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Effects of Pleistocene climate change on genetic structure and diversity of Shorea macrophylla in Kalimantan Rainforest

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Abstract

The island of Borneo is the diversity center of the Dipterocarpaceae, the most important family of tropical rainforest trees in Southeast Asia. However, changes in land use and climate have affected dipterocarp distributions on the island, raising concerns about the vulnerability (inter alia) of the endemic riparian species Shorea macrophylla. Thus, to aid conservation efforts, we have investigated the genetic diversity, structure, and demographic history of S. macrophylla. The species’ genetic diversity and structure in Kalimantan (part of Indonesia, covering 75% of the island) were explored by examining genotypes of 377 individuals representing 13 populations in three regions (Northeast, Central, and West Kalimantan) using 14 newly developed microsatellite loci. Higher genetic diversity was found, at all loci, in samples from Northeast Kalimantan than in samples from the other regions. Moderate genetic differentiation between populations was detected (FST 0.093). Bayesian clustering, principal coordinate, and neighbor joining tree analyses of the population structure consistently identified two genetically distinct groups, one in the Northeast and the other in the Central and West regions. The higher diversity of the diverged populations in Northeast Kalimantan indicates that the region may have hosted rainforest refugia during the ice age. Accordingly, analysis using DIY ABC software indicated that the Northeast and Central-West Kalimantan groups diverged 194,000 years ago. We conclude that global climate change during the Pleistocene strongly influenced the genetic diversity and structure of S. macrophylla populations in Kalimantan.

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References

  1. Aide TM, Rivera E (1998) Geographic patterns of genetic diversity in Poulsenia armata (Moraceae): implications for the theory of Pleistocene refugia and the importance of riparian forest. J Biogeogr 25:695–705

  2. Anderson JAR (1975) The potential of illipe nuts (Shorea spp.) as an agricultural crop. In: Williams et al (eds) Proceedings of symposium on south east Asian plant genetic resources, Bogor, Indonesia. BIOTROP, Bogor, pp 217–230

  3. Appanah S (1998) Introduction. In: Appanah S, Turnbul JM (eds) A review of dipterocarps: taxonomy, ecology and Silviculture. CIFOR, Bogor

  4. Appanah S, Weinland G (1993) Planting quality timber trees in peninsular Malaysia—a review, Malaysian Forest record no. 38. Forest Research Institute Malaysia, Kuala Lumpur

  5. Arruda CCB, Silva MB, Sebbenn AM, Kanashiro M, Lemes MR, Gribel R (2015) Mating system and genetic diversity of progenies before and after logging: a case study of Bagassa guianensis (Moraceae), a low-density dioecious tree of the Amazonian forest. Tree Genet Genomes 11:3–9

  6. Ashton PS (1969) Speciation among tropical forest trees—some deductions in light of recent evidence. Biol J Linn Soc 1:155–196

  7. Ashton PS (1982) Dipterocarpaceae. Flora Malesiana, Martinus Nijhoff Publishers, The Hague

  8. Ashton PS (1998) Shorea macrophylla. The IUCN Red List of Threatened Species. 1998: e. T33620A9798047. doi:https://doi.org/10.2305/IUCN.UK.1998.RLTS.T33620A9798047.en. Accessed on 16 June 2016

  9. Bao L, Kudureti A, Bai W, Chen R, Wang T, Wang H, Ge J (2015) Contributions of multiple refugia during the last glacial period to current mainland populations of Korean pine (Pinus koraiensis). Sci Rep 5(8):18608

  10. Beaumont MA, Zhang W, Balding DJ (2002) Approximate Bayesian computation in population genetics. Genetics 162:2025–2035

  11. Blacket MJ, Robin C, Good RT, Lee SF, Miller AD (2012) Universal primers for fluorescent labeling of PCR fragments--an efficient and cost-effective approach to genotyping by fluorescence. Mol Ecol Resour 12(3):456–463

  12. Brito VLG, Mori GM, Vigna BBZ, Azevedo-Silva M, Souza AP, Sazima M (2016) Genetic structure and diversity of populations of polyploid Tibouchina pulchra Cogn. (Melastomataceae) under different environmental conditions in extremes of an elevational gradient. Tree Genet Genomes 12(6):101

