Tree Genetics & Genomes

, 13:18 | Cite as

Genetic diversity of the sweet chestnut (Castanea sativa Mill.) in Central Europe and the western part of the Balkan Peninsula and evidence of marron genotype introgression into wild populations

  • Igor Poljak
  • Marilena Idžojtić
  • Zlatko Šatović
  • Marin Ježić
  • Mirna Ćurković-Perica
  • Bojan Simovski
  • Jane Acevski
  • Zlatko Liber
Original Article
Part of the following topical collections:
  1. Hybridization

Abstract

The sweet chestnut (Castanea sativa Mill.) is a widely spread and important multipurpose tree species in the Mediterranean area, which has played an important role in human history. Natural events, such as glaciations, and human influence played significant roles in the distribution and genetic makeup of the sweet chestnut. In order to better understand how natural and human-mediated past events affected the current genetic diversity and structure of the sweet chestnut, we analysed populations from Central Europe and the western part of the Balkan Peninsula, utilizing ten polymorphic nuclear microsatellite markers. The study revealed the existence of three genetically and, to a large extent, geographically distinct and well-defined groups of sweet chestnut populations. Two not entirely separated groups of populations were detected in the northern part of the studied area and one in the southern. Our results indicate that the genetic structure of sweet chestnut populations in Central Europe and the western part of the Balkan Peninsula is the result of both natural colonization events and significant and lengthy human impact. Furthermore, it has been proven that the gene flow between cultivated/grafted trees’ and wild chestnut stands can influence their genetic structure. However, our results reveal that cultivated-to-wild introgression in the sweet chestnut is dependent on the close proximity of chestnut orchards and naturally occurring populations.

Keywords

Sweet chestnut Genetic variability Population structure Introgression Microsatellites 

Supplementary material

11295_2017_1107_MOESM1_ESM.docx (14 kb)
Table S1Sample size (n) and geographic coordinates for 16 Castanea sativa populations (n = 327) (DOCX 13 kb)
11295_2017_1107_MOESM2_ESM.docx (14 kb)
Table S2Repeat motifs, size ranges, number of alleles (Na) and polymorphic information content (PIC) for ten microsatellite loci used in 15 wild Castanea sativa populations (n = 301) (DOCX 13 kb)
11295_2017_1107_MOESM3_ESM.docx (17 kb)
Table S3Pairwise FST values (lower diagonal) and their significance (upper diagonal) among 15 wild Castanea sativa populations (DOCX 16 kb)
11295_2017_1107_MOESM4_ESM.docx (57 kb)
Table S4Relatedness (r) between ‘Lovran Marron’ and individual trees sampled from 15 wild Castanea sativa populations (DOCX 57 kb)
11295_2017_1107_MOESM5_ESM.docx (29 kb)
Fig. S1Inference of K, the most probable number of clusters, using STRUCTURE software, based on microsatellite analysis of 301 total samples of Castanea sativa (DOCX 29 kb)

References

  1. Belkhir K, Castric V, Bonhomme F (2002) IDENTIX, a software to test for relatedness in a population using permutation methods. Mol Ecol Notes 2:611–614. doi:10.1046/j.1471-8278.2002.00273.x CrossRefGoogle Scholar
  2. Bennett KD, Tzedakis PC, Willis KJ (1991) Quaternary refugia of north European trees. J Biogeogr 18:103–115. doi:10.2307/2845248 CrossRefGoogle Scholar
  3. Beug HJ (1977) Vegetationsgeschichtliche Untersuchungen im Küstenbereich von Istrien (Jugoslawien). Flora 166:357–381Google Scholar
  4. Blouin MS (2003) DNA-based methods for pedigree reconstruction and kinship analysis in natural populations. Trends Ecol Evol 18:503–511. doi:10.1016/S0169-5347(03)00225-8 CrossRefGoogle Scholar
