Advertisement

Alpine Botany

, Volume 128, Issue 1, pp 35–45 | Cite as

The phylogeographic structure of Arabis alpina in the Alps shows consistent patterns across different types of molecular markers and geographic scales

  • Aude Rogivue
  • René Graf
  • Christian Parisod
  • Rolf Holderegger
  • Felix Gugerli
Original Article

Abstract

Glaciation during the Pleistocene confined alpine species to refugial areas. These range contractions had major impacts on the spatial genetic structure of alpine species. Consequently, one should take into account the often complex phylogeographic structure of species when performing genomic research, e.g. on signatures of local adaptation. Understanding the phylogeography of the widespread arctic and alpine Arabis alpina is particularly important, as this species is developing into a model species for ecological genetics. The first objective of this study was to assess the genetic variation of A. alpina across the Alps and to compare the spatial genetic patterns resulting from two different types of molecular markers, namely nuclear microsatellites and amplified fragment length polymorphisms (AFLPs). A second objective was to infer the distribution of genetic variation at the regional scale to understand the genetic structure of populations in the area of a previously suggested contact zone between genetic clusters that presumably recolonised their current range from different glacial refugia. We characterized the phylogeographic structure of 372 individuals from 127 populations across the entire Alpine range, complemented by 364 individuals from 22 populations in the western Swiss Alps. Nuclear microsatellite and AFLP markers described consistent population clustering, coherent with previous phylogeographic analyses. Furthermore, regional population structure in the western Alps of Switzerland highlighted a contact zone of genetic clusters associated with different presumed refugia. Again, this finding was in accordance with recolonisation routes formerly inferred for other plant taxa of the western Swiss Alps. Our results highlight the coincidence of large-scale patterns of genetic structure among alternative types of molecular markers and set a valuable basis for further studies on ecological genomics in A. alpina.

Keywords

AFLPs Alps Brassicaceae Microsatellites Spatial genetic pattern 

Notes

Acknowledgements

We thank Maurice Moor, Alexandra Foetisch and Sabine Brodbeck for the sampling in the western Alps of Switzerland and the IntraBioDiv Consortium for the DNA samples of the entire Alpine range. Christian Rellstab contributed to discussions, and two anonymous reviewers provided valuable comments. This study was financially supported by the Swiss National Science Foundation (GeneScale; CR32I3_149741/1).

Author contributions

Aude Rogivue and Felix Gugerli designed the study, René Graf did the lab work and the genotyping, Aude Rogivue performed all the analyses and wrote the manuscript, with contributions from Christian Parisod, Rolf Holderegger and Felix Gugerli.

Compliance with ethical standards

Conflict of interest

All authors declare that they have no conflicts of interests.

Supplementary material

35_2017_196_MOESM1_ESM.pdf (221 kb)
Online Resource 1 Three main putative recolonisation pathways in the western Alps of Switzerland based on Parisod (2008). The names of main mountain ranges are given in bold, country names and regions are in normal font. Dark grey arrows indicate the Rhodanian pathway, grey arrows the transalpine eastern pathway and white arrows the transalpine southern pathway, including the Simplon pass pathway. (PDF 221 KB)
35_2017_196_MOESM2_ESM.pdf (76 kb)
Online Resource 2 Sampling locations of the 22 populations of Arabis alpina from the regional scale study in the western Swiss Alps. (PDF 75 KB)
35_2017_196_MOESM3_ESM.pdf (265 kb)
Online Resource 3 Plot of mean likelihood LnP(D) and variance among repetitions per K value as well as the ∆K plots (Evanno et al. 2005) from the STRUCTURE analyses (Pritchard et al. 2000; Hubisz et al. 2009) of Arabis alpina for (a and b) the alpine data set using microsatellite markers, (c and d) the alpine dataset using AFLP markers, (e and f) the alpine including the regional data with microsatellite markers, (g and h) only the regional dataset with microsatellite markers and, (i and j) only the regional dataset with microsatellite markers but analysed with INSTRUCT (Gao et al. 2007). (PDF 266 KB)
35_2017_196_MOESM4_ESM.pdf (797 kb)
Online Resource 4 Genetic clustering of Arabis alpina determined by STRUCTURE analyses (Pritchard et al. 2000; Hubisz et al. 2009) of 19 microsatellite markers for K = 2–11 across the Alps. (PDF 797 KB)
35_2017_196_MOESM5_ESM.pdf (1018 kb)
Online Resource 5 Genetic clustering of Arabis alpina determined by STRUCTURE analyses (Pritchard et al. 2000; Hubisz et al. 2009) of 150 AFLP markers for K = 2–10 across the Alps. (PDF 1019 KB)
35_2017_196_MOESM6_ESM.pdf (66 kb)
Online Resource 6 Plot of the coefficients of similarity, calculated with CLUMPAK (Kopelman et al. 2015) for each K value, among the population membership coefficients of Arabis alpina using microsatellite and AFLP markers. (PDF 66 KB)
35_2017_196_MOESM7_ESM.pdf (61 kb)
Online Resource 7 Population genetic parameters inferred from 19 microsatellite markers in 18 populations of Arabis alpina. Number of sampled individuals per population, observed (H o) and expected heterozygosity (H e) and the inbreeding coefficient F IS. (PDF 61 KB)
35_2017_196_MOESM8_ESM.pdf (70 kb)
Online Resource 8 Pairwise F ST values among 18 populations of Arabis alpina in the western Swiss Alps, based on 19 nuclear microsatellite markers. (PDF 69 KB)
35_2017_196_MOESM9_ESM.pdf (1 mb)
Online Resource 9 Genetic clustering determined by STRUCTURE analyses (Pritchard et al. 2000; Hubisz et al. 2009) of the 364 individuals from 22 populations of Arabis alpina from the western Swiss Alps using 19 microsatellite markers for K = 2–15. (PDF 1033 KB)
35_2017_196_MOESM10_ESM.pdf (3.8 mb)
Online Resource 10 Genetic clustering of the 18 populations of Arabis alpina in the western Swiss Alps, using 19 microsatellite markers, determined (a) by STRUCTURE analyses (Pritchard et al. 2000; Hubisz et al. 2009) and by (b) INSTRUCT (Gao et al. 2007), which uses the estimated selfing rate to infer individual memberships. (PDF 3933 KB)

