Abstract
To establish a management plan for endangered and rare species, genetic assessment must first be conducted. The genetic characteristics of plant species are affected by demographic history, reproductive strategy, and distributional range as well as anthropological effects. Abies koreana E. H. Wilson (Pinaceae), Korean fir, is endemic to Korea and found only in sub-alpine areas of the southern Korean Peninsula and Jejudo Island. This species has been designated as critically endangered by the International Union for Conservation of Nature due to a continuous decline in its range and population fragmentation. We genotyped 176 individuals from seven natural populations and two afforested populations on the Korean Peninsula using 19 microsatellite loci. STRUCTURE analysis revealed two genetic clusters in natural populations (F st = 0.040 and R st = 0.040) despite low differentiation. We did not detect a significant reduction in genetic diversity or the signature of a genetic bottleneck despite population fragmentation and small population size. We deduced that this species exhibits a metapopulation structure, with the population on Jirisan Mountain acting as a source of genetic diversity for other local small populations on the Korean Peninsula, through contemporary asymmetric gene flow. However, the majority of afforested individuals on the Korean Peninsula originated from a different gene cluster. Thus, we recommend a conservation strategy that maintains two genetically unique clusters.
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Ægisdóttir HH, Kuss P, Stöcklin J (2009) Isolated populations of a rare alpine plant show high genetic diversity and considerable population differentiation. Ann Bot 104:1313–1322. doi:10.1093/aob/mcp242
Aguirre-Planter E, Furnier GR, Eguiarte LE (2000) Low levels of genetic variation within and high levels of genetic differentiation among populations of species of Abies from southern Mexico and Guatemala. Am J Bot 87:362–371
Allendorf FW, Luikart G, Aitken SN (2013) Conservation and the genetics of populations, 2 edn. Willey-Blackwell, Hoboken
Awad L, Fady B, Khater C, Roig A, Cheddadi R (2014) Genetic structure and diversity of the endangered fir tree of Lebanon (Abies cilicica Carr.): implications for conservation. Plos One 9:e90086. doi:10.1371/journal.pone.0090086
Barrett S, Kohn J (1991) Genetic and evolutionary consequences of small population size in plants: implications for conservation. In: Falk D, Holsinger K (eds) Genetics and conservation of rare plants. Oxford University Press, Oxford, pp 3–30
Beerli P (2006) Comparison of Bayesian and maximum-likelihood inference of population genetic parameters. Bioinformatics 22:341–345
Beerli P, Felsenstein J (2001) Maximum likelihood estimation of a migration matrix and effective population sizes in n subpopulations by using a coalescent approach. Proc Natl Acad Sci USA 98:4563–4568. doi:10.1073/pnas.081068098
Charlier J, Laikre L, Ryman N (2012) Genetic monitoring reveals temporal stability over 30 years in a small, lake-resident brown trout population. Heredity 109:246–253. doi:10.1038/hdy.2012.36
Chen C, Durand D, Forbes F, François O (2007) Bayesian clustering algorithms ascertaining spatial population structure. A new computer program and a comparison study. Mol Ecol Notes 7:747–756
Chung C-H (2007) Vegetation response to climate change on Jeju Island, South Korea, during the last deglaciation based on pollen record. Geosci J 11:147–155. doi:10.1007/bf02913928
Clark PU, Dyke AS, Shakun JD, Carlson AE, Clark J, Wohlfarth B, Mitrovica JX, Hostetler SW, McCabe AM (2009) The Last Glacial Maximum. Sci 325(5941):710–714
Collins PM, Davis BAS, Kaplan JO (2012) The mid-Holocene vegetation of the Mediterranean region and southern Europe, and comparison with the present day. J Biogeogr 39:1848–1861. doi:10.1111/j.1365-2699.2012.02738.x
Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014
Cremer E, Liepelt S, Sebastiani F et al (2006) Identification and characterization of nuclear microsatellite loci in Abies alba Mill. Mol Ecol Notes 6:374–376. doi:10.1111/j.1471-8286.2005.01238.x
Dolezal J, Altman J, Kopecky M et al. (2012) Plant diversity changes during the postglacial in East Asia: insights from forest refugia on Halla volcano, Jeju island. PloS ONE 7(3):e33065. doi:10.1371/journal.pone.0033065
Dzialuk A, Chybicki I, Gout R et al (2014) No reduction in genetic diversity of Swiss stone pine (Pinus cembra L.) in Tatra Mountains despite high fragmentation and small population size. Conserv Genet 15:1433–1445. doi:10.1007/s10592-014-0628-6
Earl D, von Holdt B (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361. doi:10.1007/s12686-011-9548-7
