Hostname: page-component-848d4c4894-5nwft Total loading time: 0 Render date: 2024-05-31T13:13:04.986Z Has data issue: false hasContentIssue false
  • English
  • Français

Intra- and interspecific genetic diversity of New Zealand hairworms (Nematomorpha)

Published online by Cambridge University Press:  09 March 2017

ZACHARY J. C. TOBIAS Open the ORCID record for ZACHARY J. C. TOBIAS [Opens in a new window] ,
ARUN K. YADAV ,
ANDREAS SCHMIDT-RHAESA  and
ROBERT POULIN
ZACHARY J. C. TOBIAS*
Affiliation:
Department of Zoology, University of Otago, P.O. Box 56, Dunedin 9054, New Zealand
ARUN K. YADAV
Affiliation:
Department of Zoology, North-Eastern Hill University, Shillong 793022, India
ANDREAS SCHMIDT-RHAESA
Affiliation:
Zoological Museum, University of Hamburg, Martin-Luther-King-Platz 3, 20146 Hamburg, Germany
ROBERT POULIN
Affiliation:
Department of Zoology, University of Otago, P.O. Box 56, Dunedin 9054, New Zealand
*
*Corresponding author: Department of Zoology, University of Otago, P.O. Box 56, Dunedin 9054, New Zealand. E-mail: zactobias44@gmail.com
Get access Rights & Permissions [Opens in a new window]

Summary

Hairworms (Nematomorpha) are a little-known group of parasites, and despite having been represented in the taxonomic literature for over a century, the implementation of molecular genetics in studies of hairworm ecology and evolution lags behind that of other parasitic taxa. In this study, we characterize the genetic diversity of the New Zealand nematomorph fauna and test for genetic structure within the most widespread species found. We provide new mitochondrial and nuclear ribosomal sequence data for three previously described species from New Zealand: Gordius paranensis, Parachordodes diblastus and Euchordodes nigromaculatus. We also present genetic data on a previously reported but undescribed Gordius sp., as well as data from specimens of a new Gordionus sp., a genus new for New Zealand. Phylogenetic analyses of CO1 and nuclear rDNA regions correspond with morphological classification based on scanning electron microscopy, and demonstrate paraphyly of the genus Gordionus and the potential for cryptic species within G. paranensis. Population-level analyses of E. nigromaculatus showed no genetic differentiation among sampling locations across the study area, in contrast to previously observed patterns in known and likely definitive hosts. Taken together, this raises the possibility that factors such as definitive host specificity, intermediate host movement, and passive dispersal of eggs and larvae may influence host–parasite population co-structure in hairworms.

Keywords

NematomorphahairwormsEuchordodes nigromaculatushost–parasite population structureNew Zealand
Type
Research Article
Information
Parasitology , Volume 144 , Issue 8 , July 2017 , pp. 1026 - 1040
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

