Abstract
Climate changes can shift species’ ranges. Knowledge on genetic variation of the leading-edge populations provides critical information to understand responses and adaptation of plants to projected climate warming. To date, the research into genetic variation of leading-edge populations has been limited, particularly in the role of wind-mediated pollen flow in maintaining high genetic variation. Castanopsis sclerophylla (Fagaceae) is a wind-pollinated and gravity-dispersed tree. In the present study, we used seven polymorphic microsatellites to genotype 482 samples from five leading-edge and 12 non-edge populations. Significant effects of recent population bottleneck events were found in three of the five leading-edge populations, indicating that the leading-edge populations might have been recolonized after the Last Glacial Maximum. Genetic diversity was higher, though not significantly, in leading-edge than in non-edge populations. Relationship between genetic diversity and latitude indicated an increasing trend of genetic diversity towards leading-edge populations. No significant difference in genetic differentiation was found between leading-edge and non-edge populations. The inconsistence with the general predictions by leading-edge colonization model could be explained by high gene flow via pollen grains. Pollen-mediated gene flow could maintain high genetic diversity within and low differentiation among leading-edge populations. In response to climate warming, high genetic variation may provide leading-edge populations raw materials for evolutionary adaptation to future environmental conditions.
Similar content being viewed by others
References
Alleaume-Benharira M, Pen IR, Ronce O (2006) Geographical patterns of adaptation within a species’ range: interactions between drift and gene flow. J Evol Biol 19:203–215
Arnaud-Haond S, Teixeira S, Massa SI, Billot C, Saenger P, Coupland G, Duarte CM, Serrao EA (2006) Genetic structure at range edge: low diversity and high inbreeding in Southeast Asian mangrove (Avicennia marina) populations. Mol Ecol 15:3515–3525
Austerlitz F, Garnier-Géré PH (2003) Modelling the impact of colonisation on genetic diversity and differentiation of forest trees: interaction of life cycle, pollen flow and seed long-distance dispersal. Heredity 90:282–290
Beaumont MA (1999) Detecting population expansion and decline using microsatellites. Genetics 153:2013–2029
Bialozyt R, Ziegenhagen B, Petit RJ (2006) Contrasting effects of long distance seed dispersal on genetic diversity during range expansion. J Evol Biol 19:12–20
Bridle JR, Polechov J, Kawata M, Butlin RK (2010) Why is adaptation prevented at ecological margins? New insights from individual-based simulations. Ecol Lett 13:485–494
Chen X-Y, Li YY, Wu TY, Zhang X, Lu HP (2003) Size-class differences in genetic structure of Metasequoia glyptostroboides Hu et Cheng (Taxodiaceae) plantations in Shanghai. Silvae Genet 52:107–109
Chen X-Y, Fan X-X, Hu X-S (2008) Roles of seed and pollen dispersal in natural regeneration of Castanopsis fargesii (Fagaceae): implications for forest management. For Ecol Manag 256:1143–1150
Chen Y, Compton SG, Liu M, Chen X-Y (2012) Fig trees at the northern limit of their range: the distributions of cryptic pollinators indicate multiple glacial refugia. Mol Ecol 21:1687–1701
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
Cottrell JE, Munro RC, Tabbener HE, Milner AD, Forrest GI, Lowe AJ (2003) Comparison of fine-scale genetic structure using nuclear microsatellites within two British oakwoods differing in population history. For Ecol Manag 176:287–303
Dieringer D, Schlötterer C (2003) Microsatellite analyser (MSA): a platform independent analysis tool for large microsatellite data sets. Mol Ecol Notes 3:167–169
Duminil J, Fineschi S, Hampe A, Jordano P, Salvini D, Vendramin GG, Petit RJ (2007) Can population genetic structure be predicted from life-history traits? Am Nat 169:662–672
Eckert CG, Samis KE, Lougheed SC (2008) Genetic variation across species’ geographical ranges: the central-marginal hypothesis and beyond. Mol Ecol 17:1170–1188
El Mousadik A, Petit RJ (1996) Chloroplast DNA phylogeography of the argan tree of Morocco. Mol Ecol 5:547–555
