Skip to main content

Advertisement

Log in

Nuclear microsatellite markers reveal the low genetic structure of Pinus mugo Turra (dwarf mountain pine) populations in Europe

  • Original Article
  • Published:
Plant Systematics and Evolution Aims and scope Submit manuscript

Abstract

Twenty-one populations (555 individuals) covering the entire native range of Pinus mugo Turra (dwarf mountain pine) were investigated for genetic variation scored at 13 nuclear microsatellite markers (nSSRs). The main objective of the present study was to determine the genetic structure across the present distribution of the species and locate populations of different genetic compositions. Most of the genetic variation was observed within the populations (95%). The assignment of populations based on Bayesian clustering methods revealed that the Sudeten populations of P. mugo form a separate genetic cluster. These stands have likely been established through the founder effects of Alpine migrants. The distribution and level of SSR polymorphisms, along with no evidence of isolation by distance or phylogeographic structure, indicate that the present populations of P. mugo have diverged relatively recently and originate from a larger glacial distribution of the species. One peripheral stand from Italy had the lowest values of most calculated genetic variation indices. This stand could therefore be more susceptible to genetic drift and a negative impact of predicted environmental changes. We discuss our findings with respect to previously published results on the genetic and morphological variation of P. mugo and with consideration for the conservation genetics of the species.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

(modified after Critchfield and Little (1971))

Fig. 2

Similar content being viewed by others

References

  • Afzal-Rafii Z, Dodd RS (2007) Chloroplast DNA supports a hypothesis of glacial refugia over postglacial recolonization in disjunct populations of black pine (Pinus nigra) in Western Europe. Molec Ecol 16:723–736. doi:10.1111/j.1365-294X.2006.03183.x

    Article  CAS  Google Scholar 

  • Boratyńska K, Boratyński A (2007) Taxonomic differences among closely related pines Pinus sylvestris, P. mugo, P. uncinata, P. rotundata and P. uliginosa as revealed in needle sclerenchyma cells. Flora 202:555–569. doi:10.1016/j.flora.2006.11.004

    Article  Google Scholar 

  • Boratyńska K, Muchewicz E, Drojma M (2004) Pinus mugo Turra geographic differentiation based on needle characters. Dendrobiology 51:9–17

    Google Scholar 

  • Boratyńska K, Dzialuk A, Lewandowski A, Marcysiak K, Jasińska AK, Sobierajska K, Tomaszewski D, Burczyk J, Boratyński A (2014) Geographic distribution of quantitative traits variation and genetic variability in natural populations of Pinus mugo in Central Europe. Dendrobiology 72:65–84. doi:10.12657/denbio.072.006

    Article  Google Scholar 

  • Boratyńska K, Jasińska AK, Boratyński A (2015) Taxonomic and geographic differentiation of Pinus mugo complex on the needle characteristics. Syst Biodivers 13:581–595. doi:10.1080/14772000.2015.1058300

    Article  Google Scholar 

  • Chapuis MP, Estoup A (2007) Microsatellite null alleles and estimation of population differentiation. Molec Biol Evol 24:621–631. doi:10.1093/molbev/msl191

    Article  CAS  PubMed  Google Scholar 

  • Chapuis MP, Lecoq M, Michalakis Y, Loiseau AG, Sword G, Piry S (2008) Do outbreaks affect genetic population structure? A worldwide survey in Locusta migratoria, a pest plagued by microsatellite null alleles. Molec Ecol 17:3640–3653. doi:10.1111/j.1365-294X.2008.03869.x

    Article  Google Scholar 

  • Chybicki I (2015) INEST 2.0. Available at: http://www.ukw.edu.pl/pracownicy/strona/igor_chybicki/software_ukw/

  • Cornuet J-M, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014

    CAS  PubMed  PubMed Central  Google Scholar 

  • Critchfield WB, Little EL (1971) Geographic distribution of the pines of the world. U.S. Department of Agriculture, Washington

