Hostname: page-component-78c5997874-8bhkd Total loading time: 0 Render date: 2024-11-05T07:50:34.008Z Has data issue: false hasContentIssue false

Molecular evidence confirms that Proctoeces humboldti and Proctoeces chilensis (Digenea: Fellodistomidae) are the same species

Published online by Cambridge University Press:  15 January 2010

I.M. Valdivia*
Affiliation:
Facultad de Recursos del Mar, Instituto de Investigaciones Oceanológicas, Universidad Antofagasta, Casilla 170, Antofagasta, Chile Programa de Doctorado en Ciencias Aplicadas, Mención en Sistemas Marinos Costeros, Universidad de Antofagasta, Antofagasta, Chile
L. Cardenas
Affiliation:
Instituto de Ecología y Evolución, Universidad Austral, Casilla 567, Isla Teja, Valdivia, Chile
K. Gonzalez
Affiliation:
Facultad de Ciencias, Universidad Católica de la Santísima Concepción, Casilla 297, Concepción, Chile
D. Jofré
Affiliation:
Facultad de Recursos del Mar, Instituto de Investigaciones Oceanológicas, Universidad Antofagasta, Casilla 170, Antofagasta, Chile
M. George-Nascimento
Affiliation:
Facultad de Ciencias, Universidad Católica de la Santísima Concepción, Casilla 297, Concepción, Chile
R. Guiñez
Affiliation:
Facultad de Recursos del Mar, Instituto de Investigaciones Oceanológicas, Universidad Antofagasta, Casilla 170, Antofagasta, Chile
M.E. Oliva
Affiliation:
Facultad de Recursos del Mar, Instituto de Investigaciones Oceanológicas, Universidad Antofagasta, Casilla 170, Antofagasta, Chile
*
*Fax: +56-55-637804 E-mail: [email protected]

Abstract

Two species of Proctoeces Odhner, 1911 have been described in marine organisms from Chile: P. humboldti George-Nascimento & Quiroga (1983), parasitizing the gonads of keyhole limpets (Fissurella spp.), and P. chilensis Oliva (1984), an intestinal parasite of Sicyases sanguineus (Teleostei); both species were subsequently considered as P. lintoni Siddiqi & Cable (1960). To assist in the resolution of the taxonomic identification of Proctoeces species in marine organisms from Chile, phylogenetic studies using DNA sequences from the V4 region of the SSU rRNA gene were performed. Several specimens of P. lintoni were isolated from keyhole limpets (Fissurella spp.) and clingfish (S. sanguineus) from Bahia San Jorge (23°40′S) and Bahia Concepción (36°50′S). Phylogenetic analyses were conducted using three different approaches: a neighbour-joining (NJ), a maximum likelihood (ML) and Bayesian inference (BI). The phylogenetic analysis confirms that specimens of Proctoeces obtained from keyhole limpets and those specimens from the clingfish are in fact the same species. We prefer to consider our specimens as Proctoeces cf. lintoni, as the morphology of Proctoeces appears to be of doubtful value and genetic information about P. lintoni Siddiqi & Cable (1960) is not available. In addition, our results strongly suggest that there are at least three species in this genus.

