Hostname: page-component-76fb5796d-skm99 Total loading time: 0 Render date: 2024-04-25T12:32:37.085Z Has data issue: false hasContentIssue false
  • English
  • Français

Cryptic species of Didymobothrium rudolphii (Cestoda: Spathebothriidea) from the sand sole, Solea lascaris, off the Portuguese coast, with an analysis of their molecules, morphology, ultrastructure and phylogeny

Published online by Cambridge University Press:  28 February 2007

J. F. MARQUES ,
M. J. SANTOS ,
D. I. GIBSON ,
H. N. CABRAL  and
P. D. OLSON
J. F. MARQUES*
Affiliation:
Universidade de Lisboa, Faculdade de Ciências, Instituto de Oceanografia, Campo Grande, 1749-016 Lisboa, Portugal
M. J. SANTOS
Affiliation:
Universidade do Porto, Faculdade de Ciências, Departamento de Zoologia e Antropologia, Praça Gomes Teixeira, 4099-002 Porto and CIMAR/CIIMAR – Centro Interdisciplinar de Investigação Marinha e Ambiental, Rua dos Bragas, 177, 4050-123 Porto, Portugal
D. I. GIBSON
Affiliation:
Department of Zoology, Natural History Museum, Cromwell Road, London SW7 5BD, UK
H. N. CABRAL
Affiliation:
Universidade de Lisboa, Faculdade de Ciências, Instituto de Oceanografia, Campo Grande, 1749-016 Lisboa, Portugal
P. D. OLSON
Affiliation:
Department of Zoology, Natural History Museum, Cromwell Road, London SW7 5BD, UK
*
*Corresponding author: Universidade de Lisboa, Faculdade de Ciências, Instituto de Oceanografia, Campo Grande, 1749-016 Lisboa, Portugal. Tel: +351 217 500 826. Fax: +351 217 500 207. E-mail: jimarques@fc.ul.pt
Get access Rights & Permissions [Opens in a new window]

Summary

Didymobothrium rudolphii (Cestoda: Spathebothriidea) was collected seasonally from the sand sole, Solea lascaris, off the northern, central and southern areas of the Portuguese coast. Morphological and molecular analyses were conducted in order to examine the possible existence of cryptic species and to facilitate the circumscription of their morphological boundaries. Data were compared between D. rudolphii specimens from each of the 3 geographical areas and 4 seasons, and principal components analysis of 18 morphological characters was used to detect differences. Two distinct genotypes were present with sequence divergences of 1·9% and 2·1% in the large subunit (lsrDNA) and second internal transcribed spacer (ITS-2) of ribosomal DNA (rDNA), respectively. The less common ‘central’ genotype was present only off the central area from summer to winter, whereas the ‘common’ genotype was present throughout the year off the northern and southern areas, but only during spring in the central area. No sequence variation was found within each genotype. The presence of 2 distinct genetic entities was supported by morphological analyses, which showed the ‘central’ genotype specimens to be more slender and elongate, although morphometric ranges overlapped considerably for most characters. Molecular phylogenetic analysis of 4 of the 5 known genera of the Spathebothriidea showed Spathebothrium to be the earliest branching lineage and the 2 genotypes of Didymobothrium formed a sister group to Cyathocephalus. The concordance of genetic differences with variation in host diet according to season and locality could account for sympatric speciation occurring in the central region of the Portuguese coast.

Keywords

DidymobothriumSpathebothriidealarge-subunit rDNAITS-2cryptic speciationsystematicsSolea lascarisBothrimonusCyathocephalusDiplocotyleSpathebothriumPortuguese coast
Type
Research Article
Information
Parasitology , Volume 134 , Issue 7 , July 2007 , pp. 1057 - 1072
Copyright
Copyright © Cambridge University Press 2007

