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Fine-scale spatial structure of genets and sexes in the dioecious plant Dioscorea japonica, which disperses by both bulbils and seeds

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Abstract

To understand the evolution of clonal reproduction and the diversity of clonal plants, it is necessary to clarify the characteristics of each clonal habit. There has been little research on whether bulbils alter spatial genetic structure (SGS) because of the lack of connection to maternal ramets. We used simple-sequence-repeat (SSR) markers to determine the fine-scale SGS of the dioecious plant Dioscorea japonica, which disperses both as bulbils and as seeds. We also evaluated the contributions of sexual and clonal reproduction and tested for spatial sex segregation (SSS). We discovered 111 genets from 394 ramets in a 2.8-ha plot. Genotypic richness (R = 0.28) and clonal diversity (Simpson’s D = 0.94, Fager’s E = 0.90) were high. We did not find SSS, suggesting that the population does not suffer from a shortage of mating pairs due to clonal reproduction. The Sp values revealed moderate SGS at the genet level (Sp = 0.013–0.014), and the genets intermingled at a local scale. Significant SGS at the ramet level showed that ramets within the same genet tended to aggregate. We also found a skewed clonal spatial distribution. The spatial extent of genets was positively correlated with the number of ramets within a genet. The contribution of bulbil production to the variance of parent–offspring gene dispersal was about one–fifth the contribution from sexual reproduction. These results suggest that the dispersal via bulbils affects the SGS in D. japonica, although its contribution to gene dispersal is small compared to the contribution of sexual reproduction.

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References

  • Alberto F, Gouveia L, Arnaud-Haond S, Perez-Llorens JL, Duarte CM, Serrao EA (2005) Within-population spatial genetic structure, neighbourhood size and clonal subrange in the seagrass Cymodocea nodosa. Mol Ecol 14:2669–2681

    Article  CAS  PubMed  Google Scholar 

  • Arizaga S, Ezcurra E (2002) Propagation mechanisms in Agave macroacantha (Agavaceae), a tropical arid-land succulent rosette. Am J Bot 89:632–641

    Article  Google Scholar 

  • Bauert MR, Kalin M, Baltisberger M, Edwards PJ (1998) No genetic variation detected within isolated relict populations of Saxifraga cernua in the Alps using RAPD markers. Mol Ecol 7:1519–1527

    Article  CAS  Google Scholar 

  • Bierzychudek P, Eckhart V (1988) Spatial segregation of the sexes of dioecious plants. Am Nat 132:34–43

    Article  Google Scholar 

  • Burke J, Bulger M, Wesselingh R, Arnold M (2000) Frequency and spatial patterning of clonal reproduction in Louisiana iris hybrid populations. Evolution 54:137–144

    CAS  PubMed  Google Scholar 

  • Cheplick GP, Kane KH (2004) Genetic relatedness and competition in Triplasis purpurea (Poaceae): resource partitioning or kin selection? Int J Plant Sci 165:623–630

    Article  Google Scholar 

  • Chung MG, Epperson BK (2000) Clonal and spatial genetic structure in Eurya emarginata (Theaceae). Heredity 84:170–177

    Article  PubMed  Google Scholar 

  • Chung JM, Lee BC, Kim JS, Park CW, Chung MY, Chung MG (2006) Fine-scale genetic structure among genetic individuals of the clone-forming monotypic genus Echinosophora koreensis (Fabaceae). Ann Bot 98:165–173

    Article  CAS  PubMed  Google Scholar 

  • Dorken ME, Eckert CG (2001) Severely reduced sexual reproduction in northern populations of a clonal plant, Decodon verticillatus (Lythraceae). J Ecol 89:339–350

    Article  Google Scholar 

  • Duncan RP (1991) Competition and the coexistence of species in a mixed Podocarp stand. J Ecol 79:1073–1084

    Article  Google Scholar 

  • Eckert CG (2000) Contributions of autogamy and geitonogamy to self-fertilization in a mass-flowering, clonal plant. Ecology 81:532–542

    Article  Google Scholar 

  • Epperson BK (2003) Geographical genetics: monographs in population biology. Princeton University Press, Princeton

    Google Scholar 

  • Eppley SM (2005) Spatial segregation of the sexes and nutrients affect reproductive success in a dioecious wind-pollinated grass. Plant Ecol 181:179–190

    Article  Google Scholar 

  • Fager E (1972) Diversity: a sampling study. Am Nat 106:293–310

    Article  Google Scholar 

  • Fenster CB, Vekemans X, Hardy OJ (2003) Quantifying gene flow from spatial genetic structure data in a metapopulation of Chamaecrista fasciculata (Leguminosae). Evolution 57:995–1007

    PubMed  Google Scholar 

  • Gabrielsen TM, Brochmann C (1998) Sex after all: high levels of diversity detected in the arctic clonal plant Saxifraga cernua using RAPD markers. Mol Ecol 7:1701–1708

