Hostname: page-component-745bb68f8f-s22k5 Total loading time: 0 Render date: 2025-01-11T04:22:09.156Z Has data issue: false hasContentIssue false
  • English
  • Français

Speciation in the genus Cloacina (Nematoda: Strongylida): species flocks and intra-host speciation

Published online by Cambridge University Press:  12 July 2017

N. B. CHILTON ,
M. A. SHUTTLEWORTH ,
F. HUBY-CHILTON ,
A. V. KOEHLER ,
A. JABBAR Open the ORCID record for A. JABBAR [Opens in a new window] ,
R. B. GASSER  and
I. BEVERIDGE
N. B. CHILTON
Affiliation:
Department of Biology, University of Saskatchewan, Saskatoon, Saskatchewan, Canada
M. A. SHUTTLEWORTH
Affiliation:
Faculty of Veterinary and Agricultural Sciences, The University of Melbourne, Parkville, Victoria, Australia
F. HUBY-CHILTON
Affiliation:
Faculty of Veterinary and Agricultural Sciences, The University of Melbourne, Parkville, Victoria, Australia
A. V. KOEHLER
Affiliation:
Faculty of Veterinary and Agricultural Sciences, The University of Melbourne, Parkville, Victoria, Australia
A. JABBAR
Affiliation:
Faculty of Veterinary and Agricultural Sciences, The University of Melbourne, Parkville, Victoria, Australia
R. B. GASSER
Affiliation:
Faculty of Veterinary and Agricultural Sciences, The University of Melbourne, Parkville, Victoria, Australia
I. BEVERIDGE*
Affiliation:
Faculty of Veterinary and Agricultural Sciences, The University of Melbourne, Parkville, Victoria, Australia
*
*Corresponding author: Faculty of Veterinary and Agricultural Sciences, The University of Melbourne, Parkville, Victoria, Australia. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Sequences of the first and second internal transcribed spacers (ITS1 + ITS2) of nuclear ribosomal DNA were employed to determine whether the congeneric assemblages of species of the strongyloid nematode genus Cloacina, found in the forestomachs of individual species of kangaroos and wallabies (Marsupialia: Macropodidae), considered to represent species flocks, were monophyletic. Nematode assemblages examined in the black-striped wallaby, Macropus (Notamacropus) dorsalis, the wallaroos, Macropus (Osphranter) antilopinus/robustus, rock wallabies, Petrogale spp., the quokka, Setonix brachyurus, and the swamp wallaby, Wallabia bicolor, were not monophyletic and appeared to have arisen by host colonization. However, a number of instances of within-host speciation were detected, suggesting that a variety of methods of speciation have contributed to the evolution of the complex assemblages of species present in this genus.

Keywords

CloacinaNematodaStrongylidaspeciationspecies flocksinternal transcribed spacers
Type
Research Article
Information
Parasitology , Volume 144 , Issue 13 , November 2017 , pp. 1828 - 1840
Check for updates
Copyright
Copyright © Cambridge University Press 2017 

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

REFERENCES

Alesandrini, S. and Bernardi, G. (1999). Ancient species flocks and recent speciation events: what can rockfish teach us about cichlids (and vice versa?). Journal of Molecular Evolution 49, 814–818.Google Scholar
Anderson, R. C. (2000). Nematode Parasites of Vertebrates. Their Development and Transmission, 2nd Edn. CABI Publishing, Wallingford, UK.Google Scholar
Anjos, D. H. S. and Rodrigues, M. L. A. (2003). Structure of the community of the Strongylidae nematodes in the dorsal colon of Equus caballus from Rio de Janeiro state – Brazil. Veterinary Parasitology 112, 109–116.Google Scholar
Arundel, J. H., Beveridge, I. and Presidente, P. J. A. (1979). Parasites and pathological findings in enclosed and free-ranging populations of Macropus rufus (Desmarest) (Marsupialia) at Menindee, New South Wales. Australian Wildlife Research 6, 361–379.Google Scholar
