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Anisakis nascettii n. sp. (Nematoda: Anisakidae) from beaked whales of the southern hemisphere: morphological description, genetic relationships between congeners and ecological data

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Abstract

A new anisakid nematode, Anisakis nascettii n. sp., is described from beaked whales Mesoplodon spp. off the coast of New Zealand and South Africa. Morphological and molecular (allozymes and mtDNA cox2 sequence) data were used for diagnostic and identification purposes. Among the 19 allozymes studied, 10 were found to be unique and characteristic for A. nascettii n. sp. Analysis of allozymes demonstrated reproductive isolation from A. ziphidarum Paggi, Nascetti, Webb, Mattiucci, Cianchi & Bullini, 1998 and mtDNA cox2 sequences depict this Anisakis species as a distinct and unique entity. Key morphological diagnostic traits for A. nascettii with respect to the genetically closely related species A. ziphidarum include: spicule length, the spicule/body length ratio, the arrangement of the caudal papillae and the shape of the plectanes of the adult males. Genetic data confirmed that Anisakis sp. A of Pontes et al. (2005), which was partly described by Iglesias et al. (2008), and Anisakis sp. of Valentini et al. (2006) are conspecific with A. nascettii. Both molecular and morphological data indicate that the new species belongs to the ‘ziphidarum-group’; however, it is genetically very distinct from A. ziphidarum (D Nei  = 0.69, K2P = 0.09), as well as from all of the previously genetically characterised Anisakis spp. All tree topologies inferred by different methods (MP, NJ and Bayesian) support the finding that A. nascettii n. sp. and A. ziphidarum are sister-species. It is also confirmed that A. nascettii n. sp. is, at the adult stage, a parasite of beaked whales of the genus Mesoplodon, whereas, as a larva, it has been identified from the squid Moroteuthis ingens Smith. Furthermore, Mesoplodon bowdoini Andrews represents a new host record for A. ziphidarum. The parallelism between the clade formed by these two anisakine taxa, i.e. A. ziphidarum and A. nascettii, and that formed by their definitive hosts further supports the hypothesis of host–parasite co-evolutionary relationships, as previously suggested for Anisakis spp. and their cetacean hosts.

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References

  • Arnason, U., Gullberg, A., & Janke, A. (2004). Mitogenomic analyses provide new insights into cetacean origin and evolution. Gene, 333, 27–34.

    Article  PubMed  CAS  Google Scholar 

  • Berland, B. (1961). Nematodes from some Norwegian marine fishes. Sarsia, 2, 1–50.

    Google Scholar 

  • Cavalli-Sforza, L. L., & Edwards, A. W. F. (1967). Phylogenetic analysis: Models and estimation procedures. American Journal of Human Genetics, 19, 233–257.

    PubMed  CAS  Google Scholar 

  • D’Amelio, S., Mathiopoulos, K. D., Santos, C. P., Pugachev, O. N., Webb, S. C., Picanço, M., et al. (2000). Genetic markers in ribosomal DNA for the identification of members of the genus Anisakis (Nematoda: Ascaridoidea) defined by polymerase-chain-reaction-based restriction fragment length polymorphism. International Journal for Parasitology, 30, 223–226.

    Article  PubMed  Google Scholar 

  • Dalebout, M. L., van Helden, A., van Waerebeek, A. K., & Baker, C. S. (1998). Molecular genetic identification of southern hemisphere beaked whales (Cetacea: Ziphiidae). Molecular Ecology, 7, 687–694.

    Google Scholar 

  • Davey, J. T. (1971). A revision of the genus Anisakis Dujardin, 1845 (Nematoda: Ascaridata). Journal of Helminthology, 45, 51–72.

    Article  Google Scholar 

  • Fagerholm, H. P. (1989). Intra-specific variability of the morphology in a single population of the seal parasite Contracaecum osculatum (Rudolphi) (Nematoda, Ascaridoidea), with a redescription of the species. Zoologica Scripta, 18, 33–41.

    Article  Google Scholar 

  • Fagerholm, H. P. (1991). Systematic implications of male caudal morphology in Ascaridoid nematode parasites. Systematic Parasitology, 19, 215–228.

    Article  Google Scholar 

  • Farjallah, S., Busi, M., Mahjoub, H. O., Slimane, B. B., Paggi, L., Said, K., et al. (2008a). Molecular characterization of larval anisakid nematodes from marine fishes off the Moroccan and Mauritanian coasts. Parasitology International, 57, 430–436.

