Spatial genetic structure and diversity of natural populations of Aesculus hippocastanum L. in Greece
Autoři:
Łukasz Walas aff001; Petros Ganatsas aff002; Grzegorz Iszkuło aff001; Peter A. Thomas aff004; Monika Dering aff001
Působiště autorů:
Institute of Dendrology, Polish Academy of Sciences, Parkowa, Kórnik, Poland
aff001; Aristotle University of Thessaloniki, School of Forestry and Natural Environment, Laboratory of Silviculture, Thessaloniki, Greece
aff002; Faculty of Biological Sciences, University of Zielona Góra, Prof. Z. Szafrana, Zielona Góra, Poland
aff003; School of Biological Sciences, Keele University, Staffordshire, United Kingdom
aff004; Harvard Forest, Harvard University, Petersham, MA, United States of America
aff005; Faculty of Forestry, Poznań University of Life Sciences, Wojska Polskiego, Poznań, Poland
aff006
Vyšlo v časopise:
PLoS ONE 14(12)
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pone.0226225
Souhrn
Horse-chestnut (Aesculus hippocastanum L.) is an endemic and relict species from the Mediterranean biodiversity hotspot and a popular ornamental tree. Knowledge about the evolutionary history of this species remains scarce. Here, we ask what historical and ecological factors shaped the pattern of genetic diversity and differentiation of this species. We genotyped 717 individuals from nine natural populations using microsatellite markers. The influence of distance, topography and habitat variables on spatial genetic structure was tested within the approaches of isolation-by-distance and isolation-by-ecology. Species niche modeling was used to project the species theoretical range through time and space. The species showed high genetic diversity and moderate differentiation for which topography, progressive range contraction through the species’ history and long-term persistence in stable climatic refugia are likely responsible. A strong geographic component was revealed among five genetic clusters that are connected with very limited gene flow. The environmental variables were a significant factor in the spatial genetic structure. Modeling results indicated that future reduction of the species range may affect its survival. The possible impact of climate changes and high need of in situ conservation are discussed.
Klíčová slova:
Climate change – Gene flow – Inbreeding – Paleoclimatology – Paleogenetics – Population genetics – Seedlings – Species diversity
Zdroje
1. Chaney RW. Tertiary centers and migration routes. Ecological Monographs 1947; 17: 139–148.
2. Wolfe JA. Tertiary climates and floristic relationships at high latitudes in the Northern Hemisphere. Palaeogeography, Palaeoclimatology, Palaeoecology 1980; 30: 313–323.
3. Mai DH. Palaeofloristic changes in Europe and the confirmation of the Arctotertiary-Palaeotropical geofloral concept. Review of Palaeobotany and Palynology 1991; 68: 29–36.
4. Milne RI, Abbott RJ. The origin and evolution of tertiary relict floras. Advances in Botanical Research 2002; 38: 281–314.
5. Thompson JD. Plant evolution in the Mediterranean. Oxford: Oxford University Press on Demand; 2005.
6. Myers N, Mittermeier RA, Mittermeier CG, Da Fonseca GA, Kent J. Biodiversity hotspots for conservation priorities. Nature 2000; 403: 853–858. doi: 10.1038/35002501 10706275
7. Mouillot D, Bellwood DR, Baraloto C, Chave J, Galzin R, Harmelin-Vivien M, Kulbicki M, Levergne S, Lavorel S, Mouguet N, Paine CET, Renaud J, Thuiller W. Rare Species Support Vulnerable Functions in High-Diversity Ecosystems. PLOS Biology 2003; 11: e1001569.
8. Feliner GN. Patterns and processes in plant phylogeography in the Mediterranean Basin. A review. Perspectives in Plant Ecology, Evolution and Systematics 2014; 16: 265–278.
9. Sarris D, Christodoulakis D, Körner C. 2007. Recent decline in precipitation and tree growth in the eastern Mediterranean. Global Change Biology 13: 1187–1200.
10. García-Ruiz JM, López-Moreno JI, Vicente-Serrano SM, Lasanta–Martínez T, Beguería S. 2011. Mediterranean water resources in a global change scenario. Earth-Science Reviews 2011; 105: 121–139.
11. Bruno D, Belmar O, Sánchez-Fernández D, Guareschi S, Millán A, Velasco J. Responses of Mediterranean aquatic and riparian communities to human pressures at different spatial scales. Ecological Indicators 2014; 45: 456–464.
12. Harrison S, Noss R. Endemism hotspots are linked to stable climatic refugia. Annals of Botany 2017; 119: 207–214. doi: 10.1093/aob/mcw248 28064195
13. Huang Y, Jacques FMB, Su T, Ferguson DK, Tang H, Chen W, Zhou Z. Distribution of Cenozoic plant relicts in China explained by drought in dry season. Scientific Reports 2015; 5: 14212. doi: 10.1038/srep14212 26369980
14. Molina-Venegas R, Aparicio A, Lavergne S, Arroyo J. Climatic and topographical correlates of plant palaeo-and neoendemism in a Mediterranean biodiversity hotspot. Annals of Botany 2016; 119: 229–238. doi: 10.1093/aob/mcw093 27288510
15. Vogiatzakis IN, Mannion AM, Griffiths GH. Mediterranean ecosystems: problems and tools for conservation. Progress in Physical Geography: Earth and Environment 2006; 30: 175–200.
