Skip to main content Skip to main navigation menu Skip to site footer
Type: Article
Published: 2020-07-01
Page range: 38–50
Abstract views: 116
PDF downloaded: 4

Genetic variability of Arthurdendyus triangulatus (Dendy, 1894), a non-native invasive land planarian

The James Hutton Institute, Dundee, DD2 5DA, Scotland, UK
The James Hutton Institute, Dundee, DD2 5DA, Scotland, UK
University of Dundee, Dundee, DD1 4HN, Scotland, UK
University of Dundee, Dundee, DD1 4HN, Scotland, UK
Biomathematics and Statistics Scotland, Dundee, DD2 5DA, Scotland, UK
The James Hutton Institute, Dundee, DD2 5DA, Scotland, UK
Platyhelminthes citizen science flatworm invasive species ITS-1 molecular diversity numt

Abstract

Arthurdendyus triangulatus (Dendy, 1894) is a land planarian native to New Zealand which has become established in the United Kingdom and the Faroe Islands during the last 60 years. The species has become prevalent and widely established in Scotland mediated by human activity mostly through the exchange of plants and associated soil. As a predator of earthworms, concerns regarding both the direct impact on earthworm abundance and diversity and the indirect impact on those birds and mammals that have earthworms as a primary dietary component led to A. triangulatus being the subject of both national and EU regulation. Whilst much is known regarding the ecology of A. triangulatus there is a significant knowledge gap regarding the genetic variability of the species. Using four DNA target regions cytochrome oxidase (CoI), elongation factor (EF), internal transcribed spacer region (ITS-1) and large subunit (LSU), we characterised the genetic variability of A. triangulatus populations across its full geographic range in Scotland and included a few populations from New Zealand, England and Northern Ireland.

                Two DNA regions, ITS-1 and CoI, revealed inter-population variability yielding well supported genetic structure in predominantly Scottish populations. We also identified considerable intra-specific and intra-individual heterogeneity in both ribosomal and mitochondrial regions, including the prevalence of pseudo-gene nuclear encoded mitochondrial DNA (Numt), the latter not previously reported for Platyhelminthes. Furthermore, given the presence of multiple ITS-1 haplotypes in individual specimens of A. triangulatus it is not possible to make definitive comment to support previously published findings that A. triangulatus was subjected to multiple introductions into the UK.

References

  1. Altschul, S.F., Gish, W., Miller, W., Myers, E.W. & Lipman, D.J. (1990) Basic local alignment search tool. Journal of Molecular Biology, 215, 403–410.

    https://doi.org/10.1016/S0022-2836(05)80360-2

    Baeza, J.A. & Fuentes, M.S. (2013) Exploring phylogenetic informativeness and nuclear copies of mitochondrial DNA (numts) in three commonly used mitochondrial genes: mitochondrial phylogeny of peppermint, cleaner and semi-terrestrial shrimps (Caridea: Lysmata, Exhippolysmata and Merguia). Zoological Journal of the Linnean Society, 168, 699–722.

    https://doi.org/10.1111/zoj.12044

    Baird, J., Fairweather, I. & Murchie, A.K. (2005a) Long-term effects of prey-availability, partnering and temperature on overall egg capsule output of ‘New Zealand flatworms’, Arthurdendyus triangulatus. Annals of Applied Biology, 146, 289–301.

    https://doi.org/10.1111/j.1744-7348.2005.040095.x

    Baird, J., McDowell, S.D.R., Fairweather, I. & Murchie, A.K. (2005b) Reproductive structures of Arthurdendyus triangulatus (Dendy): seasonality and the effect of starvation. Pedobiologia, 49, 435–442.

    https://doi.org/10.1016/j.pedobi.2005.05.003

    Bensasson, D., Zhang, D.-X. & Hewitt, G.M. (2000) Frequent assimilation of mitochondrial DNA by grasshopper nuclear genomes. Molecular Biology and Evolution, 17, 406415.

    https://doi.org/10.1093/oxfordjournals.molbev.a026320

    Blackshaw, R.P. (1990) Studies on Artioposthia triangulata (Dendy) (Tricladida: Terricola), a predator of earthworms. Annals of Applied Biology, 116, 169–176.

    https://doi.org/10.1111/j.1744-7348.1990.tb06596.x

    Blackshaw, R.P. (1992) The effect of starvation on size and survival of the terrestrial planarian Artioposthia triangulata (Dendy) (Tricladida, Terricola). Annals of Applied Biology, 120, 573–578.

    https://doi.org/10.1111/j.1744-7348.1992.tb04917.x

    Blackshaw, R.P. (1995) Changes in populations of the predatory flatworm Artioposthia triangulata and its earthworm prey in grassland. Acta Zoologica Fennica, 196, 107–110.

