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The phylogenetic relationships of endemic Australasian trichostrongylin families (Nematoda: Strongylida) parasitic in marsupials and monotremes

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Abstract

The phylogenetic relationships of the endemic (or largely endemic) Australasian trichostrongylin nematode families Herpetostrongylidae, Mackerrastrongylidae and Nicollinidae as well as endemic trichostrongylin nematodes currently placed in the families Trichostrongylidae and Molineidae were examined using the complete large subunit (28S) ribosomal RNA gene. The Herpetostrongylinae proved to be monophyletic. However, representatives of the Nicollinidae nested with the Herpetostrongylinae. The Mackerrastrongylidae was also a monophyletic group and included Peramelistrongylus, currently classified within the Trichostrongylidae. The Globocephaloidinae, currently considered to be a subfamily of the Herpetostrongylidae, was excluded from the family in the current analysis. Ollulanus and Libyostrongylus, included for the first time in a molecular phylogenetic analysis, were placed within the Trichostrongylidae. This study provided strong support for the Herpetostrongylidae (including within it the Nicollinidae, but excluding the Globocephaloidinae) and the Mackerrastrongylidae as monophyletic assemblages. Additional studies are required to resolve the relationships of the remaining endemic Australasian trichostrongylin genera.

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References

  • Audebert F, Chilton N, Justine J-L, Gallut C, Tiller A, Durette-Desset M-C (2005) Additional molecular evidence to support a sister taxon relationship between Heligmosomoidea and Molineoidea nematodes (Trichostrongylina). Parasitol Res 96:343–346

    Article  CAS  PubMed  Google Scholar 

  • Beveridge I (1979) A review of the Globocephaloidinae Inglis (Nematoda: Amidostomatidae) from macropodid marsupials. Aust J Zool 27:151–175

    Article  Google Scholar 

  • Beveridge I, Durette-Desset M-C (1986) New species of Austrostrongylus Chandler, 1924 (Nematoda: Trichostrongyloidea) from Australian marsupials, with a re-description of A. minutus Johnston & Mawson, 1938, and description of a new genus, Sutarostrongylus. Bull Mus nat Hist nat, Paris, 4e sér 8: 781–790

  • Beveridge I, Durette-Desset M-C (2009) A new species of the nematode genus Copemania (Nematoda: Trichostrongylida), parasitic in the western quoll, Dasyurus geoffroii and short-nosed bandicoot, Isoodon obesulus from south-western Western Australia. Rec W Aust Mus 25:345–349

    Google Scholar 

  • Beveridge I, Durette-Desset M-C (2010) Two new species of Filarinema Moennig, 1929 (Nematoda: Trichostrongylina) parasitic in macropodid marsupials. Trans R Soc S Aust 134:164–171

    Google Scholar 

  • Beveridge I, Spratt DM (1996) The helminth parasites of Australasian marsupials: origins and evolutionary biology. Adv Parasitol 37:136–254

    Google Scholar 

  • Beveridge I, Spratt DM, Durette-Desset M-C (2014) Order Strongylida (Railliet & Henry, 1913). In: Schmidt-Rhaesa, A. (ed) Handbook of Zoology. Gastrotricha, Cycloneuralia and Gnathifera. Vol 2. Nematoda. De Gruyter, Berlin, pp 557–612.

  • Cassone J, Durette-Desset M-C, Presidente PJA (1986) Nouvelle hypothèse sur l’évolution des Herpetostrongylinae (Nematoda, Trichostrongyloidea) parasites de marsupiaux australiens. Bull Mus nat Hist nat, Paris, 4e sér, 8: 267–283

  • Chilton NB, Hoste H, Newton LA, Beveridge I, Gasser RB (1998) Common secondary structure for the second internal transcribed spacer pre-rRNA of two subfamilies of trichostrongylid nematodes. Int J Parasitol 28:1765–1773

    Article  CAS  PubMed  Google Scholar 

  • Chilton NB, Newton LA, Beveridge I, Gasser RB (2001) Evolutionary relationships of trichostrongyloid nematodes (Strongylida) inferred from ribosomal DNA sequence data. Mol Phyl Evol 19:367–386

    Article  CAS  Google Scholar 

  • Chilton NB, Huby-Chilton F, Gasser RB (2003) First complete large subunit rRNA sequence and secondary structure for a parasitic nematode: phylogenetic and diagnostic implications. Mol Cell Probes 17:33–39

