp)Instituto ButantanMuseu Paraense Emilio GoeldiZaher, HussamOliveira, Leonardo de [UNESP]Grazziotin, Felipe G.Campagner, MichelleJared, CarlosAntoniazzi, Marta M.Prudente, Ana L.2014-12-03T13:11:04Z2014-12-03T13:11:04Z2014-03-25info:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/article28application/pdfhttp://dx.doi.org/10.1186/1471-2148-14-58Bmc Evolutionary Biology. London: Biomed Central Ltd, v. 14, 28 p., 2014.1471-2148http://hdl.handle.net/11449/11281210.1186/1471-2148-14-58WOS:000335172000001WOS000335172000001.pdfWeb of Sciencereponame:Repositório Institucional da UNESPinstname:Universidade Estadual Paulista (UNESP)instacron:UNESPengBMC Evolutionary Biology3.0271,656info:eu-repo/semantics/openAccess2023-11-01T06:11:12Zoai:repositorio.unesp.br:11449/112812Repositório InstitucionalPUBhttp://repositorio.unesp.br/oai/requestopendoar:29462024-08-05T16:37:02.610613Repositório Institucional da UNESP - Universidade Estadual Paulista (UNESP)false
dc.title.none.fl_str_mv Consuming viscous prey: a novel protein-secreting delivery system in neotropical snail-eating snakes
title Consuming viscous prey: a novel protein-secreting delivery system in neotropical snail-eating snakes
spellingShingle Consuming viscous prey: a novel protein-secreting delivery system in neotropical snail-eating snakes
Zaher, Hussam
Phylogeny
Evolution
Dipsadinae
Glands
Secretion
Muscles
Goo-eaters
title_short Consuming viscous prey: a novel protein-secreting delivery system in neotropical snail-eating snakes
title_full Consuming viscous prey: a novel protein-secreting delivery system in neotropical snail-eating snakes
title_fullStr Consuming viscous prey: a novel protein-secreting delivery system in neotropical snail-eating snakes
title_full_unstemmed Consuming viscous prey: a novel protein-secreting delivery system in neotropical snail-eating snakes
title_sort Consuming viscous prey: a novel protein-secreting delivery system in neotropical snail-eating snakes
author Zaher, Hussam
author_facet Zaher, Hussam
Oliveira, Leonardo de [UNESP]
Grazziotin, Felipe G.
Campagner, Michelle
Jared, Carlos
Antoniazzi, Marta M.
Prudente, Ana L.
author_role author
author2 Oliveira, Leonardo de [UNESP]
Grazziotin, Felipe G.
Campagner, Michelle
Jared, Carlos
Antoniazzi, Marta M.
Prudente, Ana L.
author2_role author
author
author
author
author
author
dc.contributor.none.fl_str_mv Universidade de São Paulo (USP)
Universidade Estadual Paulista (Unesp)
Instituto Butantan
Museu Paraense Emilio Goeldi
dc.contributor.author.fl_str_mv Zaher, Hussam
Oliveira, Leonardo de [UNESP]
Grazziotin, Felipe G.
Campagner, Michelle
Jared, Carlos
Antoniazzi, Marta M.
Prudente, Ana L.
dc.subject.por.fl_str_mv Phylogeny
Evolution
Dipsadinae
Glands
Secretion
Muscles
Goo-eaters
topic Phylogeny
Evolution
Dipsadinae
Glands
Secretion
Muscles
Goo-eaters
description Background: Efficient venom delivery systems are known to occur only in varanoid lizards and advanced colubroidean snakes among squamate reptiles. Although components of these venomous systems might have been present in a common ancestor, the two lineages independently evolved strikingly different venom gland systems. In snakes, venom is produced exclusively by serous glands in the upper jaw. Within the colubroidean radiation, lower jaw seromucous infralabial glands are known only in two distinct lineages-the basal pareatids and the more advanced Neotropical dipsadines known as goo-eating snakes. Goo-eaters are a highly diversified, ecologically specialized clade that feeds exclusively on invertebrates (e. g., gastropod molluscs and annelids). Their evolutionary success has been attributed to their peculiar feeding strategies, which remain surprisingly poorly understood. More specifically, it has long been thought that the more derived Dipsadini genera Dipsas and Sibynomorphus use glandular toxins secreted by their infralabial glands to extract snails from their shells.Results: Here, we report the presence in the tribe Dipsadini of a novel lower jaw protein-secreting delivery system effected by a gland that is not functionally related to adjacent teeth, but rather opens loosely on the oral epithelium near the tip of the mandible, suggesting that its secretion is not injected into the prey as a form of envenomation but rather helps control the mucus and assists in the ingestion of their highly viscous preys. A similar protein-secreting system is also present in the goo-eating genus Geophis and may share the same adaptive purpose as that hypothesized for Dipsadini. Our phylogenetic hypothesis suggests that the acquisition of a seromucous infralabial gland represents a uniquely derived trait of the goo-eating clade that evolved independently twice within the group as a functionally complex protein-secreting delivery system.Conclusions: The acquisition by snail-eating snakes of such a complex protein-secreting system suggests that the secretion from the hypertrophied infralabial glands of goo-eating snakes may have a fundamental role in mucus control and prey transport rather than envenomation of prey. Evolution of a functional secretory system that combines a solution for mucus control and transport of viscous preys is here thought to underlie the successful radiation of goo-eating snakes.
publishDate 2014
dc.date.none.fl_str_mv 2014-12-03T13:11:04Z
2014-12-03T13:11:04Z
2014-03-25
dc.type.status.fl_str_mv info:eu-repo/semantics/publishedVersion
dc.type.driver.fl_str_mv info:eu-repo/semantics/article
format article
status_str publishedVersion
dc.identifier.uri.fl_str_mv http://dx.doi.org/10.1186/1471-2148-14-58
Bmc Evolutionary Biology. London: Biomed Central Ltd, v. 14, 28 p., 2014.
1471-2148
http://hdl.handle.net/11449/112812
10.1186/1471-2148-14-58
WOS:000335172000001
WOS000335172000001.pdf
url http://dx.doi.org/10.1186/1471-2148-14-58
http://hdl.handle.net/11449/112812
identifier_str_mv Bmc Evolutionary Biology. London: Biomed Central Ltd, v. 14, 28 p., 2014.
1471-2148
10.1186/1471-2148-14-58
WOS:000335172000001
WOS000335172000001.pdf
dc.language.iso.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv BMC Evolutionary Biology
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dc.format.none.fl_str_mv 28
application/pdf
dc.publisher.none.fl_str_mv Biomed Central Ltd.
publisher.none.fl_str_mv Biomed Central Ltd.
dc.source.none.fl_str_mv Web of Science
reponame:Repositório Institucional da UNESP
instname:Universidade Estadual Paulista (UNESP)
instacron:UNESP
instname_str Universidade Estadual Paulista (UNESP)
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institution UNESP
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