Combining morphological and molecular data to classify Laxus sakihariiae sp. n., a new stilbonematine nematode (Nematoda: Desmodoridae) from the coast of Sesoko Island, Japan

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Because of their relatively simple body plan, the number of morphological characters used to differentiate between closely related nematode genera is often limited. In addition, boundaries among genera sometimes become blurred due to the appearance of new trait combinations as more new species are described. Molecular phylogenetic analyses can address the shortcomings of morphological taxonomy by clarifying relationships among closely related species and genera and can help identify which morphological characters are taxonomically informative. Here, we describe Laxus sakihariiae sp. n. from shallow subtidal sands on Sesoko Island in the Okinawa prefecture, investigate phylogenetic relationships with other stilbonematine species and genera based on SSU rDNA sequences, and provide the first LSU rDNA sequence for the subfamily. The new species can be easily distinguished from all other species of the genus by the presence in the male of subventral and ventral rows of stout and spine-like setae in the pre- and postcloacal regions. This feature suggests affinities with the closely related genus Leptonemella, although the SSU consensus tree clearly shows that the new species forms a monophyletic clade together with the other Laxus species for which sequences are available. The structure of the cephalic capsule in L. sakihariiae sp. n., which consists of a block layer between the median and basal zones of the cephalic cuticle, is consistent with the placement of this species. This trait is not currently used as a diagnostic feature, but our finding suggests that the structure of the cephalic capsule may be taxonomically useful for differentiating between some stilbonematine genera.

Combining morphological and molecular data to classify Laxus sakihariiae sp. n., a new stilbonematine nematode (Nematoda: Desmodoridae) from the coast of Sesoko Island, Japan

in Nematology

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References

ArmenterosM.Ruiz-AbiernoA.DecraemerW. (2014a). Taxonomy of Stilbonematinae (Nematoda: Desmodoridae): description of two new and three known species and phylogenetic relationships within the family. Zoological Journal of the Linnaean Society 1711-21. DOI: 10.1111/zoj.12126

ArmenterosM.Rojas-CorzoA.Ruiz-AbiernoA.DeryckeS.BackeljauT.DecraemerW. (2014b). Systematics and DNA barcoding of free-living marine nematodes with emphasis on tropical desmodorids using nuclear SSU rDNA and mitochondrial COI sequences. Nematology 16979-989. DOI: 10.1163/15685411-00002824

Bauer-NebelsickM.BlumerM.UrbancikW.OttJ.A. (1995). The glandular sensory organ of Desmodoridae (Nematoda): ultrastructure and phylogenetic implications. Invertebrate Biology 114211-219. DOI: 10.2307/3226876

BoucherG. (1975). Nématodes des sables fins infralittoraux de la Pierre Noire (Manche Occidentale). I. Desmodorida. Bulletin du Muséum National d’Histoire Naturelle 285101-128.

BulgheresiS.SchabussovaI.ChenT.MullinN.P.MaizelsR.M.OttJ.A. (2006). A new c-type lectin similar to human immunoreceptor DC-SIGN mediates symbiont acquisition by a marine nematode. Applied and Environmental Microbiology 722950-2956. DOI: 10.1128/AEM.72.4.2950-2956.2006

ChitwoodB.G. (1936). Some marine nematodes from North Carolina. Proceedings of the Helminthological Society of Washington 31-16.

CobbN.A. (1894). Tricoma and other new nematode genera. The Proceedings of the Linnean Society of New South Wales 8389-421.

CobbN.A. (1914). Antarctic marine free-living nematodes of the Shackleton Expedition. Contributions to a Science of Nematology 13-33.

CobbN.A. (1920). One hundred new nemas: type species of 100 new genera. Contributions to a Science of Nematology 9217-343.

CoomansA. (1979). A proposal for a more precise terminology of the body regions in the nematode. Annales de la Société Royale Zoologique de Belgique 108115-117.

