Ice holes microrefugia harbor genetically and functionally distinct populations of Vaccinium vitis-idaea (Ericaceae).
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
11 08 2023
11 08 2023
Historique:
received:
17
02
2023
accepted:
31
07
2023
medline:
14
8
2023
pubmed:
12
8
2023
entrez:
11
8
2023
Statut:
epublish
Résumé
In the mountain terrain, ice holes are little depressions between rock boulders that are characterized by the exit of cold air able to cool down the rock surface even in summer. This cold air creates cold microrefugia in warmer surroundings that preserve plant species probably over thousands of years under extra-zonal climatic conditions. We hypothesized that ice hole populations of the model species Vaccinium vitis-idaea (Ericaceae) show genetic differentiation from nearby zonal subalpine populations, and high functional trait distinctiveness, in agreement with genetic patterns. We genotyped almost 30,000 single nucleotide polymorphisms using restriction site-associated DNA sequencing and measured eight functional traits indicative of individual performance and ecological strategies. Genetic results showed high differentiation among the six populations suggesting isolation. On siliceous bedrock, ice hole individuals exhibited higher levels of admixture than those from subalpine populations which could have experienced more bottlenecks during demographic fluctuations related to glacial cycles. Ice hole and subalpine calcareous populations clearly separated from siliceous populations, indicating a possible effect of bedrock in shaping genetic patterns. Trait analysis reflected the bedrock effect on populations' differentiation. The significant correlation between trait and genetic distances suggests the genetic contribution in shaping intraspecific functional differentiation. In conclusion, extra-zonal populations reveal a prominent genetic and phenotypic differentiation determined by history and ecological contingency. Therefore, microrefugia populations can contribute to the overall variability of the species and lead to intraspecific-driven responses to upcoming environmental changes.
Identifiants
pubmed: 37567871
doi: 10.1038/s41598-023-39772-5
pii: 10.1038/s41598-023-39772-5
pmc: PMC10421893
doi:
Substances chimiques
Ice
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
13055Informations de copyright
© 2023. Springer Nature Limited.
Références
Comes, H. P. & Kadereit, J. W. The effect of quaternary climatic changes on plant distribution and evolution. Trends Plant Sci. 3(11), 432–438 (1998).
doi: 10.1016/S1360-1385(98)01327-2
Schönswetter, P., Stehlik, I., Holderegger, R. & Tribsch, A. Molecular evidence for glacial refugia of mountain plants in the European Alps. Mol. Ecol. 14(11), 3547–3555 (2005).
pubmed: 16156822
doi: 10.1111/j.1365-294X.2005.02683.x
Gentili, R. et al. From cold to warm-stage refugia for boreo-alpine plants in southern European and Mediterranean mountains: The last chance to survive or an opportunity for speciation?. Biodiversity 16(4), 247–261 (2015).
doi: 10.1080/14888386.2015.1116407
Stewart, J. R., Lister, A. M., Barnes, I. & Dalén, L. Refugia revisited: Individualistic responses of species in space and time. Proc. R. Soc. B: Biol. Sci. 277(1682), 661–671 (2010).
doi: 10.1098/rspb.2009.1272
Rull, V. Microrefugia. J. Biogeogr. 36(3), 481–484 (2009).
doi: 10.1111/j.1365-2699.2008.02023.x
IPCC. Climate change 2014 synthesis report. Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change, 1–112 (2014).
Greiser, C., Ehrlén, J., Meineri, E. & Hylander, K. Hiding from the climate: Characterizing microrefugia for boreal forest understory species. Glob. Change Biol. 26(2), 471–483 (2020).
doi: 10.1111/gcb.14874
Hampe, A. & Petit, R. J. Conserving biodiversity under climate change: the rear edge matters. Ecol. Lett. 8(5), 461–467 (2005).
pubmed: 21352449
doi: 10.1111/j.1461-0248.2005.00739.x
Gentili, R. et al. Potential warm-stage microrefugia for alpine plants: Feedback between geomorphological and biological processes. Ecol. Complex. 21, 87–99 (2015).
doi: 10.1016/j.ecocom.2014.11.006
Mosblech, N. A. S., Bush, M. B. & Van Woesik, R. On metapopulations and microrefugia: Palaeoecological insights. J. Biogeogr. 38(3), 419–429 (2011).
doi: 10.1111/j.1365-2699.2010.02436.x
Woolbright, S. A., Whitham, T. G., Gehring, C. A., Allan, G. J. & Bailey, J. K. Climate relicts and their associated communities as natural ecology and evolution laboratories. Trends Ecol. Evol. 29(7), 406–416 (2014).
