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      Adaptation of Lymnaea fuscus and Radix balthica to Fasciola hepatica through the experimental infection of several successive snail generations

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          Abstract

          Background

          High prevalence of Fasciola hepatica infection (>70%) was noted during several outbreaks before the 2000s in several French farms where Galba truncatula is lacking. Other lymnaeids such as Lymnaea fuscus, L. glabra and/or Radix balthica are living in meadows around these farms but only juvenile snails can sustain complete larval development of F. hepatica while older snails were resistant. The low prevalence of infection (<20%) and limited cercarial production (<50 cercariae per infected snail) noted with these juveniles could not explain the high values noted in these cattle herds. As paramphistomosis due to Calicophoron daubneyi was not still noted in these farms, the existence of another mode of infection was hypothesized. Experimental infection of several successive generations of L. glabra, originating from eggs laid by their parents already infected with this parasite resulted in a progressive increase in prevalence of snail infection and the number of shed cercariae. The aim of this paper was to determine if this mode of snail infection was specific to L. glabra, or it might occur in other lymnaeid species such as L. fuscus and R. balthica.

          Methods

          Five successive generations of L. fuscus and R. balthica were subjected to individual bimiracidial infections in the laboratory. Resulting rediae and cercariae in the first four generations were counted after snail dissection at day 50 p.e. (20°C), while the dynamics of cercarial shedding was followed in the F5 generation.

          Results

          In the first experiment, prevalence and intensity of F. hepatica infection in snails progressively increased from the F1 ( R. balthica) or F2 ( L. fuscus) generation. In the second experiment , the prevalence of F. hepatica infection and the number of shed cercariae were significantly lower in L. fuscus and R. balthica (without significant differences between both lymnaeids) than in G. truncatula.

          Conclusion

          The F. hepatica infection of several successive snail generations, coming from parents infected with this parasite, resulted in a progressive increase in prevalence and intensity of snail infection. This may explain high prevalence of fasciolosis noted in several cattle-breeding farms when the common snail host of this digenean, G. truncatula, is lacking.

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          Most cited references 39

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          Chapter 2. Fasciola, lymnaeids and human fascioliasis, with a global overview on disease transmission, epidemiology, evolutionary genetics, molecular epidemiology and control.

