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Reviewing lymnaeid vectors of fascioliasis by ribosomal DNA sequence analyses

Published online by Cambridge University Press:  12 April 2024

M.D. Bargues*
Affiliation:
Departamento de Parasitología, Facultad de Farmacia, Universidad de Valencia, Av. Vicente Andrés Estellés s/n, 46100 Burjassot, Valencia, Spain
S. Mas-Coma
Affiliation:
Departamento de Parasitología, Facultad de Farmacia, Universidad de Valencia, Av. Vicente Andrés Estellés s/n, 46100 Burjassot, Valencia, Spain
*
*Fax: 00 34 96 3544769 E-mail: M.D.Bargues@uv.es

Abstract

Snails of the family Lymnaeidae are of great parasitological importance due to the numerous helminth species they transmit, mainly trematodiases (such as fascioliasis) of considerable medical and veterinary impact. The present knowledge of the genetics and host–parasite relationships of this gastropod group is far from adequate. Fascioliasis is caused by two species, Fasciola hepatica and F. gigantica, which, as in the case of other trematodes, show a marked snail host specificity. Many lymnaeid species involved in fascioliasis transmission still show a confused systematic-taxonomic status. The need for tools to distinguish and characterize species and populations of lymnaeids is evident and the present review concerns new molecular tools developed in recent years using nuclear ribosomal DNA sequences. The small subunit or 18S gene and the internal transcribed spacers ITS-2 and ITS-1 are analysed and evaluated as markers for taxon differentiation and relationships within the Lymnaeidae from genus and species levels to subspecies and population levels. rDNA sequence differences and genetic distances, and their value for reconstructing phylogenetic trees using different methods are considered. Nuclear rDNA sequences are appropriate tools on which to base a review of the systematics and taxonomy of the family Lymnaeidae, without excluding other valuable snail characteristics already available. A reconstruction of the lymnaeid system towards a more natural classification will undoubtedly be helpful in understanding parasite transmission and epidemiological features as well the dispersion of an emerging-reemerging disease such as fascioliasis. Nomenclature for nuclear rDNA genotyping in lymnaeids includes the main rDNA sequence regions able to furnish important information on interspecific differentiation and grouping as well as intraspecific variability of lymnaeid species. The composite haplotype code includes the rDNA markers arranged in order according to their well-known usefulness, in its turn related to their respective, more or less rapid evolutionary ratios, to distinguish between different taxonomic levels, from supraspecific taxa to the species level and up to the population level.

Type
Review Article
Copyright
Copyright © Cambridge University Press 2005

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References

Adema, C.M. & Loker, E.S. (1997) Specificity and immunobiology of larval digenean–snail associations. pp. 229253 in Fried, B. & Graczyk, T.K. (Eds) Advances in trematode biology . Boca Raton, Florida, CRC Press.Google Scholar
Almeyda-Artigas, R.J., Bargues, M.D. & Mas-Coma, S. (2000 a) ITS-2 rDNA sequencing of Gnathostoma species (Nematoda) and elucidation of the species causing human gnathostomiasis in the Americas. Journal of Parasitology 86, 537544.CrossRefGoogle ScholarPubMed