References

  1. Alvarez N et al (2009) History or ecology? Substrate type as a major driver of patial genetic structure in Alpine plants. Ecol Lett 12:632–640CrossRefPubMedGoogle Scholar
  2. 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 17:2245–2257CrossRefPubMedGoogle Scholar
  3. Ansell SW, Stenøien HK, Grundmann M, Russell SJ, Koch MA, Schneider H, Vogel JC (2011) The importance of Anatolian mountains as the cradle of global diversity in Arabis alpina, a key arctic-alpine species. Ann Bot 108:241–252CrossRefPubMedPubMedCentralGoogle Scholar
  4. 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 99:133–142CrossRefPubMedGoogle Scholar
  5. Bettin O, Cornejo C, Edwards P, Holderegger R (2007) Phylogeography of the high alpine plant Senecio halleri (Asteraceae) in the European Alps: in situ glacial survival with postglacial stepwise dispersal into peripheral areas. Mol Ecol 16:2517–2524CrossRefPubMedGoogle Scholar
  6. Bonin A, Bellemain E, Bronken Eidesen P, Pompanon F, Brochmann C, Taberlet P (2004) How to track and assess genotyping errors in population genetics studies. Mol Ecol 13:3261–3273CrossRefPubMedGoogle Scholar
  7. Bovet L, Kammer P, Meylan-Bettex M, Guadagnuolo R, Matera V (2006) Cadmium accumulation capacities of Arabis alpina under environmental conditions. Environ Exp Bot 57:80–88CrossRefGoogle Scholar
  8. Briquet J (1906) Le development des flores dans les Alpes occidentales avec aperçu sur les Alpes en général. In: von Wetterstein R, Wiesner J, Zahlbruckner A (eds) Wissenschaftliche Ergebnisse des Internationalen Botanischcn Kongresses Wien 1905. Gustav Fischer, Jena, pp 130–173Google Scholar
  9. Brochmann C, Gabrielsen TM, Nordal I, Landvik JY, Elven R (2003) Glacial survival or tabula rasa? The history of North Atlantic biota revisited. Taxon 52:417–450CrossRefGoogle Scholar
  10. Brockmann-Jerosch H, Brockmann-Jerosch MC (1926) Die Geschichte der Schweizerischen Alpenflora. In: Schröter C (ed) Das Pflanzenleben der Alpen. Raustein, Zürich, pp 1110–1215Google Scholar
  11. Buehler D, Graf R, Holderegger R, Gugerli F (2011) Using the 454 pyrosequencing-based technique in the development of nuclear microsatellite loci in the alpine plant Arabis alpina (Brassicaceae). Am J Bot 98:e103–e105CrossRefPubMedGoogle Scholar
  12. 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 109:1359–1367CrossRefPubMedPubMedCentralGoogle Scholar
  13. Buehler D, Poncet BN, Holderegger R, Manel S, Taberlet P, Gugerli F (2013) An outlier locus relevant in habitat-mediated selection in an alpine plant across independent regional replicates. Evol Ecol 27:285–300CrossRefGoogle Scholar
  14. Christ H (1907) La flore de la Suisse. Georg & Cie, Bâle-Genève-LyonGoogle Scholar
  15. Delarze R (1987) L’origine des pelouses steppiques valaisannes à la lumière de leurs liens de parenté avec les régions limitrophes. Bull Murith Soc Valais Sci Nat 105:41–70Google Scholar
  16. DeWoody J, Nason JD, Hipkins VD (2006) Mitigating scoring errors in microsatellite data from wild populations. Mol Ecol Notes 6:951–957CrossRefGoogle Scholar
  17. Duforet-Frebourg N, Blum MG (2014) Non stationary patterns of isolation-by-distance: infering measures of local genetic differentiation with Bayesian kriging. Evol 68:1110–1123CrossRefGoogle Scholar
  18. Earl DA, von Holdt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361CrossRefGoogle Scholar
  19. Ehrenreich IM, Hanzawa Y, Chou L, Roe JL, Kover PX, Purugganan MD (2009) Candidate gene association mapping of Arabidopsis flowering time. Genetics 183:325–335CrossRefPubMedPubMedCentralGoogle Scholar