          Fascioliasis, caused by liver fluke species of the genus Fasciola, has always been well recognized because of its high veterinary impact but it has been among the most neglected diseases for decades with regard to human infection. However, the increasing importance of human fascioliasis worldwide has re-launched interest in fascioliasis. From the 1990s, many new concepts have been developed regarding human fascioliasis and these have furnished a new baseline for the human disease that is very different to a simple extrapolation from fascioliasis in livestock. Studies have shown that human fascioliasis presents marked heterogeneity, including different epidemiological situations and transmission patterns in different endemic areas. This heterogeneity, added to the present emergence/re-emergence of the disease both in humans and animals in many regions, confirms a worrying global scenario. The huge negative impact of fascioliasis on human communities demands rapid action. When analyzing how better to define control measures for endemic areas differing at such a level, it would be useful to have genetic markers that could distinguish each type of transmission pattern and epidemiological situation. Accordingly, this chapter covers aspects of aetiology, geographical distribution, epidemiology, transmission and control in order to obtain a solid baseline for the interpretation of future results. The origins and geographical spread of F. hepatica and F. gigantica in both the ruminant pre-domestication times and the livestock post-domestication period are analyzed. Paleontological, archaeological and historical records, as well as genetic data on recent dispersal of livestock species, are taken into account to establish an evolutionary framework for the two fasciolids across all continents. Emphasis is given to the distributional overlap of both species and the roles of transportation, transhumance and trade in the different overlap situations. Areas with only one Fasciola spp. are distinguished from local and zonal overlaps in areas where both fasciolids co-exist. Genetic techniques applied to liver flukes in recent years that are useful to elucidate the genetic characteristics of the two fasciolids are reviewed. The intra-specific and inter-specific variabilities of 'pure'F. hepatica and 'pure'F. gigantica were ascertained by means of complete sequences of ribosomal deoxyribonucleic acid (rDNA) internal transcribed spacer (ITS)-2 and ITS-1 and mitochondrial deoxyribonucleic acid (mtDNA) cox1 and nad1 from areas with only one fasciolid species. Fasciolid sequences of the same markers scattered in the literature are reviewed. The definitive haplotypes established appear to fit the proposed global evolutionary scenario. Problems posed by fasciolid cross-breeding, introgression and hybridization in overlap areas are analyzed. Nuclear rDNA appears to correlate with adult fluke characteristics and fasciolid/lymnaeid specificity, whereas mtDNA does not. However, flukes sometimes appear so intermediate that they cannot be ascribed to either F. hepatica-like or F. gigantica-like forms and snail specificity may be opposite to the one deduced from the adult morphotype. The phenotypic characteristics of adults and eggs of 'pure'F. hepatica and F. gigantica, as well as of intermediate forms in overlap areas, are compared, with emphasis on the definitive host influence on egg size in humans. Knowledge is sufficient to support F. hepatica and F. gigantica as two valid species, which recently diverged by adaptation to different pecoran and lymnaeid hosts in areas with differing environmental characteristics. Their phenotypic differences and ancient pre-domestication origins involve a broad geographical area that largely exceeds the typical, more local scenarios known for sub-species units. Phenomena such as abnormal ploidy and aspermic parthenogenesis in hybrids suggest that their separate evolution in pre-domestication times allowed them to achieve almost total genetic isolation. Recent sequencing results suggest that present assumptions on fasciolid-lymnaeid specificity might be wrong. The crucial role of lymnaeids in fascioliasis transmission, epidemiology and control was the reason for launching a worldwide lymnaeid molecular characterization initiative. This initiative has already furnished useful results on several continents. A standardized methodology for fasciolids and lymnaeids is proposed herein in order that future work is undertaken on a comparable basis. A complete understanding of molecular epidemiology is expected to help greatly in designing global actions and local interventions for control of fascioliasis.
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            European Lymnaeidae (Mollusca: Gastropoda), intermediate hosts of trematodiases, based on nuclear ribosomal DNA ITS-2 sequences.

