, Volume 128, Issue 1–3, pp 307–321 | Cite as

Seasonal dynamics of population genetic structure in cryptic taxa of the Pellioditis marina complex (Nematoda: Rhabditida)

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


The distribution patterns and genetic structure of the Pellioditis marina species complex in Belgium and The Netherlands were compared between four consecutive seasons. Different types of habitats (coast, estuary, semi-estuary and lake) with different degrees of connectivity were sampled. In addition, each habitat type was characterised by either temporal or permanent algal deposits. We screened 426 bp of the mitochondrial cytochrome oxidase c (COI) gene with the single-strand conformation polymorphism (SSCP) method in 1615 individuals of Pellioditis marina. The 51 haplotypes were divided into four (sympatric) lineages, with divergences ranging from 0.25 to 10.6%. Our results show that the lineages have different temporal dynamics, which may be linked to abiotic factors. Analysis of Molecular Variance (AMOVA) indicated a significant structuring in the PmI lineage, which correlated with habitat characteristics and which changed over time (Mantel, r = 0.51; p = 0.126). Intrapopulational diversity was similar in all locations, and temporal changes in haplotype frequencies were not higher in temporary than in permanent algal deposits. Instead, the results of the temporal survey indicated that (some) P. marina populations are characterised by a metapopulation structure. It is emphasized that a complete and correct interpretation of processes causing genetic structuring within species and of the genetic structure itself can only be done when analyses are performed at several time points.


genetic structure metapopulation mtDNA nematode Pellioditis marina SSCP temporal variation 