16. Cox RL, Underwood EC. The Importance of Conserving Biodiversity Outside of Protected Areas in Mediterranean Ecosystems. PLOS ONE 2011; 6: e14508. doi: 10.1371/journal.pone.0014508 21249126
17. Blanco‐Pastor JL, Fernández‐Mazuecos M, Vargas P. Past and future demographic dynamics of alpine species: limited genetic consequences despite dramatic range contraction in a plant from the Spanish Sierra Nevada. Molecular Ecology 2013; 22: 4177–4195. doi: 10.1111/mec.12383 23844700
18. López-Pujol J, Martinell MC, Massó S, Blanché C, Sáez L. The ‘paradigm of extremes’: extremely low genetic diversity in an extremely narrow endemic species, Coristospermum huteri (Umbelliferae). Plant Systematics and Evolution 2013; 299: 439–446.
19. Petit RJ, Hampe A. Some Evolutionary Consequences of Being a Tree. Annual Review of Ecology, Evolution, and Systematics 2006; 37: 187–214.
20. Dirzo R, Young HS, Galetti M, Ceballos G, Isaac NJ, Collen B. Defaunation in the Anthropocene. Science 2014; 345: 401–406. doi: 10.1126/science.1251817 25061202
21. Geng Q, Yao Z, Yang J, He J, Wang D, Wang Z, Liu H. Effect of Yangtze River on population genetic structure of the relict plant Parrotia subaequalis in eastern China. Ecology and Evolution 2015; 5: 4617–4627. doi: 10.1002/ece3.1734 26668727
22. Maharramova EH, Safarov HM, Kozlowski G, Borsch T, Muller LA. Analysis of nuclear microsatellites reveals limited differentiation between Colchic and Hyrcanian populations of the wind-pollinated relict tree Zelkova carpinifolia (Ulmaceae). American Journal of Botany 2015; 102: 119–128. doi: 10.3732/ajb.1400370 25587154
23. McDowell NG, Allen CD. Darcy’s law predicts widespread forest mortality under climate warming. Nature Climate Change 2015; 5: 669.
24. Tamaki S, Isoda K, Takahashi M, Yamada H, Yamashita Y. Genetic structure and diversity in relation to the recently reduced population size of the rare conifer, Pseudotsuga japonica, endemic to Japan. Conservation Genetics 2018; 19: 1243–1255.
25. Haddad NM, Bowne DR, Cunningham A, Danielson BJ, Levey DJ, Sargent S, Spira T. Corridor Use by Diverse Taxa. Ecology 2003; 84: 609–615.
26. Townsend PA, Levey DJ. An Experimental Test of Whether Habitat Corridors Affect Pollen Transfer. Ecology 2005; 86: 466–475.
27. Thompson JD. Population differentiation in Mediterranean plants: insights into colonization history and the evolution and conservation of endemic species. Heredity 1999; 82: 229–236. doi: 10.1038/sj.hdy.6885040 10336696
28. Thompson JD, Lavergne S, Affre L, Gaudeul M, Debussche M. Ecological differentiation of Mediterranean endemic plants. Taxon 2005; 54: 967–976.
29. Médail F, Diadema K. Glacial refugia influence plant diversity patterns in the Mediterranean Basin. Journal of Biogeography 2009; 36: 1333–1345.
30. Hewitt GM. Mediterranean Peninsulas: The Evolution of Hotspots. In: Zachos FE, Habel JC, eds. Biodiversity Hotspots: Distribution and Protection of Conservation Priority Areas, Berlin, Heidelberg: Springer Berlin Heidelberg 2011; 123–147.
31. Noguerales V, Cordero PJ, Ortego J. Hierarchical genetic structure shaped by topography in a narrow-endemic montane grasshopper. BMC Evolutionary Biology 2016; 16: 96. doi: 10.1186/s12862-016-0663-7 27149952
32. Kruckeberg AR, Rabinowitz D. Biological aspects of endemism in higher plants. Annual Review of Ecology and Systematics 1985; 16: 447–479.
33. Lavergne S, Thompson JD, Garnier E, Debussche M. The biology and ecology of narrow endemic and widespread plants: a comparative study of trait variation in 20 congeneric pairs. Oikos 2004; 107: 505–518.
34. Hermant M, Prinzing A, Vernon P, Convey P, Hennion F. Endemic species have highly integrated phenotypes, environmental distributions and phenotype–environment relationships. Journal of Biogeography 2013; 40: 1583–1594.
35. Shafer ABA, Wolf JBW. Widespread evidence for incipient ecological speciation: a meta-analysis of isolation-by-ecology. Ecology Letters 2013; 16: 940–950. doi: 10.1111/ele.12120 23627762
36. Edelaar P, Alonso D, Lagerveld S, Senar JC, Björklund M. Population differentiation and restricted gene flow in Spanish crossbills: not isolation-by-distance but isolation-by-ecology. Journal of Evolutionary Biology 2012; 25: 417–430. doi: 10.1111/j.1420-9101.2011.02443.x 22239460
37. Wang IJ, Bradburd GS. Isolation by environment. Molecular Ecology 2014; 23: 5649–5662. doi: 10.1111/mec.12938 25256562
38. Avtzis ND, Avtzis DN, Vergos SG, Diamandis S. A contribution to the natural distribution of Aesculus hippocastanum (Hippocastanaceae) in Greece. Phytologia Balcanica 2007; 13: 183–187.
