Advertisement

Journal of Plant Research

, Volume 131, Issue 4, pp 623–631 | Cite as

Skewed male reproductive success and pollen transfer in a small fragmented population of the heterodichogamous tree Machilus thunbergii

  • Shuntaro Watanabe
  • Koh-Ichi Takakura
  • Yuko Kaneko
  • Naohiko Noma
  • Takayoshi Nishida
Regular Paper
  • 123 Downloads

Abstract

Heterodichogamy is defined as the presence of two flower morphs that exhibit the male and female functions at different times among individuals within a population. Heterodichogamy is regarded as an adaptation to promote outcrossing through enhanced inter-morph mating, together with a 1:1 morph ratio. However, in highly fragmented populations, the morph ratio may be more likely to be biased by stochastic events. In such a situation, individuals of a minority morph within a population are expected to have higher reproductive success than those of a majority morph, which may suffer from pollen shortages of the minority morph. In this paper, we evaluated mating patterns and male reproductive success in a highly fragmented population of Machilus thunbergii, a putative heterodichogamous evergreen laurel tree. Results of paternity analysis indicated that the selfing rate was not clearly different between the two morphs. In contrast, the proportion of intra-morph mating was higher in the majority-morph (MM) mother trees than in the minority-morph (MF) mother trees. Bayesian estimated male reproductive success indicated that male reproductive success was higher in minority-morph (MF) than in majority-morph (MM) mother trees. These findings indicate that (1) the majority morph mothers, suffering a shortage of the opposite morph pollen, could partly compensate for the reduced reproductive success by intra-morph mating rather than by selfing, and (2) negative-frequency dependent selection may be involved in the maintenance of the two morphs.

Keywords

Frequency-dependent selection Heterodichogamy Machilus thunbergii Male reproductive success Paternity analysis 

Notes

Acknowledgements

We would like to thank two anonymous reviewers for careful reading and valuable comments. S.W. was supported by the Future Development Funding Program of Kyoto University Research Coordination Alliance. Y. K. was supported by a Grant-in-Aid for Scientific Research (Nos. 25340115, 15H04418) from the Ministry of Education, Culture, Sports, Science and Technology, Japan.

