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Genetic diversity and population structure of Synthesium pontoporiae (Digenea, Brachycladiidae) linked to its definitive host stocks, the endangered Franciscana dolphin, Pontoporia blainvillei (Pontoporiidae) off the coast of Brazil and Argentina

Published online by Cambridge University Press:  09 September 2013

J. Marigo ,
H.A. Cunha ,
C.P. Bertozzi ,
S.P. Souza ,
F.C.W. Rosas ,
M.J. Cremer ,
A.S. Barreto ,
L.R. de Oliveira ,
H.L. Cappozzo  and
A.L.S. Valente
...Show all authors
J. Marigo*
Affiliation:
Laboratório de Genética Molecular de Microorganismos, Instituto Oswaldo Cruz, FIOCRUZ, Rio de Janeiro, RJ, Brazil Laboratório de Avaliação e Promoção da Saúde Ambiental, Instituto Oswaldo Cruz, FIOCRUZ, Rio de Janeiro, RJ, Brazil Projeto BioPesca, Praia Grande, SP, Brazil
H.A. Cunha
Affiliation:
Laboratório de Biodiversidade Molecular (UFRJ)/Laboratório de Mamíferos Aquáticos e Bioindicadores (MAQUA, UERJ), Rio de Janeiro, RJ, Brazil
C.P. Bertozzi
Affiliation:
Projeto BioPesca, Praia Grande, SP, Brazil
S.P. Souza
Affiliation:
Instituto Terra & Mar, Ilhabela, SP, Brazil
F.C.W. Rosas
Affiliation:
Instituto Nacional de Pesquisas da Amazônia, Manaus, AM, Brazil
M.J. Cremer
Affiliation:
Universidade da Região de Joinville, Joinville, SC, Brazil
A.S. Barreto
Affiliation:
Universidade do Vale do Itajaí, Balneário Camboriú, SC, Brazil
L.R. de Oliveira
Affiliation:
Laboratório de Ecologia de Mamíferos Universidade do Vale do Rio dos Sinos (UNISINOS), Grupo de Estudos de Mamíferos Aquáticos do Rio Grande do Sul (GEMARS), Porto Alegre, RS, Brazil
H.L. Cappozzo
Affiliation:
Museo Argentino de Ciencias Naturales ‘Bernardino Rivadavia’ (MACN-CONICET)/Universidad Maimónides y Fundación Azara, CABA, Buenos Aires, Argentina
A.L.S. Valente
Affiliation:
Universidade Federal de Pelotas, Pelotas, RS, Brazil
C.P. Santos
Affiliation:
Laboratório de Avaliação e Promoção da Saúde Ambiental, Instituto Oswaldo Cruz, FIOCRUZ, Rio de Janeiro, RJ, Brazil
A.C.P. Vicente
Affiliation:
Laboratório de Genética Molecular de Microorganismos, Instituto Oswaldo Cruz, FIOCRUZ, Rio de Janeiro, RJ, Brazil
*
*E-mail: [email protected]
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Abstract

Pontoporia blainvillei (Gervais and d'Orbigny, 1844) is an endangered small cetacean endemic to South America with four Franciscana Management Areas (FMA) recognized as different population stocks. The role of the intestinal parasite Synthesium pontoporiae (Digenea: Brachycladiidae) as a possible biological marker to differentiate P. blainvillei stocks was evaluated using nuclear and mitochondrial DNA markers. Internal transcribed sequence 1 and 2 (ITS1 and ITS2) regions of S. pontoporiae did not show intraspecific variability. The mitochondrial NADH dehydrogenase subunit 3 (ND3) and cytochrome oxidase subunit I (COI) gene sequences suggested lack of population structure in S. pontoporiae and population expansion. The apparent panmixia of S. pontoporiae may be due to the high mobility of one or more of its intermediary hosts. Alternatively, it may be due to the small sample size. This result is incongruent with the previously proposed FMA.