39. Maley J. Les changements climatiques de la fin du Tertiaire en Afrique: leur conséquence sur l’apparition du Sahara et de sa végétation. The Sahara and the Nile 1980; 63–86.
40. Mijarra JMP, Manzaneque FG, Morla C. Survival and long-term maintenance of tertiary trees in the Iberian Peninsula during the Pleistocene: first record of Aesculus L. (Hippocastanaceae) in Spain. Vegetation History and Archaeobotany 2008; 17: 351.
41. Lack HW. The Discovery and Rediscovery of the Horse Chestnut. Arnoldia 2002; 61: 15–19.
42. Peçi D, Mullaj A, Dervishi A. The natural distribution of horse chestnut (Aesculus hippocastanum L) in Albania. Journal of Institute Alb-Shkenca 2012; 5: 153–157. [in Albanian]
43. Prada D, Velloza TM, Toorop PE, Pritchard HW. Genetic population structure in horse chestnut (Aesculus hippocastanum L.): effects of human-mediated expansion across Europe. Plant Species Biology 2011; 26: 43–50.
44. Jiménez-Mejías P, Fernández-Mazuecos M, Amat ME, Vargas P. Narrow endemics in European mountains: high genetic diversity within the monospecific genus Pseudomisopates (Plantaginaceae) despite isolation since the late Pleistocene. Journal of Biogeography 2015; 42: 1455–1468.
45. Ellstrand NC, Elam DR. Population Genetic Consequences of Small Population Size: Implications for Plant Conservation. Annual Review of Ecology and Systematics 1993; 24: 217–242.
46. Jennings H, Wallin K, Brennan J, Valle AD, Guzman A, Hein D, Hunter S, Lewandowski A, Olson S, Parsons H, Scheidt S, Wang Z, Werra A, Kartzinel RY, Givnish TJ. Inbreeding, low genetic diversity, and spatial genetic structure in the endemic Hawaiian lobeliads Clermontia fauriei and Cyanea pilosa ssp. longipedunculata. Conservation Genetics 2016; 17: 497–502.
47. Ostfeld RS, Keesing F. Effects of Host Diversity on Infectious Disease. Annual Review of Ecology, Evolution, and Systematics 2012; 43: 157–182.
48. Frankham R, Bradshaw CJ, Brook BW. Genetics in conservation management: revised recommendations for the 50/500 rules, Red List criteria and population viability analyses. Biological Conservation 2014; 170: 56–63.
49. Allen D, Khela S. Aesculus hippocastanum (errata version published in 2018). The IUCN Red List of Threatened Species 2017. 2017. Available at: https://doi.org/e.T202914A122961065
50. Romo A, Iszkuło G, Seghir Taleb M, Walas Ł, Boratyński A. Taxus baccata in Morocco: a tree in regression in its southern extreme. Dendrobiology 2017; 78: 63–74.
51. Maharramova E, Huseynova I, Kolbaia S, Gruenstaeudl M, Borsch T, Muller LA. Phylogeography and population genetics of the riparian relict tree Pterocarya fraxinifolia (Juglandaceae) in the South Caucasus. Systematics and Biodiversity 2018; 16: 14–27.
52. Walas Ł, Dering M, Ganatsas P, Pietras M, Pers-Kamczyc E, Iszkuło G. The present status and potential distribution of relict populations of Aesculus hippocastanum L. in Greece and the diverse infestation by Cameraria ohridella Deschka & Dimić. Plant Biosystems 2018; 152: 1048–1058.
53. Tsiroukis A. Reproductive biology and ecology of horse chestnut (Aesculus hippocastanum L.) [in Greek]. 2008. Department of Botany, Faculty of Biology, National & Kapodistrian University of Athens.
54. Orsini L, Vanoverbeke J, Swillen I, Mergeay J, De Meester L. Drivers of population genetic differentiation in the wild: isolation by dispersal limitation, isolation by adaptation and isolation by colonization. Molecular Ecology 2013; 22: 5983–5999. doi: 10.1111/mec.12561 24128305
55. Lafontaine G, Napier JD, Petit RJ, Hu FS. Invoking adaptation to decipher the genetic legacy of past climate change. Ecology 2018; 99: 1530–1546. doi: 10.1002/ecy.2382 29729183
56. Weryszko-Chmielewska E, Chwil M. Structure of floral nectaries in Aesculus hippocastanum L. Acta Botanica Croatica 2017; 76: 41–48.
57. Free JB. The Flower Constancy of Honeybees. Journal of Animal Ecology 1963; 32: 119–131.
58. Kevan PG. How large bees, Bombus and Xylocopa (Apoidea Hymenoptera) forage on trees: optimality and patterns of movement in temperate and tropical climates. Ethology Ecology & Evolution 1990; 2: 233–242.