De LeyP.BlaxterM.L. (2002). Systematic position and phylogeny. In: LeeD.L. (Ed.). The biology of nematodes. London, UKTaylor & Francis pp.  1-30.

FonsecaV.G.NicholsB.LalliasD.QuinceC.CarvalhoG.R.PowerD.M. (2012). Sample richness and genetic diversity as drivers of chimera formation in nSSU metagenetic analyses. Nucleic Acids Research 40e66. DOI: 10.1093/nar/gks002

GerlachS.A. (1950). Über einige Nematoden aus der Familie der Desmodoriden. Zoolgischen Anzeiger 145178-198.

GerlachS.A. (1956). Diagnosen neuer nematoden aus der Kieler Bucht. Kieler Meeresforschungen 1285-109.

GourbaultN.VincxM. (1990). Chromadorida (Nematoda) from Guadeloupe and Polynesia with evidence of intersexuality. Zoologica Scripta 1931-37.

GreeffR. (1869). Untersuchungen über einige merkwürdige thiergruppen des arthropoden- und wurm-typus. Archiv für Naturgeschichte 3571-121.

GuindonS.GascuelO. (2003). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52696-704. DOI: 10.1080/10635150390235520

GuindonS.DufayardJ.F.LefortV.AnisimovaM.HordijkW.GascuelO. (2010). New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology 59307-321. DOI: 10.1093/sysbio/syq010

HoltermanM.van der WurffA.van den ElsenS.van MegenH.BongersT.HolovachovO.BakkerJ.HelderJ. (2006). Phylum-wide analysis of SSU rDNA reveals deep phylogenetic relationships among nematodes and accelerated evolution toward crown clades. Molecular Biology and Evolution 131792-1800.

HoschitzM.BuchholzT.G.OttJ.A. (1999). Leptonemella juliae sp. n. and Leptonemella vestari sp. n., two new free-living marine nematodes from a subtidal sand bottom. Annalen des Naturhistorischen Museums in Wien 101B423-435.

HourstonM.WarwickR.M. (2010). New species of free-living aquatic nematodes from south-western Australia (Nematoda: Axonolaimidae and Desmodoridae). Records of the Western Australian Museum 2642-69.

InglisW.G. (1967). Interstitial nematodes from St Vincent’s Bay, New Caledonia Expédition française sur les récifs coralliens de la Nouvelle Calédonie. Editions de la Fondation Singer-Polignac Occasional Publications 229-74.

KampferS.SturmbauerC.OttJ.A. (1998). Phylogenetic analysis of rDNA sequences from Adenophorean nematodes and implications for the Adenophorea-Secernentea controversy. Invertebrate Biology 11729-36. DOI: 10.2307/3226849

KearseM.MoirR.WilsonA.Stones-HavasS.CheungM.SturrockS.BuxtonS.CooperA.MarkowitzS.DuranC. (2012). Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 281647-1649. DOI: 10.1093/bioinformatics/bts199

LeducD. (2013). One new genus and two new deep-sea nematode species (Desmodoridae, Stilbonematinae) from phosphorite nodule deposits on Chatham Rise, Southwest Pacific Ocean. Marine Biodiversity 43421-428. DOI: 10.1007/s12526-013-0171-6

LeducD.ZhaoZ.Q. (2016). Phylogenetic relationships within the Cyatholaimidae (Nematoda: Chromadorida), the taxonomic significance of cuticle pore and pore-like structures, and a description of two new species. Marine Biodiversityin press. DOI: 10.1007/s12526-016-0605-z

MiljutinaM.A.MiljutinD.M.TchesunovA.V. (2013). Seven Acantholaimus (Chromadoridae: Nematoda) species from one deep-sea sediment sample (Angola Basin, south-east Atlantic). Journal of the Marine Biological Association of the United Kingdom 93935-953. DOI: 10.1017/S0025315412000860

MouraJ.D.R.da SilvaM.C.EstevesA.M. (2014). Four new species of Desmodora (Nematoda) from the deep south-east Atlantic, and a case of intersexuality in Desmodoridae. Journal of the Marine Biological Association of the United Kingdom 9485-104. DOI: 10.1017/S0025315413001458

NebelsickM.BlumerM.NovakR.OttJ.A. (1992). A new glandular sensory organ in Catanema sp. (Nematoda, Stilbonematinae). Zoomorphology 11217-26.