  20. Ehrich D et al (2007) Genetic consequences of Pleistocene range shifts: contrast between the Arctic, the Alps and the East African mountains. Mol Ecol 16:2542–2559CrossRefPubMedGoogle Scholar
  21. Estoup A, Jarne P, Cornuet JM (2002) Homoplasy and mutation model at microsatellite loci and their consequences for population genetics analysis. Mol Ecol 11:1591–1604CrossRefPubMedGoogle Scholar
  22. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620CrossRefPubMedGoogle Scholar
  23. Gao H, Williamson S, Bustamante CD (2007) A Markov chain Monte Carlo approach for joint inference of population structure and inbreeding rates from multilocus genotype data. Genetics 176:1635–1651CrossRefPubMedPubMedCentralGoogle Scholar
  24. Gaudeul M, Till-Bottraud I, Barjon F, Manel S (2004) Genetic diversity and differentiation in Eryngium alpinum L. (Apiaceae): comparison of AFLP and microsatellite markers. Heredity 92:508–518CrossRefPubMedGoogle Scholar
  25. Gugerli F et al (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
  26. Guyot H (1934) Phytogéographie comparée du Valais et de la vallée d’Aoste. Bull Murith Soc Valais Sci Nat 52:16–35Google Scholar
  27. Hardy OJ, Vekemans X (2002) SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Resour 2:618–620CrossRefGoogle Scholar
  28. Hewitt GM (1996) Some genetic consequences of ice ages, and their role in divergence and speciation. Biol J Linn Soc 58:247–276CrossRefGoogle Scholar
  29. Hewitt GM (1999) Post-glacial re-colonization of European biota. Biol J Linn Soc 68:87–112CrossRefGoogle Scholar
  30. Hewitt G (2004) Genetic consequences of climatic oscillations in the Quaternary. Phil Trans R Soc B 359:183–195CrossRefPubMedPubMedCentralGoogle Scholar
  31. Holderegger R, Thiel-Egenter C (2009) A discussion of different types of glacial refugia used in mountain biogeography and phylogeography. J Biogeogr 36:476–480CrossRefGoogle Scholar
  32. Holderegger R, Buehler D, Gugerli F, Manel S (2010) Landscape genetics of plants. Trends Plant Sci 15:675–683CrossRefPubMedGoogle Scholar
  33. Hubisz MJ, Falush D, Stephens M, Pritchard JK (2009) Inferring weak population structure with the assistance of sample group information. Mol Ecol Resour 9:1322–1332CrossRefPubMedPubMedCentralGoogle Scholar
  34. Jaccard P (1900) Contribution au problème de l’immigration post-glacaire de la flore alpine. Bull Soc Vaud Sc Nat 36:87–130Google Scholar
  35. Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801–1806CrossRefPubMedGoogle Scholar
  36. Janes JK, Miller JM, Dupuis JR, Malenfant RM, Gorrell JC, Cullingham CI, Andrew RL (2017) The K = 2 conundrum. Mol Ecol 26:3594–3602CrossRefPubMedGoogle Scholar
  37. Jiao W-B et al (2017) Improving and correcting the contiguity of long-read genome assemblies of three plant species using optical mapping and chromosome conformation capture data. Genome Res 27.5:778–786CrossRefGoogle Scholar
  38. Kelly MA, Buoncristiani J-F, Schlüchter C (2004) A reconstruction of the last glacial maximum (LGM) ice-surface geometry in the western Swiss Alps and contiguous Alpine regions in Italy and France. Eclogae Geol Helv 97:57–75CrossRefGoogle Scholar
  39. 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 15:825–839CrossRefPubMedGoogle Scholar
  40. Kopelman NM, Mayzel J, Jakobsson M, Rosenberg NA, Mayrose I (2015) Clumpak: a program for identifying clustering modes and packaging population structure inferences across K. Mol Ecol Resour 15:1179–1191CrossRefPubMedPubMedCentralGoogle Scholar