Almeyda-Artigas, R.J., Bargues, M.D. & Mas-Coma, S. (2000 b) rDNA of Gnathostoma species (Nematoda): ITS-2 microsatellites and 5.8S gene secondary structure. Research and Reviews in Parasitology 60, 5156.Google Scholar
Backeljau, T., De Bruyn, L., De Wolf, H., Jordaens, K., Van Dongen, S., Vehagen, R. & Winnepennincxk, B. (1995) Random amplified polymorphic DNA (RAPD) and parsimony methods. Cladistics 11, 119130.CrossRefGoogle ScholarPubMed
Bargues, M.D. & Mas-Coma, S. (1997) Phylogenetic analysis of lymnaeid snails based on 18S rDNA sequences. Molecular Biology and Evolution 14, 569577.CrossRefGoogle ScholarPubMed
Bargues, M.D., Mangold, A.J., Muñoz-Antoli, C., Pointier, J.P. & Mas-Coma, S. (1997) SSU rDNA characterization of lymnaeid snails transmitting human fascioliasis in South and Central America. Journal of Parasitology 83, 10861092.CrossRefGoogle ScholarPubMed
Bargues, M.D., Vigo, M., Horak, P., Dvorak, J., Paztner, R.A., Pointier, J.P., Jackiewicz, M., Meier-Brook, C. & Mas-Coma, S. (2001) European Lymnaeidae (Mollusca: Gastropoda), intermediate hosts of trematodiases, based on nuclear ribosomal DNA ITS-2 sequences. Infection, Genetics and Evolution 1, 85107.CrossRefGoogle ScholarPubMed
Bargues, M.D., Horak, P., Paztner, R.A., Pointier, J.P., Jackiewicz, M., Meier-Brook, C. & Mas-Coma, S. (2003) Insights into the relationships of Palaearctic and Nearctic lymnaeids (Mollusca: Gastropoda) by rDNA ITS-2 sequencing and phylogeny of stagnicoline intermediate host species of Fasciola hepatica . Parasite 10, 243255.CrossRefGoogle ScholarPubMed
Bargues, M.D., Artigas, P., Jackiewicz, M., Pointier, J.P. & Mas-Coma, S. (2005) Ribosomal DNA ITS-1 sequence analysis of European stagnicoline Lymnaeidae (Gastropoda) in Glöer, P. & Falkner, G. (Eds) Beiträge zur Süβwasser-Malakologie.Google Scholar
Festschrift, für Claus Meier-Brook, und Hans, D. Boeters 2005, Heldia (Münchner Malakologische Mitteilungen) 6, 5768.Google Scholar
Boray, J.C. (1969) Experimental fascioliasis in Australia. Advances in Parasitology 7, 95210.CrossRefGoogle ScholarPubMed
Boray, J.C. (1978) The potential impact of exotic Lymnaea spp. on fascioliasis in Australia. Veterinary Parasitology 4, 127141.CrossRefGoogle Scholar
Boray, J.C. (1982) Fascioliasis. pp. 7188 in Hillyer, G.V. & Hopla, C.E. (Eds) Handbook series in zoonoses, Section C, Parasitic zoonoses . Vol. III. Boca Raton, Florida, CRC Press.Google Scholar
Burch, J.B. (1965) Chromosome numbers and systematics in euthyneuran snails. Proceedings of the First European Malacological Congress, Abstracts Book 1, 215241.Google Scholar
Burch, J.B. (1968 a) Erinna newcombi of Hawaii and Limnaea onychia of Japan. Malacological Review 1, 1530.Google Scholar
Burch, J.B. (1968 b) Morphology vs. immunology. Response. Bulletin of the American Malacological Union 34, 2528.Google Scholar
Burch, J.B. (1980) A guide to the freshwater snails of the Philippines. Malacological Review 13, 121143.Google Scholar
Burch, J.B. (1982 a) North American freshwater snails. Identification keys, generic synonymy, supplemental notes, glossary, references, index. Walkerana, Transactions of the POETS Society 1, 216365.Google Scholar
Burch, J.B. (1982 b) Freshwater snails (Mollusca: Gastropoda) of North America (North of Mexico). Environmental monitoring and support laboratory office of research and development, US Environmental Protection Agency, Cincinnati, Ohio, 249 pp.Google Scholar