Single-strand conformation polymorphism


Cytochrome oxidase c subunit 1


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  1. Anderson, F.E., Swofford, D.L. 2004Should we be worried about long-branch attraction in real data sets? Investigations using metazoan 18S rDNAMol. Phyl. Evol.33440451CrossRefGoogle Scholar
  2. Arnaud, J.F., Laval, G. 2004Stability of genetic structure and effective population size inferred from temporal changes of microsatellite DNA polymorphisms in the land snail Helix aspersa (Gastropoda: Helicidae)Biol. J. Linn. Soc.8389102CrossRefGoogle Scholar
  3. Baeyens, W.F.J. 1998Evolution of trace metal concentrations in the Scheldt estuary (1978–1995). A comparison with estuarine and ocean levelsHydrobiologia366157167CrossRefGoogle Scholar
  4. Baeyens, W.F.J., Eck, B., Lambert, C., Wollast, R., Goeyens, L. 1998General description of the Scheldt estuaryHydrobiologia366114CrossRefGoogle Scholar
  5. Barcia, A.R., López, G.E., Hernández, D., García- Machado, E. 2005Temporal variation of the population structure and genetic diversity of Farfantepenaeus notialis assessed by allozyme lociMol. Ecol.1429332942CrossRefGoogle Scholar
  6. Bohonak, A.J. 2002IBD (Isolation By Distance): a program for analyses of isolation by distanceJ. Hered.93153154PubMedCrossRefGoogle Scholar
  7. Bongers, T., Bongers, M. 1998Functional diversity of nematodesAppl. Soil Ecol.10239251CrossRefGoogle Scholar
  8. Bousset, L., Henry, P.Y., Sourrouille, P., Jarne, P. 2004Population biology of the invasive freshwater snail Physa acuta approached through genetic markers, ecological characterization and demographyMol. Ecol.1320232036PubMedCrossRefGoogle Scholar
  9. Caudill, C.C., Bucklin, A. 2004Molecular phylogeography and evolutionary history of the estuarine copepod, Acartia tonsa, on the Northwest Atlantic coastHydrobiologia51191102CrossRefGoogle Scholar
  10. Cavalli-Sforza, L.L., Edwards, A.W.F. 1967Phylogenetic analysis: models and estimation proceduresEvolution21550570CrossRefGoogle Scholar
  11. Charbonnel, N., Quesnoit, M., Razatavonjizay, R., Brémond, P., Jarne, P. 2002A spatial and temporal approach to micorevolutionary forces affecting population biology in the freshwater snail Biomphalaria pfeifferi Am. Nat.160741755CrossRefPubMedGoogle Scholar
  12. Denver, D.R., Morris, K., Lynch, M., Vassilieva, L.L., Thomas, W.K. 2000High direct estimate of the mutation rate in the mitochondrial genome of Caenorhabditis elegans Science28923422344PubMedCrossRefGoogle Scholar
  13. Derycke, S., Remerie, T., Vierstraete, A., Backeljau, T., Vanfleteren, J., Vincx, M., Moens, T. 2005Mitochondrial DNA variation and cryptic speciation within the free-living marine nematode Pellioditis marina Mar. Ecol. Prog. Ser.30091103Google Scholar
  14. Wolf, H., Blust, R., Backeljau, T. 2004The population genetic structure of Littorina littorea (Mollusca: Gastropoda) along a pollution gradient in the Scheldt estuary (The Netherlands) using RAPD analysisSci. Total Environ.3255969PubMedCrossRefGoogle Scholar
  15. Excoffier, L., Smouse, P., Quattro, J. 1992Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction dataGenetics131479491PubMedGoogle Scholar
  16. Felsenstein, J. 2004PHYLIP: Phylogeny Inference Package v 3.6University of WashingtonUSAGoogle Scholar
  17. Goudet, J., 2001. FSTAT, A Program to Estimate and Test Gene Diversities and Fixation Indices (version 2.9.3). Lausanne, SwitzerlandGoogle Scholar
  18. Hanski, I. 1991Single-species metapopulation dynamics. Brief history and conceptual domainBiol. J. Linn. Soc.421738Google Scholar
  19. Hartl, D.L., Clark, A.G. 1989Principles of Population Genetics2Sinauer AssociatesSunderlandGoogle Scholar
  20. Heath, D.D., Busch, C., Kelly, J., Atagi, D.Y. 2002Temporal change in genetic structure and effective population size in steelhead trout (Oncorhynchus mykiss)Mol. Ecol.11197214PubMedCrossRefGoogle Scholar
  21. Heip, C. 1989The ecology of the estuaries Rhine, Meuse and Scheldt in The NetherlandsTopics Mar. Biol.53457463Google Scholar
  22. Hoffman, E.A., Schueler, F.W., Blouin, M.S. 2004Effective population sizes and temporal stability of genetic structure in Rana pipiens, the northern leopard frogEvolution5825362545PubMedCrossRefGoogle Scholar
  23. Hoglund, J., Engstrom, A., Morrison, D.A., Mattsson, J.G. 2004Genetic diversity assessed by amplified fragment length polymorphism analysis of the parasitic nematode Dictyocaulus viviparus the lungworm of cattleInt. J. Parasitol.34475484PubMedCrossRefGoogle Scholar
  24. Hu, M., Chilton, N.B., Zhu, X.Q., Gasser, R.B. 2002Single-strand conformation polymorphism-based analysis of mitochondrial cytochrome c oxidase subunit 1 reveals significant substructuring in hookworm populationsElectrophoresis232734PubMedCrossRefGoogle Scholar
