Forest genomics in the Caucasus through the lens of its dominant tree species - Fagus orientalis.

Caucasus demographic history genetic diversity genetic structure genomic landscape trees whole‐genome sequencing

Journal

Molecular ecology

ISSN: 1365-294X

Titre abrégé: Mol Ecol

Pays: England

ID NLM: 9214478

Informations de publication

Date de publication:
17 Jul 2024

Historique:

revised: 29 05 2024

received: 11 01 2024

accepted: 14 06 2024

medline: 18 7 2024

pubmed: 18 7 2024

entrez: 18 7 2024

Statut: aheadofprint

Résumé

The last glacial period is known to have greatly influenced the demographic history of temperate forest trees, with important range contractions and post-glacial expansions that led to the formation of multiple genetic lineages and secondary contact zones in the Northern Hemisphere. These dynamics have been extensively studied for European and North American species but are still poorly understood in other temperate regions of rich biodiversity such as the Caucasus. Our study helps filling that gap by deciphering the genomic landscapes of F. orientalis across the South Caucasus. The use of genome-wide data confirmed a past demographic history strongly influenced by the Last Glacial Maximum, revealing two disjunct glacial refugia in the Colchis and Hyrcanian regions. The resulting patterns of genetic diversity, load and differentiation are not always concordant across the region, with genetic load pinpointing the location of the glacial refugia more efficiently than genetic diversity alone. The Hyrcanian forests show depleted genetic diversity and substantial isolation, even if long-distance gene flow is still present with the main centre of diversity in the Greater Caucasus. Finally, we characterize a strong heterogeneity of genetic diversity and differentiation along the species chromosomes, with noticeably a first chromosome showing low diversity and weak differentiation.

Identifiants

DOI: 10.1111/mec.17475 PMID: 39021282

pubmed: 39021282

doi: 10.1111/mec.17475

doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

Pagination

e17475

Subventions

Organisme : National Science Centre of Poland

ID : 2017/26/E/NZ8/01049

Organisme : Institute of Dendrology

Organisme : Polish Academy of Sciences

Organisme : Poznań University of Life Sciences

Organisme : Poznan Supercomputing and Networking Center

ID : 456

Informations de copyright

Références

Aitken, S. N., & Bemmels, J. B. (2016). Time to get moving: Assisted gene flow of forest trees. Evolutionary Applications, 9, 271–290.

Alberto, F. J., Aitken, S. N., Alía, R., González‐Martínez, S. C., Hänninen, H., Kremer, A., Lefèvre, F., Lenormand, T., Yeaman, S., Whetten, R., & Savolainen, O. (2013). Potential for evolutionary responses to climate change – evidence from tree populations. Global Change Biology, 19, 1645–1661.

Alipour, S., Yousefzadeh, H., Badehian, Z., Asadi, F., Espahbodi, K., & Dering, M. (2021). Genetic diversity and structure of the endemic and critically endangered Populus caspica in the Hyrcanian forests. Tree Genetics & Genomes, 17, 19.

April, J., Hanner, R. H., Dion‐Côté, A.‐M., & Bernatchez, L. (2013). Glacial cycles as an allopatric speciation pump in north‐eastern American freshwater fishes. Molecular Ecology, 22, 409–422.

Barrett, R. D. H., & Schluter, D. (2008). Adaptation from standing genetic variation. Trends in Ecology & Evolution, 23, 38–44.

Belmonte, J., Alarcón, M., Avila, A., Scialabba, E., & Pino, D. (2008). Long‐range transport of beech (Fagus sylvatica L.) pollen to Catalonia (north‐eastern Spain). International Journal of Biometeorology, 52, 675–687.

Bennett, A. K. D., Tzedakis, P. C., & Willis, K. J. (2008). Quaternary refugia of North European trees (Vol. 18, pp. 103–115). Blackwell Publishing. http://www.jstor.org/stable/2845248

Beridze, B., Sękiewicz, K., Walas, Ł., Thomas, P. A., Danelia, I., Fazaliyev, V., Kvartskhava, G., Sós, J., & Dering, M. (2023). Biodiversity protection against anthropogenic climate change: Conservation prioritization of Castanea sativa in the South Caucasus based on genetic and ecological metrics. Ecology and Evolution, 13, e10068.

Beridze, B., Sękiewicz, K., Walas, Ł., Thomas, P. A., Danelia, I., Kvartskhava, G., Fazaliyev, V., Bruch, A. A., & Dering, M. (2023). Evolutionary history of Castanea sativa Mill. in the Caucasus driven by middle and late pleistocene paleoenvironmental changes. AoB Plants, 15(5), plad059.

