Ko Harada, Fifi Gus Dwiyanti, Iskandar Zulkarnaen Siregar, Atok Subiakto, Lucy Chong, Bibian Diway, Ying-Fah Lee, Ikuo Ninomiya, Koichi Kamiya


Large-scale genetic structure revealed in tree populations in SE Asia, as well as in many temperate forests, has been shaped by climatic fluctuation in the late Pleistocene, most importantly by that in the last glacial period. In a comparative study of the phylogeographic patterns of two closely related dipterocarp species, Dryobalanops aromatica C.F.Gaertn. and D. beccarii Dyer, we investigated how changes in land area associated with changes in climate affected large-scale genetic structure. We examined the genetic variation of D. aromatica, collected from nine populations throughout the Sundaic region, and of D. beccarii, collected from 16 populations mainly in Borneo, using seven polymorphic microsatellite markers. The two species were clearly distinguishable in the STRUCTURE analysis, although hybridisation probably occurred in sympatric populations and also in several other populations. The D. aromatica populations were divided into two main groups by the STRUCTURE analysis: Malay–Sumatra and Borneo. Mixing of the Sumatra and Borneo clusters occurred on the Malay Peninsula, supporting the hypothesis that tropical rainforests expanded over a dried Sunda Shelf during the last glacial period. The two main genetic clusters might have been formed by repeated cycles of fluctuation in land area. The D. beccarii populations in Borneo were divided into four geographically distinct groups: western Sarawak, central inland Sarawak, central coastal Sarawak and Sabah. The population on the Malay Peninsula (Gunung Panti) was an admixture of the four Bornean clusters. This suggests that this population is a relic of the recent range expansion of D. beccarii during the last glacial period.

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ANTAO, T., LOPES, A., LOPES, R., BEJA-PEREIRA, A. & LUIKART, G. (2008). LOSITAN: a workbench to detect molecular adaptation based on a FT-outlier method. BMC Bioinforma, 9: 323.

APPANAH, S. & TURNBULL, J.M. (1998). A Review of Dipterocarps: Taxonomy, Ecology and Silviculture. Center for International Forestry Research, Bogor.

ASHTON, P.S. (1982). Dipterocarpaceae. In: VAN STEENIS, C.G.G.J. (ed.). Flora Malesiana, ser. 1, Spermat. 9, pt. 2. Martinus Nijhoff, The Hague, pp. 237–552.

BÄNFER, G., MOOG, U., FIALA, B., MOHAMED, M., WESING, K. & BLATTNER, F.R. (2006). A chloroplast genealogy of myrmecophytic Macaranga species (Euphorbiaceae) in Southeast Asia reveals hybridisation, vicariance and long distance dispersals. Molecular Ecology, 15: 4409–4424.

BEAUMONT, M.A. & NICHOLS, R.A. (1996). Evaluating loci for use in the genetic analysis of population structure. Proceedings of the Royal Society B, 263: 1619–1626.

CANNON, C.H. & MANOS, P.S. (2003). Phylogeography of the Southeast Asian stone oaks (Lithocarpus). Journal of Biogeography, 30: 211–226.

CANNON, C.H., MORLEY, R.J. & BUSH, A.B.G. (2009). The current refugial rainforests of Sundaland are unrepresentative of their biogeographic past and highly vulnerable to disturbance. Proceedings of the National Academy of Sciences U.S.A., 106: 11188–11193.

CHUA, L.S.L., SHHAIDA, M., HAMIDAH, M. & SAW, L.G. (2010). Malaysia Plant Red List, Peninsular Malaysian Dipterocarpaceae. Research Pamphlet No. 129. Forest Research Institute Malaysia, Kepong.

COMES, H.P. & KADEREIT, J.W. (1998). The effect of Quaternary climate changes on plant distribution and evolution. Trends in Plant Science, 3: 432–438.

CONSERVATION INTERNATIONAL (2010). Available online: (accessed 1 February 2018).

CORLETT, R.T. (2014). The Ecology of Tropical East Asia (2nd edn). Oxford University Press, Oxford.

CORNUET, J.M. & LUIKART, G. (1998). Description and power analysis of two tests for detecting population bottlenecks from allele frequencies. Genetics, 144: 2001–2014.

CURRAT, M., RUEDI, M., PETIT, R.J.J. & EXCOFFIER, L. (2008). The hidden side of invasions: massive introgression by local genes. Evolution, 62: 1908–1920.

DE MORAIS, C.T. & 11 others (2015). Understanding local patterns of genetic diversity in dipterocarps using a multi-site, multi-species approach: Implications for forest management and restoration. Forest Ecology and Management, 356: 153–165.

