Contrasting patterns of nuclear microsatellite genetic structure of Fraxinus mandshurica var. japonica between northern and southern populations in Japan
Corresponding Author
Li-Jiang Hu
Laboratory of Forest Ecosystem Studies, Department of Ecosystem Studies, Graduate School of Agricultural and Life Sciences, The University of Tokyo, Yayoi 1-1-1, Bunkyo-ku, Tokyo 113-8657, Japan
Biotechnology Institute of Daqing, College of Life Sciences, Northeast Forestry University, Hexing Road 26, Harbin 150040, China
Li-Jiang Hu, Laboratory of Forest Ecosystem Studies, Department of Ecosystem Studies, Graduate School of Agricultural and Life Sciences, The University of Tokyo, Yayoi 1-1-1, Bunkyo-ku, Tokyo 113-8657, Japan.E-mail: [email protected]Search for more papers by this authorKentaro Uchiyama
Laboratory of Forest Ecosystem Studies, Department of Ecosystem Studies, Graduate School of Agricultural and Life Sciences, The University of Tokyo, Yayoi 1-1-1, Bunkyo-ku, Tokyo 113-8657, Japan
Tree Genetics Laboratory, Department of Forest Genetics, Forestry and Forest Products Research Institute, Matsunosato 1, Tsukuba, Ibaraki 305-8687, Japan
Search for more papers by this authorYoko Saito
Laboratory of Forest Ecosystem Studies, Department of Ecosystem Studies, Graduate School of Agricultural and Life Sciences, The University of Tokyo, Yayoi 1-1-1, Bunkyo-ku, Tokyo 113-8657, Japan
Search for more papers by this authorYuji Ide
Laboratory of Forest Ecosystem Studies, Department of Ecosystem Studies, Graduate School of Agricultural and Life Sciences, The University of Tokyo, Yayoi 1-1-1, Bunkyo-ku, Tokyo 113-8657, Japan
Search for more papers by this authorCorresponding Author
Li-Jiang Hu
Laboratory of Forest Ecosystem Studies, Department of Ecosystem Studies, Graduate School of Agricultural and Life Sciences, The University of Tokyo, Yayoi 1-1-1, Bunkyo-ku, Tokyo 113-8657, Japan
Biotechnology Institute of Daqing, College of Life Sciences, Northeast Forestry University, Hexing Road 26, Harbin 150040, China
Li-Jiang Hu, Laboratory of Forest Ecosystem Studies, Department of Ecosystem Studies, Graduate School of Agricultural and Life Sciences, The University of Tokyo, Yayoi 1-1-1, Bunkyo-ku, Tokyo 113-8657, Japan.E-mail: [email protected]Search for more papers by this authorKentaro Uchiyama
Laboratory of Forest Ecosystem Studies, Department of Ecosystem Studies, Graduate School of Agricultural and Life Sciences, The University of Tokyo, Yayoi 1-1-1, Bunkyo-ku, Tokyo 113-8657, Japan
Tree Genetics Laboratory, Department of Forest Genetics, Forestry and Forest Products Research Institute, Matsunosato 1, Tsukuba, Ibaraki 305-8687, Japan
Search for more papers by this authorYoko Saito
Laboratory of Forest Ecosystem Studies, Department of Ecosystem Studies, Graduate School of Agricultural and Life Sciences, The University of Tokyo, Yayoi 1-1-1, Bunkyo-ku, Tokyo 113-8657, Japan
Search for more papers by this authorYuji Ide
Laboratory of Forest Ecosystem Studies, Department of Ecosystem Studies, Graduate School of Agricultural and Life Sciences, The University of Tokyo, Yayoi 1-1-1, Bunkyo-ku, Tokyo 113-8657, Japan
Search for more papers by this authorAbstract
Aim The aim of this study is to detect extant patterns of population genetic structure of Fraxinus mandshurica var. japonica in Japan, and to provide insights into the post-glacial history of this species during the Holocene.
Location Hokkaido and Honshu islands, Japan (including the Oshima and Shimokita peninsulas).
Methods We examined nine polymorphic nuclear microsatellite loci to assess genetic variation within and among 15 populations across almost the entire range of the species in Japan. Extant patterns of geographical structure were analysed using Bayesian clustering, Monmonier’s algorithm, analysis of molecular variance, Mantel tests and principal coordinates analysis. Recent bottlenecks within populations and regional genetic variation were also assessed.