    Blackshaw, R.P. & Stewart, V.I. (1992) Artioposthia triangulata (Dendy, 1894), a predatory terrestrial planarian and its potential impact on lumbricid earthworms. Agricultural Zoology Reviews, 5, 201–219.

    Blair, D. (2006) Ribosomal DNA variation in parasitic flatworms. In: Maule, A.G. & Marks, N.J. (Eds.), Parasitic flatworms: molecular biology, biochemistry, immunology and physiology. CABI, Oxon, pp. 96–124.

    https://doi.org/10.1079/9780851990279.0096

    Boag, B. & Neilson, R. (2014) The spread and movement of the New Zealand flatworm (Arthurdendyus triangulatus) in Scotland. Proceedings Crop Protection in Northern Britain, 2014, 55–59.

    Boag, B. & Neilson, R. (2019) The potential detrimental impact of the New Zealand flatworm to Scottish islands. In: Veitch, C.R., Clout, M.N., Martin, A.R., Russell, J.C. & West, C.J. (Eds.), Island Invasives: Scaling up to Meet the Challenge. IUCN, Gland, pp. 352–355.

    Boag, B., Jones, H.D. & Neilson, R. (1997) The spread of the New Zealand flatworm (Artioposthia triangulata) within Great Britain. European Journal of Soil Biology, 33, 53–56.

    Boag, B., Neilson, R. & Scrimgeour, C.M. (2006) Degrowth phenomenon in the planarian Arthurdendyus triangulatus (Tricladida: Terricola) as measured by stable isotopes. Biology and Fertility of Soils, 43, 267–270.

    https://doi.org/10.1007/s00374-006-0108-3

    Boag, B., Deeks, L., Orr, A. & Neilson, R. (2005) A spatio-temporal analysis of a New Zealand flatworm (Arthurdendyus triangulatus) population in western Scotland. Annals of Applied Biology, 147, 81–88.

    https://doi.org/10.1111/j.1744-7348.2005.00017.x

    Boag, B., Jones, H.D., Neilson, R. & Santoro, G. (1999) Spatial distribution and relationship between the New Zealand flatworm, Arthurdendyus triangulatus and earthworms in a grass field in Scotland. Pedobiologia, 43, 340–344.

    Boag, B., Palmer, L.F., Neilson, R. & Chambers, S.J. (1994) Distribution and prevalence of the predatory planarian Atrioposthia triangulata (Dendy) (Tricladida: Terricola) in Scotland. Annals of Applied Biology, 124, 165–171.

    https://doi.org/10.1111/j.1744-7348.1994.tb04124.x

    Boag, B., Evans, K.A., Yeates, G.W., Johns, P.M. & Neilson, R. (1995a) Assessment of the global potential distribution of the predatory land planarian Artioposthia triangulata (Dendy) (Tricladida: Terricola) using ecoclimatic data. New Zealand Journal of Zoology, 22, 311–318.

    https://doi.org/10.1080/03014223.1995.9518046

    Boag, B., Jones, H.D., Evans, K.A., Neilson, R., Yeates, G.W. & Johns, P.M. (1998) The application of GIS techniques to estimate the establishment and spread of Artioposthia triangulata in Scotland. Pedobiologia, 42, 504–510.

    Boag, B., Evans, K.A., Neilson, R., Yeates, G.W., Johns, P.M., Mather, J.C., Christensen, O.M. & Jones, H.D. (1995b) The potential spread of terrestrial planarians Artioposthia triangulata and Australoplana sanguinea var. alba to continental Europe. Annals of Applied Biology, 127, 385–390.

    https://doi.org/10.1111/j.1744-7348.1995.tb06682.x

    Buhay, J.E. (2009) ‘COI-like’ sequences are becoming problematic in molecular systematic and DNA barcoding studies. Journal of Crustacean Biology, 29, 96–110.

    https://doi.org/10.1651/08-3020.1

    Carbayo, F., Álvarez-Presas, M., Jones, H.D. & Riutort, M. (2016) The true identity of Obama (Platyhelminthes: Geoplanidae) flatworm spreading across Europe. Zoological Journal of the Linnean Society, 177, 5–28.

