Non-density dependent pollen dispersal of Shorea maxwelliana (Dipterocarpaceae) revealed by a Bayesian mating model based on paternity analysis in two synchronized flowering seasons

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Masuda, Shinsuke ^a,g   Tani, Naoki ^b,d   Ueno, Saneyoshi ^c   Lee, Soon Leong ^d   Muhammad, Norwati ^d   Kondo, Toshiaki ^e   Numata, Shinya ^f   Tsumura, Yoshihiko ^a,c  

^a UNIVERSITY OF TSUKUBA   (Japan)

^b JAPAN INTERNATIONAL RESEARCH CENTER FOR AGRICULTURAL SCIENCES   (Japan)

^c FORESTRY AND FOREST PRODUCTS RESEARCH INSTITUTE   (Japan)

^d FOREST RESEARCH INSTITUTE MALAYSIA   (Malaysia)

^e HIROSHIMA UNIVERSITY   (Japan)

^f TOKYO METROPOLITAN UNIVERSITY   (Japan)

^g KAJIMA CORPORATION   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ALGORITHMS; ANIMALS; BAYES THEOREM; BEETLES; DIPTEROCARPACEAE; DNA, PLANT; FLIGHT, ANIMAL; FLOWERS; GENETIC VARIATION; MICROSATELLITE REPEATS; MODELS, BIOLOGICAL; POLLEN; POLLINATION; REPRODUCTION; SEASONS; WEEVILS;

EID: 84894281785     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0082039     Document Type: Article

References (62)

