Marine Biology

, Volume 158, Issue 8, pp 1841–1856 | Cite as

Genetic heterogeneity among Eurytemora affinis populations in Western Europe

  • Gesche WinklerEmail author
  • Sami Souissi
  • Céline Poux
  • Vincent Castric
Original Paper


Evolutionary diversification of the broadly distributed copepod sibling species complex Eurytemora affinis has been documented in the northern hemisphere. However, the fine scale geographic distribution, levels of genetic subdivision, evolutionary, and demographic histories of European populations have been less explored. To gain information on genetic subdivision and to evaluate heterogeneity among European populations, we analyzed samples from 8 locations from 58° to 45°N and 0° to 23°E, using 549 base pairs of the mitochondrial cytochrome oxidase subunit I (COI) gene. We discovered three distinct lineages of E. affinis in Western Europe, namely the East Atlantic lineage, the North Sea/English Channel (NSEC) lineage, and the Baltic lineage. These geographically separated lineages showed sequences divergence of 1.7–2.1%, dating back 1.9 million years (CI: 0.9–3.0 My) with no indication of isolation by distance. Genetic divergence in Europe was much lower than among North American lineages. Interestingly, genetic structure varied distinctively among the three lineages: the East Atlantic lineage was divided between the Gironde and the Loire populations, the NSEC lineage comprised one single population unit spanning the Seine, Scheldt and Elbe rivers and the third lineage was restricted to the Baltic Proper (Sweden). We revealed high haplotype diversity in the East Atlantic and the Baltic lineages, whereas in the NSEC lineage haplotype diversity was comparatively low. All three lineages showed signs of at least one demographic expansion event during Pleistocene glaciations that marked their genetic structure. These results provide a preliminary overview of the genetic structure of E. affinis in Europe.


River Mouth Population Expansion Haplotype Network Mismatch Distribution Glacial Refugium 
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.



Funding for this research was provided by Seine-Aval, 2 conjoint projects: Fond France-Canada for Research and France-Québec #Program Samuel-De Champlain # 62.108 and the Research Federation FR1818. CP was funded by a postdoctoral grant from the University of Lille 1. We thank gratefully H. Gorokhova and S. Strake for providing samples from the Swedish Baltic and the Gulf of Riga, respectively. Special thanks are extended to S. Oesman, A. Cugat; P. Meire, Tom Maris, and M. Tackx; D. Devreker; B. Sautour and V. David for their help in sampling the Elbe, the Scheldt, the Seine, and the Gironde estuaries, respectively. We thank J. Cuguen to have generously accepted a zooplankton post doc (GW) in his botanical laboratory and P. Saumitou-Laprade for fruitful discussions. A. Courseaux and C. Godé provided excellent technical help in the laboratory. We thank C. E. Lee for providing E. affinis sequences for comparison and discussion purposes. We thank 2 anonymous reviewers for their greatly appreciated and helpful comments to improve this paper. Computational resources were provided by CRI-Lille 1 supported by the CNRS and Lille 1 University—Science and Technology. This paper is a contribution to the transversal action “genetics of copepods” within the Multidisciplinary Research Institute for Environemental Sciences (IRePSE) of Lille 1 University and Québec-Océan.

