Journal of Plant Research

, Volume 120, Issue 3, pp 413–420 | Cite as

Effects of flowering tree density on the mating system and gene flow in Shorea leprosula (Dipterocarpaceae) in Peninsular Malaysia

  • Yoko Fukue
  • Tomoyuki Kado
  • Soon Leong Lee
  • Kevin Kit Siong Ng
  • Norwati Muhammad
  • Yoshihiko TsumuraEmail author
Regular Paper


Pristine tropical rainforests in Southeast Asia have rich species diversity and are important habitats for many plant species. However, the extent of these forests has declined in recent decades and they have become fragmented due to human activities. These developments may reduce the genetic diversity of species within them and, consequently, the species’ ability to adapt to environmental changes. Our objective in the study presented here was to clarify the effect of tree density on the genetic diversity and gene flow patterns of Shorea leprosula Miq. populations in Peninsular Malaysia. For this purpose, we related genetic diversity and pollen flow parameters of seedling populations in study plots to the density of mature trees in their vicinity. The results show that gene diversity and allelic richness were not significantly correlated to the mature tree density. However, the number of rare alleles among the seedlings and the selfing rates of the mother trees were negatively correlated with the density of the adult trees. Furthermore, in a population with high mature tree density pollination distances were frequently <200 m, but in populations with low adult tree density the distances were longer. These findings suggest that the density of flowering trees affects selfing rates, gene flow and, thus, the genetic diversity of S. leprosula populations. We also found an individual S. leprosula tree with a unique reproductive system, probably apomictic, mating system.


Dipterocarp Gene flow Mating system Tree density Tropical forest 



We thank J. Ghazali, M. Yahya, P. Ramli, D. Mariam, Nor Salwah A.W. and Nurl Hudaini Mamat of the Genetic Lab at the Forest Research Institute Malaysia for their assistance in the laboratory and field. We also thank N. Tani and H. Iwata for helpful advice on the statistical analysis. The study was partly supported by the Global Environment Research Program supported by the Ministry of Environment in Japan, grant no. E-4 and Grants-in-Aid for Scientific Research (Nos. 15405026 and 18255010) provided by the Ministry of Education, Culture, Sports, Science and Technology of Japan.