    Google Scholar 

  • Di Rienzo AA, Peterson C, Garza JC, Valdes AM, Slatkin M, Freime RB (1994) Mutational processes of simple-sequence repeat loci in human populations. Proc Natl Acad Sci USA 91:3166–3170

    Article  PubMed  PubMed Central  Google Scholar 

  • Dumolin S, Demesure B, Petit RJ (1995) Inheritance of chloroplast and mitochondrial genomes in pedunculate oak investigated with an efficient PCR method. Theor Appl Genet 91:1253–1256. doi:10.1007/BF00220937

    Article  CAS  PubMed  Google Scholar 

  • Dzialuk A, Boratyński A, Boratyńska K, Burczyk J (2012) Geographic patterns of genetic diversity of Pinus mugo (Pinaceae) in Central European mountains. Dendrobiology 68:31–41

    Google Scholar 

  • Earl DA, von Holdt BM (2011) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genet Resources 4:359–361. doi:10.1007/s12686-011-9548-7

    Article  Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molec Ecol 14:2611–2620. doi:10.1111/j.1365-294X.2005.02553.x

    Article  CAS  Google Scholar 

  • García-Amorena I, Gómez Manzaneque F, Rubiales JM, Granja HM, Soares de Carvalho G, Morla C (2007) The Late Quaternary coastal forests of western Iberia: a study of their macroremains. Palaeogeogr Palaeoclimatol Palaeoecol 254:448–461. doi:10.1016/j.palaeo.2007.07.003

    Article  Google Scholar 

  • Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). Available at: http://www2.unil.ch/popgen/softwares/fstat.htm. Updated from Goudet (1995)

  • Hampe A, Petit RJ (2005) Conserving biodiversity under climate change: the rear edge matters. Ecol Lett 8:461–467. doi:10.1111/j.1461-0248.2005.00739.x

    Article  PubMed  Google Scholar 

  • Hamrick JL, Godt MJW (1996) Effects of life history traits on genetic diversity in plant species. Philos Trans Ser B Biol Sci 351:1291–1298

    Article  Google Scholar 

  • Hardy OJ, Vekemans X (2002) SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Molec Ecol Notes 2:618–620. doi:10.1046/j.1471-8286.2002.00305.x

    Article  Google Scholar 

  • Hardy OJ, Charbonnel N, Fréville H, Heuertz M (2003) Microsatellite allele sizes: a simple test to assess their significance on genetic differentiation. Genetics 163:1467–1482

    CAS  PubMed  PubMed Central  Google Scholar 

  • Heuertz M, Teufel J, González-Martínez SC, Soto A, Fady B, Alía R, Vendramin GG (2010) Geography determines genetic relationships between species of mountain pine (Pinus mugo complex) in western Europe. J Biogeogr 37:541–556. doi:10.1111/j.1365-2699.2009.02223.x

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Latałowa M, Tobolski K, Nalepka D (2004) Pinus L. subgenus Pinus (subgen. Diploxylon (Koehne) Pilger)—Pine. In: Ralska-Jasiewiczowa M (ed) Late glacial and Holocene history of vegetation in Poland based on isopollen maps. W. Szafer Institute of Botany, Kraków, pp 165–177

    Google Scholar 

  • Lewandowski A, Boratyński A, Mejnartowicz L (2000) Allozyme investigations on the genetic differentiation between closely related pines—Pinus sylvestris, P. mugo, P. uncinata, and P. uliginosa (Pinaceae). Pl Syst Evol 221:15–24. doi:10.1007/BF01086377

    Article  CAS  Google Scholar 

  • Lowry DB (2010) Landscape evolutionary genomics. Biol Lett 6:502–504. doi:10.1098/rsbl.2009.0969

    Article  PubMed  PubMed Central  Google Scholar 

  • Luikart G, Cornuet J-M (1998) Empirical evaluation of a test for identifying recently bottlenecked populations from allele frequency data. Conservation Biol 12:228–237

