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Evolutionary changes in symbiont community structure in ticks
Authors:Olivier Duron  Florian Binetruy  Valérie Noël  Julie Cremaschi  Karen D McCoy  Céline Arnathau  Olivier Plantard  John Goolsby  Adalberto A Pérez de León  Dieter J A Heylen  A Raoul Van Oosten  Yuval Gottlieb  Gad Baneth  Alberto A Guglielmone  Agustin Estrada‐Peña  Maxwell N Opara  Lionel Zenner  Fabrice Vavre  Christine Chevillon
Affiliation:1. Laboratoire MIVEGEC (Maladies Infectieuses et Vecteurs: Ecologie, Génétique, Evolution et Contr?le), Centre National de la Recherche Scientifique (UMR5290) – Institut pour la Recherche et le Développement (UR224) – Université de Montpellier, Montpellier, France;2. BIOEPAR, INRA, Oniris, Nantes, France;3. Cattle Fever Tick Research Laboratory, USDA‐ARS, Edinburg, TX, USA;4. Knipling‐Bushland U.S. Livestock Insects Research Laboratory, Veterinary Pest Genomics Center, Kerrville, TX, USA;5. Evolutionary Ecology Group, University of Antwerp, Antwerp, Belgium;6. Koret School of Veterinary Medicine, The Hebrew University of Jerusalem, Rehovot, Israel;7. Instituto Nacional de Tecnología Agropecuaria, Estación Experimental Agropecuaria Rafaela and Consejo Nacional de Investigaciones Científicas y Técnicas, Santa Fe, Argentina;8. Department of Animal Pathology, Faculty of Veterinary Medicine, University of Zaragoza, Zaragoza, Spain;9. Ticks and Tick‐borne Pathogens Research Unit (TTbPRU), Department of Veterinary Parasitology and Entomology, University of Abuja, Abuja, Nigeria;10. Laboratoire de Biométrie et Biologie évolutive (LBBE), Centre National de la Recherche Scientifique (UMR5558) – Université Claude Bernard Lyon 1, Villeurbanne, France
Abstract: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.
Keywords:co‐evolution  heritable symbiont communities  maternally inherited bacteria  symbiosis  tick
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