Begg, M., Beveridge, I., Chilton, N. B., Johnson, P. M. and O'Callaghan, M. G. (1995). Parasites of the Proserpine Rock Wallaby, Petrogale persephone (Marsupialia: Macropodidae). Australian Mammalogy 18, 45–53.Google Scholar
Beveridge, I. (1998). Taxonomic revision of the genus Cloacina von Linstow (Nematoda: Strongyloidea) from macropodid marsupials. Invertebrate Taxonomy 12, 273–508.CrossRefGoogle Scholar
Beveridge, I. (1999). New species of Cloacina Linstow, 1898 (Nematoda: Strongyloidea) parasitic in the stomach of the quokka, Setonix brachyurus (Marsupialia: Macropodidae) from Western Australia. Transactions of the Royal Society of South Australia 123, 17–30.Google Scholar
Beveridge, I. (2002). New species and new records of Cloacina von Linstow, 1898 (Nematoda: Strongyloidea) parasitic in macropodid marsupials from Papua New Guinea. Records of the South Australian Museum 35, 1–32.Google Scholar
Beveridge, I. (2014). New species of parasitic nematodes of the genus Cloacina (Nematoda: Strongyloidea) from the banded hare wallaby, Lagostrophus fasciatus (Marsupialia: Macropodidae). Transactions of the Royal Society of South Australia 138, 249–256.Google Scholar
Beveridge, I. (2016). The gastro-intestinal helminth parasites of the swamp wallaby, Wallabia bicolor (Desmarest) (Marsupialia: Macropodidae), and their regional distribution. Transactions of the Royal Society of South Australia 140, 203–227.Google Scholar
Beveridge, I. and Arundel, J. H. (1979). Helminth parasites of grey kangaroos, Macropus giganteus Shaw and M. fuliginosus (Desmarest), in eastern Australia. Australian Wildlife Research 6, 69–77.CrossRefGoogle Scholar
Beveridge, I. and Chilton, N. B. (2001). Co-evolutionary relationships between the nematode subfamily Cloacininae and its macropodid marsupial hosts. International Journal for Parasitology 31, 976–996.Google Scholar
Beveridge, I. and Jabbar, A. (2013). New species of Kiluluma Skrjabin, 1916 (Nematoda: Strongylida) from the white rhinoceros Ceratotherium simium (Burchell), with a redescription of K. solitaria Thapar, 1924. Systematic Parasitology 85, 131–145.Google Scholar
Beveridge, I. and Speare, R. (1999). New species of parasitic nematodes from Dorcopsulus vanheurni (Marsupialia : Macropodidae) from Papua New Guinea. Transactions of the Royal Society of South Australia 123, 85–100.Google Scholar
Beveridge, I. and Spratt, D. M. (1996). The helminth parasites of Australasian marsupials: origins and evolutionary biology. Advances in Parasitology 37, 136–254.Google Scholar
Beveridge, I., Spratt, D. M., Close, R. L., Barker, S. C. and Sharman, G. B. (1989). Helminth parasites of rock wallabies, Petrogale spp. (Marsupialia) from Queensland. Australian Wildlife Research 16, 273–287.Google Scholar
Beveridge, I., Chilton, N. B., Johnson, P. M., Smales, L. R., Speare, R. and Spratt, D. M. (1998). Helminth parasite communities of kangaroos and wallabies (Macropus spp. and Wallabia bicolor) from north and central Queensland. Australian Journal of Zoology 46, 473–495.Google Scholar
Beveridge, I., Chilton, N. B. and Spratt, D. M. (2002). The occurrence of species flocks in the nematode genus Cloacina (Strongyloidea: Cloacininae) parasitic in the stomachs of kangaroos and wallabies. Australian Journal of Zoology 50, 597–620.Google Scholar
Beveridge, I., Jabbar, A. and Shuttleworth, M. (2014 a). New species of Cloacina Linstow, 1898 (Nematoda: Strongylida) from the swamp wallaby, Wallabia bicolor (Desmarest, 1804) (Marsupialia). Transactions of the Royal Society of South Australia 138, 237–248.Google Scholar