    Article  Google Scholar 

  • Markert JA, Champlin DM, Gutjahr-Gobell R, Grear JS, Kuhn A, McGreevy TJ Jr, Roth A, Bagley MJ, Nacci DE (2010) Population genetic diversity and fitness in multiple environments. BMC Evol Biol 10:205. doi:10.1186/1471-2148-10-205

    Article  PubMed  PubMed Central  Google Scholar 

  • Matschiner M, Salzburger W (2009) TANDEM: integrating automated allele binning into genetics and genomics workflows. Bioinformatics 25:1982–1983. doi:10.1093/bioinformatics/btp303

    Article  CAS  PubMed  Google Scholar 

  • Monteleone I, Ferrazzini D, Belletti P (2006) Effectiveness of neutral RAPD markers to detect genetic divergence between the subspecies uncinata and mugo of Pinus mugo Turra. Silva Fenn 40:391–406

    Article  Google Scholar 

  • Neale DB, Kremer A (2011) Forest tree genomics: growing resources and applications. Nat Rev Genet 12:111–122. doi:10.1038/nrg2931

    Article  CAS  PubMed  Google Scholar 

  • Nosil P, Feder JL (2013) Genome evolution and speciation: toward quantitative descriptions of pattern and process. Evolution 67:2461–2467. doi:10.1111/evo.12191

    Article  PubMed  Google Scholar 

  • Orsini L, Vanoverbeke J, Swillen I, Mergeay J, De Meester L (2013) Drivers of population genetic differentiation in the wild: isolation by dispersal limitation, isolation by adaptation and isolation by colonization. Molec Ecol 22:5983–5999. doi:10.1111/mec.12561

    Article  Google Scholar 

  • Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Molec Ecol Notes 6:288–295. doi:10.1111/j.1471-8286.2005.01155.x

    Article  Google Scholar 

  • Peery MZ, Kirby R, Reid BN, Stoelting R, Doucet-Bëer E, Robinson S, Vásquez-Carrillo C, Pauli JN, Palsbøll PJ (2012) Reliability of genetic bottleneck tests for detecting recent population declines. Molec Ecol 21:3403–3418. doi:10.1111/j.1365-294X.2012.05635.x

    Article  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 

  • Raymond M, Rousset F (1995) An exact test for population differentiation. Evolution 49:1280–1283

    Article  Google Scholar 

  • Robledo-Arnuncio JJ, Collada C, Alía R, Gil L (2005) Genetic structure of montane isolates of Pinus sylvestris L. in a Mediterranean refugial area. J Biogeogr 32:595–605. doi:10.1111/j.1365-2699.2004.01196.x

    Article  Google Scholar 

  • Rousset F (2008) Genepop’007: a complete re-implementation of the Genepop software for Windows and Linux. Molec Ecol Resources 8:103–106. doi:10.1111/j.1471-8286.2007.01931.x

    Article  Google Scholar 

  • Sannikov SN, Petrova IV, Schweingruber F, Egorov EV, Parpan TV (2011) Genetic differentiation of Pinus mugo Turra and P. sylvestris L. populations in the Ukrainian Carpathians and the Swiss Alps. Russ J Ecol 42:270–276. doi:10.1134/s1067413611040151

    Article  Google Scholar 

  • Schoville SD, Bonin A, François O, Lobreaux S, Melodelima C, Manel S (2012) Adaptive genetic variation on the landscape: methods and cases. Annual Rev Ecol Evol Syst 43:23–43. doi:10.1146/annurev-ecolsys-110411-160248

    Article  Google Scholar 

  • Sinclair WT, Morman JD, Ennos RA (1998) Multiple origins for Scots pine (Pinus sylvestris L.) in Scotland evidence from mitochondrial DNA variation. Heredity 80:233–240. doi:10.1046/j.1365-2540.1998.00287.x