  41. Kropf M, Kadereit JW, Comes HP (2003) Differential cycles of range contraction and expansion in European high mountain plants during the Late Quaternary: insights from Pritzelago alpina (L.) O. Kuntze (Brassicaceae). Mol Ecol 12:931–949CrossRefPubMedGoogle Scholar
  42. Manel S, Poncet B, Legendre P, Gugerli F, Holderegger R (2010) Common factors drive adaptive genetic variation at different spatial scales in Arabis alpina. Mol Ecol 19:3824–3835CrossRefPubMedGoogle Scholar
  43. McNally KL et al. (2009) Genomewide SNP variation reveals relationships among landraces and modern varieties of rice. Proc Natl Acad Sci USA 106:12273–12278CrossRefPubMedPubMedCentralGoogle Scholar
  44. Meirmans PG (2015) Seven common mistakes in population genetics and how to avoid them. Mol Ecol 24:3223–3231CrossRefPubMedGoogle Scholar
  45. Merxmüller H (1952) Untersuchungen zur Sippengliederung und Arealbildung in den Alpen. I. Jb. Ver. Schutze d. Alpenpflanzen u Tiere 17:96–133Google Scholar
  46. Mosher DS, Quignon P, Bustamante CD, Sutter NB, Mellersh CS, Parker HG, Ostrander EA (2007) A mutation in the myostatin gene increases muscle mass and enhances racing performance in heterozygote dogs. PLoS Genet 3:779–786CrossRefGoogle Scholar
  47. Nybom H (2004) Comparison of different nuclear DNA markers for estimating intraspecific genetic diversity in plants. Mol Ecol 13:1143–1155CrossRefPubMedGoogle Scholar
  48. Ozenda P (1985) La végétation de la chaine alpine dans l’espace montagnard européen. Masson, ParisGoogle Scholar
  49. Parisod C (2008) Postglacial recolonisation of plants in the western Alps of Switzerland. Bot Helv 118:1–12CrossRefGoogle Scholar
  50. Parisod C, Besnard G (2007) Glacial in situ survival in the Western Alps and polytopic autopolyploidy in Biscutella laevigata L. (Brassicaceae). Mol Ecol 16:2755–2767CrossRefPubMedGoogle Scholar
  51. 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
  52. Petit RJ et al (2003) Glacial refugia: hotspots but not melting pots of genetic diversity. Science 300:1563–1565CrossRefPubMedGoogle Scholar
  53. Poncet BN et al (2010) Tracking genes of ecological relevance using a genome scan in two independent regional population samples of Arabis alpina. Mol Ecol 19:2896–2907CrossRefPubMedGoogle Scholar
  54. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedPubMedCentralGoogle Scholar
  55. Robin V, Nadeau MJ, Grootes PM, Bork HR, Nelle O (2016) Too early and too northerly: evidence of temperate trees in northern Central Europe during the Younger Dryas. New Phytol 212:259–268CrossRefPubMedGoogle Scholar
  56. Rytz W (1951) Environs de Zermatt et de Saas. Le rôle biogéographique des cols. In: Chouard P, Gauss H, Vischer W (eds) Coupe Botanique des Alpes du Tyrol à la France. Bulletin de la Société Botanique de France, Paris, pp 77–78Google Scholar
  57. Schneeweiss G, Schönswetter P (2010) The wide but disjunct range of the European mountain plant Androsace lactea L. (Primulaceae) reflects Late Pleistocene range fragmentation and post-glacial distributional stasis. J Biogeogr 37:2016–2025Google Scholar
  58. Schönswetter P, Tribsch A, Niklfeld H (2004) Amplified fragment length polymorphism (AFLP) reveals no genetic divergence of the Eastern Alpine endemic Oxytropis campestris subsp. tiroliensis (Fabaceae) from widespread subsp. campestris. Plant Syst Evol 244:245–255CrossRefGoogle Scholar
  59. Schönswetter P, Stehlik I, Holderegger R, Tribsch A (2005) Molecular evidence for glacial refugia of mountain plants in the European Alps. Mol Ecol 14:3547–3555CrossRefPubMedGoogle Scholar
  60. Sillanpää M (2011) Overview of techniques to account for confounding due to population stratification and cryptic relatedness in genomic data association analyses. Heredity 106:511–519CrossRefPubMedGoogle Scholar