Results Northern populations (Hokkaido Island and the Shimokita Peninsula) formed a single homogeneous deme, maintaining the highest level of allelic diversity on the Oshima Peninsula. By contrast, southern populations (Honshu Island) demonstrated strong substructure on both coasts. Specifically, populations on the Pacific side of Honshu exhibited significant bottlenecks and erosion of allelic diversity but preserved distinct subclusters diverging from widespread subclusters on the Japan Sea side of this island.
Main conclusions Genetic evidence and life history traits suggest that F. mandshurica occupied cryptic northern refugia on the Oshima Peninsula during the Last Glacial Maximum, which is reflected in the species’ extant northern distribution. Strong geographical structure in southern populations, in agreement with fossil pollen records, suggests geographical isolation by mountain ranges running north–south along Honshu. Given that this tree species is cold-adapted and found in riparian habitats, populations on the Pacific side of Honshu probably contracted into higher-elevation swamps during warm post-glacial periods, leading to a reduction of effective population sizes and rare allelic richness.
Supporting Information
Appendix S1 Pairwise Fst and significance test based on estimates of multilocus genotypes of 15 natural Fraxinus mandshurica var. japonica populations in Japan.
Appendix S2 Population structure of Fraxinus mandshurica var. japonica inferred from Bayesian clustering.
As a service to our authors and readers, this journal provides supporting information supplied by the authors. Such materials are peer-reviewed and may be re-organized for online delivery, but are not copy-edited or typeset. Technical support issues arising from supporting information (other than missing files) should be addressed to the authors.
Filename | Description |
---|---|
JBI_2275_sm_AppendixS1-S2.doc76 KB | Supporting info item |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
References
- Aizawa, M., Yoshimaru, H, Saito, H., Katsuki, T., Kawahara, T., Kitamura, K., Shi, F., Sabirov, R. & Kaji, M. (2009) Range-wide genetic structure in a north-east Asian spruce (Picea jezoensis) determined using nuclear microsatellite markers. Journal of Biogeography, 36, 996–1007.
- Barton, N.H. & Slatkin, M. (1986) A quasi-equilibrium theory of the distribution of rare alleles in a subdivided population. Heredity, 56, 409–415.
- Besnard, G., Khadari, B., Baradt, P. & Bervillé, A. (2002) Olea europaea (Oleaceae) phylogeography based on chloroplast DNA polymorphism. Theoretical and Applied Genetics, 104, 1353–1361.
- Bhagwat, S.A. & Willis, K.J. (2008) Species persistence in northerly glacial refugia of Europe: a matter of chance or biogeographical traits? Journal of Biogeography, 35, 464–482.
- Brachet, S., Jubier, M.F., Richard, M., Jung-Muller, B. & Frascaria-Lacoste, N. (1999) Rapid identification of microsatellite loci using 5′ anchored PCR in the common ash Fraxinus excelsior. Molecular Ecology, 8, 160–163.
- Comes, H.P. & Kadereit, J.W. (1998) The effect of Quaternary climatic changes on plant distribution and evolution. Trends in Plant Science, 3, 432–438.
- Cornuet, J.M. & Luikart, G. (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics, 144, 2001–2014.
- Dieringer, D. & Schlötterer, C. (2003) Microsatellite analyser (MSA): a platform independent analysis tool for large microsatellite data sets. Molecular Ecology Notes, 3, 167–169.
- Evanno, G., Regnaut, S. & Goudet, J. (2005) Detecting the number of clusters of individuals using the software structure: a simulation study. Molecular Ecology, 14, 2611–2620.
- Excoffier, L., Smouse, P.E. & Quattro, J.M. (1992) Analysis of molecular variance inferred from metric distance among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics, 131, 479–491.
- Falush, D., Stephens, M. & Pritchard, J.K. (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics, 164, 1567–1587.
- Frankham, R. (2005) Genetics and extinction. Biological Conservation, 126, 131–140.
- Fujii, N., Tomaru, N., Okuyama, K., Koike, T., Mikami, T. & Ueda, K. (2002) Chloroplast DNA phylogeography of Fagus crenata (Fagaceae) in Japan. Plant Systematics and Evolution, 232, 21–33.
- Goto, S., Shimatani, K., Yoshimaru, H. & Takahashi, Y. (2006) Fat-tailed gene flow in the dioecious canopy tree species Fraxinus mandshurica var. japonica revealed by microsatellites. Molecular Ecology, 15, 2985–2996.
- Goudet, J. (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). Available at: http://www2.unil.ch/popgen/softwares/fstat.htm (accessed 2 November 2009).
- Hampe, A. & Petit, R.J. (2005) Conserving biodiversity under climate change: the rear edge matters. Ecology Letters, 8, 461–467.