    Article  CAS  Google Scholar 

  • Slavov GT, Zhelev P (2004) Allozyme variation, differentiation, and inbreeding in populations of Pinus mugo in Bulgaria. Canad J Forest Res 34:2611–2617. doi:10.1139/x04-127

    Article  CAS  Google Scholar 

  • Sobierajska K, Boratyńska K (2008) Variability of needle characteristics of Pinus mugo Turra populations in the Karkonosze Mountains in Poland. Dendrobiology 59:41–49

    Google Scholar 

  • Sobierajska K, Boratyńska K, Marcysiak K (2010) Variation of cone characters in Pinus mugo (Pinaceae) populations in the Giant Mountains (Karkonosze, Sudetes). Dendrobiology 63:33–41

    Google Scholar 

  • Soranzo N, Alía R, Provan J, Powell W (2000) Patterns of variation at a mitochondrial sequence-tagged-site locus provides new insights into the postglacial history of European Pinus sylvestris populations. Molec Ecol 9:1205–1211. doi:10.1046/j.1365-294x.2000.00994.x

    Article  CAS  Google Scholar 

  • Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) Micro-Checker: software for identifying and correcting genotyping errors in microsatellite data. Molec Ecol Notes 4:535–538. doi:10.1111/j.1471-8286.2004.00684.x

    Article  Google Scholar 

  • Vendramin GG, Degen B, Petit RJ, Anzidei M, Madaghiele A, Ziegenhagen B (1999) High level of variation at Abies alba chloroplast microsatellite loci in Europe. Molec Ecol 8:1117–1126. doi:10.1046/j.1365-294x.1999.00666.x

    Article  Google Scholar 

  • Wachowiak W, Boratyńska K, Cavers S (2013) Geographical patterns of nucleotide diversity and population differentiation in three closely related European pine species in the Pinus mugo complex. Bot J Linn Soc 172:225–238. doi:10.1111/boj.12049

    Article  Google Scholar 

  • Willis KJ, Bennett KD, Birks HJB (1998) The late Quaternary dynamics of pines in Europe. In: Richardson DM (ed) Ecology and biogeography of Pinus. Cambridge University Press, Cambridge, pp 107–121

    Google Scholar 

  • Willis KJ, Rudner E, Sümegi P (2000) The full-glacial forests of Central and Southeastern Europe. Quatern Res 53:203–213. doi:10.1006/qres.1999.2119

    Article  Google Scholar 

  • Żukowska WB, Wachowiak W (2016) Utility of closely related taxa for genetic studies of adaptive variation and speciation: current state and perspectives in plants with focus on forest tree species. J Syst Evol 54:17–28

    Article  Google Scholar 

Download references

Acknowledgements

The authors would like to thank K. Boratyńska and A. Boratyński for the collection of the plant material and M. Litkowiec for technical support and valuable comments concerning the data analysis. The work was financially supported through a grant from the Polish National Science Centre (Grant No. DEC-2012/05/E/NZ9/03476).

Funding

This study was funded through a grant from the Polish National Science Centre (Grant No. DEC-2012/05/E/NZ9/03476).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Weronika B. Żukowska.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

Additional information

Handling editor: Andreas Tribsch.

Electronic supplementary material

Information on Electronic Supplementary Material

Information on Electronic Supplementary Material

Online Resource 1. Characteristics of the 22 nSSR markers initially tested.

Online Resource 2. Private alleles detected in the analysed Pinus mugo populations.

Online Resource 3. Pairwise matrix of F ST Excluding Null Alleles (F STnull) among the Pinus mugo populations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Żukowska, W.B., Wachowiak, W. Nuclear microsatellite markers reveal the low genetic structure of Pinus mugo Turra (dwarf mountain pine) populations in Europe. Plant Syst Evol 303, 641–651 (2017). https://doi.org/10.1007/s00606-017-1395-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00606-017-1395-x

Keywords

Navigation