pubmed: 24932850
doi: 10.1016/j.tree.2014.05.003
Nicotra, A. B. et al. Plant phenotypic plasticity in a changing climate. Trends Plant Sci. 15(12), 684–692 (2010).
pubmed: 20970368
doi: 10.1016/j.tplants.2010.09.008
Violle, C. et al. Let the concept of trait be functional!. Oikos 116, 882–892 (2007).
doi: 10.1111/j.0030-1299.2007.15559.x
Dobrowski, S. Z. A climatic basis for microrefugia: The influence of terrain on climate. Glob. Change Biol. 17(2), 1022–1035 (2011).
doi: 10.1111/j.1365-2486.2010.02263.x
Shimokawabe, A., Yamaura, Y., Akasaka, T. & Sato, T. The distribution of cool spots as microrefugia in a mountainous area. PLoS ONE 10(8), 1–12 (2015).
doi: 10.1371/journal.pone.0135732
Shimokawabe, A., Yamaura, Y., Sueyoshi, M., Kudo, G. & Nakamura, F. Genetic structure of Vaccinium vitis-idaea in lowland cool spot and alpine populations: Microrefugia of alpine plants in the midlatitudes. Alp. Bot. 126(2), 143–151 (2016).
doi: 10.1007/s00035-016-0169-3
SProsser, F. Le “buche del vento” di Cornacalda (Rovereto, Trentino meridionale): Aspetti floristici ed ecologici. Annale Museo Civico Di Rovereto 7, 157–176 (1992).
Burga, C. A., Voser, N. & Grebner, D. Die Eppaner Eislöcher - eine Kälteinsel im Weingebiet Südtirols. Gredleriana 5, 9–38 (2005).
Gafta, D. Ecocoenotic distinctiveness of an extrazonal ice hole biotope in the valley of Cembra (southern central Alps, Trentino). Polish Botanical Studies 22, 195–206 (2006).
Hampe, A. & Jump, A. S. Climate relicts: Past, present, future. Annu. Rev. Ecol. Evol. Syst. 42(1), 313–333 (2011).
doi: 10.1146/annurev-ecolsys-102710-145015
Ikeda, H. et al. Persistent history of the bird-dispersed arctic-alpine plant Vaccinium vitis-idaea L. (Ericaceae) in Japan. J. Plant Res. 128, 437–444 (2015).
pubmed: 25773306
doi: 10.1007/s10265-015-0709-8
Excoffier, L., Foll, M. & Petit, R. J. Genetic consequences of range expansions. Annu. Rev. Ecol. Evol. Syst. 40(1), 481–501 (2009).
doi: 10.1146/annurev.ecolsys.39.110707.173414
Hewitt, G. M. Some genetic consequences of ice ages, and their role in divergence and speciation. Biol. J. Linnean Soc. 58(3), 247–276 (1996).
doi: 10.1006/bijl.1996.0035
Petit, R. J. et al. Chloroplast DNA variation in European white oaks. Phylogeography and patterns of diversity based on data from over 2600 populations. For. Ecol. Manag. 156(1–3), 5–26 (2002).
doi: 10.1016/S0378-1127(01)00645-4
Tonin, R., Gerdol, R. & Wellstein, C. Intraspecific functional differences of subalpine plant species growing in low-altitude microrefugia and high-altitude habitats. Plant Ecol. 221, 155–166 (2020).
doi: 10.1007/s11258-020-01001-8
Westergaard, K. B. et al. Population genomic evidence for plant glacial survival in Scandinavia. Mol. Ecol. 28(4), 818–832 (2018).
doi: 10.1111/mec.14994
Mee, J. A. & Moore, J.-S. The ecological and evolutionary implications of microrefugia. J. Biogeogr. 41, 837–841 (2014).
doi: 10.1111/jbi.12254
Reichel, K., Masson, J., Malrieu, F., Arnaud-Haond, S. & Stoeckel, S. Rare sex or out of reach equilibrium? The dynamics of F IS in partially clonal organisms. BMC Genet. 17, 76 (2016).
pubmed: 27286682
pmcid: 4902967
doi: 10.1186/s12863-016-0388-z
Stoeckel, S. & Masson, J. The exact distributions of F IS under partial asexuality in small finite populations with mutation. PLoS ONE 9(1), 1–15 (2014).
doi: 10.1371/journal.pone.0085228
Persson, H. A. & Gustavsson, B. A. The extent of clonality and genetic diversity in lingonberry (Vaccinium vitis-idaea L.) revealed by RAPDs and leaf-shape. Mol. Ecol. 10, 1385–1397 (2001).