- Harbourne, M.E., Douglas, G.C., Waldren, S. & Hodkinson, T.R. (2005) Characterization and primer development for amplification of chloroplast microsatellite regions of Fraxinus excelsior. Journal of Plant Research, 118, 339–341.
- Heuertz, M. (2003) Population genetic structure in common ash: a focus on southeastern European genetic resources. PhD Thesis, Free University of Brussels, Belgium, and Public Research Centre-Gabriel Lippmann, Luxembourg.
- Heuertz, M., Carnevale, S., Fineschi, S., Sebastiani, F., Hausman, J.F., Paule, L. & Vendramin, G.G. (2006) Chloroplast DNA phylogeography of three European ashes, Fraxinus sp. (Oleaceae): roles of hybridization and contrasting mating systems. Molecular Ecology, 15, 2131–2140.
- Heuertz, M., Fineschi, S., Anzidei, M., Pastorelli, R., Salvini, D., Paule, L., Frascaria-Lacoste, N., Hardy, O.J., Vekemans, X. & Vendramin, G.G. (2004a) Chloroplast DNA variation and postglacial recolonization of common ash (Fraxinus excelsior L.) in Europe. Molecular Ecology, 13, 3437–3452.
- Heuertz, M., Hausman, J.F, Hardy, O.J, Vendramin, G.G, Frascaria-Lacosite, N. & Vekemans, X. (2004b) 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.M. (1996) Some genetic consequences of ice ages, and their role in divergence and speciation. Biological Journal of the Linnean Society, 58, 247–276.
- Hewitt, GM. (2000) The genetic legacy of the Quaternary ice ages. Nature, 405, 907–913.
- Hiraoka, K. & Tomaru, N. (2009) Genetic divergence in nuclear genomes between populations of Fagus crenata along the Japan Sea and Pacific sides of Japan. Journal of Plant Research, 122, 269–282.
- Hu, L.-J., Uchiyama, K., Shen, H.-L., Saito, Y., Tsuda, Y. & Ide, Y. (2008) Nuclear DNA microsatellites reveal genetic variation but a lack of phylogeographical structure in an endangered species, Fraxinus mandshurica, across North-east China. Annals of Botany, 102, 195–205.
- Hu, L.-J., Uchiyama, K., Shen, H.-L. & Ide, Y. (2010) Multiple-scaled spatial genetic structures of Fraxinus mandshurica over a riparian-mountain landscape in Northeast China. Conservation Genetics, 11, 77–87.
- Hurlbert, S.H. (1971) The nonconcept of species diversity: a critique and alternative parameters. Ecology, 52, 577–586.
- Hutchison, D.W. & Templeton, A.R. (1999) Correlation of pairwise genetic and geographic distance measures: inferring the relative influences of gene flow and drift on the distribution of genetic variability. Evolution, 53, 1898–1914.
- Kong, D.-M. (2004) Somatic embryogenesis and development of somatic and zygotic embryos of Fraxinus mandshurica. PhD Thesis, Northeast Forestry University, China (in Chinese with English abstract).
- Lascoux, M., Palmé, A.E., Cheddadi, R. & Latta, R. (2004) Impact of the ice ages on the genetic structure of trees and shrubs. Philosophical Transactions of the Royal Society B: Biological Sciences, 359, 197–207.
- Lefort, F., Brachet, S., Frascaria-Lacoste, N., Edwards, K.J. & Douglas, G.C. (1999) Identification and characterisation of microsatellite loci in ash (Fraxinus excelsior L.) and their conservation in the olive family (Oleaceae). Molecular Ecology, 8, 1088–1091.
- Lian, C., Oishi, R., Miyashita, N., Nara, K., Nakaya, H., Wu, B., Zhou, Z. & Hogetsu, T. (2003) Genetic structure and reproduction dynamics of Salix reinii during primary succession on Mount Fuji, as revealed by nuclear and chloroplast microsatellite analysis. Molecular Ecology, 12, 609–618.
- Magri, D., Vendramin, G.G., Comps, B., Dupanloup, I., Geburek, T., Gömöry, D., Latałowa, M., Litt, T., Paule, L., Roure, J.M., Tantau, I., van der Knaap, W.O., Petit, R.J. & de Beaulieu, J.-L. (2006) A new scenario for the Quaternary history of European beech populations: palaeobotanical evidence and genetic consequences. New Phytologist, 171, 199–221.
- Maliouchenko, O., Palmé, A.E., Buonamici, A., Vendramin, G.G. & Lascoux, M. (2007) Comparative phylogeography and population structure of European Betula species, with particular focus on B. pendula and B. pubescens. Journal of Biogeography, 34, 1601–1610.
