Evolutionary changes in symbiont community structure in ticks
- Autores
- Duron, Olivier; Binetruy, Florian; Noël, Valérie; Cremaschi, Julie; McCoy, Karen D.; Arnathau, Céline; Plantard, Olivier; Goolsby, John; Pérez de León, Adalberto A.; Heylen, Dieter J. A.; Van Oosten, A. Raoul; Gottlieb, Yuval; Baneth, Gad; Guglielmone, Alberto Alejandro; Estrada Peña, Agustin; Opara, Maxwell N.; Zenner, Lionel; Vavre, Fabrice; Chevillon, Christine
- Año de publicación
- 2017
- Idioma
- inglés
- Tipo de recurso
- artículo
- Estado
- versión publicada
- Descripción
- Ecological specialization to restricted diet niches is driven by obligate, and often maternally inherited, symbionts in many arthropod lineages. These heritable symbionts typically form evolutionarily stable associations with arthropods that can last for millions of years. Ticks were recently found to harbour such an obligate symbiont, Coxiella-LE, that synthesizes B vitamins and cofactors not obtained in sufficient quantities from blood diet. In this study, the examination of 81 tick species shows that some Coxiella-LE symbioses are evolutionarily stable with an ancient acquisition followed by codiversification as observed in ticks belonging to the Rhipicephalus genus. However, many other Coxiella-LE symbioses are characterized by low evolutionary stability with frequent host shifts and extinction events. Further examination revealed the presence of nine other genera of maternally inherited bacteria in ticks. Although these nine symbionts were primarily thought to be facultative, their distribution among tick species rather suggests that at least four may have independently replaced Coxiella-LE and likely represent alternative obligate symbionts. Phylogenetic evidence otherwise indicates that cocladogenesis is globally rare in these symbioses as most originate via horizontal transfer of an existing symbiont between unrelated tick species. As a result, the structure of these symbiont communities is not fixed and stable across the tick phylogeny. Most importantly, the symbiont communities commonly reach high levels of diversity with up to six unrelated maternally inherited bacteria coexisting within host species. We further conjecture that interactions among coexisting symbionts are pivotal drivers of community structure both among and within tick species.
Fil: Duron, Olivier. Centre National de la Recherche Scientifique; Francia
Fil: Binetruy, Florian. Centre National de la Recherche Scientifique; Francia
Fil: Noël, Valérie. Centre National de la Recherche Scientifique; Francia
Fil: Cremaschi, Julie. Centre National de la Recherche Scientifique; Francia
Fil: McCoy, Karen D.. Centre National de la Recherche Scientifique; Francia
Fil: Arnathau, Céline. Centre National de la Recherche Scientifique; Francia
Fil: Plantard, Olivier. Institut National de la Recherche Agronomique; Francia
Fil: Goolsby, John. United States Department of Agriculture. Agriculture Research Service; Estados Unidos
Fil: Pérez de León, Adalberto A.. Veterinary Pest Genomics Center; Estados Unidos
Fil: Heylen, Dieter J. A.. Universiteit Antwerp; Bélgica
Fil: Van Oosten, A. Raoul. Universiteit Antwerp; Bélgica
Fil: Gottlieb, Yuval. The Hebrew University of Jerusalem; Israel
Fil: Baneth, Gad. The Hebrew University of Jerusalem; Israel
Fil: Guglielmone, Alberto Alejandro. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Instituto Nacional de Tecnología Agropecuaria. Centro Regional Buenos Aires; Argentina
Fil: Estrada Peña, Agustin. Universidad de Zaragoza; España
Fil: Opara, Maxwell N.. University Of Abuja; Nigeria
Fil: Zenner, Lionel. Centre National de la Recherche Scientifique; Francia
Fil: Vavre, Fabrice. Centre National de la Recherche Scientifique; Francia
Fil: Chevillon, Christine. Centre National de la Recherche Scientifique; Francia - Materia
-
Co-Evolution
Heritable Symbiont Communities
Maternally Inherited Bacteria
Symbiosis
Tick - Nivel de accesibilidad
- acceso abierto
- Condiciones de uso
- https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
- Repositorio
- Institución
- Consejo Nacional de Investigaciones Científicas y Técnicas
- OAI Identificador
- oai:ri.conicet.gov.ar:11336/58622
