Marine Biology

, Volume 156, Issue 6, pp 1149–1158 | Cite as

Lack of population genetic structuring in the marine planktonic diatom Pseudo-nitzschia pungens (Bacillariophyceae) in a heterogeneous area in the Southern Bight of the North Sea

  • Griet Casteleyn
  • Katharine M. Evans
  • Thierry Backeljau
  • Sofie D’hondt
  • Victor A. Chepurnov
  • Koen Sabbe
  • Wim VyvermanEmail author
Original Paper


Several marine holoplanktonic organisms show a high degree of geographically structured diversity for which it often remains unclear to what extent this differentiation is due to the presence of cryptic taxa. For the genetically distinct diatom Pseudo-nitzschia pungens var. pungens, we used six microsatellite markers to investigate the spatial and temporal genetic composition in the heterogeneous Southern Bight of the North Sea. Although our sampling area (ca. 100 km) comprised water bodies with different environmental conditions (marine, estuary, saline lake) and different degrees of connectivity (from complete isolation to supposedly free exchange between environments), no evidence of genetic differentiation was found. Expanding our sampling area (ca. 650 km), suggested a homogenous population structure over even larger areas in the North Sea. Our results suggest that the population structure of this diatom is mainly shaped by strong homogenizing effects of gene flow preventing genetic drift, even in water bodies with limited connectivity.


Internal Transcribe Spacer Water Residence Time Nuclear Microsatellite Locus German Part Storm Surge Barrier 
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.



Financial support for this research was provided by the Research Programmes G.0292.00 and G.0197.05 of the Flemish Fund for Scientific Research (FWO) and the BOF-project GOA 12050398 of Ghent University. G.C. is funded by the Flemish Institute for the Promotion of Innovation by Science and Technology (IWT). T.B. was supported by FWO-grant G.0404.07. We thank the crew of the Zeeleeuw (VLIZ, Flemish Marine Institute) for the sampling in the North Sea and Frederik Leliaert for help with sampling in the Westerschelde, Oosterschelde and Lake Grevelingen. Andy Vierstraete is thanked for allele fragment electrophoresis.

Supplementary material

227_2009_1157_MOESM1_ESM.pdf (131 kb)
Supplementary Tables (PDF 131 kb)