  13. Brownstein MJ, Carpten JD, Smith JR (1996) Modulation of non-templated nucleotide addition by Taq DNA polymerase: primer modifications that facilitate genotyping. Biotechniques 20(6):1004–1010

  14. Bryan JE, Shearman PL, Asner GP, Knapp DE, Aoro G, Lokes B (2013) Extreme differences in forest degradation in Borneo: comparing practices in Sarawak, Sabah, and Brunei. PLoS One 8:e69679

  15. Cabrera AA, Palsbøll PJ (2017) Inferring past demographic changes from contemporary genetic data: a simulation-based evaluation of the ABC methods implemented in diyabc. Mol Ecol Res 6:1–17

  16. Cannon CH, Morley RJ, Bush ABG (2009) The current refugial rainforests of Sundaland are unrepresentative of their biogeographic past and highly vulnerable to disturbance. Proc Natl Acad Sci U S A 106:11188–11193

  17. Carnaval AC, Hickerson MJ, Haddad CFB, Rodrigues MT, Moritz C (2009) Stability predicts genetic diversity in the Brazilian Atlantic Forest hotspot. Science 23:785–789

  18. Chan HT (1980) Reproductive biology of some Malaysian dipterocarps. II. Fruiting biology and seedling studies. Malay For 43:438–451

  19. Charlesworth D, Charlesworth B (1987) Inbreeding depression and its evolutionary consequences. Annu Rev Ecol Syst 18:237–268

  20. Chung MY, Vu SH, López-Pujol J et al (2018) Comparison of genetic variation between northern and southern populations of Lilium cernuum (Liliaceae): implications for Pleistocene refugia. PLoS One 13:1–20

  21. Comps B, Gomory D, Letouzey J, Thiebaut B, Petit RJ (2001) Diverging trends between heterozygosity and allelic richness during postglacial colonization in the European beech. Genetics 157:389–397

  22. Cooke FM (2006) Asia-Pacific environment monograph 1: state, communities and forests in contemporary Borneo. ANU E Press: The Australian National University, Canberra

  23. Cornuet JM, Pudlo P, Veyssier J, Dehne-Garcia A, Gautier M, Leblois R, Marin JM, Estoup A (2014) DIYABC v2.0: a software to make approximate Bayesian computation inferences about population history using single nucleotide polymorphism, DNA sequence and microsatellite data. Bioinformatics 30(8):1187–1189

  24. de Beer JH, McDermott MJ (1996) The economic value of non-timber forest products in Southeast Asia, 2nd edn. Netherlands Committee for IUCN, Amsterdam

  25. de Mello-Martins F (2011) Historical biogeography of the Brazilian Atlantic forest and the Carnaval–Moritz model of Pleistocene refugia: what do phylogeographical studies tell us? Biol J Linn Soc 104:499–509

  26. Deb JC, Phinn S, Butt N, McAlpine CA (2017) The impact of climate change on the distribution of two threatened dipterocarp trees. Ecol Evol 7(7):2238–2248

  27. Earl DA, von Holdt BM (2012) Structure harvester: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4(2):359–361

  28. 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

  29. 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

  30. 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

  31. Gathorne-Hardy FJ, Syaukani DRG, Eggleton P, Jones DT (2002) Quaternary rainforest refugia in south-east Asia: using termites as indicators. Biol J Linn Soc 75(4):453–466

  32. Gavin DG, Fitzpatrick MC, Gugger PF, Heath KD, Rodríguez-Sánchez F, Dobrowski SZ, Hampe A, Hu FS, Ashcroft MB, Bartlein PJ, Blois JL, Carstens BC, Davis EB, de Lafontaine G, Edwards ME, Fernandez M, Henne PD, Herring EM, Holden ZA, Kong WS, Liu J, Magri D, Matzke NJ, McGlone MS, Saltré F, Stigall AL, Tsai YHE, Williams JW (2014) Climate refugia: joint inference from fossil records, species distribution models and phylogeography. New Phytol 204:37–54

  33. Geng Q, Yao Z, Yang J, He J, Wang D, Wang Z, Liu H (2015) Effect of Yangtze River on population genetic structure of the relict plant Parrotia subaequalis in eastern China. Ecol Evol 5:4617–4627

  34. Goudet J (2002) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3.2). http://www.unil.ch/izea/softwares/fstat.html. Accessed on 25 July 2017

