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Insight into species diversity of the Trichostrongylidae Leiper, 1912 (Nematoda: Strongylida) in ruminants

Published online by Cambridge University Press:  08 December 2015

A. Wyrobisz ,
J. Kowal  and
P. Nosal
A. Wyrobisz
Affiliation:
Department of Environmental Zoology, Institute of Animal Sciences, University of Agriculture in Krakow, Mickiewicza av. 24/28, 30-059Krakow, Poland
J. Kowal*
Affiliation:
Department of Environmental Zoology, Institute of Animal Sciences, University of Agriculture in Krakow, Mickiewicza av. 24/28, 30-059Krakow, Poland
P. Nosal
Affiliation:
Department of Environmental Zoology, Institute of Animal Sciences, University of Agriculture in Krakow, Mickiewicza av. 24/28, 30-059Krakow, Poland
*
*Fax: +48-12-6624053 E-mail: j.kowal@ur.krakow.pl
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Abstract

This paper focuses on the species diversity among the Trichostrongylidae Leiper, 1912 (Nematoda: Strongylida), and complexity of the family systematics. Polymorphism (subfamilies: Ostertagiinae, Cooperiinae and Haemonchinae), the presence of cryptic species (genus: Teladorsagia) and hybridization (genera: Cooperia, Haemonchus and Ostertagia) are presented and discussed, considering both morphological and molecular evidence. Some of these phenomena are common, nevertheless not sufficiently understood, which indicates the need for expanding the current state of knowledge thereof. Within the Trichostrongylidae, species distinction supported merely by morphological features is difficult, and requires confirmation by means of molecular methods. The parasitic nematode taxonomy is complicated mainly by the genus Teladorsagia, but complexity may also be expected among other Ostertagiinae (e.g. in the genera Ostertagia and Marshallagia). The data presented here show that the members of the Trichostrongylidae can significantly complicate unambiguous species identification. Hence, it is essential to consider the phenomena mentioned, to gather valid and comparable data on the biodiversity of this family.

Type
Review Article
Information
Journal of Helminthology , Volume 90 , Issue 6 , November 2016 , pp. 639 - 646
Copyright
Copyright © Cambridge University Press 2015 

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References

Achi, Y.L., Zinsstag, J., Yai, K., Yeo, N., Dorchies, P. & Jacquiet, P. (2003) Host specificity of Haemonchus spp. for domestic ruminants in the savanna in northern Ivory Coast. Veterinary Parasitology 16, 151–158.Google Scholar
Akkari, H., Jebali, J., Gharbi, M., Mhadhbi, M., Awadi, S. & Darghouth, M.A. (2013) Epidemiological study of sympatric Haemonchus species and genetic characterization of Haemonchus contortus in domestic ruminants in Tunisia. Veterinary Parasitology 193, 118–125.Google Scholar
Amarante, A.F., Bagnola, J. Jr, Amarante, M.R. & Barbosa, M.A. (1997) Host specificity of sheep and cattle nematodes in Sao Paulo state, Brazil. Veterinary Parasitology 73, 89–104.Google Scholar
Anderson, R.C. (2000) Nematode parasites of vertebrates: Their development and transmission. 2nd edn. Wallingford, CABI Publishing.Google Scholar
Andrews, R.H. & Beveridge, I. (1990) Apparent absence of genetic differences among species of Teladorsagia (Nematoda: Trichostrongylidae). Journal of Helminthology 6, 290–294.CrossRefGoogle Scholar
Becklund, W.W. & Walker, M.L. (1971) Nomenclature and morphology of Ostertagia trifurcata Ransom 1970, with data on spicule lengths of five stomach worms of ruminants. Journal of Parasitology 57, 508–516.CrossRefGoogle Scholar
Beech, R.N., Prichard, R.K. & Scott, M.E. (1994) Genetic variability of the beta-tubulin genes in benzimidazole-susceptible and -resistant strains of Haemonchus contortus . Genetics 130, 103–110.Google Scholar
Bickford, D., Lohman, D.J., Sodhi, N.S., Ng, P.K.L., Meier, R., Winker, K., Ingram, K.K. & Das, I. (2006) Cryptic species as a window on diversity and conservation. Trends in Ecology and Evolution 22, 148–155.Google Scholar
