Marine Biology

, Volume 151, Issue 5, pp 1799–1812 | Cite as

Spatiotemporal analysis of population genetic structure in Geomonhystera disjuncta (Nematoda, Monhysteridae) reveals high levels of molecular diversity

  • S. DeryckeEmail author
  • T. Backeljau
  • C. Vlaeminck
  • A. Vierstraete
  • J. Vanfleteren
  • M. Vincx
  • T. Moens
Research Article


Species identification in the phylum Nematoda is complicated due to the paucity of easily obtainable diagnostic morphological features. Furthermore, the cosmopolitan distribution of several species despite low dispersal abilities makes cryptic diversity potentially substantial within this phylum. We conducted a population genetic survey in the marine nematode Geomonhystera disjuncta in Belgium and The Netherlands in two seasons. The mitochondrial cytochrome oxidase c subunit 1 (COI) gene was screened with the single-strand conformation polymorphism method in 759 individuals. The 43 haplotypes were grouped into five lineages, with low divergences within (<3%) and high divergences between lineages (>14%). Analysis of the nuclear ITS region yielded concordant tree topologies, indicating the presence of five cryptic taxa within G. disjuncta. Analysis of Molecular Variance (AMOVA) illustrated a significant structuring in all lineages and temporal fluctuations in haplotype frequencies within and between locations. Metapopulation dynamics and/or priority effects best explained this structuring. Finally, our data indicate that the COI gene may be useful for DNA barcoding purposes.


Population Genetic Structure Nematode Species Nematode Community Haplotype Group Restricted Gene Flow 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



The authors thank Dr. T. Remerie for his suggestions and help in retrieving the data and Dr. M. Raes for his help with the morphological measurements of the specimens. S.D. acknowledges a grant from the Flemish Institute for the Promotion of Scientific-Technological Research (I.W.T.). T.M. is a postdoctoral fellow with the Flemish Fund for Scientific Research. Further financial support was obtained from Ghent University in BOF-projects 1205398 (GOA) and 01GZ0705 (GOA-BBSea).