Aguinaldo, A. M. A., Turbeville, J. M., Linford, L. S., Rivera, M. C., Garey, J. R., Raff, R. A. and Lake, J. A. (1997). Evidence for a clade of nematodes, arthropods and other moulting animals. Nature 387, 489–493.Google Scholar
Blasco-Costa, I. and Poulin, R. (2013). Host traits explain the genetic structure of parasites: a meta-analysis. Parasitology 140, 1316–1322.CrossRefGoogle ScholarPubMed
Blasco-Costa, I., Waters, J. M. and Poulin, R. (2012). Swimming against the current: genetic structure, host mobility and the drift paradox in trematode parasites. Molecular Ecology 21, 207–217.Google Scholar
Blaxter, M. L., De Ley, P., Garey, J. R., Liu, L. X., Scheldeman, P., Vierstraete, A., Vanfleteren, J. R., Mackey, L. Y., Dorris, M., Frisse, L. M. and Vida, J. T. (1998). A molecular evolutionary framework for the phylum Nematoda. Nature 392, 71–75.Google Scholar
Bleidorn, C., Schmidt-Rhaesa, A. and Garey, J. R. (2002). Systematic relationships of Nematomorpha based on molecular and morphological data. Invertebrate Biology 121, 357–364.Google Scholar
Bolek, M. G. and Coggins, J. R. (2002). Seasonal occurrence, morphology, and observations on the life history of Gordius difficilis (Nematomorpha: Gordioidea) from southeastern Wisconsin, United States. Journal of Parasitology, 88, 287–294.Google Scholar
Bolek, M. G., Schmidt-Rhaesa, A., Hanelt, B. and Richardson, D. J. (2010). Redescription of the African Chordodes albibarbatus Montgomery 1898, and description of Chordodes janovyi n. sp. (Gordiida, Nematomorpha) and its non-adult stages from Cameroon, Africa. Zootaxa 2631, 36–50.Google Scholar
Briers, R. A., Gee, J. H., Cariss, H. M. and Geoghegan, R. (2004). Inter-population dispersal by adult stoneflies detected by stable isotope enrichment. Freshwater Biology 49, 425–431.Google Scholar
Bruyndonckx, N., Henry, I., Christe, P. and Kerth, G. (2009). Spatio-temporal population genetic structure of the parasitic mite Spinturnix bechsteini is shaped by its own demography and the social system of its bat host. Molecular Ecology 18, 3581–3592.Google Scholar
Camerano, L. (1892). Descrizione di una nuova specie del genere Gordius di Palmeira (Paraná). Annali del Museo Civico di Storia Naturale di Genova 12, 965–966.Google Scholar
Camerano, L. (1894). Viaggio del dottor Alfredo Borelli nella Repubblica Argentina e nel Paraguay. Bollettino dei Musei di Zoologia ed Anatomia Comparata 9, 1–6.Google Scholar
Chinn, W. G. and Gemmell, N. J. (2004). Adaptive radiation within New Zealand endemic species of the cockroach genus Celatoblatta Johns (Blattidae): a response to Plio-Pleistocene mountain building and climate change. Molecular Ecology 13, 1507–1518.Google Scholar
Clement, M., Posada, D. C. K. A. and Crandall, K. A. (2000). TCS: a computer program to estimate gene genealogies. Molecular Ecology 9, 1657–1659.Google Scholar
Corander, J., Waldmann, P. and Sillanpää, M. J. (2003). Bayesian analysis of genetic differentiation between populations. Genetics 163, 367–374.Google Scholar
Couchoux, C., Seppä, P. and van Nouhuys, S. (2016). Strong dispersal in a parasitoid wasp overwhelms habitat fragmentation and host population dynamics. Molecular Ecology 25, 3344–3355.CrossRefGoogle Scholar
Criscione, C. D. (2008). Parasite co-structure: broad and local scale approaches. Parasite 15, 439–443.Google Scholar
Criscione, C. D. and Blouin, M. S. (2004). Life cycles shape parasite evolution: comparative population genetics of salmon trematodes. Evolution 58, 198–202.Google Scholar
Criscione, C. D. and Blouin, M. S. (2005). Effective sizes of macroparasite populations: a conceptual model. Trends in Parasitology 21, 212–217.Google Scholar
Criscione, C. D., Poulin, R. and Blouin, M. S. (2005). Molecular ecology of parasites: elucidating ecological and microevolutionary processes. Molecular Ecology 14, 2247–2257.Google Scholar
Darriba, D., Taboada, G. L., Doallo, R. and Posada, D. (2012). jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9, 772–772.CrossRefGoogle ScholarPubMed
De Villalobos, C., Zanca, F. and Ibarra-Vidal, H. (2005). Redescription and new records of freshwater Nematomorpha (Gordiida) from Chile, with the description of two new species. Revista Chilena de Historia Natural 78, 673–686.Google Scholar
Drummond, A. J. and Rambaut, A. (2007). BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology 7, 1.Google Scholar