Bolger, A. M., Lohse, M., & Usadel, B. (2014). Trimmomatic: A flexible trimmer for Illumina sequence data. Bioinformatics, 30, 2114–2120.

Brandies, P., & Hogg, B. (2019). The value of reference genomes in the conservation of threatened species. Genes, 10, 846.

Butler, J. B., Freeman, J. S., Potts, B. M., Vaillancourt, R. E., Kahrood, H. V., Ades, P. K., Rigault, P., & Tibbits, J. F. G. (2022). Patterns of genomic diversity and linkage disequilibrium across the disjunct range of the Australian forest tree Eucalyptus globulus. Tree Genetics & Genomes, 18, 28.

Ćalić, I., Koch, J., Carey, D., Addo‐Quaye, C., Carlson, J. E., & Neale, D. B. (2017). Genome‐wide association study identifies a major gene for beech bark disease resistance in American beech (Fagus grandifolia Ehrh.). BMC Genomics, 18, 547.

Capblancq, T., Butnor, J. R., Deyoung, S., Thibault, E., Munson, H., Nelson, D. M., Fitzpatrick, M. C., & Keller, S. R. (2020). Whole‐exome sequencing reveals a long‐term decline in effective population size of red spruce (Picea rubens). Evolutionary Applications, 13, 2190–2205.

Capblancq, T., Morin, X., Gueguen, M., Renaud, J., Lobreaux, S., & Bazin, E. (2020). Climate‐associated genetic variation in Fagus sylvatica and potential responses to climate change in the French Alps. Journal of Evolutionary Biology, 33, 783–796.

Capblancq, T., Munson, H., Butnor, J. R., & Keller, S. R. (2021). Genomic drivers of early‐life fitness in Picea rubens. Conservation Genetics, 22, 963–976.

Chen, J., Li, L., Milesi, P., Jansson, G., Berlin, M., Karlsson, B., Aleksic, J., Vendramin, G. G., & Lascoux, M. (2019). Genomic data provide new insights on the demographic history and the extent of recent material transfers in Norway spruce. Evolutionary Applications, 12, 1539–1551.

Christe, C., Kozlowski, G., Frey, D., Bétrisey, S., Maharramova, E., Garfì, G., Pirintsos, S., & Naciri, Y. (2014). Footprints of past intensive diversification and structuring in the genus Zelkova (Ulmaceae) in south‐western Eurasia (P Linder, Ed.). Journal of Biogeography, 41, 1081–1093.

Cingolani, P., Platts, A., Wang, L. L., Coon, M., Nguyen, T., Wang, L., Land, S. J., Lu, X., & Ruden, D. M. (2012). A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff. Fly, 6, 80–92.

Csilléry, K., Lalagüe, H., Vendramin, G. G., González‐Martínez, S. C., Fady, B., & Oddou‐Muratorio, S. (2014). Detecting short spatial scale local adaptation and epistatic selection in climate‐related candidate genes in European beech (Fagus sylvatica) populations. Molecular Ecology, 23, 4696–4708.

Dagtekin, D., Şahan, E. A., Denk, T., Köse, N., & Dalfes, H. N. (2020). Past, present and future distributions of oriental beech (Fagus orientalis) under climate change projections. PLoS One, 15, e0242280.

Dering, M., Baranowska, M., Beridze, B., Chybicki, I. J., Danelia, I., Iszkuło, G., Kvartskhava, G., Kosiński, P., Rączka, G., Thomas, P. A., Tomaszewski, D., Walas, Ł., & Sękiewicz, K. (2021). The evolutionary heritage and ecological uniqueness of Scots pine in the Caucasus ecoregion is at risk of climate changes. Scientific Reports, 11, 22845.

Dering, M., Kosiński, P., Wyka, T. P., Pers‐Kamczyc, E., Boratyński, A., Boratyńska, K., Reich, P. B., Romo, A., Zadworny, M., Żytkowiak, R., & Oleksyn, J. (2017). Tertiary remnants and Holocene colonizers: Genetic structure and phylogeography of Scots pine reveal higher genetic diversity in young boreal than in relict Mediterranean populations and a dual colonization of Fennoscandia. Diversity and Distributions, 23, 540–555.

Dussex, N., Morales, H. E., Grossen, C., Dalén, L., & Van Oosterhout, C. (2023). Purging and accumulation of genetic load in conservation. Trends in Ecology & Evolution, 38, 961–969.

Ekhvaia, J., Simeone, M. C., Silakadze, N., & Abdaladze, O. (2018). Morphological diversity and phylogeography of the Georgian durmast oak (Q. petraea subsp. iberica) and related Caucasian oak species in Georgia (South Caucasus). Tree Genetics & Genomes, 14, 17.