Ellegren H (2004) Microsatellites: simple sequences with complex evolution. Nat Rev Genet 5:435–445
Ennos RA (1994) Estimating the relative rates of pollen and seed migration among plants populations. Heredity 72:250–259
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, Foll M, Petit RJ (2009) Genetic consequences of range expansions. Annu Rev Ecol Evol Syst 40:481–501
Fan XX, Shen L, Zhang X, Chen X-Y, Fu C (2004) Assessing genetic diversity of Ginkgo biloba L. (Ginkgoaceae) populations from China by RAPD markers. Biochem Genet 42:269–278
Fang JY, Song YC, Liu HY, Piao SL (2002) Vegetation-climate relationship and its application in the division of vegetation zone in China. Acta Bot Sin 44:1105–1122
Fayard J, Klein EK, Lefevrè F (2009) Long distance dispersal and the fate of a gene from the colonization front. J Evol Biol 22:2171–2182
Goudet J (1995) FSTAT (version 1.2): a computer program to calculate F-statistics. J Hered 86:485–486
Hampe A, Petit RJ (2005) Conserving biodiversity under climate change: the rear edge matters. Ecol Lett 8:461–467
Hamrick JL, Godt MJW (1989) Allozyme diversity in plant species. In: Brown AHD, Clegg MT, Kahler AL, Weir BS (eds) Plant population genetics, breeding, and genetic resources. Sinauer, Sunderland, pp 43–63
Hamrick JL, Godt MJW (1996) Effects of life history traits on genetic diversity in plant species. Philos Trans R Soc B Biol Sci 351:1291–1298
Hansson B, Westerberg L (2002) On the correlation between heterozygosity and fitness in natural populations. Mol Ecol 11:2467–2474
Harrison SP, Yu G, Takahara H, Prentice IC (2001) Palaeovegetation: diversity of temperate plants in East Asia. Nature 413:129–130
Hedrick PW (2005) A standardized genetic differentiation measure. Evolution 59:1633–1638
Hensen I, Oberprieler C (2005) Effects of population size on genetic diversity and seed production in the rare Dictamnus albus (Rutaceae) in central Germany. Conserv Genet 6:63–73
Hewitt G (1996) Some genetic consequences of ice ages, and their role in divergence and speciation. Biol J Linnean Soc 58:247–276
Hewitt G (2000) The genetic legacy of the Quaternary ice ages. Nature 405:907–913
Honjo M, Ueno S, Tsumura Y, Handa T, Washitani I, Ohsawa R (2008) Tracing the origins of stocks of the endangered species Primula sieboldii using nuclear microsatellites and chloroplast DNA. Conserv Genet 9:1139–1147
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
Isagi Y, Suhandono S (1997) PCR primers amplifying microsatellite loci of Quercus myrsinifolia Blume and their conservation between oak species. Mol Ecol 6:897–899
Li YY, Guan SM, Yang SZ, Luo Y, Chen X-Y (2012) Genetic decline and inbreeding depression in the extremely rare tree, Ostrya rehderiana Chun (Betulaceae). Conserv Genet 13:343–347
Manni F, Guerard E, Heyer E (2004) Geographic patterns of (genetic, morphologic, linguistic) variation: how barriers can be detected by “Monmonier’s algorithm”. Hum Biol 76:173–190
Meirmans PG (2006) Using the AMOVA framework to estimate a standardized genetic differentiation measure. Evolution 60:2399–2402
Member of China Quaternary Pollen Data Base (2000) Pollen-based biome reconstruction at Middle Holocene (6 Ka BP) and Last Galcial Maximum (18 ka BP) in China. Acta Bot Sin 42:1201–1209
Monmonier M (1973) Maximum-difference barriers: an alternative numerical regionalization method. Geogr Anal 5:245–261
Muir G, Lowe AJ, Fleming CC, Vogl C (2004) High nuclear genetic diversity, high levels of outcrossing and low differentiation among remnant populations of Quercus petraea at the margin of its range in Ireland. Ann Bot London 93:691–697
Nei M, Tajima F, Tateno Y (1983) Accuracy of estimated phylogenetic trees from molecular data. J Mol Evol 19:153–170
Pannell JR, Dorken ME (2006) Colonisation as a common denominator in plant metapopulations and range expansions: effects on genetic diversity and sexual systems. Landsc Ecol 21:837–848
Parisod C, Bonvin G (2008) Fine-scale genetic structure and marginal processes in an expanding population of Biscutella laevigata L. (Brassicaceae). Heredity 101:536–542
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, 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, Luikart G, Cornuet J-M (1999) BOTTLENECK: a computer program for detecting recent reductions in the effective size using allele frequency data. J Hered 90:502–503
