Evolutionary Ecology

, Volume 27, Issue 2, pp 285–300 | Cite as

An outlier locus relevant in habitat-mediated selection in an alpine plant across independent regional replicates

  • Dominique Buehler
  • Bénédicte N. Poncet
  • Rolf Holderegger
  • Stéphanie Manel
  • Pierre Taberlet
  • Felix GugerliEmail author
Original Paper


Habitat types can induce genetic responses in species and may drive adaptive differentiation and evolutionary divergence of populations. In this study, we aimed at detecting loci indicative of adaptation for different habitat types in the alpine plant Arabis alpina. We used a dataset consisting of A. alpina plants collected in scree, nutrient-rich and moist habitat types in two independent regional replicates of the European Alps (the Swiss and French Alps). Genome scans resulting in 825 amplified fragment length polymorphisms (AFLPs) followed by outlier analysis, i.e. looking for excessive differentiation between habitat types, after accounting for heterozygosity and population structure, was used to detect loci under divergent selection for habitat type within and across the alpine regions. The outlier analyses resulted in the detection of a consistent single outlier locus, which showed a higher fragment frequency in moist compared to the other habitat types in both alpine regions. In addition, a posteriori tests for hierarchical population structuring in the dataset did not detect signals confounding selection at this locus (i.e. signals of regional population structure). Thus, we consider this locus indicative of habitat-mediated selection, and we subsequently sequence-characterized and compared it to the Arabidopsis genome. The sequence was found to be a putative homologue to the SIT4 phosphatase-associated family protein. The detection of this locus in two alpine regions and the availability of its genome sequence make this locus a strong candidate worth further exploration in the habitat-mediated selection and genetic adaptation of natural populations in the alpine plant A. alpina.


Adaptation Arabis alpina Genome scan Habitat type Natural selection Outlier analysis 



We would like to thank Doris Herrmann, René Graf, Conny Thiel-Egenter, Annina Bürgi, Nathalie Baumgartner, Fabio Rimensberger, Rolland Douzet, Serge Aubert, Ludovic Gielly, Delphine Rioux and Claire Redjadj for help in sampling and AFLP genotyping, Sabine Brodbeck for sequence characterization, György Sipos and Christoph Sperisen for advice on the functioning of SIT4 phosphatase-associated family proteins, and Sarah Bryner, Debbie Zulliger and several anonymous reviewers for their valuable comments on the manuscript. Funding was provided by the CCES-BIOCHANGE project of the ETH domain. S. M. was supported by the Institut Universitaire de France.

Supplementary material

10682_2012_9597_MOESM1_ESM.docx (51 kb)
Supplementary material 1 (DOCX 51 kb)