Type
Research Papers
Information
Journal of Helminthology , Volume 89 , Issue 1 , January 2015 , pp. 19 - 27
Copyright
Copyright © Cambridge University Press 2013 

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References

Altukhov, Y.P. (1981) The stock concept from the viewpoint of population genetics. Canadian Journal of Fisheries and Aquatic Sciences 38, 1523–1538.CrossRefGoogle Scholar
Andrade, A.L.V., Pinedo, M.C. & Pereira, J. Jr (1997) Franciscanas from southern Brazil, Uruguay and North Argentina coasts: are one or more ecological stocks? Reports of the International Whaling Commission 47, 669–673.Google Scholar
Attwood, S.W., Fatih, F.A. & Upatham, E.S. (2008) DNA-sequence variation among Schistosoma mekongi populations and related taxa; phylogeography and the current distribution of Asian schistosomiasis. PLoS Neglected Tropical Diseases 2, e200.CrossRefGoogle ScholarPubMed
Avise, J.C. (2008) Phylogeography: retrospect and prospect. Journal of Biogeography 36, 3–15.Google Scholar
Aznar, F.J., Raga, J.A., Corcuera, J. & Monzón, F. (1995) Helminths as biological tags for franciscana (Pontoporia blainvillei) (Cetacea, Pontoporiidae) in Argentinian and Uruguayan waters. Mammalia 59, 427–435.Google Scholar
Baldwin, R.E., Rew, M.B., Johansson, M.L., Banks, M.A. & Jacobson, K.C. (2011) Population structure of three species of Anisakis nematodes recovered from Pacific sardines (Sardinops sagax) distributed throughout the California current system. Journal of Parasitology 97, 545–554.CrossRefGoogle ScholarPubMed
Barbato, B.H.A., Secchi, E.R., Di Beneditto, A.P.M., Ramos, R.M.A., Bertozzi, C., Marigo, J., Bordino, P. & Kinas, P.G. (2011) Geographical variation in franciscana (Pontoporia blainvillei) external morphology. Journal of the Marine Biological Association of the United Kingdom 92, 1645–1656.CrossRefGoogle Scholar
Bessho, Y., Ohama, T. & Osawa, S. (1992) Planarian mitochondria II. The unique genetic code as deduced from cytochrome c oxidase subunit I gene sequences. Journal of Molecular Evolution 34, 331–335.Google Scholar
Bordino, P., Wells, R.S. & Stamper, M.A. (2008) Satellite tracking of Franciscana Dolphins Pontoporia blainvillei in Argentina: preliminary information on ranging, diving and social patterns. International Whaling Commission Scientific Committee Paper SC/53/IA32 presented to the IWC Scientific Committee (unpublished manuscript), June 2008, Santiago, Chile.Google Scholar
Clement, M., Posada, D. & Crandall, K.A. (2000) TCS: a computer program to estimate gene genealogies. Molecular Ecology 9, 1657–1659.Google Scholar
Costa-Urrutia, P., Abud, C., Secchi, E.R. & Lessa, E.P. (2011) Population genetic structure and social kin associations of franciscana dolphin, Pontoporia blainvillei. Journal of Heredity 103, 92–102.Google Scholar
Crandall, K. & Templeton, A.R. (1993) Empirical tests of some predictions from coalescent theory with applications to intraspecific phylogeny reconstruction. Genetics 134, 959–969.Google Scholar
Criscione, C.D. & Blouin, M.S. (2007) Parasite phylogeographical congruence with salmon host evolutionarily significant units: implications for salmon conservation. Molecular Ecology 16, 993–1005.CrossRefGoogle ScholarPubMed
Criscione, C.D., Poulin, R. & Blouin, M.S. (2005) Molecular ecology of parasites: elucidating ecological and microevolutionary processes. Molecular Ecology 14, 2247–2257.Google Scholar
Criscione, C.D., Cooper, B. & Blouin, M.S. (2006) Parasite genotypes identify source populations of migratory fish more accurately than fish genotypes. Ecology 87, 823–828.Google Scholar
Criscione, C.D., Vilas, R., Paniagua, E. & Blouin, M.S. (2011) More than meets the eye: detecting cryptic microgeographic population structure in a parasite with a complex life cycle. Molecular Ecology 20, 2510–2524.Google Scholar
Drummond, A.J. & Rambaut, A. (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology 7, 214.CrossRefGoogle ScholarPubMed
Dupanloup, I., Schneider, S. & Excoffier, L. (2002) A simulated annealing approach to define the genetic structure of populations. Molecular Ecology 11, 2571–2581.Google Scholar
Excoffier, L., Smouse, P.E. & Quattro, J.M. (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 491, 479–491.Google Scholar
Excoffier, L., Laval, G. & Schneider, S. (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online 1, 47–50.Google Scholar
