Abstract
Random genetic drift, natural selection and restricted gene dispersal are basic factors of the spatial genetic structure (SGS) in plant populations. Clonal reproduction has a profound effect on population dynamics and genetic structure and thus emerges as a potential factor in contributing to and modelling SGS. In order to assess the impact of clonality on SGS we studied clonal structure and SGS in the population of Populus alba. Six hundred and seventy-two individuals were mapped and genotyped with 16 nuclear microsatellite markers. To answer the more general question regarding the relationship between SGS and clonality we used Sp statistics, which allows for comparisons of the extent of SGS among different studies, and the comparison of published data on SGS in clonal and non-clonal tree species. Sp statistic was extracted for 14 clonal and 27 non-clonal species belonging to 7 and 18 botanical families, respectively. Results of genetic investigations conducted in the population of P. alba showed over-domination of clonal reproduction, which resulted in very low clonal diversity (R = 0.12). Significant SGS was found at both ramet (Sp = 0.095) and genet level (Sp = 0.05) and clonal reproduction was indicated as an important but not sole driving factor of SGS. Within-population structure, probably due to family structure also contributed to high SGS. High mean dominance index (D = 0.82) indicated low intermingling among genets. Literature survey revealed that clonal tree species significantly differ from non-clonal species with respect to SGS, having 2.8-fold higher SGS. This led us to conclude that clonality is a life-history trait that can have deep impact on processes acting in populations of clonal tree species leading to significant SGS.
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Amat ME, Silvertown J, Vargas P (2013) Strong spatial genetic structure reduces reproductive success in the critically endangered plant genus Pseudomisopates. J Hered 104:692–703. doi:10.1093/jhered/est042
Arnaud-Haond S, Belkhir K (2006) genclone: a computer program to analyse genotypic data, test for clonality and describe spatial clonal organization. Mol Ecol Notes 7:15–17. doi:10.1111/j.1471-8286.2006.01522.x
Balloux F, Lehmann L, Meeûs T (2003) The population genetics of clonal and partially clonal diploids. Genetics 164:1635–1644
Barsoum N, Muller E, Skot L (2004) Variations in levels of clonality among Populus nigra L. stands of different ages. Evol Ecol 18:601–624. doi:10.1007/s10682-004-5146-4
Binks RM, Millar RA, Byrne M (2015) Contrasting patterns of clonality and fine-scale genetic structure in two rare sedges with differing geographic distributions. Heredity. doi:10.1038/hdy.2015.32
Bizoux J-P, Daïnou K, Bourland N et al (2009) Spatial genetic structure in Milicia excelsa (Moraceae) indicates extensive gene dispersal in a low-density wind-pollinated tropical tree. Mol Ecol 18:4398–4408. doi:10.1111/j.1365-294X.2009.04365.x
Brundu G, Lupi R, Zapelli I et al (2008) The origin of clonal diversity and structure of Populus alba in Sardinia: evidence from nuclear and plastid microsatellite markers. Ann Bot 102:997–1006. doi:10.1093/aob/mcn192
Buzatti RS de O, Ribeiro RA, Lemos Filho JP de, Lovato MB (2012) Fine-scale spatial genetic structure of Dalbergia nigra (Fabaceae), a threatened and endemic tree of the Brazilian Atlantic Forest. Genet Mol Biol 35:838–846. doi:10.1590/S1415-47572012005000066
Brzosko E, Wróblewska A, Ratkiewicz M (2002) Spatial genetic structure and clonal diversity of island populations of lady’s slipper (Cypripedium calceolus) from the Biebrza National Park (northeast Poland). Mol Ecol 11:2499–2509. doi:10.1046/j.1365-294X.2002.01630.x
Carrillo-Angeles IG, Mandujano MC, Golubov J (2011) Influences of the genetic neighborhood on ramet reproductive success in a clonal desert cactus. Popul Ecol 53:449–458. doi:10.1007/s10144-010-0254-1
