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Multilocus phylogenetic analyses reveal that habitat selection drives the speciation of Didymozoidae (Digenea) parasitizing Pacific and Atlantic bluefin tunas

Published online by Cambridge University Press:  23 December 2009

I. MLADINEO ,
N. J. BOTT ,
B. F. NOWAK  and
B. A. BLOCK
I. MLADINEO*
Affiliation:
Hopkins Marine Station, Stanford University, 120 Oceanview Blvd, Pacific Grove 93950 CA, USA
N. J. BOTT
Affiliation:
Aquatic Sciences, South Australian Research and Development Institute, PO Box 120, Henley Beach, South Australia 5022, Australia
B. F. NOWAK
Affiliation:
National Center for Marine Conservation and Resource Sustainability, AMC, University of Tasmania, Locked Bag 1370, Launceston, Tasmania 7250, Australia
B. A. BLOCK
Affiliation:
Hopkins Marine Station, Stanford University, 120 Oceanview Blvd, Pacific Grove 93950 CA, USA
*
*Corresponding author: Institute of Oceanography & Fisheries, Laboratory of Aquaculture, 21000 Split, Croatia. Tel: +38521408047. Fax: +38521358650. E-mail: mladineo@izor.hr
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Summary

Parasite communities of wild and reared bluefin tuna display remarkable diversity. Among these, the most prevalent and abundant are the Didymozoidae (Monticelli, 1888) (Trematoda, Digenea), considered one of the most taxonomically complex digenean families. The aim of this study was to evaluate phylogenetic structure of Didymozoidae occurring in Pacific (Thunnus orientalis) and Atlantic bluefin tuna (T. thynnus) in order to increase our knowledge of didymozoid zoogeography and identify species that could successfully be employed as biological tags for stock assessment studies. For the present analyses we used 2 nuclear ribosomal DNA loci, part of the 28S gene and the second internal transcribed spacer (ITS-2) as well as a portion of the mitochondrial cytochrome c oxidase subunit 1 gene (cox1). In most parasitic groups, morphology is the primary factor in the structuring of phylogenetic relationships. In rare examples, however, habitat has been suggested as a primary factor affecting parasite evolution. During their evolution, didymozoids have spread and inhabited a remarkable number of different sites in their hosts, colonizing exterior as well as strictly interior niches. Our data suggest that habitat selection has been the leading force in shaping didymozoid phylogenetic relationships. For 2 didymozoid species (D. wedli and D. palati), cox1 sequences indicate intraspecific differences between Mexican and Adriatic populations.

Keywords

DidymozoidaephylogenyThunnus orientalisThunnus thynnus
Type
Research Article
Information
Parasitology , Volume 137 , Issue 6 , May 2010 , pp. 1013 - 1025
Copyright
Copyright © Cambridge University Press 2009