    Article  Google Scholar 

  • Gliddon C, Belhassen E, Gouyon P (1987) Genetic neighborhoods in plants with diverse systems of mating and different patterns of growth. Heredity 59:29–32

    Article  Google Scholar 

  • Goudet J (1995) FSTAT (Version 1.2): a computer program to calculate F-statistics. J Hered 86:485–486

    Google Scholar 

  • Hardy OJ, Vekemans X (2002) SPAGEDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes 2:618–620

    Article  Google Scholar 

  • Hoffman JI, Amos W (2005) Microsatellite genotyping errors: detection approaches, common sources and consequences for paternal exclusion. Mol Ecol 14:599–612

    Article  CAS  PubMed  Google Scholar 

  • Honnay O, Jacquemyn H (2008) A meta-analysis of the relation between mating system, growth form and genotypic diversity in clonal plant species. Evol Ecol 22:299–312

    Article  Google Scholar 

  • Hori Y (1984) Life-history and population dynamics of the Japanese yam, Dioscorea japonica Thunb. (in Japanese). In: Kawano S (ed) The life history and evolution of plants 2. Baifukan, Tokyo, pp 157–172

    Google Scholar 

  • Jacquemyn H, Brys R, Honnay O, Hermy M, Roldan-Ruiz I (2005) Local forest environment largely affects below-ground growth, clonal diversity and fine-scale spatial genetic structure in the temperate deciduous forest herb Paris quadrifolia. Mol Ecol 14:4479–4488

    Article  CAS  PubMed  Google Scholar 

  • Klimes L, Klimesova J, Hendriks R, van Groenendael J (1997) Clonal plant architecture: a comparative analysis of form and function. In: de Kroon H, van Groenendael J (eds) The ecology and evolution of clonal plants. Backhuys Publishers, Leiden, pp 1–29

    Google Scholar 

  • Klinkhamer P, de Jong T, de Bruyn G (1989) Plant size and pollinator visitation in Cynoglossum officinale. Oikos 54:201–204

    Article  Google Scholar 

  • Korpelainen H (1991) Sex-ratio variation and spatial segregation of the sexes in populations of Rumex acetosa and R. acetosella (Polygonaceae). Plant Syst Evol 174:183–195

    Article  Google Scholar 

  • Loiselle B, Sork V, Nason J, Graham C (1995) Spatial genetic structure of a tropical understory shrub. Am J Bot 82:1420–1425

    Article  Google Scholar 

  • Lotwick HW, Silverman BW (1982) Methods for analyzing spatial processes of several types of points. J R Stat Soc B 44:406–413

    Google Scholar 

  • Marba N, Duarte CM (1998) Rhizome elongation and seagrass clonal growth. Mar Ecol Prog Ser 174:269–280

    Article  Google Scholar 

  • Mizuki I, Takahashi A (2009) Secondary dispersal of Dioscorea japonica (Dioscoreaceae) bulbils by rodents. J For Res 14:95–100

    Article  Google Scholar 

  • Mizuki I, Ishida K, Kikuzawa K (2005a) Sexual and vegetative reproduction in the aboveground part of a dioecious clonal plant, Dioscorea japonica (Dioscoreaceae). Ecol Res 20:387–393

    Article  Google Scholar 

  • Mizuki I, Osawa N, Tsutsumi T (2005b) Thrips (Thysanoptera: Thripidae) on the flowers of a dioecious plant, Dioscorea japonica (Dioscoreaceae). Can Entomol 137:712–715

    Article  Google Scholar 

  • Mizuki I, Tani N, Ishida K, Tsumura Y (2005c) Development and characterization of microsatellite markers in a clonal plant, Dioscorea japonica Thunb. Mol Ecol Notes 5:721–723

    Article  CAS  Google Scholar 

  • Mori Y, Nagamitsu T, Kubo T (2009) Clonal growth and its effects on male and female reproductive success in Prunus ssiori (Rosaceae). Popul Ecol 51:175–186

    Article  Google Scholar 

  • Murray MG, Thompson WF (1980) Rapid isolation of high molecular-weight plant DNA. Nucleic Acids Res 8:4321–4325

    Article  CAS  PubMed  Google Scholar 

  • Nagamitsu T, Ogawa M, Ishida K, Tanouchi H (2004) Clonal diversity, genetic structure, and mode of recruitment in a Prunus ssiori population established after volcanic eruptions. Plant Ecol 174:1–10

    Article  Google Scholar 

  • Nakajima G (1942) Cytological studies in some flowering dioecious plants, with special reference to the sex chromosomes. Cytologia 12:262–270

    Google Scholar 

  • Natsume S, Watanabe M (2001) Genetic properties of Dioscorea japonica (Dioscoreaceae) growing in the Hiyama district of southwest Hokkaido (in Japanese). Res Bull Coll Exp Forests, Hokkaido University 58:1–6

