Abstract
Serbian spruce, Picea omorika (Panč.) Purk., is a cold-adapted conifer confined to an area of c. 10,000 km2 within the Balkans. This area, which has not been exposed to severe anthropogenic disturbances in the recent past, represents a long-term cryptic refugium of this species. We studied Quaternary dynamics of fragmentary distributed Serbian spruce populations to uncover genetic and demographic processes accounting for high levels of genetic diversities in this endemic species within its long-term cryptic refugium. Based on our data set [499 trees from ten populations, five nuclear microsatellites (EST-SSRs) and a mitochondrial (mtDNA) locus], we found the following: (i) continuous increase of genetic distinctiveness of populations caused by various genetic and/or demographic processes, (ii) decreasing over generations pollen flow, and (iii) almost complete lack of seed flow, are trends applicable not only for post-glacial but also for glacial populations. As a result, populations distant few kilometers or less were poorly connected and highly differentiated (nuclear DNA: average ρ ST , Hedrick’s G′ ST and Jost’s D of 0.165, 0.429 and 0.385, respectively; mtDNA: G ST = 0.632). They were characterized as independent gene pools at the nuclear DNA level. Nonetheless, levels of genetic diversity were high at both nuclear (average allelic richness = 16.14; average H E = 0.776) and mtDNA (H T = 0.231) levels. They were maintained not by pronounced gene flow but rather by frequent admixtures of highly differentiated populations, and also by species longevity and overlapping generations in the populations. However, admixtures had been possible only if populations encountered each other over time. Particular genetic and/or demographic changes of populations, such as fragmentations, admixture, size reductions/expansions and extinctions, could not be associated exclusively neither to the post-glacial nor to the last glacial as they were detected during both periods. In accordance with expectations on range alternations in cold-adapted taxa confined to refugia during warm Quaternary periods, our study species was expanding range during the last glacial and contracting range post-glacially. Recommendations for conservation of this IUCN red-listed, endemic and relict species have been provided.


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Acheré V, Favre JM, Besnard G, Jeandroz S (2005) Genomic organization of molecular differentiation in Norway spruce (Picea abies). Mol Ecol 14:3191–3201
Aizawa M, Yoshimaru H, Katsuki T, Kaji M (2008) Imprint of post-glacial history in a narrowly distributed endemic spruce, Picea alcoquiana, in central Japan observed in nuclear microsatellites and organelle DNA markers. J Biogeogr 35:1295–1307
Aizawa M, Yoshimaru H, Saito H, Katsuki T, Kawahara T, Kitamura K, Shi F, Sabirov R, Kaji M (2009) Range-wide genetic structure in a north–east Asian spruce (Picea jezoensis) determined using microsatellites markers. J Biogeogr 36:996–1007
Aleksić MJ (2008) Genetic structure of natural populations of Serbian spruce [Picea omorika (Panč.) Purk.]. Dissertation, University of Natural Resources and Applied Life Sciences, Vienna. Available at https://zidapps.boku.ac.at/abstracts/download.php?dataset_id=6870&property_id=107
Aleksić MJ, Geburek T (2010) Mitochondrial DNA reveals complex genetic structuring in a stenoendemic conifer Picea omorika [(Panč.) Purk.] caused by its long persistence within the refugial Balkan region. Plant Syst Evol 285:1–11