    Article  PubMed  CAS  Google Scholar 

  • Farjallah, S., Slimane, B. B., Busi, M., Paggi, L., Amor, N., Blel, H., et al. (2008b). Occurrence and molecular identification of Anisakis spp. from the North African coasts of Mediterranean Sea. Parasitology Research, 102, 371–379.

    Article  PubMed  Google Scholar 

  • Felsenstein, J. (1985). Confidence limits on phylogenies: An approach using the bootstrap. Evolution, 39, 783–791.

    Article  Google Scholar 

  • Felsenstein, J. (1995). PHYLIP: Phylogenetic Inference Package, version 3.57c. Department of Genetics, University of Washington, Seattle.

  • Hall, T. A. (1999). BioEdit: A user-friendly biological sequence alignment and analysis program for Windows 95/98/NT. Nucleic Acid Symposium Series, 41, 95–98.

    CAS  Google Scholar 

  • Hills, D. M., & Bull, J. J. (1993). An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Systematic Biology, 42, 182–192.

    Google Scholar 

  • Huelsenbeck, J. P., & Ronquist, F. (2001). MrBayes: Bayesian inference of phylogeny. Bioinformatics, 17, 754–755.

    Article  PubMed  CAS  Google Scholar 

  • Iglesias, R., D’Amelio, S., Ingrosso, S., Farjallah, S., Martínez-Cedeira, J. A., & García-Estévez, J. M. (2008). Molecular and morphological evidence for the occurrence of Anisakis sp. A (Nematoda, Anisakidae) in the Blainville’s beaked whale Mesoplodon densirostris. Journal of Helminthology, 82, 305–308.

    Article  PubMed  CAS  Google Scholar 

  • Larget, B., & Simon, L. D. (1999). Markov chain Monte Carlo algorithms for the Bayesian analysis of phylogenetic trees. Molecular Biology and Evolution, 16, 750–759.

    CAS  Google Scholar 

  • Leatherwood, S., & Reeves, R. (1983). The Sierra Club handbook of whales and dolphins. San Francisco: Sierra Club Books, 320 pp.

  • Mattiucci, S., Abaunza, P., Damiano, S., Garcia, A., Santos, M. N., & Nascetti, G. (2007). Distribution of Anisakis larvae identified by genetic markers and their use for stock characterization of demersal and pelagic fish from European waters: An update. Journal of Helminthology, 81, 117–127.

    Article  PubMed  CAS  Google Scholar 

  • Mattiucci, S., Farina, V., Campbell, N., Mackenzie, K., Ramos, P., Pinto, A. L., et al. (2008a). Anisakis spp. larvae (Nematoda: Anisakidae) from Atlantic horse mackerel: Their genetic identification and use as biological tags for host stock identification. Fisheries Research, 89, 146–151.

    Article  Google Scholar 

  • Mattiucci, S., & Nascetti, G. (2006). Molecular systematics, phylogeny and ecology of anisakid nematodes of the genus Anisakis Dujardin, 1845: an update. Parasite, 13, 99–113.

    PubMed  CAS  Google Scholar 

  • Mattiucci, S., & Nascetti, G. (2008). Advances and trends in the molecular systematics of anisakid nematodes, with implications for their evolutionary ecology and host–parasite co-evolutionary processes. Advances in Parasitology, 66, 47–148.

    Article  PubMed  Google Scholar 

  • Mattiucci, S., Nascetti, G., Cianchi, R., Paggi, L., Arduino, P., Margolis, L., et al. (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.

    PubMed  CAS  Google Scholar 

  • Mattiucci, S., Nascetti, G., Dailey, M., Webb, S. C., Barros, N., Cianchi, R., et al. (2005). Evidence for a new species of Anisakis Dujardin, 1845: Morphological description and genetic relationships between congeners (Nematoda: Anisakidae). Systematic Parasitology, 61, 157–171.

    Article  PubMed  Google Scholar 

  • Mattiucci, S., Paggi, L., Nascetti, G., Abollo, E., Webb, S. C., Pascual, S., et al. (2001). Genetic divergence and reproductive isolation between Anisakis brevispiculata and Anisakis physeteris (Nematoda: Anisakidae). International Journal for Parasitology, 31, 9–14.