Eo J-K, Hyun J-O (2013) Comparative anatomy of the needles of Abies koreana and its related species. Turk J Bot 37:553–560
Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620
Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567. doi:10.1111/j.1755-0998.2010.02847.x
François C, Ancelet S, Guillot G (2006) Bayesian clustering using hidden Markov random fields in spatial population genetics. Genetics 174:805–816
Frankham R, Ballou JD, Briscoe DA (2010) Introduction to conservation genetics. 2nd edn. Cambridge University Press, Cambridge
Gilpin M (1991) The genetic effective size of a metapopulation. Biol J Linn Soc 42:165–175. doi:10.1111/j.1095-8312.1991.tb00558.x
Hamrick JL (2004) Response of forest trees to global environmental changes. For Ecol Manag 197:323–335. doi:10.1016/j.foreco.2004.05.023
Hamrick JL, Godt MJW, Sherman-Bryoles SL (1992) Factors influencing levels of genetic diversity in woody plant species. New Forest 6:95–124
Hong Y-P, Ahn J-Y, Kim Y-M, Yang B-H, Song J-H (2011) Genetic variation of nSSR markers in natural populations of Abies koreana and Abies nephrolepis in South Korea. J Korean For Soc 100:577–584
Hong JK, Lim J, Lee BY, Kwak M (2016) Isolation and characterization of novel microsatellites for Abies koreana and A. nephrolepis (Pinaceae). Genet Mol Res 15:gmr.15027542. doi:10.4238/gmr.15027542
Isoda K, Shiraishi S, Watanabe S, Kitamura K (2000) Molecular evidence of natural hybridization between Abies veitchii and A. homolepis (Pinaceae) revealed by chloroplast, mitochondrial and nuclear DNA markers. Mol Ecol 9:1965–1974. doi:10.1046/j.1365-294X.2000.01088.x
Jackson JA, Laikre L, Baker CS, Kendall KC (2012) Guidelines for collecting and maintaining archives for genetic monitoring. Conserv Genet Resour 4:527–536. doi:10.1007/s12686-011-9545-x
Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801–1806. doi:10.1093/bioinformatics/btm233
Jiang ZY, Peng YL, Hu XX, Zhou YF, Liu JQ (2011) Cytoplasmic DNA variation in and genetic delimitation of Abies nephrolepis and Abies holophylla in northeastern China. Can J Forest Res 41:1555–1561. doi:10.1139/x11-069
Kim YS, Chang CS, Kim CS, Gardner M (2011) Abies koreana. The IUCN red list of threatened species 2011:e.T31244A9618913. doi:10.2305/IUCN.UK.2011-2.RLTS.T31244A9618913.en
Kim N-S, Lee H-C (2013) A study on changes and distributions of Korean fir in sub-aline zone. J Korean Environ Restor Technol 16:49–57
Kormutak A, Hong Y-P, Kwon H-Y, Kim C-S (2007) Variation in trn-L/trn-V and trn-F/trn-T spacer regions of cpDNA in Abies koreana Wilson and A. nephrolepis Traut./Maxim. J Korean For Soc 96:131–137
Kormuťák A, Lee S-W, Hong K-N, Yang B-H, Hong Y-P (2008) Crossability relationships between Korean firs Abies koreana, A. nephrolepis and A. holophylla and some other representatives of the genus Abies. Biologia 63:94–99. doi:10.2478/s11756-008-0008-0
Ledig FT, Hodgskiss PD, Johnson DR (2006) Genetic diversity and seed production in Santa Lucia fir (Abies bracteata), a relict of the Miocene broadleaved evergreen forest. Conserv Genet 7:383–398. doi:10.1007/s10592-005-9049-x
Lian C, Goto S, Hogetsu T (2007) Microsatellite markers for Sachalin fir (Abies sachalinensis Masters). Mol Ecol Notes 7:896–898. doi:10.1111/j.1471-8286.2007.01741.x
Loveless MD, Hamrick JL (1984) Ecological determinants of genetic structure in plant populations. Annu Rev Ecol Syst 15:65–95. doi:10.1146/annurev.es.15.110184.000433
Luikart G, Cornuet J-M (1998) Empirical evaluation of a test for identifying recently bottlenecked populations from allele frequency data. Conser Biol 12:228–237. doi:10.1111/j.1523-1739.1998.96388.x
Luikart G, Allendorf F, Cornuet J-M, Sherwin W (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
Montalvo AM, Ellstrand NC (2000) Transplantation of the subshrub Lotus scoparius: testing the home-site advantage hypothesis. Conser Biol 14:1034–1045
O’Connell LM, Ritland K (2004) Somatic mutations at microsatellite loci in western redcedar (Thuja plicata: Cupressaceae). J Hered 95:172–176. doi:10.1093/jhered/esh024
Ottewell KM, Bickerton DC, Byrne M, Lowe AJ (2015) Bridging the gap: a genetic assessment framework for population-level threatened plant conservation prioritization and decision-making. Divers Distrib 22:174–188. doi:10.1111/ddi.12387
Palsbøll PJ, Bérubé M, Allendorf FW (2007) Identification of management units using population genetic data. Trends Ecol Evol 22:11–16. doi:10.1016/j.tree.2006.09.003
Parchman TL, Benkman CW, Jenkins B, Buerkle CA (2011) Low levels of population genetic structure in Pinus contorta (Pinaceae) across a geographic mosaic of co-evolution. Am J Bot 98:669–679. doi:10.3732/ajb.1000378