  35. Government Regulation of the Republic of Indonesia (1999) Law of the Republic of Indonesia Number 41 of 1999 Regarding Forestry. The State Secretary of the Republic of Indonesia, Jakarta

  36. Hartl DL, Clark AG (1997) Principles of population genetics, third edn. Sinauer Associates, Sunderland

  37. Hensen I, Cierjacks A, Hirsch H, Kessler M, Romoleroux K, Renison D, Wesche K (2011) Historic and recent fragmentation coupled with altitude affect the genetic population structure of one of the world’s highest tropical tree line species. Glob Ecol Biogeogr 21:455–464

  38. Hewitt GM (2000) The genetic legacy of the quaternary ice ages. Nature 405:907–913

  39. Hewitt GM (2004) Genetic consequences of climatic oscillations in the Quaternary. Philos Trans R Soc B Biol Sci 359:183–195

  40. Ismail SA, Ghazoul J, Ravikanth G, Kushalappa CG, Uma Shaanker R, Kettle CJ (2014) Fragmentation genetics of Vateria indica: implications for management of forest genetic resources of an endemic dipterocarp. Conserv Genet 15:533–545

  41. IUCN Species Survival Commission (2015) The IUCN red list of threatened species. http://www.iucnredlist.org/ Accessed on May 2017

  42. Iwanaga H, Teshima KM, Khatab IA, Inomata N, Finkeldey R, Siregar IZ, Siregar UJ, Szmidt AE (2012) Population structure and demographic history of a tropical lowland rainforest tree species Shorea parvifolia (Dipterocarpaceae) from southeastern Asia. Ecol Evol 2(7):1663–1675

  43. Kalinowski ST (2005) HP-RARE 1.0: a computer program for performing rarefaction on measures of allelic richness. Mol Ecol Notes 5:187–189

  44. Kamiya K, Nanami S, Kenzo T, Yoneda R, Diway B, Chong L, Azani MA, Majid NM, Lum SKY, Wong K, Harada K (2012) Demographic history of Shorea curtisii (Dipterocarpaceae) inferred from chloroplast DNA sequence variations. Biotropica 44(5):577–585

  45. Kang TH, Han SH, Park SJ (2015) Development of seven microsatellite markers using next generation sequencing for the conservation on the Korean population of Dorcus hopei (E. Saunders, 1854) (Coleoptera, Lucanidae). Int J Mol Sci 16(9):21330–21341

  46. Keller LF, Waller DM (2002) Inbreeding effects in wild populations. Trends Ecol Evol 17:230–241

  47. Kimura MK, Uchiyama K, Nakao K, Moriguchi Y, Jose-Maldia LS, Tsumura Y (2014) Evidence for cryptic northern refugia in the last glacial period in Cryptomeria japonica. Ann Bot 114(8):1687–1700

  48. Konuma A, Tsumura Y, Lee CT, Lee SL, Okuda T (2000) Estimation of gene flow in the tropical rain forest tree Neobalanocarpus heimii (Dipterocarpaceae), inferred from paternity analysis. Mol Ecol 9:1843–1852

  49. Koscinski D, Handford P, Tubaro PL, Sharp S, Lougheed SC (2008) Pleistocene climatic cycling and diversification of the Andean treefrog, Hypsiboas andinus. Mol Ecol 17:2012–2025

  50. Kumar S, Tamura K, Nei M (2004) MEGA3: molecular evolutionary genetics analysis. Brief Bioinform 5:150–163

  51. Langella O (1999) Populations 1.2.32 (02/13/2011): a population genetic software. CNRS UPR9034. http://bioinformatics.org/~tryphon/populations/ Accessed on 25 July 2017

  52. Lecorre V, Dumolinlapegue S, Kremer A (1997) Genetic variation at allozyme and RAPD loci in sessile oak Quercus petraea (Matt) Liebl: the role of history and geography. Mol Ecol 6:519–529

  53. Ledig FT (1986) Conservation strategy for forest gene resources. For Ecol Manag 14:77–90

  54. Lee HS, Itoh A, Kanzaki M, Yamakura T (1997) Height growth of engkabang jantong, Shoreo macrophylla (De Vr.) in a plantation forest in Sarawak. Tropics 7:67–80