    Article  PubMed  CAS  Google Scholar 

  • Mattiucci, S., Paggi, L., Nascetti, G., Ishikura, H., Kikuchi, K., Sato, N., et al. (1998). Allozyme and morphological identification of Anisakis, Contracaecum and Pseudoterranova from Japanese waters (Nematoda: Ascaridoidea). Systematic Parasitology, 40, 81–92.

    Article  Google Scholar 

  • Mattiucci, S., Paggi, L., Nascetti, G., Portes Santos, C., Costa, G., Di Beneditto, A. P., et al. (2002). Genetic markers in the study of Anisakis typica (Diesing, 1860): larval identification and genetic relationships with other species of Anisakis Dujardin, 1845 (Nematoda: Anisakidae). Systematic Parasitology, 51, 159–170.

  • Mattiucci, S., Paoletti, M., Webb, S. C., Sardella, N., Timi, J. T., Berland, B., et al. (2008a). Genetic relationships among species of Contracaecum Railliet & Henry, 1912 and Phocascaris Höst, 1932 (Nematoda: Anisakidae) from pinnipeds inferred from mitochondrial cox2 sequences, and congruence with allozyme data. Parasite, 15, 408–419.

    PubMed  CAS  Google Scholar 

  • Mattiucci, S., Paoletti, M., Olivero-Verbel, J., Baldiris, R., Arroyo-Salgado, B., Garbin, L., et al. (2008b). Contracaecum bioccai n. sp. from the brown pelican Pelecanus occidentalis (L.) in Colombia (Nematoda: Anisakidae): Morphology, molecular evidence and its genetic relationship with congeners from fish-eating birds. Systematic Parasitology, 69, 101–121.

    Article  PubMed  Google Scholar 

  • Nadler, S. A., Carreno, R. A., Mejía-Madrid, H., Ullberg, J., Pagan, C., Houston, R., et al. (2007). Molecular phylogeny of clade III nematodes reveals multiple origins of tissue parasitism. Parasitology, 134, 1421–1442.

    Article  PubMed  CAS  Google Scholar 

  • Nadler, S. A., D’Amelio, S., Dailey, M. D., Paggi, L., Siu, S., & Sakanari, J. A. (2005). Molecular phylogenetics and diagnosis of Anisakis, Pseudoterranova, and Contracaecum from northern Pacific marine mammals. Journal of Parasitology, 91, 1413–1429.

    Article  PubMed  CAS  Google Scholar 

  • Nadler, S. A., & Hudspeth, D. S. S. (2000). Phylogeny of the Ascaridoidea (Nematoda: Ascaridida) based on three genes and morphology: Hypotheses of structural and sequence evolution. Journal of Parasitology, 86, 380–393.

    Article  PubMed  CAS  Google Scholar 

  • Nascetti, G., Paggi, L., Orecchia, P., Smith, J. W., Mattiucci, S., & Bullini, L. (1986). Electrophoretic studies on Anisakis simplex complex (Ascaridida: Anisakidae) from the Mediterranean and North East Atlantic. International Journal for Parasitology, 16, 633–640.

    Article  PubMed  CAS  Google Scholar 

  • Nei, M. (1972). Genetic distance between populations. American Naturalist, 106, 283–292.

    Article  Google Scholar 

  • Nikaido, M., Matsuno, F., Hamilton, H., Brownell, R. L., Jr., Cao, Y., Wang, D., et al. (2001). Retroposon analysis of major cetacean lineages: The monophyly of toothed whales and the paraphyly of river dolphins. Proceedings of the National Academy of Sciences, 98, 7384–7389.

    Article  CAS  Google Scholar 

  • Paggi, L., Mattiucci, S., Gibson, D. I., Berland, B., Nascetti, G., Cianchi, R., et al. (2000). Pseudoterranova decipiens species A and B (Nematoda: Ascaridoidea): Nomenclatural designation, morphological diagnostic characters and genetic markers. Systematic Parasitology, 45, 185–197.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Pontes, T., D’Amelio, S., Costa, G., & Paggi, L. (2005). Molecular characterization of larval anisakid nematodes from marine fishes of Madeira by a PCR-based approach, with evidence for a new species. Journal of Parasitology, 91, 1430–1434.

    Article  PubMed  CAS  Google Scholar 

  • Posada, D., & Buckley, T. R. (2004). Model selection and model averaging in phylogenetics: Advantages of the AIC and Bayesian approaches over likelihood ratio tests. Systematic Biology, 53, 793–808.