  1. Alonso-Blanco C, Aarts MGM, Bentsink L, Keurentjes JJB, Reymond M, Vreugdenhil D, Koornneef M (2009) What has natural variation taught us about plant development, physiology, and adaptation? Plant Cell 21:1877–1896PubMedCrossRefGoogle Scholar
  2. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410PubMedGoogle Scholar
  3. Alvarez N, Thiel-Egenter C, Tribsch A, Holderegger R, Manel S, Schönswetter P, Taberlet P, Brodbeck S, Gaudeul M, Gielly L, Küpfer P, Mansion G, Negrini R, Paun O, Pellecchia M, Rioux D, Schüpfer F, van Loo M, Winkler M, Gugerli F, IntraBioDiv Consortium (2009) History or ecology? Substrate type as a major driver of spatial genetic structure in Alpine plants. Ecol Lett 12:632–640PubMedCrossRefGoogle Scholar
  4. Ansell SW, Grundmann M, Russell SJ, Schneider H, Vogel JC (2008) Genetic discontinuity, breeding-system change and population history of Arabis alpina in the Italian Peninsula and adjacent Alps. Mol Ecol 17:2245–2257PubMedCrossRefGoogle Scholar
  5. Assefa A, Ehrich D, Taberlet P, Nemomissa S, Brochmann C (2007) Pleistocene colonization of afro-alpine ‘sky islands’ by the arctic-alpine Arabis alpina. Heredity 99:133–142PubMedCrossRefGoogle Scholar
  6. Beaumont M, Balding DJ (2004) Identifying adaptive genetic divergence among populations from genome scans. Mol Ecol 13:969–980PubMedCrossRefGoogle Scholar
  7. Beaumont MA, Nichols RA (1996) Evaluating loci for use in the genetic analysis of population structure. Proc R Soc B 263:1619–1626CrossRefGoogle Scholar
  8. Beilstein MA, Al-Shehbaz A, Kellog EA (2006) Brassicaceae phylogeny and trichome evolution. Am J Bot 93:607–619PubMedCrossRefGoogle Scholar
  9. 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 23:773–783PubMedCrossRefGoogle Scholar
  10. Buehler D, Graf R, Holderegger R, Gugerli F (2012) Contemporary gene flow and mating system of Arabis alpina in a Central European alpine landscape. Ann Bot 109:1359–1367PubMedCrossRefGoogle Scholar
  11. 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 21:945–956PubMedCrossRefGoogle Scholar
  12. Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491PubMedGoogle 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 1:47–50Google Scholar
  14. Excoffier L, Hofer T, Foll M (2009) Detecting loci under selection in a hierarchically structured population. Heredity 103:285–298PubMedCrossRefGoogle Scholar
  15. Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587PubMedGoogle Scholar
  16. Falush D, Stephens M, Pritchard JK (2007) Inference of population structure using multilocus genotype data: dominant markers and null alleles. Mol Ecol Notes 7:574–578PubMedCrossRefGoogle Scholar
  17. Galindo J, Grahame JW, Butlin RK (2011) An EST-based genome scan using 454 sequencing in the marine snail Littorina saxatilis. J Evol Biol 23:2004–2016CrossRefGoogle Scholar
  18. Gugerli F, Englisch T, Niklfeld H, Tribsch A, Mirek Z, Ronikier M, Zimmermann NE, Holderegger R, Taberlet P, IntraBioDiv Consortium (2008) Relationships among levels of biodiversity and the relevance of intraspecific diversity in conservation—a project synopsis. Perspect Plant Ecol Evol Syst 10:259–281CrossRefGoogle Scholar
  19. Herrmann D, Poncet BN, Manel S, Rioux D, Gielly L, Taberlet P, Gugerli F (2010) Selection criteria for scoring amplified fragment length polymorphisms (AFLPs) positively affect the reliability of population genetic parameter estimates. Genome 53:302–310PubMedCrossRefGoogle Scholar
  20. Hofer T, Ray N, Wegmann D, Excoffier L (2009) Large allele frequency differences between human continental groups are more likely to have occurred by drift during range expansions than by selection. Ann Hum Genet 73:95–108PubMedCrossRefGoogle Scholar
  21. Holderegger R, Herrmann D, Poncet B, Gugerli F, Thuiller W, Taberlet P, Gielly L, Rioux D, Brodbeck S, Aubert S, Manel S (2008) Land ahead: using genome scans to identify molecular markers of adaptive relevance. Plant Ecol Divers 1:273–283CrossRefGoogle Scholar
  22. Holderegger R, Buehler D, Gugerli F, Manel S (2010) Landscape genetics of plants. Trends Plant Sci 15:675–683PubMedCrossRefGoogle Scholar
