Abstract
Sweet chestnut is a tree of great economic (fruit and wood production), ecological, and cultural importance in Europe. A large-scale landscape genetic analysis of natural populations of sweet chestnut across Europe is applied to (1) evaluate the geographic patterns of genetic diversity, (2) identify spatial coincidences between genetic discontinuities and geographic barriers, and (3) propose certain chestnut populations as reservoirs of genetic diversity for conservation and breeding programs. Six polymorphic microsatellite markers were used for genotyping 1608 wild trees sampled in 73 European sites. The Geostatistical IDW technique (ArcGIS 9.3) was used to produce maps of genetic diversity parameters (He, Ar, PAr) and a synthetic map of the population membership (Q value) to the different gene pools. Genetic barriers were investigated using BARRIER 2.2 software and their locations were overlaid on a Digital Elevation Model (GTOPO30). The DIVA-GIS software was used to propose priority areas for conservation. High values of genetic diversity (He) and allelic richness (Ar) were observed in the central area of C. sativa’s European distribution range. The highest values of private allelic richness (PAr) were found in the eastern area. Three main gene pools and a significant genetic barrier separating the eastern from the central and western populations were identified. Areas with high priority for genetic conservation were indicated in Georgia, eastern Turkey, and Italy. Our results increase knowledge of the biogeographic history of C. sativa in Europe, indicate the geographic location of different gene pools, and identify potential priority reservoirs of genetic diversity.
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Anderson CD, Epperson BK, Fortin MJ (2010) Considering spatial and temporal scale in landscape-genetic studies of gene flow. Mol Ecol 19:3565–3575
Bagnoli F, Vendramin GG, Buonamici A et al (2009) Is Cupressus sempervirens native in Italy? An answer from genetic and paleobotanical data. Mol Ecol 18:2276–2286
Bagnoli F, Tsuda Y, Fineschi S et al (2016) Combining molecular and fossil data to infer demographic history of Quercus cerris: insights on European eastern glacial refugia. J Biogeogr 43:679–690
Barreneche T, Casasoli M, Roussel G et al (2004) Comparative mapping between Quercus and Castanea using simple sequence repeats (SSRs). Theor Appl Genet 108:558–556
Beatty GE, Provan J (2012) Post-glacial dispersal, rather than in site glacial survival, best explains the disjunct distribution of the Lusitanian plant species Daboeacia cantabrica (Ericaceae). Jof Biogeogr 40:335–344
Bowman J, Greenhorn JE, Marrotte R.R, McKay MM, Morris KY, Mrentice MB, Wehtje M (2016) On application of landscape genetics. Conserv Genet18 March on line
Buck EJ, Russel K, Hadonou M, James CJ, Blakesley D, Russell K (2003) Isolation and characterization of polymorphic microsatellite in European chestnut (Castanea sativa mill.). Mol Ecol Notes 3:239–241
Butchart S, Walpole M, Collen B, Strien VA (2010) Global biodiversity: indicators of recent declines. Science 328:164–1168
Cadima X, van Zonneveld M, Scheldeman X et al (2014) Endemic wild potato (Solanum spp) biodiversity status in Bolivia: reasons for conservation concerns. J Nat Conserv 22:113–131
Chapius MP, Estoup A (2007) Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol 24:621–631
Comps B, Gomory D, Letouzey J, Thiebaut B, Petit RJ (2001) Diverging trends between heterozygosity and allelic richness during postglacial colonization in european beech. Genetics 157:389–397
Conedera M, Krebs P, Tinner W, Prandella M, Torrani T (2004) The cultivation of Castanea sativa (mill.) in Europe, from its origin to its diffusion on a continental scale. Veg Hist Archaeobot 13:161–179
Cox B, Moore P (2005) Biogeography: an ecological and evolutionary approach. Wiley, Chichester
Earl DA, von Holdt BM (2012) Structure Harvester: a website and program for visualizing structure output and implementing the Evanno method. ConsGenet Res 4:359–361
Eckert CG, Samis E, 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) High level of genetic differentiation for allelic richness among populations of argan tree [Argania spinose (L.) Skeels] endemic to Morocco. Theor Appl Genet 92:832–839
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, Smouese PE, Quattro JM (1992) Analysis of molecular variance 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 (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinformatics Online 1:47–50
Falush D, Stephens M, Pritchard JK (2007) Inference of population structure using multilocus genotype data: dominant markers and null alleles. Mol Ecol Notes 7:574–578
Felsenstein J (2005) PHYLIP (phylogeny inference package). Seattle, Department of Genome Sciences, University of Washington
Fischer J, Lindenmayer DB (2007) Landscape modification and habitat fragmentation: a synthesis. Global Ecol Biogeogr 16:265–280
Gomez-Sanz V, Blanco-Andray A, Sánchez-Palomares O et al (2002) Autoecología de los castañares andaluces. Investigation Agraria Sistemas y Recursos forestales 11:205–226