References

  1. Abramowitz M, Stegun IA (1964) Handbook of mathematical functions with formulas, graphs, and mathematical table. US Government Printing Office, WashingtonGoogle Scholar
  2. Asai T (2000) Dichogamy in fullmoon maple (Acer japonicum Thunb.). Bull Hokkaido For Res Inst 37:27–40 (in Japanese)Google Scholar
  3. Austerlitz F, Dick CW, Dutech C, Klein EK, Oddou-Muratorio S, Smouse PE, Sork VL (2004) Using genetic markers to estimate the pollen dispersal curve. Mol Ecol 13:937–954CrossRefPubMedGoogle Scholar
  4. Bai WN, Zeng YF, Liao WJ, Zhang DY (2006) Flowering phenology and wind pollination efficacy of heterodichogamous Juglans mandshurica (Juglandaceae). Ann Bot 98:397–402CrossRefPubMedPubMedCentralGoogle Scholar
  5. Bai WN, Zeng YF, Zhang DY (2007) Mating patterns and pollen dispersal in a heterodichogamous tree, Juglans mandshurica (Juglandaceae). New Phyt 176:699–707CrossRefGoogle Scholar
  6. Barrett SCH (2002) The evolution of plant sexual diversity. Nat Rev Genet 3:237–284CrossRefGoogle Scholar
  7. Barrett SCH, Hodgins KA (2006) Floral design and the evolution of asymmetrical mating systems. In: Harder LD, Barret SCH (eds) Ecology and evolution of flowers. Oxford University Press, Oxford, pp 239–254Google Scholar
  8. Clark JS, Macklin E, Wood L (1998) Stages and spatial scales of recruitment limitation in southern Appalachian forests. Ecol Monogr 68:213–235CrossRefGoogle Scholar
  9. Degani C, EL-Batsri R, Gazit S (1997) Outcrossing rate,yield and selective fruit abscission in ‘Ettinger’ and‘Ardith’ avocado plots. J Am Soc Hortic Sci 122:813–817Google Scholar
  10. Eckert CG, Manicacci D, Barrett SCH (1996) Frequency dependent selection on morph ratios in tristylous Lythrum salicaria (Lythraceae). Heredity 77:581–588CrossRefGoogle Scholar
  11. Fukuhara T, Tokumaru S (2014) Inflorescence dimorphism, heterodichogamy and thrips pollination in Platycarya strobilacea (Juglandaceae). Ann Bot 113:467–476CrossRefPubMedGoogle Scholar
  12. Gelman A, Rubin DB (1992) Inference from iterative simulation using multiple sequences. Stat Sci 7:457–511CrossRefGoogle Scholar
  13. Gleeson SK (1982) Heterodichogamy in walnuts: inheritance and stable ratios. Evolution 36:892–902CrossRefPubMedGoogle Scholar
  14. Gleiser G, Verdú M, Segarra-Moragues JG, González-Martínez SC, Pannell JR (2008) Disassortative mating, sexual specialization, and the evolution of gender dimorphism in heterodichogamous Acer opalus. Evolution 62:1676–1688CrossRefPubMedGoogle Scholar
  15. Hattori T (1992) Synecological study on Persea thunbergii type forest: geographical distribution and habitat conditions of Persea thunbergii forest. Jpn J Ecol 42:215–230 (in Japanese)Google Scholar
  16. Hattori T, Nakanishi S (1985) On the distributional limits of the lucidophyllous forest in the Japanese Archipelago. J Plant Res 98:317–333Google Scholar
  17. Ishihama F, Nakano C, Ueno S, Ajima M, Tsumura Y, Washitani I (2003) Seed set and gene flow patterns in an experimental population of an endangered heterostylous herb with controlled local opposite-morph density. Funct Ecol 17:680–689CrossRefGoogle Scholar
  18. Ishihama F, Ueno S, Tsumura Y, Washitani I (2006) Effects ofdensity and floral morph on pollen flow and seedreproduction of an endangered heterostylous herb, Primula sieboldii. J Ecol 94:846–855CrossRefGoogle Scholar
  19. Kalinowski ST, Taper ML, Marshall TC (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol 16:1099–1106CrossRefPubMedGoogle Scholar
  20. Kaneko Y, Lian C, Watanabe S, Shimatani K, Sakio H, Noma N (2012) Development of microsatellites in Machilus thunbergii (Lauraceae), a warm temperate coastal tree species in Japan. Am J Bot 99:e265–e267CrossRefPubMedGoogle Scholar
  21. Kikuchi S, Shibata M, Tanaka H, Yoshimaru H, Niiyama K (2009) Analysis of the disassortative mating pattern in a heterodichogamous plant, Acer mono maxim. using microsatellite markers. Plant Ecol 204:43–54CrossRefGoogle Scholar
  22. Kimura M, Seiwa K, Suyama Y, Ueno N (2003) Flowering system of heterodichogamous Juglans ailanthifolia. Plant Species Biol 18:75–84CrossRefGoogle Scholar
  23. Kimura M, Goto S, Suyama Y, Matsui M, Woeste K, Seiwa K (2012) Morph-specific mating patterns in a low-density population of a heterodichogamous tree, Juglans ailantifolia. Plant Ecol 213:1477–1487CrossRefGoogle Scholar
  24. Klein EK, Desassis N, Oddou-Muratorio S (2008) Pollen flow in the wild service tree, Sorbus torminalis (L.) Crantz. IV. Whole interindividual variance of male fecundity estimated jointly with the dispersal kernel. Mol Ecol 17:3323–3336CrossRefPubMedGoogle Scholar