pubmed: 11412362
doi: 10.1046/j.1365-294X.2001.01280.x
Wakui, A. & Kudo, G. Ecotypic differentiation of a circumpolar Arctic-alpine species at mid-latitudes: variations in the ploidy level and reproductive system of Vaccinium vitis-idaea. AoB PLANTS 13(3), 1–13 (2021).
doi: 10.1093/aobpla/plab015
Körner, C. Alpine Plant Life 2nd edn. (Springer, 2003).
doi: 10.1007/978-3-642-18970-8
Alvarez, N. et al. History or ecology? Substrate type as a major driver of spatial genetic structure in Alpine plants. Ecol. Lett. 12, 632–640 (2009).
pubmed: 19392716
doi: 10.1111/j.1461-0248.2009.01312.x
Hulshof, C. M. et al. Intra-specific and inter-specific variation in specific leaf area reveal the importance of abiotic and biotic drivers of species diversity across elevation and latitude. J. Veg. Sci. 24(5), 921–931 (2013).
doi: 10.1111/jvs.12041
Poorter, H. & Remkes, C. Leaf area ratio and net assimilation rate of 24 wild species differing in relative growth rate. Oecologia 83(4), 553–559 (1990).
pubmed: 28313192
doi: 10.1007/BF00317209
Albert, C. H. et al. Intraspecific functional variability: Extent, structure and sources of variation. J. Ecol. 98(3), 604–613 (2010).
doi: 10.1111/j.1365-2745.2010.01651.x
Pierce, S. et al. A global method for calculating plant CSR ecological strategies applied across biomes world-wide. Funct. Ecol. 31(2), 444–457 (2017).
doi: 10.1111/1365-2435.12722
Wellstein, C. et al. Intraspecific phenotypic variability of plant functional traits in contrasting mountain grasslands habitats. Biodivers. Conserv. 22(10), 2353–2374 (2013).
doi: 10.1007/s10531-013-0484-6
Dunbar-Co, S., Sporck, M. J. & Sack, L. Leaf Trait Diversification and Design in Seven Rare Taxa of the Hawaiian Plantago Radiation. Int. J. Plant Sci. 170(1), 61–75 (2009).
doi: 10.1086/593111
Gupta, B. Correlation of tissues in leaves 2 Absolute stomatal number. Ann. Botany 25(1), 71–77 (1961).
doi: 10.1093/oxfordjournals.aob.a083734
Bucher, S. F. et al. Stomatal traits relate to habitat preferences of herbaceous species in a temperate climate. Flora 229, 107–115 (2017).
doi: 10.1016/j.flora.2017.02.011
Herrera, C. M. & Bazaga, P. Quantifying the genetic component of phenotypic variation in unpedigreed wild plants: Tailoring genomic scan for within-population use. Mol. Ecol. 18(12), 2602–2614 (2009).
pubmed: 19457184
doi: 10.1111/j.1365-294X.2009.04229.x
Pedrotti, F. Le buche di ghiaccio di Appiano. In Guida all’escursione della Società Botanica Italiana in Val D’Adige e nel Parco Nazionale dello Stelvio (pp. 31–37) (1980).
Pfaff, G. L. “Buche di ghiaccio” di Lases e la loro flora. St. Trent. Sc. Nat. 14, 177–187 (1933).
Pfaff, W. Die Eislöcher in Ueberetsch. Ihre Vegetationsverhältnisse und ihre Flora. In Schlern-Schriften (ed. Klenelsberg, R. V.) (Universitäts-Verlag Wagner, 1933).
Hijmans, R. J., Cameron, S. E., Parra, J. L., Jones, P. G. & Jarvis, A. Very high resolution interpolated climate surfaces for global land areas. Int. J. Climatol. 25(15), 1965–1978 (2005).
doi: 10.1002/joc.1276
Klimešová, J., Danihelka, J., Chrtek, J., de Bello, F. & Herben, T. CLO-PLA: A database of clonal and bud-bank traits of the Central European flora. Ecology 98(4), 1179 (2017).
pubmed: 28122127
doi: 10.1002/ecy.1745
Rachmayanti, Y., Leinemann, L., Gailing, O. & Finkeldey, R. Extraction, amplification and characterization of wood DNA from dipterocarpaceae. Plant Mol. Biol. Report. 24, 45–55 (2006).