  55. Lee SL, Ng KKS, Saw LG, Lee CT, Muhammad N, Tani N, Tsumura Y, Koskela J (2006) Linking the gaps between conservation research and conservation management of rare dipterocarps: a case study of Shorea lumutensis. Biol Conserv 131(1):72–92

  56. Lee SL, Wickneswari R, Mahani MC, Zakri AH (2000) Mating system parameters in a tropical tree species, Shorea leprosula Miq. (Dipterocarpaceae), from Malaysian lowland dipterocarp forest. Biotropica 32(4):693–702

  57. Li W, Godzik A (2006) Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22(13):1658–1659

  58. Lisiecki LE, Raymo ME (2005) A Pliocene-Pleistocene stack of 57 globally distributed benthic δ18O records. Paleoceanography 20(1):1–17

  59. Marshall DR, Brown AHD (1975) Optimum sampling strategies in genetic conservation. In: Frankel OH, Hawkes JG (eds) Crop genetic resources for today and tomorrow. Cambridge University Press, Cambridge, pp 53–80

  60. Mattioni C, Martin MA, Pollegioni P, Cherubini M, Villani F (2013) Microsatellite markers reveal a strong geographical structure in European populations of Castanea sativa (Fagaceae): evidence for multiple glacial refugia. Am J Bot 100:951–961

  61. Ministry of Forestry of Indonesia (1998) Ministerial Decree No 692/Kpts-II/1998 on Protected Forest Tree Species. Ministry of Forestry of Indonesia, Jakarta

  62. Moritz C (1994) Defining ‘evolutionary significant units. Trends Ecol Evol 9:373–375

  63. Naiman RJ, Decamps H, Pollock M (1993) The role of riparian corridors in maintaining regional biodiversity. Ecol Appl 3:209–212

  64. Naito Y, Konuma A, Iwata H, Suyama Y, Seiwa K, Okuda T, Lee SL, Muhammad N, Tsumura Y (2005) Selfing and inbreeding depression in seeds and seedlings of Neobalanocarpus heimii (Dipterocarpaceae). J Plant Res 118(6):423–430

  65. Nei M, Maruyama T, Chakraborty R (1975) The bottleneck effect and genetic variability in populations. Evolution 29:1–10

  66. Nesaretnam K, Ali ARBM (1992) Engkabang (illipe)—an excellent component for cocoa butter equivalent fat. J Sci Food Agric 60(1):15–20

  67. Newman MF, Burgess PF, Whitmore TC (1996) Borneo Island light hardwood—manual of dipterocarps for foresters. CIFOR, Bogor

  68. Ng FSP (1966) Age at first flowering in dipterocarps. Malay For 29:290–295

  69. Ng FSP (1976) Gregarious flowering of dipterocarps in Kepong. Malay For 40:126–137

  70. Ng KKS, Ang KC, Lee SL (2002) Mating system in a planted population of Shorea macrophylla (Dipterocarpaceae). J Trop For Sci 14(1):145–149

  71. Ng KKS, Lee SL, Koh CL (2004) Spatial structure and genetic diversity of two tropical tree species with contrasting breeding systems and different ploidy levels. Mol Ecol 13(3):657–669

  72. Ng KKS, Lee SL, Ueno S (2009) Impact of selective logging on genetic diversity of two tropical tree species with contrasting breeding system using direct comparison and simulation methods. For Ecol Manag 257:107–116

  73. Obayashi K, Tsumura Y, Ihara-Ujino T, Niiyama K, Tanouchi H, Suyama Y, Washitani I, Lee C, Lee SL, Muhammad N (2002) Genetic diversity and outcrossing rate between undisturbed and selectively logged forests of Shorea curtisii (Dipterocarpaceae) using microsatellite DNA analysis. Int J Plant Sci 163(1):151–158

  74. Ohtani M, Kondo T, Tani N, Ueno S, Lee LS, Ng KKS, Muhammad N, Finkeldey R, Na’iem M, Indrioko S, Kamiya K, Harada K, Diway B, Khoo E, Kawamura K, Tsumura Y (2013) Nuclear and 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. Mol Ecol 22(8):2264–2279

  75. Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research--an update. Bioinformatics 28(19):2537–2539

