Lymnaea schirazensis, an Overlooked Snail Distorting Fascioliasis Data: Genotype, Phenotype, Ecology, Worldwide Spread, Susceptibility, Applicability Marı ´a Dolores Bargues 1 *, Patricio Artigas 1 , Messaoud Khoubbane 1 , Rosmary Flores 1 , Peter Glo ¨ er 2 , Rau ´l Rojas-Garcı´a 3 , Keyhan Ashrafi 4 , Gerhard Falkner 5,6 , Santiago Mas-Coma 1 1 Departamento de Parasitologı ´a, Facultad de Farmacia, Universidad de Valencia, Valencia, Spain, 2 Mu ¨ nchner Malakologische Mitteilungen Heldia, Friedrich-Held Gesellschaft, Hetlingen, Germany, 3 Laboratorio de Biologı ´a de Para ´sitos y Vectores, Escuela de Biologı ´a, Beneme ´rita Universidad Auto ´ noma de Puebla, Puebla, Me ´ xico, 4 Department of Medical Microbiology and Parasitology, School of Medicine, Gilan University of Medical Sciences, Rasht, Iran, 5 Staatliches Museum fu ¨ r Naturkunde Stuttgart, Stuttgart, Germany, 6 De ´ partement Syste ´matique et Evolution, UMS ‘‘Taxonomie et Collections’’, Muse ´um National d’Histoire Naturelle, Paris, France Abstract Background: Lymnaeid snails transmit medical and veterinary important trematodiases, mainly fascioliasis. Vector specificity of fasciolid parasites defines disease distribution and characteristics. Different lymnaeid species appear linked to different transmission and epidemiological patterns. Pronounced susceptibility differences to absolute resistance have been described among lymnaeid populations. When assessing disease characteristics in different endemic areas, unexpected results were obtained in studies on lymnaeid susceptibility to Fasciola. We undertook studies to understand this disease transmission heterogeneity. Methodology/Principal Findings: A ten-year study in Iran, Egypt, Spain, the Dominican Republic, Mexico, Venezuela, Ecuador and Peru, demonstrated that such heterogeneity is not due to susceptibility differences, but to a hitherto overlooked cryptic species, Lymnaea schirazensis, confused with the main vector Galba truncatula and/or other Galba/ Fossaria vectors. Nuclear rDNA and mtDNA sequences and phylogenetic reconstruction highlighted an old evolutionary divergence from other Galba/Fossaria species, and a low intraspecific variability suggesting a recent spread from one geographical source. Morphometry, anatomy and egg cluster analyses allowed for phenotypic differentiation. Selfing, egg laying, and habitat characteristics indicated a migration capacity by passive transport. Studies showed that it is not a vector species (n = 8572 field collected, 20 populations): snail finding and penetration by F. hepatica miracidium occur but never lead to cercarial production (n = 338 experimentally infected). Conclusions/Significance: This species has been distorting fasciolid specificity/susceptibility and fascioliasis geographical distribution data. Hence, a large body of literature on G. truncatula should be revised. Its existence has henceforth to be considered in research. Genetic data on livestock, archeology and history along the 10,000-year post-domestication period explain its wide spread from the Neolithic Fertile Crescent. It is an efficient biomarker for the follow-up of livestock movements, a crucial aspect in fascioliasis emergence. It offers an outstanding laboratory model for genetic studies on susceptibility/resistance in F. hepatica/lymnaeid interaction, a field of applied research with disease control perspectives. Citation: Bargues MD, Artigas P, Khoubbane M, Flores R, Glo ¨er P, et al. (2011) Lymnaea schirazensis, an Overlooked Snail Distorting Fascioliasis Data: Genotype, Phenotype, Ecology, Worldwide Spread, Susceptibility, Applicability. PLoS ONE 6(9): e24567. doi:10.1371/journal.pone.0024567 Editor: Erika Martins Braga, Universidade Federal de Minas Gerais, Brazil Received February 24, 2011; Accepted August 14, 2011; Published September 29, 2011 Copyright: ß 2011 Bargues et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: Studies were funded by Projects No. PM97-0099, No. BOS2000-0570-C02-02, No. BOS2002-01978, No. SAF2006-09278 and No. SAF2010-20805 of the Ministry of Education and Ministry of Science and Innovation, Madrid; Project No. 3006/99 of the Direccio ´ n General de Cooperacio ´ n al Desarrollo, Generalitat Valenciana, Valencia; Project No. PI030545 of the Fondo de Investigacio ´ n Sanitaria (FIS), Ministry of Health, Madrid; and by the Red de Investigacio ´ n de Centros de Enfermedades Tropicales (Projects No. C03/04, No. ISCIII2005-PI050574 and No. ISCIII-RETIC RD06/0021/0017 of the Programa de Redes Tema ´ticas de Investigacio ´ n Cooperativa RETICS/FEDER), FIS, Ministry of Health, Madrid, Spain. Joint coordination activities with Mexico, Venezuela and Peru were carried out within the frame of Project No. RLA5049 of the International Atomic Energy Agency (IAEA)(Animal Production and Health Section, Joint Food and Agriculture Organization/IAEA Division of Nuclear Techniques in Food and Agriculture, Department of Nuclear Sciences and Applications, IAEA Headquaters Vienna, Austria). Part of this work was made possible thanks to a personal fellowship granted to PA by the Agencia Espan ˜ ola de Cooperacio ´ n Internacional, Ministry of Foreign Affairs, Madrid, Spain. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. The content is solely the responsibility of the authors and does not necessarily represent the official views of the funding and supporting agencies. Competing Interests: The authors have declared that no competing interests exist. * E-mail: M.D.Bargues@uv.es Introduction Freshwater snails of the family Lymnaeidae (Gastropoda) act as intermediate hosts or vectors of numerous digenean trematode species. Many lymnaeid species are of applied interest as they transmit several trematode species of large-scale medical and veterinary impact, among which fasciolids are the most important [1]. Fasciola hepatica and F. gigantica are two large-sized fasciolid trematode parasite species that cause fascioliasis, a disease which affects humans and livestock species almost everywhere [2]. This highly pathogenic liver parasitosis has been emerging in many countries of Latin America, Europe, Africa and Asia in the last two PLoS ONE | www.plosone.org 1 September 2011 | Volume 6 | Issue 9 | e24567