  5. Botstein D, White RL, Sholnick M, David RW (1980) Construction of a genetic linkage map in man using restriction fragment length polymorphisms. Am J Hum Genet 32:314–331PubMedPubMedCentralGoogle Scholar
  6. Botu M (2009) Romania. In: Avanzato D (ed) Following chestnut footprints (Castanea spp.)—cultivation and culture, folklore and history, traditions and use. Scripta Horticult 9:112–116Google Scholar
  7. Bouffier VA, Maurer WD (2009) Germany. In: Avanzato D (ed) Following chestnut footprints (Castanea spp.)—cultivation and culture, folklore and history, traditions and use. Scripta Horticult 9:53–62Google Scholar
  8. Bounous G (2009) Italy. In: Avanzato D (ed) Following chestnut footprints (Castanea spp.)—cultivation and culture, folklore and history, traditions and use. Scripta Horticult 9:72–84Google Scholar
  9. Brande A (1973) Untersuchungen zur postglazialen Vegetationsgeschichte im Gebiet der Neretva-Niederungen (Dalmatien, Herzegowina). Flora 162:1–44Google Scholar
  10. Buck EJ, Hadonou M, James CJ, Blakesley D, Russell K (2003) Isolation and characterization of polymorphic microsatellites in European chestnut (Castanea sativa Mill.). Mol Ecol Notes 3:239–241. doi:10.1046/j.1471-8286.2003.00410.x CrossRefGoogle Scholar
  11. Cavalli-Sforza LL, Edwards AW (1967) Phylogenetic analysis: models and estimation procedures. Evolution 32:550–570CrossRefGoogle Scholar
  12. Chapuis M-P, Estoup A (2007) Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol 24:621–631. doi:10.1093/molbev/msl191 PubMedCrossRefGoogle Scholar
  13. Chumacero de Schawe C, Durka W, Tscharntke T, Hensen I, Kessler M (2013) Gene flow and genetic diversity in cultivated and wild cacao (Theobroma cacao) in Bolivia. Am J Bot 100:2271–2279. doi:10.3732/ajb.1300025 PubMedCrossRefGoogle Scholar
  14. Coart E, Vekemans X, Smulders MJM, Wagner I, van Huylenbroeck J, van Bockstaele E, Roldán-Ruiz I (2003) Genetic variation in the endangered wild apple (Malus sylvestris (L.) Mill.) in Belgium as revealed by amplified fragment length polymorphism and microsatellite markers. Mol Ecol 12:845–857. doi:10.1046/j.1365-294X.2003.01778.x PubMedCrossRefGoogle Scholar
  15. Comps B, Gomory D, Letouzey J, Thiebaut B, Petit RJ (2001) Diverging trends between heterozygosity and allelic richness during postglacial colonization in the European beech. Genetics 157:389–397PubMedPubMedCentralGoogle Scholar
  16. Conedera M, Müller-Starck G, Fineschi S (1994) Genetic characterization of cultivated varieties of European chestnut (Castanea sativa Mill.) in Southern Switzerland. I. Inventory of chestnut varieties: history and perspectives. In: Antognozzi E (ed), Procedings of the International Congress on Chestnut, 20–23 October 1993, Spoleto, Italy, 299–302Google Scholar
  17. Conedera M, Krebs P, Tinner W, Prandella M, Torriani D (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. doi:10.1007/s00334-004-0038-7 CrossRefGoogle Scholar
  18. Cornille A, Giraud T, Bellard C, Tellier A, Le Cam B, Smulders MJ, Kleinschmit J, Roldán-Ruiz I, Gladieux P (2013) Postglacial recolonization history of the European crabapple (Malus sylvestris Mill.), a wild contributor to the domesticated apple. Mol Ecol 22:2249–2263. doi:10.1111/mec.12231 PubMedCrossRefGoogle Scholar
  19. Cornille A, Feurtey A, Gélin U, Ropars J, Misvanderbrugge K, Gladieux P, Giraud T (2015) Anthropogenic and natural drivers of gene flow in a temperate wild fruit tree: a basis for conservation and breeding programs in apples. Evol Appl 8:373–384. doi:10.1111/eva.12250 PubMedPubMedCentralCrossRefGoogle Scholar
  20. Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:1119–1127Google Scholar
