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New nematode species from the continental slope of New Zealand (Chromadorea, Microlaimida, and Chromadorida), and unexpected placement of the genus Molgolaimus Ditlevsen, 1921

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Abstract

The current nematode classification comprises three primarily marine basal Chromadorean orders: the Microlaimida Leduc et al., 2018; Desmodorida De Coninck, 1965; and Chromadorida Chitwood, 1933. The phylogenetic placement of several taxa within these orders, however, is unclear due to the paucity of taxonomically informative morphological characters for high-level classification and is yet to be tested by molecular phylogenetic analyses due to the absence of molecular sequences. Here, we describe Molgolaimus kaikouraensis sp. nov. and Aponema pseudotorosum sp. nov. from the continental slope of New Zealand and investigate phylogenetic relationships of these species and that of the rare desmodorid genera Onepunema and Pseudonchus, using SSU phylogenetic analyses for the first time. Whilst our analyses provided support for the current classification of Aponema within the family Microlaimidae and of Pseudonchus within the Desmodorida, we could not confirm relationships of Onepunema. We found no support for the placement of Molgolaimus with either the Desmodorida or Microlaimidae/Microlaimida as in the current and previous classifications. Instead, Molgolaimus was classified with the Chromadorida with moderate and strong support in maximum likelihood and Bayesian analyses, respectively. Congruence analysis suggests that in some cases at least, the structure of the female reproductive system is a more taxonomically informative trait for marine nematode classification than the male reproductive system or cuticle.

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References

  • Armenteros M, Ruiz-Abierno A, Decraemer W (2014) Revision of Desmodorinae and Spiriniinae (Nematoda: Desmodoridae) with redescription of eight known species. Eur J Taxon 96:1–32

  • Bik HM, Lambshead PJD, Kelley Thomas W, Hunt DH (2010) Moving towards a complete molecular framework of the Nematoda: a focus on the Enoplida and early–branching clades. BMC Evol Biol 10:353

    Article  PubMed  PubMed Central  Google Scholar 

  • Bradford-Grieve JM, Chang FH, Gall M, Pickmere S, Richards F (1997) Size–fractioned phytoplankton standing stocks and primary production during austral winter and spring 1993 in the subtropical convergence region near New Zealand. N Z J Mar Freshw Res 31:201–224

    Article  Google Scholar 

  • Carter L, Carter RM, Griggs GB (1982) Sedimentation in the Conway Trough, a deep–near–shore marine basin at the junction of the Alpine transform and Hikurangi subduction plate boundary, New Zealand. Sedimentology 29:475–497

    Article  Google Scholar 

  • Chitwood BG (1933) A revised classification of the Nematoda. J Parasitol 20:1–130

    Article  Google Scholar 

  • Cook AA, Badhury P, Debenham NJ, Meldal BHM, Blaxter ML, Smerdon GR, Austen MC, Lamnshead PJD, Rogers AD (2005) Denaturing gradient gel electrophoresis (DGGE) as a tool for identification of marine nematodes. Mar Ecol Prog Ser 291:103–113

    Article  CAS  Google Scholar 

  • Coomans A (1979) A proposal for a more precise terminology of the body regions in the nematode. Ann Soc Roy Zool Bel 108:115–117

  • De Coninck LA (1965) Systématique des Nématodes. In: Grassé PP (ed) Traité de Zoologie: Anatomie, Systématique, Biologie. Nemathelminthes (Nematodes). Masson et Cie, Paris, pp 586–531 731 pp

  • De Coninck LA, Schuurmans Stekhoven JH (1933) The freeliving marine nemas of the Belgian coast. II. With general remarks on the structure and the system of nemas. Mém Mus R Hist Nat Belg 58:3–163

  • De Leo FC, Smith CR, Rowden AA, Bowden DA, Clark MR (2010) Submarine canyons: hotspots of benthic biomass and productivity in the deep sea. Proc R Soc B 1695:2783–2792

    Article  Google Scholar 

  • De Ley P, Blaxter ML (2002) Systematic position and phylogeny. In: Lee DL (ed) The biology of nematodes. Taylor & Francis, London, pp 1–30

    Chapter  Google Scholar 

  • De Man JG (1889) Espèces et genres nouveaux de Nématodes libres de la mer du Nord et de la Manche. Mém Soc Zool France 2:1–10

  • de Man JG (1922) Neue freilebende Nematoden aus der Zuidersee. Tijdschr ned dierk Vereen 2:124–134

  • Ditlevsen H (1921) Papers from Dr. Th. Mortensens Pacific Expedition 1914-16. III Marine free-living Nematodes from the Auckland and Campbell Islands. Vidensk Med f Dansk natur Fori Kjøbenhavn 73:1–39