Dybdahl, M. F. and Lively, C. M. (1996). The geography of coevolution: comparative population structures for a snail and its trematode parasite. Evolution 50, 2264–2275.Google Scholar
Efeykin, B. D., Schmatko, V. Y. and Spiridonov, S. E. (2016). Comparative phylogenetic informativity of single ribosomal cluster regions in freshwater horsehair worms (Gordiacea, Nematomorpha). Biology Bulletin 43, 34–41.Google Scholar
Excoffier, L. and Lischer, H. E. (2010). Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 10, 564–567.Google Scholar
Excoffier, L., Smouse, P. E. and Quattro, J. M. (1992). Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131, 479–491.Google Scholar
Folmer, O., Black, M., Hoeh, W., Lutz, R. and Vrijenhoek, R. (1994). DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294–299.Google Scholar
Gandon, S. and Michalakis, Y. (2002). Local adaptation, evolutionary potential and host–parasite coevolution: interactions between migration, mutation, population size and generation time. Journal of Evolutionary Biology 15, 451–462.Google Scholar
Guindon, S., Dufayard, J. F., Lefort, V., Anisimova, M., Hordijk, W. and Gascuel, O. (2010). New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3·0. Systematic Biology 59, 307–321.Google Scholar
Hanelt, B. and Janovy, J. Jr. (2002). Morphometric analysis of nonadult characters of common species of American gordiids (Nematomorpha: Gordioidea). Journal of Parasitology 88, 557–562.Google Scholar
Hanelt, B. and Janovy, J. Jr. (2003). Spanning the gap: experimental determination of paratenic host specificity of horsehair worms (Nematomorpha: Gordiida). Invertebrate Biology 122, 12–18.Google Scholar
Hanelt, B. and Janovy, J. Jr. (2004). Life cycle and paratenesis of American gordiids (Nematomorpha: Gordiida). Journal of Parasitology 90, 240–244.Google Scholar
Hanelt, B., Thomas, F. and Schmidt-Rhaesa, A. (2005). Biology of the phylum Nematomorpha. Advances in Parasitology 59, 243–305.Google Scholar
Hanelt, B., Schmidt-Rhaesa, A. and Bolek, M. G. (2015). Cryptic species of hairworm parasites revealed by molecular data and crowdsourcing of specimen collections. Molecular Phylogenetics and Evolution 82, 211–218.Google Scholar
Harkins, C., Shannon, R., Papeş, M., Schmidt-Rhaesa, A., Hanelt, B. and Bolek, M. G. (2016). Using Gordiid cysts to discover the hidden diversity, potential distribution, and new species of Gordiids (Phylum Nematomorpha). Zootaxa 4088, 515–530.Google Scholar
Heinze, K. (1935). Über das Genus Parachordodes Camerano, 1897 nebst allgemeinen Angaben über die Familie Chordodidae. Zeitschrift für Parasitenkunde 7, 657–678.Google Scholar
Henikoff, S. and Henikoff, J. G. (1992). Amino acid substitution matrices from protein blocks. Proceedings of the National Academy of Sciences of the United States of America 89, 10915–10919.Google Scholar
Hershey, A. E., Pastor, J., Peterson, B. J. and Kling, G. W. (1993). Stable isotopes resolve the drift paradox for Baetis mayflies in an arctic river. Ecology 74, 2315–2325.Google Scholar
Jarne, P. and Theron, A. (2001). Genetic structure in natural populations of flukes and snails: a practical approach and review. Parasitology 123, 27–40.Google Scholar
Katoh, K. and Standley, D. M. (2013). MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30, 772–780.Google Scholar
Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., Buxton, S., Cooper, A., Markowitz, S., Duran, C., Thierer, T., Ashton, B., Meintjes, P. and Drummond, A. (2012). Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28, 1647–1649.Google Scholar
Keeney, D. B., King, T. M., Rowe, D. L. and Poulin, R. (2009). Contrasting mtDNA diversity and population structure in a direct-developing marine gastropod and its trematode parasites. Molecular Ecology 18, 4591–4603.Google Scholar
Kimura, M. (1980). A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16, 111–120.Google Scholar
Kimura, M. and Weiss, G. H. (1964). The stepping stone model of population structure and the decrease of genetic correlation with distance. Genetics 49, 561–576.Google Scholar
King, K. J. (2015). Phylogeography, physiology and the evolution of melanism in the alpine tree wētā, Hemideina maori . Doctoral dissertation. University of Otago, Dunedin, New Zealand.Google Scholar
