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.
Bibliographical noteFunding Information:
We are grateful to Hassane Adakal, Anaïs Appelgren, Jonathan Banks, Jean-Claude Beaucournu, Abel S. Biguezoton, Thierry Boulinier, Philippe Christe, Filipe Dantas-Torres, Guiguigbaza-Kossigan Dayo, Georges Diatta, Muriel Dietrich, Marlène Dupraz, Patrick Durand, Gislene Fournier (FAPESP: 2014/00648-3), Michel Gauthier-Clerc, Lise Gern, Daniel González-Acuña, Jacob González-Solís, Elena Gómez-Díaz, Steeve Goodman, Philippe Gourlay, Rodolphe Gozlan, Mark Hipfner, Elsa Jourdain, Marcelo Labruna, Olivier Lambert, Robert Lane, Elsa Léger, Jérome Letty, Jing-Ze Liu, Jolyon Medlock, Nil Rahola, François Renaud, Ulrich Schneppat, Slaheddine Selmi, Dave Spratt, Fréderic Stachurski, Jean-François Trape, Yann Trembley, Zati Vatansever, Laurence Vial and Sébastien Zoungrana for help at different stages of this work. Financial support was provided by recurrent funding from CNRS and IRD (OD, VN, KDM, CA, CC), CNRS-INEE (Programme PEPS-Ecologie de la Santé 2014, ‘SYMPATTIQUES’: OD, LZ), Programmes Investissement d'Avenir of the French Government (Laboratoire d'Excellence CEBA, Annual project 2016: ‘MiTick’: OD), Agence Nationale de la Recherche (ANR-13-BSV7-0018-01: KDM; ANR-11-AGRO-001-01: OP), the French Polar Institute Paul Emile Victor (programme n°333 Parasito-Arctic) and cooperative agreement between USDA-ARS and MIVEGEC (no. 58-6205-4-D08F: CC, JG, AAPdL).
© 2017 John Wiley & Sons Ltd
- heritable symbiont communities
- maternally inherited bacteria