59. Weryszko-Chmielewska E, Tietze M, Michońska M. Ecological features of the flowers of Aesculus hippocastanum L. and characteristics of Aesculus L. pollen seasons under the conditions of central-eastern Poland. Acta Agrobotanica 2012; 65: 61–68.
60. Thomas PA, Alhamd O, Iszkuło G, Dering M, Mukassabi TA. Biological Flora of the British Isles: Aesculus hippocastanum. Journal of Ecology 2019; 107: 992–1030.
61. Hoshizaki K, Suzuki W, Nakashizuka T. Evaluation of secondary dispersal in a large-seeded tree Aesculus turbinata: a test of directed dispersal. Plant Ecology 1999; 144: 167–176.
62. Dorken ME, Eckert CG. Severely reduced sexual reproduction in northern populations of a clonal plant, Decodonverticillatus (Lythraceae). Journal of Ecology 2001; 89: 339–350
63. Dumolin S, Demesure B, Petit RJ. Inheritance of chloroplast and mitochondrial genomes in pedunculate oak investigated with an efficient PCR method. Theoretical and Applied Genetics 1995; 91: 1253–1256. doi: 10.1007/BF00220937 24170054
64. Minami E. Polymorphic microsatellite markers in Japanese horse chestnut Aesculus turbinata Blume. Molecular Ecology 1998; 7: 1616–1617. 9819913
65. Peakall R, Smouse PE. GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes 2006; 6: 288–295.
66. Chybicki, I. INEST 2.0 [Computer Software]. 2016.
67. Goudet J. FSTAT, a program to estimate and test gene diversity and fixation indices (version 2.9.3). 2001. Available at: http://www2.Unil.Ch/Popgen/Softwares/Fstat.Htm
68. Guo SW, Thompson EA. Performing the exact test of Hardy-Weinberg proportion for multiple alleles. Biometrics 1992; 361–372. 1637966
69. Rousset F. GENEPOP’007: a complete re-implementation of the genepop software for Windows and Linux. Molecular Ecology Resources 2008; 8: 103–106. doi: 10.1111/j.1471-8286.2007.01931.x 21585727
70. Chapuis M-P, Estoup A. Microsatellite Null Alleles and Estimation of Population Differentiation. Molecular Biology and Evolution 2007; 24: 621–631. doi: 10.1093/molbev/msl191 17150975
71. Pritchard JK, Stephens M, Donnelly P. Inference of population structure using multilocus genotype data. Genetics 2000; 155: 945–959. 10835412
72. Kopelman NM, Mayzel J, Jakobsson M, Rosenberg NA, Mayrose I. CLUMPAK a program for identifying clustering modes and packaging population structure inferences across K. Molecular Ecology Resources 2015; 15: 1179–1191. doi: 10.1111/1755-0998.12387 25684545
73. Gao H, Williamson S, Bustamante CD. A Markov chain Monte Carlo approach for joint inference of population structure and inbreeding rates from multilocus genotype data. Genetics 2007; 176: 1635–1651. doi: 10.1534/genetics.107.072371 17483417
74. Jombart T, Devillard S, Balloux F. Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genetics 2010; 11: 94. doi: 10.1186/1471-2156-11-94 20950446
75. Jombart T. adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 2008; 24: 1403–1405. doi: 10.1093/bioinformatics/btn129 18397895
76. R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. 2013. Available at: http://www.R-project.org/
77. Wickham H. ggplot2: Elegant Graphics for Data Analysis. Springer-Verlag New York 2016.
78. Langella O. POPULATIONS, a free population genetics software. 2002. URL http://www.legs.cnrs-gif.fr.
79. Wilson GA, Rannala B. Bayesian inference of recent migration rates using multilocus genotypes. Genetics 2003; 163: 1177–1191. 12663554
80. Meirmans PG. Nonconvergence in Bayesian estimation of migration rates. Molecular Ecology Resources 2014; 14: 726–733. doi: 10.1111/1755-0998.12216 24373147
81. Rannala B, Zhu T, Yang Z. Tail paradox, partial identifiability, and influential priors in Bayesian branch length inference. Molecular Biology and Evolution 2011; 29: 325–335. doi: 10.1093/molbev/msr210 21890479
82. Beerli P, Felsenstein J. Maximum-likelihood estimation of migration rates and effective population numbers in two populations using a coalescent approach. Genetics 1999; 152: 763–773. 10353916
83. Beerli P, Palczewski M. Unified framework to evaluate panmixia and migration direction among multiple sampling locations. Genetics 2010; 185: 313–326. doi: 10.1534/genetics.109.112532 20176979
84. Phillips SJ, Dudík M, Schapire RE. A Maximum Entropy Approach to Species Distribution Modeling. In: Brodley C, eds. Proceedings of the Twenty-first International Conference on Machine Learning. New York, NY, USA: ACM, 2004; 83.
85. Elith J, Phillips SJ, Hastie T, Dudík M, Chee YE, Yates CJ. A statistical explanation of MaxEnt for ecologists. Diversity and Distributions 2011; 17: 43–57.