King, T. M., Kennedy, M. and Wallis, G. P. (2003). Phylogeographic genetic analysis of the alpine weta, Hemideina maori: evolution of a colour polymorphism and origins of a hybrid zone. Journal of the Royal Society of New Zealand 33, 715–729.Google Scholar
Kumar, S., Stecher, G. and Tamura, K. (2016). MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33, 1870–1874.Google Scholar
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, 1695–1701.Google Scholar
Leigh, J. W. and Bryant, D. (2015). POPART: full-feature software for haplotype network construction. Methods in Ecology and Evolution 6, 1110–1116.Google Scholar
Leisnham, P. T. and Jamieson, I. G. (2002). Metapopulation dynamics of a flightless alpine insect Hemideina maori in a naturally fragmented habitat. Ecological Entomology 27, 574–580.Google Scholar
MacNeale, K. H., Peckarsky, B. L. and Likens, G. E. (2005). Stable isotopes identify dispersal patterns of stonefly populations living along stream corridors. Freshwater Biology 50, 1117–1130.Google Scholar
Mazé-Guilmo, E., Blanchet, S., McCoy, K. D. and Loot, G. (2016). Host dispersal as the driver of parasite genetic structure: a paradigm lost? Ecology Letters 19, 336–347.Google Scholar
McCoy, K. D., Boulinier, T., Tirard, C. and Michalakis, Y. (2003). Host-dependent genetic structure of parasite populations: differential dispersal of seabird tick host races. Evolution 57, 288–296.Google Scholar
McCoy, K. D., Boulinier, T. and Tirard, C. (2005). Comparative host–parasite population structures: disentangling prospecting and dispersal in the black-legged kittiwake Rissa tridactyla . Molecular Ecology 14, 2825–2838.Google Scholar
McCulloch, G. A., Wallis, G. P. and Waters, J. M. (2010). Onset of glaciation drove simultaneous vicariant isolation of alpine insects in New Zealand. Evolution 64, 2033–2043.Google Scholar
Miller, M. A., Pfeiffer, W. and Schwartz, T. (2010). Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In Proceedings of the Gateway Computing Environments Workshop (GCE), New Orleans, LA, pp. 1–8.Google Scholar
Montgomery, T. H. (1898). The Gordiacea of certain American collections. Bulletin of the Museum of Comparative Zoology at Harvard University 32, 23–59.Google Scholar
Morand, S., Krasnov, B. R. and Littlewood, D. T. J. (eds) (2015). Parasite Diversity and Diversification: Evolutionary Ecology Meets Phylogenetics. Cambridge University Press, Cambridge, UK.Google Scholar
Müller, G. W. (1926). Über Gordiaceen. Zeitschrift für die Morphologie und Ökologie der Tiere 7, 134–270.Google Scholar
Müller, K. (1954). Investigations on the organic drift in North Swedish streams. Report of the Institute of Freshwater Research, Drottningholm 34, 133–148.Google Scholar
Nadler, S. A. (1995). Microevolution and the genetic structure of parasite populations. Journal of Parasitology 81, 395–403.Google Scholar
Pachepsky, E., Lutscher, F., Nisbet, R. M. and Lewis, M. A. (2005). Persistence, spread and the drift paradox. Theoretical Population Biology 67, 61–73.Google Scholar
Poinar, G. O. Jr. (1991). Hairworm (Nematomorpha: Gordioidea) parasites of New Zealand wetas (Orthoptera: Stenopelmatidae). Canadian Journal of Zoology 69, 1592–1599.Google Scholar
Poinar, G. O. Jr. (2009). Phylum Nematomorpha: horsehair worms, hairworms. In New Zealand Inventory of Biodiversity. Vol. 2, Kingdom Animalia: Chaetognatha, Ecdysozoa, Ichnofossils (ed. Gordon, D. P.), pp. 491–497. Canterbury University Press, Christchurch, NZ.Google Scholar
Poinar, G. Jr. and Brockerhoff, A. M. (2001). Nectonema zealandica n. sp. (Nematomorpha: Nectonematoidea) parasitising the purple rock crab Hemigrapsus edwardsi (Brachyura: Decapoda) in New Zealand, with notes on the prevalence of infection and host defence reactions. Systematic Parasitology 50, 149–157.Google Scholar
Poulin, R. (1995). Hairworms (Nematomorpha: Gordioidea) infecting New Zealand short-horned grasshoppers (Orthoptera: Acrididae). Journal of Parasitology 81, 121–122.Google Scholar
Poulin, R. (2007). Evolutionary Ecology of Parasites, 2nd Edn. Princeton University Press, Princeton, NJ.Google Scholar
Poulin, R. and Morand, S. (2004). Parasite Biodiversity. Smithsonian Institution Press, Washington, DC.Google Scholar
Price, P. W. (1980). Evolutionary Biology of Parasites. Princeton University Press, Princeton, NJ.Google Scholar
