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Molecular systematics of five Onchocerca species (Nematoda: Filarioidea) including the human parasite, O. volvulus, suggest sympatric speciation

Published online by Cambridge University Press:  12 April 2024

R. Morales-Hojas ,
R.A. Cheke  and
R.J. Post
R. Morales-Hojas*
Affiliation:
Natural Resources Institute, University of Greenwich at Medway, Central Avenue, Chatham Maritime, Kent, ME4 4TB, UK
R.A. Cheke
Affiliation:
Natural Resources Institute, University of Greenwich at Medway, Central Avenue, Chatham Maritime, Kent, ME4 4TB, UK
R.J. Post
Affiliation:
Department of Entomology, The Natural History Museum, Cromwell Road, London, SW7 5BD, UK
*
*Fax: +351 22 609 9157 Email: rmhojas@ibmc.up.pt
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Abstract

The genus Onchocerca (Nematoda: Filarioidea) consists of parasites of ungulate mammals with the exception of O. volvulus, which is a human parasite. The relationship between O. volvulus, O. ochengi and O. gibsoni remains unresolved. Based on morphology of the microfilariae and infective larvae, vector transmission and geographical distribution, O. ochengi and O. volvulus have been placed as sister species. Nevertheless, the cuticle morphology and chromosomal data (O. volvulus and O. gibsoni have n=4 while O. ochengi is n=5) suggest that O. gibsoni could be more closely related to O. volvulus than O. ochengi. Sequences from the 12S rRNA, 16S rRNA and ND5 mitochondrial genes have been used to reconstruct the phylogeny of five Onchocerca species including O. volvulus. Analyses with maximum likelihood and maximum parsimony showed that O. ochengi is the sister species of O. volvulus, in accordance with the classification based on morphology and geographical location. The separate specific status of the species O. gutturosa and O. lienalis was supported, although their phylogenetic relationship was not well resolved. The analyses indicated that the basal species was O. gibsoni, a South-East Asian and Australasian species, but this result was not statistically significant. The possible involvement of sympatric speciation in the evolution of this group of parasites is discussed.

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Type
Research Article
Information
Journal of Helminthology , Volume 80 , Issue 3 , September 2006 , pp. 281 - 290
Copyright
Copyright © Cambridge University Press 2006

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References

Akaike, H. (1974) A new look at the statistical model identification. IEEE Transactions on Automatic Control 19, 716–723.CrossRefGoogle Scholar
Andrews, R.H., Beveridge, I., Adams, M. & Baverstock, P.R. (1989) Genetic characteristics of three species of Onchocerca at 23 enzyme loci. Journal of Helminthology 63, 87–92.CrossRefGoogle Scholar
Bain, O. (1981) Le genre Onchocerca: hypothèses sur son évolution et clé dichotomique des espèces. Annales de Parasitologie Humaine et Comparée 56, 503–526.CrossRefGoogle Scholar
Bain, O. (2002) Evolutionary relationships among filarial nematodes. pp. 21–29 in Klei, T.R., Rajan, T.V. (Eds) The Filaria. Boston, Dordrecht and London, Kluwer Academic Publishers.CrossRefGoogle ScholarPubMed
Bain, O. & Beveridge, I. (1979) Redescription d'Onchocerca gibsoni, C. et J. 1910. Annales de Parasitologie Humaine et Comparée 54, 69–80.10.1051/parasite/1979541069CrossRefGoogle Scholar
Bain, O., Petit, G. & Poulain, B. (1978) Validité des deux espèces Onchocerca lienalis et O. gutturosa chez les bovins. Annales de Parasitologie Humaine et Comparée 53, 421–430.10.1051/parasite/1978534421CrossRefGoogle Scholar