Peakall ROD, Smouse PE (2006) Genalex 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295. doi:10.1111/j.1471-8286.2005.01155.x
Pimm SL, Gittleman JL, McCracken GF, Gilpin M (1989) Plausible alternatives to bottlenecks to explain reduced genetic diversity. Trends Ecol Evol 4:176–178. doi:10.1016/0169-5347(89)90123-7
Piovani P, Leonardi S, Piotti A, Menozzi P (2010) Conservation genetics of small relic populations of silver fir (Abies alba Mill.) in the northern Apennines. Plant Biosyst 144:683–691. doi:10.1080/11263504.2010.496199
Piry S, Luikart G, Cornuet J-M (1999) Computer note. BOTTLENECK: a computer program for detecting recent reductions in the effective size using allele frequency data. J Hered 90:502–503. doi:10.1093/jhered/90.4.502
Potter KM, Frampton J, Josserand SA, Nelson CD (2008) Genetic variation and population structure in Fraser fir (Abies fraseri): a microsatellite assessment of young trees. Can J For Res 38:2128–2137. doi:10.1139/X08-064
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Putman AI, Carbone I (2014) Challenges in analysis and interpretation of microsatellite data for population genetic studies. Ecol Evol 4(22):4399–4428. doi:10.1002/ece3.1305
Rosenberg NA (2004) Distruct: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138. doi:10.1046/j.1471-8286.2003.00566.x
Schmitt T, Muster C, Schönswetter P (2010) Are disjunct alpine and artic-alpine animal and plant spcies in the western palearctic really “Relics of a cold past”? In: Habel JC, Thorsten A (eds) Relic species phylogeography and conservation biology. Springer, Heidelberg, pp 239–252
Schwartz MK, Luikart G, Waples RS (2007) Genetic monitoring as a promising tool for conservation and management. Trends Ecol Evol 22:25–33. doi:10.1016/j.tree.2006.08.009
Sękiewicz K et al. (2014) Effect of geographic range discontinuity on species differentiation—East-Mediterranean Abies cilicica. Tree Genet Genomes 11:1–10. doi:10.1007/s11295-014-0810-5
Semerikova SA, Semerikov VL, Lascoux M (2011) Post-glacial history and introgression in Abies (Pinaceae) species of the Russian Far East inferred from both nuclear and cytoplasmic markers. J Biogeogr 38:326–340. doi:10.1111/j.1365-2699.2010.02394.x
Song K-M, Kang Y-J, Hyeon H-J (2014) Vegetation structure at the slope direction and charactersitic of seedlings of Abies koreana in Hallasan Mountain. J Environ Sci Int 23:39–46
Szpiech ZA, Jakobsson M, Rosenberg NA (2008) ADZE: a rarefaction approach for counting alleles private to combinations of populations. Bioinformatics 24:2498–2504
Tang S, Dai W, Li M, Zhang Y, Geng Y, Wang L, Zhong Y (2008) Genetic diversity of relictual and endangered plant Abies ziyuanensis (Pinaceae) revealed by AFLP and SSR markers. Genetica 133:21–30. doi:10.1007/s10709-007-9178-x
Wang L, Liu S, Zhuang Z, Guo L, Meng Z, Lin H (2013) Population genetic studies revealed local adaptation in a high gene-flow marine fish, the small yellow croaker (Larimichthys polyactis). Plos One 8:e83493. doi:10.1371/journal.pone.0083493
Wilson GA, Rannala B (2003) Bayesian inference of recent migration rates using multilocus genotypes. Genetics 163:1177–1191
Woo SY (2009) Forest decline of the world: A linkage iwth air pollution and global warming. Afr J Biotechnol 8:7409–7414
Xiang Q-P, Wei R, Shao Y-Z, Yang Z-Y, Wang X-Q, Zhang X-C (2015) Phylogenetic relationships, possible ancient hybridization, and biogeographic history of Abies (Pinaceae) based on data from nuclear, plastid, and mitochondrial genomes. Mol Phylogenet Evol 82(Part A):1–14. doi:10.1016/j.ympev.2014.10.008
Yang J-C, Yi D-K, Joo M-J, Choi K (2015) Phylogenetic study of Abies koreana and Abies nephrolepis in Korea based on mitochondiral DNA. Korean J Plant Taxon 45:254–261
Young A, Boyle T, Brown T (1996) The population genetic consequences of habitat fragmentation for plants. Trends Ecol Evol 11:413–418. doi:10.1016/0169-5347(96)10045-8
Acknowledgements
This research was supported by a grant from the National Institute of Biological Resources (NIBR), funded by the Ministry of Environment (MOE) of the Republic of Korea (#NIBR201507101). We are grateful to the Korea National Park Service for permission to collect valuable samples. The authors thank Dr. Ji Hong An and Ms. Jaram Hong for technical assistance.
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Kwak, M., Hong, JK., Park, J.H. et al. Genetic assessment of Abies koreana (Pinaceae), the endangered Korean fir, and conservation implications. Conserv Genet 18, 1165–1176 (2017). https://doi.org/10.1007/s10592-017-0968-0
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DOI: https://doi.org/10.1007/s10592-017-0968-0