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Genetic structure of Vaccinium vitis-idaea in lowland cool spot and alpine populations: microrefugia of alpine plants in the midlatitudes

Alpine Botany volume 126, pages 143–151 (2016)Cite this article

Abstract

Local cool spots (wind-holes) in lowland areas of midlatitudes may act as microrefugia for cold-adapted species outside of their typical alpine habitats. We examined the genetic structure of Vaccinium vitis-idaea, a common alpine species in Japan, in eight lowland wind-hole and five surrounding alpine populations. We collected leaf samples and genotyped seven microsatellite loci. Clonal patches (genets) were common in almost all populations. An analysis of annual shoot growth suggested that individuals in the wind-hole populations were long-lived (>500 years old). Genetic diversity (allelic richness) and differentiation (F ST) of the wind-hole populations were lower and higher than those of the alpine populations, respectively. No significant isolation-by-distance trend in the genetic structure was detected for the wind-hole or alpine populations. All wind-hole populations had negative inbreeding coefficients (F IS), suggesting no tendency toward homozygosity due to inbreeding, regardless of the small populations geographically isolated from the large alpine populations. Therefore, wind-holes may harbor genetically isolated but stable populations due to clonal growth, limited gene flow, and abortion of selfed seeds by early acting inbreeding depression. Analysis of molecular variance demonstrated that genetic variations among and within populations contributed more to regional genetic diversity than those between wind-hole and alpine populations, suggesting that the wind-hole and alpine populations are important for maintaining the genetic diversity of midlatitude V. vitis-idaea populations. On the other hand, Bayesian clustering showed that some wind-hole populations geographically close to the alpine populations had mixed genetic compositions of the alpine and wind-hole populations.

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References

  • Billington HL (1991) Effect of population size on genetic variation in a dioecious conifer. Conserv Biol 5:115–119

    Article  Google Scholar 

  • Boches PS, Bassil NV, Rowland LJ (2005) Microsatellite markers for Vaccinium from EST and genomic libraries. Mol Ecol Notes 5:657–660

    Article  CAS  Google Scholar 

  • Byers DL, Meagher TR (1992) Mate availability in small populations of plant species with homomorphic sporophytic self-incompatibility. Heredity 68:353–359

    Article  Google Scholar 

  • Dobrowski SZ (2011) A climatic basis for microrefugia: the influence of terrain on climate. Global Change Biol 17:1022–1035

    Article  Google Scholar 

  • Earl DA, vonHoldt BM (2012) Structure Harvester: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genetics Resour 4:359–361

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Forister ML et al (2010) Compounded effects of climate change and habitat alteration shift patterns of butterfly diversity. Proc Natl Acad Sci USA 107:2088–2092

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Garkava-Gustavsson L, Persson HA, Nybom H, Rumpunen K, Gustavsson BA, Bartish IV (2005) RAPD-based analysis of genetic diversity and selection of lingonberry (Vaccinium vitis-idaea L.) material for ex situ conservation. Genet Resour Crop Evol 52:723–735

    Article  CAS  Google Scholar 

  • Gentili R, Baroni C, Caccianiga M, Armiraglio S, Ghiani A, Citterio S (2015) Potential warm-stage microrefugia for alpine plants: Feedback between geomorphological and biological processes. Ecol Complex 21:87–99

    Article  Google Scholar 

  • Guillaume P, Jacquemart A-L (1999) Early-inbreeding depression in Vaccinium myrtillus and V. vitis-idaea. Protoplasma 208:107–114

    Article  Google Scholar 

  • Hampe A, Jump AS (2011) Climate relicts: past, present, future. Annu Rev Ecol Evol Syst 42:313–333

    Article  Google Scholar 

  • Hannah L, Flint L, Syphard AD, Moritz MA, Buckley LB, McCullough IM (2014) Fine-grain modeling of species’ response to climate change: holdouts, stepping-stones, and microrefugia. Trends Ecol Evol 29:390–397

    Article  PubMed  Google Scholar 

  • Hjort J, Gordon JE, Gray M, Hunter ML (2015) Why geodiversity matters in valuing nature’s stage. Conserv Biol 29:630–639

