Evolutionary origin and development of snake fangs

Evolution bites: Fang development and the diversity of modern snakes An 'evo-devo' study of venomous snakes has arrived at a new model for the evolution of snake fangs, a subject of some controversy. Many of the advanced snakes alive today use syringe-like fangs to inject venom into their...

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Veröffentlicht in:Nature (London) 2008-07, Vol.454 (7204), p.630-633
Hauptverfasser: Vonk, Freek J., Admiraal, Jeroen F., Jackson, Kate, Reshef, Ram, de Bakker, Merijn A. G., Vanderschoot, Kim, van den Berge, Iris, van Atten, Marit, Burgerhout, Erik, Beck, Andrew, Mirtschin, Peter J., Kochva, Elazar, Witte, Frans, Fry, Bryan G., Woods, Anthony E., Richardson, Michael K.
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container_issue 7204
container_start_page 630
container_title Nature (London)
container_volume 454
creator Vonk, Freek J.
Admiraal, Jeroen F.
Jackson, Kate
Reshef, Ram
de Bakker, Merijn A. G.
Vanderschoot, Kim
van den Berge, Iris
van Atten, Marit
Burgerhout, Erik
Beck, Andrew
Mirtschin, Peter J.
Kochva, Elazar
Witte, Frans
Fry, Bryan G.
Woods, Anthony E.
Richardson, Michael K.
description Evolution bites: Fang development and the diversity of modern snakes An 'evo-devo' study of venomous snakes has arrived at a new model for the evolution of snake fangs, a subject of some controversy. Many of the advanced snakes alive today use syringe-like fangs to inject venom into their prey. The fangs are either positioned at the front or rear of the upper jaw, and the controversy lies in whether the two arrangements are evolutionarily related. By visualizing tooth-forming epithelium in the upper jaw of 96 snake embryos from 8 species, the study shows that 'front-fanged' and 'rear-fanged' types are strikingly similar in morphogenesis. Front fangs develop from a rear part of the upper jaw that is displaced forward during development, and rear fangs from a specialized zone that stays put. The new model proposes that a posterior subregion of tooth-forming epithelium became developmentally uncoupled from the remaining dentition, allowing the posterior teeth to evolve independently and in close association with the venom gland, becoming highly modified in different lineages. This developmental event could have facilitated the massive radiation of advanced snakes in the Cenozoic era, resulting in the spectacular diversity of snakes seen today. The cover shows a Lataste's viper ( Vipera latastei gaditana ) with the erected fang covered by the fang sheath. Photo by Ruben Schipper. Many advanced snakes use fangs to inject venom into their prey. The fangs may be either at the front or rear of the upper jaw, but biologists have been unable to agree whether these two arrangements are evolutionarily related. It is now shown that front fangs develop in the rear part of the jaw, and that the resemblances between front and rear fangs are so striking during their development that homology is probable. Many advanced snakes use fangs—specialized teeth associated with a venom gland 1 , 2 —to introduce venom into prey or attacker. Various front- and rear-fanged groups are recognized, according to whether their fangs are positioned anterior (for example cobras and vipers) or posterior (for example grass snakes) in the upper jaw 3 , 4 , 5 . A fundamental controversy in snake evolution is whether or not front and rear fangs share the same evolutionary and developmental origin 3 , 4 , 5 , 6 , 7 , 8 , 9 . Resolving this controversy could identify a major evolutionary transition underlying the massive radiation of advanced snakes, and the associated developmental events. Here we
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G. ; Vanderschoot, Kim ; van den Berge, Iris ; van Atten, Marit ; Burgerhout, Erik ; Beck, Andrew ; Mirtschin, Peter J. ; Kochva, Elazar ; Witte, Frans ; Fry, Bryan G. ; Woods, Anthony E. ; Richardson, Michael K.</creator><creatorcontrib>Vonk, Freek J. ; Admiraal, Jeroen F. ; Jackson, Kate ; Reshef, Ram ; de Bakker, Merijn A. G. ; Vanderschoot, Kim ; van den Berge, Iris ; van Atten, Marit ; Burgerhout, Erik ; Beck, Andrew ; Mirtschin, Peter J. ; Kochva, Elazar ; Witte, Frans ; Fry, Bryan G. ; Woods, Anthony E. ; Richardson, Michael K.