86. Valade R, Kenis M, Hernandez‐Lopez A, Augustin S, Mena NM, Magnoux E, Rougerie R, Lakatos F, Roques A, Lopez-Vaamonde C et al. Mitochondrial and microsatellite DNA markers reveal a Balkan origin for the highly invasive horse-chestnut leaf miner Cameraria ohridella (Lepidoptera, Gracillariidae). Molecular Ecology 2009; 18: 3458–3470. doi: 10.1111/j.1365-294X.2009.04290.x 19627490
87. Lees DC, Lack HW, Rougerie R, Hernandez-Lopez A, Raus T, Avtzis ND, Augustin S, Lopez-Vaamonde C. Tracking origins of invasive herbivores through herbaria and archival DNA: the case of the horse-chestnut leaf miner. Frontiers in Ecology and the Environment 2011; 9: 322–328.
88. Acevski J, Simovski B. Forest associations of the National Park Mavrovo in the Republic of Macedonia. In: Horodnic SA, Duduman M-L, Palaghianu C, eds. Proceedings of the International Conference Integrated Management of Environmental Resources-Suceava, November 2011. Suceava: Editura Universităţii "Ştefan cel Mare" 2012; 17–27.
89. Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A. Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology 2005; 25: 1965–1978.
90. Kukwa M, Kolanowska M. Glacial refugia and the prediction of future habitat coverage of the South American lichen species Ochrolechia austroamericana. Scientific Reports 2016; 6: 38779. doi: 10.1038/srep38779 27929090
91. Collins M, Knutti R, Arblaster J, Dufresne J-L, Fichefet T, Friedlingstein P, Gao X, Gutowski WJ, Johns T, Krinner G, Shongwe M, Tebaldi C, Weaver AJ, Wehner MF, Allen MR, Andrews T, Beyerle U, Bitz CM, Bony S, Booth BBB. Long-term climate change: projections, commitments and irreversibility. In: Climate Change 2013: The Physical Science Basis. IPCC Working Group I Contribution to AR5. Eds. IPCC, Cambridge: Cambridge University Press. 2013.
92. Gent PR, Danabasoglu G, Donner LJ, Holland MM, Hunke EC, Jayne SR, Lawrence DM, Neale RB, Rasch PJ, Vertenstein M, Worley PH, Yang Z-L, Zhang M. The Community Climate System Model Version 4. Journal of Climate 2011; 24: 4973–4991.
93. Wang Z, Chang YI, Ying Z, Zhu L, Yang Y. A parsimonious threshold-independent protein feature selection method through the area under receiver operating characteristic curve. Bioinformatics 2007; 23: 2788–2794. doi: 10.1093/bioinformatics/btm442 17878205
94. Mas J-F, Soares Filho B, Pontius RG, Farfán Gutiérrez M, Rodrigues H. A Suite of Tools for ROC Analysis of Spatial Models. ISPRS International Journal of Geo-Information 2013; 2: 869–887.
95. QGIS Development Team. QGIS Geographic Information System. Open Source Geospatial Foundation Project. 2012. Available at: http://qgis.osgeo.org
96. McRae BH, Beier P. Circuit theory predicts gene flow in plant and animal populations. Proceedings of the National Academy of Sciences 2007; 104: 19885–19890.
97. McRae BH. Isolation by resistance. Evolution 2006; 60: 1551–1561. 17017056
98. Awad L, Fady B, Khater C, Roig A, Cheddadi R. Genetic structure and diversity of the endangered fir tree of Lebanon (Abies cilicica Carr.): implications for conservation. PLoS One 2014; 9: e90086. doi: 10.1371/journal.pone.0090086 24587219
99. Boratyński A, Wachowiak W, Dering M, Boratyńska K, Sękiewicz K, Sobierajska K, Jasińska AK, Klimko M, Montserrat JM, Romo A, Ok T, Didukh Y. The biogeography and genetic relationships of Juniperus oxycedrus and related taxa from the Mediterranean and Macaronesian regions. Botanical Journal of the Linnean Society 2014; 174: 637–653.
100. Dering M, Sękiewicz K, Boratyńska K, Litkowiec M, Iszkuło G, Romo A, Boratyński A. Genetic diversity and inter-specific relations of western Mediterranean relic Abies taxa as compared to the Iberian A. alba. Flora—Morphology, Distribution, Functional Ecology of Plants 2014; 209: 367–374.
101. Sękiewicz K, Dering M, Sękiewicz M, Boratyńska K, Iszkuło G, Litkowiec M., Ok T, Dagher-Kharrat MB, Boratyński A. Effect of geographic range discontinuity on species differentiation—East-Mediterranean Abies cilicica: a case study. Tree Genetics and Genomes 2015; 11: 810.
102. Eliades N-GH, Fady B, Gailing O, Leinemann L, Finkeldey R. Significant patterns of fine-scale spatial genetic structure in a narrow endemic wind-dispersed tree species, Cedrus brevifolia Henry. Tree Genetics & Genomes 2018; 14: 15.
103. Gómez A, Lunt DH. Refugia within refugia: patterns of phylogeographic concordance in the Iberian Peninsula. In: Weiss S, Ferrand N, eds. Phylogeography of southern European refugia. Springer, Dordrecht. 2007; 155–188.