    Article  PubMed  Google Scholar 

  • Hutchison DW, Templeton AR (1999) Correlation of pairwise genetic and geographic distance measures: inferring the relative influences of gene flow and drift on the distribution of genetic variability. Evolution 53:1898–1914

    Article  Google Scholar 

  • Hylander K, Ehrlén J, Luoto M, Meineri E (2015) Microrefugia: not for everyone. Ambio 44:60–68

    Article  PubMed Central  Google Scholar 

  • Ikeda H et al (2015) Persistent history of the bird-dispersed arctic–alpine plant Vaccinium vitis-idaea L. (Ericaceae) in Japan. J Plant Res 128:437–444

    Article  PubMed  Google Scholar 

  • Ingvarsson PK (2001) Restoration of genetic variation lost—the genetic rescue hypothesis. Trends Ecol Evol 16:62–63

    Article  PubMed  Google Scholar 

  • Iwatsuki K, Yamazaki T, Boufford DE, Ohba H (1993) Flora of Japan. Volume. IIIa. Angiospermae Dicotyledoneae Sympetalae(a). Kodansya, Tokyo

  • Kalinowski ST (2004) Counting alleles with rarefaction: private alleles and hierarchical sampling designs. Conserv Genet 5:539–543

    Article  CAS  Google Scholar 

  • Kalinowski ST (2005) hp-rare 1.0: a computer program for performing rarefaction on measures of allelic richness. Mol Ecol Notes 5:187–189

    Article  CAS  Google Scholar 

  • Kameyama Y, Kasagi T, Kudo G (2008) A hybrid zone dominated by fertile F1s of two alpine shrub species, Phyllodoce caerulea and Phyllodoce aleutica, along a snowmelt gradient. J Evol Biol 21:588–597

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lande R (1988) Genetics and demography in biological conservation. Science 241:1455–1460

    Article  CAS  PubMed  Google Scholar 

  • Lenoir J, Gegout JC, Marquet PA, de Ruffray P, Brisse H (2008) A significant upward shift in plant species optimum elevation during the 20th century. Science 320:1768–1771

    Article  CAS  PubMed  Google Scholar 

  • Lindenmayer DB, Franklin JF (2002) Conserving forest biodiversity: a comprehensive multiscaled approach. Island Press, Washington, DC

    Google Scholar 

  • Marko PB, Hart MW (2011) The complex analytical landscape of gene flow inference. Trends Ecol Evol 26:448–456

    Article  PubMed  Google Scholar 

  • McLachlan JS, Clark JS, Manos PS (2005) Molecular indicators of tree migration capacity under rapid climate change. Ecology 86:2088–2098

    Article  Google Scholar 

  • Mee JA, Moore J-S (2014) The ecological and evolutionary implications of microrefugia. J Biogeogr 41:837–841

    Article  Google Scholar 

  • Mosblech NAS, Bush MB, van Woesik R (2011) On metapopulations and microrefugia: palaeoecological insights. J Biogeogr 38:419–429

    Article  Google Scholar 

  • Parducci L et al (2012) Glacial survival of boreal trees in northern Scandinavia. Science 335:1083–1086

    Article  CAS  PubMed  Google Scholar 

  • Peakall ROD, Smouse PE (2006) Genalex 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295

    Article  Google Scholar 

  • Persson HA, Gustavsson BA (2001) The extent of clonality and genetic diversity in lingonberry (Vaccinium vitis-idaea L.) revealed by RAPDs and leaf-shape analysis. Mol Ecol 10:1385–1397

    Article  CAS  PubMed  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    CAS  PubMed  PubMed Central  Google Scholar 

  • Reed DH, Frankham R (2003) Correlation between fitness and genetic diversity. Conserv Biol 17:230–237

    Article  Google Scholar 

  • Ritchie JC (1955) Vaccinium vitis-idaea L. J Ecol 43:701–708

    Article  Google Scholar 

  • Rousset F (2008) Genepop’007: a complete re-implementation of the genepop software for Windows and Linux. Mol Ecol Resour 8:103–106

    Article  PubMed  Google Scholar 

  • Rull V (2009) Microrefugia. J Biogeogr 36:481–484

    Article  Google Scholar 

  • Růžička V (1999) The freezing scree slopes and their arachnofauna. Decheniana-Beihefte 37:141–147