</creatorcontrib><description>Evolution bites: Fang development and the diversity of modern snakes An 'evo-devo' study of venomous snakes has arrived at a new model for the evolution of snake fangs, a subject of some controversy. Many of the advanced snakes alive today use syringe-like fangs to inject venom into their prey. The fangs are either positioned at the front or rear of the upper jaw, and the controversy lies in whether the two arrangements are evolutionarily related. By visualizing tooth-forming epithelium in the upper jaw of 96 snake embryos from 8 species, the study shows that 'front-fanged' and 'rear-fanged' types are strikingly similar in morphogenesis. Front fangs develop from a rear part of the upper jaw that is displaced forward during development, and rear fangs from a specialized zone that stays put. The new model proposes that a posterior subregion of tooth-forming epithelium became developmentally uncoupled from the remaining dentition, allowing the posterior teeth to evolve independently and in close association with the venom gland, becoming highly modified in different lineages. This developmental event could have facilitated the massive radiation of advanced snakes in the Cenozoic era, resulting in the spectacular diversity of snakes seen today. The cover shows a Lataste's viper ( Vipera latastei gaditana ) with the erected fang covered by the fang sheath. Photo by Ruben Schipper. Many advanced snakes use fangs to inject venom into their prey. The fangs may be either at the front or rear of the upper jaw, but biologists have been unable to agree whether these two arrangements are evolutionarily related. It is now shown that front fangs develop in the rear part of the jaw, and that the resemblances between front and rear fangs are so striking during their development that homology is probable. Many advanced snakes use fangs—specialized teeth associated with a venom gland 1 , 2 —to introduce venom into prey or attacker. Various front- and rear-fanged groups are recognized, according to whether their fangs are positioned anterior (for example cobras and vipers) or posterior (for example grass snakes) in the upper jaw 3 , 4 , 5 . A fundamental controversy in snake evolution is whether or not front and rear fangs share the same evolutionary and developmental origin 3 , 4 , 5 , 6 , 7 , 8 , 9 . Resolving this controversy could identify a major evolutionary transition underlying the massive radiation of advanced snakes, and the associated developmental events. Here we examine this issue by visualizing the tooth-forming epithelium in the upper jaw of 96 snake embryos, covering eight species. We use the sonic hedgehog gene as a marker 10 , 11 , 12 , 13 , and three-dimensionally reconstruct the development in 41 of the embryos. We show that front fangs develop from the posterior end of the upper jaw, and are strikingly similar in morphogenesis to rear fangs. This is consistent with their being homologous. In front-fanged snakes, the anterior part of the upper jaw lacks sonic hedgehog expression, and ontogenetic allometry displaces the fang from its posterior developmental origin to its adult front position—consistent with an ancestral posterior position of the front fang. In rear-fanged snakes, the fangs develop from an independent posterior dental lamina and retain their posterior position. In light of our findings, we put forward a new model for the evolution of snake fangs: a posterior subregion of the tooth-forming epithelium became developmentally uncoupled from the remaining dentition, which allowed the posterior teeth to evolve independently and in close association with the venom gland, becoming highly modified in different lineages. This developmental event could have facilitated the massive radiation of advanced snakes in the Cenozoic era, resulting in the spectacular diversity of snakes seen today 6 , 14 , 15 .</description><identifier>ISSN: 0028-0836</identifier><identifier>EISSN: 1476-4687</identifier><identifier>DOI: 10.1038/nature07178</identifier><identifier>PMID: 18668106</identifier><identifier>CODEN: NATUAS</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>Allometry ; Amphibia. Reptilia ; Animals ; Biological and medical sciences ; Biological evolution ; Cenozoic ; Embryos ; Fundamental and applied biological sciences. Psychology ; Gene Expression Regulation, Developmental ; Genetics of eukaryotes. Biological and molecular evolution ; Hedgehog Proteins - genetics ; Hedgehog Proteins - metabolism ; Histology ; Humanities and Social Sciences ; In Situ Hybridization ; letter ; Molecular Sequence Data ; multidisciplinary ; Natural history ; Origin ; Phylogeny ; Physiological aspects ; Scanning electron microscopy ; Science ; Science (multidisciplinary) ; Snakes ; Snakes - anatomy &amp; histology ; Snakes - classification ; Snakes - embryology ; Snakes - genetics ; Teeth ; Tooth - anatomy &amp; histology ; Tooth - embryology ; Varieties ; Venom ; Vertebrates: general zoology, morphology, phylogeny, systematics, cytogenetics, geographical distribution</subject><ispartof>Nature (London), 2008-07, Vol.454 (7204), p.630-633</ispartof><rights>Macmillan Publishers Limited. All rights reserved 2008</rights><rights>2008 INIST-CNRS</rights><rights>COPYRIGHT 2008 Nature Publishing Group</rights><rights>Copyright Nature Publishing Group Jul 31, 2008</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c649t-ae0d4b1788a8368ab8d140d54890a76e9d801842a7610a55cf2e07cb7d3b516c3</citedby><cites>FETCH-LOGICAL-c649t-ae0d4b1788a8368ab8d140d54890a76e9d801842a7610a55cf2e07cb7d3b516c3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://link.springer.com/content/pdf/10.1038/nature07178$$EPDF$$P50$$Gspringer$$H</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1038/nature07178$$EHTML$$P50$$Gspringer$$H</linktohtml><link.rule.ids>314,776,780,27901,27902,41464,42533,51294</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&amp;idt=20524824$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/18668106$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Vonk, Freek J.</creatorcontrib><creatorcontrib>Admiraal, Jeroen F.</creatorcontrib><creatorcontrib>Jackson, Kate</creatorcontrib><creatorcontrib>Reshef, Ram</creatorcontrib><creatorcontrib>de Bakker, Merijn A. G.</creatorcontrib><creatorcontrib>Vanderschoot, Kim</creatorcontrib><creatorcontrib>van den Berge, Iris</creatorcontrib><creatorcontrib>van Atten, Marit</creatorcontrib><creatorcontrib>Burgerhout, Erik</creatorcontrib><creatorcontrib>Beck, Andrew</creatorcontrib><creatorcontrib>Mirtschin, Peter J.</creatorcontrib><creatorcontrib>Kochva, Elazar</creatorcontrib><creatorcontrib>Witte, Frans</creatorcontrib><creatorcontrib>Fry, Bryan G.</creatorcontrib><creatorcontrib>Woods, Anthony E.</creatorcontrib><creatorcontrib>Richardson, Michael K.</creatorcontrib><title>Evolutionary origin and development of snake fangs</title><title>Nature (London)</title><addtitle>Nature</addtitle><addtitle>Nature</addtitle><description>Evolution bites: Fang development and the diversity of modern snakes An 'evo-devo' study of venomous snakes has arrived at a new model for the evolution of snake fangs, a subject of some controversy. Many of the advanced snakes alive today use syringe-like fangs to inject venom into their prey. The fangs are either positioned at the front or rear of the upper jaw, and the controversy lies in whether the two arrangements are evolutionarily related. By visualizing tooth-forming epithelium in the upper jaw of 96 snake embryos from 8 species, the study shows that 'front-fanged' and 'rear-fanged' types are strikingly similar in morphogenesis. Front fangs develop from a rear part of the upper jaw that is displaced forward during development, and rear fangs from a specialized zone that stays put. The new model proposes that a posterior subregion of tooth-forming epithelium became developmentally uncoupled from the remaining dentition, allowing the posterior teeth to evolve independently and in close association with the venom gland, becoming highly modified in different lineages. This developmental event could have facilitated the massive radiation of advanced snakes in the Cenozoic era, resulting in the spectacular diversity of snakes seen today. The cover shows a Lataste's viper ( Vipera latastei gaditana ) with the erected fang covered by the fang sheath. Photo by Ruben Schipper. Many advanced snakes use fangs to inject venom into their prey. The fangs may be either at the front or rear of the upper jaw, but biologists have been unable to agree whether these two arrangements are evolutionarily related. It is now shown that front fangs develop in the rear part of the jaw, and that the resemblances between front and rear fangs are so striking during their development that homology is probable. Many advanced snakes use fangs—specialized teeth associated with a venom gland 1 , 2 —to introduce venom into prey or attacker. Various front- and rear-fanged groups are recognized, according to whether their fangs are positioned anterior (for example cobras and vipers) or posterior (for example grass snakes) in the upper jaw 3 , 4 , 5 . A fundamental controversy in snake evolution is whether or not front and rear fangs share the same evolutionary and developmental origin 3 , 4 , 5 , 6 , 7 , 8 , 9 . Resolving this controversy could identify a major evolutionary transition underlying the massive radiation