1. Augspurger CK (1983) Phenology, flowering synchrony, and fruit set of six neotropical shrubs. Biotropica 15: 257-267.
2. Appanah S (1985) General flowering in the climax rain forests of South-east Asia. J Trop Ecol 1: 225-240.
3. Sakai S (2002) General flowering in lowland mixed dipterocarp forests of Southeast Asia. Biol J Linnean Soc 75: 233-247.
4. Sakai S, Momose K, Yumoto T, Nagamitsu T, Nagamasu H, et al. (1999) Plant reproductive phenology over four years including an episode of general flowering in a lowland dipterocarp forest, Sarawak, Malaysia. Am J Bot 86: 1414.
5. Ashton PS, Givnish TJ, Appanah S (1988) Staggered flowering in the Dipterocarpaceae: New insights into floral induction and the evolution of mast fruiting in the aseasonal tropics. Am Nat 132: 44-66. (Pubitemid 19323994)
6. Bawa KS (1974) Breeding Systems of Tree Species of a Lowland Tropical Community. Evolution 28: 85-92.
7. Bawa KS, Bullock SH, Perry DR, Coville RE, Grayum MH (1985) Reproductive biology of Tropical lowland rain forest trees. 2. Pollination systems. Am J Bot 72: 346-356. (Pubitemid 17244074)
8. Ward M, Dick CW, Gribel R, Lowe AJ (2005) To self, or not to self ... A review of outcrossing and pollen-mediated gene flow in neotropical trees. Heredity 95: 246-254. (Pubitemid 41372103)
9. Dick CW, Hardy OJ, Jones FA, Petit RJ (2008) Spatial scales of pollen and seed-mediated gene flow in tropical rain forest trees. Tropical Plant Biology 1: 20-33.
10. Appanah S, Chan HT (1981) Thrips: the pollinators of some dipterocarps. The Malaysian Forester 44: 234-252.
11. Momose K, Yumoto T, Nagamitsu T, Kato M, Nagamasu H, et al. (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.
12. Ghazoul J, Liston KA, Boyle TJB (1998) Disturbance induced density dependent seed set in Shorea siamensis (Dipterocarpaceae), a tropical forest tree. J Ecol 86: 462-473. (Pubitemid 28329290)
13. 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: 3575-3584. (Pubitemid 39415686)
14. Kettle CJ, Maycock CR, Ghazoul J, Hollingsworth PM, Khoo E, et al. (2011) Ecological implications of a flower size/number trade-off in tropical forest trees. PloS one 6: e16111.
15. Feinsinger P, Tiebout III HM, Young BE (1991) Do tropical bird-pollinated plants exhibit density-dependent interactions? Field experiments. Ecology 72: 1953-1963.
16. Jones FA, Comita LS (2008) Neighbourhood density and genetic relatedness interact to determine fruit set and abortion rates in a continuous tropical tree population. PRoceedings of the Royal Society B 275: 2759-2767.
17. Janzen DH (1970) Herbivores and the number of tree species in tropical forests. Am Nat 104: 501-528.
18. Wright JS (2002) Plant diversity in tropical forests: a review of mechanisms of species coexistence. Oecologia 130: 1-14.
19. Burd M (1994) Bateman's principle and plant reproduction: the role of pollen limitation in fruit and seed set. The Botanical Review 60: 83-139.
20. Eckert CG, Kalisz S, Geber MA, Sargent R, Elle E, et al. (2010) Plant mating systems in a changing world. Trends Ecol Evol 25: 35-43.
21. Obayashi K, Tsumura Y, Ihara-Ujino T, Niiyama K, Tanouchi H, et al. (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: 151-158. (Pubitemid 34063166)
22. Naito Y, Kanzaki M, Iwata H, Obayashi K, Lee SL, et al. (2008) Density-dependent selfing and its effects on seed performance in a tropical canopy tree species, Shorea acuminata (Dipterocarpaceae). For Ecol Manage 256: 375-383.
23. Kondo T, Nishimura S, Naito Y, Tsumura Y, Okuda T, et al. (2011) Can Tiny Thrips Provide Sufficient Pollination Service During a General Flowering Period in Tropical Rainforest? In: Isag Y and Suyama Y, editors. Single-Pollen Genotyping. Tokyo: Springer. pp. 63-81.
24. Tani N, Tsumura Y, Fukasawa K, Kado T, Taguchi Y, et al. (2012) Male fecundity and pollen dispersal in the hill dipterocarp: significance of mass synchronized flowering and implications for conservation. J Ecol 100: 405-415.
25. Symington CF (2004) Foresters' manual of dipterocarps. In: Barlow H. S., Ashton P. S. and Appanah S., editors. Malayan forest records No 16. Kuala Lumpur: Forest Research Institute Malaysia.
26. Sun IF, Chen YY, Hubbell SP, Wright SJ, Noor N (2007) Seed predation during general flowering events of varying magnitude in a Malaysian rain forest. J Ecol 95: 818-827. (Pubitemid 46944396)
27. Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8: 4321-4325.
28. Masuda S, Tani N, Ohtani M, Lee SL, Muhammad N, et al. (2010) Isolation and characterization of 12 microsatellite loci for the tropical tree species Shorea maxwelliana and S. laevis (Dipterocarpaceae). Conservation Genetics Resources 2: 109-111.
29. Marshall TC, Slate J, Kruuk LEB, Pemberton JM (1998) Statistical confidence for likelihood-based paternity inference in natural populations. Mol Ecol 7: 639-655. (Pubitemid 28235973)
30. Kalinowski ST, Taper ML, Marshall TC (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol 16: 1099-1106.
31. Devlin B, Clegg J, Ellstrand NC (1992) The effect of flower production on male reproductive success in wild radish populations. Evolution 46: 1030-1042. (Pubitemid 23395602)
32. Robledo-Arnuncio JJ, Gil L (2005) Patterns of pollen dispersal in a small population of Pinus sylvestris L. revealed by total-exclusion paternity analysis. Heredity 94: 13-22. (Pubitemid 40020163)
33. Tani N, Tsumura Y, Kado T, Taguchi Y, Lee SL, et al. (2009) Paternity analysis-based inference of pollen dispersal patterns, male fecundity variation and influence of flowering tree density and general flowering magnitude in two dipterocarp species. Annals of Botany 104: 1421-1434.