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Evolutionary changes in symbiont community structure in ticksDuron, OlivierBinetruy, FlorianNoël, ValérieCremaschi, JulieMcCoy, Karen D.Arnathau, CélinePlantard, OlivierGoolsby, JohnPérez de León, Adalberto A.Heylen, Dieter J. A.Van Oosten, A. RaoulGottlieb, YuvalBaneth, GadGuglielmone, Alberto AlejandroEstrada Peña, AgustinOpara, Maxwell N.Zenner, LionelVavre, FabriceChevillon, ChristineCo-EvolutionHeritable Symbiont CommunitiesMaternally Inherited BacteriaSymbiosisTickhttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1Ecological specialization to restricted diet niches is driven by obligate, and often maternally inherited, symbionts in many arthropod lineages. These heritable symbionts typically form evolutionarily stable associations with arthropods that can last for millions of years. Ticks were recently found to harbour such an obligate symbiont, Coxiella-LE, that synthesizes B vitamins and cofactors not obtained in sufficient quantities from blood diet. In this study, the examination of 81 tick species shows that some Coxiella-LE symbioses are evolutionarily stable with an ancient acquisition followed by codiversification as observed in ticks belonging to the Rhipicephalus genus. However, many other Coxiella-LE symbioses are characterized by low evolutionary stability with frequent host shifts and extinction events. Further examination revealed the presence of nine other genera of maternally inherited bacteria in ticks. Although these nine symbionts were primarily thought to be facultative, their distribution among tick species rather suggests that at least four may have independently replaced Coxiella-LE and likely represent alternative obligate symbionts. Phylogenetic evidence otherwise indicates that cocladogenesis is globally rare in these symbioses as most originate via horizontal transfer of an existing symbiont between unrelated tick species. As a result, the structure of these symbiont communities is not fixed and stable across the tick phylogeny. Most importantly, the symbiont communities commonly reach high levels of diversity with up to six unrelated maternally inherited bacteria coexisting within host species. We further conjecture that interactions among coexisting symbionts are pivotal drivers of community structure both among and within tick species.Fil: Duron, Olivier. Centre National de la Recherche Scientifique; FranciaFil: Binetruy, Florian. Centre National de la Recherche Scientifique; FranciaFil: Noël, Valérie. Centre National de la Recherche Scientifique; FranciaFil: Cremaschi, Julie. Centre National de la Recherche Scientifique; FranciaFil: McCoy, Karen D.. Centre National de la Recherche Scientifique; FranciaFil: Arnathau, Céline. Centre National de la Recherche Scientifique; FranciaFil: Plantard, Olivier. Institut National de la Recherche Agronomique; FranciaFil: Goolsby, John. United States Department of Agriculture. Agriculture Research Service; Estados UnidosFil: Pérez de León, Adalberto A.. Veterinary Pest Genomics Center; Estados UnidosFil: Heylen, Dieter J. A.. Universiteit Antwerp; BélgicaFil: Van Oosten, A. Raoul. Universiteit Antwerp; BélgicaFil: Gottlieb, Yuval. The Hebrew University of Jerusalem; IsraelFil: Baneth, Gad. The Hebrew University of Jerusalem; IsraelFil: Guglielmone, Alberto Alejandro. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Instituto Nacional de Tecnología Agropecuaria. Centro Regional Buenos Aires; ArgentinaFil: Estrada Peña, Agustin. Universidad de Zaragoza; EspañaFil: Opara, Maxwell N.. University Of Abuja; NigeriaFil: Zenner, Lionel. Centre National de la Recherche Scientifique; FranciaFil: Vavre, Fabrice. Centre National de la Recherche Scientifique; FranciaFil: Chevillon, Christine. Centre National de la Recherche Scientifique; FranciaWiley Blackwell Publishing, Inc2017-06info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/58622Duron, Olivier; Binetruy, Florian; Noël, Valérie; Cremaschi, Julie; McCoy, Karen D.; et al.; Evolutionary changes in symbiont community structure in ticks; Wiley Blackwell Publishing, Inc; Molecular Ecology; 26; 11; 6-2017; 2905-29210962-1083CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/doi/10.1111/mec.14094info:eu-repo/semantics/altIdentifier/url/https://onlinelibrary.wiley.com/doi/abs/10.1111/mec.14094info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-10T13:06:15Zoai:ri.conicet.gov.ar:11336/58622instacron:CONICETInstitucionalhttp://ri.conicet.gov.ar/Organismo científico-tecnológicoNo correspondehttp://ri.conicet.gov.ar/oai/requestdasensio@conicet.gov.ar; lcarlino@conicet.gov.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:34982025-09-10 13:06:15.704CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse |
dc.title.none.fl_str_mv |
Evolutionary changes in symbiont community structure in ticks |
title |
Evolutionary changes in symbiont community structure in ticks |
spellingShingle |
Evolutionary changes in symbiont community structure in ticks Duron, Olivier Co-Evolution Heritable Symbiont Communities Maternally Inherited Bacteria Symbiosis Tick |