  23. Hubisz MJ, Falush D, Stephens M, Pritchard JK (2009) Inferring weak population structure with the assistance of sample group information. Mol Ecol Res 9:1322–1332CrossRefGoogle Scholar
  24. Jay F, Manel S, Alvarez N, Durand E, Thuiller W, Holderegger R, Taberlet P, François O (2012) Forecasting changes in population genetic structure of Alpine plants in response to global warming. Mol Ecol 21:2354–2368PubMedCrossRefGoogle Scholar
  25. Kawecki TJ, Ebert D (2004) Conceptual issues in local adaptation. Ecol Lett 7:1225–1241CrossRefGoogle Scholar
  26. Keller I, Taverna A, Seehausen O (2010) Evidence of neutral and adaptive genetic divergence between European trout populations sampled along altitudinal gradients. Mol Ecol 20:1888–1904CrossRefGoogle Scholar
  27. Koch MA, Kiefer C, Ehrich D, Vogel J, Brochmann C, Mummenhoff K (2006) Three times out of Asia Minor: the phylogeography of Arabis alpina L. (Brassicaceae). Mol Ecol 15:825–839PubMedCrossRefGoogle Scholar
  28. Körner C (2003) Alpine plant life: functional plant ecology of high mountain ecosystems. Springer, BerlinCrossRefGoogle Scholar
  29. 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 4:981–993PubMedCrossRefGoogle Scholar
  30. Luke MM, Della Seta F, Di Como CJ, Sugimoto H, Kobayashi R, Arndt KT (1996) The SAPs, a new family of proteins, associate and function positively with the SIT4 phosphatase. Mol Cell Biol 16:2744–2755PubMedGoogle Scholar
  31. Manel S, Joost S, Epperson BK, Holderegger R, Storfer A, Rosenberg MS, Scribner KT, Bonin A, Fortin MJ (2010a) Perspectives on the use of landscape genetics to detect genetic adaptive variation in the field. Mol Ecol 19:3760–3772PubMedCrossRefGoogle Scholar
  32. Manel S, Poncet BN, Legendre P, Gugerli F, Holderegger R (2010b) Common factors drive adaptive genetic variation at different spatial scales in Arabis alpina. Mol Ecol 19:3824–3835PubMedCrossRefGoogle Scholar
  33. Miller NJ, Ciosi M, Sappington TW, Ratcliffe ST, Spencer JL, Guillemaud T (2007) Genome scan of Diabrotica virgifera virgifera for genetic variation associated with crop rotation tolerance. J Appl Entomol 131:378–385CrossRefGoogle Scholar
  34. Minder AM, Widmer A (2008) A population genomic analysis of species boundaries: neutral processes, adaptive divergence and introgression between two hybridizing plant species. Mol Ecol 17:1552–1563PubMedCrossRefGoogle Scholar
  35. Nosil P, Funk DJ, Ortiz-Barrientos D (2009) Divergent selection and heterogeneous genomic divergence. Mol Ecol 18:375–402PubMedCrossRefGoogle Scholar
  36. Oetjen K, Ferber S, Dankert I, Reusch TBH (2010) New evidence for habitat-specific selection in Wadden Sea Zostera marina populations revealed by genome scanning using SNP and microsatellite markers. Mar Biol 157:81–89CrossRefGoogle Scholar
  37. Poncet BN, Herrmann D, Gugerli F, Taberlet P, Holderegger R, Gielly L, Rioux D, Thuiller W, Aubert S, Manel S (2010) Tracking genes of ecological relevance using a genome scan in two independent regional population samples of Arabis alpina. Mol Ecol 19:2896–2907PubMedCrossRefGoogle Scholar
  38. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedGoogle Scholar
  39. Reich PB, Wright IJ, Cavender-Bares J, Craine JM, Oleksyn J, Westoby M, Walters MB (2003) The evolution of plant functional variation: traits, spectra, and strategies. Int J Plant Sci 164(Suppl.):143–164CrossRefGoogle Scholar
  40. Reusch TBH, Wood TE (2007) Molecular ecology of global change. Mol Ecol 16:3973–3992PubMedCrossRefGoogle Scholar
  41. Rieseberg LH, Willis JH (2007) Plant speciation. Science 317:910–914PubMedCrossRefGoogle Scholar
  42. Robertson A (1975) Gene frequency distributions as a test of selective neutrality. Genetics 81:775–785PubMedGoogle Scholar
  43. Roden SE, Dutton PH, Morin PA (2009) AFLP fragment isolation technique as a method to produce random sequences for single nucleotide polymorphism discovery in the Green Turtle, Chelonia mydas. J Hered 100:390–393PubMedCrossRefGoogle Scholar
  44. Schlötterer C (2003) Hitchhiking mapping—functional genomics from the population genetics perspective. Trends Genet 19:32–38PubMedCrossRefGoogle Scholar