Type
Research Papers
Copyright
Copyright © Cambridge University Press 2010

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

Aiken, H., Bott, N.J., Mladineo, I., Montero, F.E., Nowak, B.F. & Hayward, C.J. (2007) Molecular evidence for cosmopolitan distribution of platyhelminth parasites of tunas (Thunnus spp.). Fish and Fisheries 8, 167180.CrossRefGoogle Scholar
Aldana, M. (2007) Variación espacial de la interacción hospedador parásito: la importancia de la densidad poblacional de los hospedadores. Unpublished PhD thesis, Universidad Católica de Chile.Google Scholar
Bowers, E.A., Bartoli, P., Russell-Pinto, F. & James, B.L. (1996) The metacercariae of sibling species of Meiogymnophallus, including M. rebecqui comb nov (Digenea: Gymnophallidae), and their effects on closely related Cerastoderma host species (Mollusca: Bivalvia). Parasitology Research 82, 505510.CrossRefGoogle ScholarPubMed
Bray, R.A. (1983) On the fellodistomid genus Proctoeces Odhner, 1911 (Digenea), with brief comments on two other fellodistomid genera. Journal of Natural History 17, 321339.CrossRefGoogle Scholar
Bray, R.A. & Gibson, D.I. (1980) The Fellodistomidae (Digenea) of fishes from the northeast Atlantic. Bulletin British Museum of Natural History (Zoology) 37, 199293.Google Scholar
Bretos, M. & Jirón, C. (1980) Trematodes in Chilean fissurellid. Veliger 22, 293.Google Scholar
Brooks, D.R. & McLennan, D.A. (1993) Parascript, parasites and the language of evolution. Washington DC, Smithsonian Press.Google Scholar
Chambers, C.B. & Cribb, T.H. (2006) Phylogeny, evolution and biogeography of the Quadrifoliovariinae Yamaguti, 1965 (Digenea: Lecithasteridae). Systematic Parasitology 63, 6182.CrossRefGoogle ScholarPubMed
Felsenstein, J. (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783791.CrossRefGoogle ScholarPubMed
Filatov, D.A. (2002) Proseq: a Software for preparation and evolutionary analysis of DNA sequence data sets. Molecular Ecology Notes 2, 621624.CrossRefGoogle Scholar
George-Nascimento, M. & Quiroga, G. (1983) Descripción de una nueva especie de tremátodo, Proctoeces humboldti n. sp. (Digenea: Fellodistomidae), parásito de las lapas Fissurella spp. Brugiere, 1789 (Mollusca: Archaeogastropoda). Parasitología al día 7, 100103.Google Scholar
George-Nascimento, M., Balboa, L., Aldana, M. & Olmos, V. (1998) Las lapas Fissurella spp. (Mollusca: Archaeogastropoda) y el pejesapo Syciases sanguineus (Pisces: Gobiesocidae) son huéspedes secuenciales de Proctoeces lintoni (Digenea: Fellodistomidae) en Chile. Revista Chilena de Historia Natural 71, 169176.Google Scholar
Hall, K.A., Cribb, T.H. & Barker, S.C. (1999) V4 region of small subunit rDNA indicates polyphyly of the Fellodistomidae (Digenea) which is supported by morphology and life-cycle data. Systematic Parasitology 43, 8192.CrossRefGoogle ScholarPubMed
Huelsenbeck, J.P. & Ronquist, F. (2005) Bayesian analysis of molecular evolution using MrBayes. pp. 183232in Nielsen, R. (Ed.) Statistical methods in molecular evolution. New York, Springer.CrossRefGoogle Scholar
Jousson, O. & Bartoli, P. (2001) Molecules, morphology and morphometrics of Cainocreadium labracis and Cainocreadium dentecis n. sp. (Digenea: Opecoelidae) parasitic in marine fishes. International Journal for Parasitology 31, 706714.CrossRefGoogle Scholar
Kaukas, A. & Rollinson, D. (1997) Interspecific variation within the ‘hypervariable’ region of the 18S ribosomal RNA gene among species of Schistosoma Weinland, 1858 (Digenea). Systematic Parasitology 36, 157160.CrossRefGoogle Scholar
Larkin, M.A., Blackshields, G., Brown, N.P., Chenna, R., McGettigan, P.A., McWilliam, H., Valentin, F., Wallace, I.M., Wilm, A., Lopez, R., Thompson, J.D., Gibson, T.J. & Higgins, D.G. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23, 29472948.CrossRefGoogle ScholarPubMed
Lo, C.M., Morgan, J.A.T., Galzina, R. & 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, 15731578.CrossRefGoogle ScholarPubMed
Loot, G., Aldana, M. & Navarrete, S.A. (2005) Effects of human exclusion on parasitism in intertidal food webs of central Chile. Conservation Biology 19, 110.CrossRefGoogle Scholar
Loot, G., Blanchet, S., Aldana, M. & Navarrete, S.A. (2008) Evidence of plasticity in the reproduction of a trematode parasite: the effect of host removal. Journal of Parasitology 94, 2327.CrossRefGoogle ScholarPubMed