Beveridge, I., Ngyuen, H., Nyein, S., Cheng, C., Koehler, A., Shuttleworth, M., Gasser, R. B. and Jabbar, A. (2014 b). Description of Cloacina atthis sp. nov. from the stomach of the euro (Macropus robustus) (Marsupialia: Macropodidae) from Western Australia based on morphological and molecular criteria. Parasitology Research 113, 3485–3493.Google Scholar
Bradley, C., Beveridge, I., Chilton, N. B. and Johnson, P. M. (2000). Helminth parasites of the purple-necked rock wallaby, Petrogale lateralis purpureicollis, from Queensland. Transactions of the Royal Society of South Australia 124, 37–40.Google Scholar
Bu, Y., Niu, H., Gasser, R. B., Beveridge, I. and Zhang, L. (2009). Strongyloid nematodes in the caeca of donkeys in Henan Province, China. Acta Parasitologica 54, 263–2268.Google Scholar
Bucknell, D., Gasser, R. B. and Beveridge, I. (1995). The prevalence and epidemiology of gastrointestinal parasites of horses in Victoria, Australia. International Journal for Parasitology 25, 711–724.Google Scholar
Bucknell, D., Hoste, H., Gasser, R. B. and Beveridge, I. (1996). The structure of the community of strongyloid nematodes of domestic equids. Journal of Helminthology 70, 185–192.Google Scholar
Canaris, A. G. and Gardner, S. L. (2003). Bibliography of helminth species described from African vertebrates 1800–1967. Faculty Publications from the Harold W. Manter Laboratory for Parasitology. Paper 3. http://digitalcommons.unl.edu/parasitologyfacpubs/3.Google Scholar
Cardillo, M., Bininda-Edmonds, O. R. P., Boakes, E. and Purvis, A. (2004). A species-level phylogenetic supertree of marsupials. Journal of Zoology (London) 264, 11–31.CrossRefGoogle Scholar
Chabaud, A. G. (1957). Revue critique des nématodes du genre Quilonia Lane, 1914 et du genre Murshidia Lane, 1914. Annales de Parasitologie humaine et comparée 32, 98–131.Google Scholar
Chilton, N. B., Beveridge, I. and Andrews, R. H. (1997 a). An electrophoretic analysis of patterns of speciation in Cloacina clarkae, C. communis, C. petrogale and C. similis (Nematoda: Strongyloidea) from macropodid marsupials. International Journal for Parasitology 27, 483–494.Google Scholar
Chilton, N. B., Beveridge, I., Hoste, H. and Gasser, R. B. (1997 b). Evidence for hybridisation between Paramacropostrongylus iugalis and P.typicus (Nematoda: Strongyloidea) in grey kangaroos, Macropus fuliginosus and M.giganteus in a zone of sympatry in eastern Australia. International Journal for Parasitology 27, 475–482.Google Scholar
Chilton, N. B., Huby-Chilton, F., Johnson, P. M., Beveridge, I. and Gasser, R. B. (2009). Genetic variation within species of the nematode genus Cloacina (Strongyloidea: Cloacininae) parasitic in the stomachs of rock wallabies, Petrogale spp. (Marsupialia: Macropodidae) in Queensland. Australian Journal of Zoology 57, 1–10.Google Scholar
Chilton, N. B., Huby-Chilton, F., Koehler, A. V., Gasser, R. B. and Beveridge, I. (2016 a). Phylogenetic relationships of species of the oesophageal parasitic nematode genera Cyclostrongylus and Spirostrongylus (Strongyloidea: Chabertiidae: Cloacininae) with their wallaby hosts (Marsupialia: Macropodidae). Molecular and Cellular Probes 30, 93–99.Google Scholar
Chilton, N. B., Huby-Chilton, F., Gasser, R. B., Koehler, A. V. and Beveridge, I. (2016 b). Pharyngostrongylus thylogale n. sp. (Nematoda: Strongylida) from the stomachs of macropodid marsupials defined by morphological and molecular criteria. Systematic Parasitology 93, 749–760.Google Scholar
Chilton, N. B., Huby-Chilton, F., Koehler, A. V., Gasser, R. B. and Beveridge, I. (2016 c). Detection of cryptic species of Rugopharynx (Nematoda: Strongylida) from the stomachs of macropodid marsupials. International Journal for Parasitology – Parasites and Wildlife 5, 124–133.Google Scholar
