Abstract
Japanese black pine (Pinus thunbergii Parl.) with high salt tolerance may be an important constitutive element sustaining terrestrial ecosystem by playing a role of windbreak forests in coastal areas. Korean peninsula would be a notable region in clarifying distribution shift in Pinus species as it has northern distribution limit of Japanese black pine in Asia. Our main object was to verify genetic evidence of stable northward extension of P. thunbergii populations in DPR Korea. We investigated genetic background of 9 populations existing in Korean peninsula using nuclear SSR markers in relation to shifts in climate factors such as temperature and precipitation. Higher genetic diversity in east group (AR = 10.7 ~ 19.5) and west group (AR = 10.3 ~ 10.7) compared to north group (AR = 6.7 ~ 8.8) was found. When number of putative clusters (K) = 2, whole individuals were divided into west group and north-east group, and when K = 3, north-east group can be separated into north group and east group. Phylogeographic relationship verified by means of nSSR markers suggest that substantial increment of air temperature in DPR Korea allowed stable anthropogenic transfer of P. thunbergii forests and that artificial afforestation may bring rapid establishment of forest ecosystem owing to climate change.
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References
Boys J, Cherry M, Dayanandan S (2005) Microsatellite analysis reveals genetically distinct populations of red pine (Pinus resinosa, Pinaceae). Am J Bot 92(5):833–841
Bridle JR, Vines TH (2007) Limits to evolution at range margins: when and why does adaptation fail? Trends Ecol Evol 22:140–147
Campbell ID, McDonald K, Flannigan MD, Kringayark J (1999) Longdistance transport of pollen into the Arctic. Nature 399:29–30
Cheaib A, Badeau V, Boe J, Chuine I, Delire C, Dufrene E, Francois C, Gritti ES, Legay M, Page C, Thuiller W, Viovy LP (2012) Climate change impacts on tree ranges: model intercomparison facilitates understanding and quantification of uncertainty. Ecol Lett 15:533–544
Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15
El M, Petit A (1996) High level of genetic differentiation for allelic richness among populations of the argan tree [Argania spinosa (L.) Skeels] endemic to Morocco. Theor Appl Genet 92:832–839
Etterson JR, Shaw RG (2010) Constraint to adaptive evolution in response to global warming. Science 294:151–154
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
Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587
Fettig CJ, Mortenson LA, Bulaon BM, Foulk PB (2018) Tree mortality following drought in the central and southern Sierra Nevada, California. US for Ecol Manag 432:164–178
Freire JA, Rodrigues GC, Tome M (2019) Climate change impacts on Pinus pinea L. Silvicultural system for cone production and ways to counter those impacts: a review complemented with data from permanent plots. Forest 10:169
Goudet J (2003) FSTAT (ver. 2.9.4), a program to estimate and test population genetics parameters. https://www2.unil.ch/popgen/softwares/fstat.htm
Graham CH, Ron S, Santos JC, Schneider CJ, Moritz C (2004) Integrating phylogenetics and environmental niche models to explore speciation mechanisms in dendrobatid frogs. Evolution 58:1781–1793
Hickerson MJ, Carstens BC, Cavender-Bares J, Crandall KA, Graham CH, Johnson JB, Rissler L, Victoriano PF, Yoder AD (2010) Phylogeography’s past, present, and future: 10 years after Avise, 2000. Mol Phylogenet Evol 54:291–301
Ho U-H, Song S-R (2020) Did genetic lineage divergence or spatial environmental variance lead to global subspecies differentiation of northern goshawk (Accipiter gentilis). Anim Biol 70:289–308
Hubisz M, Falush D, Stephens M, Pritchard J (2009) Inferring weak population structure with the assistance of sample group information. Mol Ecol Resour 9:1322–1332
Iwaizumi MG, Takahashi M, Isoda K, Austerlitz F (2013) Consecutive five-year analysis of paternal and maternal gene flow and contributions of the gametic heterogeneities to overall genetic composition of Pinus densiflora dispersed seeds. Am J Bot 100:1896–1904
Iwaizumi MG, Miyata S, Hirao T, Tamura M, Watanabe A (2018) Historical seed use and transfer affects geographic specificity in genetic diversity and structure of old planted Pinus thunbergii populations. For Ecol Manag 408:211–219
Jansen S, Konrad H, Geburek T (2017) The extent of historic translocation of Norway spruce forest reproductive material in Europe. Ann for Sci. https://doi.org/10.1007/s13595-017-0644-z
Kang YS, Ryu JG, Kim SC, Ri HJ (2002) Research of age and ancient natural environment of mankind fossil discovered from Kunbong. Thesis Collect Kim Il Sung Univ Nat Sci 48(12):91–97
Kassa A, Konrad H, Geburek T (2017) Landscape genetic structure of Olea europaea subsp. cuspidata in Ethiopian highland forest fragments. Conserv Genet 18(6):1463–1474