Aleksić MJ, Schueler S, Mengl M, Geburek T (2009) EST-SSRs developed for other Picea species amplify in Picea omorika and reveal high genetic variation in two natural populations. Belg J Bot 142:89–95
Anderson LL, Hu FS, Paige KN (2011) Phylogeographic history of white spruce during the last glacial maximum: uncovering cryptic refugia. J Hered 102:207–216
Ballian D, Longauer R, Mikić T, Paule L, Kajba D, Gömöry D (2006) Genetic structure of a rare European conifer, Serbian spruce (Picea omorika (Pančić) Purk.). Plant Syst Evol 260:53–63
Barbujani G (1987) Autocorrelation of gene frequencies under isolation by distance. Genetics 117:777–782
Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F (2004) GENETIX 4.05, logiciel sous Windows TM pour la génétique des populations. Laboratoire Génome, Populations, Interactions, CNRS UMR 5171, Université de Montpellier II, Montpellier
Bennett KD, Provan J (2008) What do we mean by ‘refugia’? Quat Sci Rev 27:2449–2455
Bennett KD, Tzedakis PC, Willis KJ (1991) Quaternary refugia of north European trees. J Biogeogr 18:103–115
Benzécri J-P (1973) L’Analyse des Données. L’Analyse des Correspondances, vol II. Dunod, Paris
Bouillé M, Bousquet J (2005) Trans-species shared polymorphisms at orthologous nuclear gene loci among distant species in the conifer Picea (Pinaceae): implications for the long-term maintenance of genetic diversity in trees. Am J Bot 92:63–73
Butcher PA, McNee SA, Krauss SL (2008) Genetic impacts of habitat loss on the rare ironstone endemic Tetratheca paynterae subsp. paynterae. Conserv Genet 10:1735–1746
Canestrelli D, Cimmaruta R, Costantini V, Nasceti G (2006) Genetic diversity and phylogeography of the Apennine yellow-bellied toad Bombina pachypus, with implications for conservation. Mol Ecol 15:3741–3754
Canestrelli D, Salvi D, Maura M, Bologna MA, Nascetti G (2012) One species, three Pleistocene evolutionary histories: phylogeography of the Italian crested newt, Triturus carnifex. PLoS One 7:e41754
Cavalli-Sforza LL, Edwards AWF (1967) Phylogenetic analysis: models and estimation procedures. Evolution 32:550–570
Chakraborty R (1990) Mitochondrial DNA polymorphism reveals hidden heterogeneity within some Asian populations. Am J Hum Genet 47:87–94
Chen C, Durand E, Forbes F, Francois O (2007) Bayesian clustering algorithms ascertaining spatial population structure: a new computer program and a comparison study. Mol Ecol Notes 7:747–756
Ciofi C, Baumont MA, Swingland IR, Bruford MW (1999) Genetic divergence and units for conservation in the Komodo dragon Varanus komodoensis. Proc R Soc Lond B Biol Sci 266:2269–2274
Clarke TE, Levin DB, Kavanaugh DH, Reimchen TE (2001) Rapid evolution in the Nebria gregaria group (Coleoptera: Carabidae) and the paleogeography of the Queen Charlotte Islands. Evolution 55:1408–1418
Cole CT (2003) Genetic variation in rare and common plants. Annu Rev Ecol Evol Syst 34:213–237
Čolić DB (1957) Neki pionirski karakteri Pančićeve omorike i njena uloga u sukcesiji biljnih zajednica. Archives des sciences bioloqiques 9(1–4):51–60 (in Serbian with English and German summary)
Comes HP, Kadereit JW (1998) The effect of quaternary climatic changes on plant distribution and evolution. Trends Plant Sci 3:432–438
Conifer Specialist Group (1998) Picea omorika. 2007 IUCN Red List of Threatened Species. http://www.iucnredlist.org/search/details.php/30313/summ
Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014
Crawford NG (2010) SMOGD: software for the measurement of genetic diversity. Mol Ecol Resour 10:556–557
Dallimore W, Jackson AB, Harrison SG (1967) A handbook of Coniferae and Ginkgoaceae, 4th edn. St. Martin’s Press, New York, p 729
