Skip to main content
Log in

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

Marine Biology Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  • Andrássy I (1981) Revision of the order Monhysterida (Nematoda) inhabiting soil and inland waters. Opus Zool 17–18:13–47

    Google Scholar 

  • Asmussen MA, Arnold J, Avise JC (1987) Definition and properties of disequilibrium statistics for associations between nuclear and cytoplasmic genotypes. Genetics 115:755–768

    CAS  PubMed  PubMed Central  Google Scholar 

  • Avise JC (2000) Phylogeography: the history and formation of species. Harvard University Press, Cambridge

    Google Scholar 

  • 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 320:1–9

    Article  CAS  Google Scholar 

  • Blaxter M (2004) The promise of a DNA taxonomy. Phil Trans R Soc Lond B 359:669–679

    Article  CAS  Google Scholar 

  • 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 360:1935–1943

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blouin MS (2002) Molecular prospecting for cryptic species of nematodes: mitochondrial DNA versus internal transcribed spacer. Int J Parasitol 32:527–531

    Article  CAS  PubMed  Google Scholar 

  • Blouin MS, Yowell CA, Courtney CH, Dame JB (1995) Host-movement and the genetic structure of populations of parasitic nematodes. Genetics 141:1007–1014

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bohonak AJ (2002) IBD (Isolation By Distance): a program for analyses of isolation by distance. J Hered 93:153–154

    Article  CAS  PubMed  Google Scholar 

  • Boileau M, Hebert PDN, Schwartz SS (1992) Non-equilibrium gene frequency divergence: persistent founder effects in natural populations. J Evol Biol 5:25–39

    Article  Google Scholar 

  • Bongers T, Bongers M (1998) Functional diversity of nematodes. Appl Soil Ecol 10:239–251

    Article  Google Scholar 

  • Caudill CC, Bucklin A (2004) Molecular phylogeography and evolutionary history of the estuarine copepod Acartia tonsa, on the Northwest Atlantic coast. Hydrobiologia 511:91–102

    Article  Google Scholar 

  • Cavalli-Sforza LL, Edwards AWF (1967) Phylogenetic analysis: models and estimation procedures. Evolution 21:550–570

    Article  CAS  PubMed  Google Scholar 

  • Clement M, Posada D, Crandall KA (2000) TCE: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659

    Article  CAS  PubMed  Google Scholar 

  • Coomans A (2002) Present status and future of nematode systematics. Nematology 4:573–582

    Article  Google Scholar 

  • De Coninck LA, Schuurmans Stekhoven JH (1933) The free-living marine nemas of the Belgian coast II. Mém Mus R Hist Nat Belg 58:1–163

    Google Scholar 

  • 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 16:185–190

    Article  CAS  Google Scholar 

  • 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 360:1945–1958

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • De Meester L, Gómez A, Okamura B, Schwenk K (2002) The monopolization hypothesis and the dispersal-gene flow paradox in aquatic organisms. Acta Oecol 23:121–135

    Article  Google Scholar 

  • 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 300:91–103

    Article  CAS  Google Scholar 

  • 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 128:307–321

    Article  CAS  PubMed  Google Scholar 

  • 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)

  • 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 22:115–123

    Google Scholar 

  • Felsenstein J (2004) PHYLIP: Phylogeny inference package v 3.6, University of Washington, USA

    Google Scholar 

  • Ferguson JWH (2002). On the use of genetic divergence for identifying species. Biol J Linn Soc 75:509–516

    Article  Google Scholar 

  • Floyd R, Abebe E, Papert A, Blaxter M (2002) Molecular barcodes for soil nematode identification. Mol Ecol 11:839–850

    Article  CAS  PubMed  Google Scholar 

  • Gerlach SA (1965) Freilebende Meeresnematoden aus der Gezeitenzone von Spitzbergen. Veröff Inst Meeresforsch Bremerh 9:109–172

    Google Scholar 

  • Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). Lausanne, Switzerland

  • Govindarajan AL, Piraino S, Gravili C, Kubota S (2005) Species identification of bivalve-inhabiting marine hydrozoans of the genus Eugymnanthea. Invert Biol 124:1–10

    Article  Google Scholar 

  • Hasegawa M, Kishino K, Yano T (1985) Dating the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 22:160–174

    Article  CAS  PubMed  Google Scholar 

  • Hebert PDN, Cywinska A, Ball SL, deWaard JR (2003a) Biological identifications through DNA barcodes. Proc R Soc Lond B 270:313–321

    Article  CAS  Google Scholar 

  • 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):96–99

    Article  Google Scholar 

  • Heip C, Vincx M, Vranken G (1985) The ecology of marine nematodes. Oceanogr Mar Biol Annu Rev 23:399–489

    Google Scholar 

  • Hillis DM, Dixon MT (1991)Ribosomal DNA: molecular evolution and phylogenetic inference. Q Rev Biol 66:411–437

    Article  CAS  PubMed  Google Scholar 

  • 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 34:475–484

    Article  CAS  Google Scholar 

  • 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 46:655–661

    Article  Google Scholar 

  • 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 23:27–34

    Article  PubMed  Google Scholar 

  • Huelsenbeck JP, Ronquist F (2005) Mr Bayes v 3.1.2, Bayesian Analysis of Phylogeny. University of California, San Diego and Florida State University