34. Wright S (1943) Isolation by distance. Genetics 28: 114-138.
35. Clark JS (1998) Why trees migrate so fast: confronting theory with dispersal biology and the paleorecord. The American Naturalist 152: 204-224.
36. Austerlitz F, Dick CW, Dutech C, Klein EK, Oddou-Muratorio S, et al. (2004) Using genetic markers to estimate the pollen dispersal curve. Mol Ecol 13: 937-954. (Pubitemid 38390598)
37. Klein EK, Desassis N, Oddou-Muratorio S (2008) Pollen flow in the wildservice tree, Sorbus torminalis (L.) Crantz. IV. Whole interindividual variance of male fecundity estimated jointly with the dispersal kernel. Mol Ecol 17: 3323-3336. (Pubitemid 352030128)
38. Oddou-Muratorio S, Klein EK, Austerlitz F (2005) Pollen flow in the wildservice tree, Sorbus torminalis (L.) Crantz. II. Pollen dispersal and heterogeneity in mating success inferred from parent-offspring analysis. Mol Ecol 14: 4441-4452. (Pubitemid 44943721)
39. Abramowitz M, Stegun IA (1964) Handbook of mathematical functions with formulas, graphs, and mathematical table. Washington, D.C.: US Government Printing Office.
40. Clark JS, Silman M, Kern R, Macklin E, HilleRisLambers J (1999) Seed dispersal near and far: Patterns across temperate and tropical forests. Ecology 80: 1475-1494. (Pubitemid 29355288)
41. Austerlitz F, Smouse PE (2002) Two-generation analysis of pollen flow across a landscape. IV. Estimating the dispersal parameter. Genetics 161: 355-363. (Pubitemid 34564062)
42. Adams WT, Birkes DS (1991) Estimating mating patterns in forest tree populations. In: Fineschi S., Malvolti M. E., Cannata F. and Hattermer H. H., editors. Biochemical Markers in the Population Genetics of Forest Trees. The Hague, The Netherlands: SPB Academic Publishing. pp. 157-172.
43. Burczyk J, Adams WT, Moran GF, Griffin AR (2002) Complex patterns of mating revealed in a Eucalyptus regnans seed orchard using allozyme markers and the neighbourhood model. Mol Ecol 11: 2379-2391. (Pubitemid 35301908)
44. Clark JS, Gelfand AE (2006) A future for models and data in environmental science. Trends Ecol Evol 21: 375-380. (Pubitemid 43947338)
45. Plummer M (2003) JAGS: A program for analysis of Bayesian graphical models using Gibbs sampling. pp. 20 22.
46. Tani N, Fukasawa K (2012) R scripts for mating models to estimate parameters of pollen dispersal kernel and male fecundity. http://researchmap.jp/ taninaoki/Script/: ReaD & Researchmap.
47. Best NG, Cowles MK, Vines K (1995) CODA: Convergence diagnosis and output analysis software for Gibbs sampling output, Version 0.30. MRC Biostatistics Unit, Cambridge University.
48. Gelman A, Rubin DB (1992) Inference from iterative simulation using multiple sequences. Statistical Science 7: 457-511.
49. Kitamura K, Rahman M, Ochiai Y, Yoshimaru H (1994) Estimation of the outcrossing rate on Dryobalanops aromatica Gaertn. f. in primary and secondary forests in Brunei, Borneo, Southeast Asia. Plant species biology 9: 37-41. (Pubitemid 2119968)
50. Murawski DA, Gunatilleke I, Bawa KS (1994) The effects of selective logging on inbreeding in Shorea megistophylla (Dipterocarpaceae) from Sri-Lanka. Conserv Biol 8: 997-1002.
51. Cloutier D, Hardy OJ, Caron H, Ciampi AY, Degen B, et al. (2007) Low inbreeding and high pollen dispersal distances in populations of two Amazonian forest tree species. Biotropica 39: 406-415. (Pubitemid 46642790)
52. Quesada M, Stoner KE, Lobo JA, Herrerias-Diego Y, Palacios-Guevara C, et al. (2004) Effects of Forest Fragmentation on Pollinator Activity and Consequences for Plant Reproductive Success and Mating Patterns in Bat-pollinated Bombacaceous Trees. Biotropica 36: 131-138. (Pubitemid 38774143)
53. Dick CW, Etchelecu G, Austerlitz F (2003) Pollen dispersal of tropical trees (Dinizia excelsa: Fabaceae) by native insects and African honeybees in pristine and fragmented Amazonian rainforest. Mol Ecol 12: 753-764. (Pubitemid 36380433)
54. Lourmas M, Kjellberg F, Dessard H, Joly HI, Chevallier MH (2007) Reduced density due to logging and its consequences on mating system and pollen flow in the African mahogany Entandrophragma cylindricum . Heredity 99: 151-160. (Pubitemid 47123469)
55. Rocha OJ, Aguilar G (2001) Variation in the breeding behavior of the dry forest tree Enterolobium cyclocarpum (Guanacaste) in Costa Rica. Am J Bot 88: 1600-1606. (Pubitemid 33650833)
56. Hall P, Walker S, Bawa K (1996) Effect of forest fragmentation on genetic diversity and mating system in a tropical tree, Pithecellobium elegans. Conserv Biol 10: 757-768. (Pubitemid 27048266)
57. Kenta T, Shimizu KK, Nakagawa M, Okada K, Hamid AA, et al. (2002) Multiple factors contribute to outcrossing in a tropical emergent Dipterocarpus tempehes, including a new pollen-tube guidance mechanism for self-incompatibility. Am J Bot 89: 60.
58. Nagamitsu T, Ichikawa S, Ozawa M, Shimamura R, Kachi N, et al. (2001) Microsatellite analysis of the breeding system and seed dispersal in Shorea leprosula (Dipterocarpaceae). Int J Plant Sci 162: 155-159. (Pubitemid 32116862)
59. Murawski DA, Dayanandan B, Bawa KS (1994) Outcrossing rates of 2 endemic Shorea species from Sri-Lankan tropical rain forests. Biotropica 26: 23-29.
60. Finger A, Kettle C, Kaiser-Bunbury C, Valentin T, Mougal J, et al. (2012) Forest fragmentation genetics in a formerly widespread island endemic tree: Vateriopsis seychellarum (Dipterocarpaceae). Mol Ecol 21: 2369-2382.
61. 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.
62. Matsuki Y, Tateno R, Shibata M, Isagi Y (2008) Pollination efficiencies of flower-visiting insects as determined by direct genetic analysis of pollen origin. Am J Bot 95: 925-930.