title_short |
Evolutionary changes in symbiont community structure in ticks |
title_full |
Evolutionary changes in symbiont community structure in ticks |
title_fullStr |
Evolutionary changes in symbiont community structure in ticks |
title_full_unstemmed |
Evolutionary changes in symbiont community structure in ticks |
title_sort |
Evolutionary changes in symbiont community structure in ticks |
dc.creator.none.fl_str_mv |
Duron, Olivier Binetruy, Florian Noël, Valérie Cremaschi, Julie McCoy, Karen D. Arnathau, Céline Plantard, Olivier Goolsby, John Pérez de León, Adalberto A. Heylen, Dieter J. A. Van Oosten, A. Raoul Gottlieb, Yuval Baneth, Gad Guglielmone, Alberto Alejandro Estrada Peña, Agustin Opara, Maxwell N. Zenner, Lionel Vavre, Fabrice Chevillon, Christine |
author |
Duron, Olivier |
author_facet |
Duron, Olivier Binetruy, Florian Noël, Valérie Cremaschi, Julie McCoy, Karen D. Arnathau, Céline Plantard, Olivier Goolsby, John Pérez de León, Adalberto A. Heylen, Dieter J. A. Van Oosten, A. Raoul Gottlieb, Yuval Baneth, Gad Guglielmone, Alberto Alejandro Estrada Peña, Agustin Opara, Maxwell N. Zenner, Lionel Vavre, Fabrice Chevillon, Christine |
author_role |
author |
author2 |
Binetruy, Florian Noël, Valérie Cremaschi, Julie McCoy, Karen D. Arnathau, Céline Plantard, Olivier Goolsby, John Pérez de León, Adalberto A. Heylen, Dieter J. A. Van Oosten, A. Raoul Gottlieb, Yuval Baneth, Gad Guglielmone, Alberto Alejandro Estrada Peña, Agustin Opara, Maxwell N. Zenner, Lionel Vavre, Fabrice Chevillon, Christine |
author2_role |
author author author author author author author author author author author author author author author author author author |
dc.subject.none.fl_str_mv |
Co-Evolution Heritable Symbiont Communities Maternally Inherited Bacteria Symbiosis Tick |
topic |
Co-Evolution Heritable Symbiont Communities Maternally Inherited Bacteria Symbiosis Tick |
purl_subject.fl_str_mv |
https://purl.org/becyt/ford/1.6 https://purl.org/becyt/ford/1 |
dc.description.none.fl_txt_mv |
Ecological specialization to restricted diet niches is driven by obligate, and often maternally inherited, symbionts in many arthropod lineages. These heritable symbionts typically form evolutionarily stable associations with arthropods that can last for millions of years. Ticks were recently found to harbour such an obligate symbiont, Coxiella-LE, that synthesizes B vitamins and cofactors not obtained in sufficient quantities from blood diet. In this study, the examination of 81 tick species shows that some Coxiella-LE symbioses are evolutionarily stable with an ancient acquisition followed by codiversification as observed in ticks belonging to the Rhipicephalus genus. However, many other Coxiella-LE symbioses are characterized by low evolutionary stability with frequent host shifts and extinction events. Further examination revealed the presence of nine other genera of maternally inherited bacteria in ticks. Although these nine symbionts were primarily thought to be facultative, their distribution among tick species rather suggests that at least four may have independently replaced Coxiella-LE and likely represent alternative obligate symbionts. Phylogenetic evidence otherwise indicates that cocladogenesis is globally rare in these symbioses as most originate via horizontal transfer of an existing symbiont between unrelated tick species. As a result, the structure of these symbiont communities is not fixed and stable across the tick phylogeny. Most importantly, the symbiont communities commonly reach high levels of diversity with up to six unrelated maternally inherited bacteria coexisting within host species. We further conjecture that interactions among coexisting symbionts are pivotal drivers of community structure both among and within tick species. Fil: Duron, Olivier. Centre National de la Recherche Scientifique; Francia Fil: Binetruy, Florian. Centre National de la Recherche Scientifique; Francia Fil: Noël, Valérie. Centre National de la Recherche Scientifique; Francia Fil: Cremaschi, Julie. Centre National de la Recherche Scientifique; Francia Fil: McCoy, Karen D.. Centre National de la Recherche Scientifique; Francia Fil: Arnathau, Céline. Centre National de la Recherche Scientifique; Francia Fil: Plantard, Olivier. Institut National de la Recherche Agronomique; Francia Fil: Goolsby, John. United States Department of Agriculture. Agriculture Research Service; Estados Unidos Fil: Pérez de León, Adalberto A.. Veterinary Pest Genomics Center; Estados Unidos Fil: Heylen, Dieter J. A.. Universiteit Antwerp; Bélgica Fil: Van Oosten, A. Raoul. Universiteit Antwerp; Bélgica Fil: Gottlieb, Yuval. The Hebrew University of Jerusalem; Israel Fil: Baneth, Gad. The Hebrew University of Jerusalem; Israel Fil: Guglielmone, Alberto Alejandro. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Instituto Nacional de Tecnología Agropecuaria. Centro Regional Buenos Aires; Argentina Fil: Estrada Peña, Agustin. Universidad de Zaragoza; España Fil: Opara, Maxwell N.. University Of Abuja; Nigeria Fil: Zenner, Lionel. Centre National de la Recherche Scientifique; Francia Fil: Vavre, Fabrice. Centre National de la Recherche Scientifique; Francia Fil: Chevillon, Christine. Centre National de la Recherche Scientifique; Francia |
