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.
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References
Alvarez N et al (2009) History or ecology? Substrate type as a major driver of patial genetic structure in Alpine plants. Ecol Lett 12:632–640
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 17:2245–2257
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 108:241–252
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 99:133–142
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 16:2517–2524
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 13:3261–3273
Bovet L, Kammer P, Meylan-Bettex M, Guadagnuolo R, Matera V (2006) Cadmium accumulation capacities of Arabis alpina under environmental conditions. Environ Exp Bot 57:80–88
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 130–173
Brochmann C, Gabrielsen TM, Nordal I, Landvik JY, Elven R (2003) Glacial survival or tabula rasa? The history of North Atlantic biota revisited. Taxon 52:417–450
Brockmann-Jerosch H, Brockmann-Jerosch MC (1926) Die Geschichte der Schweizerischen Alpenflora. In: Schröter C (ed) Das Pflanzenleben der Alpen. Raustein, Zürich, pp 1110–1215
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–e105
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 109:1359–1367
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 27:285–300
Christ H (1907) La flore de la Suisse. Georg & Cie, Bâle-Genève-Lyon
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 105:41–70
DeWoody J, Nason JD, Hipkins VD (2006) Mitigating scoring errors in microsatellite data from wild populations. Mol Ecol Notes 6:951–957
Duforet-Frebourg N, Blum MG (2014) Non stationary patterns of isolation-by-distance: infering measures of local genetic differentiation with Bayesian kriging. Evol 68:1110–1123
Earl DA, von Holdt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361
Ehrenreich IM, Hanzawa Y, Chou L, Roe JL, Kover PX, Purugganan MD (2009) Candidate gene association mapping of Arabidopsis flowering time. Genetics 183:325–335
Ehrich D et al (2007) Genetic consequences of Pleistocene range shifts: contrast between the Arctic, the Alps and the East African mountains. Mol Ecol 16:2542–2559
Estoup A, Jarne P, Cornuet JM (2002) Homoplasy and mutation model at microsatellite loci and their consequences for population genetics analysis. Mol Ecol 11:1591–1604
Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620
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 176:1635–1651
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 92:508–518
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 10:259–281
Guyot H (1934) Phytogéographie comparée du Valais et de la vallée d’Aoste. Bull Murith Soc Valais Sci Nat 52:16–35
Hardy OJ, Vekemans X (2002) SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Resour 2:618–620
Hewitt GM (1996) Some genetic consequences of ice ages, and their role in divergence and speciation. Biol J Linn Soc 58:247–276
Hewitt GM (1999) Post-glacial re-colonization of European biota. Biol J Linn Soc 68:87–112
Hewitt G (2004) Genetic consequences of climatic oscillations in the Quaternary. Phil Trans R Soc B 359:183–195
Holderegger R, Thiel-Egenter C (2009) A discussion of different types of glacial refugia used in mountain biogeography and phylogeography. J Biogeogr 36:476–480
Holderegger R, Buehler D, Gugerli F, Manel S (2010) Landscape genetics of plants. Trends Plant Sci 15:675–683
Hubisz MJ, Falush D, Stephens M, Pritchard JK (2009) Inferring weak population structure with the assistance of sample group information. Mol Ecol Resour 9:1322–1332
Jaccard P (1900) Contribution au problème de l’immigration post-glacaire de la flore alpine. Bull Soc Vaud Sc Nat 36:87–130
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 23:1801–1806
Janes JK, Miller JM, Dupuis JR, Malenfant RM, Gorrell JC, Cullingham CI, Andrew RL (2017) The K = 2 conundrum. Mol Ecol 26:3594–3602
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 27.5:778–786
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 97:57–75
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 15:825–839
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 15:1179–1191
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 12:931–949
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 19:3824–3835
McNally KL et al. (2009) Genomewide SNP variation reveals relationships among landraces and modern varieties of rice. Proc Natl Acad Sci USA 106:12273–12278
Meirmans PG (2015) Seven common mistakes in population genetics and how to avoid them. Mol Ecol 24:3223–3231
Merxmüller H (1952) Untersuchungen zur Sippengliederung und Arealbildung in den Alpen. I. Jb. Ver. Schutze d. Alpenpflanzen u Tiere 17:96–133
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 3:779–786
Nybom H (2004) Comparison of different nuclear DNA markers for estimating intraspecific genetic diversity in plants. Mol Ecol 13:1143–1155
Ozenda P (1985) La végétation de la chaine alpine dans l’espace montagnard européen. Masson, Paris
Parisod C (2008) Postglacial recolonisation of plants in the western Alps of Switzerland. Bot Helv 118:1–12
Parisod C, Besnard G (2007) Glacial in situ survival in the Western Alps and polytopic autopolyploidy in Biscutella laevigata L. (Brassicaceae). Mol Ecol 16:2755–2767
Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295
Petit RJ et al (2003) Glacial refugia: hotspots but not melting pots of genetic diversity. Science 300:1563–1565
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 19:2896–2907
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
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 212:259–268
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 77–78
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 37:2016–2025
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 244:245–255
Schönswetter P, Stehlik I, Holderegger R, Tribsch A (2005) Molecular evidence for glacial refugia of mountain plants in the European Alps. Mol Ecol 14:3547–3555
Sillanpää M (2011) Overview of techniques to account for confounding due to population stratification and cryptic relatedness in genomic data association analyses. Heredity 106:511–519
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 102:293–302
Stehlik I (2003) Resistance or emigration? Response of alpine plants to the ice ages. Taxon 52:499–510
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 11:2027–2036
Stehlik I, Schneller JJ, Bachmann K (2002b) Immigration and in situ glacial survival of the low-alpine Erinus alpinus (Scrophulariaceae). Biol J Linn Soc 77:87–103
Taberlet P, Fumagalli L, Wust-Saucy AG, Cosson JF (1998) Comparative phylogeography and postglacial colonization routes in Europe. Mol Ecol 7:453–464
Taberlet P et al (2012a) Genetic diversity in widespread species is not congruent with species richness in alpine plant communities. Ecol Lett 15:1439–1448
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
Tedder A, Ansell S, Lao X, Vogel J, Mable B (2011) Sporophytic self-incompatibility genes and mating system variation in Arabis alpina. Ann Bot 108:699–713
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 100:764–771
Thiel-Egenter C et al (2011) Break zones in the distributions of alleles and species in alpine plants. J Biogeogr 38:772–782
Wang R et al (2009) PEP1 regulates perennial flowering in Arabis alpina. Nature 459:423–427
Welten M (1982) Vegetationsgeschichtliche Untersuchungen in den westlichen Schweizer Alpen: Bern-Wallis. Mém Soc Hel Sci Nat 95:12–27
Willing E-M et al (2015) Genome expansion of Arabis alpina linked with retrotransposition and reduced symmetric DNA methylation. Nat Plants 1:14023
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 66:355–367
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 14:1681–1695
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 22:1626–1639
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).
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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.
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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)
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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)
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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)
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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)
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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)
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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)
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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)
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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)
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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)
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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)
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Rogivue, A., Graf, R., Parisod, C. et al. The phylogeographic structure of Arabis alpina in the Alps shows consistent patterns across different types of molecular markers and geographic scales. Alp Botany 128, 35–45 (2018). https://doi.org/10.1007/s00035-017-0196-8
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DOI: https://doi.org/10.1007/s00035-017-0196-8