Abstract
Shorea (Dipterocarpaceae) is a large genus in which many closely related species often grow together in Southeast Asian lowland tropical rain forests. Many Shorea species share common pollinators, and earlier studies suggested occurrence of interspecific hybridization and introgression. Here, we show morphological and molecular evidence of hybridization between Shorea species. In the census of all the trees of Shorea curtisii, Shorea leprosula, and Shorea parvifolia (>30 cm dbh) within the 164-ha area of Bukit Timah Nature Reserve in Singapore, we found 21 morphologically recognizable hybrid individuals. All of the putative hybrids could be distinguished obviously from the parental species on the basis of vegetative characters. Population genetic analysis of DNA sequences of two nuclear (GapC and PgiC) and chloroplast (trnL-trnF) regions demonstrated that each of the three species had several species-specific mutations. The nuclear sequences of the putative hybrids were heterozygote at all the species-specific sites between two parental species. Hybrid between S. curtisii and S. leprosula was found most, while S. curtisii × S. parvifolia and S. leprosula × S. parvifolia hybrids were also found. Almost no shared polymorphism between populations of the parental species suggests rarity of introgression. The study indicated that natural hybridization between sympatric Shorea species should not be uncommon, but all of the hybrid individuals were F1, and the post-F1 hybrids were considerably rare.
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References
Anderson E (1948) Hybridization of the habitat. Evolution 2:1–9
Appanah S, Rasol AMM (1990) Smaller trees can fruit in logged dipterocarp forests. J Trop For Sci 3:80–87
Arnold ML (1993) Rarity of hybrid formation and introgression in Louisiana irises. Plant Gen Newsl 9:14–17
Arnold ML (1997) Natural Hybridization and Evolution: Oxford Series in Ecology and Evolution. Oxford Univ Press, Oxford
Ashton PS (1963) Taxonomic notes on Bornean Dipterocarpaceae. Gard Bull Singapore 20:229–284
Ashton PS (1969) Speciation among tropical forest trees: some deductions in the light of recent evidence. Biol J Linn Soc 1:155–196
Ashton PS (1982) Dipterocarpaceae. Flora Malesiana 9:237–552
Ashton PS (1988) Dipterocarp biology as a window to the understanding of tropical forest structure. Ann Rev Ecolog Syst 19:347–370
Ashton PS (2004) Dipterocarpaceae. Tree Flora of Sabah and Sarawak 5:63–388
Bawa KS (1998) Conservation of genetic resources in the Dipterocarpaceae. In: Appanah S, Turnbull JM (eds) A review of dipterocarps taxonomy, ecology and silviculture. Center for International Forestry Research, Bogor, pp 45–55
Cao CP, Finkeldey R, Siregar IZ, Siregar UJ, Gailing O (2006) Genetic diversity within and among populations of Shorea leprosula Miq. and Shorea parvifolia Dyer (Dipterocarpaceae) in Indonesia detected by AFLPs. Tree Genet Genomes 4:225–239
Chan HT (1981) Reproductive biology of some Malaysian dipterocarps III. Breeding systems. Malays For 44:28–35
Chan HT, Appanah S (1980) Reproductive biology of some Malaysian dipterocarps I: Flowering biology. Malays For 43:132–143
Corlett RT (1992) The ecological transformation of Singapore: 1819–1990. J Biogeogr 19:411–420
Coyne JA, Orr HA (2004) Speciation. Sinauer, Sunderland
Ellstrand NC, Whitkus R, Rieseberg LH (1996) Distribution of spontaneous plant hybrids. Proc Natl Acad Sci USA 93:5090–5093
Howard DJ, Prezler RW, Williams J, Fenchel S, Boeckler WJ (1997) How discrete are oak species? Insight from a hybrid zone between Quercus grisea and Quercus gambelii. Evolution 51:747–755
Ishiyama H, Kado T, Iwasaki M, Ab Shukor N, Szmidt AE, Yamazaki T (2003) Nucleotide variation in the GapC region of four species of Shorea and its putative hybrids. Tropics 13:89–99
Ishiyama H, Inomata N, Yamazaki T, Ab Shukor N, Szmidt AE (2008) Demographic history and interspecific hybridization of four Shorea species from Peninsular Malaysia inferred from nucleotide polymorphism in nuclear gene regions. Can J For Res 38:996–1007
Kameyama Y, Toyama M, Ohara M (2005) Hybrid origins and F1 dominance in the free-floating sterile bladderwort, Utricularia australis f. australis (Lentibulariaceae). Am J Bot 92:469–476
Kamiya K, Harada K, Tachida H, Ashton PS (2005) Phylogeny of PgiC gene in Shorea and its closely related genera (Dipterocarpaceae), the dominant trees in Southeast Asian tropical rain forests. Am J Bot 92:775–788
Keim P, Paige KN, Whitham TG, Lark KG (1989) Genetic analysis of an interspecific hybrid swarm of Populus: occurrence of unidirectional introgression. Genetics 123:557–565