  • Hugot JP, Baujard P, Morand S (2001) Biodiversity in helminthes and nematodes as a field of study: an overview. Nematology 3:199–208

    Article  Google Scholar 

  • Jacobs L (1987) A checklist of the Monhysteridae (Nematoda, Monhysterida). Rand Afrikaans University, Johannesburg

    Google Scholar 

  • Kliman RM, Hey J (1993) DNA sequence variation at the period locus within and among species of the Drosophila melanogaster complex. Genetics 133:375–387

    CAS  PubMed  PubMed Central  Google Scholar 

  • Knowlton N (2000) Molecular genetic analysis of species boundaries in the sea. Hydrobiologia 420:73–90

    Article  CAS  Google Scholar 

  • Kumar S, Tamura K, Nei M (2004) MEGA3: Integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163

    Article  CAS  PubMed  Google Scholar 

  • 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 438–492

  • Latta RG, Linhart YB, Mitton JB (2001) Cytonuclear disequilibrium and genetic drift in a natural population of Ponderosa Pine. Genetics 158:843–850

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mallet J, Willmott K (2003) Taxonomy: renaissance or Tower of Babel? TREE 18:57–59

    Google Scholar 

  • 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 360:1917–1924

    Article  CAS  Google Scholar 

  • Mickevich ME, Farris JS (1981) The implications of congruence in Menidia. Syst Zool 27:143–158

    Article  Google Scholar 

  • Miller MP (1997) Tools for population genetic analysis (TFPGA) 1.3 A Windows program for the analysis of allozyme and molecular population genetic data

  • 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 243:137–154

    Article  Google Scholar 

  • Mokievsky VO, Filippova KA, Chesunov AV (2005) Nematode fauna associated with detached kelp accumulations in the subtidal zone of the White Sea. Oceanology 45:689–697

    Google Scholar 

  • Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York

    Google Scholar 

  • Nicholas KB, Nicholas HB (1997) Genedoc: a tool for editing and annotating multiple sequence alignments. Distributed by the author

  • Nylander JAA (2004) MrModeltest v2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University

  • 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 19:306–313

    Article  CAS  PubMed  Google Scholar 

  • 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 13:1991–1999

    Article  CAS  PubMed  Google Scholar 

  • 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 13:2899–2908

    Article  CAS  PubMed  Google Scholar 

  • 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 53:793–808

    Article  PubMed  Google Scholar 

  • Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818

    Article  CAS  PubMed  Google Scholar 

  • Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225

    Article  PubMed  Google Scholar 

  • 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 18:1088–1102

    Article  CAS  PubMed  Google Scholar 

  • Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–569

    CAS  PubMed  Google Scholar 

  • 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 135:399–405

    Article  CAS  Google Scholar 

  • 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, Switzerland

  • Sivasundar A, Hey J (2005) Sampling from natural populations with RNAi reveals high outcrossing and population structure in Caenorhabditis elegans. Curr Biol 15:1598–1602

    Article  CAS  PubMed  Google Scholar 

  • Slatkin M (1987) Gene flow and the geographic structure of natural populations. Science 236:787–792

    Article  CAS  PubMed  Google Scholar 

  • StatSoft, Inc. (2001). STATISTICA (data analysis software system), version 6. http://www.statsoft.com

  • Swofford DL (1998) PAUP*. Phylogenetic Analysis Using Parsimony (*and other methods). Version 4. Sinauer Associates, Sunderland

    Google Scholar 

  • Tautz D, Arctander P, Minelli A, Thomas RH, Vogler AP (2003) A plea for DNA taxonomy. TREE 18:70–74

    Google Scholar 

  • 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 24:4876–4882

    Article  Google Scholar 

  • Ullberg J (2004) Dispersal in free-living, marine, benthic nematodes: passive or active processes? PhD Dissertation, Stockholm University, Sweden, p 27

  • Vincx M (1990) Diversity of nematode communities in the Southern bight of the North Sea. Neth J Sea Res 25:181–188

    Article  Google Scholar 

  • 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 187–195

    Google Scholar 

  • Vincx M, Meire P, Heip C (1990) The distribution of nematode communities in the Southern Bight of the North-Sea. Cah Biol Mar 31:107–129

    Google Scholar 

  • Vranken G (1987) An autecological study of free-living marine nematodes. Acad Anal- Meded K Acad Belg Kl Wet 49:73–97

    Google Scholar 

  • 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 77:296–301

    Article  CAS  PubMed  Google Scholar 

  • Warwick RM, Platt HM, Somerfield PJ (1998) Free-living marine nematodes Part III. Monhysterids. Synopsis of the British fauna 53, Dorset Press, Great Britain

Download references

Acknowledgments

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).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to S. Derycke.

Additional information

Communicated by O. Kinne.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Derycke, S., Backeljau, T., Vlaeminck, C. et al. Spatiotemporal analysis of population genetic structure in Geomonhystera disjuncta (Nematoda, Monhysteridae) reveals high levels of molecular diversity. Mar Biol 151, 1799–1812 (2007). https://doi.org/10.1007/s00227-007-0609-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-007-0609-0

Keywords

Navigation