Erichsen, E. O., Budde, K. B., Sagheb‐Talebi, K., Bagnoli, F., Vendramin, G. G., & Hansen, O. K. (2018). Hyrcanian forests—Stable rear‐edge populations harbouring high genetic diversity of Fraxinus excelsior, a common European tree species. Diversity and Distributions, 24, 1521–1533.

Excoffier, L., Dupanloup, I., Huerta‐Sánchez, E., Sousa, V. C., & Foll, M. (2013). Robust demographic inference from genomic and SNP data. PLoS Genetics, 9, e1003905.

Fady, B., Esposito, E., Abulaila, K., Aleksic, J. M., Alia, R., Alizoti, P., Apostol, E.‐N., Aravanopoulos, P., Ballian, D., Kharrat, M. B. D., Carrasquinho, I., Albassatneh, M. C., Curtu, A. L., David‐Schwartz, R., de Dato, G., Douaihy, B., Eliades, N. G. H., Fresta, L., Gaouar, S. B. S., … Westergren, M. (2022). Forest genetics research in the Mediterranean basin: Bibliometric analysis, knowledge gaps, and perspectives. Current Forestry Reports, 8, 277–298.

Fernández‐López, J., Fernández‐Cruz, J., & Míguez‐Soto, B. (2021). The demographic history of Castanea sativa Mill. in southwest Europe: A natural population structure modified by translocations. Molecular Ecology, 30, 3930–3947.

Forester, B. R., Landguth, E. L., Hand, B. K., & Balkenhol, N. (2021). Landscape genomics for wildlife research. In P. A. Hohenlohe & O. P. Rajora (Eds.), Population genomics: Wildlife (pp. 145–184). Springer International Publishing.

Formenti, G., Theissinger, K., Fernandes, C., Bista, I., Bombarely, A., Bleidorn, C., Ciofi, C., Crottini, A., Godoy, J. A., Höglund, J., Malukiewicz, J., Mouton, A., Oomen, R. A., Paez, S., Palsbøll, P. J., Pampoulie, C., Ruiz‐López, M. J., Svardal, H., Theofanopoulou, C., … Zammit, G. (2022). The era of reference genomes in conservation genomics. Trends in Ecology & Evolution, 37, 197–202.

Fox, E. A., Wright, A. E., Fumagalli, M., & Vieira, F. G. (2019). ngsLD: Evaluating linkage disequilibrium using genotype likelihoods. Bioinformatics, 35, 3855–3856.

Frankham, R., Ballou, J. D., & Briscoe, D. A. (2010). Introduction to conservation genetics. Cambridge University Press.

Frankham, R., Bradshaw, C. J. A., & Brook, B. W. (2014). Genetics in conservation management: Revised recommendations for the 50/500 rules, Red List criteria and population viability analyses. Biological Conservation, 170, 56–63.

Franks, S. J., & Hoffmann, A. A. (2012). Genetics of climate change adaptation. Annual Review of Genetics, 46, 185–208.

Gholizadeh, H., Naqinezhad, A., & Chytrý, M. (2020). Classification of the Hyrcanian forest vegetation, northern Iran. Applied Vegetation Science, 23, 107–126.

González‐Martínez, S. C., Ridout, K., & Pannell, J. R. (2017). Range expansion compromises adaptive evolution in an outcrossing plant. Current Biology, 27, 2544–2551.e4.

Guo, J., Wang, B., Liu, Z., Mao, J., Wang, X., & Zhao, W. (2023). Low genetic diversity and population connectivity fuel vulnerability to climate change for the tertiary relict pine Pinus bungeana. Journal of Systematics and Evolution, 61, 143–156.

Heuertz, M., De Paoli, E., Källman, T., Larsson, H., Jurman, I., Morgante, M., Lascoux, M., & Gyllenstrand, N. (2006). Multilocus patterns of nucleotide diversity, linkage disequilibrium and demographic history of Norway spruce [Picea abies (L.) Karst]. Genetics, 174, 2095–2105.

Heuertz, M., Hausman, J.‐F., Hardy, O. J., Vendramin, G. G., Frascaria‐Lacoste, N., & Vekemans, X. (2004). Nuclear microsatellites reveal contrasting patterns of genetic structure between western and Southeastern European populations of the common ash (Fraxinus excelsior L.). Evolution, 58, 976–988.

Hewitt, G. (2000). The genetic legacy of the quaternary ice ages. Nature, 405, 907–913.

Hoban, S., Kallow, S., & Trivedi, C. (2018). Implementing a new approach to effective conservation of genetic diversity, with ash (Fraxinus excelsior) in the UK as a case study. Biological Conservation, 225, 10–21.