Castiglione S, Cicatelli A, Lupi R et al (2010) Genetic structure and introgression in riparian populations of Populus alba L. Plant Biosys 144:656–668. doi:10.1080/11263504.2010.496188
Cerón-Souza I, Bermingham E, McMillan WO, Jones FA (2012) Comparative genetic structure of two mangrove species in Caribbean and Pacific estuaries of Panama. BMC Evolut Biol 12:205. doi:10.1186/1471-2148-12-205
Chenault N, Arnaud-Haond S, Juteau M et al (2011) SSR-based analysis of clonality, spatial genetic structure and introgression from the Lombardy poplar into a natural population of Populus nigra L. along the Loire River. Tree Gen Genom 7:1249–1262. doi:10.1007/s11295-011-0410-6
Chong C, Edwards W, Pearson R, Waycott M (2013) Sprouting and genetic structure vary with flood disturbance in the tropical riverine paperbark tree, Melaleuca leucadendra (Myrtaceae). Am J Bot 100:2250–2260. doi:10.3732/ajb.1200614
Chung MG, Epperson BK (1999) Spatial genetic structure of clonal and sexual reproduction in populations of Adenophora grandiflora (Campanulaceae). Evolution 53:1068–1078. doi:10.2307/2640812
Chung MY, Suh Y, Lopez-Pujol J, Nason J, Chung MG (2005) Clonal and fine-scale genetic structure in populations of a restricted Korean endemic, Hosta jonesi (Liliaceae) and the implications for conservation. Ann Bot 96:279–288. doi:10.1093/aob/mci176
Chybicki IJ, Burczyk J (2008) Simultaneous estimation of null alleles and inbreeding coefficients. J Hered 100:106–113. doi:10.1093/jhered/esn088
Chybicki IJ, Oleksa A, Burczyk J (2011) Increased inbreeding and strong kinship structure in Taxus baccata estimated from both AFLP and SSR data. Heredity 107:589-600. doi:10.1038/hdy.2011.51
Chybicki IJ, Trojankiewicz M, Oleksa A et al (2009) Isolation-by-distance within naturally established populations of European beech (Fagus sylvatica). Botany 87:791–798. doi:10.1139/B09-049
De Kroons H, Hutchings MJ (1995) Morphological plasticity in clonal plants: the foraging concept reconsidered. J Ecol 83:143. doi:10.2307/2261158
de Witte LC, Stöcklin J (2010) Longevity of clonal plants: why it matters and how to measure it. Ann Bot 106:859–870. doi:10.1093/aob/mcq191
Dent EA, von Holdt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Cons Gen Res 4:359–361. doi:10.1007/s12686-011-9548-7
DeWoody J, Rowe CA, Hipkins VD, Mock KE (2008) “Pando” lives: molecular genetic evidence of a giant aspen clone in central Utah. Western North American Naturalist 68:493–497. doi:10.3398/1527-0904-68.4.493
Dodd RS, Mayer W, Nettel A, Afzal-Rafii Z (2013) Clonal growth and fine-scale genetic structure in Tanoak (Notholithocarpus densiflorus: fagaceae). J Hered 104:105–114. doi:10.1093/jhered/ess080
Dorken ME, Eckert CG (2001) Severely reduced sexual reproduction in northern populations of a clonal plant, Decodon verticillatus (Lythraceae). J Ecol 89:339–350. doi:10.1046/j.1365-2745.2001.00558.x
Doust LL (1981) Population dynamics and local specialization in a clonal Perennial (Ranunculus repens): I. The dynamics of ramets in contrasting habitats. J Ecol 69:743. doi:10.2307/2259633
Dutech C, Sork VL, Irwin AJ et al (2005) Gene flow and fine-scale genetic structure in a wind-pollinated tree species, Quercus lobata (Fagaceaee). Am J Bot 92:252–261. doi:10.3732/ajb.92.2.252
Dumolin S, Demesure B, Petit RJ (1995) Inheritance of chloroplast and mitochondrial genomes in pedunculate oak investigated with an efficient PCR method. Theo Appl Genet 91:1253–1256. doi:10.1007/BF00220937
Earl DA, von Holdt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing Structure output and implementing the Evanno method. Cons Gen Res 4:359–361. doi:10.1007/s12686-011-9548-7
Epperson BK (1992) Spatial structure of genetic variation within populations of forest trees. In: Adams WT, Strauss SH, Copes DL, Griffin AR (eds) Population genetics of forest trees. Springer, Netherlands, pp 257–278