    Article  PubMed  Google Scholar 

  • Posada, D., & Crandall, K. A. (1998). Modeltest: Testing the model of DNA substitution. Bioinformatics, 1, 817–818.

    Article  Google Scholar 

  • Quiazon, K. M. A., Yoshinaga, T., Ogawa, K., & Yukami, R. (2008). Morphological differences between larvae and in vitro-cultured adults of Anisakis simplex (sensu stricto) and Anisakis pegreffii (Nematoda: Anisakidae). Parasitology International, 57, 483–489.

    Article  PubMed  Google Scholar 

  • Reeder, T. W. (2003). A phylogeny of the Australian Sphenomorphus group (Scincidae: Squamata) and the phylogenetic placement of the crocodile skinks (Tribolonotus): Bayesian approaches to assessing congruence and obtaining confidence in maximum likelihood inferred relationships. Molecular Phylogenetics and Evolution, 27, 384–397.

    Article  PubMed  CAS  Google Scholar 

  • Ross, G. J. B. (1984). The smaller cetaceans of the south east coast of southern Africa. Annals of the Cape Provincial Museums (Natural History), 15, 173–410.

    Google Scholar 

  • Santos, M. B., Pierce, G. J., Herman, J., López, A., Guerra, A., Mente, E., et al. (2001). Feeding ecology of Cuvier’s beaked whale (Ziphius cavirostris): A review with new information on the diet of this species. Journal of the Marine Biological Association of the United Kingdom, 81, 687–694.

    Google Scholar 

  • Saraiva, A., Faranda, A., Damiano, S., Hermida, M., Santos, M. J., Ventura, C. H., et al. (2007). Six species of Anisakis (Nematoda: Anisakidae) parasites of the black scabbardfish, Aphanopus carbo from NE Atlantic waters: Genetic markers and fish biology. Parassitologia, 49, 229.

    Google Scholar 

  • Swofford, D. L. (2003). PAUP*. Phylogenetic analysis using parsimony (*and Other Methods). Sunderland, MA: Sinauer Associates.

    Google Scholar 

  • Swofford, D. L., & Selander, R. B. A. (1997). Biosys2. A computer program for the analysis of allelic variation genetics. Urbana, IL: University of Illinois.

    Google Scholar 

  • Tamura, K., Dudley, J., Nei, M., & Kumar, S. (2007). MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Molecular Biology and Evolution, 24, 1596–1599.

    Article  PubMed  CAS  Google Scholar 

  • Thompson, J. D., Higgins, D. G., & Gibson, T. J. (1994). CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weigh matrix choice. Nucleic Acids Research, 22, 4673–4680.

    Article  PubMed  CAS  Google Scholar 

  • Umehara, A., Kawakami, Y., Araki, J., & Uchida, A. (2007). Molecular identification of the etiological agent of the human anisakiasis in Japan. Parasitology International, 56, 211–215.

    Article  PubMed  CAS  Google Scholar 

  • Umehara, A., Kawakami, Y., Araki, J., & Uchida, A. (2008). Multiplex PCR for the identification of Anisakis simplex sensu stricto, Anisakis pegreffii and the other anisakid nematodes. Parasitology International, 57, 49–53.

    Article  PubMed  CAS  Google Scholar 

  • Valentini, A., Mattiucci, S., Bondanelli, P., Webb, S. C., Mignucci-Giannone, A., Colom-Llavina, M. M., et al. (2006). Genetic relationships among Anisakis species (Nematoda: Anisakidae) inferred from mitochondrial cox-2 sequences, and comparison with allozyme data. Journal of Parasitology, 92, 156–166.

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

The authors are very grateful to Mr T. Leung (Otago University, New Zealand), Mr Mike Morrissey (Department of Conservation, Kaikoura, New Zealand) and Dr Peter Best (South African Museum, Cape Town, South Africa) for providing samples used in this study. We wish to thank two anonymous referees, whose remarks and suggestions were useful in improving the manuscript. The research was partly supported by grants from the I Faculty of Medicine of the ‘Sapienza-University of Rome’.

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Mattiucci, S., Paoletti, M. & Webb, S.C. Anisakis nascettii n. sp. (Nematoda: Anisakidae) from beaked whales of the southern hemisphere: morphological description, genetic relationships between congeners and ecological data. Syst Parasitol 74, 199–217 (2009). https://doi.org/10.1007/s11230-009-9212-8

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