  76. Perumal M, Wasli ME, Soo Ying H, Lat J, Sani H (2017) Survivorship and growth performance of Shorea macrophylla (de Vriese) after enrichment planting for reforestation purpose at Sarawak, Malaysia. Online J Bio Sci 17(1):7.17

  77. Peterson BK, Weber JN, Kay EH, Fisher HS, Hoekstra HE (2012) Double digest RADseq: an inexpensive method for de novo SNP discovery and genotyping in model and non-model species. PLoS One 7(5):e37135

  78. Petit RJ, Aguinagalde I, Beaulieu J, Bittkau C, Brewer S et al (2003) Glacial refugia: hotspots but not melting pots of genetic diversity. Science 300:1563–1565

  79. Petit RJ, El Mousadik A, Pons O (1998) Identifying populations for conservation on the basis of genetic markers. Conserv Biol 12:844–855

  80. Petit RJ, Hampe A (2006) Some evolutionary consequences of being a tree. Annu Rev Ecol Evol Syst 37:187–214

  81. Petit RJ, Jouzel J, Raynaud D et al (1999) Climate and atmospheric history of the past 420,000 years from the Vostok ice core, Antarctica. Nature 399:429–436

  82. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

  83. Ramírez-Barahona S, Eguiarte LE (2013) The role of glacial cycles in promoting genetic diversity in the Neotropics: the case of cloud forests during the last glacial maximum. Ecol Evol 3(3):725–738

  84. Reed DH, Frankham R (2003) Correlation between fitness and genetic diversity. Conserv Biol 17(1):1230–1237

  85. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

  86. Saw LG, Sam YY (2000) Conservation of Dipterocarpaceae in Peninsular Malaysia. J Trop For Sci 12:593–615

  87. Slatkin M (1987) Gene flow and the geographic structure of populations. Science 236:787–792

  88. Slik JWF, Poulsen AD, Ashton PS, Cannon CH, Eichhorn KAO, Kartawinata K, Lanniari I, Nagamasu H, Nakagawa M, van Nieuwstadt MGL, Payne J, Purwaningsih SA, Sidiyasa K, Verburg RW, Webb CO, Wilkie P (2003) A floristic analysis of the lowland dipterocarp forests of Borneo. J Biogeogr 30:1517–1531

  89. Sodhi NS, Posa MRC, Lee TM, Bickford D, Koh LP, Brook BW (2010) The state and conservation of southeast Asian biodiversity. Biodivers Conserv 19(2):317–328

  90. Stewart JR, Lister AM, Barnes I, Dalen L (2010) Refugia revisited: individualistic responses of species in space and time. Proc R Soc Lond B 277:661–671

  91. Szczecinska M, Sramko G, Wolosz K, Sawicki J (2016) Genetic diversity and population structure of the rare and endangered plant species Pulsatilla patens (L.) mill in east Central Europe. PLoS One 11(3):e0151730

  92. Takeuchi Y, Ichikawa S, Konuma A, Tomaru N, Niiyama K, Lee SL, Muhammad N, Tsumura Y (2004) Comparison of the fine-scale genetic structure of three dipterocarp species. Heredity 92:323–328

  93. Tani N, Tsumura Y, Fukasawa K et al (2015) Mixed mating system are regulated by fecundity in Shorea curtisii (Dipterocarpaceae) as revealed by comparison under different pollen limited conditions. PLoS One 10:1–20

  94. Thomas MF (2000) Late quaternary environmental changes and the alluvial record in humid tropical environments. Quat Int 72:23–36

  95. Tinio CE, Finkeldey R, Prinz K, Fernando ES (2014) Genetic variation in natural and planted populations of Shorea guiso (Dipterocarpaceae) in the Philippines revealed by microsatellite DNA markers. Asia Life Sci 23:75–91

  96. Tompsett PB, Kemp R (1996) DABATTS: Database of tropical tree seed research with special reference to the Dipterocarpaceae, Meliaceae and Araucariaceae. Royal Botanic Gardens, Kew

  97. Tsumura Y (2011) Gene flow, mating systems, and inbreeding depression in natural populations of tropical trees. In: Wickneswari R, Cannon C (eds) Managing the future of Southeast Asia’s valuable tropical rainforests. A Practitioner’s guide to Forest genetics. Springer, Dordrecht, pp 57–68