Blouin, M.S. (2002) Molecular prospecting for cryptic species of nematodes: mitochondrial DNA versus internal transcribed spacer. International Journal for Parasitology 32, 527–531.Google Scholar
Blouin, M.S., Yowell, C.A., Courtney, C.H. & Dame, J.B. (1995) Host movement and the genetic structure of populations of parasitic nematodes. Genetics 141, 1007–1014.Google Scholar
Blouin, M.S., Liu, J. & Berry, R.E. (1999) Life cycle variation and the genetic structure of nematode populations. Heredity 83, 253–259.Google Scholar
Braisher, T.L., Gemmel, N.J., Grenfell, B.T. & Amos, W. (2004) Host isolation and patterns of genetic variability in three populations of Teladorsagia from sheep. International Journal for Parasitology 34, 1197–1204.Google Scholar
Brasil, B.S., Nunes, R.L., Bastianetto, E., Drummond, M.G., Carvalho, D.C., Leite, R.C., Molento, M.B. & Oliviera, D.A. (2012) Genetic diversity patterns of Haemonchus placei and Haemonchus contortus populations isolated from domestic ruminants in Brazil. International Journal for Parasitology 42, 469–479.CrossRefGoogle ScholarPubMed
Cabaret, J., Morales, G. & Gruner, L. (1984) Characterization of Teladorsagia circumcincta and T. trifurcata. I. Epidemiological and biological aspects. Annales de Parasitologie Humaine et Comparée 59, 607–617.Google Scholar
Chaudhry, U., Miller, M., Yazwinski, T., Kaplan, R. & Gilleard, J. (2014a) The presence of benzimidazole resistance mutations in Haemonchus placei from US cattle. Veterinary Parasitology 29, 411–415.CrossRefGoogle Scholar
Chaudhry, U., Redman, E.M., Abbas, M., Raman, M. & Ashraf, K. (2014b) Genetic evidence for hybridization between Haemonchus contortus and Haemonchus placei in natural field populations and its implications for interspecies transmission of anthelmintic resistance. International Journal for Parasitology 45, 149–159.Google Scholar
Copland, J.W. (1965) Establishment of a pure infection of the nematode Ostertagia circumcincta in the sheep. Nature 208, 1129–1130.Google Scholar
Craig, B.H., Pilkington, J.G. & Pemberton, J.M. (2006) Gastrointestinal nematode species burdens and host mortality in a feral sheep population. Parasitology 133, 485–496.Google Scholar
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
Dallas, J.F., Irvine, R.J. & Halvorsen, O. (2000) DNA evidence that Ostertagia gruehneri and Ostertagia arctica (Nematoda: Ostertagiinae) in reindeer from Norway and Svalbard are conspecific. International Journal for Parasitology 30, 655–658.Google Scholar
Dallas, J.F., Irvine, R.J. & Halvorsen, O. (2001) DNA evidence that Marshallagia marshalli Ransom, 1907 and M. occidentalis Ransom, 1907 (Nematoda: Ostertagiinae) from Svalbard reindeer are conspecific. Systematic Parasitology 50, 101–103.Google Scholar
Daskalov, P.B. (1971) Haemonchus contortus: genetically determined polymorphism in females. Experimental Parasitology 29, 351–366.CrossRefGoogle ScholarPubMed
Daskalov, P.B. (1974) On the reproductive relationships between Ostertagia circumcincta, Teladorsagia davtiani and O. trifurcata (Nematoda, Trichostrongylidae). Izvestya na Tsentralnata Khelmintologicgna Laboratoriya 17, 59–72.Google Scholar
Dróżdz, J. (1965) Studies on helminths and helminthiases in Cervidae . Acta Parasitologica Polonica 13, 445–481.Google Scholar
Dróżdż, J. (1979) Genetic isolation as a criterion for defining a species within the parasitic nematodes. Wiadomości Parazytologiczne 25, 171–183.Google Scholar
Dróżdż, J. (1995) Polymorphism in the Ostertagiinae (Lopez-Neyra, 1947) and comments on the systematics of these nematodes. Systematic Parasitology 32, 91–99.Google Scholar
Dróżdż, J. (2000) Influence of the migration of animals on formatting of their parasitofauna. Medycyna Weterynaryjna 56, 154–157.Google Scholar
Dróżdż, J. & Dudziński, W. (1993) Changes in the intensity of infection of the roe deer, Capreolus capreolus (L.), with abomasum nematodes in relation to host density in a hunting ground. Acta Parasitologica 38, 29–32.Google Scholar