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

Agustí, C., Aznar, F. J., Olson, P. D., Littlewood, D. T. J., Kostadinova, A. and Raga, J. A. (2005). Morphological and molecular characterization of tetraphyllidean merocercoids (Platyhleminthes: Cestoda) of striped dolphins (Stenella coeruleoalba) from the western Mediterranean. Parasitology 130, 461–474.Google Scholar
Aznar, F. J., Agustí, C., Littlewood, D. T. J., Raga, J. A. and Olson, P. D. (2007). The role of cetaceans in the tetraphyllidean life cycle: molecular and ecological data from the western Mediterranean. International Journal for Parasitology 37, 243–255.Google Scholar
Brickle, P., Olson, P. D., Littlewood, D. T. J., Bishop, A. and Arkhipkin, A. (2001). Parasites of Loligo gahi from waters off the Falkland Islands with a molecular-based identification of their cestode larvae. Canadian Journal of Zoology 79, 2289–2296.Google Scholar
Brunanska, M., Poddubnaya, L. G. and Dezfuli, B. S. (2005). Vitellogenesis in two spathebothriidean cestodes. Parasitology Research 96, 390–397.Google Scholar
Burt, M. D. B. and Sandeman, I. M. (1969). Biology of Bothrimonus (=Diplocotyle) (Pseudophyllidea: Cestoda) Part I. History, description, synonymy, and systematics. Journal of the Fisheries Research Board of Canada 26, 975–996.Google Scholar
Cabral, H. N., Lopes, M. and Loeper, R. (2002). Trophic niche overlap between flatfishes in a nursery area in the Portuguese coast. Scientia Marina 66, 293–300.Google Scholar
Davydov, V. G., Poddubnaya, L. G. and Kuperman, B. I. (1997). An ultrastructure of some systems of the Diplocotyle olrikii (Cestoda: Cyathocephalata) in relation to peculiarities of its life cycle. Parazitologiya 31, 132–141. (In Russian.)Google Scholar
Georgiev, B., Biserkov, V. and Genov, T. (1986). In toto staining method for cestodes with iron acetocarmine. Helminthologia 23, 279–281.Google Scholar
Gibson, D. I. (1994). Order Spathebothriidea Wardle and McLeod, 1952. In Keys to the Cestode Parasites of Vertebrates (ed. Khalil, L. F., Jones, A. and Bray, R. A.), pp. 15–19. CAB International, Wallingford.Google Scholar
Gibson, D. I. and Valtonen, E. T. (1983). Two interesting records of tapeworms from Finnish fishes. Aquilo, Ser. Zoologica 22, 45–49.Google Scholar
Hanzelová, V., Kuchta, R., Scholz, T. and Shinn, A. P. (2005). Morphometric analysis of four species of Eubothrium (Cestoda: Pseudophyllidea) parasites of salmonid fish: an interspecific and intraspecific comparison. Parasitology International 54, 207–214.Google Scholar
Infante, C., Catanese, G. and Manchado, M. (2004). Phylogenetic relationships among ten sole species (Soleidae, Pleuronectiformes) from the Gulf of Cádiz (Spain) based on mitochondrial DNA sequences. Marine Biotechnology 6, 612–624.Google Scholar
Link, J. S., Fogarty, M. J. and Langton, R. W. (2005). The trophic ecology of flatfishes. In Flatfishes Biology and Exploitation (ed. Gibson, R. N.), pp. 185–212. Blackwell Publishing, Oxford.Google Scholar
Mackiewicz, J. S. (2003). Caryophyllidea (Cestoidea): molecules, morphology and evolution. Acta Parasitologica 48, 143–154.Google Scholar
MacKinnon, B. M. and Burt, M. D. B. (1984). The comparative ultrastructure of spermatozoa from Bothrimonus sturionis Duv. 1842 (Pseudophyllidae) Pseudanthobothrium hanseni Baer, 1956 (Tetraphyllidae), and Monoecocestus americanus Stiles, 1895 (Cyclophyllidea). Canadian Journal of Zoology 62, 1059–1066.Google Scholar
Maddison, W. P. and Maddison, D. R. (2005). MacClade: Analysis of Phylogeny and Character Evolution. Sinauer Associates, Sunderland, Massachusetts.Google Scholar
McGinnis, S. and Madden, T. L. (2004). BLAST: at the core of powerful and diverse set of sequence analysis tools. Nucleic Acids Research 32, W20–W25.Google Scholar
Monticelli, S. (1890). Note helminthologiche. Bollettino Società Naturalisti di Napoli 4, 189–208.Google Scholar
Monticelli, S. (1892). Sul genere Bothrimonus, Duvernoy e proposte per una classificazione dei Cestodi. Monitore Zoologico Italiano 5, 100–108.Google Scholar
Nolan, M. and Cribb, T. H. (2005). The use and implications of ribosomal DNA sequencing for the discrimination of digenean species. Advances in Parasitology 60, 102–156.Google Scholar
Nybelin, O. N. (1922). Anatomisch-systematische Studien über Pseudophyllideen. Göteborgs Kungl, Vetenskaps-och Vitterhets-Samhälles Handlingar, Fjärde-Följden 26, 1–228.Google Scholar
Nylander, J. A. A. (2004). MrModelTest, program distributed by the author. Evolutionary Biology, Uppsala University, Sweden.Google Scholar