    Article  CAS  PubMed  Google Scholar 

  • Chilton NB, Huby-Chilton F, Gasser RB, Beveridge I (2006) The evolutionary origins of nematodes within the order Strongylida are related to predilection sites within hosts. Mol Phyl Evol 40:118–128

    Article  CAS  Google Scholar 

  • Durette-Desset M-C (1980) Nouveaux nématodes trichostrongyloïdes parasites de sauriens en Malaysie et à Bornéo. Bull Mus nat Hist nat, Paris, 4e sér, 2: 697–706

  • Durette-Desset M-C (1983) Keys to genera of the superfamily Trichostrongyloidea. In: Anderson, R.C., & Chabaud, A.G. (eds) CIH keys to the nematode parasites of vertebrates. No.10. Farnham Royal; Commonwealth Agricultural Bureaux, pp 1–68

  • Durette-Desset M-C (1985) Trichostrongyloid nematodes and their vertebrate hosts: reconstruction of the phylogeny of a parasitic group. Adv Parasitol 24:239–306

    Article  CAS  PubMed  Google Scholar 

  • Durette-Desset M-C, Beveridge I (1981) Peramelistrongylus Mawson, 1960 et Profilarinema n. gen., nematodes trichostrongyloides paraissant faire transition entre les Strongyloidea et le genre atypique Filarinema Mönnig, 1929. Ann Parasitol Hum Comp 56:183–191

    Google Scholar 

  • Durette-Desset M-C, Beveridge I (2012) Redescriptions and descriptions of new species of Austrostrongylus Chandler, 1924 (Nematoda: Trichostrongylina), from Australian marsupials with a comparative study of features of the synlophe. Zootaxa 3512:1–41

    Google Scholar 

  • Durette-Desset M-C, Cassone J (1980) Mackerrastrongylus Mawson, 1960, et Sprattellus n.gen. (Nematoda, Trichostrongyloidea) parasites de Perameloidea et de Dasyuroidea (Marsupiaux australiens). Bull Mus nat Hist nat, Paris, 4e sér, 4: 943–954

  • Durette-Desset M-C, Cassone J (1983) A taxonomic revision of the trichostrongyloid nematode parasites of the echidna, Tachyglossus aculeatus (Monotremata). Aust J Zool 31:257–284

    Article  Google Scholar 

  • Durette-Desset M-C, Chabaud AG (1981) Nouvel essai de classification des nematodes Trichostrongyloidea. Ann Parasitol Hum Comp 56:297–312

    CAS  PubMed  Google Scholar 

  • Durette-Desset M-C, Chabaud AG (1993) Nomenclature des Strongylida au-dessus du groupe-famille. Ann Parasitol Hum Comp 68:111–112

    CAS  PubMed  Google Scholar 

  • Durette-Desset M-C, Hugot JP, Darlu P, Chabaud AG (1999) A cladistic analysis of the Trichostrongyloidea (Nematoda). Int J Parasitol 29:1065–1086

    Article  CAS  PubMed  Google Scholar 

  • Fazenda I, Gasser RB, Carvalho L, Beveridge I (2010) Resurrection and redescription of Globocephaloides wallabiae Johnston et Mawson, 1939 (Nematoda: Trichostrongyloidea) from macropodid marsupials in north-eastern Australia. Acta Parasitol 55:138–143

    Article  Google Scholar 

  • Fuller S, Baverstock P, King D (1998) Biogeographic origins of goannas (Varanidae): a molecular perspective. Mol Phyl Evol 9:294–307

    Article  CAS  Google Scholar 

  • Gasser RB, Hu M, Chilton NB, Campbell BE, Jex AJ, Otranto D, Cafarchia C, Beveridge I, Zhu X (2006) Single-strand conformation polymorphism (SSCP) for the analysis of genetic variation. Nat Protoc 1(6):3121–3128

  • Gouÿ de Bellocq J, Ferté H, Depaquit J, Justine J-L, Tiller A, Durette-Desset M-C (2001) Phylogeny of the Trichostrongylina (Nematoda) inferred from 28S rDNA sequences. Mol Phyl Evol 19:430–442

    Article  Google Scholar 

  • Humphery-Smith I (1983) An hypothesis on the evolution of the Herpetostrongylinae (Trichostrongyloidea: Nematoda) in Australian marsupials, and their relationships with Viannaidae, parasites of South American marsupials. Aust J Zool 31:931–942

    Article  Google Scholar 

  • Inglis WG (1968) The geographical and evolutionary relationships of Australian trichostrongyloid parasites and their hosts. J Linn Soc (Zool) 47:327–347