Grivet D, Petit RJ (2003) Chloroplast DNA phylogeography of hornbeam in Europe: evidence for a bottleneck at the outset of glacial colonization. Conserv Genet 4:47–56
Hengl T (2009) A practical guide to geostatistical mapping. University of Amsterdam, Amsterdam
Hewitt GM (2000) The genetic legacy of the quaternary ice age. Nature 405:907–913
Holderegger R, Buehler D, Gugerli F, Manel S (2010) Landscape genetics of plants. Trends Plant Sci 15:675–683
Hubisz MJ, Falush D, Stephen M, Pritchard JK (2009) Inferring weak population structure with the assistance of sample group information. Mol Ecol Res 9:1322–1332
Huntley B, Birks HJB (1983) An atlas of past and present pollen maps for Europe: 0–13,000 years ago. CUP, Cambridge
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
Jezic M, Krstin L, Poljak I et al (2014) Castanea sativa: genotype-dependent recovery from chestnut blight. Tree Genet Genomes 10:101–110
Kalinowski ST (2004) Counting alleles with rarefaction: private alleles and hierarchical sampling design. Conserv Genet 5:539–543
Kalinowski ST (2005) HP-rare: a computer program for performing rarefaction on measures of allelic diversity. Mol Ecol Notes 5:187–189
Keller D, Holderegger R, van Strien MJ, Bolliger J (2015) How to make landscape genetics beneficial for conservation management? Conserv Genet 16:503–512
Krebs P, Conedera M, Prandella D, Torrioni D, Felber M, Tinner W (2004) Quaternary refugia of sweet chestnut (Castanea sativa mill.): an extended palynological approach. Veget Hist and Archaeob 13:145–160
Latta RG (2006) Integrating patterns across multiple genetic markers to infer spatial processes. Landscape Ecol 21:809–820
Lusini I, Velichkov I, Pollegioni P et al (2014) Estimating the genetic diversity and spatial structure of Bulgarian Castanea sativa populations by SSRs: implication for conservation. Conserv Genet 15:283–293
Manel S, Holderegger R (2013) Ten years of landscape genetics. Trends Ecol Evol 10:614–621
Manel S, Schwartz MK, Luikhart G, Taberlet P (2003) Landscape genetics: combining landscape ecology and population genetics. Trends Ecol and Evol 18:189–197
Manni F, Guerard E, Heyer E (2004) Geographic patterns of (genetic, morphologic, and linguistic) variation: how barriers can be detected by using Monmonier’s algorithm. Hum Biol 76:173–190
Marinoni D, Akkak A, Bonus G, Edwards KJ, Botta R (2003) Development and characterization of microsatellite markers in Castanea sativa (mill.). Mol Breeding 11:127–136
Martin MA, Mattioni C, Molina JR et al (2012) Landscape genetic structure of chestnut (Castanea sativa mill.) in Spain. Tree Genet Genomes 8:127–136
Martin MA, Mattioni C, Lusini I et al (2014) New insights into the genetic structure of Araucaria araucana forests based on molecular and historic evidences. Tree Genet Genomes 10:839–851
Mattioni C, Martin MA, Pollegioni P, Cherubini M, Villani F (2013) Microsatellite markers reveals a strong geographical structure in European populations of Castanea sativa (Fagaceae): evidence for multiple glacial refugia. Am J Bot 100:1–11
Mayol M, Riba M, Gonzalez-Martinez SC et al (2015) Adapting through glacial cycles: insights from a long-lived tree (Taxus baccata). New Phytol 208:973–986
Nei M (1973) Analysis of gene diversity in subdivided populations. P Natl Acad Sci USA 70:3321–3323
Nei M, Roychoudhry AK (1974) Sampling variance of heterozygosity and genetic distance. Genetics 76:379–390
Paetkau D, Waits LP, Clarkson PL, Craighead L, Vyse E, Ward R, Strobeck C (1998) Variation in genetic diversity across the range of North American Brown Bears. Conserv Biol 12(2):418–429
Peakall R, Smouse PE (2005) GeneAlex6: genetic analysis in excel. Population genetic software for teaching and research. Australian National University, Canberra, Australia http://anu.edu.au/BoZo/GenAl Ex/
Petit RJ, Mousadik EA, Pons O (1998) Identifying populations for conservation on the basis of genetic markers. Conserv Biol 12:844–855
Petit RJ, Aguinagalde I, de Beaulieu JL et al (2003) Glacial refugia: hotspotsbut not melting pots of genetic diversity. Science 300:1563–1565
Phillips J, Kyratzis A, Christoudoulou C, Kell S, Maxted N (2014) Development of a national crop wild relative conservation strategy for Cyprus. Genet Resour Crop Evol 61:817–827
Pollegioni P, Woeste K, Chiocchini F et al (2014) Landscape genetics of Persian walnut (Juglans regia L.) across its Asian range. Tree Genet Genomes 10:1027–1043
Pollegioni P, Woeste KE, Chiocchini F et al (2015) Ancient humans influenced the current spatial genetic structure of common walnut populations in Asia. PLoS One 10:e0135980. doi:10.1371/journal.pone.0135980
Pritchard JK, Wen W (2004) Documentation for STRUCTURE software version 2.3.4. Department of Human Genetics. University of Chicago, Chicago IIlinois USA Available at http://pritch.bsd.uchicago.edu
Provan J, Bennet KD (2008) Phylogeographic insights into criptic glacial refugia. Trends Ecol Evol 23:564–571
Rambaut, A. (2011) “FigTree, version 1.3. 1.” Computer program distributed by the author, website: http://treebioedac.uk/software/figtree/ [accessed Jan. 4.]