- Manni, F., Guérard, E. & Heyer, E. (2004) Geographic patterns of (genetic, morphologic, linguistic) variation: how barriers can be detected by using Monmonier’s algorithm. Human Biology, 76, 173–190.
- Mantel, N.A. (1967) The detection of disease clustering and a generalized regression approach. Cancer Research, 27, 209–220.
- Maudet, C., Miller, C., Bassano, B., Breitenmoser-Wursten, C., Gauthier, D., Obexer-Ruff, G., Michallet, J., Taberlet, P. & Luikart, G. (2002) Microsatellite DNA and recent statistical methods in wildlife conservation management: applications in Alpine ibex [Capra ibex (ibex)]. Molecular Ecology, 11, 421–436.
-
Monmonier, M. (1973) Maximum-difference barriers: an alternative numerical regionalization method.
Geographical Analysis, 3, 245–261.
10.1111/j.1538-4632.1973.tb01011.x Google Scholar
- Nei, M., Maruyama, T. & Chakraborty, R. (1975) The bottleneck effect and genetic variability in populations. Evolution, 29, 1–10.
- Nei, M., Tajima, F. & Tateno, Y. (1983) Accuracy of estimated phylogenic trees from molecular data. Journal of Molecular Evolution, 19, 153–170.
- O’Brien, S.J. (1994) Genetic and phylogenetic analyses of endangered species. Annual Review of Genetics, 28, 467–489.
-
Ohmori, H. &
Yanagimachi, O. (1988) Thermal conditions both of the upper and lower limits of the Fagus crenata forest zone, and changes in summer temperature from the latest Pleistocene to the Middle Holocene in Japan.
The Quaternary Research, 27, 81–100
(in Japanese with English abstract).
10.4116/jaqua.27.81 Google Scholar
-
Ohshima, K. (1990) The history of straits around the Japanese islands in the late-Quaternary.
The Quaternary Research, 29, 193–208
(in Japanese with English abstract).
10.4116/jaqua.29.193 Google Scholar
- Okaura, T. & Harada, K. (2002) Phylogeographical structure revealed by chloroplast DNA variation in Japanese beech (Fagus crenata Blume). Heredity, 88, 322–329.
- Okaura, T., Quang, N.C., Ubukata, M. & Harada, K. (2007) Phylogeographic structure and late Quaternary population history of the Japanese oak Quercus mongolica var. crispula and related species revealed by chloroplast 16 DNA variation. Genes & Genetic Systems, 82, 465–477.
- Peakall, R. & Smouse, P.E. (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes, 6, 288–295.
- Petit, R.J., Aguinagalde, I., de Beaulieu, J.L., Bittkau, C., Brewer, S., Cheddadi, R., Ennos, R.A., Fineschi, S., Grivet, D., Lascoux, M., Mohanty, A., Müller-Starck, G., Musch, B., Palme, A., Martin Clemente, 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., Duminil, J., Fineschi, S., Hampe, A., Salvini, D. & Vendramin, G.G. (2005) Comparative organization of chloroplast, mitochondrial and nuclear diversity in plant populations. Molecular Ecology, 14, 689–702.
- Piry, S., Luikart, G. & Cornuet, J.M. (1999) BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data. Journal of Heredity, 90, 499–503.
- Pritchard, J.K., Stephens, M. & Donnelly, P. (2000) Inference of population structure using multilocus genotype data. Genetics, 155, 945–959.
- Pritchard, J.K., Wen, X.Q. & Falush, D. (2007) STRUCTURE (Version 2.2). University of Chicago, Chicago, IL. Available at: http://pritch.bsd.uchicago.edu/software (accessed 2 November 2009).
- Provan, J. & Bennett, K.D. (2008) Phylogeographic insights into cryptic glacial refugia. Trends in Ecology and Evolution, 23, 564–570.
- Rice, W.R. (1989) Analyzing tables of statistical tests. Evolution, 43, 223–225.
- Rousset, F. (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics, 145, 1219–1228.
- Rousset, F. (2008) genepop’007: a complete re-implementation of the genepop software for Windows and Linux. Molecular Ecology Resources, 8, 103–106.
-
Sakio, H. &
Yamamoto, F. (2008) Ecology of riparian forests in japan: disturbance, life-history and regeneration. Springer, Tokyo.
10.1007/978-4-431-76737-4 Google Scholar
-
Sasaki, T.,
Sugai, T.,
Yanagida, M.,
Morita, Y.,
Furusawa, A.,
Moriya, T.,
Nakagawa, T. &
Miyagi, T. (2006) Reconstruction of depositional environment and paleoclimate changes from a small basin deposit during the past 300,000 years, central Japan.