  1. Ågren J (1996) Population size, pollinator limitation, and seed set in the self-incompatible herb, Lythrum salicaria. Ecology 77:1779–1790CrossRefGoogle Scholar
  2. Appanah S, Chan HT (1981) Thrips: the pollinators of some dipterocarps. Malays For 44: 234–252Google Scholar
  3. Ashton PS (1982) Dipterocarpaceae. In: Van Steenis CGGJ (ed) Flora Malesiana, Series 1, Spermatophyta, vol. 9. Martinus Nijhoff, The Hague, pp 237–552Google Scholar
  4. Asker SE, Jerling L (1992) Apomixis in plants. CRC, Boca RatonGoogle Scholar
  5. Austerlitz F, Smouse PE (2001) Two-generation analysis of pollen flow across a landscape. IV. Estimating the dispersal parameter. Genetics 161:355–363Google Scholar
  6. Bawa KS (1998) Conservation of genetic resources in the Dipterocarpaceae (Chap. 2). In: Appanah S, Turnbull JM (eds) A review of dipterocarps: taxonomy, ecology and silviculture. Center for International Forestry Research, Bogor, pp 45–55Google Scholar
  7. Carman JG (1997) Asynchronous expression of duplicate genes in angiosperms may cause apomixis, bispory, tetraspory, and polyembryony. Biol J Linn Soc 61:51–94CrossRefGoogle Scholar
  8. Collevatti RG, Grattapaglia D, Hay JD (2001) Population genetic structure of the endangered tropical tree species Caryocar brasiliense, based on variability at microsatellite loci. Mol Ecol 10:349–356PubMedCrossRefGoogle Scholar
  9. Ellegren H, Moore S, Robinson N, Byrne K, Ward W, Sheldon BC (1997) Microsatellite evolution—a reciprocal study of repeat lengths at homologous loci in cattle and sheep. Mol Biol Evol 14:854–860PubMedGoogle Scholar
  10. Ernst A (1918) Die Bastardierung als Ursache der Apogamie im Pflanzenreiche. Jena Ger Fischer (in German)Google Scholar
  11. Forest Research Institute Malaysia (2002) Bulletin fenologi biji benih dan anak benih. No.293-No.298, Forest Research Institute Malaysia, Kepong (in Malaysian)Google Scholar
  12. Frankham R, Ballou JD, Briscoe DA (2002) Introduction to conservation genetics. Cambridge University Press, Cambridge, p 617Google Scholar
  13. Ghazoul J, Liston KA, Boyle TJB (1998) Disturbance-induced density-dependent seed set in Shorea siamensis (Dipterocarpaceae), a tropical forest tree. J Ecol 86:462–473CrossRefGoogle Scholar
  14. 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. Mol Ecol 15:2985–2996PubMedCrossRefGoogle Scholar
  15. Goudet J (2000) FSTAT: a program to estimate and test gene diversities and fixation indices, Ver. 2.9.1. Available via
  16. Grimanelli D, Leblanc O, Perotti E, Grossniklaus U (2001) Developmental genetics of gametophytic apomixis. Trends Genet 17:597–604PubMedCrossRefGoogle Scholar
  17. Hamrick JL (2004) Response of forest trees to global environmental changes. For Ecol Manag 197:323–335CrossRefGoogle Scholar
  18. He P, Friebe BR, Gill BS, Zhou JM (2003) Allopolyploidy alters gene expression in the highly stable hexaploid wheat. Plant Mol Biol 52:401–414PubMedCrossRefGoogle Scholar
  19. Kaur A, Ha CO, Jong K, Sands VE, Chan HT, Soepadmo E, Ashton PS (1978) Apomixis may be widespread among trees of the climax rain forest. Nature 271:440–442CrossRefGoogle Scholar
  20. Kenta T, Isagi Y, Nakagawa M, Yamashita M, Nakashizuka T (2004) Variation in pollen dispersal between years with different pollination conditions in a tropical emergent tree. Mol Ecol 13:3575–3584PubMedCrossRefGoogle Scholar
  21. Konuma A, Tsumura Y, Lee CT, Lee SL, Okuda T (2000) Estimation of gene flow in the tropical-rainforest tree Neobalanocarpus heimii (Dipterocarpaceae), inferred from paternity analysis. Mol Ecol 9:1843–1852PubMedCrossRefGoogle Scholar
  22. Latouche-Hallé C, Ramboer A, Bandou E, Caron H, Kremer A (2004) Long-distance pollen flow and tolerance to selfing in a neotropical tree species. Mol Ecol 13:1055–1064PubMedCrossRefGoogle Scholar
  23. Lee SL, Tani N, Ng KKS, Tsumura Y (2004) Isolation and characterization of 20 microsatellite loci for an important tropical tree Shorea leprosula (Dipterocarpaceae) and their applicability to S. parvifolia. Mol Ecol Notes 4:222–225CrossRefGoogle Scholar
  24. Lee SL, Wickneswari R, Mahani MC, Zakari AH (2000) Mating system parameters in a tropical tree species, Shorea leprosula Miq. (Dipterocarpaceae) from Malaysian lowland dipterocarp forest. Biotropica 32:693–702CrossRefGoogle Scholar
  25. Marshall TC, Slate J, Kruuk LEB, Pemberton JM (1998) Statistical confidence for likelihood-based paternity inference in natural populations. Mol Ecol 7:639–655PubMedCrossRefGoogle Scholar