  21. Delplancke M, Alvarez N, Espíndola A, Joly H, Benoit L, Brouck E, Arrigo N (2011) Gene flow among wild and domesticated almond species: insights from chloroplast and nuclear markers. Evol Appl 5:317–329. doi:10.1111/j.1752-4571.2011.00223.x PubMedPubMedCentralCrossRefGoogle Scholar
  22. Dempster AP, Laird NM, Rubin DB (1977) Maximum likelihood from incomplete data via the EM algorithm. J Roy Stat Soc B Met 39:1–38Google Scholar
  23. Ehrich D, Gaudeul M, Assefa A, Koch MA, Mummenhoff K, Nemomissa S, Consortium I, Brochmann C (2007) Genetic consequences of Pleistocene range shifts: contrast between the Arctic, the Alps and the East African mountains. Mol Ecol 16:2542–2559. doi:10.1111/j.1365-294X.2007.03299.x PubMedCrossRefGoogle Scholar
  24. Ellstrand NC, Prentice HC, Hancock JF (1999) Gene flow and introgression from domesticated plants into their wild relatives. Annu Rev Ecol Syst 30:539–563. doi:10.1146/annurev.ecolsys.30.1.539 CrossRefGoogle Scholar
  25. 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 PubMedCrossRefGoogle Scholar
  26. Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitocondreal DNA restriction sites. Genetics 131:479–491PubMedPubMedCentralGoogle Scholar
  27. Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50Google Scholar
  28. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791. doi:10.2307/2408678 CrossRefGoogle Scholar
  29. Felsenstein J (1993) Phylip: phylogeny inference package. Computer program. University of Washington, SeattleGoogle Scholar
  30. Fernández-López J, Pereira-Lorenzo S (1993) Index and distribution of chestnut (Castanea sativa Mill.) traditional cultivars in Galicia. Instituto Nacional de Investigación y Technología Agraria y Alimentaria, Madrid, Spain (in Spanish)Google Scholar
  31. Fineschi S, Taurchini D, Villani F, Vendramin GG (2000) Chloroplast DNA polymorphism reveals little geographical structure in Castanea sativa Mill. (Fagaceae) throughout southern European countries. Mol Ecol 9:1495–1503. doi:10.1046/j.1365-294x.2000.01029.x PubMedCrossRefGoogle Scholar
  32. Gassert F, Schulte U, Husemann M, Ulrich W, Rödder D, Hochkirch A, Engel E, Meyer J, Habel JC (2013) From southern refugia to the northern range margin: genetic population structure of the common wall lizard, Podarcis muralis. J Biogeog 40:1475–1489. doi:10.1111/jbi.12109 CrossRefGoogle Scholar
  33. Gobbin D, Hohl L, Conza L, Jermini M, Gessler C, Conedera M (2007) Microsatellite-based characterization of the Castanea sativa cultivar heritage of southern Switzerland. Genome 50:1089–1103. doi:10.1139/G07-086 PubMedCrossRefGoogle Scholar
  34. Gomes-Laranjo J, Peixoto F, Costa R, Ferreira-Cardoso J (2009) Portugal. In: Avanzato D (ed) Following chestnut footprints (Castanea spp.)—cultivation and culture, folklore and history, traditions and use. Scripta Horticult 9:106–111Google Scholar
  35. Goodnight KF, Queller DC (1999) Computer software for performing likelihood tests of pedigree relationship using genetic markers. Mol Ecol 8:1231–1234. doi:10.1046/j.1365-294x.1999.00664.x CrossRefGoogle Scholar
  36. Goudet J (1995) FSTAT (vers. 1.2): a computer program to calculate F-statistics. J Hered 86:485–486CrossRefGoogle Scholar
  37. Goudet J (2002) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3.2). http://www2.unil.ch/popgen/softwares/fstat.htm
  38. Goulão L, Valdiviesso T, Santana C, Moniz Oliveira C (2001) Comparison between phenetic characterization using RAPD and ISSR markers and phenotypic data of cultivated chestnut (Castanea sativa Mill.). Genet Resour Crop Ev 48:329–338. doi:10.1023/A:1012053731052 CrossRefGoogle Scholar