DIERINGER, D. & SCHLÖTTERER, C. (2003). MICROSATELLITE ANALYSER (MSA): a platform independent analysis tool for large microsatellite data sets. Molecular Ecology Resources, 3: 167–169.

DOYLE, J.J. & DOYLE, J.L. (1990). Isolation of plant DNA from fresh tissue. Focus, 12: 13–15.

DWIYANTI, F.G., CHONG, L., DIWAY, B., LEE, Y.F., SIREGAR, I.Z., ATOK, S., KAMIYA, K., NINOMIYA, I. & HARADA, K. (2015). Population genetic diversity in the genus Dryobalanops Gaertn. f. (Dipterocarpaceae) based on nuclear microsatellite markers. J-SustaiN, 3: 12–20.

EARL, D.A. & VON HOLDT, B.M. (2012). STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources, 4: 359–361.

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.

FAO (2010). Global Forest Resources Assessment 2010. United Nations Food and Agriculture Organization, Rome. Available online: (accessed 3 September 2017).

FINGER, A., KETTLE, C.J., KAISER-BUNBURY, C.N., VALENTIN, T., MOUGAL, J. & GHAZOUL, J. (2012). Forest fragmentation genetics in a formerly widespread island endemic tree: Vateriopsis seychellarum (Dipterocarpaceae). Molecular Evolution, 21: 2369–2382.

FUKUE, Y., KADO, T., LEE, S.-L., NG, K.K.S., MUHAMMAD, N. & TSUMURA, Y. (2007). Effects of flowering tree density on the mating system and gene flow in Shorea leprosula (Dipterocarpaceae) in Peninsular Malaysia. Journal of Plant Research, 120: 413–420.

GHAZOUL, J. & SHEIL, D. (2010). Tropical Rain Forest Ecology, Diversity, and Conservation. Oxford University Press, Oxford.

GORONG, A.J., SINAGA, M.H. & ENGSTROM, M.D. (2004). Vicariance or dispersal? Historical biogeography of three Sunda shelf murine rodents (Maxomys surifer, Leopoldamys sabanus and Maxomys whiteheadi). Biological Journal of the Linnean Society, 81: 91–109.

GOUDET, J. (2001). FSTAT (version Available online: (accessed 30 September 2016).

HAMRICK, J.L., GODT, M.J.W. & SHERMAN-BROYLES, S.L. (1992). Factors influencing levels of genetic diversity in woody plant species. New Forests, 6: 95–124.

HANSEN, M.C., STEHMAN, S.V. & POTAPOV, P.V. (2010). Quantification of global gross forest cover loss. Proceedings of the National Academy of Sciences of the USA, 107: 8650–8655.

HARATA, T., NANAMI, S., YAMAKURA, T., MATSUYAMA, S., DIWAY, B.M., TAN, S. & ITOH, A. (2011). Fine-scale spatial genetic structure of ten Dipterocarp tree species in a Bornean rain forests. Biotropica. doi: 10.1111/j.1744-1729.2011.00836.x

HEANEY, L.R. (1991). A synopsis of climatic and vegetational change in Southeast Asia. Climate Change, 19: 53–61.

HEUERTZ, M., HUSMAN, J.-F., JARDY, 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.M. (2000). The genetic legacy of the Quaternary ice ages. Nature, 405: 907–913.

ISHIYAMA, H., INOMATA, N., YAMAZAKI, T., SHUKOR, N.A.A. & SZMIDT, A.E. (2008). Demographic history and interspecific hybridization of four Shorea species (Dipterocarpaceae) from Peninsula Malaysia inferred from nucleotide polymorphism in nuclear gene regions. Canadian Journal of Forest Research, 38: 996–1007.

ISMAIL, S.A., GHAZOUL, J., RAVIKANTH, G., UMA SHAANKER, R., KUSHALAPPA, C.G. & KETTLE, C.J. (2012). Does long-distance pollen dispersal preclude inbreeding in tropical trees? Fragmentation genetics of Dysoxylum malabaricum in an agro-forest landscape. Molecular Ecology, 21: 5484–5496.

IUCN (2017).The IUCN Red List of Threatened Species. Version 2017-1. Available online: (accessed 12 May 2017).

IWANAGA, H., TESHIMA, K.M., KHTAB, I.A., INOMATA, N., FINKELDEY, R., SIREGAR, I.Z., SIREGAR, U.J. & SZMIDT, A.E. (2012). Population structure and demographic history of a tropical lowland rainforest tree species Shorea parvifolia (Dipterocarpaceae) from Southeastern Asia. Ecology and Evolution, 2: 1663–1675.