            Freshwater snails of the family Lymnaeidae are of a great parasitological importance because of the very numerous helminth species they transmit, mainly trematodiases of large medical and veterinary impact. The present knowledge on the genetics of lymnaeids and on their parasite-host inter-relationships is far from being sufficient. The family is immersed in a systematic-taxonomic confusion. The necessity for a tool which enables species distinction and population characterization is evident. This paper aims to review the European Lymnaeidae basing on the second internal transcribed spacer ITS-2 of the nuclear ribosomal DNA. The ITS-2 sequences of 66 populations of 13 European and 1 North American lymnaeid species, including the five generic (or subgeneric) taxa Lymnaea sensu stricto, Stagnicola, Omphiscola, Radix and Galba, have been obtained. The ITS-2 proves to be a useful marker for resolving supraspecific, specific and population relationships in Lymnaeidae. Three different groupings according to their ITS-2 length could be distinguished: Radix and Galba may be considered the oldest taxa (370-406 bp lengths), and Lymnaea s. str., European Stagnicola and Omphiscola (468-491 bp lengths) the most recent, American Stagnicola and Hinkleyia being intermediate (434-450 bp lengths). This hypothesis agrees with the phylogeny of lymnaeids based on palaeontological data, chromosome numbers and radular dentition. ITS-2 sequences present a conserved central region flanked by two variable lateral regions corresponding to the 5' and 3' ends. The number of repeats of two microsatellites found in this conserved central region allows to differentiate Radix from all other lymnaeids. Phylogenetic trees showed four clades: (A) Lymnaea s. str., European Stagnicola and Omphiscola; (B) Radix species; (C) Galba truncatula; and (D) North American stagnicolines. ITS-2 results suggest that retaining Stagnicola as a subgenus of Lymnaea may be the most appropriate and that genus status for Omphiscola is justified. Radix shows a complexity suggesting different evolutionary lines, whereas G. truncatula appears to be very homogeneous. North American and European stagnicolines do not belong to the same supraspecific taxon; the genus Hinkleyia may be used for the American stagnicolines. Genetic distances and sequence differences allowed us to distinguish the upper limit to be expected within a single species and to how different sister species may be. S. palustris, S. fuscus and S. corvus proved to be valid species, but S. turricula may not be considered a species independent from S. palustris. Marked nucleotide divergences and genetic distances detected between different S. fuscus populations may be interpreted as a process of geographic differentiation developping in the present. Among Radix, six valid species could be distinguished: R. auricularia, R. ampla, R. peregra (=R. ovata;=R. balthica), R. labiata, R. lagotis and Radix sp. The information which the ITS-2 marker furnishes is of applied interest concerning the molluscan host specificity of the different trematode species. The phylogenetic trees inferred from the ITS-2 sequences are able to differentiate between lymnaeids transmitting and those non-transmitting fasciolids, as well as between those transmitting F. hepatica and those transmitting F. gigantica. The Fasciola specificity is linked to the two oldest genera which moreover cluster together in the phylogenetic trees, suggesting an origin of the Fasciola ancestors related to the origin of this branch. European Trichobilharzia species causing human dermatitis are transmitted only by lymnaeids of the Radix and Lymnaea s. str.-Stagnicola groups. Results suggest the convenience of reinvestigating compatibility differences after accurate lymnaeid species classification by ITS-2 sequencing. Similarly, ITS-2 sequencing would allow a step forward in the appropriate rearrangement of the actual systematic confusion among echinostomatids.
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              Bridging gaps in the molecular phylogeny of the Lymnaeidae (Gastropoda: Pulmonata), vectors of Fascioliasis

              Background Lymnaeidae snails play a prominent role in the transmission of helminths, mainly trematodes of medical and veterinary importance (e.g., Fasciola liver flukes). As this family exhibits a great diversity in shell morphology but extremely homogeneous anatomical traits, the systematics of Lymnaeidae has long been controversial. Using the most complete dataset to date, we examined phylogenetic relationships among 50 taxa of this family using a supermatrix approach (concatenation of the 16 S, ITS-1 and ITS-2 genes, representing 5054 base pairs) involving both Maximum Likelihood and Bayesian Inference. Results Our phylogenetic analysis demonstrates the existence of three deep clades of Lymnaeidae representing the main geographic origin of species (America, Eurasia and the Indo-Pacific region). This phylogeny allowed us to discuss on potential biological invasions and map important characters, such as, the susceptibility to infection by Fasciola hepatica and F. gigantica, and the haploid number of chromosomes (n). We found that intermediate hosts of F. gigantica cluster within one deep clade, while intermediate hosts of F. hepatica are widely spread across the phylogeny. In addition, chromosome number seems to have evolved from n = 18 to n = 17 and n = 16. Conclusion Our study contributes to deepen our understanding of Lymnaeidae phylogeny by both sampling at worldwide scale and combining information from various genes (supermatrix approach). This phylogeny provides insights into the evolutionary relationships among genera and species and demonstrates that the nomenclature of most genera in the Lymnaeidae does not reflect evolutionary relationships. This study highlights the importance of performing basic studies in systematics to guide epidemiological control programs.
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                Author and article information

                Contributors
                Journal
                Parasit Vectors
                Parasit Vectors
                Parasites & Vectors
                BioMed Central
                1756-3305
                2014
                1 July 2014
                : 7
                : 296
                Affiliations
                [1 ]INSERM 1094, Faculties of Medicine and Pharmacy, Limoges 87025, France
                [2 ]PADESCA Laboratory, Veterinary Science Institute, University Constantine 1, El Khroub 25100, Algeria
                Article
                1756-3305-7-296
                10.1186/1756-3305-7-296
                4090179
                24986589
                Copyright © 2014 Rondelaud et al.; licensee BioMed Central Ltd.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

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