  39. Guo SW, Thompson EA (1992) Performing the exact test of Hardy-Weinberg proportion for multiple alleles. Biometrics 48:361–372PubMedCrossRefGoogle Scholar
  40. 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 PubMedCrossRefGoogle Scholar
  41. Havrdová A, Douda J, Krak K (2015) Higher genetic diversity in recolonized areas than in refugia of Alnus glutinosa triggered by continent-wide lineage admixture. Mol Ecol 18:4759–4777. doi:10.1111/mec.13348 CrossRefGoogle Scholar
  42. Hennion B (2009) France. In: Avanzato D (ed) Following chestnut footprints (Castanea spp.)—cultivation and culture, folklore and history, traditions and use. Scripta Horticult 9:44–47Google Scholar
  43. Heuertz M, Fineschi S, Anzidei M, Pastorelli R, Salvini D, Paule L, Frascaria-Lacoste N, Hardy OJ, Vekemans X, Vendramin GG (2004a) Chloroplast DNA variation and postglacial recolonization of common ash (Fraxinus excelsior L.) in Europe. Mol Ecol 13:3437–3452. doi:10.1111/j.1365-294X.2004.02333.x PubMedCrossRefGoogle Scholar
  44. Heuertz M, Hausman JF, Hardy OJ, Vendramin GG, Frascaria-Lacoste N, Vekemans X (2004b) Nuclear microsatellites reveal contrasting patterns of genetic structure between western and southern European populations of the common ash (Fraxinus excelsior L.). Evolution 58:976–988. doi:10.1111/j.0014-3820.2004.tb00432.x PubMedGoogle Scholar
  45. Heuertz M, Carnevale S, Fineschi S, Sebastiani F, Hausman JF, Paule L, Vendramin GG (2006) Chloroplast DNA phylogeography of European ashes, Fraxinus sp. (Oleaceae): roles of hybridization and life history traits. Mol Ecol 15:2131–2140. doi:10.1111/j.1365-294X.2006.02897.x PubMedCrossRefGoogle Scholar
  46. Hewitt GM (1996) Some genetic consequences of ice ages, and their role in divergence and speciation. Biol J Linn Soc 58:247–276. doi:10.1111/j.1095-8312.1996.tb01434.x CrossRefGoogle Scholar
  47. Hewitt GM (1999) Post-glacial re-colonization of European biota. Biol J Linn Soc 68:87–112. doi:10.1006/bijl.1999.0332 CrossRefGoogle Scholar
  48. Hewitt GM (2000) The genetic legacy of the Quaternary ice ages. Nature 405:907–913. doi:10.1038/35016000 PubMedCrossRefGoogle Scholar
  49. Hewitt GM (2001) Speciation, hybrid zones and phylogeography—or seeing genes in space and time. Mol Ecol 10:537–549. doi:10.1046/j.1365-294x.2001.01202.x PubMedCrossRefGoogle Scholar
  50. Holm S (1979) A simple sequentially rejective multiple test procedure. Scand J Stat 6:65–70. doi:10.2307/4615733 Google Scholar
  51. Huntley B, Birks H (1983) An atlas of past and present pollen maps for Europe: 0–13000 years ago. Cambridge University Press, CambridgeGoogle Scholar
  52. Idžojtić M, Zebec M, Poljak I, Medak J (2009) Variation of sweet chestnut (Castanea sativa Mill.) populations in Croatia according to the morphology of fruits. Sauteria 18:232–333Google Scholar
  53. Idžojtić M, Zebec M, Poljak I, Šatović Z, Liber Z (2012) Analiza genetske raznolikosti “lovranskog maruna” (Castanea sativa Mill.) korištenjem mikrosatelitnih biljega. Sumar List 136(9–10):577–585Google Scholar
  54. Jahns S, van den Bogaard C (1998) New palynological and tephrostratigraphical investigations of two salt lagoons on the island of Mljet, south Dalmatia, Croatia. Veg Hist Archaeobot 7:219–234. doi:10.1007/BF01146195 CrossRefGoogle Scholar
  55. Ježić M, Krstin LJ, Poljak I, Liber Z, Idžojtić M, Jelić M, Meštrović J, Zebec M, Ćurković-Perica M (2014) Castanea sativa: genotype-dependent recovery from chestnut blight. Tree Genet Genomes 10:101–110. doi:10.1007/s11295-013-0667-z CrossRefGoogle Scholar
  56. Johnson GP (1988) Revision of Castanea sect. Balanocastanon (Fagaceae). J Arnold Arboretum 69:25–49Google Scholar