Pluess AR (2011) Pursuing glacier retreat: genetic structure of a rapidly expanding Larix decidua population. Mol Ecol 20:473–485
Preifer M, Passalacqua NG, Bartram S, Schatz B, Croce A, Carey PD, Kraudelt H, Jeltsch F (2010) Conservation priorities differ at opposing species borders of a European orchid. Biol Conserv 143:2207–2220
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Puşcaş M, Taberlet P, Choler P (2008) No positive correlation between species and genetic diversity in European alpine grasslands dominated by Carex curvula. Divers Distrib 14:852–861
R Development Core Team (2010) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Ray N, Excoffier L (2010) A first step towards inferring levels of long-distance dispersal during past expansions. Mol Ecol Resour 10:902–914
Shi MM, Michalski SG, Chen X-Y, Durka W (2011) Isolation by elevation: genetic structure at neutral and putatively non-neutral loci in a dominant tree of subtropical forests, Castanopsis eyrei. PLoS One 6:e21302
Stanley R, Linskens H (1974) Pollen: biology, biochemistry and management. Springer, Berlin
Straub SCK, Doyle JJ (2009) Conservation genetics of Amorpha georgiana (Fabaceae), an endangered legume of the Southeastern United States. Mol Ecol 18:4349–4365
Streiff R, Ducousso A, Lexer C, Steinkellner H, Gloessl J, Kremer A (1999) Pollen dispersal inferred from paternity analysis in a mixed oak stand of Quercus robur L. and Q. petraea (Matt.) Liebl. Mol Ecol 8:831–841
Sun XJ, Song CQ, Chen XD (1999) China Quaternary pollen database (CPD) and “Biome 6000” project. Adv Earth Sci 14:407–411
Sutherland BG, Belaj A, Nier S, Cottrell JE, Vaughan SP, Hubert J, Russell K (2010) Molecular biodiversity and population structure in common ash (Fraxinus excelsior L.) in Britain: implications for conservation. Mol Ecol 19:2196–2211
Ueno S, Yoshimaru H, Kawahara T, Yamamoto S (2000) Isolation of microsatellite markers in Castanopsis cuspidata var. sieboldii Nakai from an enriched library. Mol Ecol 9:1188–1190
Ueno S, Yoshimaru H, Kawahara T, Yamamoto S (2003) A further six microsatellite markers for Castanopsis cuspidata var. sieboldii Nakai. Conserv Genet 4:813–815
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
van Rossum F, Vekemans X, Meerts P, Gratia E, Lefebvre C (1997) Allozyme variation in relation to ecotypic differentiation and population size in marginal populations of Silene nutans. Heredity 78:552–560
Wang W-T (1992) On some distribution patterns and some migration routes found in the eastern Asiatic region. Acta Phytotaxon Sin 30:1–24
Wang R, Compton SG, Chen X-Y (2011) Fragmentation can increase spatial genetic structure without decreasing pollen-mediated gene flow in a wind-pollinated tree. Mol Ecol 20:4421–4432
Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370
Yakimowski SB, Eckert CG (2008) Populations do not become less genetically diverse or more differentiated towards the northern limit of the geographical range in clonal Vaccinium stamineum (Ericaceae). New Phytol 180:534–544
Yu J, Li J, Chen H (2009) Diurnal variation of surface wind over central eastern China. Climate Dynam 33:1089–1097
Zhang X, Shi M–M, Shen D-W, Chen X-Y (2012) Habitat loss other than fragmentation per se decreased nuclear and chloroplast genetic diversity in a monoecious tree. PLoS One 7:e39146
Zheng Z (2000) Late Quaternary vegetational and climatic changes in the tropical and subtropical areas of China. Acta Micropalae Sin 17:125–146
Acknowledgments
We appreciate Walter Durka to give constructive suggestions and supply some statistical helps. We thank Naoki Tani and two anonymous reviewers for helpful comments and suggestes and Shuo Yu, Mei-Hua Liu, Dawei Gao, Bang-Quan Gao and Xiao-Yan Wang for helps in sample collection. This work was supported by the National Natural Science Foundation of China (30970430, 30470287) and the Fundamental Research Funds for the Central Universities (78220028).
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Shi, MM., Chen, XY. Leading-edge populations do not show low genetic diversity or high differentiation in a wind-pollinated tree. Popul Ecol 54, 591–600 (2012). https://doi.org/10.1007/s10144-012-0332-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10144-012-0332-7