Clancy, T. F. and Croft, D. B. (2008). Common wallaroo: Macropus robustus Gould, 1841. In The Mammals of Australia, 3rd Edn (ed. van Dyck, S. and Strahan, R.), pp. 346–348. Reed New Holland Publishers, Chatswood, Australia.Google Scholar
Clegg, S. M., Hale, P. and Moritz, C. (1998). Molecular population genetics of the red kangaroo (Macropus rufus): mt DNA variation. Molecular Ecology 7, 679–686.Google Scholar
Coghlan, B. A., Goldizen, A. W., Thomson, V. A. and Seddon, J. M. (2015). Phylogeography of eastern grey kangaroos, Macropus giganteus, suggests a mesic refugium in eastern Australia. PLoS ONE 10(5), e0128160.Google Scholar
de Torres, P. J. (2008). Quokka: Setonix brachyurus (Quoy & Gaimard, 1830). In The Mammals of Australia, 3rd Edn (ed. van Dyck, S. and Strahan, R.), pp. 402–404. Reed New Holland Publishers, Chatswood, Australia.Google Scholar
Edgar, R. C. (2004). MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5(1), 1.Google Scholar
Franzen, J. L. (2010). The Rise of Horses: 55 Million Years of Evolution. John Hopkins University Press, Baltimore.CrossRefGoogle Scholar
Gasser, R. B., Chilton, N. B., Hoste, H. and Beveridge, I. (1993). Rapid sequencing of rDNA from single worms and eggs of parasitic helminths. Nucleic Acids Research 21, 2525–2526.Google Scholar
Gibson, D. I. (1979). Materials and methods in helminth alpha-taxonomy. Parasitology 79, 36.Google Scholar
Gouÿ de Bellocq, J., Ferté, H., Depaquit, J., Justine, J.-L., Tiller, A. and Durette-Desset, M.-C. (2001). Phylogeny of the Trichostrongylina (Nematoda) inferred from 28S rDNA sequences. Molecular Phylogenetics and Evolution 19, 430–442.Google Scholar
Greenwood, P. H. (1984). What is a species flock? In Evolution of Fish Species Flocks (ed. Echelle, A. A. and Kornfield, I.), pp. 13–19. University of Maine at Orono Press, Orono, USA.Google Scholar
Hoste, H. and Beveridge, I. (1993). Interspecific and intergeneric relations between nematodes parasitic in the stomachs of kangaroos and wallabies. Transactions of the Royal Society of South Australia 117, 171–178.Google Scholar
Hung, G. C., Chilton, N. B., Beveridge, I. and Gasser, R. G. (2000). A molecular systematic framework for equine strongyles based on ribosomal DNA sequence data. International Journal for Parasitology 30, 95–103.Google Scholar
Huyse, T. and Volckaert, F. A. M. (2005). Comparing host and parasite phylogenies: Gyrodactylus flatworms jumping from goby to goby. Systematic Biology 54, 710–718.Google Scholar
Inglis, W. G. (1971). Speciation in parasitic nematodes. Advances in Parasitology 9, 201–223.Google Scholar
Jarman, P. J. and Phillips, C. M. (1989). Diets in a community on macropod species. In Kangaroos, Wallabies and Rat-kangaroos (ed. Grigg, G., Jarman, P. and Hume, I.), pp. 143–149. Surrey Beatty & Sons, Chipping Norton, Australia.Google Scholar
Johnson, P. M. (2008). Black-striped wallaby: Macropus dorsalis (Gray, 1837). In The Mammals of Australia, 3rd Edn (ed. van Dyck, S. and Strahan, R.), pp. 329–330. Reed New Holland Publishers, Chatswood, Australia.Google Scholar
Johnston, T. H. and Mawson, P. M. (1938). Strongyle nematodes from central Australian kangaroos and wallabies. Transactions of the Royal Society of South Australia 62, 263–286.Google Scholar
Kennedy, C. R. and Bush, A. O. (1992). Species richness in helminth communities: the importance of multiple congeners. Parasitology 104, 187–197.Google Scholar
Kunz, W. (2002). When is a parasite species a species? Trends in Parasitology 18, 121–124.Google Scholar
Kuzmina, T. A., Zvegintsova, N. S. and Zharkikh, T. L. (2009). Strongylid community structure of the Przewalski's horses (Equus ferus przewalskii) from the biosphere reserve ‘Askania-Nova’, Ukraine. Vestnik zoologii 43, 5–11.Google Scholar