  25. Inglis W.G. & Coles J.W, 1961. The species of Rhabditis (Nematoda) found in rotting seaweed on British beaches. Bull. Br. Mus. (Natl. Hist.) Zool. 320–333.Google Scholar
  26. Jorde, P.E., Ryman, N. 1996Demographic genetics of Brown trout (Salmo trutta) and estimation of effective population size from temporal change of allele frequenciesGenetics14313691381PubMedGoogle Scholar
  27. Kanda, N., Allendorf, F.W. 2001Genetic population structure of bull trout from the flathead river basin as shown by microsatellites and mitochondrial DNA markersTrans. Am. Fish Soc.13092106CrossRefGoogle Scholar
  28. Kimura, M. 1981Estimation of evolutionary distances between homologues nucleotide sequencesProc. Natl. Acad. Sci. USA78454458PubMedCrossRefGoogle Scholar
  29. Kirkendale, L.A., Meyer, C.P. 2004Phylogeography of the Patelloida profunda group (Gastropoda: Lottidae): diversification in a dispersal-driven marine systemMol. Ecol.1327492762PubMedCrossRefGoogle Scholar
  30. Kovatch, C.E., Schizas, N.V., Chandler, T., Coull, B.C., Quattro, J.M. 2000Tolerance and genetic relatedness of three meiobenthic copepod populations exposed to sediment-associated contaminant mixtures: role of environmental historyEnviron. Toxicol. Chem.19912919CrossRefGoogle Scholar
  31. Kumar, S., Tamura, K., Nei, M. 2004MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignmentBrief. Bioinform.5150163PubMedCrossRefGoogle Scholar
  32. Lee, T., O’ Foighil, D. 2004Hidden Floridian biodiversity: mitochondrial and nuclear gene trees reveal four cryptic species within the scorched mussel, Brachidontes exustus, species complexMol. Ecol.1335273542PubMedCrossRefGoogle Scholar
  33. Martínez, P., Belcari, P., Sanjuan, A., Guerra, A. 2005Allozyme analysis of geographical and seasonal variation of Ilex coindetii (Cephalopoda: Ommastrephidae) from central Mediterranean and Iberian AtlanticJ. Mar. Biol. Assoc. UK85177184CrossRefGoogle Scholar
  34. McElroy, T.C., Kandl, K.L., Garcia, L., Trexler, J.C. 2003Extinction-colonization dynamics structure genetic variation of spotted sunfish (Lepomis punctatus) in the Florida EvergladesMol. Ecol.12355368PubMedCrossRefGoogle Scholar
  35. McGovern, T.M., Hellberg, M.E. 2003Cryptic species, cryptic endosymbionts, and geographical variation in chemical defences in the bryozoan Bugula neritina Mol. Ecol.1212071215PubMedCrossRefGoogle Scholar
  36. Miller, M.P., 1997. Tools for Population Genetic Analysis (TFPGA) 1.3. A Windows Program for the Analysis of Allozyme and Molecular Population Genetic Data. Department of Biological Sciences, Northern Arizona UniversityGoogle Scholar
  37. Moens, T., Vincx, M. 1997Observations on the feeding ecology of estuarine nematodesJ. Mar. Biol. Assoc. UK77211227CrossRefGoogle Scholar
  38. Moens, T., Vincx, M. 2000aTemperature and salinity constraints on the life cycle of two brackish-water nematode speciesJ. Exp. Mar. Biol. Ecol.243115135CrossRefGoogle Scholar
  39. Moens, T., Vincx, M. 2000bTemperature, salinity and food thresholds in two brackish water bacterivorous nematode species: assessing niches from food absorption and respirationJ. Exp. Mar. Biol. Ecol.243137154CrossRefGoogle Scholar
  40. Nei, M. 1987Molecular Evolutionary GeneticsColumbia University PressNew York, NY, USAGoogle Scholar
  41. Nieberding, C., Libois, R., Douady, C.J., Morand, S., Michaux, J.R. 2005Phylogeography of a nematode (Heligmosomoides polygyrus) in the western Palearctic region: persistence of northern cryptic populations during ice ages?Mol. Ecol.14765779PubMedCrossRefGoogle Scholar
  42. Nylander, J.A. 2001Taxon Sampling in Phylogenetic Analysis: Problems and Strategies Reviewed. Introductory Research Essay 1Uppsala UniversitySwedenGoogle Scholar
  43. Omilian, A.R., Taylor, D.J. 2001Rate acceleration and long-branch attraction in a conserved gene of cryptic Daphniid (Crustacea) speciesMol. Biol. Evol.1822012212PubMedGoogle Scholar
  44. Ostergaard, S., Hansen, M.M., Loeschcke, V., Nielsen, E.E. 2003Long-term temporal changes of genetic composition in brown trout (Salmo trutta L.) population inhabiting an unstable environmentMol. Ecol.1231233135PubMedCrossRefGoogle Scholar
  45. Ovenden, J.R., Salini, J., O’Connor, S., Street, R. 2004Pronounced genetic population structure in a potentially vagile fish species (Pristipomoides multidens, Teleostei; Perciformes; Lutjanidae) from the East Indies triangleMol. Ecol.1319911999PubMedCrossRefGoogle Scholar
  46. Papetti, C., Zane, L., Bortolotto, E., Bucklin, A., Patarnello, T. 2005Genetic differentiation and local temporal stability of population structure in the euphausiid Meganyctiphanes norvegica Mar. Ecol. Prog. Ser.289225235Google Scholar
  47. Perrin, C., Wing, S.R., Roy, M.S. 2004Effects of hydrographic barriers on population genetic structure of the sea star Coscinasterias muricata (Echinodermata, Asteroidea) in the New Zealand fiordsMol. Ecol.1321832195PubMedCrossRefGoogle Scholar
