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The diversity and evolution of nematodes (Pharyngodonidae) infecting New Zealand lizards


Host–parasite co-evolutionary studies can shed light on diversity and the processes that shape it. Molecular methods have proven to be an indispensable tool in this task, often uncovering unseen diversity. This study used two nuclear markers (18S rRNA and 28S rRNA) and one mitochondrial (cytochrome oxidase subunit I) marker to investigate the diversity of nematodes of the family Pharyngodonidae parasitizing New Zealand (NZ) lizards (lygosomine skinks and diplodactylid geckos) and to explore their co-evolutionary history. A Bayesian approach was used to infer phylogenetic relationships of the parasitic nematodes. Analyses revealed that nematodes parasitizing skinks, currently classified as Skrjabinodon, are more closely related to Spauligodon than to Skrjabinodon infecting NZ geckos. Genetic analyses also uncovered previously undetected diversity within NZ gecko nematodes and provided evidence for several provisionally cryptic species. We also examined the level of host–parasite phylogenetic congruence using a global-fit approach. Significant congruence was detected between gecko-Skrjabinodon phylogenies, but our results indicated that strict co-speciation is not the main co-evolutionary process shaping the associations between NZ skinks and geckos and their parasitic nematodes. However, further sampling is required to fully resolve co-phylogenetic patterns of diversification in this host–parasite system.

Corresponding author
*Corresponding author: Department of Zoology, University of Otago, P.O. Box 56, Dunedin 9054, New Zealand. E-mail:
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Ainsworth, R. (1985). An evaluation of some island biogeographic theories using lizards and lizard parasites in the wellington region. Masters of Science, Victoria University, Wellington.
Ainsworth, R. (1990). Male dimorphism in two new species of nematode (Pharyngodonidae: Oxyurida) from New Zealand lizards. The Journal of Parasitology 76, 812822.
Ainsworth, R. (1992). A revision of the Pharyngodoninae, nematodes of frogs and lizards . Doctor of Philosophy, Victoria University, Wellington.
Anderson, R. C. (2000). Nematode Parasites of Vertebrates: Their Development and Transmission , 2nd Edn. CABI Publishing, Wallingford.
Araujo, S. B. L., Braga, M. P., Brooks, D. R., Agosta, S. J., Hoberg, E. P., von Hartenthal, F. W. and Boeger, W. A. (2015). Understanding host-switching by ecological fitting. PLoS ONE 10, e0139552.
Balbuena, J. A., Míguez-Lozano, R. and Blasco-Costa, I. (2013). PACo: a novel procrustes application to cophylogenetic analysis. PLoS ONE 8, e61048.
Ballard, J. W. O. and Whitlock, M. C. (2004). The incomplete natural history of mitochondria. Molecular Ecology 13, 729744.
Barwick, R. E. (1959). The life history of the common New Zealand skink Leiolopisma zelandica (Gray, 1843). Transactions of the Royal Society of New Zealand 86, 331380.
Bell, T. (2014). Standardized common names for New Zealand reptiles. BioGecko 2, 811.
Blouin, M. S., Yowell, C. A., Courtney, C. H. and Dame, J. B. (1998). Substitution bias, rapid saturation, and the use of mtDNA for nematode systematics. Molecular Biology and Evolution 15, 17191727.
Brooks, D. R. (1979). Testing the context and extent of host–parasite coevolution. Systematic Zoology 28, 299307.
Brooks, D. R. (1991). Phylogeny, Ecology, and Behavior: A Research Program in Comparative Biology. The University of Chicago Press, Chicago.
Chapple, D. G., Ritchie, P. A. and Daugherty, C. H. (2009). Origin, diversification, and systematics of the New Zealand skink fauna (Reptilia: Scincidae). Molecular Phylogenetics and Evolution 52, 470487.
Clark, W. C. (1982). Parasites of New Zealand reptiles. In New Zealand Herpetology: Proceedings of a Symposium Held at the Victoria University of Wellington, No. 2 (ed. Alison, F. R.). New Zealand Wildlife Service, Department of Internal Affairs, Wellington, NZ.
Collins, R. A. and Cruickshank, R. H. (2013). The seven deadly sins of DNA barcoding. Molecular Ecology Resources 13, 969975.