    Google Scholar 

  • Růžička V, Zacharda M, Šmilauer P, Kučera T (2015) Can paleorefugia of cold-adapted species in talus slopes resist global warming? Boreal Environ Res 20:403–412

    Google Scholar 

  • Sato K (1995) An outline of the cool-spots site vegetation of Hokkaido, Japan. Bull Higashi Taisetsu Museum Nat Hist 17:107–115

    Google Scholar 

  • Sato K, Kudo G, Uemura S (1993) Cool-spots site vegetation in Izariiri-Heide, northern Japan. Jpn J Ecol 43:91–98

    Google Scholar 

  • Shiboi T (1975) Supplementally report on the periglacial phenomena observed in Kitami District. Mem Kitami Inst Techn 7:163–194

    Google Scholar 

  • Shimizu C (2004) An information on the cool air blow holes (wind-holes) including the ice caves in Japan: references to the surrounding landforms and the existence of sporadic perm afrost. Komazawa Geogr 40:121–148

    Google Scholar 

  • Shimokawabe A, Yamaura Y, Akasaka T, Sato T, Shida Y, Yamanaka S, Nakamura F (2015) The distribution of cool spots as microrefugia in a mountainous area. PLoS One 10:e0135732

    Article  PubMed  PubMed Central  Google Scholar 

  • Stewart JR, Lister AM (2001) Cryptic northern refugia and the origins of the modern biota. Trends Ecol Evol 16:608–613

    Article  Google Scholar 

  • Thuiller W (2007) Climate change and the ecologist. Nature 448:550–552

    Article  CAS  PubMed  Google Scholar 

  • Thuiller W, Lavorel S, Araujo MB, Sykes MT, Prentice IC (2005) Climate change threats to plant diversity in Europe. Proc Natl Acad Sci USA 102:8245–8250

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Umezawa S (2007) Wild flowers of Hokkaido, New edn. Hokkaido University Press, Sapporo

    Google Scholar 

  • Walther G-R, Beißner S, Burga CA (2005) Trends in the upward shift of alpine plants. J Veg Sci 16:541–548

    Article  Google Scholar 

  • Wright S (1943) Isolation by distance. Genetics 28:114–138

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wright S (1965) The interpretation of population structure by F-statistics with special regard to systems of mating. Evolution 19:395–420

    Article  Google Scholar 

Download references

Acknowledgments

We thank the members of the Department of Forest Science and the Forest Ecosystem Management Group of Hokkaido University for their field assistance and helpful discussions during this study. We are also grateful to A. Hirao for technical comments on this study. The manuscript was greatly improved by the comments from J. Stöcklin and two anonymous reviewers. AS was supported by a Sasakawa Scientific Research Grant from the Japan Science Society (no. 26-542). AS, YY, MS, and FN were supported by the Japan Society for the Promotion of Science (JSPS) KAKENHI Grant no. 23248021, and YY was supported by JSPS KAKENHI Grant no. 20580947.

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Authors and Affiliations

  1. Graduate School of Agriculture, Hokkaido University, Sapporo, Japan

    Ayuma Shimokawabe, Yuichi Yamaura, Masanao Sueyoshi & Futoshi Nakamura

  2. Department of Forest Vegetation, Forestry and Forest Products Research Institute, Tsukuba, Ibaraki, Japan

    Yuichi Yamaura

  3. Aqua Restoration Research Center, Public Works Research Institute, Kakamigahara, Gifu, Japan

    Masanao Sueyoshi

  4. Faculty of Environmental Earth Science, Hokkaido University, Sapporo, Hokkaido, Japan

    Gaku Kudo

Authors
  1. Ayuma Shimokawabe
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  2. Yuichi Yamaura
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  3. Masanao Sueyoshi
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  4. Gaku Kudo
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  5. Futoshi Nakamura
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Correspondence to Yuichi Yamaura.

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Shimokawabe, A., Yamaura, Y., Sueyoshi, M. et al. Genetic structure of Vaccinium vitis-idaea in lowland cool spot and alpine populations: microrefugia of alpine plants in the midlatitudes. Alp Botany 126, 143–151 (2016). https://doi.org/10.1007/s00035-016-0169-3

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