Burch, J.B. (1988) North American freshwater snails. Introduction, systematics, nomenclature, identification, morphology, habitats, distribution. Walkerana, Transactions of the POETS Society 2, 180.Google Scholar
Burch, J.B. & Ayers, P.A. (1973) Breeding experiments with Stagnicola elodes and Stagnicola emarginata . Malacological Review 6, 5152.Google Scholar
Burch, J.B. & Lindsay, G.K. (1968) An immunological approach to lymnaeid systematics. Bulletin of the American Malacological Union 34, 2223.Google Scholar
Burch, J.B. & Lindsay, G.K. (1973 a) Taxonomic groupings in the Lymnaeidae. Bulletin of the American Malacological Union 38, 15.Google Scholar
Burch, J.B. & Lindsay, G.K. (1973 b) Apparent hybrids from a laboratory culture of Lymnaea stagnalis and Bulimnea megasoma . Malacological Review 6, 6162.Google Scholar
Coutellec-Vreto, M.A., Guiller, A. & Daguzan, J. (1994) Allozyme variation in some populations of the freshwater snails Lymnaea peregra , L. auricularia and L. stagnalis (Gastropoda: Pulmonata). Journal of Molluscan Studies 60, 393403.CrossRefGoogle Scholar
Chen, M.G. & Mott, K.E. (1990) Progress in assessment of morbidity due to Fasciola hepatica infection: a review of recent literature. Tropical Diseases Bulletin 87, R1R38.Google Scholar
Davis, G.M. (1978) Experimental methods in molluscan systematics. pp. 99169 in Fretter, V. & Peake, J. (Eds) Pulmonates, Vol. 2A. Systematics, evolution and ecology , London, Academic Press.Google Scholar
De Rijk, P., Neefs, J.M., Van De Peer, Y. & De Wachter, R. (1992) Compilation of small ribosomal subunit RNA sequences. Nucleic Acids Research 20, 20752089.CrossRefGoogle ScholarPubMed
Glöer, P. & Meier-Brook, C. (1998) Süsswassermollusken. Ein Bestimmungsschlüssel für die Bundesrepublik Deutschland . (11th and 12th edns) Deutscher Jugendbund für Naturbeobachtung, Hamburg, Germany.Google Scholar
Gonzalez, I.L., Chambers, C., Gorski, J.L., Stambolian, D., Schmickel, R.D. & Sylvester, J.E. (1990) Sequence and structure correlation of human ribosomal transcribed spacers. Journal of Molecular Biology 212, 2735.CrossRefGoogle ScholarPubMed
Gutierrez, A., Pointier, J.P., Fraga, J., Jobet, E., Modat, S., Perez, R.T., Yong, M., Sanchez, J., Loker, E.S. & Theron, A. (2003) Fasciola hepatica: identification of molecular markers for resistant and susceptible Pseudosuccinea columella snail hosts. Experimental Parasitology 105, 211218.CrossRefGoogle ScholarPubMed
Hubendick, B. (1951) Recent Lymnaeidae. Their variation, morphology, taxonomy, nomenclature, and distribution. Kungliga Svenska Vetenskapsakademiens Handlingar, Fjärde Serien 3, 1223+5 pl.Google Scholar
Hubendick, B. (1978) Systematics and comparative morphology of the Basommatophora. pp. 147 in Fretter, V. & Peake, J. (Eds) Pulmonates, Vol. 2A. Systematics, evolution and ecology , London, Academic Press.Google Scholar
Inaba, A. (1969) Cytotaxonomic studies of lymnaeid snails. Malacologia 7, 143168.Google Scholar
Jabbour-Zahab, R., Pointier, J.P., Jourdane, J., Jarne, P., Oviedo, J.A., Bargues, M.D., Mas-Coma, S., Angles, R., Perera, G., Balzan, C., Khallaayoune, K. & Renaud, F. (1997) Phylogeography and genetic divergence of some lymnaeid snails, intermediate hosts of human and animal fascioliasis, with special reference to lymnaeids from the Bolivian Altiplano. Acta Tropica 64, 191203.CrossRefGoogle ScholarPubMed