Hoban, S., Paz‐Vinas, I., Aitken, S., Bertola, L. D., Breed, M. F., Bruford, M. W., Funk, W. C., Grueber, C. E., Heuertz, M., Hohenlohe, P., Hunter, M. E., Jaffé, R., Fernandes, M. L., Mergeay, J., Moharrek, F., O'Brien, D., Segelbacher, G., Vernesi, C., Waits, L., & Laikre, L. (2021). Effective population size remains a suitable, pragmatic indicator of genetic diversity for all species, including forest trees. Biological Conservation, 253, 108906.

Hoban, S. M., Hauffe, H. C., Pérez‐Espona, S., Bertorelle, G., Frith, K., Galbusera, P., Hoelzel, A. R., Nichols, R., Primmer, C., Siegismund, H. R., Sihvonen, M., Vernesi, C., Vilà, C., the ConGRESS Consortium, & Bruford, M. W. (2013). How to bring genetic diversity to the forefront of conservation policy and management. Conservation Genetics Resources, 5, 593–598.

Hoffmann, A. A., & Sgró, C. M. (2011). Climate change and evolutionary adaptation. Nature, 470, 479–485.

Holliday, J. A., Aitken, S. N., Cooke, J. E. K., Fady, B., Gonz Alez‐Martinez, S. C., Heuertz, M., Jaramillo‐Correa, J. P., Lexer, C., Staton, M., Whetten, R. W., & Plomion, C. (2017). Advances in ecological genomics in forest trees and applications to genetic resources conservation and breeding. Molecular Ecology, 26, 706–717.

IPCC. (2023). Climate change 2022 – Impacts, adaptation and vulnerability: Working group II contribution to the sixth assessment report of the intergovernmental panel on climate change. Cambridge University Press.

Janfaza, S., Yousefzadeh, H., Hosseini Nasr, S. M., Botta, R., Asadi Abkenar, A., & Marinoni, D. T. (2017). Genetic diversity of Castanea sativa an endangered species in the Hyrcanian forest. Silva Fennica, 51, 1705.

Jaramillo‐Correa, J. P., Verdú, M., & González‐Martínez, S. C. (2010). The contribution of recombination to heterozygosity differs among plant evolutionary lineages and life‐forms. BMC Evolutionary Biology, 10, 22.

Jiang, L., Bao, Q., He, W., Fan, D., Cheng, S., López‐Pujol, J., Chung, M. G., Sakaguchi, S., Sánchez‐González, A., Gedik, A., Li, D.‐Z., Kou, Y.‐X., & Zhang, Z.‐Y. (2022). Phylogeny and biogeography of Fagus (Fagaceae) based on 28 nuclear single/low‐copy loci. Journal of Systematics and Evolution, 60, 759–772.

Khalatbari Limaki, M., Es‐hagh Nimvari, M., Alavi, S. J., Mataji, A., & Kazemnezhad, F. (2021). Potential elevation shift of oriental beech (Fagus orientalis L.) in Hyrcanian mixed forest ecoregion under future global warming. Ecological Modelling, 455, 109637.

Kim, S., Plagnol, V., Hu, T. T., Toomajian, C., Clark, R. M., Ossowski, S., Ecker, J. R., Weigel, D., & Nordborg, M. (2007). Recombination and linkage disequilibrium in Arabidopsis thaliana. Nature Genetics, 39, 1151–1155.

Kirkpatrick, M., & Jarne, P. (2000). The effects of a bottleneck on inbreeding depression and the genetic load. The American Naturalist, 155, 154–166.

Korneliussen, T. S., Albrechtsen, A., & Nielsen, R. (2014). ANGSD: Analysis of next generation sequencing data. BMC Bioinformatics, 15, 356–368.

Korneliussen, T. S., Moltke, I., Albrechtsen, A., & Nielsen, R. (2013). Calculation of Tajima's D and other neutrality test statistics from low depth next‐generation sequencing data. BMC Bioinformatics, 14, 289.

Kurz, M., Kölz, A., Gorges, J., Pablo Carmona, B., Brang, P., Vitasse, Y., Kohler, M., Rezzonico, F., Smits, T. H. M., Bauhus, J., Rudow, A., Kim Hansen, O., Vatanparast, M., Sevik, H., Zhelev, P., Gömöry, D., Paule, L., Sperisen, C., & Csilléry, K. (2023). Tracing the origin of oriental beech stands across Western Europe and reporting hybridization with European beech – Implications for assisted gene flow. Forest Ecology and Management, 531, 120801.

