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, Agustín; Opara, Maxwell N.; Zenner, Lionel; Vavre, Fabrice; Chevillon, Christine
Año de publicación
2017
Idioma
inglés
Tipo de recurso
artículo
Estado
versión aceptada
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. Laboratoire Maladies Infectieuses et Vecteurs: Ecologie, Génétique, Evolution et Contrôle; Francia. Institut pour la Recherche et le Développement; Francia. Université de Montpellier; Francia
Fil: Binetruy, Florian. Centre National de la Recherche Scientifique. Laboratoire Maladies Infectieuses et Vecteurs: Ecologie, Génétique, Evolution et Contrôle; Francia. Institut pour la Recherche et le Développement; Francia. Université de Montpellier; Francia
Fil: Noël, Valérie. Centre National de la Recherche Scientifique. Laboratoire Maladies Infectieuses et Vecteurs: Ecologie, Génétique, Evolution et Contrôle; Francia. Institut pour la Recherche et le Développement; Francia. Université de Montpellier; Francia
Fil: Cremaschi, Julie. Centre National de la Recherche Scientifique. Laboratoire Maladies Infectieuses et Vecteurs: Ecologie, Génétique, Evolution et Contrôle; Francia. Institut pour la Recherche et le Développement; Francia. Université de Montpellier; Francia
Fil: McCoy, Karen D. Centre National de la Recherche Scientifique. Laboratoire Maladies Infectieuses et Vecteurs: Ecologie, Génétique, Evolution et Contrôle; Francia. Institut pour la Recherche et le Développement; Francia. Université de Montpellier; Francia
Fil: Arnathau, Céline. Centre National de la Recherche Scientifique. Laboratoire Maladies Infectieuses et Vecteurs: Ecologie, Génétique, Evolution et Contrôle; Francia. Institut pour la Recherche et le Développement; Francia. Université de Montpellier; Francia
Fil: Plantard, Olivier. Institut National de la Recherche Agronomique. Unité de recherche Biologie, Epidémiologie et analyse de risque en Santé Animale; Francia
Fil: Goolsby, John. United States Department of Agriculture. Cattle Fever Tick Research Laboratory; Estados Unidos
Fil: Pérez de León, Adalberto A. Veterinary Pest Genomics Center. Knipling-Bushland U.S. Livestock Insects Research Laboratory; Estados Unidos
Fil: Heylen, Dieter J. A. University of Antwerp. Evolutionary Ecology Group; Béigica
Fil: Van Oosten, A. Raoul. University of Antwerp. Evolutionary Ecology Group; Béigica
Fil: Gottlieb, Yuval. Hebrew University of Jerusalem. Koret School of Veterinary Medicine; Israel
Fil: Baneth, Gad. Hebrew University of Jerusalem. Koret School of Veterinary Medicine; Israel
Fil: Guglielmone, Alberto Alejandro. Instituto Nacional de Tecnología Agropecuaria (INTA). Estación Experimental Regional Agropecuaria Rafaela; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Estrada-Peña, Agustin. University of Zaragoza. Faculty of Veterinary Medicine. Department of Animal Pathology; España
Fil: Opara, Maxwell N. University of Abuja. Department of Veterinary Parasitology and Entomology. Ticks and Tick-borne Pathogens Research Unit; Nigeria
Fil: Zenner, Lionel. Centre National de la Recherche Scientifique. Laboratoire de Biométrie et Biologie Évolutive; Francia. Université Claude Bernard; Francia
Fil: Vavre, Fabrice. Centre National de la Recherche Scientifique. Laboratoire de Biométrie et Biologie Évolutive; Francia. Université Claude Bernard; Francia
Fil: Chevillon, Christine. Centre National de la Recherche Scientifique. Laboratoire Maladies Infectieuses et Vecteurs: Ecologie, Génétique, Evolution et Contrôle; Francia. Institut pour la Recherche et le Développement; Francia. Université de Montpellier; Francia
Fuente
Molecular ecology 26 (11) : 2905–2921. (June 2017)
Materia
Simbiontico
Symbionts
Bacteria
Coxiella
Rhipicephalus
Garrapatas
Nivel de accesibilidad
acceso restringido
Condiciones de uso
Repositorio
INTA Digital (INTA)
Institución
Instituto Nacional de Tecnología Agropecuaria
OAI Identificador