Lichtenfels, J. R. (1980). Keys to genera of the superfamily Strongyloidea. In CIH Keys to the Nematode Parasites of Vertebrates. No. 7 (ed. Anderson, R. C., Chabaud, A. G. and Willmott, S.), pp. 1–41. CABI International, Farnham Royal, England.Google Scholar
Lichtenfels, J. R., Kharchenko, V. A. and Dvojnos, G. M. (2008). Illustrated identification keys to strongylid parasites (Strongylidae: Nematoda) of horses, zebras and asses (Equidae). Veterinary Parasitology 156, 4–161.Google Scholar
Lott, M. J., Hose, G. C. and Power, M. L. (2014). Towards the molecular characterisation of parasitic nematode assemblages; an evaluation of terminal-restriction fragment length polymorphism (T-RFLP) analysis. Experimental Parasitology 144, 76–83.Google Scholar
Maddison, W. P. and Maddison, D. R. (2015). Mesquite: a modular system for evolutionary analysis. Version 3.04. http://mesquiteproject.org.Google Scholar
Mayr, E. (1984). Evolution of fish species flocks. In Evolution of Fish Species Flocks (ed. Echelle, A. A. and Kornfield, I.), pp. 3–11. University of Maine at Orono Press, Orono, USA.Google Scholar
McCoy, K. D. (2003). Sympatric speciation in parasites – what is sympatry? Trends in Parasitology 19, 400–404.CrossRefGoogle ScholarPubMed
McDonnell, A., Love, S., Tait, A., Lichtenfels, J. R. and Matthews, J. B. (2000). Phylogenetic analysis of partial mitochondrial cyrochrome oxidase c subunit 1 and large RNA sequences and nuclear internal transcribed spacer 1 sequences from species of Cyathostominae and Strongylinae (Nematoda, Order Strongylida), parasites of horses. Parasitology 121, 649–659.Google Scholar
Meredith, R. W., Westerman, M. and Springer, M. S. (2008). A phylogeny and timescale for the living genera of kangaroos and kin (Macropodiformes: Marsupialia) based on nuclear DNA sequences. Australian Journal of Zoology 56, 395–410.Google Scholar
Mfitilodze, M. W. and Hutchinson, G. W. (1985). The site distribution of adult strongyle parasites in the large intestines of horses in tropical Australia. International Journal for Parasitology 15, 313–319.Google Scholar
Morales-Hojas, R., Cheke, R. A. and Post, R. J. (2006). Molecular systematics of five Onchocerca species (Nematoda: Filarioidea) including the human parasite, O. volvulus, suggest sympatric speciation. Journal of Helminthology 80, 281–290.Google Scholar
Mykytowycz, R. (1964). A survey of the endoparasites of the red kangaroo, Megaleia rufa (Desmarest). Parasitology 54, 677–693.CrossRefGoogle ScholarPubMed
Neaves, L. E., Zenger, K. R., Prince, R. I. T., Eldridge, M. D. B. and Cooper, D. W. (2009). Landscape discontinuities influence gene flow and genetic structure in a large, vagile Australian mammal, Macropus fuliginosus . Molecular Ecology 18, 3363–3378.Google Scholar
Ogbourne, C. P. (1976). The prevalence, relative abundance and site distribution of nematodes of the subfamily Cyathostominae in horses killed in Britain. Journal of Helminthology 50, 201–214.Google Scholar
Pamment, D., Beveridge, I. and Gasser, R. B. (1994). The distribution of nematode parasites within the stomach of the western grey kangaroos, Macropus fuliginosus . Transactions of the Royal Society of South Australia 118, 187–196.Google Scholar
Petter, A. (1966). Equilibre des espèces dans les populations de nématodes parasites du colon des tortues terrestres. Mémoires du Muséum national d'Histoire naturelle, Paris (Zoolgie) 39, 1–252.Google Scholar
Posada, D. (2008). jModelTest: phylogenetic model averaging. Molecular Biology and Evolution 25, 1253–1256.Google Scholar