of advanced snakes, and the associated developmental events. Here we examine this issue by visualizing the tooth-forming epithelium in the upper jaw of 96 snake embryos, covering eight species. We use the sonic hedgehog gene as a marker 10 , 11 , 12 , 13 , and three-dimensionally reconstruct the development in 41 of the embryos. We show that front fangs develop from the posterior end of the upper jaw, and are strikingly similar in morphogenesis to rear fangs. This is consistent with their being homologous. In front-fanged snakes, the anterior part of the upper jaw lacks sonic hedgehog expression, and ontogenetic allometry displaces the fang from its posterior developmental origin to its adult front position—consistent with an ancestral posterior position of the front fang. In rear-fanged snakes, the fangs develop from an independent posterior dental lamina and retain their posterior position. In light of our findings, we put forward a new model for the evolution of snake fangs: a posterior subregion of the tooth-forming epithelium became developmentally uncoupled from the remaining dentition, which allowed the posterior teeth to evolve independently and in close association with the venom gland, becoming highly modified in different lineages. This developmental event could have facilitated the massive radiation of advanced snakes in the Cenozoic era, resulting in the spectacular diversity of snakes seen today 6 , 14 , 15 .</description><subject>Allometry</subject><subject>Amphibia. 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G. ; Vanderschoot, Kim ; van den Berge, Iris ; van Atten, Marit ; Burgerhout, Erik ; Beck, Andrew ; Mirtschin, Peter J. ; Kochva, Elazar ; Witte, Frans ; Fry, Bryan G. ; Woods, Anthony E. ; Richardson, Michael K.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c649t-ae0d4b1788a8368ab8d140d54890a76e9d801842a7610a55cf2e07cb7d3b516c3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2008</creationdate><topic>Allometry</topic><topic>Amphibia. Reptilia</topic><topic>Animals</topic><topic>Biological and medical sciences</topic><topic>Biological evolution</topic><topic>Cenozoic</topic><topic>Embryos</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>Gene Expression Regulation, Developmental</topic><topic>Genetics of eukaryotes. 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Aerospace Collection</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Environmental Science Database</collection><collection>Earth, Atmospheric &amp; Aquatic Science Database</collection><collection>Materials Science Collection</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest One Psychology</collection><collection>Engineering Collection</collection><collection>Environmental Science Collection</collection><collection>ProQuest Central Basic</collection><collection>University of Michigan</collection><collection>Genetics Abstracts</collection><collection>SIRS Editorial</collection><collection>Environment Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>Nature (London)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Vonk, Freek J.</au><au>Admiraal, Jeroen F.</au><au>Jackson, Kate</au><au>Reshef, Ram</au><au>de Bakker, Merijn A. G.</au><au>Vanderschoot, Kim</au><au>van den Berge, Iris</au><au>van Atten, Marit</au><au>Burgerhout, Erik</au><au>Beck, Andrew</au><au>Mirtschin, Peter J.</au><au>Kochva, Elazar</au><au>Witte, Frans</au><au>Fry, Bryan G.</au><au>Woods, Anthony E.</au><au>Richardson, Michael K.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Evolutionary origin and development of snake fangs</atitle><jtitle>Nature (London)</jtitle><stitle>Nature</stitle><addtitle>Nature</addtitle><date>2008-07-31</date><risdate>2008</risdate><volume>454</volume><issue>7204</issue><spage>630</spage><epage>633</epage><pages>630-633</pages><issn>0028-0836</issn><eissn>1476-4687</eissn><coden>NATUAS</coden><abstract>Evolution bites: Fang development and the diversity of modern snakes An 'evo-devo' study of venomous snakes has arrived at a new model for the evolution of snake fangs, a subject of some controversy. Many of the advanced snakes alive today use syringe-like fangs to inject venom into their prey. The fangs are either positioned at the front or rear of the upper jaw, and the controversy lies in whether the two arrangements are evolutionarily related. By visualizing tooth-forming epithelium in the upper jaw of 96 snake embryos from 8 species, the study shows that 'front-fanged' and 'rear-fanged' types are strikingly similar in morphogenesis. Front fangs develop from a rear