  1. Amato A, Kooistra WHCF, Levialdi Ghiron JH, Mann DG, Pröschold T, Montresor M (2007) Reproductive isolation among sympatric cryptic species in marine diatoms. Protist 158:193–207CrossRefGoogle Scholar
  2. Barber PH, Palumbi SR, Erdmann MV, Moosa MK (2000) A marine Wallace’s line. Nature 406:92–693CrossRefGoogle Scholar
  3. Bucklin A, Kaartvedt S, Guarnieri M, Goswami U (2000) Population genetics of drifting (Calanus spp.) and resident (Acartia clausi) plankton in Norwegian fjords. J Plankton Res 22:1237–1251CrossRefGoogle Scholar
  4. Casteleyn G, Chepurnov VA, Leliaert F, Mann DG, Bates SS, Lundholm N, Rhodes L, Sabbe K, Vyverman W (2008) Pseudo-nitzschia pungens (Bacillariophyceae): a cosmopolitan diatom species? Harmful Algae 7:241–257CrossRefGoogle Scholar
  5. Casteleyn G, Adams NG, Vanormelingen P, Debeer AE, Sabbe K, Vyverman W (2009) Natural hybrids in the marine diatom Pseudo-nitzschia pungens (Bacillariophyceae): genetic and morphological evidence. Protist, doi: CrossRefGoogle Scholar
  6. Chepurnov VA, Mann DG, Sabbe K, Vyverman W (2004) Experimental studies on sexual reproduction in diatoms. Int Rev Cytol 237:91–154CrossRefGoogle Scholar
  7. Chepurnov VA, Mann DG, Sabbe K, Vannerum K, Casteleyn G, Verleyen E, Peperzak L, Vyverman W (2005) Sexual reproduction, mating system, chloroplast dynamics and abrupt cell size reduction in Pseudo-nitzschia pungens from the North Sea (Bacillariophyta). Eur J Phycol 40:379–395CrossRefGoogle Scholar
  8. Churro CI, Carvalho CC, Rodrigues F, Craveiro SC, Calado AJ, Casteleyn G, Lundholm N (2009) Diversity and abundance of potentially toxic Pseudo-nitzschia Peragallo in Aveiro coastal lagoon, Portugal and description of a new variety, P. pungens var. aveirensis var. nov. Diatom Res (in press)Google Scholar
  9. Cousyn C, De Meester L, Colbourne JK, Brendonck L, Verschuren D, Volckaert F (2001) Rapid, local adaptation of zooplankton behavior to changes in predation pressure in the absence of neutral genetic changes. Proc Natl Acad Sci USA 98:6256–6260CrossRefGoogle Scholar
  10. Darling KF, Wade CA (2008) The genetic diversity of planktic foraminifera and the global distribution of ribosomal RNA genotypes. Mar Micropaleontol 67:216–238CrossRefGoogle Scholar
  11. Darling KF, Kucera M, Pudsey CJ, Wade CM (2004) Molecular evidence links cryptic diversification in polar planktonic protists to quaternary climate dynamics. Proc Natl Acad Sci USA 101:7657–7662CrossRefGoogle Scholar
  12. De Galan S, Elskens M, Goeyens L, Pollentier A, Brion N, Baeyens W (2004) Spatial and temporal trends in nutrient concentrations in the Belgian continental area of the North Sea during the period 1993–2000. Estuar Coast Shelf Sci 61:517–528CrossRefGoogle Scholar
  13. De Vargas C, Norris R, Zaninetti L, Gibb SW, Pawlowski J (1999) Molecular evidence of cryptic speciation in planktonic foraminifers and their relation to oceanic provinces. Proc Natl Acad Sci USA 96:2864–2868CrossRefGoogle Scholar
  14. De Wolf H, Backeljau T, Blust R (2000) Heavy metal accumulation in the periwinkle Littorina littorea, along a pollution gradient in the Scheldt estuary. Sci Total Environ 262:111–121CrossRefGoogle Scholar
  15. 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
  16. Derycke S, Backeljau T, Vlaeminck C, Vierstraete A, Vanfleteren J, Vincx M, Moens T (2007a) Spatiotemporal analysis of population genetic structure in Geomonhystera disjuncta (Nematoda, Monhysteridae) reveals high levels of molecular diversity. Mar Biol 151:1799–1812CrossRefGoogle Scholar
  17. Derycke S, Van Vynckt R, Vanoverbeke J, Vincx M, Moens T (2007b) Colonization patterns of Nematoda on decomposing algae in the estuarine environment: community assembly and genetic structure of the dominant species Pellioditis marina. Limnol Oceanogr 52:992–1001CrossRefGoogle Scholar
  18. Evans KM, Hayes PK (2004) Microsatellite markers for the cosmopolitan marine diatom Pseudo-nitzschia pungens. Mol Ecol Notes 4:125–126CrossRefGoogle Scholar
  19. Evans KM, Kuhn SF, Hayes PK (2005) High levels of genetic diversity and low levels of genetic differentiation in North Sea Pseudo-nitzschia pungens (Bacillariophyceae) populations. J Phycol 41:506–514CrossRefGoogle Scholar
  20. Feder JL, Chilcote CA, Bush GL (1990) The geographic pattern of genetic differentiation between host associated populations of Rhagoletis pomonella (Diptera: Tephritidae) in the Eastern United States and Canada. Evolution 44:570–594CrossRefGoogle Scholar
  21. Gerringa LJA, Poortvliet TCW, Hummel H (1996) Comparison of chemical speciation of copper in the Oosterschelde and Westerschelde estuaries, the Netherlands. Estuar Coast Shelf Sci 42:629–643CrossRefGoogle Scholar
  22. Gerringa LJA, Hummel H, Moerdijk-Poortvliet TCW (1998) Relations between free copper and salinity, dissolved and particulate organic carbon in the Oosterschelde and Westerschelde, Netherlands. J Sea Res 40:193–203CrossRefGoogle Scholar
  23. Goetze E (2005) Global population genetic structure and biogeography of the oceanic copepods Eucalanus hyalinus and E. spinifer. Evolution 59:2378–2398PubMedGoogle Scholar
  24. Goudet J (2001) fstat, a program to estimate and test gene diversities and fixation indices (version 2.9.3). Available from
  25. Guo SW, Thompson EA (1992) Performing the exact test of Hardy–Weinberg proportion for multiple alleles. Biometrics 48:361–372CrossRefGoogle Scholar
  26. Halkett F, Plantegenest M, Prunier-Leterme N, Mieuzet L, Delmotte F, Simon JC (2005) Admixed sexual and facultatively asexual aphid lineages at mating sites. Mol Ecol 14:325–336CrossRefGoogle Scholar