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References

REFERENCES

Aiken, H. M., Bott, N. J., Mladineo, I., Montero, F. E., Nowak, B. F. and Hayward, C. J. (2007). Molecular evidence for cosmopolitan distribution of platyhelminth parasites of tunas (Thunnus spp.). Fish & Fisheries 8, 167–180.CrossRefGoogle Scholar
Anderson, G. R. and Barker, S. C. (1993). Species differentiation in the Didymozoidae (Digenea): restriction fragment length differences in internal transcribed spacer and 5.8S ribosomal DNA. International Journal for Parasitology 23, 133–136.CrossRefGoogle ScholarPubMed
Blair, D., Bray, R. A. and Barker, S. C. (1998). Molecules and morphology in phylogenetic studies of the Hemiuroidea (Digenea: Trematoda: Platyhelminthes). Molecular Phylogenetics and Evolution 9, 15–25.CrossRefGoogle ScholarPubMed
Block, B. A., Keen, J. E., Castillo, P., Dewar, H., Freund, E. V., Marcinek, D. J., Brill, R. W. and Farwell, C. (1997). Environmental preference of yellowfin tuna (Thunnus albacares) at the northern extent of its range. Marine Biology 130, 119–132.CrossRefGoogle Scholar
Block, B. A. and Stevens, E. D. (2001). Tunas: Physiology, Ecology and Evolution (Fish physiology). Academic Press, San Diego, CA, USA.Google Scholar
Block, B. A., Teo, S. L. H., Walli, A., Boustany, A., Stokesbury, M. J. W., Farwell, C. J., Weng, K. C., Dewar, H. and Williams, T. D. (2005). Electronic tagging and population structure of Atlantic bluefin tuna. Nature, London 28, 1121–1127.CrossRefGoogle Scholar
Blouin, M. S., Yowell, C. A., Courtney, C. H. and Dame, J. B. (1995). Host movement and the genetic-structure of populations of parasitic nematodes. Genetics 141, 1007–1014.CrossRefGoogle ScholarPubMed
Brusca, R. C. (1981). A monography on the Isopoda, Cymothoidae (Crustacea) of the Eastern Pacific. Zoological Journal of Linnean Society 73, 117–199.CrossRefGoogle Scholar
Chambers, C. B. and Cribb, T. H. (2006). Phylogeny, evolution and biogeography of the Quadrifoliovariinae Yamaguti, 1965 (Digenea: Lecithasteridae). Systematic Parasitology 63, 59–80.CrossRefGoogle ScholarPubMed
Cressey, R. and Cressey, H. B. (1980). Parasitic copepods of mackerel and tuna-like fishes (Scombridae) of the world. Smithsonian Contributions to Zoology 311, 1–186.Google Scholar
Cribb, T. H., Bray, R. A., Wright, T. and Pichelin, S. (2002). The trematodes of groupers (Serranidae: Epinephelinae): knowledge, nature and evolution. Parasitology 124 (Suppl.) S23–S42.CrossRefGoogle ScholarPubMed
Di Maio, A. and Mladineo, I. (2008). Ultrastructure of Didymocystis semiglobularis (Didymozoidae, Digenea) cysts in the gills of Pacific bluefin tuna (Thunnus orientalis). Parasitology Research 103, 641–647.CrossRefGoogle ScholarPubMed
Fromentin, J.-M. and Powers, J. E. (2005). Atlantic bluefin tuna: population dynamic, ecology, fisheries and management. Fish & Fisheries 5, 281–306.CrossRefGoogle Scholar
Hills, D. M. and Bull, J. J. (1993). An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Systematic Biology 42, 182–192.CrossRefGoogle Scholar
Huelsenbeck, J. P. and Ronquist, F. (2001). MrBayes: Bayesian inference of phylogeny. Bioinformatics 17, 754–755.CrossRefGoogle Scholar
Holt, R. and Boulinier, T. (2005). Ecosystems and parasitism: the spatial dimension. In Parasitism & Ecology (ed. Thomas, F., Renaud, F. and Guégan, J.-F.), pp. 68–84. Oxford University Press, Oxford, UK.Google Scholar
Huyse, T., Poulin, R. and Théron, A. (2005). Speciation in parasites: a population genetics approach. Trends in Parasitology 21, 469–475.CrossRefGoogle ScholarPubMed
Ishii, N. (1935). Studies on the family Didymozooidae (Monticelli 1888). Japanese Journal of Zoology 6, 279–335.Google Scholar
Jones, C. M., Miller, T. L., Grutter, A. S. and Cribb, T. H. (2008). Notatory-stage cymothoid isopods: description, molecular identification and evolution of attachment. International Journal for Parasitology 38, 477–491.CrossRefGoogle ScholarPubMed
Kaci-Chaouch, T., Verneau, O. and Desdevises, Y. (2008). Host specificity is linked to intraspecific variability in the genus Lamellodiscus (Monogenea). Parasitology 135, 1–10.CrossRefGoogle ScholarPubMed
Ketmaier, V., Joyce, D. A., Horton, T. and Mariani, S. (2008). A molecular phylogenetic framework for the evolution of parasitic strategies in cymothoid isopods (Crustacea). Journal of Zoological Systematics and Evolutionary Research 46, 19–23.Google Scholar
Kitagawa, T., Boustany, A. M., Farwell, C. J., Williams, T. D., Castleton, M. R., Block, B. A. (2007). Horizontal and vertical movements of juvenile bluefin tuna (Thunnus orientalis) in relation to seasons and oceanographic conditions in the eastern Pacific Ocean. Fisheries and Oceanography 16, 409–421.CrossRefGoogle Scholar
Larget, B. and Simon, D. L. (1999). Markov chain Monte Carlo algorithms for the Bayesian analysis of phylogenetic trees. Molecular Biology and Evolution 16, 750–759.CrossRefGoogle Scholar
Lester, R. G. J. and Newman, L. J. (1986). First rediae and cercariae to be described from heteropods. Journal of Parasitology 72, 195–197.CrossRefGoogle Scholar
Lo, C. M., Morgan, J. A. T., Galzin, R. and Cribb, T. H. (2001). Identical digeneans in coral reef fishes from French Polynesia and the Great Barrier Reef (Australia) demonstrated by morphology and molecules. International Journal for Parasitology 31, 1573–1578.CrossRefGoogle ScholarPubMed
Mattiucci, S., Paoletti, M., Damiano, S. and Nascetti, G. (2007). Molecular detection of sibling species in anisakid nematodes. Parassitologia 49, 147–153.Google ScholarPubMed
Mattiucci, S. and 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.CrossRefGoogle ScholarPubMed
MacKenzie, K. (2002). Parasites as biological tags in population studies of marine organisms: an update. Parasitology 124, S153–S163.CrossRefGoogle ScholarPubMed
MacKenzie, K. (2005). Zoogeography, parasites as biological tags. In Marine Parasitology (ed. Rohde, K.),pp. 351–355. CABI Publishing, Wallingford, UK.Google Scholar
Marcinek, D. J., Blackwell, S. B., Dewar, H., Freund, E. V., Farwell, C., Dau, D., Seitz, A. C. and Block, B. A. (2001). Depth and muscle temperature of Pacific bluefin tuna examined with acoustic pop-up satellite archival tags. Marine Biology 138, 869–885.CrossRefGoogle Scholar
Miura, O., Torchin, M. E., Kuris, A. M., Hechinger, R. F. and Chiba, S. (2006). Introduced cryptic species of parasites exhibit different invasion pathways. Proceedings of the National Academy of Sciences, USA 103, 19818–19823.CrossRefGoogle ScholarPubMed
Miyake, P. M., De la Serna, J. M., Di Natale, A., Farrugia, A., Katavić, I., Miyabe, N. and Tičina, V. (2003). General review of bluefin tuna farming in the Mediterranean area. Collective Volume of Scientific Papers ICCAT 55, 114–124.Google Scholar
Mladineo, I. and Tudor, M. (2004). Digenea of Adriatic cage-reared bluefin tuna Thunnus thynnus thynnus. Bulletin of the European Association of Fish Pathologists 24, 114–153.Google Scholar
Mladineo, I. (2006). Histopathology of five species of Didymocystis spp. (Digenea: Didymozoidae) in cage reared bluefin tuna (Thunnus thynnus thynnus). Veterinary Research Communications 30, 475–484.CrossRefGoogle ScholarPubMed
Mladineo, I., Žilić, J. and Čanković, M. (2008). Health survey of bluefin tuna, Thunnus thynnus (Linnaeus, 1758), reared in Adriatic cages from 2003 to 2006. Journal of the World Aquaculture Society 39, 281–289.CrossRefGoogle Scholar
Munday, B. L., Sawada, Y., Cribb, T. and Hayward, C. J. (2003). Diseases of tunas, Thunnus spp. Journal of Fish Diseases 26, 187–206.CrossRefGoogle ScholarPubMed
Nadler, S. A. (1995). Microevolution and the genetic structure of parasite populations. Journal of Parasitology 81, 395–403.CrossRefGoogle ScholarPubMed
Nikolaeva, V. M. (1985). Trematodes – Didymozoidae fauna, distribution and biology. In NOAA Technical Report NMFS 25 Parasitology and Pathology of Marine Organisms of the World Ocean (ed. Hargis, W. J.), pp. 67–72. Springfield, VA, USA.Google Scholar
Nowak, B. F., Mladineo, I., Aiken, H., Bott, N. J. and Hayward, C. J. (2006). Results of health surveys of two species of farmed tuna: southern bluefin tuna (Thunnus maccoyii) in Australia and northern bluefin tuna (Thunnus thynnus) in the Mediterranean. Bulletin of the European Association of Fish Pathologists 26, 38–42.Google Scholar
Olson, P. D. and Tkach, V. V. (2005). Advances and trends in the molecular systematics of the parasitic platyhelminths. Advances in Parasitology 60, 165–243.CrossRefGoogle Scholar
Palm, H. W., Waeschenbach, A. and Littlewood, D. T. J. (2007). Genetic diversity in the trypanorhynch cestode Tentacularia coryphaene Bosc, 1797: evidence for a cosmopolitan distribution and low host specificity in the teleost intermediate host. Parasitology Research 101, 153–159.CrossRefGoogle ScholarPubMed
Poulin, R. (1998). Evolutionary Ecology of Parasites. From Individuals to Communities. Chapman and Hall, London, UK.Google Scholar
Pozdnyakov, S. E. and Gibson, D. I. (2008). Family Didymozoidae Monticelli, 1888. In Keys to the Trematoda, Vol. 3 (ed. Bray, R. A., Gibson, D. I. and Jones, A.),pp. 631–734. CABI and Natural History Museum, London, UK.CrossRefGoogle Scholar
Rannala, B. and Michalakis, Y. (2002). Population genetics and cospeciation. In Tangled Trees: Phylogenesis, Cospeciation and Coevolution (ed. Page, R. D. M.),pp. 120–143. University of Chicago Press, Chicago, IL, USA.Google Scholar
Rohde, K. (1991). Intra- and interspecific interactions in low density populations in resource-rich habitats. Oikos 60, 91–104.CrossRefGoogle Scholar
Valentini, A., Mattiucci, S., Bondanelli, P., Webb, S. C., Mignucci-Giannone, A. A., Colom-Llavina, M. M. and Nascetti, G. (2006). Genetic relationships among Anisakis species (Nematoda: Anisakidae) inferred from mitochondrial cox2 sequences, and comparison with allozyme data. Journal of Parasitology 92, 156–166.CrossRefGoogle ScholarPubMed
Vilas, R., Criscione, C. D. and Blouin, M. S. (2005). A comparison between mitochondrial DNA and the ribosomal internal transcribed regions in prospecting for cryptic species of platyhelminth parasites. Parasitology 131, 839–846.CrossRefGoogle ScholarPubMed
Vossbrinck, C. R. and Debrunner-Vossbrick, B. A. (2005). Molecular phylogeny of the Microsporidia: ecological, ultrastructural and taxonomic considerations. Folia Parasitologica 52, 131–142.CrossRefGoogle ScholarPubMed
Yamaguti, S. (1958). Systema Helminthum. Vol. I. The Digenetic Trematodes of Vertebrates – Part I. Interscience Publishing, Inc., New York, USA.Google Scholar
Yamaguti, S. (1970). Digenetic Trematodes of Hawaiian Fishes. Keigaku Publishing Co. Tokyo, Japan.Google Scholar