  45. Schmidt PS, Serrão EA, Pearson GA, Riginos C, Rawson PD, Hilbish TJ, Brawley SH, Trussell GC, Carrington E, Wethey DS, Grahame JW, Bonhomme F, Rand DM (2008) Ecological genetics in the North Atlantic: environmental gradients and adaptation at specific loci. Ecology 89(Suppl.):91–107CrossRefGoogle Scholar
  46. Schönswetter P, Stehlik I, Holderegger R, Tribsch A (2005) Molecular evidence for glacial refugia of mountain plants in the European Alps. Mol Ecol 14:3547–3555PubMedCrossRefGoogle Scholar
  47. Schultze-Motel W (1986) Arabis alpina. In: Hegi G (ed) Ilustrierte Flora von Mitteleuropa V4. Parey, BerlinGoogle Scholar
  48. Sgrò CM, Lowe AJ, Hoffmann AA (2011) Building evolutionary resilience for conserving biodiversity under climate change. Evol Appl 4:326–337CrossRefGoogle Scholar
  49. Shikano T, Ramadevi J, Merilä J (2010) Identification of local- and habitat-dependent selection: scanning functionally important genes in nine-spined sticklebacks (Pungitius pungitius). Mol Biol Evol 27:2775–2789PubMedCrossRefGoogle Scholar
  50. Sobel JM, Chen GF, Watt LR, Schemske DW (2009) The biology of speciation. Evolution 64:295–315PubMedCrossRefGoogle Scholar
  51. Stinchcombe JR, Hoekstra HE (2007) Combining population genomics and quantitative genetics: finding the genes underlying ecologically important traits. Heredity 100:158–170PubMedCrossRefGoogle Scholar
  52. Storz JF (2005) Using genome scans of DNA polymorphism to infer adaptive population divergence. Mol Ecol 14:671–688PubMedCrossRefGoogle Scholar
  53. Tedder A, Ansell SW, Lao X, Vogel JC, Mable BK (2011) Sporophytic self-incompatibility genes and mating system variation in Arabis. Ann Bot 108:699–713PubMedCrossRefGoogle Scholar
  54. The Arabidopsis Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815CrossRefGoogle Scholar
  55. Thiel-Egenter C, Alvarez N, Holderegger R, Tribsch A, Englisch T, Wohlgemuth T, Colli L, Gaudeul M, Gielly L, Jogan N, Linder HP, Negrini R, Niklfeld H, Pellecchia M, Rioux D, Schönswetter P, Taberlet P, van Loo M, Winkler M, IntraBioDiv Consortium, Gugerli F (2011) Break zones in the distributions of alleles and species in alpine plants. J Biogeogr 38:772–782CrossRefGoogle Scholar
  56. Titz W (1971) Zur evolution der Gattung Arabis im Alpenraum. Ber Deut Bot Ges 84:697–704Google Scholar
  57. Turner TL, Bourne EC, Von Wettberg EJ, Hu TT, Nuzhdin SV (2010) Population resequencing reveals local adaptation of Arabidopsis lyrata to serpentine soils. Nat Genet 42:260–263PubMedCrossRefGoogle Scholar
  58. Vasemägi A, Primmer CR (2005) Challenges for identifying functionally important genetic variation: the promise of combining complementary research strategies. Mol Ecol 14:3623–3642PubMedCrossRefGoogle Scholar
  59. Verhoeven KJF, Poorter H, Nevo E, Biere A (2008) Habitat-specific natural selection at a flowering-time QTL is a main driver of local adaptation in two wild barley populations. Mol Ecol 17:3416–3424PubMedGoogle Scholar
  60. Wang R, Farrona S, Vincent C, Joecker A, Schoof H, Turck F, Alonso-Blanco C, Coupland G, Albani MC (2009) PEP1 regulates perennial flowering in Arabis alpina. Nature 459:423–427PubMedCrossRefGoogle Scholar
  61. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370CrossRefGoogle Scholar
  62. 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
  63. Wood HM, Grahame JW, Humphray S, Rogers J, Butlin RK (2008) Sequence differentiation in regions identified by a genome scan for local adaptation. Mol Ecol 17:3123–3135PubMedCrossRefGoogle Scholar
  64. Wright S (1951) The genetical structure of populations. Ann Eugen 15:323–354Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  • Dominique Buehler
    • 1
    • 2
  • Bénédicte N. Poncet
    • 3
  • Rolf Holderegger
    • 1
    • 2
  • Stéphanie Manel
    • 3
    • 4
  • Pierre Taberlet
    • 3
  • Felix Gugerli
    • 1
    Email author
  1. 1.WSL Swiss Federal Research InstituteBirmensdorfSwitzerland
  2. 2.Department of Environmental SciencesETH ZürichZürichSwitzerland
  3. 3.Laboratoire d’Écologie Alpine (LECA), CNRS UMR 5553Université Joseph FourierGrenoble cedex 9France
  4. 4.UMR 151 UP/IRD, Laboratoire Population–Environnement DéveloppementUniversité Aix-MarseilleMarseille cedex 3France

Personalised recommendations