    Carbayo, F., Álvarez-Presas, M., Olivares, C.T., Marques, F.P.L., Froehlich, E.M. & Riutort, M. (2013) Molecular phylogeny of Geoplaninae (Platyhelminthes) challenges current classification: proposal of taxonomic actions. Zoologica Scripta, 42, 508–528.

    https://doi.org/10.1111/zsc.12019

    Cardoso, J.M.S., Fonseca, L. & Abrantes, I. (2011) Genetic diversity of ITS sequences of Bursaphelenchus xylophilus. Genetics and Molecular Research, 11, 4508–4515.

    Carranza, S., Baguñà, J. & Riutort, M. (1999) Origin and evolution of paralogous rRNA gene clusters within the flatworm family Dugesiidae (Platyhelminthes, Tricladida). Journal of Molecular Evolution, 49, 250–259.

    https://doi.org/10.1007/PL00006547

    Christensen, O.M. & Mather, J.G. (1995) Colonisation by the land planarian Artioposthia triangulata and impact on lumbricid earthworms at a horticultural site. Pedobiologia, 39, 144–154.

    Dick, J.T.A., Alexander, M.E., Jeschke, J.M., Ricciardi, A., MacIsaac, H.J., Robinson, T.B., Kumschick, S., Weyl, O.L.F., Dunn, A.M. & Hatcher, M.J. (2014) Advancing impact prediction and hypothesis testing in invasion ecology using a comparative functional response approach. Biological Invasions, 16, 735–753.

    https://doi.org/10.1007/s10530-013-0550-8

    Dynes, C., Fleming, C.C. & Murchie, A.K. (2001) Genetic variation in native and introduced populations of the ‘New Zealand flatworm’, Arthurdendyus triangulatus. Annals of Applied Biology, 139, 165–174.

    https://doi.org/10.1111/j.1744-7348.2001.tb00393.x

    Emelyanov, V.V. (2001) Rickettsiaceae, rickettsia-like endosymbionts, and the origin of mitochondria. Bioscience Reports, 21, 1–17.

    https://doi.org/10.1023/A:1010409415723

    EPPO (2001a) Guidelines on Arthurdendyus triangulatus. EPPO Bulletin, 31, 1–3.

    https://doi.org/10.1111/j.1365-2338.2001.tb00958.x

    EPPO (2001b) Import requirements concerning Arthurdendyus triangulatus. EPPO Bulletin, 31, 5–6.

    EPPO (2001c) Nursery inspection, exclusion and treatment for Arthurdendyus triangulatus. EPPO Bulletin, 31, 7–10.

    Erpenbeck, D., Voigt, O., Adamski, M., Woodcroft, B.J., Hooper, J.N.A., Wörheide, G. & Degnan, B.M. (2011) NUMTs in the sponge genome reveal conserved transposition mechanisms in metazoans. Molecular Biology and Evolution, 28, 1–5.

    https://doi.org/10.1093/molbev/msq217

    Gandolfi, A., Bonilauri, P., Rossi, V. & Menozzi, P. (2001) Intraindividual and intraspecies variability of ITS1 sequences in the ancient asexual Darwinula stevensoni (Crustacea: Ostracoda). Heredity, 87, 449–455.

    https://doi.org/10.1046/j.1365-2540.2001.00927.x

    Handley, L.L. (2015) How will the ‘molecular revolution’ contribute to biological recording? Biological Journal of the Linnean Society, 115, 750–766.

    Hulme, P.E. (2009) Trade, transport and trouble: managing invasive species pathways in an era of globalization. Journal of Applied Ecology, 46, 10–18.

    https://doi.org/10.1111/j.1365-2664.2008.01600.x

    Johns, P.M. & Boag, B. (2003) The spread and distribution of terrestrial planarians (Turbellaria: Tricladida: Geoplanidae) within New Zealand. New Zealand Journal of Ecology, 27, 201–206.