Dróżdż, J., Lachowicz, J., Demiaszkiewicz, A.W. & Sulgostowska, T. (1987) Abomasum nematodes in field and forest roe deer Capreolus capreolus (L.) over the yearly cycle. Acta Parasitologica Polonica 32, 339–348.Google Scholar
Dróżdż, J., Demiaszkiewicz, A.W. & Lachowicz, J. (1992) The helminth fauna of the roe deer Capreolus capreolus (L.) in a hunting area inhabited by red deer, elk and European bison (Borecka Forest, Poland) over the yearly cycle. Acta Parasitologica 37, 83–88.Google Scholar
Ford, E.B. (1953) The genetics of polymorphism in the Lepidoptera. Advances in Genetics 5, 43–87.Google Scholar
Gasbarre, L.C., Smith, L.L., Hoberg, E.P. & Pilitt, P.A. (2009a) Further characterization of a cattle nematode population with demonstrated resistance to current anthelmintics. Veterinary Parasitology 166, 275–280.Google Scholar
Gasbarre, L.C., Smith, L.L., Lichtenfels, J.R. & Pilitt, P.A. (2009b) The identification of cattle nematode parasites resistant to multiple classes of anthelmintics in a commercial cattle population in the US. Veterinary Parasitology 166, 281–285.Google Scholar
Gasnier, N. & Cabaret, J. (1996) Evidence for the existence of a sheep and a goat line of Teladorsagia circumcincta (Nematoda). Parasitology Research 82, 546–550.CrossRefGoogle Scholar
Gasnier, N., Cabaret, J. & Suarez, V. (1993) Species and morphs in the Ostertagiinae: an allozyme study of seven species. International Journal for Parasitology 23, 765–770.CrossRefGoogle ScholarPubMed
Gasnier, N., Cabaret, J. & Durette, D. (1997) Sheep and goat lines of Teladorsagia circumcincta (Nematoda): from allozyme to morphological identification. Journal of Parasitology 83, 527–529.Google Scholar
Gibbons, L.M. (1979) Revision of the genus Haemonchus Cobb, 1898 (Nematoda: Trichostrongylidae). Systematic Parasitology 1, 3–24.Google Scholar
Gibbons, L.M. & Khalil, L.F. (1982) A key for the identification of genera of the nematode family Trichostrongylidae Leiper, 1912. Journal of Helminthology 56, 185–233.CrossRefGoogle ScholarPubMed
Grillo, V., Jackson, F., Cabaret, J. & Gilleard, J.S. (2007) Population genetic analysis of the ovine parasitic nematode Teladorsagia circumcincta and evidence for a cryptic species. International Journal for Parasitology 37, 435–447.CrossRefGoogle ScholarPubMed
Grillo, V., Craig, B.H., Wimmer, B. & Gilleard, J.S. (2008) Microsatellite genotyping supports the hypothesis that Teladorsagia davtiani and Teladorsagia trifurcata are morphotypes of Teladorsagia circumcincta . Molecular and Biochemical Parasitology 159, 59–63.Google Scholar
Hoberg, E.P., Monsen, K.J., Kutz, S. & Blouin, M.S. (1999) Structure, biodiversity, and historical biogeography of nematode fauna in holarctic ruminants: morphological and molecular diagnoses of Teladorsagia boreoarcticus n. sp. (Nematoda: Ostertaginae), a dimorphic cryptic species in muskoxen (Ovibos moschatus). Journal of Parasitology 85, 910–934.Google Scholar
Hoberg, E.P., Lichtenfels, J.R. & Gibbons, L. (2004) Phylogeny for species of Haemonchus (Nematoda: Trichostrongyloidea): considerations of their evolutionary history and global biogeography among Camelidae and Pecora (Artiodactyla). Journal of Parasitology 90, 1085–1102.Google Scholar
Hoberg, E.P., Abrams, A. & Pilitt, P.A. (2009) Robustostrongylus aferensis gen. nov. et sp. nov. (Nematoda: Trichostrongyloidea) in kob (Kobus kob) and hartebeest (Alcelaphus buselaphus jacksoni) (Artiodactyla) from Sub-saharan Africa, with further ruminations on the Ostertagiinae. Journal of Parasitology 95, 702–717.Google Scholar
Hoberg, E.P., Abrams, A., Pilitt, P.A. & Kutz, S.J. (2012a) Discovery and description of the ‘davtiani’ morphotype for Teladorsagia boreoarcticus (Trichostrongylidae: Ostertagiinae) abomasal parasites in muskoxen, Ovibos moschatus, and caribou, Rangifer tarandus, from the North American Arctic: implications for parasite faunal diversity. Journal of Parasitology 98, 355–364.Google Scholar