JAKOBSSON, M. & ROSENBERG, N.A. (2007). CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics, 23: 1801–1806.

KAMIYA, K., GAN, Y.Y., SHAWN, K., LUM, Y., KHOO, M.S., CHUA, S.C. & FAIZU, N.N.K. (2011). Morphological and molecular evidence of natural hybridization in Shorea (Dipterocarpaceae). Tree Genetics & Genomes, 7: 293–306.

KAMIYA, K. & 10 others (2012). Demographic history of Shorea curtisii (Dipterocarpaceae) inferred from chloroplast DNA sequence variations. Biotropica, 44: 577–585.

KETTLE, C.J., HOLLINGSWORTH, P.M., BURSLEM, D.F.R.P., MAYCOCK, C.R., KHOO, E. & GHAZOUL, J. (2011). Determinants of fine-scale spatial genetic structure in three co-occurring rain forest canopy trees in Borneo. Perspectives in Plant Ecology, Evolution and Systematics, 13: 45–54.

KETTLE, C.J., MAYCOCK, C.R. & BURSLEM, D. (2012). New directions in Dipterocarp biology and conservation: A synthesis. Biotropica, 44: 658–660.

LANGNER, A., MIETTINEN, J. & SIEGERT, F. (2007). Land cover change 2002–2005 in Borneo and the role of fire derived from MODIS imagery. Global Change Biology, 13: 2329–2340.

LEE, S.L., TANI, N., NG, K.K.S. & TSUMURA, Y. (2004). Isolation and characterization of 20 microsatellite loci for an important tropical tree Shorea leprosula (Dipterocarpaceae) and their applicability to S. parvifolia. Molecular Ecology Notes, 4: 222–225.

LI, W.-H. (1997). Molecular Evolution. Sinauer Associates, Massachusetts, USA.

LUIKART, G., ALLENDORF, F.W., CORNUET, J.-M. & SHERWIN, W.B. (1998). Distortion of allele frequency distribution provides a test for recent population bottleneck. Journal of Heredity, 89: 238–247.

MANDANG, Y.I. & KAGEMORI, N. (2004). A fossil wood of Dipterocarpaceae from Pliocene deposit in the west region of Java Island, Indonesia. Bioderversitas, 5: 28–35.

MANEL, S., SCHWARTZ, M.K., LUIKART, G. & TABERLET, P. (2003). Landscape genetics: combining landscape ecology and population genetics. Trends in Ecology and Evolution, 18: 189–197.

MANNI, F., GUERARD, E. & HEYER, E. (2004). Geographic patterns of (genetic, morphologic, linguistic) variation: how barriers can be detected by ‘Monmonier’s algorithm’. Human Biology, 76: 173–190.

MIETTINEN, J.K., SHI, C.-H. & LIEW, S.-C. (2011). Deforestation rates in insular Southeast Asia between 2000 and 2010. Global Change Biology, 17: 2261–2270.

MONMONIER, M. (1973). Maximum-difference barriers; an alternative numerical regionalization method. Geographical Analysis, 3: 245–261.

MOYLE, R.G., SCHILTHUIZEN, M., RAHMAN, M.A. & SHELDON, F.H. (2005). Molecular phylogenetic analysis of the white-crowned forktail Enicurus leschenaulti in Borneo. Journal of Avian Biology, 36: 96–101.

MYERS, N., MITTERMEIER, R.A., DA FONSECA, G.A.B. & KENT, J. (2000). Biodiversity hotspots for conservation priorities. Nature, 403: 853–858.

NAITO, Y., KANZAKI, M., IWATA, H., OBAYASHI, K., LEE, S.-L., MUHAMMAD, N., OKUDA, T. & TSUMURA, Y. (2008). Density-dependent selfing and its effects on seed performance in a tropical canopy tree species, Shorea acuminata (Dipterocarpaceae). Forest Ecology and Management, 256: 375–383.

NAITO, Y., KONUMA, A., IWATA, H., SUYAMA, Y., SEIWA, K., OKUDA, T., LEE, S.-L., MUHAMMAD, N. & TSUMURA, Y. (2005). Selfing and inbreeding depression in seeds and seedlings of Neobalanocarpus heimii (Dipterocarpaceae). Journal of Plant Research, 118: 423–430.

NANAMI, S., IKEDA, S., TANI, N., TAN, S., DIWAY, B., HARADA, K., TSUMURA, Y., ITOH, A. & YAMAKURA, T. (2007). Development of microsatellite markers for Dryobalanops aromatica (Dipterocarpaceae), a tropical emergent tree in Southeast Asia. Molecular Ecology Notes, 7: 623–625.