  1. Andrássy I (1981) Revision of the order Monhysterida (Nematoda) inhabiting soil and inland waters. Opus Zool 17–18:13–47Google Scholar
  2. Asmussen MA, Arnold J, Avise JC (1987) Definition and properties of disequilibrium statistics for associations between nuclear and cytoplasmic genotypes. Genetics 115:755–768PubMedPubMedCentralGoogle Scholar
  3. Avise JC (2000) Phylogeography: the history and formation of species. Harvard University Press, CambridgeGoogle Scholar
  4. Bhadury P, Austen MC, Bilton DT, Lambshead PJD, Rogers AD, Smerdon GR (2006) Development and evaluation of a DNA-barcoding approach for the rapid identification of nematodes. Mar Ecol Progr Ser 320:1–9CrossRefGoogle Scholar
  5. Blaxter M (2004) The promise of a DNA taxonomy. Phil Trans R Soc Lond B 359:669–679CrossRefGoogle Scholar
  6. Blaxter M, Mann J, Chapman T, Thomas F, Whitton C, Floyd R, Abebe E (2005) Defining operational taxonomic units using DNA barcode data. Phil Trans R Soc B 360:1935–1943CrossRefGoogle Scholar
  7. Blouin MS (2002) Molecular prospecting for cryptic species of nematodes: mitochondrial DNA versus internal transcribed spacer. Int J Parasitol 32:527–531CrossRefGoogle Scholar
  8. Blouin MS, Yowell CA, Courtney CH, Dame JB (1995) Host-movement and the genetic structure of populations of parasitic nematodes. Genetics 141:1007–1014PubMedPubMedCentralGoogle Scholar
  9. Bohonak AJ (2002) IBD (Isolation By Distance): a program for analyses of isolation by distance. J Hered 93:153–154CrossRefGoogle Scholar
  10. Boileau M, Hebert PDN, Schwartz SS (1992) Non-equilibrium gene frequency divergence: persistent founder effects in natural populations. J Evol Biol 5:25–39CrossRefGoogle Scholar
  11. Bongers T, Bongers M (1998) Functional diversity of nematodes. Appl Soil Ecol 10:239–251CrossRefGoogle Scholar
  12. Caudill CC, Bucklin A (2004) Molecular phylogeography and evolutionary history of the estuarine copepod Acartia tonsa, on the Northwest Atlantic coast. Hydrobiologia 511:91–102CrossRefGoogle Scholar
  13. Cavalli-Sforza LL, Edwards AWF (1967) Phylogenetic analysis: models and estimation procedures. Evolution 21:550–570CrossRefGoogle Scholar
  14. Clement M, Posada D, Crandall KA (2000) TCE: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659CrossRefGoogle Scholar
  15. Coomans A (2002) Present status and future of nematode systematics. Nematology 4:573–582CrossRefGoogle Scholar
  16. De Coninck LA, Schuurmans Stekhoven JH (1933) The free-living marine nemas of the Belgian coast II. Mém Mus R Hist Nat Belg 58:1–163Google Scholar
  17. De Gruijter JM, Polderman AM, Zhu XQ, Gasser RB (2002) Screening for haplotypic variability within Oesophagostomum bifurcum (Nematoda) employing a single-strand conformation polymorphism approach. Mol Cell Prob 16:185–190CrossRefGoogle Scholar
  18. De Ley P, Tandingan De Ley I, Morris K, Abebe E, Mundo-Ocampo M, Yoder M, Heras J, Waumann D, Rocha-Olivares A, Burr AH, Baldwin JG, Thomas WK (2005) An integrated approach to fast and informative morphological vouchering of nematodes for applications in molecular barcoding. Phil Trans R Soc B 360:1945–1958CrossRefGoogle Scholar
  19. De Meester L, Gómez A, Okamura B, Schwenk K (2002) The monopolization hypothesis and the dispersal-gene flow paradox in aquatic organisms. Acta Oecol 23:121–135CrossRefGoogle Scholar
  20. Derycke S, Remerie T, Vierstraete A, Backeljau T, Vanfleteren J, Vincx M, Moens T (2005) Mitochondrial DNA variation and cryptic speciation within the free-living marine nematode Pellioditis marina. Mar Ecol Prog Ser 300:91–103CrossRefGoogle Scholar
  21. Derycke S, Backeljau T, Vlaeminck C, Vierstraete A, Vanfleteren J, Vincx M, Moens T (2006) Seasonal dynamics of population genetic structure in cryptic taxa of the Pellioditis marina complex (Nematoda: Rhabditida). Genetica 128:307–321CrossRefGoogle Scholar
  22. Derycke S, Van Vynckt R, Vanoverbeke J, Vincx M, Moens T (2007) Colonization patterns of Nematoda on decomposing algae in the estuarine environment: Community assembly and genetic structure of the dominant species Pellioditis marina. Limnol Oceanogr (in press)Google Scholar
  23. Faust MA, Gulledge RA (1996) Associations of microalgae and meiofauna in floating detritus at a mangrove island, Twin Cays, Belize. J Exp Mar Biol Ecol 22:115–123Google Scholar
  24. Felsenstein J (2004) PHYLIP: Phylogeny inference package v 3.6, University of Washington, USAGoogle Scholar
  25. Ferguson JWH (2002). On the use of genetic divergence for identifying species. Biol J Linn Soc 75:509–516CrossRefGoogle Scholar
  26. Floyd R, Abebe E, Papert A, Blaxter M (2002) Molecular barcodes for soil nematode identification. Mol Ecol 11:839–850CrossRefGoogle Scholar
