Abstract
Genetic variation at 21 gene-enzyme systems was studied in a sample of an adult population of Anisakis typica (Diesing, 1860) recovered in the dolphin Sotalia fluviatilis from the Atlantic coast of Brazil. The characteristic alleles, detected in this population, made it possible to identify as A. typica, Anisakis larvae with a Type I morphology (sensu Berland, 1961) from various fishes: Thunnus thynnus and Auxis thazard from Brazil waters, Trachurus picturatus and Scomber japonicus from Madeiran waters, Scomberomorus commerson, Euthynnus affinis, Sarda orientalis and Coryphaena hippurus from the Somali coast of the Indian Ocean, and Merluccius merluccius from the Eastern Mediterranean. Characteristic allozymes are given for the identification, at any life-stage and in both sexes, of A. typica and the other Anisakis species so far studied genetically. The distribution of A. typica in warmer temperate and tropical waters is confirmed; the definitive hosts so far identified for this species belong to delphinids, phocoenids and pontoporids. The present findings represent the first established records of intermediate/paratenic hosts of A. typica and extend its range to Somali waters of the Indian Ocean and to the Eastern Mediterranean Sea. A remarkable genetic homogeneity was observed in larval and adult samples of A. typica despite their different geographical origin; interpopulation genetic distances were low, ranging from D Nei=0.004 (Eastern Mediterranean versus Somali) to D Nei=0.010 (Brazilian versus Somali). Accordingly, indirect estimates of gene flow gave a rather high average value of Nm = 6.00. Genetic divergence of A. typica was, on average, D Nei=1.12 from the members of the A. simplex complex (A. simplex s.s, A. pegreffii, A. simplex C) and D Nei=1.41 from A. ziphidarum, which all share Type I larvae; higher values were found from both A. physeteris (D Nei=2.77)
Similar content being viewed by others
References
Abril, E., Almor, P., Raga, J.A. & Duguy, R. (1986) Parasitism by Anisakis typica (Diesing, 1860) in the striped dolphin (Stenella coeruleoalba) of the North-East Atlantic. Bulletin de la Société Zoologique de France, 111, 131–133.
Andreade, A., Pinedo, M.C. & Pereira, J., Jr (1997) The gastrointestinal helminths of the Franciscana, Pontoporia Blainvillei, in southern Brazil. Annual Report of the International Whaling Commission 47.
Andrews, R.H. & Chilton, N.B. (1999) Multilocus enzyme electrophoresis: a valuable technique for providing answers to problems in parasite systematics. International Journal for Parasitology, 29, 213–253.
Aznar, F.J., Raga, J.A., Corcuera, J. & Monzon, F. (1995) Helminths as biological tags for franciscana (Pontoporia Blainvillei) (Cetacea: Pontoporidae) in Argentinian and Uruguayan waters. Mammalia, 59, 427–435.
Bagrov, A.A. (1982) On morphological variability of larvae of nematodes of the genus Anisakis (Nematoda, Anisakidae). Parazitologiya, 16, 469–475. (In Russian).
Baylis, H.A. (1929) Parasitic Nematoda and Acanthocephala collected in 1925-27. Discovery Reports, 1, 541–560.
Berland, B. (1961) Nematodes from some Norwegian marine fishes. Sarsia, 2, 1–50.
Beveridge, I., Chilton, N.B. & Andrews, R.H. (1995) Relationships within the Rugopharynx delta species complex (Nematoda: Strongyloidea) from Australian marsupials inferred from allozyme electrophoresis. Systematic Parasitology, 32, 149–156.
Brewer, G.J. & Sing, C.F. (1970) An introduction to isoenzyme techniques. New York & London: Academic Press, 186 pp.
Cannon, L.R.G. (1977) Some aspects of the biology of Peponocephala electra (Cetacea: Delphinidae). II. Parasites. Australian Journal of Marine and Freshwater Research, 28, 717–722.
Cavalli-Sforza, L.L. & Edwards, A.W.F. (1967) Phylogenetic analysis: models and estimation procedures. American Journal of Human Genetics, 19, 233–257.
Chilton, N.B., Beveridge I. & Andrews, R.H. (1997) An electrophoretic analysis of patterns of speciation in Cloacina clarkae, C. communis, C. petrogale and C. similis (Nematoda: Strongyloidea) from macropodid marsupials. International Journal for Parasitology, 27, 483–493.
