Hostname: page-component-78c5997874-94fs2 Total loading time: 0 Render date: 2024-11-10T12:47:53.323Z Has data issue: false hasContentIssue false
  • English
  • Français

Cross-fertilization as a reproductive strategy in a tissue flukes Didymosulcus katsuwonicola (Platyhelmintes: Didymozoidae) inferred by genetic analysis

Published online by Cambridge University Press:  03 July 2015

IVONA MLADINEO ,
MARINA TOMAŠ  and
RINO STANIĆ
IVONA MLADINEO*
Affiliation:
Institute of Oceanography & Fisheries, 21000 Split, Croatia
MARINA TOMAŠ
Affiliation:
Institute of Oceanography & Fisheries, 21000 Split, Croatia
RINO STANIĆ
Affiliation:
Sardina doo, Milna, Island of Brač, Croatia
*
*Corresponding author. Institute of Oceanography & Fisheries, 21000 Split, Croatia. E-mail: mladineo@izor.hr
Get access Rights & Permissions [Opens in a new window]

Summary

Mitochondrial DNA locus cytochrome oxidase I was used to asses intraspecific genetic diversity of a didymozoid species Didymosulcus katsuwonicola. Adult forms of this species live encapsulated in pairs in the gills of the reared Atlantic bluefin tuna (Thunnus thynnus). The life cycle of this food-borne parasites and its migration in the host tissues after releasing from the digestive tract to the definitive site in the gills are unknown. Our goal was to assess whether two encysted didymozoids share the same haplotype, indicative of a common maternal origin, as well as the extent of cross- in respect to self-fertilization strategy. Intraspecific comparison showed high haplotype diversity, while the presence of two matching haplotypes within a single cyst encompassed only 17% of sampled individuals. This infers that cross-fertilization between paired individuals within the cyst is more common mechanism than self-fertilization. Such hermaphroditic parasite's trait suggests the existence of intricate infection and reproduction mechanisms, presumably as an adaptation for successful fulfillment of their indirect life cycle through dissemination of genetically more diverse and consequently more fit offspring.