Baker, R.H. & DeSalle, R. (1997) Multiple sources of character information and the phylogeny of Hawaiian drosophilids. Systematic Biology 46, 654–673.CrossRefGoogle ScholarPubMed
Baker, R.H., Yu, X. & DeSalle, R. (1998) Assessing the relative contribution of molecular and morphological characters in simultaneous analysis trees. Molecular Phylogenetics and Evolution 9, 427–436.CrossRefGoogle ScholarPubMed
Bandi, C., Anderson, T.J.C., Genchi, C. & Blaxter, M.L. (1998) Phylogeny of Wolbachia in filarial nematodes. Proceedings of the Royal Society of London Series B–Biological Sciences 265, 2407–2413.CrossRefGoogle ScholarPubMed
Barker, F.K. & Lutzoni, F.M. (2002) The utility of the incongruence length difference test. Systematic Biology 51, 625–637.10.1080/10635150290102302CrossRefGoogle ScholarPubMed
Bossuyt, F. & Milinkovitch, M.C. (2001) Amphibians as indicators of early Tertiary ‘Out-of-India’ dispersal of vertebrates. Science 292, 93–95.CrossRefGoogle ScholarPubMed
Bremer, K. (1994) Branch support and tree stability. Cladistics 10, 295–304.CrossRefGoogle Scholar
Brooks, D.R. & McLennan, D.A. (1993) Parascript: parasites and the language of evolution. Washington DC Smithsonian Institution Press.Google Scholar
Burnham, G. (1998) Onchocerciasis. Lancet 351, 1341–1346.CrossRefGoogle ScholarPubMed
Bush, G.L. (1994) Sympatric speciation in animals: new wine in old bottles. Trends in Ecology and Evolution 9, 285–288.CrossRefGoogle ScholarPubMed
Casiraghi, M., Anderson, T.J.C., Bandi, C., Bazzochi, C. & Genchi, C. (2001) A phylogenetic analysis of filarial nematodes: comparison with the phylogeny of Wolbachia endosymbionts. Parasitology 122, 93–103.10.1017/S0031182000007149CrossRefGoogle ScholarPubMed
Casiraghi, M., Bain, O., Guerrero, R., Martin, C., Pocacqua, V., Gardner, S.L., Franceschi, A. & Bandi, C. (2004) Mapping the presence of Wolbachia pipientis on the phylogeny of filarial nematodes: evidence for symbiont loss during evolution. International Journal for Parasitology 34, 191–203.CrossRefGoogle ScholarPubMed
Chabaud, A.G. & Bain, O. (1994) The evolutionary expansion of the Spirurida. International Journal for Parasitology 24, 1179–1201.CrossRefGoogle ScholarPubMed
Copeman, D.B. (1993) Molecular variation in Onchocerca spp. Acta Tropica 53, 307–317.CrossRefGoogle ScholarPubMed
Crosskey, R.W. (1990) 711 pp. The natural history of blackflies. Chichester, John Wiley & Sons.Google Scholar
Cunningham, C.W. (1997a) Can three incongruence tests predict when data should be combined? Molecular Biology and Evolution 14, 733–740.CrossRefGoogle ScholarPubMed
Cunningham, C.W. (1997b) Is congruence between data partitions a reliable predictor of phylogenetic accuracy? Empirically testing an iterative procedure for choosing among phylogenetic methods. Systematic Biology 46, 464–478.10.1093/sysbio/46.3.464CrossRefGoogle ScholarPubMed
Darlu, P. & Lecointre, G. (2002) When does the incongruence length difference test fail? Molecular Biology and Evolution 19, 432–437.CrossRefGoogle ScholarPubMed
Dolphin, K., Belshaw, R., Orme, C.D. & Quicke, D.L. (2000) Noise and incongruence: interpreting results of the incongruence length difference test. Molecular Phylogenetics and Evolution 17, 401–406.10.1006/mpev.2000.0845CrossRefGoogle ScholarPubMed
Duke, B.O.L. (1990) Human onchocerciasis–an overview of the disease. Acta Leidensia 59, 9–24.Google ScholarPubMed
Eberhard, M.L., Ortega, Y., Dial, S., Schiller, C.A., Sears, A.W. & Greiner, E. (2000) Ocular Onchocerca infections in two dogs in western United States. Veterinary Parasitology 90, 333–338.CrossRefGoogle ScholarPubMed