  • Edgar RC (2004a) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Edgar RC (2004b) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 19:5–113

    Google Scholar 

  • Filipjev IN (1917) Un nématode libre nouveau de la mer Caspienne, Chromadorissa gen. nov. (Chromadoridae, Chromadorini). Zool Zhurnal 2:24–30

    Google Scholar 

  • Filipjev IN (1918) Free-living marine nematodes of the Sevastopol area. Transactions of the Zoological Laboratory and the S evastopol Biological Station of the Russian Academy of Sciences 2:1–203

  • Filipjev IN (1922) New data on free nematodes of the Black Sea (Novye dannye o svobodnykh nematodakh Chernogo Moria.). Trudy Stavropol'skogo Sel'skokhoziaistvennogo Instituta 1:13–184

  • Filipjev IN (1929) Classification of free-living Nematoda and relations to parasitic forms. J Parasitol 15:281–282

  • Filipjev IN (1934) The classification of the free-living nematodes and their relation to the parasitic nematodes. Smithson Misc Coll 89:1–63

  • Fonseca G, Bezerra TN (2014) Order Araeolaimida De Coninck & Schuurmans Stekhoven, 1933. In: Shmidt-Rhaesa A (ed) Handbook of zoology, Gastrotricha, Cyclioneura and Gnathifera Volume 2: Nematoda. De Gruyter, Hamburg, pp 467–486

    Google Scholar 

  • Fonseca G, Vanreusel A, Decraemer W (2006) Taxonomy and biogeography of Molgolaimus (Ditlevsen, 1921 (Nematoda: Chromadoria)) with reference to the origins of deep–sea nematodes. Antarct Sci 18:23–50

    Article  Google Scholar 

  • Furstenberg J, Vincx M (1992) Two new species of the family Microlaimidae (Nematoda: order Chromadorida) from South-Africa. Cah Biol Mar 33:245–251

    Google Scholar 

  • Gerlach SA (1950) Die Nematoden-Gattung Microlaimus. Zoologische Jahrbücher. Abteilung für Systematik, Ökologie und Geographie der Tiere 79:188–208

  • Gerlach SA (1959) Neue Meeres-Nematoden aus dem Supralitoral der Deutschen Küsten. Internationele Revue der Gemsamten Hydrobiologie 44:463–467

    Article  Google Scholar 

  • Gerlach SA (1963) Freilebende meeresnematoden von den Malediven II. Kiel Meeresfosch 19:67–103

    Google Scholar 

  • Gerlach A, Riemann F (1973) The Bremerhaven checklist of aquatic nematodes. A catalogue of Nematoda Adenophorea excluding the Dorylaimida. Part 1. Veröff Inst Meer Bremerhaven 4:1–736

  • Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321

    Article  CAS  PubMed  Google Scholar 

  • Holterman M, Van Der Wurff A, Van Den Elsen S, Van Megen H, Bongers T, Holovachov O, Bakker J, Helder J (2006) Phylum-wide analysis of SSU rDNA reveals deep phylogenetic relationships among nematodes and accelerated evolution toward crown clades. Mol Biol Evol 13:1792–1800

    Article  CAS  Google Scholar 

  • Holterman M, Holovachov O, van den Elsen S, van Megen H, Bongers T, Bakker J, Helder J (2008) Small subunit ribosomal DNA-based phylogeny of basal Chromadoria (Nematoda) suggests that transitions from marine to terrestrial habitats (and vice versa) require relatively simple adaptations. Mol Phylogenet Evol 48:758–763

    Article  CAS  PubMed  Google Scholar 

  • Jensen P (1978) Revision of Microlaimidae, erection of Molgolaimidae fam. N., and remarks on the systematic position of Paramicrolaimus (Nematoda, Desmodorida). Zool Scr 7:159–173

    Article  Google Scholar 

  • Jensen P (1988) Four new nematode species, abundant in the deep-sea benthos of the Norwegian Sea. Sarsia 73:149–155

    Article  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, Mentjies P, Drummond A (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649

    Article  PubMed  PubMed Central  Google Scholar 

  • Leduc D, Verschelde D (2013) One new genus and two new free–living nematode species (Desmodorida, Desmodoridae) from the continental margin of New Zealand, Southwest Pacific. Zootaxa 3609:274–290

    Article  PubMed  Google Scholar 

  • Leduc D, Verschelde D (2015) New Spirinia and Stygodesmodora species (Nematoda, Spiriniinae) from the Southwest Pacific, and a revision of the related genera Spirinia, Chromaspirina and Perspiria. Eur J Taxon 118:1–25