Eriksson O (1989) Seedling dynamics and life histories in clonal plants. Oikos 55:231. doi:10.2307/3565427
Eriksson O (1997) Clonal life histories and the evolution of seed recruitment. In: de Kroon H, van Groenendael J (eds) The ecology and evolution of clonal plants. Backhuys Publishers, Leiden, pp 211–226
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. doi:10.1111/j.1365-294X.2005.02553.x
Fischer M, Kleunen MV (2001) On the evolution of clonal plant life histories. Evol Ecol 15:565–582. doi:10.1023/A:1016013721469
Fussi B, Lexer C, Heinze B (2010) Phylogeography of Populus alba (L.) and Populus tremula (L.) in Central Europe: secondary contact and hybridisation during recolonisation from disconnected refugia. Tree Gen Genom 6:439–450. doi:10.1007/s11295-009-0262-5
García MB, Picó FX, Ehrlén J (2008) Life span correlates with population dynamics in perennial herbaceous plants. Am J Bot 95:258–262. doi:10.3732/ajb.95.2.258
Gilbert KJ, Andrew RL, Bock DG, Franklin M, Kane NC, Moore JS, Moyers BT, Renaut S, Rennison DJ, Veen T, Vines TH (2012) Recommendations for utilizing and reporting population genetic analyses: the reproducibility of genetic clustering using the program Structure. Mol Ecol 21:4925–4930. doi:10.1111/j.1365-294X.2012.05754.x
Hardy OJ, Vekemans X (2002) spagedi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes 2:618–620. doi:10.1046/j.1471-8286.2002.00305.x
Hardy OJ, Maggia L, Bandou E et al (2006) Fine-scale genetic structure and gene dispersal inferences in 10 Neotropical tree species. Mol Ecol 15:559–571. doi:10.1111/j.1365-294X.2005.02785.x
He R, Wang J, Huang H (2012) Long-distance gene dispersal inferred from spatial genetic structure in Handeliodendron bodinieri, an endangered tree from karst forest in southwest China. Biochem Sys Ecol 44:295–302. doi:10.1016/j.bse.2012.06.005
Heuertz M, Vekemans X, Hausman J-F et al (2003) Estimating seed vs. pollen dispersal from spatial genetic structure in the common ash. Mol Ecol 12:2483–2495
Hirao AS (2010) Kinship between parents reduces offspring fitness in a natural population of Rhododendron brachycarpum. Ann Bot 105:637–646. doi:10.1093/aob/mcq018
Hirayama K, Sakimoto M (2008) Clonal structure and diversity of Cryptomeria japonica along a slope in a cool-temperate, old-growth mixed forest in the snowy region of Japan. Can J For Res 38:2804–2813. doi:10.1139/X08-127
Honnay O, Bossuyt B (2005) Prolonged clonal growth: escape route or route to extinction? Oikos 108:427–432. doi:10.1111/j.0030-1299.2005.13569.x
Imbert E, Lefèvre F (2003) Dispersal and gene flow of Populus nigra (Salicaceae) along a dynamic river system. J Ecol 91:447–456. doi:10.1046/j.1365-2745.2003.00772.x
Jelinski DE, Cheliak WM (1992) Genetic Diversity and Spatial Subdivision of Populus tremuloides (Salicaceae) in a Heterogeneous Landscape. Am J Bot 79:728. doi:10.2307/2444937
Jones FA, Hamrick JL, Peterson CJ, Squiers ER (2006) Inferring colonization history from analyses of spatial genetic structure within populations of Pinus strobus and Quercus rubra. Mol Ecol 15:851–861. doi:10.1111/j.1365-294X.2005.02830.x
Jump AS, Rico L, Coll M, Peñuelas J (2012) Wide variation in spatial genetic structure between natural populations of the European beech (Fagus sylvatica) and its implications for SGS comparability. Heredity 108:633–639
Kemperman JA, Barnes BV (1976) Clone size in American aspens. Can J Bot 54:2603–2607. doi:10.1139/b76-280
Kettle CJ, Hollingsworth PM, Burslem DFRP et al (2011) Determinants of fine-scale spatial genetic structure in three co-occurring rain forest canopy trees in Borneo. Persp Plant Ecol Evol Sys 13:47–56. doi:10.1016/j.ppees.2010.11.002