  57. Konovalov DA, Heg D (2008) A maximum-likelihood relatedness estimator allowing for negative relatedness values. Mol Ecol Notes 8:256–263. doi:10.1111/j.1471-8286.2007.01940.x
  58. Konovalov DA, Manning C, Henshaw MT (2004) KINGROUP: a program for pedigree relationship reconstruction and kin group assignments using genetic markers. Mol Ecol Notes 4:779–782. doi:10.1111/j.1471-8286.2004.00796.x CrossRefGoogle Scholar
  59. Krebs P, Conedera M, Pradella M, Torrioni D, Felber M, Tinner W (2004) Quaternary refugia of sweet chestnut (Castanea sativa Mill.): an extended palynological approach. Veg Hist Archaeobot 13:145–160. doi:10.1007/s00334-004-0041-z CrossRefGoogle Scholar
  60. Lang P, Dane F, Kubisiak TL, Huang HW (2007) Molecular evidence for an Asian origin and a unique westward migration of species in the genus Castanea via Europe to North America. Mol Phylogenet Evol 43:49–59. doi:10.1016/j.ympev.2006.07.022 PubMedCrossRefGoogle Scholar
  61. Liepelt S, Cheddadi R, de Beaulieu JL, Fady B, Gömöry D, Hussendörfer D, Konnert M, Litt T, Longauer R, Terhürne-Berson R, Ziegenhagen B (2009) Postglacial range expansion and its genetic imprints in Abies alba (Mill.)—a synthesis from palaeobotanic and genetic data. Rev Palaeobot Palyno 153:139–149. doi:10.1016/j.revpalbo.2008.07.007 CrossRefGoogle Scholar
  62. Liu J (2002) POWERMARKER—a powerful software for marker data analysis. North Carolina State University, Bioinformatics Research Center, RaleighGoogle Scholar
  63. Luikart GF, Allendorf W, Cornuet JM, Sherwin WB (1998) Distortion of allele frequency distributions provides a test for recent population bottlenecks. J Hered 89:238–247. doi:10.1093/jhered/89.3.238 PubMedCrossRefGoogle Scholar
  64. Lusini I, Velichkov I, Pollegioni P, Chiocchini F, Hinkov G, Zlatanov T, Cherubini M, Mattioni C (2014) Estimating the genetic diversity and spatial structure of Bulgarian Castanea sativa populations by SSRs: implications for conservation. Conserv Genet 15:283–293. doi:10.1007/s10592-013-0537-0
  65. Lynch M, Ritland K (1999) Estimation of pairwise relatedness with molecular markers. Genetics 152:1753–1766PubMedPubMedCentralGoogle Scholar
  66. Magri D, Vendramin GG, Comps B, Dupanloup I, Geburek T, Gömöry D, Latałowa M, Litt T, Paule L, Roure JM, Tantau I, van der Knaap WO, Petit R, de Beaulieu JL (2006) A new scenario for the quaternary history of European beech populations: palaeobotanical evidence and genetic consequences. New Phytol 171:199–221. doi:10.1111/j.1469-8137.2006.01740.x PubMedCrossRefGoogle Scholar
  67. Marinoni D, Akkak A, Bounous G, Edwards KJ, Botta R (2003) Development and characterization of microsatellite markers in Castanea sativa Mill. Mol Breeding 11:127–136. doi:10.1023/A:1022456013692 CrossRefGoogle Scholar
  68. Martín MA, Moral A, Martín LM, Alvarez JB (2007) The genetic resources of European sweet chestnut (Castanea sativa Miller) in Andalusia, Spain. Genet Resour Crop Evol 54:379–387. doi:10.1007/s10722-005-5969-z CrossRefGoogle Scholar
  69. Martín MA, Alvarez JB, Mattioni C, Cherubini M, Villani F, Martín LM (2009) Identification and characterisation of traditional chestnut varieties of southern Spain using morphological and simple sequence repeats (SSRs) markers. Ann Appl Biol 154:389–398. doi:10.1111/j.1744-7348.2008.00309.x CrossRefGoogle Scholar
  70. Martín MA, Mattioni C, Cherubini M, Taurchini D, Villani F (2010a) Genetic diversity in European chestnut populations by means of genomic and genic microsatellite markers. Tree Genet Genomes 6:735–744. doi:10.1007/s11295-010-0287-9
  71. Martín MA, Alvarez JB, Martín LM, Mattioni C, Cherubini M, Villani F, Ruiz JC (2010b) Traditional chestnut cultivars in southern Spain: a case of endangered genetic resources. Acta Hortic 866:143–150. doi:10.17660/ActaHortic.2010.866.15 CrossRefGoogle Scholar