Lai, Y. T., Yeung, C. K. L., Omland, K. E., Pang, E. L., Hao, Y., Liao, B. Y., Cao, H. F., Zhang, B. W., Yeh, C. F., Hung, C. M., Hung, H. Y., Yang, M. Y., Liang, W., Hsu, Y. C., Yao, C. T., Dong, L., Lin, K., & Li, S. H. (2019). Standing genetic variation as the predominant source for adaptation of a songbird. Proceedings of the National Academy of Sciences of the United States of America, 116, 2152–2157.

Larsson, H., Källman, T., Gyllenstrand, N., & Lascoux, M. (2013). Distribution of long‐range linkage disequilibrium and Tajima's D values in Scandinavian populations of Norway spruce (Picea abies). G3: Genes, Genomes, Genetics, 3, 795–806.

Levsen, N. D., Tiffin, P., & Olson, M. S. (2012). Pleistocene speciation in the genus Populus (Salicaceae). Systematic Biology, 61, 401–412.

Li, H. (2011). Improving SNP discovery by base alignment quality. Bioinformatics, 27, 1157–1158.

Li, H., & Durbin, R. (2009). Fast and accurate long‐read alignment with Burrows‐Wheeler transform. Bioinformatics, 25, 1754–1760.

Li, H., Handsaker, B., Wysoker, A., Fennell, T., Ruan, J., Homer, N., Marth, G., Abecasis, G., & Durbin, R. (2009). The sequence alignment/map format and SAMtools. Bioinformatics, 25, 2078–2079.

Lin, Y.‐C., Wang, J., Delhomme, N., Schiffthaler, B., Sundström, G., Zuccolo, A., Nystedt, B., Hvidsten, T. R., De La Torre, A., Cossu, R. M., Hoeppner, M. P., Lantz, H., Scofield, D. G., Zamani, N., Johansson, A., Mannapperuma, C., Robinson, K. M., Mähler, N., Leitch, I. J., … Va, Y. (2018). Functional and evolutionary genomic inferences in Populus through genome and population sequencing of American and European aspen. Proceedings of the National Academy of Sciences of the United States of America, 115, E10970–E10978.

Liu, X., & Fu, Y. X. (2015). Exploring population size changes using SNP frequency spectra. Nature Genetics, 47, 555–559.

Lumibao, C. Y., Hoban, S. M., & McLachlan, J. (2017). Ice ages leave genetic diversity ‘hotspots’ in Europe but not in Eastern North America. Ecology Letters, 20, 1459–1468.

Maharramova, E., Huseynova, I., Kolbaia, S., Gruenstaeudl, M., Borsch, T., & Muller, L. A. H. (2018). Phylogeography and population genetics of the riparian relict tree Pterocarya fraxinifolia (Juglandaceae) in the South Caucasus. Systematics and Biodiversity, 16, 14–27.

Mahler, S., Shatilova, I., & Bruch, A. A. (2022). Neogene long‐term trends in climate of the Colchic vegetation refuge in Western Georgia – Uplift versus global cooling. Review of Palaeobotany and Palynology, 296, 104546.

Mattioni, C., Martin, M. A., 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. American Journal of Botany, 100, 951–961.

Mayol, M., Riba, M., González‐Martínez, S. C., Bagnoli, F., De Beaulieu, J., Berganzo, E., Burgarella, C., Dubreuil, M., Krajmerová, D., Paule, L., & Romšáková, I. (2015). Adapting through glacial cycles: Insights from a long‐lived tree (Taxus baccata). New Phytologist, 208, 973–986.

Meisner, J., & Albrechtsen, A. (2018). Inferring population structure and admixture proportions in low‐depth NGS data. Genetics, 210, 719–731.

Mishra, B., Ulaszewski, B., Meger, J., Aury, J.‐M., Bodénès, C., Lesur‐Kupin, I., Pfenninger, M., Da Silva, C., Gupta, D. K., Guichoux, E., Heer, K., Lalanne, C., Labadie, K., Opgenoorth, L., Ploch, S., Le Provost, G., Salse, J., Scotti, I., Wötzel, S., … Thines, M. (2022). A chromosome‐level genome assembly of the European beech (Fagus sylvatica) reveals anomalies for organelle DNA integration, repeat content and distribution of SNPs. Frontiers in Genetics, 12, 691058.

Mitka, J., Wróblewska, A., Boroń, P., Kucharzyk, S., & Stachurska‐Swakoń, A. (2023). Perhaps there were northern refugia in LGM? The phylogeographic structure of the thermophilic tree Carpinus betulus in the Carpathian region. Science of the Total Environment, 905, 167214.

Mittermeier, R. A., Turner, W. R., Larsen, F. W., Brooks, T. M., & Gascon, C. (2011). Global biodiversity conservation: The critical role of hotspots. In F. E. Zachos & J. C. Habel (Eds.), Biodiversity hotspots: Distribution and protection of conservation priority areas (pp. 3–22). Springer Berlin Heidelberg.