  • Leduc D, Wharton DA (2008) Three new species of free-living nematodes from inter-tidal sediments in southern New Zealand. Nematology 10:743–755

    Article  Google Scholar 

  • Leduc D, Rowden AA, Nodder SD, Berkenbusch K, Probert PK, Hadfield MG (2014) Unusually high food availability in Kaikoura canyon linked to distinct deep–sea nematode community. Deep–Sea Res II 104:310–318

    Article  Google Scholar 

  • Leduc D, Verdon V, Zhao ZQ (2018) Phylogenetic position of the Paramicrolaimidae, description of a new Paramicrolaimus species and erection of a new order to accommodate the Microlaimoidea (Nematoda: Chromadorea). Zool J Linnaean Soc 183:52–69

    Article  Google Scholar 

  • Lorenzen S (1971) Die Nematodenfauna im Verklappungsgebiet für Industrieabwässer nordwestlich von Helgoland: I. Araeolaimida und Monhysterida. Zool Anz 187:223–248

    Google Scholar 

  • Lorenzen S (1973) Freilebende Meeresnematoden aus dem sublittoral der Nordsee und der Kieler Bucht. Veröff Inst Meer Bremerhaven 14:103–130

  • Lorenzen S (1981) Entwurf eines phylogenetischen Systems der freilebenden Nematoden. Veröff Inst Meer Bremerhaven 7:472S

  • Meldal BHM, Debenham NJ, De Ley P, De Ley IT, Vanfleteren JR, Vierstraete AR, Bert W, Borgonie G, Moens T, Tyler PA, Austen MC, Blaxter ML, Rogers AD, Lambshead PJD (2007) An improved molecular phylogeny of the Nematoda with special emphasis on marine taxa. Mol Phylogenet Evol 42:622–636

    Article  CAS  PubMed  Google Scholar 

  • Micoletzky H (1922) Die freilebenden Erdnematoden. Archiv für Naturgeschichte 87A:1–650

  • Micoletzky H (1923) Freilebende Nematoden der Wolga mit besonderer Berücksichtigung der Umgebung von Saratow. Arbeiten der Biologischen Wolga-Station 7:3–29

  • Miljutin DM, Miljutina MA (2009) Deep-sea nematodes of the family Microlaimidae from the Clarion-Clipperton Fracture Zone (North-Eastern Tropic Pacific), with the descriptions of three new species. Zootaxa 2096:137–172

    Article  Google Scholar 

  • Murphy DG (1966) An initial report on a collection of Chilean marine nematodes. Mitteilungen der Hamburger Zoologische Museum Institut 63:29–50

    Google Scholar 

  • Murphy RJ, Pinkerton MH, Richardson KM, Bradford-Grieve JM (2001) Phytoplankton distributions around New Zealand derived from SeaWiFS remote–sensed ocean colour data. N Z J Mar Freshw Res 35:343–362

    Article  Google Scholar 

  • Muthumbi AW, Vincx M (1996) Nematodes from the Indian Ocean: description of six new species of the genus Molgolaimus Ditlevsen, 1921 (Nematoda: Desmodoridae). Bull Inst R Sciences Nat Belg Bio 66:17–28

  • Muthumbi AW, Vincx M (1999) Microlaimidae (Microlaimoidea: Nematoda) from the Indian Ocean: description of nine new and known species. Hydrobiologia 397:39–58

    Article  Google Scholar 

  • Nunn GB (1992) Nematode molecular evolution. Ph.D. Thesis, University of Nottingham, UK

  • Nylander JAA (2004) MrModeltest 2.3. Program distributed by the author. Evolutionary Biology Centre. Uppsala University, Uppsala

    Google Scholar 

  • Pastor de Ward CT (1980) Aponema papillatum sp. nov., nueva especie de nematode marino de puerto deseado, (Santa Cruz, Argentina). Centro de Investigacion de Biologia Marina Contribucion Cientifica 160:1–11

  • Platt HM (1973) Freeliving marine nematodes from Strangford Lough, Northern Ireland. Cah Biol Mar 14:295–321

    Google Scholar 

  • Portnova D (2009) Free-living nematodes from the deep-sea Hakon Mosby mud volcano, including the description of two new and three known species. Zootaxa 2096:197–213

    Article  Google Scholar 

  • Rambaut A, Drummond AJ (2007) Tracer v 1.4, Available from http://beast.bio.ed.ac.uk/Tracer