Egyed, Z., Sréter, T., Széll, Z., Nyirö, G., Márialigeti, K. & Varga, I. (2002) Molecular phylogenetic analysis of Onchocerca lupi and its Wolbachia endosymbiont. Veterinary Parasitology 108, 153–161.CrossRefGoogle ScholarPubMed
Eichler, D.A. (1973) Studies on Onchocerca gutturosa and its development in Simulium ornatum. 4. Systematics of O. gutturosa . Journal of Helminthology 47, 89–96.CrossRefGoogle ScholarPubMed
Eichler, D.A. & Nelson, G.S. (1971) Studies on Onchocerca gutturosa (Neumann, 1910) and its development in Simulium ornatum (Meigen, 1818). I. Observations on, O. gutturosa in cattle in South-East England. Journal of Helminthology 45, 245–258.10.1017/S0022149X00007136CrossRefGoogle Scholar
Farias, I.P., Orti, G., Sampaio, I., Schneider, H. & Meyer, A. (2001) The cytochrome b gene as a phylogenetic marker: the limits of resolution for analyzing relationships among cichlid fishes. Journal of Molecular Evolution 53, 89–103.CrossRefGoogle ScholarPubMed
Farris, J.S. (1970) Methods for computing Wagner trees. Systematic Zoology 19, 83–92.CrossRefGoogle Scholar
Farris, J.S., Källersjö, S.M., Kluge, A.G. & Bult, C. (1994) Testing significance of incongruence. Cladistics 10, 315–319.CrossRefGoogle Scholar
Farris, J.S., Källersjö, S.M., Kluge, A.G. & Bult, C. (1995) Constructing a significance test for incongruence. Systematic Biology 44, 570–572.CrossRefGoogle Scholar
Felsenstein, J. (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. Journal of Molecular Evolution 17, 368–376.CrossRefGoogle ScholarPubMed
Felsenstein, J. (1985) Confidence limits on phylogenies: an approach using bootstrap. Evolution 39, 783–791.CrossRefGoogle ScholarPubMed
Flockhart, H.A. (1982) The identification of some Onchocerca spp. of cattle by isoenzyme analysis. Tropenmedizin und Parasitologie 33, 51–56.Google ScholarPubMed
Garate, T., Cabrera, Z., Copeman, D.B., Harnett, W., McLaren, D.J., Patterson, M. & Parkhouse, R.M. (1991) Surface antigens of male worms and microfilariae of Onchocerca gibsoni . International Journal for Parasitology 21, 37–45.CrossRefGoogle ScholarPubMed
Goldman, N. (1993) Statistical tests of models of DNA substitution. Journal of Molecular Evolution 36, 182–198.10.1007/BF00166252CrossRefGoogle ScholarPubMed
Hasegawa, M., Kishino, H. & Yano, T. (1985) Dating of the human–ape splitting by a molecular clock of mitochondrial DNA. Journal of Molecular Evolution 22, 160–174.10.1007/BF02101694CrossRefGoogle ScholarPubMed
Hoerauf, A., Buttner, D.W., Adjei, O. & Pearlman, E. (2003) Onchocerciasis. British Medical Journal 326, 207–210.CrossRefGoogle ScholarPubMed
Juste, J.B., Álvarez, Y., Tabarés, E., Garrido-Pertierra, A., Ibáñez, C. & Bautista, J.M. (1999) Phylogeography of African fruitbats (Megachiroptera). Molecular Phylogenetics and Evolution 13, 596–604.Google Scholar
Keddie, E.M., Higazi, T. & Unnasch, T.R. (1998) The mitochondrial genome of Onchocerca volvulus: sequence, structure and phylogenetic analysis. Molecular and Biochemical Parasitology 95, 111–127.CrossRefGoogle ScholarPubMed
Marshall, F. & Hildebrand, E. (2002) Cattle before crops: the beginnings of food production in Africa. Journal of World Prehistory 16, 99–143.10.1023/A:1019954903395CrossRefGoogle Scholar
McCoy, K.D. (2003) Sympatric speciation in parasites–what is sympatry? Trends in Parasitology 19, 400–404.CrossRefGoogle ScholarPubMed
Mickevich, M.F. & Farris, W.M. (1981) The implications of congruence in Menidia. Systematic Zoology 30, 351–370.CrossRefGoogle Scholar