The Quaternary Research, 45, 275–286
(in Japanese with English abstract).
10.4116/jaqua.45.275 Google Scholar
- Stewart, J.R. & Lister, A.M. (2001) Cryptic northern refugia and the origins of the modern biota. Trends in Ecology and Evolution, 16, 608–613.
- 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.
- Takahashi, T., Tani, N., Taira, H. & Tsumura, Y. (2005) Microsatellite markers reveal high allelic variation in natural populations of Cryptomeria japonica near refugial areas of the last glacial period. Journal of Plant Research, 118, 83–90.
- Takahashi, Y., Goto, S., Kasahara, H., Inukai, M., Takada, N., Iguchi, K. & Shibano, S. (2001) Sex expressions and size structures of a dioecious canopy tree species, Fraxinus mandshurica var. japonica. Journal of Japanese Forestry Society, 83, 334–339 (in Japanese).
-
Takiya, M. &
Hagiwara, N. (1997) Vegetational history of Mt. Yokotsudake, southwestern Hokkaido, since the Last Glacial.
The Quaternary Research, 36, 217–234
(in Japanese with English abstract).
10.4116/jaqua.36.217 Google Scholar
- Terhürne-Berson, R., Litt, T. & Cheddadi, R. (2004) The spread of Abies throughout Europe since the last glacial period: combined macrofossil and pollen data. Vegetation History and Archaeobotany, 13, 257–268.
- Tsuda, Y. & Ide, Y. (2005) Wide-range analysis of genetic structure of Betula maximowicziana, a long-lived pioneer tree species and noble hardwood in the cool temperate zone of Japan. Molecular Ecology, 14, 3929–3941.
- Tsuda, Y. & Ide, Y. (2009) Chloroplast DNA phylogeography of Betula maximowicziana, a long-lived pioneer tree species and noble hardwood in Japan. Journal of Plant Research, doi: 10.1007/s10265-009-0280-2.
- Tsukada, M. (1981) The last 12,000 years – the vegetation history of Japan. II. New pollen zones. Japanese Journal of Ecology, 31, 201–215 (in Japanese with English abstract).
- Tsukada, M. (1982a) Late-Quaternary development of Fagus forest in the Japanese Archipelago. Japanese Journal of Ecology, 32, 113–118.
- Tsukada, M. (1982b) Late-Quaternary shift of Fagus distribution. Botanical Magazine, Tokyo, 95, 203–217.
- Tsumura, Y. (2006) The phylogeographic structure of Japanese coniferous species as revealed by genetic markers. Taxon, 55, 53–66.
- Tzedakis, P.C., Lawson, I.T., Frogley, M.R., Hewitt, G.M. & Preece, R.C. (2002) Buffered tree population changes in a Quaternary refugium: evolutionary implication. Science, 297, 2044–2047.
- Verdú, M., González-Martínez, S.C., Montilla, A.I., Mateu, I. & Pannell, J.R. (2006) Ovule discounting in an outcrossing, cryptically dioecious tree. Evolution, 60, 2056–2063.
- Weir, B.S. & Cockerham, C.C. (1984) Estimating F-statistics for the analysis of population structure. Evolution, 38, 1358–1370.
- Widmer, A. & Lexer, C. (2001) Glacial refugia: sanctuaries for allelic richness, but not for gene diversity. Trends in Ecology and Evolution, 16, 267–269.
- Willis, K.J., Rudner, E. & Sümegi, P. (2000) The full glacial forests of central and southeastern Europe. Quaternary Research, 53, 203–213.
- Willis, K.J. & Van Andel, T.H. (2004) Trees or no trees? The environments of central and eastern Europe during the last glaciation. Quaternary Science Reviews, 23, 2369–2387.
- Wright, S. (1943) Isolation by distance. Genetics, 28, 114–138.
- Wu, Z.-Y. (1980) Vegetation of China. Chinese Science Press, Beijing (in Chinese).
- Yamamoto, F., Sakata, T. & Terazawa, K. (1995) Physiological, morphological and anatomical responses of Fraxinus mandshurica seedlings to flooding. Tree Physiology, 15, 713–719.
- Yasuda, Y. & Miyoshi, N. (1998) Vegetational history in the Japanese Archipelago. Asakura Publishing Company, Tokyo (in Japanese).
- Yu, G., Chen, X., Ni, J. et al. (2000) Palaeovegetation of China: a pollen data-based synthesis for the mid-Holocene and last glacial maximum. Journal of Biogeography, 27, 635–664.