part of the upper jaw that is displaced forward during development, and rear fangs from a specialized zone that stays put. The new model proposes that a posterior subregion of tooth-forming epithelium became developmentally uncoupled from the remaining dentition, allowing the posterior teeth to evolve independently and in close association with the venom gland, becoming highly modified in different lineages. This developmental event could have facilitated the massive radiation of advanced snakes in the Cenozoic era, resulting in the spectacular diversity of snakes seen today. The cover shows a Lataste's viper ( Vipera latastei gaditana ) with the erected fang covered by the fang sheath. Photo by Ruben Schipper. Many advanced snakes use fangs to inject venom into their prey. The fangs may be either at the front or rear of the upper jaw, but biologists have been unable to agree whether these two arrangements are evolutionarily related. It is now shown that front fangs develop in the rear part of the jaw, and that the resemblances between front and rear fangs are so striking during their development that homology is probable. Many advanced snakes use fangs—specialized teeth associated with a venom gland 1 , 2 —to introduce venom into prey or attacker. Various front- and rear-fanged groups are recognized, according to whether their fangs are positioned anterior (for example cobras and vipers) or posterior (for example grass snakes) in the upper jaw 3 , 4 , 5 . A fundamental controversy in snake evolution is whether or not front and rear fangs share the same evolutionary and developmental origin 3 , 4 , 5 , 6 , 7 , 8 , 9 . Resolving this controversy could identify a major evolutionary transition underlying the massive radiation of advanced snakes, and the associated developmental events. Here we examine this issue by visualizing the tooth-forming epithelium in the upper jaw of 96 snake embryos, covering eight species. We use the sonic hedgehog gene as a marker 10 , 11 , 12 , 13 , and three-dimensionally reconstruct the development in 41 of the embryos. We show that front fangs develop from the posterior end of the upper jaw, and are strikingly similar in morphogenesis to rear fangs. This is consistent with their being homologous. In front-fanged snakes, the anterior part of the upper jaw lacks sonic hedgehog expression, and ontogenetic allometry displaces the fang from its posterior developmental origin to its adult front position—consistent with an ancestral posterior position of the front fang. In rear-fanged snakes, the fangs develop from an independent posterior dental lamina and retain their posterior position. In light of our findings, we put forward a new model for the evolution of snake fangs: a posterior subregion of the tooth-forming epithelium became developmentally uncoupled from the remaining dentition, which allowed the posterior teeth to evolve independently and in close association with the venom gland, becoming highly modified in different lineages. This developmental event could have facilitated the massive radiation of advanced snakes in the Cenozoic era, resulting in the spectacular diversity of snakes seen today 6 , 14 , 15 .</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>18668106</pmid><doi>10.1038/nature07178</doi><tpages>4</tpages></addata></record>
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identifier ISSN: 0028-0836
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issn 0028-0836
1476-4687
language eng
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source MEDLINE; Nature Journals Online; SpringerLink Journals - AutoHoldings
subjects Allometry
Amphibia. Reptilia
Animals
Biological and medical sciences
Biological evolution
Cenozoic
Embryos
Fundamental and applied biological sciences. Psychology
Gene Expression Regulation, Developmental
Genetics of eukaryotes. Biological and molecular evolution
Hedgehog Proteins - genetics
Hedgehog Proteins - metabolism
Histology
Humanities and Social Sciences
In Situ Hybridization
letter
Molecular Sequence Data
multidisciplinary
Natural history
Origin
Phylogeny
Physiological aspects
Scanning electron microscopy
Science
Science (multidisciplinary)
Snakes
Snakes - anatomy & histology
Snakes - classification
Snakes - embryology
Snakes - genetics
Teeth
Tooth - anatomy & histology
Tooth - embryology
Varieties
Venom
Vertebrates: general zoology, morphology, phylogeny, systematics, cytogenetics, geographical distribution
title Evolutionary origin and development of snake fangs
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