  27. Gerlach SA (1965) Freilebende Meeresnematoden aus der Gezeitenzone von Spitzbergen. Veröff Inst Meeresforsch Bremerh 9:109–172Google Scholar
  28. Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). Lausanne, SwitzerlandGoogle Scholar
  29. Govindarajan AL, Piraino S, Gravili C, Kubota S (2005) Species identification of bivalve-inhabiting marine hydrozoans of the genus Eugymnanthea. Invert Biol 124:1–10CrossRefGoogle Scholar
  30. Hasegawa M, Kishino K, Yano T (1985) Dating the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 22:160–174CrossRefGoogle Scholar
  31. Hebert PDN, Cywinska A, Ball SL, deWaard JR (2003a) Biological identifications through DNA barcodes. Proc R Soc Lond B 270:313–321CrossRefGoogle Scholar
  32. Hebert PDN, Ratnasingham S, deWaard JR (2003b) Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proc R Soc Lond B 270(suppl):96–99CrossRefGoogle Scholar
  33. Heip C, Vincx M, Vranken G (1985) The ecology of marine nematodes. Oceanogr Mar Biol Annu Rev 23:399–489Google Scholar
  34. Hillis DM, Dixon MT (1991)Ribosomal DNA: molecular evolution and phylogenetic inference. Q Rev Biol 66:411–437CrossRefGoogle Scholar
  35. Hoglund J, Engstrom A, Morrison DA, Mattson JG (2004) Genetic diversity assessed by amplified fragment length polymorphism analysis of the parasitic nematode Dictyocaulus viviparous, the lungworm of cattle. Int J Par 34:475–484CrossRefGoogle Scholar
  36. Hopper BE (1969) Marine nematodes of Canada II. Marine nematodes from the Minas Basin-Scots Bay area of the bay of Fundy, Nova Scotia. Can J Zool 46:655–661CrossRefGoogle Scholar
  37. Hu M, Chilton NB, Zhu XQ, Gasser RB (2002) Single-strand conformation polymorphism-based analysis of mitochondrial cytochrome c oxidase subunit 1 reveals significant substructuring in hookworm populations. Electrophoresis 23:27–34CrossRefGoogle Scholar
  38. Huelsenbeck JP, Ronquist F (2005) Mr Bayes v 3.1.2, Bayesian Analysis of Phylogeny. University of California, San Diego and Florida State UniversityGoogle Scholar
  39. Hugot JP, Baujard P, Morand S (2001) Biodiversity in helminthes and nematodes as a field of study: an overview. Nematology 3:199–208CrossRefGoogle Scholar
  40. Jacobs L (1987) A checklist of the Monhysteridae (Nematoda, Monhysterida). Rand Afrikaans University, JohannesburgGoogle Scholar
  41. Kliman RM, Hey J (1993) DNA sequence variation at the period locus within and among species of the Drosophila melanogaster complex. Genetics 133:375–387PubMedPubMedCentralGoogle Scholar
  42. Knowlton N (2000) Molecular genetic analysis of species boundaries in the sea. Hydrobiologia 420:73–90CrossRefGoogle Scholar
  43. Kumar S, Tamura K, Nei M (2004) MEGA3: Integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163CrossRefGoogle Scholar
  44. Lambshead PJD (2004) Marine nematode biodiversity. In: Chen ZX, Chen SY, Dickson DW (eds) Nematode morphology, physiology and ecology, vol 1. Tsinghua University Press, Beijing, pp 438–492Google Scholar
  45. Latta RG, Linhart YB, Mitton JB (2001) Cytonuclear disequilibrium and genetic drift in a natural population of Ponderosa Pine. Genetics 158:843–850PubMedPubMedCentralGoogle Scholar
  46. Mallet J, Willmott K (2003) Taxonomy: renaissance or Tower of Babel? TREE 18:57–59Google Scholar
  47. Markmann M, Tautz D (2005) Reverse taxonomy: an approach towards determining the diversity of meiobenthic organisms based on ribosomal RNA signature sequences. Philos Trans R Lond B 360:1917–1924CrossRefGoogle Scholar
  48. Mickevich ME, Farris JS (1981) The implications of congruence in Menidia. Syst Zool 27:143–158CrossRefGoogle Scholar
  49. Miller MP (1997) Tools for population genetic analysis (TFPGA) 1.3 A Windows program for the analysis of allozyme and molecular population genetic dataGoogle Scholar
  50. Moens T, Vincx M (2000) Temperature, salinity and food thresholds in two brackish-water bacterivorous nematode species: assessing niches from food absorption and respiration experiments. J Exp Mar Biol Ecol 243:137–154CrossRefGoogle Scholar
  51. Mokievsky VO, Filippova KA, Chesunov AV (2005) Nematode fauna associated with detached kelp accumulations in the subtidal zone of the White Sea. Oceanology 45:689–697Google Scholar
  52. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New YorkGoogle Scholar
  53. Nicholas KB, Nicholas HB (1997) Genedoc: a tool for editing and annotating multiple sequence alignments. Distributed by the authorGoogle Scholar
  54. Nylander JAA (2004) MrModeltest v2. Program distributed by the author. Evolutionary Biology Centre, Uppsala UniversityGoogle Scholar