  72. Martín MA, Mattioni C, Cherubini M, Taurchini D, Villani F (2010c) Genetic characterization of traditional chestnut varieties in Italy using microsatellites (simple sequence repeats). Ann Appl Biol 157:37–44. doi:10.1111/j.1744-7348.2010.00407.x CrossRefGoogle Scholar
  73. Martín MA, Mattioni C, Molina JR, Alvarez JB, Cherubini M, Herrera MA, Villani F, Martín LM (2012) Landscape genetic structure of chestnut (Castanea sativa Mill.) in Spain. Tree Genet Genomes 8:127–136. doi:10.1007/s11295-011-0427-x CrossRefGoogle Scholar
  74. Martín MA, Mattioni C, Cherubini M, Villani F, Martín LM (2016) A comparative study of European chestnut varieties in relation to adaptive markers. Agroforest Syst. doi:10.1007/s10457-016-9911-5 Google Scholar
  75. Mattioni C, Cherubini M, Micheli E, Villani F, Bucci G (2008) Role of domestication in shaping Castanea sativa genetic variation in Europe. Tree Genet Genomes 4:563–574. doi:10.1007/s11295-008-0132-6 CrossRefGoogle Scholar
  76. Mattioni C, Martín MA, Pollegioni P, Cherubini M, Villani F (2013) Microsatellite markers reveal a strong geographical structure in European populations of Castanea sativa (Fagaceae): evidence for multiple glacial refugia. Am J Bot 100:951–961. doi:10.3732/ajb.1200194 PubMedCrossRefGoogle Scholar
  77. Medak J, Idžojtić M, Novak-Agbaba S, Ćurković-Perica M, Mujić I, Poljak I, Juretić D, Prgomet Ž (2009) Croatia. In: Avanzato D (ed) Following chestnut footprints (Castanea spp.)—cultivation and culture, folklore and history, traditions and use. Scripta Horticult 9:40–43Google Scholar
  78. Milligan BG (2003) Maximum-likelihood estimation of relatedness. Genetics 163:1153–1167PubMedPubMedCentralGoogle Scholar
  79. O’Connor K, Powell M, Nock C, Shapcott A (2015) Crop to wild gene flow and genetic diversity in a vulnerable Macadamia (Proteaceae) species in New South Wales, Australia. Biol Conserv 191:504–511. doi:10.1016/j.biocon.2015.08.001 CrossRefGoogle Scholar
  80. Pamilo P (1990) Comparison of relatedness estimators. Evolution 44:1378–1382CrossRefGoogle Scholar
  81. Pascual M, Aquadro CF, Soto V, Serra L (2001) Microsatellite variation in colonizing and palearctic populations of Drosophila suboscura. Mol Biol Evol 18:731–740. doi:10.1093/oxfordjournals.molbev.a003855 PubMedCrossRefGoogle Scholar
  82. Pereira-Lorenzo S, Fernandez-Lopez J, Moreno-Gonzalez J (1996) Variability and grouping of northwestern Spanish chestnut cultivars. II. Isoenzymatic traits. J Am Soc Hortic Sci 121:190–197Google Scholar
  83. Pereira-Lorenzo S, Ramos-Cabrer AM, Díaz-Hernández B, Ascasíbar-Errasti J, Sau F, Ciordia-Ara M (2001a) Spanish chestnut cultivars. Hortic Sci 36:344–347Google Scholar
  84. Pereira-Lorenzo S, Ríos D, González-Pérez J, Cubas F, Perdomo A, Calzadilla C, Ramos-Cabrer AM (2001b) Chestnut cultivars on the Canary Islands. For Snow Landsc Res 76:445–450Google Scholar
  85. Pereira-Lorenzo S, Díaz-Hernández MB, Ramos-Cabrer AM (2006) Use of highly discriminating morphological characters and isozymes in the study of Spanish chestnut cultivars. J Am Soc Hortic Sci 131:770–779Google Scholar
  86. Pereira-Lorenzo S, Díaz-Hernández MB, Ramos-Cabrer AM (2009) Spain. In: Avanzato D (ed) Following chestnut footprints (Castanea spp.)—cultivation and culture, folklore and history, traditions and use. Scripta Horticult 9:134–141Google Scholar
  87. Pereira-Lorenzo S, Lourenço Costa RM, Ramos-Cabrer AM, Marques Ribeiro CA, Serra da Silva MF, Manzano G, Barreneche T (2010) Variation in grafted European chestnut and hybrids by microsatellites reveals two main origins in the Iberian Peninsula. Tree Genet Genomes 6:701–715. doi:10.1007/s11295-010-0285-y CrossRefGoogle Scholar