Dan T, Ikeda H, Mitsui Y, Isagi Y, Setoguchi H (2009) Genetic structure of refugial populations of the temperate plant Shortia rotundifolia (Diapensiaceae) on a subtropical island. Conserv Genet 10:859–867
David P, Pujol B, Viard F, Castella V, Goudet J (2007) Reliable selfing rate estimates from imperfect population genetic data. Mol Ecol 16:2474–2487
Delgado P, Pinero D, Chaos A, Perez-Nasser N, Alvarez-Buylla ER (1999) High population differentiation and genetic variation in the endangered Mexican pine Pinus rzedowskii (Pinaceae). Am J Bot 86:669–676
Dizdarević M, Lakušić R, Grgić P, L Kutleša, Pavlović B, Jonlija R (1984) Ekološke osnove poimanja reliktnosti vrste Picea omorika Pančić. Bilten Društva ekologa Bosne i Herzegovine, Ser A 2:5–56 (in Bosnian with English abstract)
Dumolin-Lapègue S, Demesure B, Fineschi S, Le Core V, Petit RJ (1997) Phylogeographic structure of white oaks throughout the European continent. Genetics 146:1475–1487
Durand E, Chen C, François O (2009) TESS version 2.3 reference manual. http://membrestimc.imag.fr/Olivier.Francois/manual.pdf. Accessed June 2012
Ennos RA (1994) Estimating the relative rates of pollen and seed migration among plant populations. Heredity 72:250–259
Eriksson G (2005) Evolution and evolutionary factors, adaptation and adaptability. In: Geburek T, Turok J (eds) Conservation and management of forest genetic resources in Europe. Arbora Publishers, Zvolen, pp 199–211
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
Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491
Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50
Felsenstein J (2003) PHYLIP: Phylogeny Inference Package version 3.61. University of Washington, Seattle. http://evolution.gs.washington.edu/phylip.html
Frajman B, Oxelman B (2007) Reticulate phylogenetics and phytogeographical structure of Heliosperma (Sileneae, Caryophyllaceae) inferred from chloroplast and nuclear DNA sequences. Mol Phylogenet Evol 43:140–155
Francois O, Ancelet S, Guillot G (2006) Bayesian clustering using hidden Markov random fields in spatial population genetics. Genetics 174:805–816
Fraser DJ, Bernatchez LB (2001) Adaptive evolutionary conservation: towards a unified concept for defining conservation units. Mol Ecol 10:2741–2752
Gajić M, Vilotić D, Karadžić D, Mihajlović L, Isajev V (1994) Serbian spruce—Picea omorika (Pančić) Purkynĕ on the territory of the National Park Tara. The National Park Tara, Bajina Bašta and the Faculty of Forestry, Belgrade (in Serbian)
Gamache I, Jaramillo-Correa JP, Payette S, Bousquet J (2003) Diverging patterns of mitochondrial and nuclear DNA diversity in subarctic black spruce: imprint of a founder effect associated with postglacial colonization. Mol Ecol 12:891–901
Gao H, Williamson S, Bustamante CD (2007) An Markov chain Monte Carlo approach for joint inference of population structure and inbreeding rates from multi-locus genotype data. Genetics 176:1635–1651
Garza JC, Williamson EG (2001) Detection of reduction in population size using data from microsatellite loci. Mol Ecol 10:305–318
Ge X-J, Yu Y, Zhao N-X, Chen H-S, Qi W-Q (2003) Genetic variation in the endangered Inner Mongolia endemic shrub Tetraena mongolica Maxim (Zygophyllaceae). Biol Conserv 111:427–434
Geburek T (1986) Some results of inbreeding depression in Serbian spruce (Picea omorica (Panč.) Purk.). Silvae Genet 35:169–172
Geist J, Kuehn R (2005) Genetic diversity and differentiation of central European freshwater pearl mussel (Margaritifera margaritifera L.) populations: implications for conservation and management. Mol Ecol 14:425–439