Darriba, D., Taboada, G. L., Doallo, R. and Posada, D. (2012). jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9, 772.
Dasmahapatra, K. K., Elias, M., Hill, R. I., Hoffman, J. I. and Mallet, J. (2010). Mitochondrial DNA barcoding detects some species that are real, and some that are not. Molecular Ecology Resources 10, 264273.
de Gruijter, J. M., Polderman, A. M., Zhu, X. Q. and Gasser, R. B. (2002). Screening for haplotypic variability within Oesophagostomum bifurcum (Nematoda) employing a single-strand conformation polymorphism approach. Molecular and Cellular Probes 16, 185190.
de Vienne, D. M., Refregier, G., Lopez-Villavicencio, M., Tellier, A., Hood, M. E. and Giraud, T. (2013). Cospeciation vs host-shift speciation: methods for testing, evidence from natural associations and relation to coevolution. New Phytologist 198, 347385.
Derycke, S., Remerie, T., Vierstraete, A., Backeljau, T., Vanfleteren, J., Vincx, M. and Moens, T. (2005). Mitochondrial DNA variation and cryptic speciation within the free-living marine nematode Pellioditis marina . Marine Ecology Progress Series 300, 91103.
Falk, B. J. and Perkins, S. L. (2013). Host specificity shapes population structure of pinworm parasites in Caribbean reptiles. Molecular Ecology 22, 45764590.
Fenner, A. L., Godfrey, S. S. and Bull, C. M. (2011). Using social networks to deduce whether residents or dispersers spread parasites in a lizard population. The Journal of Animal Ecology 80, 835843.
Floyd, R. M., Rogers, A. D., Lambshead, P. J. D. and Smith, C. R. (2005). Nematode-specific PCR primers for the 18S small subunit rRNA gene. Molecular Ecology Notes 5, 611612.
Foitová, I., Koubková, B., Baruš, V. and Nurcahyo, W. (2008). Presence and species identification of the gapeworm Mammomonogamus laryngeus (Railliet, 1899) (Syngamidae: Nematoda) in a semi-wild population of Sumatran orangutan (Pongo abelii) in Indonesia. Research in Veterinary Science 84, 232236.
Frézal, L. and Leblois, R. (2008). Four years of DNA barcoding: current advances and prospects. Infection, Genetics and Evolution 8, 727736.
Fujita, M. K., Leaché, A. D., Burbrink, F. T., Mcguire, J. A. and Moritz, C. (2012). Coalescent-based species delimitation in an integrative taxonomy. Trends in Ecology & Evolution 27, 480488.
Gill, B. J., Bejakovtch, D. and Whitaker, A. H. (2001). Records of foreign reptiles and amphibians accidentally imported to New Zealand. New Zealand Journal of Zoology 28, 351359.
Grillo, V., Jackson, F., Cabaret, J. and 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, 435447.
Gyawali, P., Khanal, S. and Shrestha, B. (2013). Intestinal helminth fauna in sleepy lizard (Tiliqua rugosa) in Australia. International Journal of Veterinary Science 2, 1720.
Hickson, R. E., Slack, K. E. and Lockhart, P. (2000). Phylogeny recapitulates geography, or why New Zealand has so many species of skinks. Biological Journal of the Linnean Society 70, 415433.
Hoberg, E. P. and Brooks, D. R. (2008). A macroevolutionary mosaic: episodic host-switching, geographical colonization and diversification in complex host–parasite systems. Journal of Biogeography 35, 15331550.
Hoberg, E. P. and Brooks, D. R. (2015). Evolution in action: climate change, biodiversity dynamics and emerging infectious disease. Philosophical Transactions of the Royal Society of London B Biological Sciences 370, 20130553.
Hodda, M. (2011). Phylum Nematoda Cobb 1932. In Zhang Z. -Q. (Ed.) Animal biodiversity: an outer of higher-level classification and survey of taxonomic richness. Zootaxa 3148, 6395.
Hu, M., Chilton, N. B., Zhu, X. and Gasser, R. B. (2002). Single-strand conformation polymorphism-based analysis of mitochondrial cytochrome c oxidase subunit 1 reveals significant substructuring in hookworm populations. Electrophoresis 23, 2734.