Mosca, E., Cruz, F., Gómez‐Garrido, J., Bianco, L., Rellstab, C., Brodbeck, S., Csilléry, K., Fady, B., Fladung, M., Fussi, B., Gömöry, D., González‐Martínez, S. C., Grivet, D., Gut, M., Hansen, O. K., Heer, K., Kaya, Z., Krutovsky, K. V., Kersten, B., … Neale, D. B. (2019). A reference genome sequence for the European silver fir (Abies alba Mill.): A community‐generated genomic resource. G3: Genes, Genomes, Genetics, 9, 2039–2049.

Myburg, A. A., Grattapaglia, D., Tuskan, G. A., Hellsten, U., Hayes, R. D., Grimwood, J., Jenkins, J., Lindquist, E., Tice, H., Bauer, D., Goodstein, D. M., Dubchak, I., Poliakov, A., Mizrachi, E., Kullan, A. R. K., Hussey, S. G., Pinard, D., van der Merwe, K., Singh, P., … Schmutz, J. (2014). The genome of Eucalyptus grandis. Nature, 510, 356–362.

Myers, N., Mittermeier, R. A., Mittermeier, C. G., Da Fonseca, G. A. B., & Kent, J. (2000). Biodiversity hotspots for conservation priorities. Nature, 403, 853–858.

Myles, S., Chia, J. M., Hurwitz, B., Simon, C., Zhong, G. Y., Buckler, E., & Ware, D. (2010). Rapid genomic characterization of the genus Vitis. PLoS One, 5, e8219.

Nakhutsrishvili, G. (2012). The vegetation of Georgia (South Caucasus). Springer Science & Business Media.

Nakhutsrishvili, G., & Abdaladze, O. (2017). Plant diversity of the central great Caucasus. In G. Nakhutsrishvili, O. Abdaladze, K. Batsatsashvili, E. Spehn, & C. Körner (Eds.), Plant diversity in the central great Caucasus: A quantitative assessment (pp. 17–111). Springer International Publishing.

Nakhutsrishvili, G., Zazanashvili, N., Batsatsashvili, K., & Montalvo Mancheno, C. S. (2015). Colchic and Hyrcanian forests of the Caucasus: Similarities, differences and conservation status. Flora Mediterranea, 25, 185–192.

Nakhutsrishvili, G. S. (1998). The vegetation of the Subnival Belt of the Caucasus Mountains. Arctic and Alpine Research, 30, 222.

Neale, D. B., Wegrzyn, J. L., Stevens, K. A., Zimin, A. V., Puiu, D., Crepeau, M. W., Cardeno, C., Koriabine, M., Holtz‐Morris, A. E., Liechty, J. D., Martínez‐García, P. J., Vasquez‐Gross, H. A., Lin, B. Y., Zieve, J. J., Dougherty, W. M., Fuentes‐Soriano, S., Wu, L. S., Gilbert, D., Marçais, G., … Langley, C. H. (2014). Decoding the massive genome of loblolly pine using haploid DNA and novel assembly strategies. Genome Biology, 15, R59.

Nei, M. (1987). Molecular evolutionary genetics. Columbia University Press.

Nevado, B., Contreras‐Ortiz, N., Hughes, C., & Filatov, D. A. (2018). Pleistocene glacial cycles drive isolation, gene flow and speciation in the high‐elevation Andes. New Phytologist, 219, 779–793.

Nieto, F. G. (2014). Patterns and processes in plant phylogeography in the Mediterranean Basin. A review. Perspectives in Plant Ecology, Evolution and Systematics, 16, 265–278.

Nikolaishvili, D. (2015). Anthropogenic changes of Caucasus forest landscapes. Earth Science, 4, 54.

Nocchi, G., Brown, N., Coker, T. L. R., Plumb, W. J., Stocks, J. J., Denman, S., & Buggs, R. J. A. (2022). Genomic structure and diversity of oak populations in British parklands. Plants, People, Planet, 4, 167–181.

Nosil, P., Funk, D. J., & Ortiz‐Barrientos, D. (2009). Divergent selection and heterogeneous genomic divergence. Molecular Ecology, 18, 375–402.

Nystedt, B., Street, N. R., Wetterbom, A., Zuccolo, A., Lin, Y.‐C., Scofield, D. G., Vezzi, F., Delhomme, N., Giacomello, S., Alexeyenko, A., Vicedomini, R., Sahlin, K., Sherwood, E., Elfstrand, M., Gramzow, L., Holmberg, K., Hällman, J., Keech, O., Klasson, L., … Jansson, S. (2013). The Norway spruce genome sequence and conifer genome evolution. Nature, 497, 579–584.