Gigov A (1956) Dosadašnji nalazi o postglacijalnoj istoriji šuma Srbije. Institut za ekologiju i biogeografiju, Zbornik radova 7(3):1–25 (in Serbian with German summary)
Gitzendanner MA, Soltis PS (2000) Patterns of genetic variation in rare and widespread plant congeners. Am J Bot 87:783–792
Gómez A, Lunt DH (2007) Refugia within refugia: patterns of phylogeographic concordance in the Iberian Peninsula. In: Weiss S, Ferrand N (eds) Phylogeography of southern European refugia. Springer, Berlin, pp 155–188
Goodman SJ (1997) RSTCALC: a collection of computer programs for calculating estimates of genetic differentiation from microsatellite data and determining their significance. Mol Ecol 6:881–885
Goudet J (2001) FSTST, a program to estimate and test gene diversities and fixation indices version 2.9.3.2, updated from Goudet 1995. Available at http://www2.unil.ch/popgen/softwares/fstat.htm
Grassi F, Minuto L, Casazza G, Labra M, Sala F (2009) Haplotype richness in refugial areas: phylogeographical structure of Saxifraga callosa. J Plant Res 122:377–387
Guo SW, Thompson EA (1992) Performing the exact test of Hardy–Weinberg proportion for multiple alleles. Biometrics 48:361–372
Hamrick JL, Godt MJW (1996) Effects of life history traits on genetic diversity in plant species. Philos Trans R Soc Lond B Biol Sci 352:1291–1298
Hardy OJ, Vekemans X (2002) SPAGeDi: a versatile computer program to analyze spatial genetic structure at the individual or population levels. Mol Ecol Notes 2:618–620
Hedrick PW (2005) A standardized genetic differentiation measure. Evolution 59:1633–1638
Hewitt GM (1996) Some genetic consequences of ice ages, and their role in divergence and speciation. Biol J Linn Soc Lond 58:247–276
Hewitt G (1999) Post-glacial recolonisation of European biota. Biol J Linn Soc 68:87–112
Hewitt G (2000) The genetic legacy of the Quaternary ice ages. Nature 405:907–913
Hewitt GM (2001) Speciation, hybrid zones and phylogeography—or seeing genes in space and time. Mol Ecol 10:537–549
Hewitt GM (2004) Genetic consequences of climatic oscillations in the Quaternary. Philos Trans R Soc Lond B Biol Sci 359:183–195
Honnay O, Jacquemyn H (2007) Susceptibility of common and rare plant species to the genetic consequences of habitat fragmentation. Conserv Biol 21:823–831
Horn A, Stauffer C, Lieutier F, Kerdelhué C (2009) Complex postglacial history of the temperate bark beetle Tomicus piniperda L. (Coleoptera, Scolytinae). Heredity 103:238–247
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
Hughes PD, Woodward JC, Gibbard PL (2007) Middle Pleistocene cold stage climates in the Mediterranean: new evidence from the glacial record. Earth Planet Sci Lett 253:50–56
Jaramillo-Correa JP, Beaulieu J, Ledig FT, Bousquet J (2006) Decoupled mitochondrial and chloroplast DNA population structure reveals Holocene collapse and population isolation in a threatened Mexican-endemic conifer. Mol Ecol 15:2787–2800
Johnson NK, Cicero C (2004) New mitochondrial DNA data affirm the importance of Pleistocene speciation in North American birds. Evolution 58:1122–1130
Jost L (2008) G ST and its relatives do not measure differentiation. Mol Ecol 17:4015–4026
Katsuki T, Shimada K, Yoshimaru H (2011) Process to extinction and genetic structure of a threatened Japanese conifer, Picea koyamae. J For Res 16:292–301
Klumpp RT (2005) Seed and pollen storage: European Focus. In: Geburek T, Turok J (eds) Conservation and management of forest genetic resources in Europe. Arbora Publishers, Zvolen, pp 601–622