  26. Momose K, Yumoto T, Nagamitsu T, Kato M, Nagamasu H, Sakai S, Harrison RD, Itioka T, Hamid AA, Inoue T (1998) Pollination biology in a lowland dipterocarp forest in Sarawak, Malaysia. 1. Characteristics of the plant-pollinator community in a lowland dipterocarp forest. Am J Bot 85:1477–1501CrossRefGoogle Scholar
  27. Murcia C (1995) Edge effects in fragmented forests: implications for conservation. Trends Ecol Evol 10:58–62CrossRefGoogle Scholar
  28. Nagamitsu T, Ichikawa S, Ozawa M, Shimamura R, Kachi N, Tsumura Y, Muhanmmad N (2001) Microsatellite analysis of the breeding system and seed dispersal in Shorea leprosula (Dipterocarpaceae). Int J Plant Sci 162:155–159CrossRefGoogle Scholar
  29. Naito Y, Konuma A, Iwata H, Suyama Y, Seiwa K, Okuda T, Lee SL, Norwati M, Tsumura Y (2005) Selfing and inbreeding depression in seeds and seedlings of Neobalanocarpus heimii. (Dipterocarpaceae). J Plant Res 118:423–430PubMedCrossRefGoogle Scholar
  30. Ng K KS, 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 13:657–669PubMedCrossRefGoogle Scholar
  31. Obayashi K, Tsumura Y, Ihara-Ujino T, Niiyama K, Tanouchi H, Suyama Y, Washitani I, Lee C-T, Lee SL, Muhammad N (2002) Genetic diversity and outcrossing rate between undisturbed and selectively logged forests of Shorea curtisii (Dipterocarpaceae) using microsatellite. Int J Plant Sci 163:151–158CrossRefGoogle Scholar
  32. Rubinsztein DC, Amos W, Leggo J, Goodburn S, Jain S, Li SH, Margolis RL (1995) Microsatellite evolution-evidence for directionality and variation in rate between species. Nat Genet 10:337–343PubMedCrossRefGoogle Scholar
  33. Sakai S, Momose K, Yumoto T, Kato M, Inoue T (1999) Beetle pollination of Shorea parvifolia (section Mutica, Dipterocarpaceae) in a general flowering period in Sarawak, Malaysia. Am J Bot 86:62–69CrossRefGoogle Scholar
  34. Stacy EA, Hamrick JL, Nason JD, Hubbell SP, Foster RB, Condit R (1996) Pollen dispersal in low-density populations of three Neotropical tree species. Am Nat 148:275–298CrossRefGoogle Scholar
  35. Symington CF (2004) Malayan forest records no.16 foresters’ manual of Dipterocarps. Forest Research Institute Malaysia, Kuala LumpurGoogle Scholar
  36. 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 92:323–328PubMedCrossRefGoogle Scholar
  37. Tsumura Y, Kawahara T, Wickneswari R, Yoshimura K (1996) Molecular phylogeny of Dipterocarpaceae in Southeast Asia using PCR-RFLP analysis of chloroplast genes. Theoret Appl Genet 93:22–29CrossRefGoogle Scholar
  38. Tsumura Y, Ujino-Ihara T, Obayashi K, Konuma A, Nagamitsu T (2003) Mating system and gene flow of Dipterocarps revealed by genetic markers. Pasoh-ecology of a lowland rain forest in Southeast Asia. Springer, Tokyo Berlin Heidelberg, pp 285–292Google Scholar
  39. Ujino T, Kawahara T, Tsumura Y, Nagamitsu T, Wickneswari R, Yoshimaru H (1998) Development and polymorphism of simple sequence repeat DNA markers for Shorea curtisii and other Dipterocarpaceae species. Heredity 81:422–428PubMedCrossRefGoogle Scholar
  40. White GM, Boshier DH, Powell W (2002) Increased pollen flow counteracts fragmentation in a tropical dry forest: an example from Swietenia humilis Zuccarini. Proc Natl Acad Sci USA 99:2038–2042PubMedCrossRefGoogle Scholar
  41. Wyatt-Smith J (1963) Manual of Malayan silviculture for inland forest. Malayan Forest Record 23, Forest Department, Kuala LumpurGoogle Scholar
  42. Zakri AH, Saw LG, Rajanaidu N (1989) National conservation strategies of plant genetic resources in Malaysia. In: Zakri AH (eds) Genetic resources of under-utilised plant in Malaysia. Forest Research Institute Malaysia, Kuala Lumpur, pp 161–179Google Scholar

Copyright information

© The Botanical Society of Japan and Springer 2007

Authors and Affiliations

  • Yoko Fukue
    • 1
    • 4
  • Tomoyuki Kado
    • 2
  • Soon Leong Lee
    • 3
  • Kevin Kit Siong Ng
    • 3
  • Norwati Muhammad
    • 3
  • Yoshihiko Tsumura
    • 1
    • 2
    Email author
  1. 1.Graduate School of Life and Environmental SciencesUniversity of TsukubaTsukubaJapan
  2. 2.Department of Forest Genetics Forestry and Forest Products Research InstituteTsukubaJapan
  3. 3.Forest Research Institute MalaysiaKuala LumpurMalaysia
  4. 4.Forestry Research InstituteOji Paper Company LimitedKameyamaJapan

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