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Population Structure and Genetic Diversity in the Invasive Freshwater Snail Galba Schirazensis (Lymnaeidae) M

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Population Structure and Genetic Diversity in the Invasive Freshwater Snail Galba Schirazensis (Lymnaeidae) M 425 ARTICLE Population structure and genetic diversity in the invasive freshwater snail Galba schirazensis (Lymnaeidae) M. Lounnas, A.C. Correa, P. Alda, P. David, M.-P. Dubois, M. Calvopiña, Y. Caron, M. Celi-Erazo, B.T. Dung, P. Jarne, E.S. Loker, O. Noya, R. Rodríguez-Hidalgo, C. Toty, N. Uribe, J.-P. Pointier, and S. Hurtrez-Boussès Abstract: We studied the population genetic structure of the freshwater snail Galba schirazensis (Küster, 1862), a potential vector of infectious diseases such as fascioliasis. Galba schirazensis has now a worldwide distribution but a poorly known origin because this species has been distinguished only recently from the morphologically similar and cosmopolitan Galba truncatula (O.F. Müller, 1774). We developed specific microsatellite markers and sequenced a mitochondrial gene (cytochrome oxidase subunit I (CO1)) to study individuals of G. schirazensis from the Old World and the New World. We found very low genetic diversity within populations, no heterozygotes, and marked population structure — a pattern observed in other highly selfing lymnaeid species with recently enlarged distributions as a result of biological invasions. The total lack of observed heterozygosity in the few populations of G. schirazensis that displayed some allelic diversity suggests high selfing rates. We also found that the center of diversity, and by extension the origin area of this species, should be found in the New World, whereas Old World populations should rather result from a recent introduction of a genetically uniform population. The microsatellite markers developed here will help to clarify the history of expansion of G. schirazensis and might help to understand its role as a potential vector of infectious diseases. Key words: lymnaeids, Lymnaea, Galba schirazensis, Galba truncatula, vector, microsatellites, selfing. Résumé : Nous avons étudié la structure génétique des populations du gastéropode d’eau douce Galba schirazensis (Küster, 1862), un vecteur potentiel de maladies infectieuses telles que la fasciolose. Galba schirazensis présente aujourd’hui une répartition planétaire, mais une origine méconnue puisque cette espèce n’a que récemment été distinguée de Galba truncatula (O.F. Müller, 1774), une espèce cosmopolite semblable sur le plan morphologique. Nous avons mis au point des marqueurs microsatellites spécifiques et séquencé un gène mitochondrial (la sous-unité I de la cytochrome oxidase (CO1)) pour étudier des individus de G. schirazensis de l’Ancien Monde et du Nouveau Monde. Nous n’avons noté qu’une très faible diversité génétique au sein des populations, aucun hétérozygote et une structure marquée des populations, des caractéristiques observées chez d’autres espèces For personal use only. de lymnées très autofécondes dont les aires de répartition ont beaucoup cru récemment dans la foulée d’invasions biologiques. L’absence totale d’hétérozygotie observée dans les quelques populations de G. schirazensis qui présentaient un certain degré de diversité allélique indiquerait des taux d’autofécondation élevés. Nous avons également observé que le centre de diversité et, par extension, la région d’origine de cette espèce devraient se trouver dans le Nouveau Monde, alors que les populations de l’Ancien Monde seraient plutôt le résultat de l’introduction récente d’une population uniforme sur le plan génétique. Les marqueurs Received 15 December 2016. Accepted 26 June 2017. M. Lounnas, A.C. Correa, and C. Toty. MIVEGEC, UMR UM – CNRS 5290 – IRD 224 Maladies Infectieuses et Vecteurs : Ecologie, Génétique, Evolution et Contrôle, Centre IRD, BP 64501, 34394 Montpellier CEDEX 5, France. P. Alda. MIVEGEC, UMR UM – CNRS 5290 – IRD 224 Maladies Infectieuses et Vecteurs : Ecologie, Génétique, Evolution et Contrôle, Centre IRD, BP 64501, 34394 Montpellier CEDEX 5, France; Laboratorio de Zoologı´a de Invertebrados I, Departamento de Biologı´a, Bioquı´mica y Farmacia, Universidad Nacional del Sur, San Juan No. 670, B8000ICN, Bahı´a Blanca, Buenos Aires, Argentina. Can. J. Zool. Downloaded from www.nrcresearchpress.com by 195.83.99.4 on 06/06/18 P. David, M.