Jackiewicz, M. (1988) The penis as a valuable diagnostic feature in lower taxonomic units of the family Lymnaeidae (Gastropoda, Pulmonata). Malakologische Abhandlungen 13, 2326.Google Scholar
Jackiewicz, M. (1989) Innenstruktur der Prostata und des Praeputiums bei Omphiscola glabra (O.F. Müll.) (Gastropoda, Basommatophora: Lymnaeidae). Malakologische Abhandlungen 14, 713.Google Scholar
Jackiewicz, M. (1993) Phylogeny and relationships within the European species of the family Lymnaeidae. Folia Malacologica 5, 6195.CrossRefGoogle Scholar
Jackiewicz, M. (1998) European species of the family Lymnaeidae (Gastropoda: Pulmonata: Basommatophora). Genus 9, 193.Google Scholar
Jarne, P. & Delay, B. (1990 a) Population genetics of Lymnaea peregra (Müller) (Gastropoda: Pulmonata) in Lake Geneva. Journal of Molluscan Studies 56, 317322.CrossRefGoogle Scholar
Jarne, P. & Delay, B. (1990 b) Inbreeding depression and self-fertilization in Lymnaea peregra (Gastropoda: Pulmonata). Heredity 64, 169175.CrossRefGoogle Scholar
Jarne, P. & Lagoda, P.J.L. (1996) Microsatellites, from molecules to populations and back. Trends in Ecology and Evolution 11, 424429.CrossRefGoogle ScholarPubMed
Jarne, P., Vianey-Liaud, M. & Delay, B. (1993) Selfing and crossing in hermaphrodite freshwater gastropods (Basommatophora): where, when and why. Biological Journal of the Linnean Society 49, 99125.CrossRefGoogle Scholar
Jarne, P., David, P. & Viard, F. (1998) Microsatellites, transposable elements and the X chromosome. Molecular Biology and Evolution 15, 2834.CrossRefGoogle ScholarPubMed
Kalbe, M., Haberl, B. & Haas, W. (1997) Miracidial host-finding in Fasciola hepatica and Trichobilharzia ocellata is stimulated by species-specific glycoconjugates released from the host snails. Parasitology Research 83, 806812.CrossRefGoogle ScholarPubMed
Kendall, S.B. & Parfitt, J.W. (1959) Studies on the susceptibility of some species of Lymnaea to infection with Fasciola gigantica and F. hepatica . Annals of Tropical Medicine and Parasitology 53, 220227.CrossRefGoogle Scholar
Malek, E.A. (1980) Snail-transmitted parasitic diseases , Vol. 1 and 2. Boca Raton, Florida, CRC Press.Google Scholar
Malek, E.A. (1985) Snail hosts of schistosomiasis and other snail-transmitted diseases in tropical America: a manual. Pan American Health Organization, Scientific Publication 478, 1325.Google Scholar
Mas-Coma, S. (1999) Los espaciadores transcritos internos (ITSs) del ADN ribosomal como marcadores en sistemática, ecología, evolución y filogenia de parásitos y vectores. XIV Congreso Latinoamericano de Parasitología (FLAP), Acapulco, México, Libro de Resúmenes 1, 56.Google Scholar
Mas-Coma, S. (2004 a) Human fascioliasis. pp. 305322 in Cotruvo, J.A., Dufour, A., Rees, G., Bartram, J., Carr, R., Cliver, D.O., Craun, G.F., Fayer, R. & Gannon, V.P.J. (Eds) Waterborne zoonoses: identification, causes and control . World Health Organization (WHO) London, IWA Publishing.Google Scholar
Mas-Coma, S. (2004 b) Human fascioliasis: epidemiological patterns in human endemic areas of South America, Africa and Asia. Southeast Asian Journal of Tropical Medicine and Public Health 35, 111.Google Scholar
Mas-Coma, S. & Bargues, M.D. (1997) Human liver flukes: a review. Research and Reviews in Parasitology 57, 145218.Google Scholar