doi: 10.1007/BF02914045
Baird, N. A. et al. Rapid SNP discovery and genetic mapping using sequenced RAD markers. PLoS ONE 3(10), 1–7 (2008).
doi: 10.1371/journal.pone.0003376
Paun, O. et al. Processes driving the adaptive radiation of a tropical tree (Diospyros, Ebenaceae) in New Caledonia, a biodiversity hotspot. Syst. Biol. 65(2), 212–227 (2016).
pubmed: 26430059
doi: 10.1093/sysbio/syv076
Catchen, J., Hohenlohe, P. A., Bassham, S., Amores, A. & Cresko, W. A. Stacks: An analysis tool set for population genomics. Mol. Ecol. 22(11), 3124–3140 (2013).
pubmed: 23701397
pmcid: 3936987
doi: 10.1111/mec.12354
Malinsky, M., Trucchi, E., Lawson, D. J. & Falush, D. RADpainter and fineRADstructure: Population inference from RADseq Data. Mol. Biol. Evol. 35(5), 1284–1290 (2018).
pubmed: 29474601
pmcid: 5913677
doi: 10.1093/molbev/msy023
Pérez-Harguindeguy, N. et al. New handbook for standardised measurement of plant functional traits worldwide. Aust. J. Bot. 61(3), 167–234 (2013).
doi: 10.1071/BT12225
Hilu, K. W. & Randall, J. L. Convenient method for studying grass leaf epidermis. Taxon 33(3), 413–415 (1984).
doi: 10.1002/j.1996-8175.1984.tb03896.x
Wang, R. et al. Elevation-related variation in leaf stomatal traits as a function of plant functional type: Evidence from Changbai. PLoS ONE 9(12), 1–15 (2014).
doi: 10.1371/journal.pone.0115395
Jombart, T., Lyon, D. & Biome, L. D. adegenet: A R package for the multivariate analysis of genetic markers. Bioinformatics 24(11), 1403–1405 (2008).
pubmed: 18397895
doi: 10.1093/bioinformatics/btn129
Rousset, F., Lopez, L., & Belkhir, K. Package ‘genepop’ 16. http://kimura.univ-montp2.fr/~rousset/Genepop.htm (2020).
Danecek, P. et al. The variant call format and VCFtools. Bioinformatics 27(15), 2156–2158 (2011).
pubmed: 21653522
pmcid: 3137218
doi: 10.1093/bioinformatics/btr330
Pritchard, J. K., Stephens, M. & Donnelly, P. Inference of population structure using multilocus genotype data. Genetics 155, 945–959 (2000).
pubmed: 10835412
pmcid: 1461096
doi: 10.1093/genetics/155.2.945
Earl, D. A., Cruz, S. & VonHoldt, B. M. STRUCTURE HARVESTER: A website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv. Genet. Resour. 4, 359–361 (2012).
doi: 10.1007/s12686-011-9548-7
Francis, R. M. An R package and web app to analyse and visualize population structure. POPHELPER Mol. Ecol. Resour. 17, 27–32 (2017).
pubmed: 26850166
doi: 10.1111/1755-0998.12509
Lischer, H. E. L. & Excoffier, L. PGDSpider: An automated data conversion tool for connecting population genetics and genomics programs. Bioinformatics 28(2), 298–299 (2012).
pubmed: 22110245
doi: 10.1093/bioinformatics/btr642
Excoffier, L. & Lischer, H. E. Arlequin suite ver 3.5: A new series of programs to perform population genetics analyses under Linux and Windows. Mol. Ecol. Resour. 10, 564–567 (2010).
pubmed: 21565059
doi: 10.1111/j.1755-0998.2010.02847.x
Kamvar, Z. N. et al. Package ‘poppr’ - Genetic analysis of populations with mixed reproduction. (2018).
Dray, S. & Dufour, A.-B. The ade4 package: implementing the duality diagram for ecologists. J. Stat. Softw. 22(4), 1–20 (2007).
doi: 10.18637/jss.v022.i04
Pelé, J., Bécu, J., Abdi, H. & Chabbert, M. Bios2mds: An R package for comparing orthologous protein families by metric multidimensional scaling. BMC Bioinf. 13, 1–7 (2012).
doi: 10.1186/1471-2105-13-133
Karbstein, K., Prinz, K., Hellwig, F. & Römermann, C. Plant intraspecific functional trait variation is related to within-habitat heterogeneity and genetic diversity in Trifolium montanum L. Ecol. Evol. 10, 5015–5033 (2020).
pubmed: 32551078
pmcid: 7297743
doi: 10.1002/ece3.6255