Kimura MK, Kabeya D, Saito T et al (2013) Effects of genetic and environmental factors on clonal reproduction in old-growth natural populations of Cryptomeria japonica. For Ecol Manage 304:10–19. doi:10.1016/j.foreco.2013.04.030
Klimeš L, Klimešowá J, Hendriks B, van Groenendael J (1997) Clonal plant architecture: a comparative analysis of forms and function. In: de Kroon H, van Groenendael J (eds) The ecology and evolution of clonal plants. Backhuys Publishers, Leiden, pp 1–29
Łabendzinski S (1922) Ochrona Przyrody 1922 Rok 03. Państwowa Komisja Ochrony Przyrody
Lasso E, Dalling JW, Bermingham E (2011) Strong spatial genetic structure in five tropical Piper species: should the Baker-Fedorov hypothesis be revived for tropical shrubs? Ecol Evol 1:502–516. doi:10.1002/ece3.40
Lembicz M, Piszczałka P, Grzybowski T et al (2011) Microsatellite identification of ramet genotypes in a clonal plant with phalanx growth: the case of Cirsium rivulare (Asteraceae). Flora 206:792–798. doi:10.1016/j.flora.2011.04.006
Lexer C, Fay MF, Joseph JA et al (2005) Barrier to gene flow between two ecologically divergent Populus species, P. alba (white poplar) and P. tremula (European aspen): the role of ecology and life history in gene introgression. Mol Ecol 14:1045–1057. doi:10.1111/j.1365-294X.2005.02469.x
Loiselle BA, Sork VL, Nason J, Graham C (1995) Spatial genetic structure of a tropical understory Shrub, Psychotria officinalis (Rubiaceae). Am J Bot 82:1420–1425. doi:10.2307/2445869
Louâpre P, Bittebière A-K, Clément B et al (2012) How past and present influence the foraging of clonal plants? PLoS ONE 7:e38288. doi:10.1371/journal.pone.0038288
Macaya-Sanz D, Heuertz M, Lopez-de-Heredia U et al (2012) The Atlantic-Mediterranean watershed, river basins and glacial history shape the genetic structure of Iberian poplars. Mol Ecol 21:3593–3609. doi:10.1111/j.1365-294X.2012.05619.x
Mandák B, Hadincová V, Mahelka V, Wildová R (2013) European Invasion of North American Pinus strobus at Large and Fine Scales: High Genetic Diversity and Fine-Scale Genetic Clustering over Time in the Adventive Range. PLoS One 8:e68514. doi:10.1371/journal.pone.0068514
Mathiasen P, Premoli AC (2013) Fine-scale genetic structure of Nothofagus pumilio (lenga) at contrasting elevations of the altitudinal gradient. Genetica 141:95–105. doi:10.1007/s10709-013-9709-6
Meeus S, Honnay O, Jacquemyn H (2013) Differences in fine-scale spatial genetic structure across the distribution range of the distylous forest herb Pulmonaria officinalis (Boraginaceae). BMC Genet 14:101. doi:10.1186/1471-2156-14-101
Menz MHM, Phillips RD, Dixon KW et al (2013) Mate-searching behaviour of common and rare wasps and the implications for pollen movement of the sexually deceptive orchids they pollinate. PLoS OnE 8:e59111. doi:10.1371/journal.pone.0059111
Mock KE, Rowe CA, Hooten MB et al (2008) Clonal dynamics in western North American aspen (Populus tremuloides). Mol Ecol 17:4827–4844. doi:10.1111/j.1365-294X.2008.03963.x
Nazareno AG, Alzate-Marin AL, Pereira RAS (2013) Dioecy, more than monoecy, affects plant spatial genetic structure: the case study of Ficus. Ecol Evol 3:3495–3508. doi:10.1002/ece3.739
Ndiade-Bourobou D, Hardy OJ, Favreau B et al (2010) Long-distance seed and pollen dispersal inferred from spatial genetic structure in the very low-density rainforest tree, Baillonella toxisperma Pierre, in Central Africa. Mol Ecol 19:4949–4962. doi:10.1111/j.1365-294X.2010.04864.x
Oddou-Muratorio S, Klein EK (2008) Comparing direct vs. indirect estimates of gene flow within a population of a scattered tree species. Mol Ecol 17:2743–2754. doi:10.1111/j.1365-294X.2008.03783.x
Oddou-Muratorio S, Bontemps A, Klein EK et al (2010) Comparison of direct and indirect genetic methods for estimating seed and pollen dispersal in Fagus sylvatica and Fagus crenata. For Ecol Manage 259:2151–2159. doi:10.1016/j.foreco.2010.03.001