Hoberg, E.P., Abrams, A., Pilitt, P.A. & Jenkins, E.J. (2012b) Discovery and description of a new trichostrongyloid species (Nematoda: Ostertagiinae), abomasal parasites in mountain goat, Oreamnos americanus, from the Western Cordillera of North America. Journal of Parasitology 98, 817–846.Google Scholar
Hoberg, E.P., Agosta, S.J., Boeger, W.A. & Brooks, D.R. (2015) An integrated parasitology: revealing the elephant through tradition and invention. Trends in Parasitology 31, 128–133.Google Scholar
Hogg, R., Whitaker, K., Collins, R., Holmes, P., Mitchell, S., Anscombe, J., Redman, L. & Gilleard, J. (2010) Haemonchosis in large ruminants in the UK. Veterinary Record 166, 373–374.Google Scholar
Humbert, J.F. & Cabaret, J. (1995) Use of random amplified polymorphic DNA for identification of ruminant trichostrongylid nematodes. Parasitology Research 81, 1–5.Google Scholar
Isenstein, R.S. (1971a) The polymorphic relationship of Cooperia oncophora (Railliet 1898) Ransom 1907, to Cooperia surnabada Antipin 1931 (Nematoda: Trichostrongylidae). Journal of Parasitology 57, 316–319.CrossRefGoogle ScholarPubMed
Isenstein, R.S. (1971b) Hybridization of two species of nematodes parasitic in ruminants, Cooperia oncophora (Railliet 1898) Ransom 1907, and Cooperia pectinata Ransom 1907. Journal of Parasitology 57, 320–326.Google Scholar
Jacquiet, P., Cabaret, J., Thiam, E. & Cheikh, D. (1998) Experimental and natural Haemonchus spp. cross infections of domestic ruminants in Sahelian West Africa. Annals of the New York Academy of Sciences 849, 465–469.Google Scholar
Kutz, S.J., Ducrocq, J., Verocai, G.G., Hoar, B.M., Colwell, D.D., Beckmen, K.B., Polley, L., Elkin, B. & Hoberg, E.P. (2012) Parasites in ungulates of Arctic North America and Greenland: a view of contemporary diversity, ecology, and impact in a world under change. Advances of Parasitology 70, 124–127.Google Scholar
Kuznetsov, D.N. (2011) Taxonomic revision of the genus Orloffia (Nematoda: Ostertagiinae) based on an ITS2 rDNA study. Biology Bulletin 38, 608–614.Google Scholar
Lancaster, M.B. & Hong, C. (1971) The nematode fauna of the Chillingham Wild White cattle. British Veterinary Journal 127, 113–117.CrossRefGoogle ScholarPubMed
Lancaster, M.B. & Hong, C. (1981) Polymorphism in nematodes. Systematic Parasitology 3, 29–31.Google Scholar
Lancaster, M.B. & Hong, C. (1990) The identification of females within the subfamily Ostertagiinae Lopez-Neyra 1947. Veterinary Parasitology 35, 21–27.Google Scholar
Leignel, V. & Humbert, J.F. (2001) Mitochondrial DNA variation in benzimidazole-resistant and -susceptible populations of the small ruminant parasite Teladorsagia circumcincta . Journal of Heredity 92, 503–506.Google Scholar
Leignel, V., Cabaret, J. & Humbert, J.F. (2002) New molecular evidence that Teladorsagia circumcincta (Nematoda: Trichostrongylidea) is a species complex. Journal of Parasitology 88, 135–140.Google Scholar
Le Jambre, L.F. (1977) Genetics of vulvar morph types in Haemonchus contortus: Haemonchus contortus cayugensis from the Finger Lakes region of New York. International Journal for Parasitology 7, 9–14.Google Scholar
Le Jambre, L.F. (1979) Hybridization studies of Haemonchus contortus (Rudolphi, 1803) and H. placei (Place, 1893) (Nematoda: Trichostrongylidae). International Journal for Parasitology 9, 455–463.Google Scholar
Le Jambre, L.F. (1981) Hybridization of Australian Haemonchus placei (Place, 1893), Haemonchus contortus cayugensis (Das & Whitlock, 1960) and Haemonchus contortus (Rudolphi, 1803) from Louisiana. International Journal for Parasitology 11, 323–330.Google Scholar
Le Jambre, L.F. & Royal, W.M. (1980) Meiotic abnormalities in backcross lines of hybrid Haemonchus . International Journal for Parasitology 10, 281–286.CrossRefGoogle ScholarPubMed
Lichtenfels, J.R. & Hoberg, E.P. (1993) The systematics of nematodes that cause osteragiasis in domestic and wild ruminants in North America: an update and a key to species. Veterinary Parasitology 46, 33–53.Google Scholar