Parducci, L., Jørgensen, T., Tollefsrud, M. M., Elverland, E., Alm, T., Fontana, S. L., Bennett, K. D., Haile, J., Matetovici, I., Suyama, Y., Edwards, M. E., Andersen, K., Rasmussen, M., Boessenkool, S., Coissac, E., Brochmann, C., Taberlet, P., Houmark‐Nielsen, M., Larsen, N. K., … Willerslev, E. (2012). Glacial survival of boreal trees in northern Scandinavia. Science, 335, 1083–1086.

Pavy, N., Namroud, M. C., Gagnon, F., Isabel, N., & Bousquet, J. (2012). The heterogeneous levels of linkage disequilibrium in white spruce genes and comparative analysis with other conifers. Heredity, 108, 273–284.

Peischl, S., Dupanloup, I., Kirkpatrick, M., & Excoffier, L. (2013). On the accumulation of deleterious mutations during range expansions. Molecular Ecology, 22, 5972–5982.

Peischl, S., Kirkpatrick, M., & Excoffier, L. (2015). Expansion load and the evolutionary dynamics of a species range. American Naturalist, 185, E81–E93.

Petit, J., Aguinagalde, I., Beaulieu, J. D., Bittkau, C., Brewer, S., Cheddadi, R., Ennos, R., Fineschi, S., Grivet, D., Lascoux, M., Mohanty, A., Müller‐Starck, G., Demesure‐Musch, B., Palmé, A., Martín, J. P., Rendell, S., & Vendramin, G. G. (2003). Glacial refugia: Hotspots but not melting pots of genetic diversity. Science, 300, 1563–1565.

Petit, R. J., & Hampe, A. (2006). Some evolutionary consequences of being a tree. Annual Review of Ecology, Evolution, and Systematics, 37, 187–214.

Plomion, C., Aury, J.‐M., Amselem, J., Leroy, T., Murat, F., Duplessis, S., Faye, S., Francillonne, N., Labadie, K., Le Provost, G., Lesur, I., Bartholomé, J., Faivre‐Rampant, P., Kohler, A., Leplé, J.‐C., Chantret, N., Chen, J., Diévart, A., Alaeitabar, T., … Salse, J. (2018). Oak genome reveals facets of long lifespan. Nature Plants, 4, 440–452.

Pollegioni, P., Woeste, K. E., Chiocchini, F., Olimpieri, I., Tortolano, V., Clark, J., Hemery, G. E., Mapelli, S., & Malvolti, M. E. (2014). Landscape genetics of Persian walnut (Juglans regia L.) across its Asian range. Tree Genetics & Genomes, 10, 1027–1043.

Potter, K. M., Jetton, R. M., Bower, A., Jacobs, D. F., Man, G., Hipkins, V. D., & Westwood, M. (2017). Banking on the future: Progress, challenges and opportunities for the genetic conservation of forest trees. New Forests, 48, 153–180.

Prakash, A., Capblancq, T., Shallows, K., Saville, D., Landau, D., Landress, C., Jacobs, T., & Keller, S. (2024). Bringing genomics to the field: An integrative approach to seed sourcing for forest restoration. Applications in Plant Sciences, 12, e11600.

Presgraves, D. C. (2018). Evaluating genomic signatures of “the large X‐effect” during complex speciation. Molecular Ecology, 27, 3822–3830.

Provan, J. (2013). The effects of past, present and future climate change on range‐wide genetic diversity in northern North Atlantic marine species. Frontiers of Biogeography, 5, 60–66.

Provan, J., & Bennett, K. (2008). Phylogeographic insights into cryptic glacial refugia. Trends in Ecology & Evolution, 23, 564–571.

R Core Team. (2020). R: A Language and Environment for Statistical Computing.

Rougemont, Q., Moore, J.‐S., Leroy, T., Normandeau, E., Rondeau, E. B., Withler, R. E., Van Doornik, D. M., Crane, P. A., Naish, K. A., Garza, J. C., Beacham, T. D., Koop, B. F., & Bernatchez, L. (2020). Demographic history shaped geographical patterns of deleterious mutation load in a broadly distributed Pacific Salmon. PLoS Genetics, 16, e1008348.

Rubel, E. A. (1914). The forests of the Western Caucasus. The Journal of Ecology, 2, 39.

Sawyer, S. L., Mukherjee, N., Pakstis, A. J., Feuk, L., Kidd, J. R., Brookes, A. J., & Kidd, K. K. (2005). Linkage disequilibrium patterns vary substantially among populations. European Journal of Human Genetics, 13, 677–686.

Scotti‐Saintagne, C., Boivin, T., Suez, M., Musch, B., Scotti, I., & Fady, B. (2021). Signature of mid‐Pleistocene lineages in the European silver fir (Abies alba Mill.) at its geographic distribution margin. Ecology and Evolution, 11, 10984–10999.