NunnG.B. (1992). Nematode molecular evolution. Ph.D. Thesis University of Nottingham Nottingham UK.

OttJ.A.NovakR. (1989). Living at an interface: meiofauna at the oxygen/sulfide boundary of marine sediments. In: RylandJ.S.TylerP.A. (Eds). Reproduction genetics and distribution of marine organisms. 23rd European marine biology symposium. Fredensbourg, DenmarkOlsen & Olsen pp.  415-422.

OttJ.A.NovakR.SchiemerF.HentschelU.NebelsickM.PolzM. (1991). Tackling the sulfide gradient: a novel strategy involving marine nematodes and chemoautotrophic ectosymbionts. PSZNI Marine Ecology 12261-279.

OttJ.A.Bauer-NebelsickM.NovotnyV. (1995). The genus Laxus Cobb, 1894 (Stilbonematinae: Nematoda): description of two new species with ectosymbiotic chemoautotrophic bacteria. Proceedings of the Biological Society of Washington 108508-527.

OttJ.A.Gruber-VodickaH.R.LeishN.ZimmermannJ. (2014). Phylogenetic confirmation of the genus Robbea (Nematoda: Desmodoridae, Stilbonematinae) with the description of three new species. Systematics and Biodiversity 12434-455. DOI: 10.1080/14772000.2014.941038

PlattH.M.ZhangZ.N. (1982). New species of marine nematodes from Loch Ewe, Scotland. Bulletin of the British Museum of Natural History 42227-246.

RiemannF.ThiermannF.BockL. (2003). Leptonemella species (Desmodoridae, Stilbonematinae), benthic marine nematodes with ectosymbiotic bacteria, from littoral sand of the North Sea island of Sylt: taxonomy and ecological aspects. Helgoland Marine Research 57118-131. DOI: 10.1007/s10152-003-0149-z

RonquistF.HuelsenbeckJ.P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 191572-1574. DOI: 10.1093/bioinformatics/btg180

ShimadaD. (2014). Free-living nematodes (Nematoda: Enoplida) from Rebun Island. Rishiri Studies 3367-71.

ShimadaD.KajiharaH. (2014). Two new species of free-living marine nematodes of Adoncholaimus Filipjev, 1918 (Oncholaimida: Oncholaimidae: Adoncholaiminae) from Hokkaido, northern Japan, with a key to species and discussion of genus. Nematology 16437-451. DOI: 10.1163/15685411-00002776

ShimadaD.KakuiK. (2015). First record of the free-living marine nematode Deontostoma magnificum (Timm, 1951) Platonova, 1962 (Nematoda: Leptosomatidae) from Japan. Nematological Research 4513-18. DOI: 10.3725/jjn.45.13

ShimadaD.KajiharaH.MawatariS.F. (2009). Three new species of free-living marine nematodes (Nematoda: Enoplida) from northern Japan. Species Diversity 14137-150.

ShimadaD.KakuiK.KajiharaH. (2012). A new species of deep-sea nematode, Micoletzkyia mawatarii sp. nov. (Nematoda: Enoplida: Phanodermatidae) from Northern Japan. Species Diversity 17221-226.

SinnigerF.ReimerJ.D.PawlowskiJ. (2010). The Parazoanthidae (Hexacorallia: Zoantharia) DNA taxonomy: description of two new genera. Marine Biodiversity 4057-70. DOI: 10.1007/s12526-009-0034-3

SomerfieldP.J.WarwickR.M. (1996). Meiofauna in marine pollution monitoring programmes: a laboratory manual. Lowestoft, UKMinistry of Agriculture, Fisheries and Food.