Fernández, M., Aznar, F.J., Latorre, A. & Raga, J.A. (1998a) Molecular phylogeny of the families Campulidae and Nasitrematidae (Trematoda) based on mtDNA sequence comparison. International Journal for Parasitology 28, 767–775.Google Scholar
Fernández, M., Littlewood, D.T., Latorre, A., Raga, J.A. & Rollinson, D. (1998b) Phylogenetic relationships of the family Campulidae (Trematoda) based on 18S rRNA sequences. Parasitology 117, 383–391.Google Scholar
Gibson, D.I. (2002) Trematodes in marine mammals: morphology, systematics and origins. pp. 59–63in Proceedings of the Tenth International Congress of Parasitology. Vancouver, Canada. Bologna, Italy, Monduzzi Medimond Editore.Google Scholar
Hansen, E.K. & Poulin, R. (2006) Spatial covariation between infection levels and intermediate host densities in two trematode species. Journal of Helminthology 80, 255–259.Google Scholar
IBAMA, (2001) Mamíferos Aquáticos do Brasil: Plano de Ação – Versão II. 706 pp. Brasília, IBAMA (Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis, Ministério do Meio Ambiente).Google Scholar
Jarne, P. & Théron, A. (2001) Genetic structure in natural populations of flukes and snails: a practical approach and review. Parasitology 123, S27–S40.CrossRefGoogle ScholarPubMed
Klimpel, S., Busch, M., Kuhn, T., Rohde, A. & Palm, H. (2010) The Anisakis simplex complex off the South Shetland Islands (Antarctica): endemic populations versus introduction through migratory hosts. Marine Ecology Progress Series 403, 1–11.Google Scholar
MacKenzie, K. (2002) Parasites as biological tags in population studies of marine organisms: an update. Parasitology 124, S153–S163.Google Scholar
Marigo, J., Rosas, F.C.W., Andrade, A.L.V., Oliveira, M.R., Dias, R.A. & Catão-Dias, J.L. (2002) Parasites of Franciscana (Pontoporia blainvillei) from São Paulo and Paraná States, Brazil. Latin American Journal of Aquatic Mammals 1, 115–122.Google Scholar
Marigo, J., Vicente, A.C.P., Valente, A.L.S., Measures, L. & Santos, C.P. (2008) Redescription of Synthesium pontoporiae n. comb. with notes on S. tursionis and S. seymouri n. comb. (Digenea: Brachycladiidae Odhner, 1905). Journal of Parasitology 94, 505–514.Google Scholar
Marigo, J., Thompson, C.C., Santos, C.P. & Iñiguez, A.M. (2011) The Synthesium Brachycladiidae Odhner, 1905 (Digenea) association with hosts based on nuclear and mitochondrial genes. Parasitology International 60, 530–533.Google Scholar
Mattiucci, S. & Nascetti, G. (2007) Genetic diversity and infection levels of anisakid nematodes parasitic in fish and marine mammals from Boreal and Austral hemispheres. Veterinary Parasitology 148, 43–57.CrossRefGoogle ScholarPubMed
Mattiucci, S., Farina, V., Campbell, N., Mackenzie, K., Ramos, P., Pinto, A., Abaunza, P. & Nascetti, G. (2008) Anisakis spp. larvae (Nematoda: Anisakidae) from Atlantic horse mackerel: their genetic identification and use as biological tags for host stock characterization. Fisheries Research 89, 146–151.Google Scholar
Mendez, M., Rosenbaum, H.C. & Bordino, P. (2007) Conservation genetics of the franciscana dolphin in northern Argentina: population structure, by-catch impacts, and management implications. Conservation Genetics 9, 419–435.Google Scholar
Mendez, M., Rosenbaum, H.C., Subramaniam, A., Yackulic, C. & Bordino, P. (2010) Isolation by environmental distance in mobile marine species: molecular ecology of franciscana dolphins at their southern range. Molecular Ecology 19, 2212–2228.Google Scholar
Meyer, A., Kocher, T.D., Basasibwaki, P. & Wilson, A.C. (1990) Monophyletic origin of Lake Victoria cichlid fishes suggested by mitochondrial DNA sequence. Nature 347, 550–553.CrossRefGoogle Scholar
Morgan, J.A., Dejong, R.J., Adeoye, G.O., Ansa, E.D.O., Barbosa, C.S., Brémond, P., Cesari, I.M., Charbonnel, N., Corrêa, L.R., Coulibaly, G., et al., (2005) Origin and diversification of the human parasite Schistosoma mansoni. Molecular Ecology 14, 3889–3902.Google Scholar
Ott, P.H., Oliveira, L.R., Barreto, A.S., Secchi, E.R., Almeida, R., Moreno, I.B., Danilewicz, D. & Bonatto, S. (2008) Unidades de manejo da toninha, Pontoporia blainvillei: uma avaliação molecular do limite entre as FMAS II e IIIp. 81 in XIII Reunión de Trabajo de Especialistas em Mamíferos Acuáticos de América del Sur y 7o. Congresso SOLAMAC (Sociedade Latino Americana de Especialistas em Mamíferos Aquáticos), Montevideo, Uruguai, 13–17 October.Google Scholar