Prugnolle, F., Liu, H., De Meeûs, T. and Balloux, F. (2005 a). Population genetics of complex life-cycle parasites: an illustration with trematodes. International Journal for Parasitology 35, 255–263.Google Scholar
Prugnolle, F., Théron, A., Pointier, J. P., Jabbour-Zahab, R., Jarne, P., Durand, P. and Meeûs, T. D. (2005 b). Dispersal in a parasitic worm and its two hosts: consequence for local adaptation. Evolution 59, 296–303.Google Scholar
Ronquist, F. and Huelsenbeck, J. P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.Google Scholar
Sato, T., Watanabe, K., Tamotsu, S., Ichikawa, A. and Schmidt-Rhaesa, A. (2012). Diversity of nematomorph and cohabiting nematode parasites in riparian ecosystems around the Kii Peninsula, Japan. Canadian Journal of Zoology 90, 829–838.Google Scholar
Schmidt-Rhaesa, A. (2001). Variation of cuticular characters in the Nematomorpha: studies on Gordionus violaceus (Baird, 1853) and G. wolterstorffii (Camerano, 1888) from Britain and Ireland. Systematic Parasitology 49, 41–57.Google Scholar
Schmidt-Rhaesa, A. (2008). New data on New Zealand horsehair worms (Nematomorpha, Gordiida). Mitteilungen aus dem Hamburgischen Zoologischen Museum und Institut 105, 5–12.Google Scholar
Schmidt-Rhaesa, A. (2013). Nematomorpha. In Gastrotricha, Cycloneuralia, and Gnathifera, Vol. 1. Nematomorpha, Priapulida, Kinorhyncha, Loricifera (ed. Schmidt-Rhaesa, A.), pp. 29–146. Handbook of Zoology. de Gruyter, Berlin, Germany.Google Scholar
Schmidt-Rhaesa, A. and Schwarz, C. J. (2016). Nematomorpha from the Philippines, with description of two new species. Zootaxa 4158, 246–260.Google Scholar
Schmidt-Rhaesa, A., Thomas, F. and Poulin, R. (2000). Redescription of Gordius paranensis Camerano, 1892 (Nematomorpha), a species new for New Zealand. Journal of Natural History 34, 333–340.Google Scholar
Sørensen, M. V., Hebsgaard, M. B., Heiner, I., Glenner, H., Willerslev, E. and Kristensen, R. M. (2008). New data from an enigmatic phylum: evidence from molecular sequence data supports a sister-group relationship between Loricifera and Nematomorpha. Journal of Zoological Systematics and Evolutionary Research 46, 231–239.Google Scholar
Stamatakis, A. (2014). RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313.Google Scholar
Thomas, F., Schmidt-Rhaesa, A. and Poulin, R. (1999). Microhabitat characteristics and reproductive status of male Euchordodes nigromaculatus (Nematomorpha). Journal of Helminthology 73, 91–93.Google Scholar
Thomas, F., Schmidt-Rhaesa, A., Martin, G., Manu, C., Durand, P. and Renaud, F. (2002). Do hairworms (Nematomorpha) manipulate the water seeking behaviour of their terrestrial hosts? Journal of Evolutionary Biology 15, 356–361.Google Scholar
Trewick, S. A. (2008). DNA Barcoding is not enough: mismatch of taxonomy and genealogy in New Zealand grasshoppers (Orthoptera: Acrididae). Cladistics 24, 240–254.Google Scholar
Trewick, S. A. and Wallis, G. P. (2001). Bridging the “beech-gap”: New Zealand invertebrate phylogeography implicates Pleistocene glaciation and Pliocene isolation. Evolution 55, 2170–2180.Google Scholar
Trewick, S. A., Wallis, G. P. and Morgan-Richards, M. (2000). Phylogeographical pattern correlates with Pliocene mountain building in the alpine scree weta (Orthoptera, Anostostomatidae). Molecular Ecology 9, 657–666.Google Scholar
Trewick, S. A., Wallis, G. P. and Morgan-Richards, M. (2011). The invertebrate life of New Zealand: a phylogeographic approach. Insects 2, 297–325.Google Scholar
Walsh, P. S., Metzger, D. A. and Higuchi, R. (1991). Chelex 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. BioTechniques 10, 506–513.Google Scholar
White, E. G. (1978). Energetics and consumption rates of alpine grasshoppers (Orthoptera: Acrididae) in New Zealand. Oecologia 33, 17–44.Google Scholar
Winterbourn, M. J. (2005). Dispersal, feeding and parasitism of adult stoneflies (Plecoptera) at a New Zealand forest stream. Aquatic Insects 27, 155–166.Google Scholar
Winterbourn, M. J. and Pohe, S. R. (2016). Feeding and parasitism of adult Stenoperla spp. (Plecoptera: Eustheniidae) in New Zealand. Austral Entomology. doi:10.1111/aen.12222.Google Scholar
Zervos, S. (1989). Stadial and seasonal occurrence of gregarines and nematomorphs in two New Zealand cockroaches. New Zealand Journal of Zoology 16, 143–146.Google Scholar
Supplementary material: PDF

Tobias supplementary material

Tables and Figures

Download Tobias supplementary material(PDF)
PDF 456.9 KB