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spelling 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, AgustínOpara, Maxwell N.Zenner, LionelVavre, FabriceChevillon, ChristineSimbionticoSymbiontsBacteriaCoxiellaRhipicephalusGarrapatasEcological 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. Laboratoire Maladies Infectieuses et Vecteurs: Ecologie, Génétique, Evolution et Contrôle; Francia. Institut pour la Recherche et le Développement; Francia. Université de Montpellier; FranciaFil: Binetruy, Florian. Centre National de la Recherche Scientifique. Laboratoire Maladies Infectieuses et Vecteurs: Ecologie, Génétique, Evolution et Contrôle; Francia. Institut pour la Recherche et le Développement; Francia. Université de Montpellier; FranciaFil: Noël, Valérie. Centre National de la Recherche Scientifique. Laboratoire Maladies Infectieuses et Vecteurs: Ecologie, Génétique, Evolution et Contrôle; Francia. Institut pour la Recherche et le Développement; Francia. Université de Montpellier; FranciaFil: Cremaschi, Julie. Centre National de la Recherche Scientifique. Laboratoire Maladies Infectieuses et Vecteurs: Ecologie, Génétique, Evolution et Contrôle; Francia. Institut pour la Recherche et le Développement; Francia. Université de Montpellier; FranciaFil: McCoy, Karen D. Centre National de la Recherche Scientifique. Laboratoire Maladies Infectieuses et Vecteurs: Ecologie, Génétique, Evolution et Contrôle; Francia. Institut pour la Recherche et le Développement; Francia. Université de Montpellier; FranciaFil: Arnathau, Céline. Centre National de la Recherche Scientifique. Laboratoire Maladies Infectieuses et Vecteurs: Ecologie, Génétique, Evolution et Contrôle; Francia. Institut pour la Recherche et le Développement; Francia. Université de Montpellier; FranciaFil: Plantard, Olivier. Institut National de la Recherche Agronomique. Unité de recherche Biologie, Epidémiologie et analyse de risque en Santé Animale; FranciaFil: Goolsby, John. United States Department of Agriculture. Cattle Fever Tick Research Laboratory; Estados UnidosFil: Pérez de León, Adalberto A. Veterinary Pest Genomics Center. Knipling-Bushland U.S. Livestock Insects Research Laboratory; Estados UnidosFil: Heylen, Dieter J. A. University of Antwerp. Evolutionary Ecology Group; BéigicaFil: Van Oosten, A. Raoul. University of Antwerp. Evolutionary Ecology Group; BéigicaFil: Gottlieb, Yuval. Hebrew University of Jerusalem. Koret School of Veterinary Medicine; IsraelFil: Baneth, Gad. Hebrew University of Jerusalem. Koret School of Veterinary Medicine; IsraelFil: Guglielmone, Alberto Alejandro. Instituto Nacional de Tecnología Agropecuaria (INTA). Estación Experimental Regional Agropecuaria Rafaela; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaFil: Estrada-Peña, Agustin. University of Zaragoza. Faculty of Veterinary Medicine. Department of Animal Pathology; EspañaFil: Opara, Maxwell N. University of Abuja. Department of Veterinary Parasitology and Entomology. Ticks and Tick-borne Pathogens Research Unit; NigeriaFil: Zenner, Lionel. Centre National de la Recherche Scientifique. Laboratoire de Biométrie et Biologie Évolutive; Francia. Université Claude Bernard; FranciaFil: Vavre, Fabrice. Centre National de la Recherche Scientifique. Laboratoire de Biométrie et Biologie Évolutive; Francia. Université Claude Bernard; FranciaFil: Chevillon, Christine. Centre National de la Recherche Scientifique. Laboratoire Maladies Infectieuses et Vecteurs: Ecologie, Génétique, Evolution et Contrôle; Francia. Institut pour la Recherche et le Développement; Francia. Université de Montpellier; Francia2017-10-09T17:25:08Z2017-10-09T17:25:08Z2017-06info:eu-repo/semantics/articleinfo:eu-repo/semantics/acceptedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfhttp://hdl.handle.net/20.500.12123/1437http://onlinelibrary.wiley.com/doi/10.1111/mec.14094/abstract1365-294X (Online)0962-1083 (Print)DOI: 10.1111/mec.14094Molecular ecology 26 (11) : 2905–2921. (June 2017)reponame:INTA Digital (INTA)instname:Instituto Nacional de Tecnología Agropecuariaenginfo:eu-repo/semantics/restrictedAccess2025-09-29T13:44:12Zoai:localhost:20.500.12123/1437instacron:INTAInstitucionalhttp://repositorio.inta.gob.ar/Organismo científico-tecnológicoNo correspondehttp://repositorio.inta.gob.ar/oai/requesttripaldi.nicolas@inta.gob.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:l2025-09-29 13:44:12.436INTA Digital (INTA) - Instituto Nacional de Tecnología Agropecuariafalse
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
Simbiontico
Symbionts
Bacteria
Coxiella
Rhipicephalus
Garrapatas
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, Agustín
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, Agustín
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, Agustín