  55. Otranto D, Testini G, De Luca F, Hu M, Shamsi S, Gasser RB (2005) Analysis of genetic variability within Thelazia callipaeda (Nematoda: Thelazioidea) from Europe and Asia by sequencing and mutation scanning of the mitochondrial cytochrome c oxidase subunit 1 gene. Mol Cell Probes 19:306–313CrossRefGoogle Scholar
  56. Ovenden JR, Salini J, O’Connor S, Street R (2004) Pronounced genetic population structure in a potentially vagile fish species (Pristipomoides multidens, Teleostei; Perciformes; Lutjanidae) from the East Indies triangle. Mol Ecol 13:1991–1999CrossRefGoogle Scholar
  57. Picard D, Plantard O, Scurrah M, Mugniéry D (2004) Inbreeding and population structure of the potato cyst nematode (Globodera pallida) in its native area (Peru). Mol Ecol 13:2899–2908CrossRefGoogle Scholar
  58. Posada D, Buckley TR (2004) Model selection and model averaging in phylogenetics: advantages of Akaike information criterion and Bayesian approaches over likelihood ratio tests. Syst Biol 53:793–808CrossRefGoogle Scholar
  59. Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818CrossRefGoogle Scholar
  60. Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225CrossRefGoogle Scholar
  61. Rocha-Olivares A, Fleeger JW, Foltz DW (2001) Decoupling of molecular and morphological evolution in deep lineages of a meiobenthic harpacticoid copepod. Mol Biol Evol 18:1088–1102CrossRefGoogle Scholar
  62. Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–569PubMedPubMedCentralGoogle Scholar
  63. Schizas NV, Street GT, Coull BC, Chandler GT, Quattro JM (1999) Molecular population structure of the marine benthic copepod Microarthridion littorale along the south eastern and Gulf coasts of the USA. Mar Biol 135:399–405CrossRefGoogle Scholar
  64. Schneider S, Roessli D, Excoffier L (2000) Arlequin ver. 2.000: A software for population genetics data analysis. Genetics and Biometry Laboratory, University of Geneva, SwitzerlandGoogle Scholar
  65. Sivasundar A, Hey J (2005) Sampling from natural populations with RNAi reveals high outcrossing and population structure in Caenorhabditis elegans. Curr Biol 15:1598–1602CrossRefGoogle Scholar
  66. Slatkin M (1987) Gene flow and the geographic structure of natural populations. Science 236:787–792CrossRefGoogle Scholar
  67. StatSoft, Inc. (2001). STATISTICA (data analysis software system), version 6.
  68. Swofford DL (1998) PAUP*. Phylogenetic Analysis Using Parsimony (*and other methods). Version 4. Sinauer Associates, SunderlandGoogle Scholar
  69. Tautz D, Arctander P, Minelli A, Thomas RH, Vogler AP (2003) A plea for DNA taxonomy. TREE 18:70–74Google Scholar
  70. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The Clustal_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 24:4876–4882CrossRefGoogle Scholar
  71. Ullberg J (2004) Dispersal in free-living, marine, benthic nematodes: passive or active processes? PhD Dissertation, Stockholm University, Sweden, p 27Google Scholar
  72. Vincx M (1990) Diversity of nematode communities in the Southern bight of the North Sea. Neth J Sea Res 25:181–188CrossRefGoogle Scholar
  73. Vincx M (1996) Meiofauna in marine and freshwater sediments. In: Hall GS (ed) Methods for the examination of organismal diversity in soils and sediments. CAB International IUBS UNESCO, New York, pp 187–195Google Scholar
  74. Vincx M, Meire P, Heip C (1990) The distribution of nematode communities in the Southern Bight of the North-Sea. Cah Biol Mar 31:107–129Google Scholar
  75. Vranken G (1987) An autecological study of free-living marine nematodes. Acad Anal- Meded K Acad Belg Kl Wet 49:73–97Google Scholar
  76. Vranken G, Herman PJM, Heip C (1988) Studies of life-history and energetics of marine and brackish-water nematodes. I. Demography of Monhystera disjuncta at different temperature and feeding conditions. Oecologia 77:296–301CrossRefGoogle Scholar
  77. Warwick RM, Platt HM, Somerfield PJ (1998) Free-living marine nematodes Part III. Monhysterids. Synopsis of the British fauna 53, Dorset Press, Great BritainGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • S. Derycke
    • 1
    • 5
    Email author
  • T. Backeljau
    • 2
    • 3
  • C. Vlaeminck
    • 1
  • A. Vierstraete
    • 4
    • 5
  • J. Vanfleteren
    • 4
    • 5
  • M. Vincx
    • 1
  • T. Moens
    • 1
  1. 1.Department of Biology, Marine Biology SectionGhent UniversityGhentBelgium
  2. 2.Royal Belgian Institute of Natural SciencesBrusselsBelgium
  3. 3.Evolutionary Biology Group, Department of BiologyUniversity of AntwerpAntwerpBelgium
  4. 4.Department of BiologyGhent UniversityGhentBelgium
  5. 5.CeMoFe, Ghent UniversityGhentBelgium

Personalised recommendations