Knowles LL (2000) Tests of Pleistocene speciation in montane grasshoppers (genus Melanoplus) from the sky islands of western North America. Evolution 54:1337–1348
Kohlermann L (1950) Untersuchungen über die Windverbreitung der Früchte und Samen mitteleuropäischer Waldbäume. Forstwiss Cbl 69:606–624
Komlodi JM (1970) Studies on the vegetational history of Picea omorica Panc. on the Great Hungarian Plain. Annales Universitatis Scientiarum Budapestinensis de Rolando Eötvös Nominatae, Sectio biologica 12:143–156
Kremer A (1994) Diversité génétique et variabilité des caractères phènotypiques chez les arbres forestiers. Genet Sel Evol 26(Suppl 1):105–123
Kryštufek B, Buzan EV, Hutchinson WF, Hänfling B (2007) Phylogeography of the rare Balkan endemic Martino’s vole, Dinaromys bogdanovi, reveals strong differentiation within the western Balkan Peninsula. Mol Ecol 16:1221–1232
Kuittinen H, Savolainen O (1992) Picea omorika is a self-fertile but outcrossing conifer. Heredity 68:183–187
Kuittinen H, Muona O, Kärkkäinen K, Borzan Ž (1991) Serbian spruce, a narrow endemic, contains much genetic variation. Can J For Res 21:363–367
Langner W (1959) Selbstfertilität und Inzucht bei Picea omorica (Pančić) Purkyne. Silvae Genet 8:84–93
Laroche J, Li P, Maggia L, Bousquet J (1997) Molecular evolution of angiosperm mitochondrial introns and exons. Proc Nat Acad Sci USA 94:5722–5727
Leimu R, Mutikainen P, Koricheva J, Fisher M (2006) How general are positive relationships between plant population size, fitness and genetic variation? J Ecol 94:942–952
Lewis PO, Crawford DJ (1995) Pleistocene refugium endemics exhibit greater allozyme diversity than widespread congeners in the genus Polygonella (Polygonaceae). Am J Bot 82:141–149
Lippé C, Dumont P, Bernatchez L (2006) High genetic diversity and no inbreeding in the endangered copper redhorse, Moxostoma hubbsi (Catostomidae, Pisces): the positive sides of a long generation time. Mol Ecol 15:1769–1780
Lockwood JD, Aleksić MJ, Zou J, Wang J, Liu J, Renner SS (2013) A new phylogeny for the genus Picea from plastid, mitochondrial and nuclear sequences. Mol Phylogenet Evol. doi:10.1016/j.ympev.2013.07.004
Magri D, Fineschi S, Bellarosa R, Buonamici A, Sebastiani F, Schirone B, Simeone MC, Vendramin GG (2007) The distribution of Quercus suber chloroplast haplotypes matches the paleogeographical history of the western Mediterranean. Mol Ecol 16:5259–5266
Mantel N (1967) The detection of disease clustering and generalize regression approach. Cancer Res 27:209–220
Mataruga M, Isajev D, Gardner M, Christian T, Thomas P (2011) Picea omorika. In: IUCN 2012. IUCN Red List of Threatened Species. Version 2012.2. http://www.iucnredlist.org
McKay JK, Latta RG (2002) Adaptive population divergence: markers, QTL and traits. Trends Ecol Evol 17:285–291
Médail F, Diadema K (2009) Glacial refugia influence plant diversity patterns in the Mediterranean Basin. J Biogeogr 36:1333–1345
Medrano M, Herrera CM (2008) Geographical structuring of genetic diversity across the whole distribution range of Narcissus longispathus, a habitat-specialist, Mediterranean narrow endemic. Ann Bot 102:183–194
Melbourne BA, Hastings A (2008) Extinction risk depends strongly on factors contributing to stochasticity. Nature 454:100–103
Meloni M, Perini D, Binelli G (2007) The distribution of genetic variation in Norway spruce (Picea abies Karst.) populations in western Alps. J Biogeogr 34:929–938
Michalakis Y, Excoffier L (1996) A generic estimation of population subdivision using distances between alleles with special reference for microsatellite loci. Genetics 142:1061–1064