Mas-Coma, S., Bargues, M.D. & Esteban, J.G. (1999 a) Human fasciolosis. pp. 411434 in Dalton, J.P. (Eds) Fasciolosis . Wallingford, Oxon, CAB International.Google Scholar
Mas-Coma, S., Esteban, J.G. & Bargues, M.D. (1999 b) Epidemiology of human fascioliasis: a review and proposed new classification. Bulletin of the World Health Organization 77, 340346.Google ScholarPubMed
Mas-Coma, S., Bargues, M.D., Marty, A.M. & Neafie, R.C. (2000) Hepatic trematodiases. pp. 6992 in Meyers, W.M., Neafie, R.C., Marty, A.M. & Wear, D.J. (Eds) Pathology of infectious diseases. Vol. 1. Helminthiases , Washington DC, Armed Forces Institute of Pathology and American Registry of Pathology.Google Scholar
Mas-Coma, S., Funatsu, I.R. & Bargues, M.D. (2001) Fasciola hepatica and lymnaeid snails occurring at very high altitude in South America. Parasitology 123, S115S127.CrossRefGoogle ScholarPubMed
Mas-Coma, S., Bargues, M.D., Valero, M.A. & Fuentes, M.V. (2003) Adaptation capacities of Fasciola hepatica and their relationships with human fascioliasis: from below sea level up to the very high altitude. pp. 81123 in Combes, C. & Jourdane, J. (Eds) Taxonomy, ecology and evolution of metazoan parasites . Vol. 2. Perpignan, Presses Universitaires de Perpignan.Google Scholar
Meier-Brook, C. & Bargues, M.D. (2002) Catascopia, a new genus for three Nearctic and one Palaearctic stagnicoline species (Gastropoda: Lymnaeidae). Folia Malacologica 10, 8384.CrossRefGoogle Scholar
Meunier, C., Tirard, C., Hurtrez-Bousses, S., Durand, P., Bargues, M.D., Mas-Coma, S., Pointier, J.P., Jourdane, J. & Renaud, F. (2001) Lack of molluscan host diversity and the transmission of an emerging parasitic disease in Bolivia. Molecular Ecology 10, 13331340.CrossRefGoogle ScholarPubMed
Oviedo, J.A., Bargues, M.D. & Mas-Coma, S. (1995) Lymnaeid snails in the human fascioliasis high endemic zone of the Northern Bolivian Altiplano. Research and Reviews in Parasitology 55, 3543.Google Scholar
Patterson, C.M. & Burch, J.B. (1978) Chromosomes of pulmonate molluscs. pp. 171217 in Fretter, V. & Peake, J. (Eds) Pulmonates, Vol. 2A. Systematics, evolution and ecology , London, Academic Press.Google Scholar
Perez-Reyes, R., Jimenez-Nava, J.J. & Varela-Ramirez, A. (1985) Fascioliasis en el Estado de Chihuahua. México. I. Susceptibilidad de Fossaria modicella (Say, 1825), huésped intermediario local. Revista Latino-Americana de Microbiología 27, 367372.Google ScholarPubMed
Remigio, E.A. (2002) Molecular phylogenetic relationships in the aquatic snail genus Lymnaea, the intermediate host of the causative agent of fascioliasis: insights from broader taxon sampling. Parasitology Research 88, 687696.Google ScholarPubMed
Remigio, E.A. & Blair, D. (1997 a) Molecular systematics of the freshwater snail family Lymnaeidae (Pulmonata: Basommatophora) utilising mitochondrial ribosomal DNA sequences. Journal of Molluscan Studies 63, 173185.CrossRefGoogle Scholar
Remigio, E.A. & Blair, D. (1997 b) Relationships among problematic North American stagnicoline snails (Pulmonata: Lymnaeidae) reinvestigated using nuclear ribosomal DNA internal transcribed spacer sequences. Canadian Journal of Zoology 75, 15401545.CrossRefGoogle Scholar
Rollinson, D. & Southgate, V.R. (1985) Schistosome and snail populations: genetic variability and parasite transmission. pp. 91109 in Rollinson, D. & Anderson, R.M. (Eds) Ecology and genetics of host–parasite interactions , London, Academic Press.Google Scholar