NEI, M. (1978). Estimation of average heterozygosity and genetic distance from a number of individuals. Genetics, 89: 538–590.

NEWMAN, M.F., BURGESS, P.F. & WHITMORE, T.C. (1998). Foresters’ Manual of Dipterocarps: Borneo Island, medium and heavy hard woods. Royal Botanic Garden Edinburgh/Center for International Forestry Research, Jakarta.

OBAYASHI, K., TSUMURA, Y., IHARA-UJINO, T., NIIYAMA, K., TANOUCHI, H., SUYAMA, Y., WASHITANI, I., LEE, C.-T., LEE, S.-L. & MUHAMMAD, N. (2002). Genetic diversity and outcrossing rate between undisturbed and selectively logged forest of Shorea curtisii (Dipterocarpaceae) using microsatellite. International Journal of Plant Sciences, 163: 151–158.

OHTANI, M. & 15 others (2013). Nuclear chloroplast DNA phylogeography reveals Pleistocene divergence and subsequent secondary contact of two genetic lineages of the tropical rainforest tree species Shorea leprosula (Dipterocarpaceae) in South-East Asia. Molecular Ecology, 22: 2264–2279.

OOSTERHOUT, C.V., HUTCHINSON, W.F., WILLS, D.P.M. & SHIPLEY, P. (2004). MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes, 4: 535–538.

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.

PRITCHARD, J.K., STEPHEN, M. & DONNELLY, P. (2000). Inference of population structure using multilocus genotype data. Genetics, 155: 945–959.

RAES, N., CANNON, C.H., HIJMANS, R.J., PIESSENS, T., SAW, L.G., VAN WELZEN, P.C. & SLIK, J.W.F. (2014). Historical distribution of Sundaland’s dipterocarp rainforests at Quaternary glacial Maxima. Proceedings of the National Academy of Sciences of the USA, 111: 16790–16795.

RIDDER-NUMAN, J.W.A. (1998). Historical biogeography of Spatholobus (Leguminosae-Papilionoideae) and allies in SE Asia. In: HALL, R. &

HOLLOWAY, J.D. (eds) Biogeography and Geological Evolution of SE Asia. Backhuys Publishers, Leiden, pp. 259–277.

RIESEBERG, L.H., KIM, S.C., RANDELL, R.A., WHITNEY, K.D., GROSS, B.L., LEXER, C. & CLAY, K. (2007). Hybridization and the colonization of novel habitats by annual sunflowers. Genetica, 129: 149–165.


ROSENBERG, N.A. (2004). DISTRUCT: a program for the graphical display of population structure. Molecular Ecology Notes, 4: 137–138.

SLOOTEN, D.F. VAN (1932). The Dipterocarpaceae of the Dutch East Indies. VI. The genus Dryobalanops. Bulletin du Jardin botanique de Buitenzorg, série III, 3: 1–45.

SODHI, N.K., KOH, L.P., BROOKS, B.W. & NG, P.K.L. (2004). Southeast Asian biodiversity: an impending disaster. Trends in Ecology and Evolution, 19: 654–660.

SYMINGTON, C.F. (2004). Foresters’ Manual of Dipterocarps (2nd edn, rev. ASHTON, P.S. & APPANAH, S.). Malayan Forest Records, No. 16. Forest Research Institute Malaysia and Malaysian Nature Society, Kuala Lumpur.

TAKEUCHI, Y., ICHIKAWA, S., KONUMA, A., TOMARU, N., NIIYAMA, K., LEE, S.-L., MUHAMMAD, N. & TSUMURA, Y. (2004). Comparison of the fine-scale genetic structure of three dipterocarp species. Heredity, 92: 323–328.

TÜXEN, R. (1956). Die heutige potentielle natürliche Vegetation als Gegenstand der Vegetatonskartierung. Angew. Pflanzensoziol., 13: 5–42.

VORIS, H.K. (2000). Maps of Pleistocene sea levels in Southeast Asia: shorelines, river systems and time durations. Journal of Biogeography, 27: 1153–1167.

WARREN, K.S., VERSCHOOR, E., LANGENHUIZEN, S., HERIYANTO, SWAN, R.A., VIGILANT, L. & HEENEY, J.L. (2001) Speciation and intrasubspecific variation of Bornean orangutans, Pongo pygmaeus pygmaeus. Molecular Biology and Evolution, 18: 472–480.

WEIR, B.S. & COCKERHAM, C.C. (1984). Estimating F-statistics for the analysis of population structure. Evolution, 38: 1358–1370.


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