Milivojević M, Menković L, Ćalić J (2008) Pleistocene glacial relief of the central part of Mt. Prokletije (Albanian Alps). Quat Int 190:112–122
Moritz C (1994) Defining ‘evolutionary significant units’ for conservation. Trends Ecol Evol 9:373–375
Muona O (1989) Population genetics in forest tree improvement. In: Brown AHD, Clegg MT, Kahler AL, Weir BD (eds) Plant population genetics, breeding and genetic resources. Sinauer Association, Sunderland, pp 285–301
Nasri N, Bojović S, Vendramin GG, Fady B (2008) Population genetic structure of the relict Serbian spruce, Picea omorika, inferred from plastid DNA. Plant Syst Evol 271:1–7
Near TJ, Benard MF (2004) Rapid allopatric speciation in logperch darters (Percidae: Percina). Evolution 58:2798–2808
Nei M (1978) Estimation of average heterozygosity and genetic distance for small number of individuals. Genetics 89:583–590
Ostojić D (2005) Ekološki činioci prirodnog održavanja i obnove cenopopulacija Pančićeve omorike u NP Tara. Dissertation, Faculty of Forestry, University of Belgrade
Pančić J (1877) Eine neue Conifere in den oestlischen Alpen. Serbischen Staatsdrukerei, Belgrade
Petit RJ, El Mousadik A, Pons O (1998) Identifying populations for conservation on the basis of genetic markers. Conserv Biol 12:844–855
Petit RJ, Aguinagalde I, de Beaulieu J-L, Bittkau C, Brewer S, Cheddadi R et al (2003) Glacial refugia: hotspots but not melting pots of genetic diversity. Science 300:1563–1565
Petit RJ, Duminil J, Fineschi S, Hampe A, Salvini D, Vendramin GG (2005) Comparative organization of chloroplast, mitochondrial and nuclear diversity in plant populations. Mol Ecol 14:689–701
Piry S, Luikar G, Cornuet JM (1999) BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data. J Hered 90:502–503
Podnar M, Mayer W, Tvrtković N (2004) Mitochondrial phylogeography of the Dalmatian wall lizard, Podarcis melisellensis (Lacertidae). Org Divers Evol 4:307–317
Pons O, Petit RJ (1996) Measuring and testing genetic differentiation with ordered versus unordered alleles. Genetics 144:1237–1245
Previšić A, Walton C, Kučinić M, Mitrikeski PT, Kerovec M (2009) Pleistocene divergence of Dinaric Drusus endemics (Trichoptera, Limnephilidae) in multiple micro-refugia within the Balkan Peninsula. Mol Ecol 18:634–647
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Provan J, Bennett KD (2008) Phylogeographic insights into cryptic glacial refugia. Trends Ecol Evol 23:564–571
Ravazzi C (2002) Late Quaternary history of spruce in southern Europe. Rev Palaeobot Palynol 120:131–177
Reed DH, Frankham R (2001) How closely correlated are molecular and quantitative measures of genetic variation? A meta-analysis. Evolution 55:1095–1103
Ribera I, Vogler AP (2004) Speciation in Iberian diving beetles in Pleistocene refugia (Coleoptera, Dytiscidae). Mol Ecol 13:179–193
Rousset F (2008) GENEPOP’007: a complete re-implementation of the GENEPOP software for Windows and Linux. Mol Ecol Resour 8:103–106
Rull V (2009) Microrefugia. J Biogeogr 36:481–484
Rungis D, Bérubé Y, Zhang J, Ralph S, Ritland CE, Ellis BE et al (2004) Robust simple sequence repeat markers for spruce (Picea spp.) from expressed sequence tags. Theor Appl Genet 109:1283–1294
Schemske DW, Lande R (1985) The evolution of self-fertilization and inbreeding depression in plants. II. Empirical observations. Evolution 39:41–52
Schmidt PA (1998) Picea A. Dietr. In: Schütt P, Schuck HJ, Lang U, Roloff A (eds) Enzyklopädie der Holzgwächse. 14. Erg. Lfg., 12/95. Ecomed-Verlag, Landsberg, pp 1–14