Kihos DW, Clark C, Thompson WC (1981) The hybrid nature of Encelia lanciniata (Compositae: Heliantheae) and control of population composition by post-dispersal selection. Syst Bot 6:399–411
LaFrankie JV, Chan HT (1991) Confirmation of sequential flowering in Shorea (Dipterocarpaceae). Biotropica 23:200–203
LaFrankie JV, Davies SJ, Wan LK, Lee SK, Lum SKY (2005) Forest trees of Bukit Timah: Population ecology in a tropical forest fragment. Simply Green, Singapore
Levin DA, Francisco-Ortega J, Jansen RK (1996) Hybridization and the extinction of rare plant species. Conserv Biol 10:10–16
Lewontin RC, Birch LC (1966) Hybridization as a source of variation for adaptation to new environments. Evolution 20:315–336
Mallet J (2005) Hybridization as an invasion of the genome. Trends Ecol Evol 20:229–237
Mallet J (2007) Hybrid speciation. Nature 446:279–283
Milne RI, Abbott RJ, Wolff K, Chamberlain DF (1999) Hybridization among sympatric species of Rhododendron (Ericaceae) in Turkey: morphological and molecular evidence. Am J Bot 86:1776–1785
Milne RI, Terzioglu S, Abbott RJ (2003) A hybrid zone dominated by fertile F1s: maintenance of species barriers in Rhododendron. Mol Ecol 12:2719–2729
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. I. Characteristics of the plant-pollinator community in a lowland dipterocarp forest. Am J Bot 85:1477–1501
Naito Y, Kanzaki M, Numata S, Obayashi K, Konuma A, Nishimura S, Ohta S, Tsumura Y, Okuda T, Lee SL Muhammad N (2008) Size-related flowering and fecundity in the tropical canopy tree species, Shorea acuminata (Dipterocarpaceae) during two consecutive general flowering. J Plant Res 121:33–42
Nason JD, Ellstrand NC, Arnold ML (1992) Patterns of hybridization and introgression in populations of oaks, manzanias, and irises. Am J Bot 79:101–111
Ng KKS, Lee SL, Saw LG, Plotkin JB, Koh CL (2006) Spatial structure and genetic diversity of three tropical tree species with different habitat preferences within a natural forest. Tree Genet Genomes 2:121–131
Rieseberg LH, Carney SC (1998) Plant Hybridization. New Phytol 140:598–624
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 86:62–69
Seehausen O, Takimoto G, Roy D, Jokela J (2008) Speciation reversal and biodiversity dynamics with hybridization in changing environments. Mol Ecol 17:30–44
Stebbins GL (1950) Variation and evolution in plants. Columbia Univ Press, New York
Symington CF (1943) Foresters’ manual of dipterocarps, Malaysian Forest Records No. 16. Penerbit Universiti Malaya, Kuala Lumpur, Malaysia
Symington CF (2004) Foresters’ manual of dipterocarps, Revised by Ashton PS, Appanah S, Malaysian Forest Records No. 16. Forest Research Institute Malaysia, Kepong, Malaysia
Taberlet P, Gielly L, Pautou G, Bouvet J (1991) Universal primers for amplification of three non-coding regions of chloroplast DNA. Plant Mol Biol 17:1105–1109
Weeks A, Simpson BB (2004) Molecular genetic evidence for interspecific hybridization among endemic Hispaniolan Bursera (Burseraceae). Am J Bot 91:976–984
Whittemore AT, Schaal BA (1991) Interspecific gene flow in sympatric oaks. Proc Natl Acad Sci USA 88:2240–2544
Wyatt-Smith J (1964) A preliminary vegetation map of Malaysia with descriptions of vegetation types. J Trop Geogr 18:200–213
Zha HG, Milne RI, Hang S (2008) Morphological and molecular evidence of natural hybridization between two distantly related Rhododendron species from the Sino-Himalaya. Bot J Linn Soc 156:119–129
Zhou R, Shi S, Wu CI (2005) Molecular criteria for determining new hybrid species–An application to the Sonneratia hybrids. Mol Phylogenet Evol 35:595–601
Acknowledgements
This study was conducted under permission from National Parks Board, Singapore (NP/RP713 and NP/RP862). Authors thank to the staff of the Singapore Botanic Gardens Herbarium and the herbarium of the Forest Research Institute of Malaysia for access to specimens; to Stuart Davies and Peter Ashton for invaluable help during the development of this paper; and to anonymous reviewers for helpful comments. This research was supported by the Academic Research Fund, National Institute of Education, Nanyang Technological University, Singapore (RP19/00 and RP24/96), and by the Global Environment Research Fund from the Ministry of the Environment, Japan (E-091 and RF-1010).
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Kamiya, K., Gan, Y.Y., Lum, S.K.Y. et al. Morphological and molecular evidence of natural hybridization in Shorea (Dipterocarpaceae). Tree Genetics & Genomes 7, 297–306 (2011). https://doi.org/10.1007/s11295-010-0332-8
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DOI: https://doi.org/10.1007/s11295-010-0332-8