Ohsako T (2010) Clonal and spatial genetic structure within populations of a coastal plant, Carex kobomugi (Cyperaceae). Am J Bot 97:458–470. doi:10.3732/ajb.0900262
Pandey M, Gailing O, Hattemer HH, Finkeldey R (2011) Fine-scale spatial genetic structure of sycamore maple (Acer pseudoplatanus L.). Eur J Forest Res 131:739–746. doi:10.1007/s10342-011-0546-9
Pandey M, Rajora OP (2012) Higher fine-scale genetic structure in peripheral than in core populations of a long-lived and mixed-mating conifer - eastern white cedar (Thuja occidentalis L.). BMC Evol Biol 12:48. doi:10.1186/1471-2148-12-48
Pardini EA, Hamrick JL (2008) Inferring recruitment history from spatial genetic structure within populations of the colonizing tree Albizia julibrissin (Fabaceae). Mol Ecol 17:2865–2879. doi:10.1111/j.1365-294X.2008.03807.x
Peakall R, Smouse PE (2006) genalex 6: genetic analysis in excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295. doi:10.1111/j.1471-8286.2005.01155.x
Peterson CHJ, Jones RH (1997) Clonality in woody plants: a review and comparison with clonal herbs. In: Kroon D, van Groenendael J (eds) The ecology and evolution of clonal plants. Backhuys Publishers, Leiden, pp 263–289
Petit RJ, Hampe A (2006) Some evolutionary consequences of being a tree. Annu Rev Ecol Evol Syst 37:187–214. doi:10.1146/annurev.ecolsys.37.091305.110215
Pospíšková M, Šálková I (2006) Population structure and parentage analysis of black poplar along the Morava River. Can J For Res 36:1067–1076. doi:10.1139/x06-003
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Rathmacher G, Niggemann M, Köhnen M et al (2010) Short-distance gene flow in Populus nigra L. accounts for small-scale spatial genetic structures: implications for in situ conservation measures. Conserv Genet 11:1327–1338. doi:10.1007/s10592-009-9961-6
Raymond M, Rousset F (1995) An exact test for population differentiation. Evolution 49:1280. doi:10.2307/2410454
Rousset F (2008) genepop’007: a complete re-implementation of the genepop software for Windows and Linux. Mol Ecol Res 8:103–106. doi:10.1111/j.1471-8286.2007.01931.x
Sant’Anna CS, Sebbenn AM, Klabunde GHF et al (2013) Realized pollen and seed dispersal within a continuous population of the dioecious coniferous Brazilian pine [Araucaria angustifolia (Bertol.) Kuntze]. Conserv Genet 14:601–613. doi:10.1007/s10592-013-0451-5
Santos-del-Blanco L, de-Lucas AI, González-Martínez SC et al (2013) Extensive clonal assemblies in Populus alba and Populus x canescens from the Iberian Peninsula. Tree Gen Genom 9:499–510. doi:10.1007/s11295-012-0574-8
Scholz JB (1896) Vegetationsverhaltnisse des preussischen Weichselgelandes
Schoot J van der, Pospíšková M, Vosman B, Smulders MJM (2000) Development and characterization of microsatellite markers in black poplar (Populus nigra L.). Theor Appl Genet 101:317–322. doi:10.1007/s001220051485
Schueler S, Schlünzen KH (2006) Modeling of oak pollen dispersal on the landscape level with a mesoscale atmospheric model. Environ Model Assess 11:179–194. doi:10.1007/s10666-006-9044-8
Scobie AR, Wilcock CC (2009) Limited mate availability decreases reproductive success of fragmented populations of Linnaea borealis, a rare, clonal self-incompatible plant. Ann Bot. doi:10.1093/aob/mcp007
Scofield DG, Sork VL, Smouse PE (2010) Influence of acorn woodpecker social behaviour on transport of coast live oak (Quercus agrifolia) acorns in a southern California oak savanna. J Ecol 98:561–572. doi:10.1111/j.1365-2745.2010.01649.x
Setsuko S, Ishida K, Tomaru N (2004) Size distribution and genetic structure in relation to clonal growth within a population of Magnolia tomentosa Thunb. (Magnoliaceae). Mol Ecol 13:2645–2653. doi:10.1111/j.1365-294X.2004.02271.x
Silva CRS, Albuquerque PSB, Ervedosa FR et al (2011) Understanding the genetic diversity, spatial genetic structure and mating system at the hierarchical levels of fruits and individuals of a continuous Theobroma cacao population from the Brazilian Amazon. Heredity 106:973–985. doi:10.1038/hdy.2010.145