104. Stewart JR, Lister AM, Barnes I, Dalén L. Refugia revisited: individualistic responses of species in space and time. Proceedings of the Royal Society of London B: Biological Sciences 2010; 277: 661–671.
105. Sękiewicz K, Dering M, Romo A, Dagher-Kharrat MB, Boratyńska K, Ok T, Boratyński A. Phylogenetic and biogeographic insights into long-lived Mediterranean Cupressus taxa with a schizo-endemic distribution and Tertiary origin. Botanical Journal of the Linnean Society 2018; 188: 190–212.
106. Médail F, Baumel A. Using phylogeography to define conservation priorities: The case of narrow endemic plants in the Mediterranean Basin hotspot. Biological Conservation 2018; 224: 258–266.
107. Torres-Díaz C, Ruiz E, González F, Fuentes G, Cavieres LA. Genetic Diversity in Nothofagus alessandrii (Fagaceae), an Endangered Endemic Tree Species of the Coastal Maulino Forest of Central Chile. Annals of Botany 2007; 100: 75–82. doi: 10.1093/aob/mcm073 17513870
108. Aleksić JM, Geburek T. Quaternary population dynamics of an endemic conifer, Picea omorika, and their conservation implications. Conservation Genetics 2014; 15: 87–107.
109. Dodd RS, DeSilva R. Long-term demographic decline and late glacial divergence in a Californian paleoendemic: Sequoiadendron giganteum (giant sequoia). Ecology and Evolution 2016; 6: 3342–3355. doi: 10.1002/ece3.2122 27252835
110. Millar MA, Byrne M, Coates DJ, Roberts JD. Contrasting diversity and demographic signals in sympatric narrow-range endemic shrubs of the south-west Western Australian semi-arid zone. Biological Journal of the Linnean Society 2016; 118: 315–329.
111. Hu Y, Dang M, Feng X, Woeste K, Zhao P. Genetic diversity and population structure in the narrow endemic Chinese walnut Juglans hopeiensis Hu: implications for conservation. Tree Genetics & Genomes 2017; 13: 91.
112. Jian H, Li S, Guo J, Li S, Wang Q, Yan H, Qiu, X, Zhang Y, Cai Z, Volis S, Tang K. High genetic diversity and differentiation of an extremely narrowly distributed and critically endangered decaploid rose (Rosa praelucens): implications for its conservation. Conservation Genetics 2018; 19: 761–776.
113. Lázaro-Nogal A, Matesanz S, García-Fernández A, Traveset A, Valladares F. Population size, center–periphery, and seed dispersers’ effects on the genetic diversity and population structure of the Mediterranean relict shrub Cneorum tricoccon. Ecology and Evolution 2017; 7: 7231–7242. doi: 10.1002/ece3.2940 28944013
114. Mitchell RJ, Karron JD, Holmquist KG, Bell JM. The influence of Mimulus ringens floral display size on pollinator visitation patterns. Functional Ecology 2004; 18: 116–124.
115. Hampe A, Petit RJ. Conserving biodiversity under climate change: the rear edge matters. Ecology Letters 2005; 8: 461–467. doi: 10.1111/j.1461-0248.2005.00739.x 21352449
116. Dering M, Rączka G, Szmyt J. Sex-specific pattern of spatial genetic structure in dioecious and clonal tree species, Populus alba L. Tree Genetics & Genomes 2016; 12: 70.
117. Garza JC, Williamson EG. Detection of reduction in population size using data from microsatellite loci. Molecular ecology 2001; 10: 305–318 doi: 10.1046/j.1365-294x.2001.01190.x 11298947
118. Lowe WH, Kovach RP, Allendorf FW. Population Genetics and Demography Unite Ecology and Evolution. Trends in Ecology & Evolution 2017; 32: 141–152.
119. Jump AS, Peñuelas J. Genetic effects of chronic habitat fragmentation in a wind-pollinated tree. Proceedings of the National Academy of Sciences 2006; 103: 8096–8100.
120. Karhu A, Vogl C, Moran GF, Bell JC, Savolainen O. Analysis of microsatellite variation in Pinus radiata reveals effects of genetic drift but no recent bottlenecks. Journal of Evolutionary Biology 2006; 19: 167–175. doi: 10.1111/j.1420-9101.2005.00982.x 16405588
121. Broquet T, Angelone S, Jaquiery J, Joly P, Lena J-P, Lengagne T, Plenet S, Luquet E, Perrin N. Genetic Bottlenecks Driven by Population Disconnection. Conservation Biology 2010; 24: 1596–1605. doi: 10.1111/j.1523-1739.2010.01556.x 20666803
122. Setoguchi H, Mitsui Y, Ikeda H, Nomura N, Tamura A. Genetic structure of the critically endangered plant Tricyrtis ishiiana (Convallariaceae) in relict populations of Japan. Conservation Genetics 2011; 12: 491–501.
123. Manchester SR, Chen Z-D, Lu A-M, Uemura K. Eastern Asian endemic seed plant genera and their paleogeographic history throughout the Northern Hemisphere. Journal of Systematics and Evolution 2009; 47: 1–42.