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 Simbiontico
Symbionts
Bacteria
Coxiella
Rhipicephalus
Garrapatas
topic Simbiontico
Symbionts
Bacteria
Coxiella
Rhipicephalus
Garrapatas
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. Laboratoire Maladies Infectieuses et Vecteurs: Ecologie, Génétique, Evolution et Contrôle; Francia. Institut pour la Recherche et le Développement; Francia. Université de Montpellier; Francia
Fil: Binetruy, Florian. Centre National de la Recherche Scientifique. Laboratoire Maladies Infectieuses et Vecteurs: Ecologie, Génétique, Evolution et Contrôle; Francia. Institut pour la Recherche et le Développement; Francia. Université de Montpellier; Francia
Fil: Noël, Valérie. Centre National de la Recherche Scientifique. Laboratoire Maladies Infectieuses et Vecteurs: Ecologie, Génétique, Evolution et Contrôle; Francia. Institut pour la Recherche et le Développement; Francia. Université de Montpellier; Francia
Fil: Cremaschi, Julie. Centre National de la Recherche Scientifique. Laboratoire Maladies Infectieuses et Vecteurs: Ecologie, Génétique, Evolution et Contrôle; Francia. Institut pour la Recherche et le Développement; Francia. Université de Montpellier; Francia
Fil: McCoy, Karen D. Centre National de la Recherche Scientifique. Laboratoire Maladies Infectieuses et Vecteurs: Ecologie, Génétique, Evolution et Contrôle; Francia. Institut pour la Recherche et le Développement; Francia. Université de Montpellier; Francia
Fil: Arnathau, Céline. Centre National de la Recherche Scientifique. Laboratoire Maladies Infectieuses et Vecteurs: Ecologie, Génétique, Evolution et Contrôle; Francia. Institut pour la Recherche et le Développement; Francia. Université de Montpellier; Francia
Fil: Plantard, Olivier. Institut National de la Recherche Agronomique. Unité de recherche Biologie, Epidémiologie et analyse de risque en Santé Animale; Francia
Fil: Goolsby, John. United States Department of Agriculture. Cattle Fever Tick Research Laboratory; Estados Unidos
Fil: Pérez de León, Adalberto A. Veterinary Pest Genomics Center. Knipling-Bushland U.S. Livestock Insects Research Laboratory; Estados Unidos
Fil: Heylen, Dieter J. A. University of Antwerp. Evolutionary Ecology Group; Béigica
Fil: Van Oosten, A. Raoul. University of Antwerp. Evolutionary Ecology Group; Béigica
Fil: Gottlieb, Yuval. Hebrew University of Jerusalem. Koret School of Veterinary Medicine; Israel
Fil: Baneth, Gad. Hebrew University of Jerusalem. Koret School of Veterinary Medicine; Israel
Fil: Guglielmone, Alberto Alejandro. Instituto Nacional de Tecnología Agropecuaria (INTA). Estación Experimental Regional Agropecuaria Rafaela; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Estrada-Peña, Agustin. University of Zaragoza. Faculty of Veterinary Medicine. Department of Animal Pathology; España
Fil: Opara, Maxwell N. University of Abuja. Department of Veterinary Parasitology and Entomology. Ticks and Tick-borne Pathogens Research Unit; Nigeria
Fil: Zenner, Lionel. Centre National de la Recherche Scientifique. Laboratoire de Biométrie et Biologie Évolutive; Francia. Université Claude Bernard; Francia
Fil: Vavre, Fabrice. Centre National de la Recherche Scientifique. Laboratoire de Biométrie et Biologie Évolutive; Francia. Université Claude Bernard; Francia
Fil: Chevillon, Christine. Centre National de la Recherche Scientifique. Laboratoire Maladies Infectieuses et Vecteurs: Ecologie, Génétique, Evolution et Contrôle; Francia. Institut pour la Recherche et le Développement; Francia. Université de Montpellier; 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 2017-10-09T17:25:08Z
2017-10-09T17:25:08Z
2017-06
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dc.identifier.none.fl_str_mv http://hdl.handle.net/20.500.12123/1437
http://onlinelibrary.wiley.com/doi/10.1111/mec.14094/abstract
1365-294X (Online)
0962-1083 (Print)
DOI: 10.1111/mec.14094
url http://hdl.handle.net/20.500.12123/1437
http://onlinelibrary.wiley.com/doi/10.1111/mec.14094/abstract
identifier_str_mv 1365-294X (Online)
0962-1083 (Print)
DOI: 10.1111/mec.14094
dc.language.none.fl_str_mv eng
language eng
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dc.format.none.fl_str_mv application/pdf
dc.source.none.fl_str_mv Molecular ecology 26 (11) : 2905–2921. (June 2017)
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