Jackson, J. A. (1999). Analysis of parasite host-switching: limitations on the use of phylogenies. Parasitology 119, S111S123.
Jewell, T. (2006). Identifying Geckos in Otago. Science & Technical Publication, Department of Conservation, Wellington, NZ.
Jones, H. I. (2013). Gastrointestinal nematodes from three species of Australian leaf-tailed geckos (Reptilia: Saltuarius spp.), with descriptions of new species of Skrjabinodon (Oxyuroidea: Pharyngodonidae) and Hedruris (Habronematoidea: Hedruridae). Comparative Parasitology 80, 4759.
Jorge, F., Carretero, M., Roca, V., Poulin, R. and Perera, A. (2013 a). What you get is what they have? Detectability of intestinal parasites in reptiles using faeces. Parasitology Research 112, 40014007.
Jorge, F., Perera, A., Carretero, M. A., James Harris, D. and Roca, V. (2013 b). Cryptic species unveiled: the case of the nematode Spauligodon atlanticus . Journal of Zoological Systematics and Evolutionary Research 51, 187202.
Jorge, F., Roca, V., Perera, A., Harris, D. and Carretero, M. (2011). A phylogenetic assessment of the colonisation patterns in Spauligodon atlanticus Astasio-Arbiza et al. 1987 (Nematoda: Oxyurida: Pharyngodonidae), a parasite of lizards of the genus Gallotia Boulenger: no simple answers. Systematic Parasitology 80, 5366.
Jorge, F., Perera, A., Roca, V., Carretero, M. A., Harris, D. J. and Poulin, R. (2014). Evolution of alternative male morphotypes in oxyurid nematodes: a case of convergence? Journal of Evolutionary Biology 27, 16311643.
Karpiej, K., Dzido, J., Rokicki, J. and Kijewska, A. (2013). Anisakid nematodes of Greenland halibut reinhardtius hippoglossoides from the Barents Sea. The Journal of Parasitology 99, 650654.
Katoh, K., Misawa, K., Kuma, K.-I. and Miyata, T. (2002). MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research 30, 30593066.
Klassen, G. J. (1992). Coevolution: a history of the macroevolutionary approach to studying host–parasite associations. The Journal of Parasitology 78, 573587.
Lanfear, R., Calcott, B., Ho, S. Y. and Guindon, S. (2012). PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology and Evolution 29, 16951701.
Nielsen, S. V., Bauer, A. M., Jackman, T. R., Hitchmough, R. A. and Daugherty, C. H. (2011). New Zealand geckos (Diplodactylidae): cryptic diversity in a post-Gondwanan lineage with trans-Tasman affinities. Molecular Phylogenetics and Evolution 59, 122.
Paterson, A. M. and Banks, J. (2001). Analytical approaches to measuring cospeciation of host and parasites: through a glass, darkly. International Journal for Parasitology 31, 10121022.
Ronquist, F., Teslenko, M., Van Der Mark, P., Ayres, D. L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M. A. and Huelsenbeck, J. P. (2012). MrBayes 3·2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539542.
Streicher, J. W., Schulte, J. A. I. and Wiens, J. J. (2016). How should genes and taxa be sampled for phylogenomic analyses with missing data? An empirical study in iguanian lizards. Systematic Biology 65, 128145.
Szöllosi, G. J., Tannier, E., Daubin, V. and Boussau, B. (2013). The inference of gene trees with species trees. Systematic Biology 64, 4262.
Tamura, K., Stecher, G., Peterson, D., Filipski, A. and Kumar, S. (2013). MEGA6: molecular Evolutionary Genetics Analysis Version 6.0. Molecular Biology and Evolution 30, 27252729.
Tan, N., Chilton, N. B., Huby-Chilton, F., Jex, A. R., Gasser, R. B. and Beveridge, I. (2012). Molecular evidence for a cryptic species within the parasitic nematode Macroponema comani (Strongyloidea: Cloacininae). Molecular and Cellular Probes 26, 170174.
Whiting, M. F. (2002). Mecoptera is paraphyletic: multiple genes and phylogeny of Mecoptera and Siphonaptera. Zoologica Scripta 31, 93104.
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