Keywords

Bluefin tunaDidymosulcus katsuwonicolaDigeneaThunnus thynnus
Type
Research Article
Information
Parasitology , Volume 142 , Issue 11 , September 2015 , pp. 1422 - 1429
Check for updates
Copyright
Copyright © Cambridge University Press 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Avise, J. C. (2000). Phylogeography: The History and Formation of Species. Harvard University Press, Cambridge, UK.Google Scholar
Bandelt, H. J., Forster, P. and Rohl, A. (1999). Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution 16, 37–48.Google Scholar
Basch, P. F. (1990). Why do schistosomes have separate sexes? Parasitology Today 6, 160–163.Google 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.Google Scholar
Bonett, R. M., Steffen, M. A., Trujano-Alvarez, A. L., Martin, S. D., Bursey, C. R. and McAllister, C. T. (2011). Distribution, abundance, and genetic diversity of Clinostomum spp. metacercariae (Trematoda: Digenea) in a modified Ozark stream system. Journal of Parasitology 97, 177–184.Google Scholar
Christen, M., Kurtz, J. and Milinski, M. (2002). Outcrossing increases infection success and competitive ability: experimental evidence from a hermaphrodite parasite. Evolution 56, 2243–2251.Google Scholar
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
Excoffier, L. and Lischer, H. E. L. (2010). Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular and Ecological Resources 10, 564–567.Google Scholar
Fu, Y. X. (1997). Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147, 915–925.Google Scholar
Galaktionov, K. V. and Dobrovolskij, A. A. (2010). The Biology and Evolution of Trematodes. Kluwer Academic Publishers, Dordrecht, The Netherlands.Google Scholar
Harpending, H. C. (1994). Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution. Human Biology 66, 591–600.Google Scholar
Huelsenbeck, J. P. and Ronquist, F. (2001). MrBayes: Bayesian inference of phylogeny. Bioinformatics 17, 754–755.Google Scholar
Jourdane, J., Imbert-Establet, D. and Tchuem Tchuenté, L. A. (1995). Parthenogenesis in Schistosomatidae. Parasitology Today 11, 427–430.Google 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.Google 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
Lester, R. J. G. (1980). Host-parasite relations in some didymozoid trematodes. Journal of Parasitology 66, 527–531.CrossRefGoogle Scholar
Li, M., Shi, S.-F., Brown, C. L. and Yang, T.-B. (2011). Phylogeographical pattern of Mazocraeoides gonialosae (Monogenea, Mazocraeidae) on the dotted gizzard shad, Konosirus punctatus, along the coast of China. International Journal for Parasitology 41, 1263–1272.CrossRefGoogle ScholarPubMed
Librado, P. and Rózas, J. (2009). DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 1451.Google Scholar
Maynard Smith, J. (1989). Evolutionary Genetics. Oxford University Press, Oxford, UK.Google Scholar
Mes, T. H. M. (2003). Demographic expansion of parasitic nematodes of livestock based on mitochondrial DNA regions that conflict with the infinite-sites mode. Molecular Ecology 12, 1555–1566.Google Scholar
Mladineo, I. (2006). Histopathology of five species of Didymocystis spp. (Digenea: Didymozoidae) in cage reared bluefin tuna (Thunnus thynnus thynnus). Veterinay Research Communications 30, 475–484.Google Scholar
Mladineo, I., Žilić, J. and Čanković, M. (2008). Health survey of bluefin tuna, Thunnus thynnus (Linnaeus, 1758), reared in Adriatic cages from 2006 to 2006. Journal of World Aquaculture Society 39, 281–289.CrossRefGoogle Scholar
Mladineo, I., Bott, N. J., Nowak, B. F. and Block, B. A. (2010). Multilocus phylogenetic analyses reveal that habitat selection drives the speciation of Didymozoidae (Digenea) parasitizing Pacific and Atlantic bluefin tunas. Parasitology 137, 1013–1025.CrossRefGoogle ScholarPubMed
Mladineo, I., Šegvić, T. and Petrić, M. (2011). Do captive conditions favor shedding of parasites in the reared Atlantic bluefin tuna (Thunnus thynnus)? Parasitology International 60, 25–33.Google Scholar
Nei, M. (1987). Molecular Evolutionary Genetics. Columbia University Press, New York, USA.CrossRefGoogle Scholar
Posada, D. (2008). jModelTest: phylogenetic model averaging. Molecular Biology and Evolution 25, 1253–1256.CrossRefGoogle ScholarPubMed
Posada, D. and Crandall, K. A. (1998). Modeltest: testing the model of DNA substitution. Bioinformatics 14, 817–818.Google Scholar
Poulin, R. (1998). Evolutionary Ecology of Parasites: From Individuals to Communities. Chapman & Hill, London, UK.Google Scholar
Pozdnyakov, S. E. (1996). Trematode Suborder Didymozoata. Tikhookeanskii Naucho-Issledovatel'skii Rybokhozyaistvennyi Tsentr, Vladivostok, Russia. In Russian.Google Scholar
Pozdnyakov, S. E. and Gibson, D. I. (2008). Family Didymozoidae Monticelli, 1888. In Keys to the Trematoda, Vol. 3 (ed. Bray, R., Gibson, D. and Jones, A.), pp. 631–734. CABI Publishing, Wallingford, UK.Google Scholar
Rogers, A. R. and Harpending, H. (1992). Population growth makes waves in the distribution of pairwise genetic differences. Molecular Biology and Evolution 9, 552–569.Google Scholar
Schneider, S. and Excoffier, L. (1999). Estimation of past demographic parameters from the distribution of pairwise distances when the mutation rates wary among sites: application to human mitochondrial DNA. Genetics 152, 1079–1089.Google Scholar
Tajima, F. (1983). Evolutionary relationship of DNA sequences in finite populations. Genetics 105, 437–467.Google Scholar
Tajima, F. (1989). Statistical-method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123, 585–595.Google Scholar
Tamura, K. and Nei, M. (1993). Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology and Evolution 10, 512–526.Google Scholar
Tamura, K., Dudley, J., Nei, M. and Kumar, S. (2007). MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24, 1596–1599.Google Scholar
Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, J. and Higgins, D. G. (1997). The Clustal X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acid Research 25, 4876–4882.Google Scholar
Timon-David, J. (1937). Les kystes à Didymocystis weldi du thon. Étude anatomo-pathologique. Annales Parasitologie Humaine et Comparative 15, 520–523. In French.Google Scholar
Trouvé, S., Renaud, F., Durand, P. and Jourdane, J. (1996). Selfing and outcrossing in a parasitic hermaphrodite helminth (Trematoda, Echinostomatidae). Heredity 77, 1–8.CrossRefGoogle Scholar
Supplementary material: File

Mladineo supplementary material

Tables S1 and S2

Download Mladineo supplementary material(File)
File 514.1 KB