124. Young A, Boyle T, Brown T. The population genetic consequences of habitat fragmentation for plants. Trends in Ecology & Evolution 1996; 11: 413–418
125. Pluess AR, Stöcklin J. Genetic diversity and fitness in Scabiosa columbaria in the Swiss Jura in relation to population size. Conservation Genetics 2004; 5: 145–156.
126. Jackson ND, Fahrig L. Habitat amount, not habitat configuration, best predicts population genetic structure in fragmented landscapes. Landscape Ecology 2016; 31: 951–968.
127. Fady-Welterlen B. Is there really more biodiversity in Mediterranean forest ecosystems? Taxon 2005; 54: 905–910.
128. Piotti A, Leonarduzzi C, Postolache D, Bagnoli F, Spanu I, Brousseau L, Urbinati C, Leonardi S, Vendramin GG. Unexpected scenarios from Mediterranean refugial areas: disentangling complex demographic dynamics along the Apennine distribution of silver fir. Journal of Biogeography 2017; 44: 1547–1558.
129. Dubreuil M, Riba M, González‐Martínez SC, Vendramin GG, Sebastiani F, Mayol M. Genetic effects of chronic habitat fragmentation revisited: Strong genetic structure in a temperate tree, Taxus baccata (Taxaceae), with great dispersal capability. American Journal of Botany 2010; 97: 303–310. doi: 10.3732/ajb.0900148 21622391
130. González-Martínez SC, Dubreuil M, Riba M, Vendramin GG, Sebastiani F, Mayol M. Spatial genetic structure of Taxus baccata L. in the western Mediterranean Basin: Past and present limits to gene movement over a broad geographic scale. Molecular Phylogenetics and Evolution 2010; 55: 805–815. doi: 10.1016/j.ympev.2010.03.001 20211747
131. Mayol M, Riba M, González-Martínez SC, Bagnoli F, Beaulieu J-L, Berganzo E, Burgarella C, Dubreuil M, Krajmerová D, Paule L, Romšáková I, Vettori C, Vincenot L, Vendramin GG. 2015. Adapting through glacial cycles: insights from a long-lived tree (Taxus baccata). New Phytologist 208: 973–986. doi: 10.1111/nph.13496 26096330
132. García D, Ramón Obeso J. Facilitation by herbivore-mediated nurse plants in a threatened tree, Taxus baccata: local effects and landscape level consistency. Ecography 2003; 26: 739–750.
133. Devaney JL, Jansen MAK, Whelan PM. Spatial patterns of natural regeneration in stands of English yew (Taxus baccata L.); Negative neighbourhood effects. Forest Ecology and Management 2014; 321: 52–60.
134. Iszkuło G, Pers-Kamczyc E, Nalepka D, Rabska M, Walas Ł, Dering M. Postglacial migration dynamics helps to explain current scattered distribution of Taxus baccata. Dendrobiology 2016; 76: 81–89.
135. Bujoczek L, Bujoczek M. The dynamics of the Taxus baccata L. population and the factors affecting its regeneration in the Jasień Nature Reserve. Dendrobiology 2018; 80: 24–36.
136. Hampe A, Arroyo J. Recruitment and regeneration in populations of an endangered South Iberian Tertiary relict tree. Biological Conservation 2002; 107: 263–271.
137. Lázaro A, Traveset A, Castillo A. Spatial concordance at a regional scale in the regeneration process of a circum-Mediterranean relict (Buxus balearica): connecting seed dispersal to seedling establishment. Ecography 2006; 29: 683–696.
138. Baali-Cherif D, Besnard G. High genetic diversity and clonal growth in relict populations of Olea europaea subsp. laperrinei (Oleaceae) from Hoggar, Algeria. Annals of Botany 2005; 96: 823–830. doi: 10.1093/aob/mci232 16043438
139. Neophytou C, Konnert M, Fussi B. Western and eastern post-glacial migration pathways shape the genetic structure of sycamore maple (Acer pseudoplatanus L.) in Germany. Forest Ecology and Management 2019; 432: 83–93.
140. Skourlis K, Doutsos T. The Pindos Fold-and-thrust belt (Greece): inversion kinematics of a passive continental margin. International Journal of Earth Sciences, 2003; 92: 891–903.
141. Robledo-Arnuncio JJ, Collada C, Alia R, Gil L. Genetic structure of montane isolates of Pinus sylvestris L. in a Mediterranean refugial area. Journal of Biogeography 2005; 32: 595–605.
142. Ohsawa T, Ide Y. Global patterns of genetic variation in plant species along vertical and horizontal gradients on mountains. Global Ecology and Biogeography 2008; 17: 152–163.
143. Breed MF, Ottewell KM, Gardner MG, Marklund MH, Dormontt EE, Lowe AJ. Mating patterns and pollinator mobility are critical traits in forest fragmentation genetics. Heredity 2015; 115: 108. doi: 10.1038/hdy.2013.48 24002239
144. Ottewell K, Grey E, Castillo F, Karubian J. The pollen dispersal kernel and mating system of an insect-pollinated tropical palm, Oenocarpus bataua. Heredity 2012; 109: 332. doi: 10.1038/hdy.2012.40 22892637
145. Hoshizaki K. Rodent seed hoarding and regeneration of Aesculus turbinata: patterns, processes and implications. In: Tamura T., Sakio H. Ecology of Riparian Forests in Japan 2008; pp. 107–122. Springer, Tokyo.