  88. Petit RJ, Brewer S, Bordács S, Burg K, Cheddadi R, Coart E, Cottrell J, Csaikl UM, van Dam B, Deans JD, Espinel S, Fineschi S, Finkeldey R, Glaz I, Goicoechea PG, Jensen JS, König AO, Lowe AJ, Madsen SF, Mátyás G, Munro RC, Popescu F, Slade D, Tabbener H, de Vries SGM, Ziegenhagen B, de Beaulieu JL, Kremer A (2002) Identification of refugia and post-glacial colonisation routes of European white oaks based on chloroplast DNA and fossil pollen evidence. Forest Ecol Manag 156:49–74. doi:10.1016/S0378-1127(01)00634-x CrossRefGoogle Scholar
  89. Petit RJ, Aguinagalde I, de Beaulieu JL (2003) Glacial refugia: hotspots but not meltingpots of genetic diversity. Science 300:1563–1565. doi:10.1126/science.1083264 PubMedCrossRefGoogle Scholar
  90. Piry S, Luikart G, Cornuet JM (1999) BOTTLENECK: a computer programme for detecting recent reductions in the effective population size using allele frequency data. J Hered 90:502–503. doi:10.1093/jhered/90.4.502 CrossRefGoogle Scholar
  91. Poljak I (2014) Morphological and genetic diversity of populations and chemical composition of fruits of European sweet chestnut (Castanea sativa Mill.) in Croatia. Dissertation, Faculty of Forestry, University of Zagreb (in Croatian)Google Scholar
  92. Poljak I, Vahčić N, Gačić M, Idžojtić M (2016) Morphological characterization and chemical composition of fruits of the traditional Croatian chestnut variety ‘Lovran Marron’. Food Technol Biotechnol 54:189–199. doi:10.17113/ftb.54.02.16.4319 PubMedPubMedCentralCrossRefGoogle Scholar
  93. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedPubMedCentralGoogle Scholar
  94. Queller DC, Goodnight KF (1989) Estimating relatedness using genetic markers. Evolution 43:258–275CrossRefGoogle Scholar
  95. Ramos-Cabrer AM, Pereira-Lorenzo S (2005) Genetic relationship between Castanea sativa Mill. trees from North-western to South Spain based on morphological traits and isoenzymes. Genet Resour Crop Ev 52:879–890. doi:10.1007/s10722-003-6094-5 CrossRefGoogle Scholar
  96. Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249CrossRefGoogle Scholar
  97. Rice WR (1989) Analysing tables of statistical tests. Evolution 43:223–225. doi:10.2307/2409177 CrossRefGoogle Scholar
  98. SAS Institute (2004) SAS/STAT® 9.1 user’s guide. SAS Institute Inc., Cary, NCGoogle Scholar
  99. Schmidt R, Müller J, Drescher-Schneider R, Krisai R, Szeroczynska K, Barić A (2000) Changes in lake level and trophy at Lake Vrane, a large karstic lake on the Island of Cres (Croatia), with respect to paleoclimate and anthropogenic impacts during the last approx. 16,000 years. J Limnol 2:113–130. doi:10.4081/jlimnol.2000.113 CrossRefGoogle Scholar
  100. Soylu A, Serdar Ü, Ertan E, Mert C (2009) Turkey. In: Avanzato D (ed) Following chestnut footprints (Castanea spp.)—cultivation and culture, folklore and history, traditions and use. Scripta Horticult 9:155–160Google Scholar
  101. Sučić J (1953) O arealu pitomog kestena (Castanea sativa Mill.) na području Srebrenice, sa kratkim osvrtom na ostala nalazišta kestena u NR BiH. Institut za naučna šumarska istraživanja u Sarajevu, SarajevoGoogle Scholar
  102. Šoštarić R, Küster H (2001) Roman plant remains from Veli Brijun (island of Brioni), Croatia. Veg Hist Archaeobot 10:227–233. doi:10.1007/PL00006934 CrossRefGoogle Scholar
  103. Taberlet P, Fumagalli L, Wust-Saucy AG, Cosson JF (1998) Comparative phylogeography and postglacial colonization routes in Europe. Mol Ecol 7:453–464. doi:10.1046/j.1365-294x.1998.00289.x PubMedCrossRefGoogle Scholar