Potter, S., Cooper, S. J. B., Metcalfe, C. J., Taggart, D. A. and Eldridge, M. D. B. (2012). Phylogenetic relationships of rock-wallabies, Petrogale (Marsupialia: Macropodidae) and their biogeographic history within Australia. Molecular Phylogenetics and Evolution 62, 640–652.Google Scholar
Poulin, R. (2007). Evolutionary Ecology of Parasites, 2nd Edn. Princeton University Press, New Jersey.Google Scholar
Price, P. W. (1980). Evolutionary Biology of Parasites. Princeton University Press, New Jersey.Google Scholar
Prideaux, G. J. and Warburton, N. M. (2010). An osteology-based appraisal of the phylogeny and evolution of kangaroos and wallabies (Marsupialia: Macropodidae). Zoological Journal of the Linnean Society 159, 954–987.Google Scholar
Ribbink, A. J. (1984). Is the species flock concept tenable. In Evolution of Fish Species Flocks (ed. Echelle, A. A. and Kornfield, I.), pp. 21–25. University of Maine at Orono Press, Orono, USA.Google Scholar
Ronquist, F. and Huelsenbeck, J. P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.Google Scholar
Round, M. C. (1968). Checklist of the helminth parasites of African mammals of the orders Carnivora, Tubulidentata, Proboscidea, Hyracoidea, Artiodactyla and Perissodactyla. Technical Communication No. 38 of the Commonwealth Institute of Helminthology, St Albans.Google Scholar
Schad, G. A. (1963). Niche diversification in a parasite species flock. Nature, London 198, 404–406.Google Scholar
Seehausen, O. (2006). African cichlid fish: a model system in adaptive radiation research. Proceedings of the Royal Society (B) 273, 1987–1998.Google Scholar
Shuttleworth, M. A., Beveridge, I., Chilton, N. B., Koehler, A. V., Gasser, R. B. and Jabbar, A. (2014). Genetic variation within and among species of Cloacina (Strongyloidea: Cloacininae) from the swamp wallaby, Wallabia bicolor (Marsupialia: Macropodidae). Infection, Genetics and Evolution 28, 261–269.Google Scholar
Shuttleworth, M. A., Jabbar, A. and Beveridge, I. (2016 a). Description and molecular characterisation of Cloacina johnstoni sp. nov. (Nematoda: Strongyloidea) from the wallaroo, Macropus robustus (Marsupialia: Macropodidae) and relationships with the synhospitalic species C. macropodis . Parasitology Research 115, 3357–3363.Google Scholar
Shuttleworth, M. A., Beveridge, I., Koehler, A. V., Gasser, R. B. and Jabbar, A. (2016 b). Molecular characterization of species of Cloacina (Strongyloidea: Cloacininae) from the common wallaroo, Macropus robustus (Marsupialia: Macropodidae) in Australia. Infection, Genetics and Evolution 44, 245–253.Google Scholar
Šimková, A., Desdevises, Y., Gelnar, M. and Morand, S. (2000). Co-existence of nine gill ectoparasites (Dactylogyrus: Monogenea) parasitising the roach (Rutilus rutilus L.): history and present ecology. International Journal for Parasitology 30, 1077–1088.Google Scholar
Šimková, A., Gelnar, M. and Morand, S. (2001). Order and disorder in ectoparasite communities: the case of congeneric gill monogeneans (Dactylogyrus spp.). International Journal for Parasitology 31, 1205–1210.Google Scholar
Šimková, A., Morand, S., Jobet, E., Gelnar, M. and Verneau, O. (2004). Molecular phylogeny of congeneric monogenean parasites (Gyrodactylus): a case of intra-host speciation. Evolution 58, 1001–1018.Google Scholar
Smales, L. R. (1977). The life history of Labiostrongylus eugenii, a nematode parasite of the Kangaroo Island wallaby (Macropus eugenii): the parasitic stages. International Journal for Parasitology 7, 457–461.Google Scholar
Stancampiano, L., Mughini Gras, L. and Poglayen, G. (2010). Spatial niche competition among helminth parasites in horse's large intestine. Veterinary Parasitology 170, 88–95.Google Scholar
van Dyck, S. and Strahan, R. (2008). The Mammals of Australia, 3rd Edn. Reed New Holland Publishers, Chatswood, Australia.Google Scholar