Scotti I, Paglia G, Magni F, Morgante M (2006) Population genetics of Norway spruce (Picea abies Karst.) at regional scale: sensitivity of different microsatellite motif classes in detecting differentiation. Ann For Sci 63:485–491
Šijačić-Nikolić M, Milovanović J, Katičić-Trupčević I (2009) Model of Serbian spruce genetic diversity conservation applying MPBS method for adaptability improvement. Int J Biodiv Conserv 1:001–003
Slatkin M (1993) Isolation by distance in equilibrium and nonequilibrium populations. Evolution 43:1349–1368
Slatkin M (1995) A measure of population subdivision based on microsatellite allele frequencies. Genetics 139:457–462
Stanković S (1960) The Balkan lake Ohrid and its living world. Dr. W. Junk, Den Haag
Stevanović V (1996) Analysis of the central European and Mediterranean orophytic element on the mountains of the west and central Balkan peninsula, with special reference to endemics. Bocconea 5:77–97
Stevanović V, Jovanović S, Lakušić D, Niketić M (1995) Diverzitet vaskularne flore Jugoslavije sa pregledom vrsta od međunarodnog značaja. In: Stevanović V, Vasić V (eds) Biodiverzitet Jugoslavije sa pregledom vrsta od međunarodnog značaja. Biološki fakultet i Ecolibri, Beograd, pp 183–217
Stewart JR, Dalén L (2008) Is the glacial refugium concept relevant for northern species? A comment on Pruett and Winker 2005. Clim Change 86:1–2
Stewart JR, Lister AM (2001) Cryptic northern refugia and the origins of the modern biota. Trends Ecol Evol 16:608–613
Stewart JR, Lister AM, Barnes I, Dalén L (2010) Refugia revisited: individualistic responses of species in space and time. Proc R Soc B 277:661–671
Stojanović LL (1995) Pančićeva omorika na karakterističnim nalazištima u Srbiji: Uticaj nekih faktora staništa i sastojina na dinamiku razvitka stabala. Javno preduzeće Nacionalni Park Tara, Bajina Bašta, p 96 (in Serbian with English Abstract)
Surina B, Schönswetter P, Schneeweiss GM (2011) Quaternary range dynamics of ecologically divergent species (Edraianthus serpyllifolius and E. tenuifolius, Campanulaceae) within the Balkan refugium. J Biogeogr 38:1381–1393
Taberlet P, Fumagalli L, Wust-Saucy AG, Cosson JF (1998) Comparative phylogeography and postglacial colonization routes in Europe. Mol Ecol 7:453–464
Tallmon DA, Koyuk A, Luikart G, Beaumont MA (2008) ONeSAMP: a program to estimate effective population size using approximate Bayesian computation. Mol Ecol Resour 8:299–301
Tucić B, Stojković B (2001) Shade avoidance syndrome in Picea omorika seedlings: a growth-room experiment. J Evol Biol 14:444–455
Tucović A, Isajev V (1982) Uticaj različitih tipova oprašivanja na neka svojstva šišarica i semena omorike. Glasnik Šumarskog Fakulteta u Beogradu, Ser. C, Pejzažna arhitektura 59:59–65 (in Serbian with English abstract)
Turill WB (1929) The plant life of the Balkan peninsula. A phylogeographical study. Oxford and the Clarendon Press, Oxford
Tzedakis PC, Lawson IT, Frogley MR, Hewitt GM, Preece RC (2002) Buffered tree population changes in a Quaternary refugium: evolutionary implications. Science 297:2044–2047
Unger GM, Konrad H, Geburek T (2011) Does spatial genetic structure increase with altitude? An answer from Picea abies in Tyrol, Austria. Plant Syst Evol 292:133–141
Ursenbacher S, Schweiger S, Tomović L, Crnobrnja-Isailović J, Fumagalli L, Mayer W (2008) Molecular phylogeography of the nose-horned viper (Vipera ammodytes, Linnaeus (1758)): evidence for high genetic diversity and multiple refugia in the Balkan peninsula. Mol Phylogenet Evol 46:1116–1128