Silvertown J (2008) The evolutionary maintenance of sexual reproduction: evidence from the ecological distribution of asexual reproduction in clonal plants. Inter J Plant Sci 169:157–168. doi:10.1086/523357
Slavov GT, Leonardi S, Adams WT et al (2010) Population substructure in continuous and fragmented stands of Populus trichocarpa. Heredity 105:348–357. doi:10.1038/hdy.2010.73
Tang S, Li Y, Geng Y, Zhang G, Wang L, Zhong Y (2007) Clonal and spatial genetic structure in natural populations of Luohanguo (Siraitia grosvenorii), an economic species endemic to South China, as revealed by RAPD markers. Biochem Sys Ecol 35:557–565. doi:10.1016/j.bse.2007.03.002
Troupin D, Nathan R, Vendramin GG (2006) Analysis of spatial genetic structure in an expanding Pinus halepensis population reveals development of fine-scale genetic clustering over time. Mol Ecol 15:3617–3630. doi:10.1111/j.1365-294X.2006.03047.x
Tuskan GA, Gunter LE, Yang ZK et al (2004) Characterization of microsatellites revealed by genomic sequencing of Populus trichocarpa. Can J For Res 34:85–93. doi:10.1139/x03-283
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. doi:10.1007/s00606-010-0407-x
Vallejo-Marín M, Dorken ME, Barrett SCH (2010) The ecological and evolutionary consequences of clonality for plant mating. Ann Rev Ecol Evol Syst 41:193–213. doi:10.1146/annurev.ecolsys.110308.120258
Van der Merwe M, Spain CS, Rossetto M (2010) Enhancing the survival and expansion potential of a founder population through clonality. New Phytol 188:868–878. doi:10.1111/j.1469-8137.2010.03396.x
Van Loo M, Joseph JA, Heinze B et al (2008) Clonality and spatial genetic structure in Populus × canescens and its sympatric backcross parent P. alba in a Central European hybrid zone. New Phytol 177:506–516. doi:10.1111/j.1469-8137.2007.02266.x
Vandepitte K, Roldán-Ruiz I, Leus L et al (2009) Canopy closure shapes clonal diversity and fine-scale genetic structure in the dioecious understorey perennial Mercurialis perennis. J Ecol 97:404–414. doi:10.1111/j.1365-2745.2009.01484.x
Vaughan SP, Cottrell JE, Moodley DJ et al (2007) Distribution and fine-scale spatial-genetic structure in British wild cherry (Prunus avium L.). Heredity 98:274–283. doi:10.1038/sj.hdy.6800935
Vekemans X, Hardy OJ (2004) New insights from fine-scale spatial genetic structure analyses in plant populations. Mol Ecol 13:921–935. doi:10.1046/j.1365-294X.2004.02076.x
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. doi:10.1111/j.1365-294X.2011.05293.x
Watkinson AR, Powell JC (1993) seedling recruitment and the maintenance of clonal diversity in plant populations – a computer simulation of Ranununculus repens. J Ecol 81:707–717. doi:10.2307/2261668
Wright S (1943) Isolation by distance. Genetics 28:114–138
Xu L, Yu F-H, Drunen E van, et al (2012) Trampling, defoliation and physiological integration affect growth, morphological and mechanical properties of a root-suckering clonal tree. Ann Bot Mcs 006 doi:10.1093/aob/mcs006
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The authors thank G. Iszkuło for dendrochronological analysis and helpful comments and discussions on the manuscript. We thank also A. Misiorny, M. Ratajczak and M. Litkowiec for their help in field and laboratory works. This project (“SONATA”) was financially supported by National Centre of Science in Poland, project number: 2011/01/D/NZ8/01855.
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Dering, M., Chybicki, I.J. & Rączka, G. Clonality as a driver of spatial genetic structure in populations of clonal tree species. J Plant Res 128, 731–745 (2015). https://doi.org/10.1007/s10265-015-0742-7
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DOI: https://doi.org/10.1007/s10265-015-0742-7