SteinerG. (1927). Epsilonematidae: a new nemic family. Journal of Parasitology 1465-66.

TchesunovA.V. (2013). Marine free-living nematodes of the subfamily Stilbonematinae (Nematoda, Desmodoridae): taxonomic review with descriptions of a few species from the Nha Trang Bay, Central Vietnam. Meiofauna Marina 2071-94.

TchesunovA.V.IngelsJ.PopovaE.V. (2012). Marine free-living nematodes associated with symbiotic bacteria in deep-sea canyons of north-east Atlantic Ocean. Journal of the Marine Biological Association of the United Kingdom 921257-1271. DOI: 10.1017/S0025315411002116

UrbancikW.Bauer-NebelsickM.OttJ.A. (1996a). The ultrastructure of the cuticle of Nematoda. I. The body cuticle within the Stilbonematinae (Adenophorea, Desmodoridae). Zoomorphology 11651-64.

UrbancikW.NovotnyV.OttJ.A. (1996b). The ultrastructure of the cuticle of Nematoda. II. The cephalic cuticle of Stilbonematinae (Adenophorea, Desmodoridae). Zoomorphology 11665-75.

van MegenH.van den ElsenS.HoltermanM.KarssenG.MooymanP.BongersT.HolovachovO.BakkerJ.HelderJ. (2009). A phylogenetic tree of nematodes based on about 1200 full-length small subunit ribosomal DNA sequences. Nematology 11927-950. DOI: 10.1163/156854109X456862

YoshikawaN. (1992). Brief review of Japanese researches on free-living nematodes. In: NakasoneK. (Ed.). Progress in nematology. Tsukuba, JapanJapanese Society of Nematology pp.  64-70.

ZhuoK.LiaoJ.CuiR.LiY. (2009). First record of female intersex in Hirschmanniella shamimi Ahmad, 1972 (Nematoda: Pratylenchidae), with a checklist of intersexes in plant nematodes. Zootaxa 197361-68. DOI: 10.5281/zenodo.185096

Figures

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    Laxus sakihariiae sp. n. A: Anterior body region of male; B: Surface view of male cephalic region; C: Optical section of male cephalic region; D: Posterior body region of male; E: Posterior body region of female. (Scale bar: A = 50 μm; B, C = 40 μm; D = 65 μm; E = 58 μm.)

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    Laxus sakihariiae sp. n. A: Cephalic region of female; B: Female reproductive system; C: Entire male. (Scale bar: A = 40 μm; B = 215 μm; C = 355 μm.)

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    Laxus sakihariiae sp. n. Light micrographs. A: Subventral glandular sensory organs (lateral view); B: Sublateral sensory organs (apical view). (Scale bar = 20 μm.)

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    Laxus sakihariiae sp. n. Scanning electron micrographs. A: Entire juvenile; B, C: juvenile cephalic region; D, E: Male cephalic region; F: Apical view of female cephalic region; G: Mouth opening of male. (Scale bar: A = 200 μm; B, D = 15 μm; C = 16 μm; E = 12 μm; F = 9 μm; G = 4 μm.)

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    Laxus sakihariiae sp. n. Scanning electron micrographs. A: Ventral view of male posterior body region; B: Apical view of tail tip showing outlets of caudal glands and postcloacal conical setae; C: Ventral view of male precloacal setae and spines; D: Lateral view of female posterior body region. (Scale bar: A = 40 μm; B = 9 μm; C = 13 μm; D = 21 μm.)

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    Bayesian tree inferred from SSU sequences under the general time-reversible (GTR) + gamma distribution (G) model. Only SSU sequences longer than 1400 bp were included. Posterior probabilities (left) and bootstrap values (right) from the ML analyses greater than or equal to 50% are given on appropriate clades. The scale stands for substitutions per site.

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