description |
Ecological specialization to restricted diet niches is driven by obligate, and often maternally inherited, symbionts in many arthropod lineages. These heritable symbionts typically form evolutionarily stable associations with arthropods that can last for millions of years. Ticks were recently found to harbour such an obligate symbiont, Coxiella-LE, that synthesizes B vitamins and cofactors not obtained in sufficient quantities from blood diet. In this study, the examination of 81 tick species shows that some Coxiella-LE symbioses are evolutionarily stable with an ancient acquisition followed by codiversification as observed in ticks belonging to the Rhipicephalus genus. However, many other Coxiella-LE symbioses are characterized by low evolutionary stability with frequent host shifts and extinction events. Further examination revealed the presence of nine other genera of maternally inherited bacteria in ticks. Although these nine symbionts were primarily thought to be facultative, their distribution among tick species rather suggests that at least four may have independently replaced Coxiella-LE and likely represent alternative obligate symbionts. Phylogenetic evidence otherwise indicates that cocladogenesis is globally rare in these symbioses as most originate via horizontal transfer of an existing symbiont between unrelated tick species. As a result, the structure of these symbiont communities is not fixed and stable across the tick phylogeny. Most importantly, the symbiont communities commonly reach high levels of diversity with up to six unrelated maternally inherited bacteria coexisting within host species. We further conjecture that interactions among coexisting symbionts are pivotal drivers of community structure both among and within tick species. |
publishDate |
2017 |
dc.date.none.fl_str_mv |
2017-06 |
dc.type.none.fl_str_mv |
info:eu-repo/semantics/article info:eu-repo/semantics/publishedVersion http://purl.org/coar/resource_type/c_6501 info:ar-repo/semantics/articulo |
format |
article |
status_str |
publishedVersion |
dc.identifier.none.fl_str_mv |
http://hdl.handle.net/11336/58622 Duron, Olivier; Binetruy, Florian; Noël, Valérie; Cremaschi, Julie; McCoy, Karen D.; et al.; Evolutionary changes in symbiont community structure in ticks; Wiley Blackwell Publishing, Inc; Molecular Ecology; 26; 11; 6-2017; 2905-2921 0962-1083 CONICET Digital CONICET |
url |
http://hdl.handle.net/11336/58622 |
identifier_str_mv |
Duron, Olivier; Binetruy, Florian; Noël, Valérie; Cremaschi, Julie; McCoy, Karen D.; et al.; Evolutionary changes in symbiont community structure in ticks; Wiley Blackwell Publishing, Inc; Molecular Ecology; 26; 11; 6-2017; 2905-2921 0962-1083 CONICET Digital CONICET |
dc.language.none.fl_str_mv |
eng |
language |
eng |
dc.relation.none.fl_str_mv |
info:eu-repo/semantics/altIdentifier/doi/10.1111/mec.14094 info:eu-repo/semantics/altIdentifier/url/https://onlinelibrary.wiley.com/doi/abs/10.1111/mec.14094 |
dc.rights.none.fl_str_mv |
info:eu-repo/semantics/openAccess https://creativecommons.org/licenses/by-nc-sa/2.5/ar/ |
eu_rights_str_mv |
openAccess |
rights_invalid_str_mv |
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/ |
dc.format.none.fl_str_mv |
application/pdf application/pdf |
dc.publisher.none.fl_str_mv |
Wiley Blackwell Publishing, Inc |
publisher.none.fl_str_mv |
Wiley Blackwell Publishing, Inc |
dc.source.none.fl_str_mv |
reponame:CONICET Digital (CONICET) instname:Consejo Nacional de Investigaciones Científicas y Técnicas |
reponame_str |
CONICET Digital (CONICET) |
collection |
CONICET Digital (CONICET) |
instname_str |
Consejo Nacional de Investigaciones Científicas y Técnicas |
repository.name.fl_str_mv |
CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicas |
repository.mail.fl_str_mv |
dasensio@conicet.gov.ar; lcarlino@conicet.gov.ar |
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1842980254051729408 |
score |
12.993085 |