    Jones, H.D. & Boag, B. (1996) The distribution of New Zealand and Australian terrestrial flatworms (Platyhelminthes: Turbellaria: Tricladida: Terricola) in the British Isles—the Scottish survey and MEGALAB WORMS. Journal of Natural History, 30, 955–975.

    https://doi.org/10.1080/00222939600770511

    Jones, H.D., Santoro, G., Boag, B. & Neilson, R. (2001) The diversity of earthworms in 200 Scottish fields and the possible effect of New Zealand land flatworms (Arthurdendyus triangulata) on earthworm populations. Annals of Applied Biology, 139, 75–92.

    https://doi.org/10.1111/j.1744-7348.2001.tb00132.x

    Justine, J., Winsor, L., Gey, D., Gros, P. & Thévenot, J. (2014) The invasive New Guinea flatworm Platydemus manokwari in France, the first record for Europe: time for action is now. PeerJ, 2, e297.

    https://doi.org/10.7717/peerj.297

    Justine, J., Winsor, L., Barriere, P., Fanai, C., Gey, D., Han, A.W.K., La Quay-Velazquez, G., Lee, B.P.Y.H., Lefevre, J.-M. & Meyer, J.-Y. (2015) The invasive land planarian Platydemus manokwari (Platyhelminthes, Geoplanidae): records from six new localities, including the first in the USA. PeerJ, 3, e1037.

    https://doi.org/10.7717/peerj.1037

    Karanth, K.P. (2008) Primate numts and reticulate evolution of capped and golden leaf monkeys (Primates: Colobinae). Journal of Bioscience, 33, 761–770.

    https://doi.org/10.1007/s12038-008-0096-6

    Katoh, K. & Standley, D.M. (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution, 30, 772–780.

    Králová-Hromadová, I., Štefka, J., Špakulová, M., Orosová, M., Bombarová, M., Hanzelová, V., Bazsalovicsová, E. & Scholz, T. (2010) Intra-individual internal transcribed spacer 1 (ITS1) and (ITS2) ribosomal sequence variation linked with multiple rDNA loci: A case of triploid Atractolytocestus huronensis, the monozoic cestode of common carp. International Journal of Parasitology, 40, 175-181.

    Kulhanek, S.A., Ricciardi, A. & Leung, B. (2011) Is invasion history a useful tool for predicting the impacts of the world’s worst aquatic invasive species? Ecological Applications, 21, 189–202.

    https://doi.org/10.1890/09-1452.1

    Littlewood, D.T.J. (2008) Platyhelminth systematics and the emergence of new characters. Parasite, 15, 333–341.

    https://doi.org/10.1051/parasite/2008153333

    Lopez, J.V., Yuhki, N., Masuda, R., Modi, W. & O’Brien, S.J. (1994) Numt: a recent transfer and tandem amplification of mitochondrial DNA to the nuclear genome of the domestic cat. Journal of Molecular Evolution, 39, 174–190.

    Milne, I., Lindner, D., Bayer, M., Husmeier, D., McGuire, G., Marshall, D.F. & Wright, F. (2009) TOPALI v2: a rich graphical interface for evolutionary analyses of multiple alignments on HPC clusters and multi-core desktops. Bioinformatics, 25, 126–127.

    https://doi.org/10.1093/bioinformatics/btn575

    Mourier, T., Hansen, A.J., Willerslev, E. & Arctander, P. (2001) The human genome project reveals a continuous transfer of large mitochondrial fragments to the nucleus. Molecular Biology and Evolution, 18, 1833–1837.

    https://doi.org/10.1093/oxfordjournals.molbev.a003971

    Murchie, A.K. & Gordon, A.W. (2013) The impact of the ‘New Zealand flatworm’, Arthurdendyus triangulatus, on earthworm populations in the field. Biological Invasions, 15, 569–586.

    https://doi.org/10.1007/s10530-012-0309-7

    Ricciardi, A. & Cohen, J. (2007) The invasiveness of an introduced species does not predict its impact. Biological Invasions, 9, 309-315.

    https://doi.org/10.1007/s10530-006-9034-4

    Rice, P., Longden, I. & Bleasby, A. (2000) EMBOSS: the European Molecular Biology Open Software Suite. Trends in Genetics, 16, 276–277.

    https://doi.org/10.1016/S0168-9525(00)02024-2

    Roques, A., Rabitsch, W., Rasplus, J.-Y., Lopez-Vamonde, C., Nentwig, W. & Kenis, M. (2009) Alien terrestrial invertebrates of Europe. Handbook of Alien Species in Europe. Springer, Berlin, pp. 63–79.