Utescher T, Djordjević-Milutinović D, Bruch A, Mosbrugger V (2007) Palaeoclimate and vegetation change in Serbia during the last 30 Ma. Palaeogeogr Palaeoclimatol Palaeoecol 253:141–152
Van Geert A, Van Rossum F, Triest L (2008) Genetic diversity in adult and seedling populations of Primula vulgaris in a fragmented agricultural landscape. Conserv Genet 9:845–853
van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538
Vendramin GG, Fady B, González-Martínez SC, Hu FS, Scotti I, Sebastiani F, Soto Á, Petit RJ (2008) Genetically depauperate but widespread: the case of an emblematic Mediterranean pine. Evolution 62:680–688
Vidaković M (1991) Conifers, morphology and variation, 2nd edn. Grafički zavod Hrvatske, Zagreb
Vinceti B, Loo J, Gaisberger H, van Zonneveld MJ, Schueler S, Konrad K, Kadu CAC, Geburek T (2013) Conservation priorities for Prunus africana defined with the aid of spatial analysis of genetic data and climatic variables. PLoS ONE 8:e59987–e59987
Walter R, Epperson BK (2005) Geographic pattern of genetic diversity in Pinus resinosa: contact zone between descendants of glacial refugia. Am J Bot 92:92–100
Wang Y, Luo J, Xue X, Korpelainen H, Li C (2005) Diversity of microsatellite markers in the populations of Picea asperata from mountains of China. Plant Sci 168:707–714
Weir BS (1996) Genetic data analysis II, 2nd edn. Sinauer, Sunderland
Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370
Widmer A, Lexer C (2001) Glacial refugia: sanctuaries for allelic richness, but not for gene diversity. Trends Ecol Evol 16:267–269
Willis KJ, Rudner E, Sümegi P (2000) The full-glacial forests of central and southeastern Europe. Quat Res 53:203–213
Wright S (1943) Isolation by distance. Genetics 28:114–138
Wright S (1951) The genetical structure of populations. Ann Eugen 15:323–354
Young A, Boyle T, Brown T (1996) The population genetic consequences of habitat fragmentation for plants. Trends Ecol Evol 11:413–418
Zawko G, Krauss L, Dixon KW, Sivasithamparam K (2001) Conservation genetics of the rare and endangered Leucopogon obtectus (Ericaceae). Mol Ecol 10:2389–2396
Zhang Q, Chiang TY, George M, Liu JQ, Abbott RJ (2005) Phylogeography of the Qinghai-Tibetan Plateau endemic Juniperus przewalskii (Cupressaceae) inferred from chloroplast DNA sequence variation. Mol Ecol 14:3513–3524
Acknowledgments
This work was financially supported by the Republic of Austria, Biodiversity International and Research Grant 173005 of the Ministry of Education and Science of the Republic of Serbia. The authors would like to thank M. Mengl, L. Weißenbacher, M. Lakić, D. Milekić for assistance in the field, B. Heinze, B. Fussi, V. Stevanović, N. Tucić and B. Tucić for constructive suggestions regarding data interpretation, D. Stojanović and N. Rajčević for support in data analyses, Z. Barina for providing literature, J. C. Garza for providing MRatio software and helping in data interpretation, and to acknowledge the Cornell University’s Computational Biology Service (CBSU). All samples were collected with the permission and support of the Tara National Park (Republic of Serbia), the Ministry of Agriculture, Forestry and Water Management and the Forest Enterprise Šume Republike Srpske (Republic of Srpska, Bosnia and Herzegovina).
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Aleksić, J.M., Geburek, T. Quaternary population dynamics of an endemic conifer, Picea omorika, and their conservation implications. Conserv Genet 15, 87–107 (2014). https://doi.org/10.1007/s10592-013-0523-6
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DOI: https://doi.org/10.1007/s10592-013-0523-6