  48. Picard, D., Plantard, O., Scurrah, M., Mugniéry, D. 2004Inbreeding and population structure of the potato cyst nematode (Globodera pallida) in its native area (Peru)Mol. Ecol.1328992908PubMedCrossRefGoogle Scholar
  49. Posada, D., Crandall, K.A. 1998Modeltest: testing the model of DNA substitutionBioinformatics14817818PubMedCrossRefGoogle Scholar
  50. Posada, D., Buckley, T.R. 2004Model selection and model averaging in phylogenetics: advantages of Akaike information criterion and Bayesian approaches over likelihood ratio testsSyst. Biol.53793808PubMedCrossRefGoogle Scholar
  51. Remerie, T., T. Bourgois, D. Peelaers, A. Vierstraete, J. Vanfleteren & A. Vanreusel, 2006. Phylogeographic patterns of the mysid Mesopodopsis slabberi (Crustacea, Mysida) in Western Europe: evidence for high molecular diversity and cryptic speciation. Mar. Biol. (in press)Google Scholar
  52. Rice, W.R. 1989Analyzing tables of statistical testsEvolution43223225CrossRefGoogle Scholar
  53. Rocha-Olivares, A., Fleeger, J.W., Foltz, D.W. 2001Decoupling of molecular and morphological evolution in deep lineages of a meiobenthic harpacticoid copepodMol. Biol. Evol.1810881102PubMedGoogle Scholar
  54. Rocha-Olivares, A., Fleeger, J.W., Foltz, D.W. 2004Differential tolerance among cryptic species: a potential cause of pollutant-related reductions in genetic diversityEnviron. Toxicol. Chem.2321322137PubMedCrossRefGoogle Scholar
  55. Rohlf, F.J., 2000. NTSYSpc Version 2.1. Numerical Taxonomy and Multivariate Analysis System. Exeter Software, SetauketGoogle Scholar
  56. Schizas, N.V., Street, G.T., Coull, B.C., Chandler, G.T., Quattro, J.M. 1999Molecular population structure of the marine benthic copepod Microarthridion littorale along the south eastern and Gulf coasts of the USAMar. Biol.135399405CrossRefGoogle Scholar
  57. Schizas, N.V., Chandler, G.T., Coull, B.C., Klosterhaus, S.L., Quattro, J.M. 2001Differential survival of three mitochondrial lineages of a marine benthic copepod exposed to a pesticide mixtureEnviron. Sci. Technol.35535538PubMedCrossRefGoogle Scholar
  58. Schneider, S., Roessli, D., Excoffier, L. 2000Arlequin ver. 2.000: A Software for Population Genetics Data AnalysisGenetics and Biometry Laboratory, University of GenevaSwitzerlandGoogle Scholar
  59. Sivasundar, A., Hey,  J.  2005Sampling from natural populations with RNAi reveals high outcrossing and population structure in Caenorhabditis elegans Curr. Biol.1515981602PubMedCrossRefGoogle Scholar
  60. Statsoft Inc., 2000. Statistica for Windows. Tulsa, USAGoogle Scholar
  61. Sturmbauer, C., Opadiya, G.B., Niederstätter, H., Riedmann, A., Dallinger, R. 1999Mitochondrial DNA reveals cryptic oligochaete species differing in cadmium resistanceMol. Biol. Evol.16967974PubMedGoogle Scholar
  62. Swofford, D.L., 1998. PAUP*. Phylogenetic Analysis Using Parsimony (*and other methods). Version 4. Sinauer Associates, Sunderland, MassachusettsGoogle Scholar
  63. Tajima, F. 1983Evolutionary relationship of DNA sequences in finite populationsGenetics123585595Google Scholar
  64. Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F., Higgins, D.G. 1997The Clustal_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis toolsNucleic Acids Res.2448764882CrossRefGoogle Scholar
  65. Tietjen, J.H., Lee, J.J., Rullman, J., Greengart, A., Trompeter, J. 1970Gnotobiotic culture and physiological ecology of the marine nematode Rhabditis marina BastianLimnol. Oceanogr.15535543CrossRefGoogle Scholar
  66. Vranken, G., Heip, C. 1983Calculation of the intrinsic rate of natural increase, rm, with Rhabditis marina Bastian 1865 (Nematoda)Nematologica29468477CrossRefGoogle Scholar
  67. Waples, R.S. 1989A generalized approach for estimating effective population size from temporal changes in allele frequencyGenetics121379391PubMedGoogle Scholar
  68. Williams, S.T., Knowlton, N., Weigt, L.A., Jara, J.A. 2001Evidence for three major clades within the snapping shrimp genus Alpheus inferred from nuclear and mitochondrial gene sequence dataMol. Phylogenet. Evol.9131140Google Scholar
  69. Zhu, X.Q., Gasser, R.B. 1998Single-strand conformation polymorphism (SSCP)-based mutation scanning approaches to fingerprint sequence variation in ribosomal DNA of ascaridoid nematodesElectrophoresis1913661373PubMedCrossRefGoogle Scholar

Copyright information

© Springer 2006

Authors and Affiliations

  • S. Derycke
    • 1
    • 5
    • 6
    Email author
  • T. Backeljau
    • 2
    • 3
  • C. Vlaeminck
    • 5
  • 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 AntwerpAntwerpenBelgium
  4. 4.Department of BiologyGhent UniversityGhentBelgium
  5. 5.CeMoFeGhent UniversityGhentBelgium
  6. 6.S. DeryckeGhentBelgium

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