  61. Skrede I, Borgen L, Brochmann C (2009) Genetic structuring in three closely related circumpolar plant species: AFLP versus microsatellite markers and high-arctic versus arctic-alpine distributions. Heredity 102:293–302CrossRefPubMedGoogle Scholar
  62. Stehlik I (2003) Resistance or emigration? Response of alpine plants to the ice ages. Taxon 52:499–510CrossRefGoogle Scholar
  63. Stehlik I, Blattner F, Holderegger R, Bachmann K (2002a) Nunatak survival of the high Alpine plant Eritrichium nanum (L.) Gaudin in the central Alps during the ice ages. Mol Ecol 11:2027–2036CrossRefPubMedGoogle Scholar
  64. Stehlik I, Schneller JJ, Bachmann K (2002b) Immigration and in situ glacial survival of the low-alpine Erinus alpinus (Scrophulariaceae). Biol J Linn Soc 77:87–103CrossRefGoogle Scholar
  65. Taberlet P, Fumagalli L, Wust-Saucy AG, Cosson JF (1998) Comparative phylogeography and postglacial colonization routes in Europe. Mol Ecol 7:453–464CrossRefPubMedGoogle Scholar
  66. Taberlet P et al (2012a) Genetic diversity in widespread species is not congruent with species richness in alpine plant communities. Ecol Lett 15:1439–1448CrossRefPubMedGoogle Scholar
  67. Taberlet P et al (2012b) Data from: Genetic diversity in widespread species is not congruent with species richness in alpine plant communities. In: Dryad Data Repository, http://dx.doi.org/10.5061/dryad.s4q6s. Accessed 20 Oct 2016
  68. Tedder A, Ansell S, Lao X, Vogel J, Mable B (2011) Sporophytic self-incompatibility genes and mating system variation in Arabis alpina. Ann Bot 108:699–713CrossRefPubMedPubMedCentralGoogle Scholar
  69. Teulat B et al (2000) An analysis of genetic diversity in coconut (Cocos nucifera) populations from across the geographic range using sequence-tagged microsatellites (SSRs) and AFLPs. Theor Appl Genet 100:764–771CrossRefGoogle Scholar
  70. Thiel-Egenter C et al (2011) Break zones in the distributions of alleles and species in alpine plants. J Biogeogr 38:772–782CrossRefGoogle Scholar
  71. Wang R et al (2009) PEP1 regulates perennial flowering in Arabis alpina. Nature 459:423–427CrossRefPubMedGoogle Scholar
  72. Welten M (1982) Vegetationsgeschichtliche Untersuchungen in den westlichen Schweizer Alpen: Bern-Wallis. Mém Soc Hel Sci Nat 95:12–27Google Scholar
  73. Willing E-M et al (2015) Genome expansion of Arabis alpina linked with retrotransposition and reduced symmetric DNA methylation. Nat Plants 1:14023CrossRefPubMedGoogle Scholar
  74. Wingler A, Juvany M, Cuthbert C, Munné-Bosch S (2014) Adaptation to altitude affects the senescence response to chilling in the perennial plant Arabis alpina. J Exp Bot 66:355–367CrossRefPubMedPubMedCentralGoogle Scholar
  75. Woodhead M, Russell J, Squirrell J, Hollingsworth P, Mackenzie K, Gibby M, Powell W (2005) Comparative analysis of population genetic structure in Athyrium distentifolium (Pteridophyta) using AFLPs and SSRs from anonymous and transcribed gene regions. Mol Ecol 14:1681–1695CrossRefPubMedGoogle Scholar
  76. Zulliger D, Schnyder E, Gugerli F (2013) Are adaptive loci transferable across genomes of related species? Outlier and environmental association analyses in Alpine Brassicaceae species. Mol Ecol 22:1626–1639CrossRefPubMedGoogle Scholar

Copyright information

© Swiss Botanical Society 2017

Authors and Affiliations

  1. 1.WSL Swiss Federal Research InstituteBirmensdorfSwitzerland
  2. 2.Institute of Plant SciencesUniversity of BernBernSwitzerland
  3. 3.Institute of Integrative BiologyETH ZürichZurichSwitzerland

Personalised recommendations