Muller, R. (1979) Identification of Onchocerca. pp. 175–206 in 17th Symposium of the British Society for Parasitology (Eds) Problems in the identification of parasites and their vectors. Oxford, Blackwell.Google Scholar
Muller, R. (1983) Species recognition in human filarioids. pp. 339–349 in Stone, A.R., Platt, H.M. & Khalil, L.F. (Eds) Concepts in nematode systematics. London and New York, Academic Press.Google Scholar
Murray, M.G. & Thompson, W.F. (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Research 8, 4321–4325.CrossRefGoogle ScholarPubMed
Posada, D. & Crandall, K.A. (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14, 817–818.CrossRefGoogle ScholarPubMed
Post, R.J. McCall, P.J., Trees, A.J., Delves, C.J. & Kouyate, B. (1989) Chromosomes of six species of Onchocerca (Nematoda: Filarioidea). Tropical Medicine and Parasitology 40, 292–294.Google Scholar
Post, R.J., Bain, O. & Kläger, S. (1991) Chromosome numbers in Onchocerca dukei and O. tarsicola . Journal of Helminthology 65, 208–210.CrossRefGoogle ScholarPubMed
Rambaut, A. (1996) Se-Al: Sequence Alignment Editor. Available at http://evolve.zoo.ox.ac.uk/.Google Scholar
Shimodaira, H. & Hasegawa, M. (1999) Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Molecular Biology and Evolution 16, 1114–1116.CrossRefGoogle Scholar
Sorenson, M.D. (1999) TreeRot, version 2. Boston University, Boston, Massachusetts.Google Scholar
Steward, J.S. (1937) The occurrence of Onchocerca gutturosa Neumann in cattle in England, with an account of its life history and development in Simulium ornatum Mg. Parasitology 29, 212–219.CrossRefGoogle Scholar
Strimmer, K. & von Haeseler, A. (1996) Quartet Puzzling: a quartet Maximum-Likelihood method for reconstructing tree topologies. Molecular Biology and Evolution 13, 964–969.CrossRefGoogle Scholar
Strimmer, K. & von Haeseler, A. (1997) Likelihood-mapping: a simple method to visualize phylogenetic content of a sequence alignment. Proceedings of the National Academy of Sciences, USA 94, 6815–6819.CrossRefGoogle ScholarPubMed
Swofford, D.L. (2002) PAUP*: Phylogenetic Analysis Using Parsimony (and other methods), ver. 4.0b10. Sinauer, Sunderland.Google Scholar
Tajima, F. (1993) Simple methods for testing the molecular evolutionary clock hypothesis. Genetics 135, 599–607.CrossRefGoogle ScholarPubMed
Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F. & Higgins, D.G. (1997) The CLUSTAL X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 24, 4876–4882.10.1093/nar/25.24.4876CrossRefGoogle Scholar
Trees, A.J., Graham, S.P., Renz, A., Bianco, A.E. & Tanya, V. (2000) Onchocerca ochengi infections in cattle as a model for human onchocerciasis: recent developments. Parasitology 120, S133–142.CrossRefGoogle Scholar
Unnasch, T.R. & Williams, S.A. (2000) The genomes of Onchocerca volvulus . International Journal for Parasitology 30, 543–552.CrossRefGoogle ScholarPubMed
Vankan, D.M., Copeman, D.B. & Novak, M. (1988) An evaluation of implanted male Onchocerca gibsoni in mice as a screen for macrofilaricides against Onchocerca volvulus . Tropical Medicine and Parasitology 39 (Suppl.4), 472–474.Google ScholarPubMed
Xie, H., Bain, O. & Williams, S.A. (1994) Molecular phylogenetic studies on filarial parasites based on 5S ribosomal spacer sequences. Parasite 1, 141–151.CrossRefGoogle ScholarPubMed
Zimmerman, P.A., Katholi, C.R., Wooten, M.C., Lang-Unnasch, N. & Unnasch, T.R. (1994) Recent evolutionary history of American Onchocerca volvulus, based on analysis of a tandemly repeated DNA sequence family. Molecular Biology and Evolution 11, 384–392.Google ScholarPubMed