Rands MRW, Adams WM, Bennun L et al (2010) Biodiversity conservation: challenges beyond. Science 329:1298–1303
Rebelo AG, Siegfried WR (1992) Where should nature reserves be located in the cape floristic region, South Africa? Models for the spatial configuration of a reserve network aimed at maximizing the protection of floral diversity. Conserv Biol 6:243–252
Rosenberg NA (2004) Distruct: a program for the graphical display of population structure. Mol Ecol Not 4:137–138
Scheldeman X, van Zonneveld M (2010) Training manual on spatial analysis of plant diversity and distribution. Biodiversity International, Rome, Italy
Shepard D (1968) A two-dimensional interpolation function for irregularly-spaced data. In: Blue RBS, Rosenberg AM (eds) Proceedings of the 1968 ACM National Conference. ACM Press, New York, pp 517–524
Sneath PHA, Sokal RR (1973) The estimation of taxonomic resemblance. In: Kennedy D, Park RB (eds) Numerical taxonomy. The principles and practice of numerical classification. Freeman, San Francisco, pp 129–132.
Sork VL, Aitken SN, Dyer RJ, Eckert AJ, Legendre P, Neale DB (2013) Putting the landscape into the genomics of trees: approaches for understanding local adaptation and population responses to changing climate. Tree Genet Genomes 9:901–911
Souto C, Mathiasen P, Acosta M (2015) Identifying genetic hotspots by mapping molecular diversity of widespread trees: when commonness matters. J Hered 106:537–545
Squatriti P (2013) Landscape and change in early medieval Italy: chestnut, economy and culture, 1st edn. Cambridge University Press, Cambridge
Storfer A, Murphy MA, Evans JS et al (2007) Putting the ‘landscape’ in landscape genetics. Heredity 98:128–142
Storfer A, Murphy MA, Spear SF, Holderegger R, Waits LP (2010) Landscape genetics: where are we now? Mol Ecol 19:3496–3514
Takezaki N, Nei M, Tamura K (2010) POPTREE2: software for constructing population trees from allele frequency data and computing other population statistics with windows interface. Mol Biol Evol 27:747–752
van Zonneveld M, Scheldeman X, Escribano P (2012) Mapping genetic diversity of cherimoya (Annona cherimola mill.): application of spatial analysis for conservation and use of plant genetic resources. PLoS One 7:1–14
Vannini A, Natili G, Anselmi N, Mantaghi A, Vettraini AM (2010) Distribution and gradient analysis of ink disease in chestnut forests. Forest Pathol 40:73–86
Villani F, Sansotta A, Cherubini M, Cesaroni D, Sbordoni V (1999) Genetic structure of natural populations of Castanea sativa in Turkey: evidence of a hybrid zone. Journal Evolution Biol 12:233–244
Vinceti B, Loo J, Gaisberger H et al (2013) Conservation priorities for Prunus africana defined with the aid of spatial analysis of genetic data and climatic variables. PLoS One 8(3):e 59987. doi:10.1371/journal.pone.0059987
Widmer A, Lexer C (2001) Glacial refugia: sanctuaries for allelic richness, but not for gene diversity. Trends Ecol Evol 16:267–269
Acknowledgements
The authors would like to thank Dr. I. Beritognolo and Dr. D. Postolache for their critical review of the manuscript. Thanks are due to all the people who collected chestnut samples, especially Dr. P. Aravanopoulos, Dr. R. Botta, M. Akhalkatsi, Z. Manvelidze, V.D. Leiba, M.D. Pinkovskij, A.V. Romanishin, and O. Ibadlo for providing us the leaf samples from northern Italy, Greece, Georgia, Russia, and Azerbaijan, respectively. M.A. Martín is grateful to the Secretaría General de Ciencia, Tecnología e Innovación de la Consejería de Economía e Infraestructuras, from the Regional Government of Extremadura (Spain) for the financial support.
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Inference of K, the most probable number of clusters, using the software STRUCTURE. Second order of change of the log-likehood of the data (ΔK) as a function of K, calculated over six replicates (TIFF 2118 kb)
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Mattioni, C., Martin, M.A., Chiocchini, F. et al. Landscape genetics structure of European sweet chestnut (Castanea sativa Mill): indications for conservation priorities. Tree Genetics & Genomes 13, 39 (2017). https://doi.org/10.1007/s11295-017-1123-2
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DOI: https://doi.org/10.1007/s11295-017-1123-2