Host races in Ixodes ricinus, the European vector of Lyme borreliosis Florent Kempf a,⇑,1 , Thierry De Meeûs b,c,1 , Elise Vaumourin a , Valérie Noel a , Veronika Taragel’ová d , Olivier Plantard e , Dieter J.A. Heylen f , Cyril Eraud g , Christine Chevillon a , Karen D. McCoy a a MIVEGEC, UMR 5290 CNRS-IRD-UM1-um2, Centre IRD, 911 Avenue Agropolis, BP 64501, 34394 Montpellier, France b UMR 177 IRD-CIRAD ‘INTERTRYP’, Centre International de Recherche-Développement sur l’Elevage en zone Subhumide (CIRDES), 01 BP 454 Bobo-Dioulasso 01, Burkina Faso c CNRS, Délégation Languedoc-Roussillon, 1919, Route de Mende, 34293 Montpellier, France d Institute of Zoology, Slovak Academy of Sciences, Dúbravská Cesta 9, Bratislava 84506, Slovakia e INRA, UMR 1300 BiOEpAR (Bio-agression, Epidémiologie et Analyse de Risques en santé animale), Ecole Nationale Vétérinaire, Agroalimentaire et de l’Alimentation Nantes Atlantique, Atlanpole – La Chantrerie, BP 40706, 44307 Nantes, France f Evolutionary Ecology Group, Department of Biology, University of Antwerp, Groenenborgerlaan 171, 2020 Antwerpen, Belgium g Office National de la Chasse et de la Faune Sauvage, CNERA Avifaune Migratrice, Station de Chizé, 79360 Villiers-en-Bois, France article info Article history: Received 6 July 2011 Received in revised form 20 September 2011 Accepted 21 September 2011 Available online 29 September 2011 Keywords: Host specialization Generalist–specialist Microsatellites Ticks Vector-borne diseases abstract Ixodes ricinus is a European tick that transmits numerous pathogenic agents, including the bacteria that cause Lyme disease (some genospecies of Borrelia burgdorferi sensu lato complex). This tick has been con- sidered as a classic example of an extreme generalist vector. However, host-associations in such vector species are difficult to determine from field observations alone and recent work suggests that host spec- ificity may be more frequent in ticks than previously thought. The presence of host-associated vector groups can significantly alter the circulation and evolutionary pathway of associated pathogens. In this paper, we explicitly test for host-associated genetic structure in I. ricinus. We analyzed genetic variability at 11 microsatellite markers in a large sample of ticks collected directly from trapped wild animals (birds, rodents, lizards, wild boar and roe deer) at five sites in Western and Central Europe. We found significant levels of genetic structure both among host individuals and among host types within local populations, suggesting that host use is not random in I. ricinus. These results help explain previous patterns of struc- ture found in off-host tick samples, along with epidemiological observations of Lyme disease. Ó 2011 Elsevier B.V. All rights reserved. 1. Introduction Ticks are parasites of great interest in both applied and funda- mental sciences. They present a wide array of life cycles, exploit a large range of host species and are second only to mosquitoes in their importance as vectors of human and livestock disease agents (Parola and Raoult, 2001). Ticks of the Ixodes ricinus com- plex are of notable significance; they are present across the North- ern temperate zone and transmit a great variety of pathogens of medical and veterinary importance (e.g., Cotté et al., 2010), includ- ing the bacteria responsible for Lyme borreliosis (LB), some geno- species of Borrelia burgdorferi sensu lato species complex (Gern and Humair, 2002). The population dynamics, ecology, and basic biology of I. ricinus species complex, along with its interaction with B. burgdorferi s.l. are well documented, particularly for the Euro- pean species I. ricinus (e.g., Gern and Humair, 2002; Kurtenbach et al., 2006 and references therein). Many studies have described the catholic feeding habits of I. ricinus; it can be observed on a wide array of vertebrate hosts including small, medium and large mam- mals, birds and lizards (Hoogstraal and Aeschlimann, 1982). For this reason, I. ricinus is traditionally considered as an extreme gen- eralist vector. Nonetheless, we still have only limited knowledge about how these ticks interact locally with their different potential host species and the consequences of these interactions for disease transmission. One way to address such questions is by examining population genetic structure in association with local host exploi- tation (McCoy et al., 1999). As in many other tick systems, genetic analyses of I. ricinus have focused on large scale patterns using questing ticks collected from the vegetation (e.g., Estrada-Peña et al., 1996; Delaye et al., 1997; De Meeûs et al., 2002, 2004a,b; Paulauskas et al., 2006; Kempf et al., 2010; Nourredine et al., 2011). Several of these studies have revealed unexpectedly high levels of heterozygote deficiencies within populations, deviations present even after correcting for po- tential technical biases (De Meeûs et al., 2002, 2004a). One cause for differences between expected and observed heterozygosities can be the erroneous sampling of individuals from different iso- lated sub-groups (i.e., a Wahlund effect). Indeed, recent work has demonstrated the existence of cryptic sub-groups within I. ricinus populations (Kempf et al., 2010), along with patterns of assortative 1567-1348/$ - see front matter Ó 2011 Elsevier B.V. All rights reserved. doi:10.1016/j.meegid.2011.09.016 ⇑ Corresponding author. E-mail address: florentkempf@hotmail.com (F. Kempf). 1 These two authors contributed equally. Infection, Genetics and Evolution 11 (2011) 2043–2048 Contents lists available at SciVerse ScienceDirect Infection, Genetics and Evolution journal homepage: www.elsevier.com/locate/meegid