  25. Kominami Y (2009) Machilus thunbergii Sieb. et Zucc. In: Watanabe S (ed) Silvics of Japan. J-FIC, Tokyo, pp 459–477 (in Japanese)Google Scholar
  26. Kominami Y, Sato T, Takeshita K, Manabe T, Endo A, Noma N (2003) Classification of bird-dispersed plants by fruiting phenology, fruits size and growth form in a primary lucidophyllous forest: an analysis, with implication for the conservation of fruit-bird interactions. Ornithol Sci 2:3–23CrossRefGoogle Scholar
  27. Kubitzki K, Kurz H (1984) Synchronized dichogamy and dioecy in Neotropical Lauraceae. Plant Syst Evol 147:253–266CrossRefGoogle Scholar
  28. Lloyd DG, Webb CJ (1986) The avoidance of interference between the presentation of pollen and stigmas in angiosperms I. Dichogamy. New Zeal J Bot 24:135–162CrossRefGoogle Scholar
  29. Marshall TC, Slate J, Kruuk LEB, Pemberton JM (1998) Statistical confidence for likelihood-based paternity inference in natural populations. Mol Ecol 7:639–655CrossRefPubMedGoogle Scholar
  30. Meagher TR (1986) Analysis of paternity within a natural population of Chamaelirium luteum. I. Identification of most-likely male parents. Am Nat 128:199–215CrossRefGoogle Scholar
  31. Murawski DA, Hamrick JL (1991) The effect of the density of flowering individuals on the mating systems of nine tropical tree species. Heredity 67:167–174CrossRefGoogle Scholar
  32. 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 118:423–430CrossRefPubMedGoogle Scholar
  33. Noma N, Yumoto T (1997) Fruiting phenology of animal-dispersed plants in response to winter migration of frugivores in a warm temperate forest on Yakushima Island, Japan. Ecol Res 12:119–129CrossRefGoogle Scholar
  34. R Development Core Team (2012) R: A language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  35. Renner SS (2001) How common is heterodichogamy? Trends Ecol Evol 16:595–597CrossRefGoogle Scholar
  36. Setsuko S, Nagamitsu T, Tomaru N (2013) Pollen flow and effects of population structure on selfing rates and female and male reproductive success in fragmented Magnolia stellata populations. BMC Ecol 13:10CrossRefPubMedPubMedCentralGoogle Scholar
  37. Shang H, Luo Y-B, Bai W-N (2012) Influence of asymmetrical mating patterns and male reproductive success on the maintenance of sexual polymorphism in Acer pictum subsp. mono (Aceraceae). Mol Ecol 21:3879–3892CrossRefGoogle Scholar
  38. Stout AB (1923) A study in cross-pollination of avocados in Southern California. California Avocado Association Annual Report 1922–1923 8:29–45Google Scholar
  39. Tagawa H (1973) An investigation of initial regeneration in an evergreen broadleaved forest of MINAMATA special research area of IBP. I. Juvenile production and the distribution of two dominant species. Reports from the EBINO Biological Laboratory. Kyushu Univ 1:73–80Google Scholar
  40. Tani N, Tsumura Y, Kado T, Taguchi Y, Lee SL, Muhammad N, Ng KKS, Numata S, Nishimura S, Konuma A, Okuda T (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. Ann Bot 104:1421–1434CrossRefPubMedPubMedCentralGoogle Scholar
  41. Tani N, Tsumura Y, Fukasawa K, Kado T, Taguchi Y, Lee SL, Lee CT, Muhammad N, Niiyama K, Otani T, Yagihashi T, Ripin A, Kassim AR (2012) Male fecundity and pollen dispersal in hill dipterocarps: significance of mass synchronized flowering and implications for conservation. J Ecol 100:405–415CrossRefGoogle Scholar
  42. Teichert H, Dötterl S, Gottsberger G (2011) Heterodichogamy and nitidulid beetle pollination in Anaxagorea prinoides, an early divergent Annonaceae. Plant Syst Evol 291:25–33CrossRefGoogle Scholar
  43. Vogler DW, Kalisz S (2001) Sex among the flowers: the distribution of plant mating systems. Evolution 55:202–204CrossRefPubMedGoogle Scholar
  44. Watanabe S, Noma N, Nishida T (2016) Flowering phenology and mating success of the heterodichogamous tree Machilus thunbergii Sieb. et Zucc (Lauraceae). Plant Species Biol 31:29–37CrossRefGoogle Scholar
  45. Yampolsky E, Yampolsky HY (1922) Distribution of sex forms in the phanerogamic flora. Bibliotheca Genetica 3:1–62Google Scholar
  46. Yumoto T (1987) Pollination systems in a warm–temperate evergreen broad-leaved forest on Yaku Island. Ecol Res 2:133–145CrossRefGoogle Scholar

Copyright information

© The Botanical Society of Japan and Springer Japan KK, part of Springer Nature 2018

Authors and Affiliations

  • Shuntaro Watanabe
    • 1
  • Koh-Ichi Takakura
    • 2
  • Yuko Kaneko
    • 3
  • Naohiko Noma
    • 2
  • Takayoshi Nishida
    • 2
  1. 1.Field Science Education and Research Centre (FSERC)Kyoto UniversityKyotoJapan
  2. 2.School of Environmental ScienceThe University of Shiga PrefectureHikoneJapan
  3. 3.Natural Science LaboratoryToyo UniversityTokyoJapan

Personalised recommendations