Okaka, C. E. (2000). Maturity of the procercoid of Cyathocephalus truncatus (Eucestoda: Spathebothriidae) in Gammarus pulex (Crustacea: Amphipoda) and the tapeworms life cycle using the amphipod as the sole host. Helminthologia 37, 153–157.Google Scholar
Olson, P. D., Cribb, T. H., Tkach, V. V., Bray, R. A. and Littlewood, D. T. J. (2003). Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda). International Journal for Parasitology 33, 733–755.Google Scholar
Olson, P. D., Littlewood, D. T. J., Griffiths, D., Kennedy, C. R. and Arme, C. (2002). Evidence for the co-existence of separate strains or species of Ligula in Lough Neagh, Northern Ireland. Journal of Helminthology 76, 171–174.Google Scholar
Olson, P. D., Littlewood, D. T. J., Bray, R. A. and Mariaux, J. (2001). Interrelationships and evolution of the tapeworms (Platyhelminthes: Cestoda). Molecular Phylogenetics and Evolution 19, 443–467.Google Scholar
Olson, P. D. and Tkach, V. V. (2005). Advances and trends in the molecular systematics of the parasitic Platyhelminthes. Advances in Parasitology 60, 165–243.Google Scholar
Pertierra, A. A. G. (2002). Redescription of Proteocephalus bagri and P. rhamdiae (Cestoda: Proteocephalidea), parasites of Ramdia quelen (Siluriformes: Pimelodidae) from South America, with comments on morphological variation. Folia Parasitologica 49, 55–66.Google Scholar
Poddubnaya, L. G., Mackiewicz, J. S. and Kuperman, B. I. (2003). Ultrastructure of Archigetes sieboldi (Cestoda: Caryophyllidea): relationship between progenesis, development and evolution. Folia Parasitologica 50, 275–292.Google Scholar
Poddubnaya, L. G., Mackiewicz, J. S., Brunanska, M. and Scholz, T. (2005). Ultrastructural studies on the reproductive system of progenetic Diplocotyle olrikii (Cestoda, Spathebothriidea): Ovarian tissue. Acta Parasitologica 50, 199–207.Google Scholar
Poddubnaya, L. G., Gibson, D. I., Swiderski, Z. and Olson, P. D. (2006). Vitellocyte ultrastructure in the cestode Didymobothrium rudolphii (Monticelli, 1890): possible evidence for the recognition of divergent taxa within the Spathebothriidea. Acta Parasitologica 51, 255–263.Google Scholar
Posada, D. and Crandall, K. A. (1998). Modeltest: testing the model of DNA substitution. Bioinformatics 14, 817–818.Google Scholar
Protasova, E. N. and Roytman, V. A. (1995). [Cyathocephalates, tapeworm helminths of marine and freshwater fish (Cestoda: Pseudophyllidea: Cyathocephalata).] Osnovy Tsestodologii, Vol. 12. Institute of Parasitology, Russian Academy of Sciences, Moscow.Google Scholar
Renaud, F. and Gabrion, C. (1988). Speciation in Cestoda: evidence for two sibling species in the complex Bothrimonus nylandicus (Schneider 1902) (Cestoda: Cyathocephalidae). Parasitology 97, 139–147.Google Scholar
Renaud, F., Gabrion, C. and Pasteur, N. (1986). Geographical divergence in Bothriocephalus (Cestoda) of fishes demonstrated by enzyme electrophoresis. International Journal for Parasitology 16, 553–558.Google Scholar
Reyda, F. B. and Olson, P. D. (2003). Cestodes of cestodes of Peruvian freshwater stingrays. Journal of Parasitology 89, 1018–1024.Google Scholar
Ronquist, F. and Huelsenbeck, J. (2003). MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.Google Scholar
Sandeman, I. M. and Burt, M. D. B. (1972). Biology of Bothrimonus (=Diplocotyle) (Pseudophyllidea: Cestoda): ecology, life cycle, and evolution; a review and synthesis. Journal of Fisheries Research Board of Canada 29, 1381–1395.Google Scholar
Schneider, G. (1902). Bothrimonus nylandicus n. sp. Archiv für Naturgeschichte 1, 72–78.Google Scholar
Swofford, D. L. (2001). PAUP*. Phylogenetic Analysis Using Parsimony (*and other Methods). Version 4. Sinauer Associates, Massachusetts.Google Scholar
SPSS 13.0 (2004). SPSS Inc., Chicago.Google Scholar
ter Braak, C. J. F. and Smilauer, P. (2002). Canoco for Windows Version 4.5. Biometris – Plant Research International, Wageningen, The Netherlands.Google Scholar
Verneau, O., Renaud, F. and Catzeflis, F. (1997). Evolutionary relationships of sibling tapeworm species (Cestoda) parasitizing teleost fishes. Molecular Biology and Evolution 14, 630–636.Google Scholar
Zehnder, M. P. and de Chambrier, A. (2000). Morphological and molecular analyses of the genera Peltidocotyle Diesing, 1850 and Othinoscolex Woodland, 1933, and morphological study of Woodlandiella Freze, 1965 (Eucestoda, Proteocephalidea), parasites of South American siluriform fishes (Pimelodidae). Systematic Parasitology 46, 33–43.Google Scholar