McCarthy, A.M. (1990) Speciation of echinostomes: evidence for the existence of two sympatric sibling species in the complex Echinoparyphium recurvatum (von Linstow 1873) (Digenea: Echinostomatidae). Parasitology 101, 3542.CrossRefGoogle Scholar
Miller, T.L. & Cribb, T.H. (2007) Coevolution of Retrovarium n. gen. (Digenea: Cryptogonimidae) in Lutjanidae and Haemulidae (Perciformes) in the Indo-West Pacific. International Journal for Parasitology 37, 10231045.CrossRefGoogle ScholarPubMed
Nei, M. & Kumar, S. (2000) Molecular evolution and phylogenetics. 333 pp. Oxford, Oxford University Press.CrossRefGoogle Scholar
Nolan, M. & Cribb, T. (2005) The use and implications of ribosomal DNA sequencing for the discrimination of Digenean species. Advances in Parasitology 60, 101163.CrossRefGoogle ScholarPubMed
Oliva, M.E. (1984) Proctoeces chilensis nueva especie (Trematoda: Strigeatoidea: Fellodistomidae), parásito en Syciases sanguineus Müller & Tronschel, 1843 (Pisces: Teleostei). Boletín de la Sociedad de Biología de Concepción, Chile 55, 8792.Google Scholar
Oliva, M.E. (1992) Parasitic castration of Fissurella crassa (Mollusca: Archaeogastropoda) due to an adult digenea Proctoeces lintoni. Memorias Instituto Oswaldo Cruz 87, 3742.CrossRefGoogle Scholar
Oliva, M.E. & Díaz, M. (1988) Aspectos cuantitativos de la infección por Proctoeces humboldti (Trematoda: Fellodistomidae) en la lapa Fissurella crassa (Mollusca: Archaeogastropoda). Revista Chilena de Historia Natural 61, 2735.Google Scholar
Oliva, M.E. & Díaz, M. (1992) An ecological approach of Proctoeces lintoni (Digenea: Fellodistomidae) infection in the key hole limpet Fissurella limbata Sowerby, 1835 (Archaeogastropoda) from northern Chile. Acta Parasitologica 37, 115118.Google Scholar
Oliva, M.E. & Huaquin, L.G. (2000) Progenesis in Proctoeces lintoni (Fellodistomidae), a parasite of Fissurella crassa (Archaeogastropoda) in a latitudinal gradient in the Pacific Coast of South America. Journal of Parasitology 86, 768772.CrossRefGoogle Scholar
Oliva, M.E. & Zegers, J. (1988) Variaciones intraespecíficas del adulto de Proctoeces lintoni Siddiqi & Cable, 1960 (Trematoda: Fellodistomidae) en hospedadores vertebrados e invertebrados. Studies on Neotropical Fauna and Environment 23, 189195.CrossRefGoogle Scholar
Olson, P.D., Cribb, T.H., Tkach, V.V., Bray, R.A. & Littlewood, D.T.J. (2003) Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda). International Journal for Parasitology 33, 733755.CrossRefGoogle ScholarPubMed
Osorio, C., Díaz, H. & Rios, M. (1986) Prevalencia de Proctoeces humboldti George Nascimento y Quiroga 1983 (Digenea: Fellodistomidae) en la población de Fissurella maxima Sowerby 1835 (Mollusca, Gastropoda) de Los Vilos, Chile. Revista de Biología Marina 22, 157168.Google Scholar
Ostrowski de Nunez, M. (2001) Life cycles of two new sibling species of Ascocotyle (Ascocotyle) (Digenea, Heterophyidae) in the Neotropical Region. Acta Parasitologica 46, 119129.Google Scholar
Palm, H.W., Waeschenbach, A. & Littlewood, D.T.J. (2007) Genetic diversity in the trypanorhynch cestode Tentacularia coryphaenae Bosc, 1797: evidence for a cosmopolitan distribution and low host specificity in the teleost intermediate host. Parasitology Research 101, 153159.CrossRefGoogle ScholarPubMed
Posada, D. & Crandall, K.A. (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 1, 817818.CrossRefGoogle Scholar
Rozas, J., Sánchez-Delbarrio, J.C., Messeguer, X. & Rozas, R. (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19, 24962497.CrossRefGoogle ScholarPubMed
Sambrook, J., Fritsch, E.F. & Maniatis, T. (1989) Molecular cloning: a laboratory manual. 2nd edn. Cold Spring Harbor, New York, Cold Spring Harbor Laboratory Press.Google Scholar
Sorensen, R.E., Curtis, J. & Minchella, D.J. (1998) Intraspecific variation in the rDNA loci of 37-collar-spined echinostomes from North America: implications for sequence-based diagnoses and phylogenetics. Journal of Parasitology 84, 992997.CrossRefGoogle ScholarPubMed
Steinauer, M.L., Nickol, B.B. & Orti, G. (2007) Cryptic speciation and patterns of phenotypic variation of a highly variable acanthocephalan parasite. Molecular Ecology 16, 40974109.CrossRefGoogle ScholarPubMed
Swofford, D.L. (2001) PAUP* 4.0b: Phylogenetic analysis using parsimony (*and other methods). Sunderland, Massachusetts, Sinauer Associates.Google Scholar