  98. Tsumura Y, Kado T, Yoshida K, Abe H, Ohtani M, Taguchi Y, Fukue Y, Tani N, Ueno S, Yoshimura K, Kamiya K, Harada K, Takeuchi Y, Diway B, Finkeldey R, Na’iem M, Indrioko S, Ng KKS, Muhammad N, Lee SL (2011) Molecular database for classifying Shorea species (Dipterocarpaceae) and techniques for checking the legitimacy of timber and wood products. J Plant Res 124(1):35–48

  99. Tsumura Y, Uchiyama K, Moriguchi Y, Kimura MK, Ueno S, Ujino-Ihara T (2014) Genetic differentiation and evolutionary adaptation in Cryptomeria japonica. G3 4:2389–2402

  100. Ueno S, Moriguchi Y, Uchiyama K, Ujino-Ihara T, Futamura N, Sakurai T, Shinohara K, Tsumura Y (2012) A second generation framework for the analysis of microsatellites in expressed sequence tags and the development of EST-SSR markers for a conifer, Cryptomeria japonica. BMC Genomics 13:136

  101. van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) Micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538

  102. Voris HK (2000) Maps of Pleistocene sea levels in Southeast Asia: shorelines, river systems and time durations. J Biogeogr 27:1153–1167

  103. White TL, Adams WT, Neale DB (2007) Forest genetics. CAB International, Wallingford

  104. Widiyatno IS, Na’iem M, Uchiyama K, Numata S, Ohtani M, Matsumoto A, Tsumura Y (2016) Effects of different silvicultural systems on the genetic diversity of Shorea parvifolia populations in the tropical rainforest of Southeast Asia. Tree Genet Genomes 12(4):73

  105. Widiyatno W, Soekotjo S, Na’iem M, Purnomo S, Setiyanto PE (2014) Early performance of 23 dipterocarp species planted in the logged-over rainforest. J Trop For Sci 26(2):259–266

  106. Wright S (1978) Evolution and the genetics of populations, variability within and among natural populations, vol 4. University of Chicago Press, Chicago

  107. Wurster CM, Bird MI, Bull ID, Creed F, Bryantd C, Dungait JAJ, Paz V (2010) Forest contraction in north equatorial Southeast Asia during the last glacial period. Proc Natl Acad Sci U S A 107:15508–15511

  108. Yan BQ, Wang T, Hu LL (2009) Population genetic diversity and structure of Schisandra sphenanthera: a medicinal plant in China. Chin J Ecol 28:811–819

  109. Yang Y, Duke NC, Peng F, Li J, Yang S, Zhong C, Zhou R, Shi S (2016) Ancient geographical barriers drive differentiation among Sonneratia caseolaris populations and recent divergence from S. lanceolata. Front Plant Sci 7(10):1618

  110. You X, Liu J, Zhang L (2015) Ecological modeling of riparian vegetation under disturbances: a review. Ecol Model 318:293–300

  111. Zhang ZY, Zheng XM, Ge S (2007) Population genetic structure of Vitex negundo (Verbenaceae) in three gorge areas of the Yangtze River: the riverine barrier to seed dispersal in plants. Biochem Syst Ecol 35:506–516

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Acknowledgements

We sincerely thank Prof. Ryo Ohsawa (University of Tsukuba) for providing laboratory facilities for DNA extraction. Thanks are also due to Ghani Purnomo, Sawitri, Dicky Wahono, Intracawood Manufacturing Ltd., Wana Inti Kahuripan Ltd., Sari Bumi Kusuma Ltd., Suka Jaya Makmur Ltd., and Intracawood Manufacturing Ltd., for their kind support during the sample collection. A MEXT Japan scholarship supported this study.

Data archiving statement

All genotyping data used in this study was deposited in the Dryad data repository, https://doi.org/10.5061/dryad.92j7j53.

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Correspondence to Yoshihiko Tsumura.

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Communicated by W. Ratnam

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Utomo, S., Uchiyama, K., Ueno, S. et al. Effects of Pleistocene climate change on genetic structure and diversity of Shorea macrophylla in Kalimantan Rainforest. Tree Genetics & Genomes 14, 44 (2018). https://doi.org/10.1007/s11295-018-1261-1

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Keywords

  • Shorea macrophylla
  • Genetic diversity and structure
  • Pleistocene climate change
  • Refugia
  • Kalimantan