Supplementary material

227_2011_1696_MOESM1_ESM.eps (13.9 mb)
Fig. 1S: Phylogenetic tree resulting from the ML analysis. The bootstrap values are given in Figure 5. The scale bar represents the number of substitutions per site. (EPS 14265 kb)


  1. Albaina A, Villate F, Uriarte I (2009) Zooplankton communities in two contrasting Basque estuaries (1999–2001): reporting changes associated with ecosystem health. J Plankton Res 31:739–752CrossRefGoogle Scholar
  2. Alekseev V, Abramson N, Sukhikh N (2009) Introduction of sibling species to the ecosystem of the Baltic Sea. Doklady Biol Sci 429:544–547CrossRefGoogle Scholar
  3. Appeltans W, Hannouti A, Van Damme S, Soetaert K, Vanthomme R, Tackx M (2003) Zooplankton in the Schelde estuary (Belgium The Netherlands). The distribution of Eurytemora affinis: effect of oxygen? J Plankton Res 25:1441–1445CrossRefGoogle Scholar
  4. Avise JC (1998) Conservation genetics in the marine realm. J Hered 89:377–382CrossRefGoogle Scholar
  5. Avise JC, Neigel JE, Arnold J (1984) Demographic influences on mitochondrial-DNA lineage survivorship in animal populations. J Mol Evol 20:99–105Google Scholar
  6. Beyrend-Dur D, Souissi S, Devreker D, Winkler G, Hwang JS (2009) Life cycle traits of two transatlantic populations of Eurytemora affinis (Copepoda: Calanoida): salinity effects. J Plankton Res 31:713–728CrossRefGoogle Scholar
  7. Bilton DT, Paula J, Bishop JDD (2002) Dispersal, genetic differentiation and speciation in estuarine organisms. Estuar Coast Shelf Sci 55:937–952CrossRefGoogle Scholar
  8. 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
  9. Burkill PH, Kendrall TF (1982) Production of the copepod Eurytemora affinis in the Bristol Channel. Mar Ecol Progr Ser 7:21–31CrossRefGoogle Scholar
  10. Cailleaud K, Maillet G, Budzinski H, Souissi S, Forget-Leray J (2007) Effects of salinity and temperature on the expression of enzymatic biomarkers in Eurytemora affinis (Calanoida, Copepoda). Comp Biochem Physiol Part A Mol Integr Physiol 147:841–849CrossRefGoogle Scholar
  11. Cailleaud K, Forget-Leray J, Peuhiet L et al (2009) Tidal influence on the distribution of hydrophobic organic contaminants in the Seine Estuary and biomarker responses on the copepod Eurytemora affinis. Environ Pollut 157:64–71CrossRefGoogle Scholar
  12. Castel J (1995) Long-term changes in the population of Eurytemora affinis (Copepoda, Calanoida) in the Gironde estuary (1978–1992). Hydrobiologia 311:85–101CrossRefGoogle Scholar
  13. 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
  14. Chen G, Hare MP (2008) Cryptic ecological diversification of a planktonic estuarine copepod, Acartia tonsa. Mol Ecol 17:1451–1468CrossRefGoogle Scholar
  15. Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659CrossRefGoogle Scholar
  16. David V, Sautour B, Chardy P, Leconte M (2005) Long-term changes of the zooplankton variability in a turbid environment: the Gironde estuary (France). Estuar Coast Shelf Sci 64:171–184CrossRefGoogle Scholar
  17. David V, Chardy P, Sautour B (2006) Fitting a predator-prey model to zooplankton time-series data in the Gironde estuary (France): Ecological significance of the parameters. Estuar Coast Shelf Sci 67:605–617CrossRefGoogle Scholar
  18. David V, Sautour B, Chardy P (2007) The paradox between the long-term decrease of egg mass size of the calanoid copepod Eurytemora affinis and its long-term constant abundance in a highly turbid estuary (Gironde estuary, France). J Plankton Res 29:377–389CrossRefGoogle Scholar
  19. Dawson AG (1992) Ice age earth: late quaternary geology and climate. Routledge, LondonGoogle Scholar
  20. Delhez EJM (1996) Modelling the general circulation on the north-western European continental shelf in the perspective of interdisciplinary environmental studies. Bull Soc Roy Sci Liège 65:51–54Google Scholar
  21. Delhez EJM, Deleersnijder E (2002) The concept of age in marine modelling: 2. Concentration distribution function in the English Channel and the North Sea. J Mar Syst 31:279–297CrossRefGoogle Scholar
  22. Devreker D, Souissi S, Seuront L (2004) Development and mortality of the first naupliar stages of Eurytemora affinis (Copepoda, Calanoida) under different conditions of salinity and temperature. J Exp Mar Biol Ecol 303:31–46CrossRefGoogle Scholar
  23. Devreker D, Souissi S, Forget-Leray J, Leboulenger F (2007) Effects of salinity and temperature on the post-embryonic development of Eurytemora affinis (Copepoda; Calanoida) from the Seine estuary: a laboratory study. J Plankton Res 29:117–133CrossRefGoogle Scholar
  24. Devreker D, Souissi S, Molinero JC, Nkubito F (2008) Trade-offs of the copepod Eurytemora affinis in mega-tidal estuaries: insights from high frequency sampling in the Seine estuary. J Plankton Res 30:1329–1342CrossRefGoogle Scholar
  25. Devreker D, Souissi S, Winkler G, Forget-Leray J, Leboulenger F (2009) Effects of salinity, temperature and individual variability on the reproduction of Eurytemora affinis (Copepoda; Calanoida) from the Seine estuary: a laboratory study. J Exp Mar Biol Ecol 368:113–123CrossRefGoogle Scholar
  26. Dodson JJ, Tremblay S, Colombani F, Carscadden JE, Lecomte F (2007) Trans-Arctic dispersals and the evolution of a circumpolar marine fish species complex, the capelin (Mallotus villosus). Mol Ecol 16:5030–5043CrossRefGoogle Scholar
  27. Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214CrossRefGoogle Scholar
  28. Dur G, Souissi S, Devreker D, Ginot V, Schmitt FG, Hwang JS (2009) An individual-based model to study the reproduction of egg bearing copepods: application to Eurytemora affinis (Copepoda Calanoida) from the Seine estuary, France. Ecol Model 220:1073–1089CrossRefGoogle Scholar
  29. Escaravage V, Soetaert K (1995) Secondary production of the brackish copepod communities and their contribution to the carbon fluxes in the Westernscheldt estuary (The Netherlands). Hydrobiologia 311:103–114CrossRefGoogle Scholar
  30. Excoffier L, Laval G, Schneider S (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinforma 1:47–50Google Scholar
  31. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791CrossRefGoogle Scholar
  32. Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotech 3:294–299Google Scholar
  33. Gasparini S, Castel J, Irigoien X (1999) Impact of suspended particulate matter on egg production of the estuarine copepod, Eurytemora affinis. J Mar Syst 22:195–205CrossRefGoogle Scholar
  34. Gelembiuk GW, May GE, Lee CE (2006) Phylogeography and systematics of zebra mussels and related species. Mol Ecol 15:1033–1050CrossRefGoogle Scholar
  35. Ger KA, Teh SJ, Goldman CR (2009) Microcystin-LR toxicity on dominant copepods Eurytemora affinis and Pseudodiaptomus forbesi of the upper San Francisco Estuary. Sci Tot Environ 407:4852–4857CrossRefGoogle Scholar
  36. Gorokhova E, Fagerberg T, Hansson S (2004) Predation by herring (Clupea harengus) and sprat (Sprattus sprattus) on Cercopagis pengoi in a western Baltic Sea bay. Ices J Mar Sci 61:959–965CrossRefGoogle Scholar
  37. Grant WS, Bowen BW (1998) Shallow population histories in deep evolutionary lineages of marine fishes: insights from sardines and anchovies and lessons for conservation. J Hered 89:415–426CrossRefGoogle Scholar
  38. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. System Biol 59:307–321CrossRefGoogle Scholar
  39. Gysels ES, Hellemans B, Pampoulie C, Volckaert FAM (2004) Phylogeography of the common goby, Pomatoschistus microps, with particular emphasis on the colonization of the Mediterranean and the North Sea. Mol Ecol 13:403–417CrossRefGoogle Scholar
  40. Hansson S, Larsson U, Johansson S (1990) Selective predation by herring and mysids, and zooplankton community structure in a Baltic Sea coastal area. J Plankton Res 12:1099–1116CrossRefGoogle Scholar
  41. Hirche HJ (1992) Egg production of Eurytemora affinis—effect of k-strategy. Estuar Coast Shelf Sci 35:395–407CrossRefGoogle Scholar
  42. Hoelzel AR, Green A (1992) Analysis of population-level variation by sequencing PCR-amplified DNA. In: Hoelzel AR (ed) Molecular genetic analysis of populations: a practical approach. Oxford University Press, New YorkGoogle Scholar
  43. Irigoien X, Castel J, Sautour B, Heip C (1993) In situ grazing activity of planktonic copepods in the Gironde Estuary. Cah Biol Mar 34:225–237Google Scholar
  44. Jeppesen E, Sondergaard M, Pedersen AR et al (2007) Salinity induced regime shift in shallow brackish lagoons. Ecosystems 10:47–57CrossRefGoogle Scholar
  45. Johannesson K, Andre C (2006) Life on the margin: genetic isolation and diversity loss in a peripheral marine ecosystem, the Baltic Sea. Mol Ecol 15:2013–2029CrossRefGoogle Scholar
  46. Jolly MT, Jollivet D, Gentil F, Thiebaut E, Viard F (2005) Sharp genetic break between Atlantic and English Channel populations of the polychaete Pectinaria koreni, along the North coast of France. Heredity 94:23–32CrossRefGoogle Scholar
  47. Jolly MT, Viard F, Gentil F, Thiebaut E, Jollivet D (2006) Comparative phylogeography of two coastal polychaete tubeworms in the Northeast Atlantic supports shared history and vicariant events. Mol Ecol 15:1841–1855CrossRefGoogle Scholar
  48. Kimmel DG, Roman MR (2004) Long-term trends in mesozooplankton abundance in Chesapeake Bay, USA: influence of freshwater input. Mar Ecol Progr Ser 267:71–83CrossRefGoogle Scholar
  49. Kimmel DG, Miller WD, Roman MR (2006) Regional scale climate forcing of mesozooplankton dynamics in Chesapeake Bay. Estuaries Coasts 29:375–387Google Scholar
  50. Kimmerer W (2005) Long-term changes in apparent uptake of silica in the San Francisco estuary. Limnol Oceanogr 50:793–798CrossRefGoogle Scholar
  51. Knowlton N (1993) Sibling species in the sea. Ann Rev Ecol System 24:189–216CrossRefGoogle Scholar
  52. Knowlton N (2000) Molecular genetic analyses of species boundaries in the sea. Hydrobiologia 420:73–90CrossRefGoogle Scholar
  53. Knowlton N, Weigt LA (1998) New dates and new rates for divergence across the Isthmus of Panama. Proc Roy Soc Lond Ser B Biol Sci 265:2257–2263CrossRefGoogle Scholar
  54. Koljonen ML, Jansson H, Paaver T, Vasin O, Koskiniemi J (1999) Phylogeographic lineages and differentiation pattern of Atlantic salmon (Salmo salar) in the Baltic Sea with management implications. Can J Fish Aquat Sci 56:1766–1780Google Scholar
  55. Köpcke B, Kausch H (1996) Distribution and varibility in abundance of Neomysis integer and Mesopodopsis slabberi in relation to environmental factors in the Elbe Estuary. Arch Hydrobiol Suppl 110:263–282Google Scholar
  56. Kuhner MK (2006) lamarc 2.0: maximum likelihood and Bayesian estimation of population parameters. Bioinformatics 22:768–770CrossRefGoogle Scholar
  57. Lecomte F, Dodson JJ, Georges S (2000) Impact de la pêcherie commerciale de Charlevoix sur les populations d’éperlans de l’estuaire moyen du Saint-Laurent, p. 47. Société de la Faune et des Parcs du Québec, Direction régionale de Québec, QuébecGoogle Scholar
  58. Lee CE (1999a) Independent invasions of fresh water: comparison of sodium pumping ability among lineages of the copepod Eurytemora affinis. Am Zool 39:93Google Scholar
  59. Lee CE (1999b) Rapid and repeated invasions of fresh water by the copepod Eurytemora affinis. Evolution 53:1423–1434CrossRefGoogle Scholar
  60. Lee CE (2000) Global phylogeography of a cryptic copepod species complex and reproductive isolation between genetically proximate “populations”. Evolution 54:2014–2027CrossRefGoogle Scholar
  61. Lee CE (2002) Evolutionary genetics of invasive species. Trends Ecol Evol 17:386–391CrossRefGoogle Scholar
  62. Lee CE, Frost BW (2002) Morphological stasis in the Eurytemora affinis species complex (Copepoda : Temoridae). Hydrobiologia 480:111–128CrossRefGoogle Scholar
  63. Lee CE, Gelembiuk GW (2008) Evolutionary origins of invasive populations. Evol Appl 1:427–448Google Scholar
  64. Lee CE, Remfert JL, Gelembiuk GW (2003) Evolution of physiological tolerance and performance during freshwater invasions. Integr Comp Biol 43:439–449CrossRefGoogle Scholar
  65. Luttikhuizen PC, Drent J, Baker AJ (2003) Disjunct distribution of highly diverged mitochondrial lineage clade and population subdivision in a marine bivalve with pelagic larval dispersal. Mol Ecol 12:2215–2229CrossRefGoogle Scholar
  66. Mallin MA, Paerl HW (1994) Planktonic trophic transfer in an estuary—seasonal, diel, and community structure effects. Ecology 75:2168–2184CrossRefGoogle Scholar
  67. Mialet B, Azemar F, Maris T, Sossou C, Ruiz P, Lionard M, Van Damme S, Lecerf A, Muylaert K, Toumi N, Meire P, Tackx M (2010) Spatial spring distribution of the copepod Eurytemora affinis (Copepoda, Calanoida) in a restoring estuary, the Scheldt (Belgium). Estuar Coast Shelf Sci 88:116–124CrossRefGoogle Scholar
  68. Michalec F-G, Souissi S, Dur G, Mahjoub M-S, Schmitt FG, Hwang J-S (2010) Differences in behavioral responses of Eurytemora affinis (Copepoda, Calanoida) reproductive stages to salinity variations. J Plankton Res 32:805–813CrossRefGoogle Scholar
  69. Mouny P, Dauvin JC (2002) Environmental control of mesozooplankton community structure in the Seine estuary (English Channel). Oceanol Acta 25:13–22CrossRefGoogle Scholar
  70. Mouny P, Dauvin JC, Bessineton C, Elkaim B, Simon S (1998) Biological components from the Seine estuary: first results. Hydrobiologia 374:333–347CrossRefGoogle Scholar
  71. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New YorkGoogle Scholar
  72. Nikula R, Strelkov P, Vainola R (2007) Diversity and trans-Arctic invasion history of mitochondrial lineages in the North Atlantic Macoma balthica complex (Bivalvia : Tellinidae). Evolution 61:928–941CrossRefGoogle Scholar
  73. North EW, Houde ED (2003) Linking ETM physics, zooplankton prey, and fish early-life histories to striped bass Morone saxatilis and white perch M. americana recruitment. Mar Ecol Progr Ser 260:219–236CrossRefGoogle Scholar
  74. Osinov A, Bernatchez L (1996) Atlantic and Danubean phylogenetic groupings of brown trout (Salmo trutta L.) complex: genetic divergence, evolution, and conservation. J Ichthyol 36:762–786Google Scholar
  75. Peijnenburg K, Breeuwer JAJ, Pierrot-Bults AC, Menken SBJ (2004) Phylogeography of the planktonic chaetognath Sagitta setosa reveals isolation in European seas. Evolution 58:1472–1487Google Scholar
  76. Peitsch A (1993) Difficulties in estimating mortality rates of Eurytemora affinis in the brackish water region of the Elbe estuary. Cah Biol Mar 34:215–224Google Scholar
  77. Peitsch A, Koepcke B, Bernat N (2000) Long-term investigation of the distribution of Eurytemora affinis (Calanoida; Copepoda) in the Elbe Estuary. Limnologica 30:175–182Google Scholar
  78. Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256CrossRefGoogle Scholar
  79. Provan J, Wattier RA, Maggs CA (2005) Phylogeographic analysis of the red seaweed Palmaria palmata reveals a Pleistocene marine glacial refugium in the English Channel. Mol Ecol 14:793–803CrossRefGoogle Scholar
  80. Raymond M, Rousset F (1995) GENEPOP Version 1.2: population genetic software for exact test and ecumenism. J Hered 86:248–249Google Scholar
  81. Remerie T, Vierstraete A, Weekers PHH, Vanfleteren JR, Vanreusel A (2009) Phylogeography of an estuarine mysid, Neomysis integer (Crustacea, Mysida), along the north-east Atlantic coasts. J Biogeogr 36:39–54CrossRefGoogle Scholar
  82. Roman J, Palumbi SR (2004) A global invader at home: population structure of the green crab, Carcinus maenas, in Europe. Mol Ecol 13:2891–2898CrossRefGoogle Scholar
  83. Rozas J, Sanchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497CrossRefGoogle Scholar
  84. Sautour B, Castel J (1995) Comparative spring distribution of zooplankton in three macrotidal European estuaries. Hydrobiologia 311:1–3CrossRefGoogle Scholar
  85. Schluter D (2001) Ecology and the origin of species. Trends Ecol Evol 16:372–380CrossRefGoogle Scholar
  86. Schneider S, Excoffier L (1999) Estimation of demographic parameters from the distribution of pairwise differences when the mutation rates vary among sites: application to human mitochondrial DNA. Genetics 152:1079–1089Google Scholar
  87. Simenstad C, Small L, McIntire C (1990) Consumption processes and food web structure in the Columbia River estuary. Progr Oceanogr 25:1–4CrossRefGoogle Scholar
  88. Sirois P, Dodson J (2000) Influence of turbidity, food density and parasites on the ingestion and growth of larval rainbow smelt Osmerus mordax in an estuarine turbidity maximum. Mar Ecol Progr Ser 193:167–179CrossRefGoogle Scholar
  89. Skelly DA, Chau K, Chang YM, Winkler G, Lee CE (in revision) Limits to range expansions into freshwater habitats: Physiological contrasts between sympatric invasive and noninvasive populations of the copepod Eurytemora affinis Google Scholar
  90. Sotka EE, Wares JP, Barth JA, Grosberg RK, Palumbi SR (2004) Strong genetic clines and geographical variation in gene flow in the rocky intertidal barnacle Balanus glandula. Mol Ecol 13:2143–2156CrossRefGoogle Scholar
  91. Souissi A, Souissi S, Devreker D, Hwang JS (2010) Occurence of intersexuality in a laboratory culture of the copepod Eurytemora affinis from the Seine estuary (France). Mar Biol 157:851–861CrossRefGoogle Scholar
  92. Tackx M, Irigoien X, Daro N et al (1995) Copepod feeding in the Western-Scheldt and the Gironde. Hydrobiologia 311:1–3CrossRefGoogle Scholar
  93. Tackx MLM, Herman PJM, Gasparini S, Irigoien X, Billiones R, Daro MH (2003) Selective feeding of Eurytemora affinis (Copepoda, Calanoida) in temperate estuaries: model and field observations. Estuar Coast Shelf Sci 56:305–311CrossRefGoogle Scholar
  94. Tackx MLM, De Pauw N, Van Mieghem R et al (2004) Zooplankton in the Scheldt estuary, Belgium and the Netherlands. Spatial and temporal patterns. J Plankton Res 26:133–141CrossRefGoogle Scholar
  95. Verspoor E, McCarthy EM, Knox D (1999) The phylogeography of European Atlantic salmon (Salmo salar L.) based on RFLP analysis of the ND1/16sRNA region of the mtDNA. Biol J Linn Soc 68:129–146Google Scholar
  96. Vuorinen I, Ranta E (1987) Dynamics of marine meso-zooplankton at Seili, northern Baltic sea, in 1967–1975. Ophelia 28:31–48Google Scholar
  97. Winkler G, Dodson JJ, Bertrand N, Thivierge D, Vincent WF (2003) Trophic coupling across the St. Lawrence River estuarine transition zone. Mar Ecol Progr Ser 251:59–73CrossRefGoogle Scholar
  98. Winkler G, Martineau C, Dodson JJ, Vincent WF, Johnson LE (2007) Trophic dynamics of two sympatric mysid species in an estuarine transition zone. Mar Ecol Progr Ser 332:171–187CrossRefGoogle Scholar
  99. Winkler G, Dodson JJ, Lee CE (2008) Heterogeneity within the native range: population genetic analyses of sympatric invasive and noninvasive clades of the freshwater invading copepod Eurytemora affinis. Mol Ecol 17:415–430CrossRefGoogle Scholar
  100. Wright S (1943) Isolation by distance. Genetics 28:114–139Google Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Gesche Winkler
    • 1
    Email author
  • Sami Souissi
    • 2
    • 3
    • 4
  • Céline Poux
    • 2
    • 5
  • Vincent Castric
    • 2
    • 5
  1. 1.Institut des Sciences de la Mer de Rimouski, Québec-OcéanUniversité de Québec à RimouskiRimouskiCanada
  2. 2.Université Lille Nord de FranceLilleFrance
  3. 3.USTL, LOG, Station Marine de WimereuxWimereuxFrance
  4. 4.CNRS-UMR 8187, LOGWimereuxFrance
  5. 5.Université des Sciences et Technologies de Lille-Lille 1Villeneuve d’Ascq CedexFrance

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