    Article  Google Scholar 

  • Mackerras MJ (1958) Catalogue of Australian mammals and their recorded internal parasites. Proc Linn Soc N S Wales 83:101–160

    Google Scholar 

  • Metcalfe I (2002) Tectonic history of the south-east Asian-Australian region. In: Kershaw P, David B, Tapper N, Penny D, Brown J (eds). Bridging Wallace’s Line: the environmental and cultural history and dynamics of the south-east Asian- Australian region. Adv Geoecol 34: 29–48

  • Newton LA, Chilton NB, Beveridge I, Gasser RB (1998a) Genetic evidence indicating that Cooperia surnabada and Cooperia oncophora are one species. Int J Parasitol 28:331–336

    Article  CAS  PubMed  Google Scholar 

  • Newton LA, Chilton NB, Beveridge I, Gasser RB (1998b) Differences in the second internal transcribed spacer of four species of Nematodirus (Nematoda: Molineidae). Int J Parasitol 28:337–341

    Article  CAS  PubMed  Google Scholar 

  • Obendorf DL (1979) The helminth parasites of Rattus fuscipes (Waterhouse) from Victoria, including description of two new nematode species. Aust J Zool 27:867–879

    Article  Google Scholar 

  • Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25(7):1253–1256

  • Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818

    Article  CAS  PubMed  Google Scholar 

  • Rawlings LH, Rabosky DL, Donnellan SC, Hutchinson MN (2008) Python phylogenetics; inference from morphology and mitochondrial DNA. Biol J Linn Soc 93:603–619

    Article  Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MrBayes 3: bayesian phylogenetic inference under mixed models. Bioinformatics 19(12):1572–1574

  • Rowe KC, Reno ML, Richmond DM, Adkins RM, Steppan SJ (2008) Pliocene colonization and adaptive radiations in Australian and New Guinea (Sahul): multilocus systematics of the old endemic rodents. Mol Phyl Evol 47:84–101

    Article  CAS  Google Scholar 

  • Scheibel RP, Catzfelis F, Jiménez FA (2014) The relationships of the marsupial-dwelling Viannaiidae and description of Travassostrongylus scheibelorum n.sp. (Trichostrongylina: Heligmosomoidea), from mouse opossums (Didelphidae) from French Guiana. Folia Parasitol 61:242–254

    Article  CAS  PubMed  Google Scholar 

  • Smales LR (1997) A review of the helminth parasites of Australian rodents. Aust J Zool 45:502–521

    Article  Google Scholar 

  • Spratt DM, Beveridge I, Walter EL (1991) A catalogue of Australasian monotremes and marsupials and their recorded helminth parasites. Rec S Aust Mus, Monogr Ser 1:1–105

    Google Scholar 

  • Stevenson LA, Gasser RB, Chilton NB (1996) The ITS-2 rDNA of Teladorsagia circumcincta, T. trifurcata and T. davtiani (Nematoda: Trichostrongylidae) indicates that these taxa are one species. Int J Parasitol 26:1123–1126

    Article  CAS  PubMed  Google Scholar 

  • Swofford DL (1999) PAUP: Phylogenetic Analysis Using Parsimony, version 4.0b2. Computer program distributed by Sinauer Associates, Inc. Publishers, Sunderand, Massachusetts

  • Talavera G, Castresana J (2007) Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol 56:564–577

    Article  CAS  PubMed  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL-X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucl Acids Res 25:4876–4882

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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Acknowledgments

We wish to thank the Australian Research Grants Council and the Australian Biological Resources Study for financial support.

Compliance with ethical standards

All legal requirements were fulfilled in the collection of the parasite specimens used in this study. The only specimens which required specific permits for collection were covered by the following permits: RP-91-095 (1995) from the Victorian Department of Conservation and Environment and permits 10000019 (1998) and 10000434 (1999) from the Victorian Department of Natural Resources and Environment.

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The authors declare that they have no competing interests.

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Correspondence to Neil B. Chilton.

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Chilton, N.B., Huby-Chilton, F., Koehler, A.V. et al. The phylogenetic relationships of endemic Australasian trichostrongylin families (Nematoda: Strongylida) parasitic in marsupials and monotremes. Parasitol Res 114, 3665–3673 (2015). https://doi.org/10.1007/s00436-015-4594-9

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  • DOI: https://doi.org/10.1007/s00436-015-4594-9

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