Skip to main content Accessibility help
×
Home

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

  • N. B. CHILTON (a1), M. A. SHUTTLEWORTH (a2), F. HUBY-CHILTON (a2), A. V. KOEHLER (a2), A. JABBAR (a2), R. B. GASSER (a2) and I. BEVERIDGE (a2)...

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.

Copyright

Corresponding author

*Corresponding author: Faculty of Veterinary and Agricultural Sciences, The University of Melbourne, Parkville, Victoria, Australia. E-mail: ibeve@unimelb.edu.au

References

Hide All
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, 814818.
Anderson, R. C. (2000). Nematode Parasites of Vertebrates. Their Development and Transmission, 2nd Edn. CABI Publishing, Wallingford, UK.
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, 109116.
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, 361379.
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, 4553.
Beveridge, I. (1998). Taxonomic revision of the genus Cloacina von Linstow (Nematoda: Strongyloidea) from macropodid marsupials. Invertebrate Taxonomy 12, 273508.
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, 1730.
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, 132.
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, 249256.
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, 203227.
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, 6977.
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, 976996.
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, 131145.
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, 85100.
Beveridge, I. and Spratt, D. M. (1996). The helminth parasites of Australasian marsupials: origins and evolutionary biology. Advances in Parasitology 37, 136254.
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, 273287.
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, 473495.
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, 597620.
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, 237248.
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, 34853493.
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, 3740.
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, 2632268.
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, 711724.
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, 185192.
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.
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, 1131.
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, 98131.
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, 483494.
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, 475482.
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, 110.
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, 9399.
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, 749760.
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, 124133.
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. 346348. Reed New Holland Publishers, Chatswood, Australia.
Clegg, S. M., Hale, P. and Moritz, C. (1998). Molecular population genetics of the red kangaroo (Macropus rufus): mt DNA variation. Molecular Ecology 7, 679686.
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.
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. 402404. Reed New Holland Publishers, Chatswood, Australia.
Edgar, R. C. (2004). MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5(1), 1.
Franzen, J. L. (2010). The Rise of Horses: 55 Million Years of Evolution. John Hopkins University Press, Baltimore.
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, 25252526.
Gibson, D. I. (1979). Materials and methods in helminth alpha-taxonomy. Parasitology 79, 36.
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, 430442.
Greenwood, P. H. (1984). What is a species flock? In Evolution of Fish Species Flocks (ed. Echelle, A. A. and Kornfield, I.), pp. 1319. University of Maine at Orono Press, Orono, USA.
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, 171178.
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, 95103.
Huyse, T. and Volckaert, F. A. M. (2005). Comparing host and parasite phylogenies: Gyrodactylus flatworms jumping from goby to goby. Systematic Biology 54, 710718.
Inglis, W. G. (1971). Speciation in parasitic nematodes. Advances in Parasitology 9, 201223.
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. 143149. Surrey Beatty & Sons, Chipping Norton, Australia.
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. 329330. Reed New Holland Publishers, Chatswood, Australia.
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, 263286.
Kennedy, C. R. and Bush, A. O. (1992). Species richness in helminth communities: the importance of multiple congeners. Parasitology 104, 187197.
Kunz, W. (2002). When is a parasite species a species? Trends in Parasitology 18, 121124.
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, 511.
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. 141. CABI International, Farnham Royal, England.
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, 4161.
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, 7683.
Maddison, W. P. and Maddison, D. R. (2015). Mesquite: a modular system for evolutionary analysis. Version 3.04. http://mesquiteproject.org.
Mayr, E. (1984). Evolution of fish species flocks. In Evolution of Fish Species Flocks (ed. Echelle, A. A. and Kornfield, I.), pp. 311. University of Maine at Orono Press, Orono, USA.
McCoy, K. D. (2003). Sympatric speciation in parasites – what is sympatry? Trends in Parasitology 19, 400404.
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, 649659.
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, 395410.
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, 313319.
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, 281290.
Mykytowycz, R. (1964). A survey of the endoparasites of the red kangaroo, Megaleia rufa (Desmarest). Parasitology 54, 677693.
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, 33633378.
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, 201214.
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, 187196.
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, 1252.
Posada, D. (2008). jModelTest: phylogenetic model averaging. Molecular Biology and Evolution 25, 12531256.
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, 640652.
Poulin, R. (2007). Evolutionary Ecology of Parasites, 2nd Edn. Princeton University Press, New Jersey.
Price, P. W. (1980). Evolutionary Biology of Parasites. Princeton University Press, New Jersey.
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, 954987.
Ribbink, A. J. (1984). Is the species flock concept tenable. In Evolution of Fish Species Flocks (ed. Echelle, A. A. and Kornfield, I.), pp. 2125. University of Maine at Orono Press, Orono, USA.
Ronquist, F. and Huelsenbeck, J. P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 15721574.
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.
Schad, G. A. (1963). Niche diversification in a parasite species flock. Nature, London 198, 404406.
Seehausen, O. (2006). African cichlid fish: a model system in adaptive radiation research. Proceedings of the Royal Society (B) 273, 19871998.
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, 261269.
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, 33573363.
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, 245253.
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, 10771088.
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, 12051210.
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, 10011018.
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, 457461.
Stancampiano, L., Mughini Gras, L. and Poglayen, G. (2010). Spatial niche competition among helminth parasites in horse's large intestine. Veterinary Parasitology 170, 8895.
van Dyck, S. and Strahan, R. (2008). The Mammals of Australia, 3rd Edn. Reed New Holland Publishers, Chatswood, Australia.

Keywords

Related content

Powered by UNSILO

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

  • N. B. CHILTON (a1), M. A. SHUTTLEWORTH (a2), F. HUBY-CHILTON (a2), A. V. KOEHLER (a2), A. JABBAR (a2), R. B. GASSER (a2) and I. BEVERIDGE (a2)...

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed.