Marine Biology

, Volume 157, Issue 1, pp 81–89

New evidence for habitat-specific selection in Wadden Sea Zostera marina populations revealed by genome scanning using SNP and microsatellite markers

  • Katharina Oetjen
  • Steven Ferber
  • Ilka Dankert
  • Thorsten B. H. Reusch
Original Paper


Eelgrass Zostera marina is an ecosystem-engineering species of outstanding importance for coastal soft sediment habitats that lives in widely diverging habitats. Our first goal was to detect divergent selection and habitat adaptation at the molecular genetic level; hence, we compared three pairs of permanently submerged versus intertidal populations using genome scans, a genetic marker-based approach. Three different statistical approaches for outlier identification revealed divergent selection at 6 loci among 46 markers (6 SNPs, 29 EST microsatellites and 11 anonymous microsatellites). These outlier loci were repeatedly detected in parallel habitat comparisons, suggesting the influence of habitat-specific selection. A second goal was to test the consistency of the general genome scan approach by doubling the number of gene-linked microsatellites and adding single nucleotide polymorphism (SNP) loci, a novel marker type for seagrasses, compared to a previous study. Reassuringly, results with respect to selection were consistent among most marker loci. Functionally interesting marker loci were linked to genes involved in osmoregulation and water balance, suggesting different osmotic stress, and reproductive processes (seed maturation), pointing to different life history strategies. The identified outlier loci are valuable candidates for further investigation into the genetic basis of natural selection.

Supplementary material

227_2009_1297_MOESM1_ESM.doc (250 kb)
Supplementary material 1 (DOC 250 kb)


  1. Akey JM, Eberle MA, Rieder MJ, Carlson CS, Shriver MD, Nickerson DA et al (2004) Population history and natural selection shape patterns of genetic variation in 132 genes. PLOS Biol 2:1591–1599CrossRefGoogle Scholar
  2. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM et al (2000) Gene ontology: tool for the unification of biology. Nat Genet 25:25–29CrossRefPubMedGoogle Scholar
  3. Beaumont MA, Balding DJ (2004) Identifying adaptive genetic divergence among populations from genome scans. Mol Ecol 13:969–980CrossRefPubMedGoogle Scholar
  4. Beaumont MA, Nichols RA (1996) Evaluating loci for use in the genetic analysis of population structure. Proc Biol Sci 263:1619–1626CrossRefGoogle Scholar
  5. Bonin A, Taberlet P, Miaud C, Pompanon F (2006) Explorative genome scan to detect candidate loci for adaptation along a gradient of altitude in the common frog (Rana temporaria). Mol Biol Evol 23:773–783CrossRefPubMedGoogle Scholar
  6. Bouck A, Vision T (2007) The molecular ecologist’s guide to expressed sequence tags. Mol Ecol 16:907–924CrossRefPubMedGoogle Scholar
  7. Campbell D, Bernatchez L (2004) Genomic scan using AFLP markers as a means to assess the role of directional selection in the divergence of sympatric whitefish ecotypes. Mol Biol Evol 21:945–956CrossRefPubMedGoogle Scholar
  8. Costanza R, d’Arge R, de Groot R, Farber S, Grasso M, Hannon B et al (1997) The value of the world’s ecosystem services and natural capital. Nature 387:253–260CrossRefGoogle Scholar
  9. den Hartog C (1970) The seagrasses of the world. Verh K Ned Akad We. Afd Natuurkd II 59:1–275Google Scholar
  10. Dieringer D, Schlötterer C (2003) MICROSATELLITE ANALYSER (MSA): a platform independent analysis tool for large microsatellite data sets. Mol Ecol Notes 3:167–169CrossRefGoogle Scholar
  11. Duarte CM (2002) The future of seagrass meadows. Environ Cons 29:192–206Google Scholar
  12. Egan SP, Nosil Patrik, Funk DanielJ (2008) Selection and genomic differentiation during ecological speciation: isolating the contributions of host association via a comparative genome scan of Neochlamisus bebbianae leaf beetles. Evolution 62:1162–1181CrossRefPubMedGoogle Scholar
  13. Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50PubMedGoogle Scholar
  14. Ferber S, Reusch TBH, Stam WT, Olsen JL (2008) Characterization of single nucleotide polymorphism markers for eelgrass (Zostera marina). Mol Ecol Resour 8:1429–1435CrossRefGoogle Scholar
  15. Glaubitz JC, Rhodes OE, Dewoody JA (2003) Prospects for inferring pairwise relationships with single nucleotide polymorphisms. Mol Ecol 12:1039–1047CrossRefPubMedGoogle Scholar
  16. Harr B, Kauer M, Schlötterer C (2003) Hitchhiking mapping: a population-based fine-mapping strategy for adaptive mutations in Drosophila melanogaster (vol 99, pg 12949, 2002). Proc Natl Acad Sci USA 100:3004CrossRefGoogle Scholar
  17. Harris MA, Clark JI, Ireland A, Lomax J, Ashburner M, Collins R et al (2006) The gene ontology (GO) project in 2006. Nucleic Acids Res 34:D322–D326CrossRefGoogle Scholar
  18. Hemminga M, Duarte C (2000) Seagrass ecology. Cambridge University Press, CambridgeGoogle Scholar
  19. Kane NC, Rieseberg LH (2007) Selective sweeps reveal candidate genes for adaptation to drought and salt tolerance in common sunflower, Helianthus annuus. Genetics 175:1823–1834CrossRefPubMedGoogle Scholar
  20. Kauer MO, Dieringer D, Schlötterer C (2003) A microsatellite variability screen for positive selection associated with the “Out of Africa” habitat expansion of Drosophila melanogaster. Genetics 165:1137–1148PubMedGoogle Scholar
  21. Lewontin RC, Krakauer J (1973) Distribution of gene frequency as a test of theory of selective neutrality of polymorphisms. Genetics 74:175–195PubMedGoogle Scholar
  22. Luikart G, England PR, Tallmon D, Jordan S, Taberlet P (2003) The power and promise of population genomics: from genotyping to genome typing. Nat Rev Genet 4:981–994CrossRefPubMedGoogle Scholar
  23. Luu D-T, Maurel C (2005) Aquaporins in a challenging environment: molecular gears for adjusting plant water status. Plant Cell Environ 28:85–96CrossRefGoogle Scholar
  24. Mäkinen HS, Cano JM, Merilä J (2008) Identifying footprints of directional and balancing selection in marine and freshwater three-spined stickleback Gasterosteus aculeatus populations. Mol Ecol 17:3565–3582CrossRefPubMedGoogle Scholar
  25. Massa SI, Arnaud-Haond S, Pearson GA, Serrao E (2009) Temperature tolerance and survival of intertidal populations of the seagrass Zostera noltii (Hornemann) in southern Europe (Ria Formosa, Portugal). Hydrobiologia. doi:10.1007/s10750-008-9609-4
  26. Namroud M-C, Beaulieu Jean, Juge Nicolas, Laroche Jerome, Bousquet Jean (2008) Scanning the genome for gene single nucleotide polymorphisms involved in adaptive population differentiation in white spruce. Mol Ecol 17:3599–3613CrossRefPubMedGoogle Scholar
  27. Nielsen R (2005) Molecular signatures of natural selection. Annu Rev Genet 39:197–218CrossRefPubMedGoogle Scholar
  28. Oetjen K, Reusch TBH (2007) Genome scans detect consistent divergent selection among subtidal vs. intertidal populations of the marine angiosperm Zostera marina. Mol Ecol 16:5156–5157PubMedCrossRefGoogle Scholar
  29. Olsen JL, Stam WT, Coyer JA, Reusch TBH, Billingham M, Bostrom C et al (2004) North Atlantic phylogeography and large-scale population differentiation of the seagrass Zostera marina L. Mol Ecol 13:1923–1941CrossRefPubMedGoogle Scholar
  30. Orth RJ, Carruthers TJB, Dennison WC, Duarte CM, Fourqurean JW, Heck KL et al (2006) A global crisis for seagrass ecosystems. Bioscience 56:987–996CrossRefGoogle Scholar
  31. Ouborg NJ, Vriezen WH (2007) An ecologist’s guide to ecogenomics. J Ecol 95:8–16CrossRefGoogle Scholar
  32. Reise K (1985) Tidal flat ecology: an experimental approach to species interactions. Springer, BerlinGoogle Scholar
  33. Reise K, Jager Z, De Jong D, Van Katwijk M, Schanz A (2005) Seagrass—Wadden Sea ecosystem no. 19. Common Wadden Sea Secretariat, WilhelmshavenGoogle Scholar
  34. Rengmark AH, Slettan A, Skaala O, Lie O, Lingaas F (2006) Genetic variability in wild and farmed Atlantic salmon (Salmo salar) strains estimated by SNP and microsatellites. Aquaculture 253:229–237CrossRefGoogle Scholar
  35. Reusch TBH (2002) Microsatellites reveal high population connectivity in eelgrass (Zostera marina) in two contrasting coastal areas. Limnol Oceanogr 47:78–85CrossRefGoogle Scholar
  36. Reusch TBH, Veron AS, Preuss C, Weiner J, Wissler L, Beck A et al (2008) Comparative analysis of expressed sequence tag (EST) libraries in the seagrass Zostera marina subjected to temperature stress. Mar Biotechnol 10:297–309CrossRefPubMedGoogle Scholar
  37. Ryynanen HJ, Tonteri A, Vasemagi A, Primmer CR (2007) A comparison of Biallelic markers and microsatellites for the estimation of population and conservation genetic parameters in Atlantic Salmon (Salmo salar). J Hered 98:692–704CrossRefPubMedGoogle Scholar
  38. Schlötterer C (2002a) A microsatellite-based multilocus screen for the identification of local selective sweeps. Genetics 160:753–763PubMedGoogle Scholar
  39. Schlötterer C (2002b) Towards a molecular characterization of adaptation in local populations. Curr Opin Genet Dev 12:683–687CrossRefPubMedGoogle Scholar
  40. Schlötterer C (2003) Hitchhiking mapping—functional genomics from the population genetics perspective. Trends Genet 19:32–38CrossRefPubMedGoogle Scholar
  41. Scotti-Saintagne C, Mariette S, Porth I, Goicoechea PG, Barreneche T, Bodenes K et al (2004) Genome scanning for interspecific differentiation between two closely related oak species Quercus robur L. and Q. petraea (Matt.) Liebl. Genetics 168:1615–1626CrossRefPubMedGoogle Scholar
  42. Silander JA (1979) Microevolution and clone structure in Spartina patens. Science 203:658–660CrossRefPubMedGoogle Scholar
  43. Smith JM, Haigh J (1974) Hitch-hiking effect of a favorable gene. Genet Res 23:23–35CrossRefPubMedGoogle Scholar
  44. Stinchcombe JR, Hoekstra HE (2008) Combining population genomics and quantitative genetics: finding the genes underlying ecologically important traits. Heredity 100:158–170CrossRefPubMedGoogle Scholar
  45. Storz JF (2005) Using genome scans of DNA polymorphism to infer adaptive population divergence. Mol Ecol 14:671–688CrossRefPubMedGoogle Scholar
  46. Teshima KM, Coop G, Przeworski M (2006) How reliable are empirical genomic scans for selective sweeps? Genome Res 16:702–712CrossRefPubMedGoogle Scholar
  47. Thornton KR, Jensen JD (2007) Controlling the false-positive rate in multilocus genome scans for selection. Genetics 175:737–750CrossRefPubMedGoogle Scholar
  48. Tsumura Y, Kado T, Takahashi T, Tani N, Ujino-Ihara T, Iwata H (2007) Genome scan to detect genetic structure and adaptive genes of natural populations of Cryptomeria japonica. Genetics 176:2393–2403CrossRefPubMedGoogle Scholar
  49. van Katwijk MM, Hermus DCR (2000) Effects of water dynamics on Zostera marina: transplantation experiments in the intertidal Dutch Wadden Sea. Mar Ecol Prog Ser 208:107–118CrossRefGoogle Scholar
  50. Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538CrossRefGoogle Scholar
  51. Vasemagi A, Nilsson J, Primmer CR (2005) Expressed sequence tag-linked microsatellites as a source of gene-associated polymorphisms for detecting signatures of divergent selection in Atlantic salmon (Salmo salar L.). Mol Biol Evol 22:1067–1076CrossRefPubMedGoogle Scholar
  52. Vitalis R, Dawson K, Boursot P (2001) Interpretation of variation across marker loci as evidence of selection. Genetics 158:1811–1823PubMedGoogle Scholar
  53. Vitalis R, Dawson K, Boursot P, Belkhir K (2003) DetSel 1.0: a computer program to detect markers responding to selection. J Hered 94:429–431CrossRefPubMedGoogle Scholar
  54. Waycott M, Duarte CM, Carruthers TJB, Orth RJ, Dennison WC, Olyarnik S et al (2009) Accelerating loss of seagrasses across the globe threatens coastal ecosystems. Proc Natl Acad Sci USA 106:12377–12381CrossRefPubMedGoogle Scholar
  55. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370CrossRefGoogle Scholar
  56. Wilding CS, Butlin RK, Grahame J (2001) Differential gene exchange between parapatric morphs of Littorina saxatilis detected using AFLP markers. J Evol Biol 14:611–619CrossRefGoogle Scholar
  57. Wissler L, Dattolo E, Moore AD, Reusch TBH, Olsen JL, Migliaccio M, Bornberg-Bauer E, Procaccini G (2009) Dr. Zompo: an online data repository for Zostera marina and Posidonia oceanica ESTs. Database 2009: bap009Google Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Katharina Oetjen
    • 1
    • 3
  • Steven Ferber
    • 2
  • Ilka Dankert
    • 1
  • Thorsten B. H. Reusch
    • 3
  1. 1.Institute for Evolution and Biodiversity, Plant Evolutionary EcologyUniversity of MünsterMünsterGermany
  2. 2.Department of Marine Benthic Ecology and Evolution, Centre for Ecological and Evolutionary Studies (CEES)University of GroningenHarenThe Netherlands
  3. 3.Evolutionary Ecology of Marine FishesLeibniz-Institut für Meereswissenschaften (IFM-GEOMAR)KielGermany

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