-P. Dubois, and P. Jarne. Centre d’Ecologie Fonctionnelle et d’Evolution, UMR 5175, CNRS – Université de Montpellier – Université Paul Valéry Montpellier – EPHE, 1919 route de Mende, 34293 Montpellier CEDEX 5, France. M. Calvopiña. Carrera de Medicina, Facultad de Ciencias Médicas, Universidad Central del Ecuador, Quito, Ecuador. Y. Caron and B.T. Dung. Research Unit in Parasitology and Parasitic Diseases, Fundamental and Applied Research for Animals and Health (FARAH), Faculty of Veterinary Medicine, University of Liège, Belgium. M. Celi-Erazo. CIZ, Universidad Central de Ecuador, Quito, Ecuador. E.S. Loker. Center for Evolutionary and Theoretical Immunology, Museum of Southwestern Biology, Department of Biology, University of New Mexico, Albuquerque, NM 87131, USA. O. Noya. Centro para Estudios Sobre Malaria, Instituto de Altos Estudios “Dr. Arnoldo Gabaldón” – Instituto Nacional de Higiene “Rafael Rangel” del Ministerio del Poder Popular para la Salud y Sección de Biohelmintiasis, Instituto de Medicina Tropical, Facultad de Medicina, Universidad Central de Venezuela, Caracas, Venezuela. R. Rodríguez-Hidalgo. CIZ, Universidad Central de Ecuador, Quito, Ecuador; Facultad de Medicina Veterinaria y Zootecnia, Universidad Central del Ecuador, Quito, Ecuador. N. Uribe. Escuela de Bacteriología y Laboratorio Clínico, Facultad de Salud, Universidad Industrial de Santander, Bucaramanga, Colombia. J.-P. Pointier. USR 3278 CNRS–EPHE, CRIOBE Université de Perpignan, 68860 Perpignan-CEDEX, France. S. Hurtrez-Boussès. MIVEGEC, UMR UM – CNRS 5290 – IRD 224 Maladies Infectieuses et Vecteurs : Ecologie, Génétique, Evolution et Contrôle, Centre IRD, BP 64501, 34394 Montpellier CEDEX 5, France; Département de Biologie–Ecologie, Faculté des Sciences, Université Montpellier, 34095 Montpellier CEDEX 5, France. Corresponding author: Manon Lounnas (email: [email protected]). Copyright remains with the author(s) or their institution(s). Permission for reuse (free in most cases) can be obtained from RightsLink. Can. J. Zool. 96: 425–435 (2018) dx.doi.org/10.1139/cjz-2016-0319 Published at www.nrcresearchpress.com/cjz on 22 November 2017. 426 Can. J. Zool. Vol. 96, 2018 microsatellites ainsi mis au point aideront à préciser l’histoire de l’expansion de G. schirazensis et pourraient aider à comprendre son rôle comme vecteur potentiel de maladies infectieuses. [Traduit par la Rédaction] Mots-clés : lymnéidés, Lymnaea, Galba schirazensis, Galba truncatula, vecteur, microsatellites, autofécondation. Introduction of these markers by testing amplification in the morphologically During the last century, human activities and climatic change similar and closely related Galba species, i.e., G. truncatula, G. cubensis, have considerably accelerated the spread of species across their and G. viator. We also sequenced a mitochondrial gene (cyto- natural barriers and modified their areas of distribution (Kolar chrome oxidase subunit I (CO1)) to further elucidate the phylogeo- and Lodge 2001), threatening local biodiversity (Davis 2009). To graphic relationships among these populations and the populations better understand these threats, it is important to more fully studied by Bargues et al. (2011) and Correa et al. (2011). characterize the species involved and the expansion pathways. Materials and methods Freshwater systems are particularly sensitive to bioinvasion risks (Beisel and Lévêque 2010). The Mollusca includes a large number Development of specific microsatellite markers of species invasive in freshwater habitats (Nunes et al. 2015). We Snail DNA was extracted from four pooled individuals identi- here focus on the family Lymnaeidae in which several species have fied by Correa et al. (2011) as Galba sp. to reach a total of 2–3 ␮gof shown widespread long-distance colonization (Jabbour-Zahab et al. total DNA. These individuals were collected in Río Negro, Antio- 1997; Meunier et al. 2001; Kopp et al. 2012; Lounnas et al. 2017b). quia, Colombia (06°07=21== N, 75°26=57== W). DNA was extracted Long-distance dispersal can occur as a result of human activities, from foot tissue using the DNeasy Blood and Tissue Kit (Qiagen) such as aquarium trade (Duggan 2010). Lymnaeids display marked and individuals were identified to species using the nuclear genes resistance to desiccation, which increases their survival probabil- 18S (GenBank accession numbers JN614335, JN614339, JN614340, ity (Chapuis and Ferdy 2012). If released in conducive new envi- JN614342), ITS-1 (HQ283253, JN614429, JN614430, JN614432), ITS-2 ronments, then even a single individual can found a population (HQ283263, JN614455, JN614456, JN614458), and the mtDNA gene because lymnaeids are capable of self-fertilization, which also CO1 (JN614370, JN614371, JN614373, JN614374). All these sequences happens to be the main reproductive mode in some species (e.g., showed 99%–100% similarity with the sequences of G. schirazensis Meunier et al. 2004b; Escobar et al. 2011; Lounnas et al. 2017a). reported by Bargues et al. (2011). Such colonization events may also spread food- and water-borne Microsatellite loci were isolated from two enriched libraries trematodes carried by lymnaeids (Meunier et al. 2001; Mas-Coma (TC10 and TG10) following protocols described in Dubois et al. et al. 2005; Correa et al. 2010), either because dispersing snails are (2005) and using biotin-labeled microsatellite oligoprobes and themselves infected or because their presence
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