  104. Temunović M, Franjić J, Šatović Z, Grgurev M, Frascaria-Lacoste N, Fernández-Manjarrés JF (2012) Environmental heterogeneity explains the genetic structure of continental and Mediterranean populations of Fraxinus angustifolia Vahl. PLoS One 7:e42764. doi:10.1371/journal.pone.0042764 PubMedPubMedCentralCrossRefGoogle Scholar
  105. Temunović M, Frascaria-Lacoste N, Franjić J, Šatović Z, Fernández-Manjarrés JF (2013) Identifying refugia from climate change using coupled ecological and genetic data in a transitional Mediterranean-temperate tree species. Mol Ecol 22:2128–2142. doi:10.1111/mec.12252 PubMedCrossRefGoogle Scholar
  106. Torello Marinoni D, Akkak A, Beltramo C, Guaraldo P, Boccacci P, Bounous G, Ferrara AM, Ebone A, Viotto E, Botta R (2013) Genetic and morphological characterization of chestnut (Castanea sativa Mill.) germplasm in Piedmont (north-western Italy). Tree Genet Genomes 9:1017–1030. doi:10.1007/s11295-013-0613-0 CrossRefGoogle Scholar
  107. 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. doi:10.1111/j.1471-8286.2004.00684.x CrossRefGoogle Scholar
  108. van Zeist W, Bottema S (1991) Late Quaternary vegetation of the Near East. Reichert L, WiesbadenGoogle Scholar
  109. van Zeist W, Woldring H, Stapert D (1975) Late quaternary vegetation and climate of southwestern Turkey. Palaeohistoria 17:53–143Google Scholar
  110. Villani F, Pigliucci M, Benedettelli S, Cherubini M (1991) Genetic differentiation among Turkish chestnut (Castanea sativa Mill.) populations. Heredity 66:131–136. doi:10.1038/hdy.1991.16 CrossRefGoogle Scholar
  111. Villani F, Pigliucci M, Lauteri M, Cherubini M (1992) Congruence between genetic, morphometric, and physiological data on differentiation of Turkish chestnut (Castanea sativa). Genome 35:251–256. doi:10.1139/g92-038 CrossRefGoogle Scholar
  112. Villani F, Pigliucci M, Cherubini M (1994) Evolution of Castanea sativa Mill. in Turkey and Europe. Genet Res 63:109–116. doi:10.1017/S0016672300032213 CrossRefGoogle Scholar
  113. Villani F, Ansotta AS, Cherubini M, Cesaroni D, Sbordoni V (1999) Genetic structure of natural populations of Castanea sativa in Turkey: evidence of a hybrid zone. J Evolution Biol 12:233–244. doi:10.1046/j.1420-9101.1999.00033.x CrossRefGoogle Scholar
  114. Wang JL (2002) An estimator for pairwise relatedness using molecular markers. Genetics 160:1203–1215PubMedPubMedCentralGoogle Scholar
  115. Wolf DE, Takebayashi N, Rieseberg LH (2001) Predicting the risk of extinction through hybridization. Conserv Biol 15:1039–1053. doi:10.1046/j.1523-1739.2001.0150041039.x CrossRefGoogle Scholar
  116. Zeller Z (2013) History of the Nagymaros chestnut groves. In: Radócz L (ed) Chestnut cultivation and revitalization program in Nagymaros. Debrecen University, Hungary, pp 13–18Google Scholar
  117. Zeller Z, Bürgés G (2013) Environmental role and value of the Nagymaros chestnut groves. In: Radócz L (ed) Chestnut cultivation and revitalization program in Nagymaros. Debrecen University, Hungary, pp 19–23Google Scholar
  118. Zohary D, Hopf M (1988) Domestication of plants in the Old World. Oxford University Press, New YorkGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  1. 1.Department of Forest Genetics, Dendrology and Botany, Faculty of ForestryUniversity of ZagrebZagrebCroatia
  2. 2.Department for Seed Science and Technology, Faculty of AgricultureUniversity of ZagrebZagrebCroatia
  3. 3.Centre of Excellence for Biodiversity and Molecular Plant BreedingZagrebCroatia
  4. 4.Department of Biology, Faculty of ScienceUniversity of ZagrebZagrebCroatia
  5. 5.Department of Botany and Dendrology, Faculty of ForestrySs. Cyril and Methodius University in SkopjeSkopjeMacedonia

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