    Shen, P.P., Zhou, H. & Gu, J.-G. (2012) Novel polymorphism of internal transcribed spacers (ITS) and their utilization in phylogenetic analysis of Neanthes glandicincta (Annelida: Polychaeta: Nereididae). Ecotoxicology, 21, 1717–1725.

    https://doi.org/10.1007/s10646-012-0959-3

    Shine, C., Kettunen, M., ten Brink, P., Genovesi, P. & Gollasch, S. (2009) Technical support to EU strategy on invasive species (IAS)—Recommendations on policy options to control the negative impacts of IAS on biodiversity in Europe and the EU. Final report for the European Commission. Institute for European Environmental Policy (IEEP), Brussels, 35 pp.

    Sluys, R. (2016) Invasion of the flatworms. American Scientist, 104, 288–295.

    https://doi.org/10.1511/2016.122.288

    Song, H., Buhay, J.E., Whiting, M.F. & Crandall, K.A. (2008) Many species in one: DNA barcoding overestimates the number of species when nuclear mitochondrial pseudogenes are coamplified. Proceedings of the National Academy of Science USA, 105, 13486–13491.

    https://doi.org/10.1073/pnas.0803076105

    Sunnucks, P., Blacket, M.J., Taylor, J.M., Sands, C.J., Ciavaglia, S.A., Garrick, R.C., Tait, N.N., Rowell, D.M. & Pavlova, A. (2006) A tale of two flatties: different responses of two terrestrial flatworms to past environmental climatic fluctuations at Tallaganda in montane southeastern Australia. Molecular Ecology, 15, 4513–4531.

    https://doi.org/10.1111/j.1365-294X.2006.03107.x

    Telford, M.J., Herniou, E.A., Russell, R.B. & Littlewood, D.T. (2000) Changes in mitochondrial genetic codes as phylogenetic characters: two examples from the flatworms. Proceedings of the National Academy of Science USA, 97, 11359–11364.

    https://doi.org/10.1073/pnas.97.21.11359

    Vié, J.C., Hilton-Taylor, C. & Stuart, S.N. (2008) The 2008 review of the IUCN Red List of threatened species. IUCN, Gland, 157 pp.

    Wernersson, R. (2006) Virtual Ribosome—a comprehensive DNA translation tool with support for integration of sequence feature annotation. NAS, web server issue 34, W385–W388.

    https://doi.org/10.1093/nar/gkl252

    Williams, S.T. & Knowlton, N. (2001) Mitochondrial pseudogenes are pervasive and often insidious in the snapping shrimp genus Alpheus. Molecular Biology and Evolution, 18, 1484–1493.

    https://doi.org/10.1093/oxfordjournals.molbev.a003934

    Winsor, L., Johns, P.M. & Barker, G.M. (2004) Terrestrial planarians (Platyhelminthes: Tricladida: Terricola) predaceous on terrestrial gastropods. In: Barker, G.M. (Ed.), Natural Enemies of Terrestrial Molluscs. CABI, Oxfordshire, pp. 227–278.

    https://doi.org/10.1079/9780851993195.0227

    Wolff, J.N., Shearman, D.C.A., Brooks, R.C. & Ballard, J.W.O. (2012) Selective enrichment and sequencing of whole mitochondrial genomes in the presence of nuclear encoded mitochondrial pseudogenes (Numts). Plos One, 7, e37142.

    https://doi.org/10.1371/journal.pone.0037142

    Zischler, H. (2000) Nuclear integrations of mitochondrial DNA in primates: inference of associated mutational events. Electrophoresis, 21, 531–536.

    https://doi.org/10.1002/(SICI)1522-2683(20000201)21:3%3C531::AID-ELPS531%3E3.0.CO;2-P