Conti, J.A. & Frohlich, R.K. (1984) Gastrointestinal parasitism in pigmy killer whales. Proceedings of the Helminthological Society of Washington, 51, 364–365.
Crusz, H. (1946) Contributions to the helminthology of Ceylon. II. Notes on some parasitic nematodes, with a description of Anisakis tursiopis sp. nov. Ceylon Journal of Sciences, B, Zoology, 23, 57–66.
Davey, J.T. (1971) A revision of the genus Anisakis Dujardin, 1845 (Nematoda: Ascaridida). Journal of Helminthology, 45, 51–72.
Diesing, K.M. (1860) Revision der Nematoden. Akademie der Wissenschaften zu Wien, Sitzungsberichte, Mathematischnaturwissenchaftlische Klasse, 42, 595–763.
Dollfus, R. (1968) Nematodes des cetaces odontocetes (Globicephalus et Tursiops). Récoltes au large de la côte Mediterranéenne du Maroc par Herry Aloncl. Bulletin de l'Institut des Pêches Maritimes du Maroc, 16, 35–53.
Forrester, D.J. & Robertson, W.D. (1975) Helminths of rough-toothed dolphin, Steno bredanensis Lesson 1828, from Florida Waters. Journal of Parasitology, 61, 922.
Guttman, L.A. (1968) A general nonmetric technique for finding the smallest coordinate space for a configuration of points. Psycometrika, 33, 469–506.
Harris, H. (1966) Enzyme polymorphism in man. Proceedings of the Royal Society Series B, 164, 298–310.
Hillis, D.M., Moritz, C. & Mable, B.K. (1996) Molecular systematics. Sunderland, Mass.: Sinauer Associates Inc. Publishers, 655 pp.
Kagei, N., Oshima, T. & Takemura, A. (1967) Survey of Anisakis spp. (Anisakidae: Nematoda) in marine mammals of the coast of Japan. Japanese Journal of Parasitology, 16, 427–435.
Kagei, N., Tobayama, T. & Nagasaki, Y. (1976) On the helminthum of franciscana, Pontoporia blainvillei. Science Report of The Whales Researches Institute, 28, 161–166.
Mattiucci, S., Nascetti, G., Bullini, L., Orecchia, P. & Paggi, L (1986) Genetic structure of Anisakis physeteris and its differentiation from the Anisakis simplex complex (Ascaridida: Anisakidae). Parasitology, 93, 383–387.
Mattiucci, S., Nascetti, G., Cianchi, R., Paggi, L., Arduino, P., Margolis, L., Brattey, J., Webb, S.C., D'Amelio, S., Orecchia, P. & Bullini, L. (1997) Genetic and ecological data on the Anisakis simplex complex with evidence for a new species (Nematoda, Ascaridoidea, Anisakidae). Journal of Parasitology, 83, 401–416
Mattiucci, S., Paggi, L., Nascetti, G., Ishikura, H., Kikuchi, K., Sato, N., Cianchi, R. & Bullini, L. (1998) Allozyme and morphological identification of Anisakis, Contracaecum and Pseudoterranova from Japanese waters (Nematoda, Ascaridoidea). Systematic Parasitology, 40, 81–92.
Mattiucci, S., Paggi L., Nascetti G., Abollo E., Webb, S.C., Pascual., S., Cianchi, R. & Bullini, L. (2001) Genetic divergence and reproductive isolation between Anisakis brevispiculata and Anisakis physeteris (Nematoda: Anisakidae). International Journal for Parasitology, 31, 9–14.
Mignucci-Giannone, A.A., Hoberg, H.P., Siegel-Causey, D. & Williams, E.H. Jr (1998) Metazoan parasites and other symbionts of cetaceans in the Caribbean. Journal of Parasitology, 84, 939–946.
Nascetti, G., Paggi, L., Orecchia, P., Smith, J.W., Mattiucci, S. & Bullini L. (1986) Electrophoretic studies on the Anisakis simplex complex (Ascaridida: Anisakidae) from the Mediterranean and North East Atlantic. International Journal for Parasitology, 16, 633–640.
Nei, M. (1972) Genetic distance between populations. The American Naturalist, 106, 283–292.