Lichtenfels, J.R. & Pilitt, P.A. (1989) Cuticular ridge patterns of Marshallagia marshalli and Ostertagia occidentalis (Nematoda: Trichostrongylidae) parasitic in ruminants of North America. Proceedings of the Helminthological Society of Washington 56, 171–182.Google Scholar
Lichtenfels, J.R. & Pilitt, P.A. (1991) A redescription of Ostertagia bisonis (Nematoda: Trichostrongyloidea) and a key to species of Ostertagiinae with a tapering lateral synlophe from domestic ruminants in North America. Journal of the Helminthological Society of Washington 58, 231–244.Google Scholar
Lichtenfels, J.R., Pilitt, P.A. & Lancaster, M.B. (1988a) Cuticular ridge patterns of seven species of Ostertagiinae (Nematoda) parasitic in domestic ruminants. Proceedings of the Helminthological Society of Washington 55, 77–86.Google Scholar
Lichtenfels, J.R., Pilitt, P.A. & Lancaster, M.B. (1988b) Systematic of the nematodes that cause ostertaginasis in cattle, sheep and goats in North America. Veterinary Parasitology 27, 3–12.Google Scholar
Lichtenfels, J.R., Pilitt, P.A. & Fruetel, M. (1990) Cuticular ridge pattern in Ostertagia gruehneri and Ostertagia arctica (Nematode: Trichostrongylidea) from caribou, Rangifer tarandus . Journal of the Helminthological Society of Washington 57, 61–68.Google Scholar
Lichtenfels, J.R., Pilitt, P.A. & Hoberg, E.P. (1994) New morphological characters for identifying individual specimens of Haemonchus spp. (Nematoda: Trichostrongyloidea) and a key to species of ruminants of North America. Journal of Parasitology 80, 107–119.Google Scholar
Lichtenfels, J.R., Hoberg, E.P. & Zarlenga, D.S. (1997) Systematics of gastrointestinal nematodes of domestic ruminants: advances between 1992 and 1995 and proposals for future research. Veterinary Parasitology 72, 225–245.Google Scholar
Lienard, E., Depaquit, J. & Ferte, H. (2006) Spiculopteragia mathevossiani Ruchliadev, 1948 is the minor morph of Spiculopteragia spiculoptera (Gushanskaya, 1931): molecular evidence. Veterinary Research 37, 683–694.Google Scholar
Santin-Duran, M., de la Feuente, C., Alunda, J.M., Rosenthal, B.M. & Hoberg, E.P. (2002) Identical ITS-1 and ITS-2 sequences suggest Spiculopteragia asymmetrica and Spiculopteragia quadrispiculata (Nematoda: Trichostrongylidae) constitute morphologically distinct variants of a single species. Journal of Parasitology 88, 417–418.CrossRefGoogle ScholarPubMed
Stevenson, L.A., Gasser, R.B. & Chilton, N.B. (1996) The ITS-2 rDNA of Teladorsagia circumcincta, T. trifurcata and T. davtiani (Nematoda: Trichostrongylidae) indicates that these taxa are one species. International Journal for Parasitology 26, 1123–1126.Google Scholar
Suarez, V.H. & Cabaret, J. (1991) Similarities between species of the Ostertagiinae (Nematoda: Trichostrongylidea) in relation to host-specificity and climatic environment. Systematic Parasitology 20, 179–185.Google Scholar
Suarez, V.H. & Cabaret, J. (1992) Interbreeding in the subfamily Ostertagiinae (Nematoda: Trichostrongylidae) of ruminants. Journal of Parasitology 78, 402–405.Google Scholar
Suarez, V.H., Durette-Desset, M.C. & Cabaret, J. (1993) Description of Ostertagia ostertagi and Ostertagia leptospicularis hybrids in experimentally infected sheep. Journal of Parasitology 79, 874–878.CrossRefGoogle ScholarPubMed
Sultan, K., Omar, M., Makouloutou, P., Kaneshiro, Y., Saita, E., Yokoyama, M., Suzuki, K., Hosoi, E. & Sato, H. (2014) Molecular genetic conspecificity of Spiculopteragia houdemeri (Schwartz, 1926) and S. andreevae (Dróżdż, 1965) (Nematoda: Ostrtagiinae) from wild ruminants in Japan. Journal of Helminthology 88, 1–12.Google Scholar
Zarlenga, D.S., Hoberg, E.P., Stringfellow, F. & Lichtenfels, J.R. (1998) Comparisons of two polymorphic species of Ostertagia and phylogenetic relationships within the Ostertagiinae (Nematoda: Trichostrongylidae) inferred from ribosomal DNA repeat and mitochondrial DNA sequences. Journal of Parasitology 84, 806–812.Google Scholar