Sękiewicz, K., Danelia, I., Farzaliyev, V., Gholizadeh, H., Iszkuło, G., Naqinezhad, A., Ramezani, E., Thomas, P. A., Tomaszewski, D., Walas, Ł., & Dering, M. (2022). Past climatic refugia and landscape resistance explain spatial genetic structure in oriental beech in the South Caucasus. Ecology and Evolution, 12, e9320.

Skotte, L., Korneliussen, T. S., & Albrechtsen, A. (2013). Estimating individual admixture proportions from next generation sequencing data. Genetics, 195, 693–702.

Sollars, E. S. A., Harper, A. L., Kelly, L. J., Sambles, C. M., Ramirez‐Gonzalez, R. H., Swarbreck, D., Kaithakottil, G., Cooper, E. D., Uauy, C., Havlickova, L., Worswick, G., Studholme, D. J., Zohren, J., Salmon, D. L., Clavijo, B. J., Li, Y., He, Z., Fellgett, A., McKinney, L. V., … Buggs, R. J. A. (2017). Genome sequence and genetic diversity of European ash trees. Nature, 541, 212–216.

Stewart, J. R., Lister, A. M., Barnes, I., & Dalén, L. (2010). Refugia revisited: Individualistic responses of species in space and time. Proceedings of the Royal Society B: Biological Sciences, 277, 661–671.

Taberlet, P., Fumagalli, L., Wust‐Saucy, A.‐G., & Cosson, J.‐F. (1998). Comparative phylogeography and postglacial colonization routes in Europe. Molecular Ecology, 7, 453–464.

Tajima, F. (1983). Evolutionary relationship of DNA sequences in finite populations. Genetics, 105, 437–460.

Tajima, F. (1989). Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics, 123, 585–595.

Tarasov, A., Vilella, A. J., Cuppen, E., Nijman, I. J., & Prins, P. (2017). Genome analysis Sambamba: Fast processing of NGS alignment formats. Bioinformatics, 31, 2032–2034.

Tarkhnishvili, D., Gavashelishvili, A., & Mumladze, L. (2012). Palaeoclimatic models help to understand current distribution of Caucasian forest species: Modeling west asian forest refugia. Biological Journal of the Linnean Society, 105, 231–248.

Tollefsrud, M. M., Myking, T., Sønstebø, J. H., Lygis, V., Hietala, A. M., & Heuertz, M. (2016). Genetic structure in the northern range margins of common ash, Fraxinus excelsior L. PLoS One, 11, e0167104.

Tuskan, G. A., DiFazio, S., Jansson, S., Bohlmann, J., Grigoriev, I., Hellsten, U., Putnam, N., Ralph, S., Rombauts, S., Salamov, A., Schein, J., Sterck, L., Aerts, A., Bhalerao, R. R., Bhalerao, R. P., Blaudez, D., Boerjan, W., Brun, A., Brunner, A., … Rokhsar, D. (2006). The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science, 313, 1596–1604.

Tzedakis, P. C., Emerson, B. C., & Hewitt, G. M. (2013). Cryptic or mystic? Glacial tree refugia in northern Europe. Trends in Ecology & Evolution, 28, 696–704.

Wagner, S., Collet, C., Madsen, P., Nakashizuka, T., Nyland, R. D., & Sagheb‐Talebi, K. (2010). Beech regeneration research: From ecological to silvicultural aspects. Forest Ecology and Management, 259, 2172–2182.

Wahlsteen, E., Avramidou, E. V., Bozic, G., Mediouni, R. M., Schuldt, B., & Sobolewska, H. (2023). Continental‐wide population genetics and post‐Pleistocene range expansion in field maple (Acer campestre L.), a subdominant temperate broadleaved tree species. Tree Genetics & Genomes, 19, 15.

Warren, R. L., Keeling, C. I., Yuen, M. M. S., Raymond, A., Taylor, G. A., Vandervalk, B. P., Mohamadi, H., Paulino, D., Chiu, R., Jackman, S. D., Robertson, G., Yang, C., Boyle, B., Hoffmann, M., Weigel, D., Nelson, D. R., Ritland, C., Isabel, N., Jaquish, B., … Bohlmann, J. (2015). Improved white spruce (Picea glauca) genome assemblies and annotation of large gene families of conifer terpenoid and phenolic defense metabolism. Plant Journal, 83, 189–212.

Willi, Y., Fracassetti, M., Zoller, S., & Van Buskirk, J. (2018). Accumulation of mutational load at the edges of a species range. Molecular Biology and Evolution, 35, 781–791.