Roos, M.H., Hoekstra, R., Plas, M.E., Otsen, M. & Lenstra, J.A. (1998) Polymorphic DNA markers in the genome of parasitic nematodes. Journal of Helminthology 72, 291294.CrossRefGoogle ScholarPubMed
Rudolph, P.H. & Burch, J.B. (1989) Electrophorectic analysis of enzymes in three species of Stagnicola (Pulmonata: Lymnaeidae). Journal of Medical and Applied Malacology 1, 5764.Google Scholar
Rybska, E., Pacak, A., Szweykowska-Kulinska, Z. & Lesicki, A. (2000) Taxonomy of European Lymnaeidae (Gastropoda: Pulmonata) in studies with the use of molecular biology techniques. I. Preliminary view on the subgenus Stagnicola Leach, 1830 on the basis of RAPD analysis. Folia Malacologica 8, 277284.CrossRefGoogle Scholar
Samadi, S., Roumegoux, A., Bargues, M.D., Mas-Coma, S., Yong, M. & Pointier, J.P. (2000) Morphological studies of lymnaeid snails from the human fascioliasis endemic zone of Bolivia. Journal of Molluscan Studies 66, 3144.CrossRefGoogle Scholar
Stothard, J.R., Bremond, P., Andriamaro, L., Loxton, N.J., Sellin, B., Sellin, E. & Rollinson, D. (2000) Molecular characterization of the freshwater snail Lymnaea natalensis (Gastropoda: Lymnaeidae) on Madagascar with an observation of an unusual polymorphism in ribosomal small subunit genes. Journal of Zoology 252, 303315.CrossRefGoogle Scholar
Te, G.A. (1976) A summary of pulmonate distribution information contained in Zilch's 1959–1960 monograph: Gastropoda, Teil 2, Euthyneura. Malacological Review 9, 3953.Google Scholar
Torres, R.A., Ganal, M. & Hembleben, V. (1990) GC balance in the internal transcribed spacers ITS1 and ITS2 of nuclear ribosomal RNA genes. Journal of Molecular Evolution 30, 170181.CrossRefGoogle Scholar
Trouve, S., Degen, L., Meunier, C., Tirard, C., Hurtrez-Bousses, S., Durand, P., Guegan, J.F., Goudet, J. & Renaud, F. (2000) Microsatellites in the hermaphroditic snail, Lymnaea truncatula, intermediate host of the liver fluke, Fasciola hepatica . Molecular Ecolology 9, 16621663.CrossRefGoogle ScholarPubMed
Ueno, H., Arandia, R., Morales, G. & Medina, G. (1975) Fascioliasis of livestock and snail host for Fasciola in the Altiplano region of Bolivia. National Institute of Animal Health Quarterly 15, 6167.Google ScholarPubMed
Vigo, M., Bargues, M.D., Yong, M., Arenas, J.A., Naquira, C., Paraense, W.L., Pointier, J.P. & Mas-Coma, S. (2000) Molecular characterisation of a snail species transmitting fascioliasis, Lymnaea columella (Gastropoda: Lymnaeidae), from Cuba, Guadeloupe, Venezuela, Peru and Brazil. VX International Congress for Tropical Medicine and Malaria, Cartagena, Colombia, Abstracts Book 2, 96.Google Scholar
Walter, H.J. (1968) Evolution, taxonomic revolution, and zoogeography of the Lymnaeidae. Bulletin of the American Malacological Union 34, 1820.Google Scholar
Wheeler, W.C. & Honeycutt, R.L. (1988) Paired sequence difference in ribosomal RNAs: evolutionary and phylogenetic implications. Molecular Biology and Evolution 51, 9096.Google Scholar
Winnepenninckx, B., Backeljau, T. & De Wachter, R. (1994) Small ribosomal subunit RNA and the phylogeny of Mollusca. Nautilus 2, 98110.Google Scholar
Wright, C.A. (1973) Flukes and snails . New York, Macmillan.Google Scholar
Zilch, A. (19591960) Gastropoda (Euthyneura). pp. 91102 in Schindewolf, O. (Ed.) Handbuch der Paleozoologie . Berlin, Borntraeger.Google Scholar