Keenan T, Serra JM, Lloret F, Nilyerola M, Sabate S (2010) Predicting the future of forests in the Mediterranean under climate change, with niche- and process-based models: CO2 matters! Glob. Change Biol 10:1365–2486
Kirkpatrick M, Barton NH (1997) Evolution of a species range. Am Nat 150:1–23
Konta F (2001) The present conditions and functions of the coastal forests in Japan. J Jpn Soc Coast for 1:1–4
Lech U, Aleksandra WP, Konrad C, Paulina L, Ewa P, Algis A (2019) Genetic resources of relict populations of Pinus sylvestris (L.) in Western Carpathians assessed by chloroplast microsatellites. Biologia 74:1077–1086
Lenoir J, Gegout JC, Marquet PA, De Ruffray P, Brise H (2008) A significant upward shift in plant species optimum elevation during 20th century. Science 320:1768–1771
Li HY, Jiang J, Liu GF, Ma XJ, Dong JX, Lin SJ (2005) Genetic variation and division of Pinus sylvestris provenances by ISSR markers. J for Res 16(3):216–218
Mao P, Guo L, Gao Y, Qi L, Cao B (2019) Effects of seed size and sand burial on germination and early growth of seedlings for coastal Pinus thunbergii Parl. In the Northern Sandong Peninsula, China. Forests 10:281
Misi D, Puchalka R, Pearson C, Robertson I, Koprowski M (2019) Differences in the climate-growth relationship of scots pine: a case study from poland and hungary. Forersts 10:243
Murai H, Ishikawa M, Endo J, Tadaki Y (1992) The coastal forest in Japan. Soft Science Inc, Tokyo
Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York
Newman CE, Rissler LJ (2011) Phylogenetic analyses of the southern leopard frog: the impact of the geography and climate on the distribution of genetic lineages vs. subspecies. Mol Ecol 20:5295–5312
Ogawa M (1979) Microbial flora in Pinus thunbergii forest of coastal sand dune. Bull for Prod Res Inst 305:107–124
Om GC, Ren G, Jong SI, Li S, Ryang CH, Zhang P (2019) Long-term change in surface air temperature over DPR Korea, 1918–2015. Theor Appl Climatol 138:363–372
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Pritchard JK, Wen X, Falush D (2009) STRUCTURE version 2.3.1 [computer program]. Available from:http://pritch.bsd.uchicago.edu/structure.html
Raffl H, Konrad H, Curtu LA, Geburek T (2018) Genetic evidence of human mediated, historical seed transfer from the Tyrolean Alps to the Romanian Carpathians in Larix decidua (Mill) forests. Ann for Sci. https://doi.org/10.1007/s13595-018-0776-9
Robledo-Arnuncio JJ (2011) Wind pollination over mesoscale distances: an investigation with Scots pine. New Phytol 190:222–233
Rogers SO, Bendich AJ (1988) Extraction of DNA from plant tissues. Plant Mol Biol (manual) A6:1–10
Rosell JA, Olson ME, Weeks A, De-Nova JA, Medina-Lemos R, Pérez-Camacho J, Feria TP, Gómez-Bermejo R, Montero JC, Eguiarte LE (2010) Diversification in species complexes: tests of species origin and delimitation in the Bursera simaruba clade of tropical trees (Burseraceae). Mol Phylogenet Evol 57:798–811
Ruiz-Sanchez E, Sosa V (2010) Delimiting species boundaries within the Neotropical bamboo Otatea (Poaceae: Bambusoideae) using molecular, morphological and ecological data. Mol Phylogenet Evol 54(912):344–356
Soberón J, Peterson AT (2005) Interpretation of models of fundamental ecological niches and species’ distributional areas. Biodivers Inf 2:1–10
Thuiller W (2003) BIOMOD – optimizing predictions of species distributions and projecting potential future shifts under global change. Glob Change Biol 9:1353–1362
Varis S, Pakkanen A, Galofré A, Pulkkinen P (2009) The extent of southnorth pollen transfer in Finnish Scots pine. Silva Fenn 43:717–726
Wiens JJ, Graham CH (2005) Niche conservatism: integrating evolution, ecology, and conservation biology. Annu Rev Ecol Evol S 36:519–539
Williams CG (2010) Long-distance pine pollen still germinates after meso-scale dispersal. Am J Bot 97:846–855
Yang YX, Wang ML, Liu ZL, Zhu J, Yan MY (2016) Nucleotide polymorphism and phylogeographic history of an endangered conifer species Pinus bungeana. Biochem Syst Ecol 64:89–96
Yeh FC, Boyle TJB (1997) Population genetic analysis of co-dominant and dominant markers and quantitative traits. Belg J Bot 29:157
Zhu J, Matsuzaki T, Sakioka K (2000) Windspeeds within a single crown of Japanese black pine (Pinus thunbergii Parl.). For Ecol Manage 135:19–31
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We thank all volunteers who collected samples and assisted laboratory work and data analysis.
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UH and SS designed the study and conducted the experiments, and HP, KK, TH and IJ analyzed the data; UH and SS collected data and wrote the first draft; and all authors contributed to revisions substantially.
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Ho, UH., Song, SR., Pak, HS. et al. Genetic evidence of stable northward extension of Pinus thunbergii Parl. forests in the Democratic People’s Republic of Korea. Genet Resour Crop Evol 69, 2105–2114 (2022). https://doi.org/10.1007/s10722-022-01359-w
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DOI: https://doi.org/10.1007/s10722-022-01359-w