146. Hoshizaki K, Suzuki W, Sasaki S. Impacts of secondary seed dispersal and herbivory on seedling survival in Aesculus turbinata. Journal of Vegetation Science 1997; 8: 735–742.
147. Magri D, Di Rita F, Aranbarri J, Fletcher W, González-Sampériz P. Quaternary disappearance of tree taxa from Southern Europe: Timing and trends. Quaternary Science Reviews 2017; 163: 23–55.
148. Gobet E, Schwörer Ch, van Leeuwen J, Wahab SA, Nielsen EH, Kotova N, Makhortykh S, Kiosak D, Tinner W. Vegetation shifts at the monumental Ukrainian site of Kamyana Mohyla during the Neolithisation period. In: Makhorytkh S., Capitani A., eds. Archaeology and paleoecology of the Ukrainian steppe. IA NAS, Kyiv, 2017; 51–65.
149. Van Zeist W, Woldring H. A postglacial pollen diagram from Lake Van in east Anatolia. Review of Palaeobotany and Palynology 1978; 26: 249–276
150. Feliner GN. Southern European glacial refugia: a tale of tales. Taxon 2011; 60: 365–372.
151. Isagi Y, Saito D, Kawaguchi H, Tateno R, Watanabe S. Effective pollen dispersal is enhanced by the genetic structure of an Aesculus turbinata population. Journal of Ecology 2007; 95: 983–990.
152. Casazza G, Giordani P, Benesperi R, Foggi B, Viciani D, Filigheddu R, Farris E, Bagella S, Pisanu S, Mariotti MG. Climate change hastens the urgency of conservation for range-restricted plant species in the central-northern Mediterranean region. Biological Conservation 2014; 179: 129–138.
153. Tang CQ, Dong Y-F, Herrando-Moraira S, Matsui T, Ohashi H, He L-Y, Nakao K. Tanaka N, Tomita M, Li X-S, Yan H-Z, Peng M-C, Hu J, Yang R-H, Li W-J, Yan K, Hou X, Zhang Z-Y, López-Pujol J. Potential effects of climate change on geographic distribution of the Tertiary relict tree species Davidia involucrata in China. Scientific Reports 2017; 7: 43822. doi: 10.1038/srep43822 28272437
154. Joffre R, Rambal S, Ratte JP. The dehesa system of southern Spain and Portugal as a natural ecosystem mimic. Agroforestry Systems 1999; 45: 57–79.
155. Pulido F, Valladares F, Calleja JA, Moreno G, González‐Bornay G. Tertiary relict trees in a Mediterranean climate: abiotic constraints on the persistence of Prunus lusitanica at the eroding edge of its range. Journal of Biogeography 2008; 35: 1425–1435.
156. Allen CD, Macalady AK, Chenchouni H, Bachelet D, McDowell N, Vennetier M, Kitzberger T, Rigling A, Breshears DD, Hogg EHT, Gonzalez P, Fensham R, Zhang Z, Castro J, Demidova N, Lim J-H, Allard G, Running SW, Semerci A, Cobb N. A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. Forest Ecology and Management 2010; 259: 660–684.
157. Giorgi F, Lionello P. Climate change projections for the Mediterranean region. Global and planetary change, 2008; 63: 90–104.
158. Smith DM, Scaife AA, Boer GJ, Caian M, Doblas-Reyes FJ, Guemas V, Hawkins E, Hazeleger W, Hermanson L, Ho CK, Ishii M, Kharin V, Kimoto M, Kirtman B, Lean J, Matei D, Merryfield WJ, Müller WA, Pohlmann H, Rosati A, Wouters B, Wyser K. Real-time multi-model decadal climate predictions. Climate Dynamics 2013; 41: 2875–2888.
159. Salazar E, Hammerling D, Wang X, Sansó B, Finley AO, Mearns LO. Observation-based blended projections from ensembles of regional climate models. Climatic Change 2016; 138: 55–69.
160. Phitos D, Constantinidis T, Kamari G. The Red Data Book of Rare and Threatened Plants of Greece. Hellenic Botanical Society, Patras. 2009.
Článek vyšel v časopise
PLOS One
2019 Číslo 12
- S diagnostikou Parkinsonovy nemoci může nově pomoci AI nástroj pro hodnocení mrkacího reflexu
- Je libo čepici místo mozkového implantátu?
- Pomůže v budoucnu s triáží na pohotovostech umělá inteligence?
- AI může chirurgům poskytnout cenná data i zpětnou vazbu v reálném čase
- Nová metoda odlišení nádorové tkáně může zpřesnit resekci glioblastomů
Nejčtenější v tomto čísle
- Methylsulfonylmethane increases osteogenesis and regulates the mineralization of the matrix by transglutaminase 2 in SHED cells
- Oregano powder reduces Streptococcus and increases SCFA concentration in a mixed bacterial culture assay
- The characteristic of patulous eustachian tube patients diagnosed by the JOS diagnostic criteria
- Parametric CAD modeling for open source scientific hardware: Comparing OpenSCAD and FreeCAD Python scripts