  27. Heip C (1989) The ecology of the estuaries of Rhine, Meuse and Scheldt in the Netherlands. In: Ross JD (eds) Topics in marine biology: proceedings of the 22nd European marine biology symposium, Barcelona. Sci Mar 53:457–463Google Scholar
  28. Hellberg ME, Burton RS, Neigel JE, Palumbi SR (2002) Genetic assessment of connectivity among marine populations. Bull Mar Sci 70:273–290Google Scholar
  29. Koskinen MT, Haugen TO, Primmer CR (2002) Contemporary fisherian life-history evolution in small salmonid populations. Nature 419:826–830CrossRefGoogle Scholar
  30. Lee AJ (1980) North Sea: physical oceanography. In: Banner FT, Collins MB, Massie KS (eds) The North-West European shelf sea: the seabed and the sea in motion. II. Physical and chemical oceanography, and physical resources. Elsevier, Amsterdam, pp 467–493Google Scholar
  31. Nagai S, Lian C, Yamaguchi S, Hamaguchi M, Matsuyama Y, Itakura S, Shimada H, Kaga S, Yamauchi H, Sonda Y, Nishikawa T, Kim CH, Hogetsu T (2007) Microsatellite markers reveal population genetic structure of the toxic dinoflagellate Alexandrium tamarense (Dinophyceae) in Japanese coastal waters. J Phycol 43:43–54CrossRefGoogle Scholar
  32. Nienhuis PH (1978) Lake Grevelingen: a case study of ecosystem changes in a closed estuary. Hydrobiol Bull 12:246–259CrossRefGoogle Scholar
  33. Palumbi SR (1994) Genetic-divergence, reproductive isolation and marine speciation. Annu Rev Ecol Syst 25:547–572CrossRefGoogle Scholar
  34. Pampoulie C, Gysels ES, Maes GE, Hellemans B, Leentjes V, Jones AG, Volckaert FAM (2004) Evidence for fine-scale genetic structure and estuarine colonisation in a potential high gene flow marine goby (Pomatoschistus minutus). Heredity 92:434–445CrossRefGoogle Scholar
  35. Park SDE (2001) Trypanotolerance in West African cattle and the population genetic effects of selection. Ph.D. thesis, University of DublinGoogle Scholar
  36. Peakall R, Smouse PE (2006) GenAlEx 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295CrossRefGoogle Scholar
  37. Peakall R, Smouse PE, Huff DR (1995) Evolutionary implications of allozyme and RAPD variation in diploid populations of dioecious buffalograss [Buchloe dactyloides (Nutt.) Engelm.]. Mol Ecol 4:135–147CrossRefGoogle Scholar
  38. Peijnenburg KTCA, Fauvelot C, Breeuwer AJ, Menken BJ (2006) Spatial and temporal genetic structure of the planktonic Sagitta setosa (Chaetognatha) in European seas as revealed by mitochondrial and nuclear DNA markers. Mol Ecol 15:3319–3338CrossRefGoogle Scholar
  39. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedPubMedCentralGoogle Scholar
  40. Pritchard JK, Wen X, Falush D (2007) Documentation for structure software: Version 2.2. Available from
  41. Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225CrossRefGoogle Scholar
  42. Rousset F (2008) genepop’007: a complete re-implementation of the genepop software for Windows and Linux. Mol Ecol Res 8:103–106CrossRefGoogle Scholar
  43. Rynearson TA, Armbrust EV (2004) Genetic differentiation among populations of the planktonic marine diatom Ditylum brightwellii (Bacillariophyceae). J Phycol 40:34–43CrossRefGoogle Scholar
  44. Rynearson TA, Armbrust EV (2005) Maintenance of clonal diversity during a spring bloom of the centric diatom Ditylum brightwellii. Mol Ecol 14:1631–1640CrossRefGoogle Scholar
  45. Rynearson TA, Newton JA, Armbrust EV (2006) Spring bloom development, genetic variation, and population succession in the planktonic diatom Ditylum brightwellii. Limnol Oceanogr 51:1249–1261CrossRefGoogle Scholar
  46. Smaal AC, Nienhuis PH (1992) The Eastern Scheldt (The Netherlands), from an estuary to a tidal bay: a review of responses at the ecosystem level. Neth J Sea Res 30:161–173CrossRefGoogle Scholar
  47. Soetaert K, Herman PMJ (1995) Estimating estuarine residence times in the Westerschelde (The Netherlands) using a box model with fixed dispersion coefficients. Hydrobiologia 311:215–224CrossRefGoogle Scholar
  48. Valiere N (2002) gimlet: a computer program for analysing genetic individual identification data. Mol Ecol Notes 2:377–379Google Scholar
  49. Van Loon EE, Cleary DFR, Fauvelot C (2007) ares: software to compare allelic richness between uneven samples. Mol Ecol Notes 7:579–582CrossRefGoogle Scholar
  50. Van Oosterhout C, Hutchinson WF, Wills DPM (2004) micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538CrossRefGoogle Scholar
  51. Van Raaphorst W, Philippart CJM, Smit JPC, Dijkstra FJ, Malschaert JFP (1998) Distribution of suspended particulate matter in the North Sea as inferred from NOAA/AVHRR reflectance images and in situ observations. J Sea Res 39:197–215CrossRefGoogle Scholar
  52. Waits LP, Luikart G, Taberlet P (2001) Estimating the probability of identity among genotypes in natural populations: cautions and guidelines. Mol Ecol 10:249–256CrossRefGoogle Scholar
  53. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370Google Scholar
  54. Wright S (1951) The genetical structure of populations. Ann Eugen 15:323–354CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Griet Casteleyn
    • 1
  • Katharine M. Evans
    • 2
  • Thierry Backeljau
    • 3
    • 4
  • Sofie D’hondt
    • 1
  • Victor A. Chepurnov
    • 1
    • 5
  • Koen Sabbe
    • 1
  • Wim Vyverman
    • 1
    Email author
  1. 1.Laboratory of Protistology and Aquatic Ecology, Biology DepartmentGhent UniversityGhentBelgium
  2. 2.Royal Botanic Garden EdinburghEdinburghUK
  3. 3.Royal Belgian Institute of Natural SciencesBrusselsBelgium
  4. 4.Evolutionary Ecology Group, Department of BiologyUniversity of AntwerpAntwerpBelgium
  5. 5.SBAE Industries NVWaarschootBelgium

Personalised recommendations