  • Revkova TN (2017) Two new species of free–living nematode genera Microlaimus de Man, 1880 and Aponema Jensen, 1978 (Nematoda: Microlaimidae) from the Black Sea. Zootaxa 4344:387–394

    Article  PubMed  Google Scholar 

  • Shi B, Xu K (2017) Spirobolbolaimus undulatus sp. nov. in intertidal sediment from the East China Sea, with transfer of two Microlaimus species to Molgolaimus (Nematoda, Desmodorida). J Mar Biol Assoc U K 97:1335–1342

    Article  Google Scholar 

  • Somerfield PJ, Warwick RM (1996) Meiofauna in marine pollution monitoring Programmes: a laboratory manual. Ministry of Agriculture, Fisheries and Food, Lowestoft

    Google Scholar 

  • Swofford DL (2002) PAUP*. Phylogentic analysis using parsimony (* and other methods). Version 4.0b10. Sinauer associates, Sunderland, MA

  • Tchesunov AV (2014) Order Chromadorida Chitwood, 1933. In: Scmidt-Rhaesa A (ed) Handbook of Zoology, Gastrotricha, Cyclioneuralia and Gnathifera. Volume 2: Nematoda. CABI Publishing, Cambridge

    Google Scholar 

  • Timm RW (1961) The marine nematodes of the bay of Bengal. Proc Pak Academy Science 1:25–88

  • van Megen H, van den Elsen S, Holterman M, Karssen G, Mooyman P, Bongers T, Holovachov O, Bakker J, Helder J (2009) A phylogenetic tree of nematodes based on about 1200 full-length small subunit ribosomal DNA sequences. Nematology 11:927–950

    Article  CAS  Google Scholar 

  • Vitiello P (1970) Nématodes libres marins des vases profondes du Golfe du Lion. II Chromadorida. Téthys 2:449–500

    Google Scholar 

  • Vitiello P (1973) Nouvelles espèces de Desmodorida (Nematoda) des côtes de Provence. Téthys 5:137–146

    Google Scholar 

  • Warwick RM (1970) Fourteen new species of free-living marine nematodes from the Exe estuary. Bull Br Mus Nat Hist 19:137–177

    Google Scholar 

  • Wieser W (1954) Free-living marine nematodes II. Chromadoroidea. Acta Universitets Lunds 50:1–148

  • Zheng JW, Subbotin SA, He SS, Gu JF, Moens M (2002) Molecular characterisation of some Asian isolates of Bursaphelenchus xylophilus and B. mucronatus using PCR-RFLPs and sequences of ribosomal DNA. Russ J Nematol 11:17–22

    Google Scholar 

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Acknowledgements

We thank the crew and scientific personnel of RV Tangaroa (voyages TAN1701 and TAN1708). We thank two anonymous reviewers for providing constructive criticisms on the manuscript.

Funding

This research was funded by the NIWA under Coasts and Oceans Research programme 2 (2018/19 SCI) and supported by core funding for Crown Research Institutes from the Science and Innovation Group of the Ministry of Business, Innovation and Employment.

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Authors and Affiliations

  1. National Institute of Water and Atmospheric Research, Wellington, 14-901, New Zealand

    Daniel Leduc

  2. Key Laboratory of the Ministry of Education for Coastal and Wetland Ecosystems, Xiamen University, Xiamen, 361102, China

    Sujing Fu

  3. Landcare Research, Private Bag 92170, Auckland Mail Centre, Auckland, 1142, New Zealand

    Zeng Qi Zhao

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  1. Daniel Leduc
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  2. Sujing Fu
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  3. Zeng Qi Zhao
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Correspondence to Daniel Leduc.

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All necessary permits for sampling and observational field studies have been obtained by the authors from the competent authorities and are mentioned in the acknowledgements, if applicable. The study is compliant with CBD and Nagoya protocols.

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Communicated by M. Schratzberger

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This article is registered in ZooBank under urn:lsid:zoobank.org:pub: D17A8CBD-01EB-4B38-A954-E91E7FF1788F.

Aponema pseudotorosum is registered under urn:lsid:zoobank.org:act: C77EECD9-EB73-45D7-AABA-EFA2C0D23BFC.

Molgolaimus kaikouraensis is registered under urn:lsid:zoobank.org:act:7EF1D501-92E7-4CF5-BBE2-C099FB73B591.

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Leduc, D., Fu, S. & Zhao, Z.Q. New nematode species from the continental slope of New Zealand (Chromadorea, Microlaimida, and Chromadorida), and unexpected placement of the genus Molgolaimus Ditlevsen, 1921. Mar Biodiv 49, 2267–2280 (2019). https://doi.org/10.1007/s12526-019-00961-z

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