Pinedo, M.C. (1991) Development and variation of the franciscana (Pontoporia blainvillei). PhD thesis, University of California, Santa Cruz.Google Scholar
Posada, D. (2008) jModelTest: phylogenetic model averaging. Molecular Biology and Evolution 25, 1253–1256.Google Scholar
Prugnolle, F., Liu, H., de Meeus, T. & Balloux, F. (2005a) Population genetics of complex life-cycle parasites: an illustration with trematodes. International Journal of Parasitology 35, 255–263.Google Scholar
Prugnolle, F., Theron, A., Pointier, J.P., Jabbour-Zahab, R., Jarne, P., Durand, P. & de Meeûs, T. (2005b) Dispersal in a parasitic worm and its two hosts and its consequence for local adaptation. Evolution 59, 296–303.Google Scholar
Reeves, R. & Leatherwood, S. (1994) Dolphins, porpoises and whales: 1994–1998 Action Plan for the Conservation of Cetaceans. Gland, Switzerland, IUCN (International Union for Conservation of Nature).Google Scholar
Rodrigues, A.R. & Gasalla, M.A. (2008) Spatial and temporal patterns in size and maturation of Loligo plei and Loligo sanpaulensis (Cephalopoda:Loliginidae) in southeastern Brazilian waters, between 23°S and 27°S. Scientia Marina 72, 631–643.Google Scholar
Rozas, J., Sánchez-Delbarrio, J.C., Messeguer, X. & Rozas, R. (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19, 2496–2497.Google Scholar
Sardiña, P. & Lopez Cazorla, A. (2005) Feeding interrelationships and comparative morphology of two young sciaenids co-occurring in South-western Atlantic waters. Hydrobiologia 548, 41–49.Google Scholar
Secchi, E.R., Wang, J.Y., Murray, B.W., Rocha-Campos, C.C. & White, B.N. (1998) Population differentiation in the franciscana (Pontoporia blainvillei) from two geographic locations in Brazil as determined from mitochondrial DNA control region sequences. Canadian Journal of Zoology 76, 1622–1627.Google Scholar
Secchi, E.R., Danilewicz, D., Ott, P.H., Ramos, R., Lazaro, M., Marigo, J. & Wang, J.Y. (2002) Report of the working group on stock identity. Latin American Journal of Aquatic Mammals 1, 47–54.Google Scholar
Secchi, E.R., Danilewicz, D. & Ott, P.H. (2003) Applying the phylogeographic concept to identify franciscana dolphin stocks: implications to meet management objectives. Journal of Cetacean Research and Management 5, 61–68.Google Scholar
Semyenova, S.K., Morozova, E.V., Chrisanfova, G.G., Asatrian, A.M., Movsessian, S.O. & Ryskov, A.P. (2003) RAPD variability and genetic diversity in two populations of liver fluke, Fasciola hepatica. Acta Parasitologica 48, 125–130.Google Scholar
Shrivastava, J., Gower, C.M., Balolong, E., Wang, T.P., Qian, B.Z. & Webster, J.P. (2005) Population genetics of multi-host parasites – the case for molecular epidemiological studies of Schistosoma japonicum using larval stages from naturally infected hosts. Parasitology 131, 617–626.Google Scholar
Siciliano, S., Di Beneditto, A.P.M. & Ramos, R.M.A. (2002) A toninha, Pontoporia blainvillei (Gervais and d'Orbigny, 1844) (Mammalia, Cetacea, Pontoporiidae), nos estados do Rio de Janeiro e Espírito Santo, costa sudeste do Brasil: Caracterizaçãoo dos habitats e fatores de isolamento das populações. Boletim do Museu Nacional, Serie Zoologia 476, 1–15.Google Scholar
Théron, A., Sire, C., Rognon, A., Prugnolle, F. & Durand, P. (2004) Molecular ecology of Schistosoma mansoni transmission inferred from the genetic composition of larval and adult infrapopulations within intermediate and definitive hosts. Parasitology 129, 571–585.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, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 4673–4680.Google Scholar
Vilas, R., Paniagua, E. & Sanmartin, M.L. (2003) Genetic variation within and among infrapopulations of the marine digenetic trematode Lecithochirium fusiforme. Parasitology 126, 465–472.Google Scholar
Wang, J.Y. (2002) Stock identity. pp. 1115–1118in Perrin, W.F., Würsig, B. & Thewissen, J.G.M. (Eds) Enciclopedia of marine mammals. San Diego, Academic Press, Elsevier.Google Scholar
Zhu, X., Gasser, R.B., Jacobs, D.E., Hung, G.C. & Chilton, N.B. (2000) Relationships among some ascaridoid nematodes based on ribosomal DNA sequence data. Parasitology Research 86, 738–744.Google Scholar
Zhu, X.Q., Podolska, M., Liu, J.S., Yu, H.Q., Chen, H.H., Lin, Z.X., Luo, C.B., Song, H.Q. & Lin, R.Q. (2007) Identification of anisakid nematodes with zoonotic potential from Europe and China by single-strand conformation polymorphism analysis of nuclear ribosomal DNA. Parasitology Research 101, 1703–1707.Google Scholar