Paggi, L., Nascetti, G., Webb, S.C., Mattiucci, S., Cianchi, R. & Bullini, L. (1998) A new species of Anisakis Dujardin, 1845 (Nematoda, Anisakidae) from beaked whales (Ziphiidae): allozyme and morphological evidence. Systematic Parasitology, 40, 161–174.
Praderi, R. (1984) Mortalidad de franciscana, Pontoporia Blainvillei, en pesquerias artesanales de tiburon de la costa Atlantica Uruguayana. Revista del Museo Argentino de Ciencias Naturales ‘Bernardino Rivadavia’ e Instituto Nacional de Investigation de las Ciencias Naturales, 13, 259–272.
Praderi, R. (1985). Incidental mortality of dolphins (Pontoporia Blainvillei) in Uruguay. National Geographic Society Research Report, 21, 395–403.
Poulik, M.D. (1957) Starch gel electrophoresis in a discontinuous system of buffers. Nature, 180, 1477.
Raga, J.A & Balbuena, J.A. (1987) Algunas caracteristicas zoogeograficas de los helminthos de los cetaceos en el Mediterraneo, con especial referencia a la helmithofauna del delfin listado. In: Sans-Coma, V., Mas-Coma, S. & Gsalbez, J. (Eds) Mamiferos y helminthos. Barcelona: Ketres Editores, pp. 195–201.
Rogers, J.S. (1972) Measures of genetic similarities and genetic distance. Studies in Genetics VII, University of Texas Publications, 7213, 145–153.
Richardson, B.J., Baverstock, P.R. & Adams, M. (1986) Allozyme electrophoresis. A handbook for animal systematics and population studies. Sydney: Academic Press, 410 pp.
Santos, C.P., Rohde, K., Ramos, R., Di Beneditto, A.P. & Capistrano, L. (1996) Helminths of cetaceans on the southeastern coast of Brazil. Journal of the Helminthological Society of Washington, 63, 149–152.
Selander, R.K, Smith, M.H., Yang, S.Y. & Gentry, J.B. (1971) Biochemical polymorphism and systematics in the genus Peromyscus. I. Variation of the old-field mouse (Peromyscus polionotus). Studies in Genetics VI, University of Texas Publications, 7103, 49–90.
Shipley, A.E. (1905) Notes on a collection of parasites belonging to the Museum of the University College, Dundee. Proceedings of the Cambridge Philosophical Society. Biological Sciences. London, 13, 95–102.
Smith, J.W. & Wootten, R. (1978) Anisakis and Anisakiasis. Advances in Parasitology, 16, 93–163.
Sokal, R.R. & Rholf, F.J. (1981) Biometry. 2nd Edition. New York: W.H. Freeman and Company, 859 pp.
Stiles, C.H. & Hassall, A. (1899) Internal parasites of the fur seal. In: The fur seals and fur seal islands of the North Pacific Ocean. Washington: Government Printing Office, Part III, pp. 99–107.
Swofford, D.L. & Selander, R.B. (1989) BYOSYS-1, a computer program for the analysis of allelic variation in population genetics and biochemical systematics, version 1.7. Champaign: Illinois Natural History Survey, 31 pp.
Wilkinson, L. & Leland, F.J. (1989) SYSTAT: The system for statistics. Evanson, Illinois: SYSTAT Inc.
Wright, S. (1943) Isolation by distance. Genetics, 28, 114–138.
Wright, S. (1951) The genetical structure of populations. Annals of Eugenics, 15, 323–354.
Wright, S. (1978) Evolution and the genetics of populations.Vol. 4. Variability within and among natural populations. Chicago, Illinois: The University of Chicago Press, 580 pp.
Zerbini, A.N. & Santos, M.C. (1997) First record of the pygmy killer whale Feresa attenuata (Gray, 1874) for the Brazilian coast. Aquatic Mammals, 23, 105–109.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Mattiucci, S., Paggi, L., Nascetti, G. et al. Genetic markers in the study of Anisakis typica (Diesing, 1860): larval identification and genetic relationships with other species of Anisakis Dujardin, 1845 (Nematoda: Anisakidae). Syst Parasitol 51, 159–170 (2002). https://doi.org/10.1023/A:1014554900808
Issue Date:
DOI: https://doi.org/10.1023/A:1014554900808