    CAS  Google Scholar 

  • Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590

    CAS  PubMed  Google Scholar 

  • Ohwi J, Kitagawa M (1983) New flora of Japan revised, Shibundo, Tokyo (in Japanese, title translated by I. Mizuki)

  • Parks JC, Werth CR (1993) A study of spatial features of clones in a population of bracken fern, Pteridium aquilinum (Dennstaedtiaceae). Am J Bot 80:537–544

    Article  Google Scholar 

  • Pelissier R, Goreaud F (2007) ads: Spatial point patterns analysis. R package version 1.2–5

  • Persson HA, Gustavsson BA (2001) The extent of clonality and genetic diversity in lingonberry (Vaccinium vitis-idaea L.) revealed by RAPDs and leaf-shape analysis. Mol Ecol 10:1385–1397

    Article  CAS  PubMed  Google Scholar 

  • Pielou EC (1966) Measurement of diversity in different types of biological collections. J Theor Biol 13:131–144

    Article  Google Scholar 

  • R Development Core Team (2008) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Reusch TBH, Stam WT, Olsen JL (2000) A microsatellite-based estimation of clonal diversity and population subdivision in Zostera marina, a marine flowering plant. Mol Ecol 9:127–140

    Article  CAS  PubMed  Google Scholar 

  • Ripley B (1977) Modelling spatial patterns. J R Stat Soc B 39:172–212

    Google Scholar 

  • Ruggiero MV, Reusch TBH, Procaccini G (2005) Local genetic structure in a clonal dioecious angiosperm. Mol Ecol 14:957–967

    Article  CAS  PubMed  Google Scholar 

  • Salisbury E (1942) The reproductive capacity of plants: studies in quantitative biology. Bell and Sons, London

    Google Scholar 

  • Salzman GA, Parker AM (1985) Neighbors ameliorate local salinity stress for a rhizomatous plant in a heterogeneous environment. Oecologia 65:273–277

    Article  Google Scholar 

  • Silvertown J, Charlesworth D (2001) Introduction to plant population biology, 4th edn. Blackwell Science, Oxford

    Google Scholar 

  • Thomas JR, Gibson DJ, Middleton BA (2005) Water dispersal of vegetative bulbils of the invasive exotic Dioscorea oppositifolia L. in southern Illinois. J Torrey Bot Soc 132:187–196

    Article  Google Scholar 

  • Torimaru T, Tomaru N (2005) Fine-scale clonal structure and diversity within patches of a clone-forming dioecious shrub, Ilex leucoclada (Aquifoliaceae). Ann Bot 95:295–304

    CAS  PubMed  Google Scholar 

  • van Kleunen M, Fischer M, Schmid B (2000) Costs of plasticity in foraging characteristics of the clonal plant Ranunculus reptans. Evolution 54(6):1947–1955

    Article  PubMed  Google Scholar 

  • Van Rossum F, Bonnin I, Fenart S, Pauwels M, Petit D, Saumitou-Laprade P (2004) Spatial genetic structure within a metallicolous population of Arabidopsis halleri, a clonal, self-incompatible and heavy-metal-tolerant species. Mol Ecol 13:2959–2967

    Article  PubMed  Google Scholar 

  • Vandepitte K, Roldán-Ruiz I, Leus L, Jacquemyn H, Honnay O (2009) Canopy closure shapes clonal diversity and fine-scale genetic structure in the dioecious understorey perennial Mercurialis perennis. J Ecol 97:404–414

    Article  Google Scholar 

  • Vekemans X, Hardy OJ (2004) New insights from fine-scale spatial genetic structure analyses in plant populations. Mol Ecol 13:921–935

    Article  CAS  PubMed  Google Scholar 

  • Wang CN, Cronk QCB (2003) Meristem fate and bulbil formation in Titanotrichum (Gesneriaceae). Am J Bot 90:1696–1707

    Article  Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 36(6):1358–1370

    Article  Google Scholar 

Download references

Acknowledgments

Financial support was provided by a JSPS Fellowship (No. 16000940) from the Japanese Society for the Promotion of Science. Yong scientist financial supports of Dep of Biol Environ, Akita pref University supported to attend the Clonal plant workshop 2009. The authors thank K. Kikuzawa, S. Nanami, D. Fujiki, M. Ikeuchi, N. Tsujimura, A. Kimura, and the staff of Hiruzen Experimental forest station, Tottori University Forest for their support of this study. We are grateful to Oliver Honnay and Hans Jacquemyn for organizing the Clonal plant workshop 2009 and this special issues.

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Mizuki, I., Ishida, K., Tani, N. et al. Fine-scale spatial structure of genets and sexes in the dioecious plant Dioscorea japonica, which disperses by both bulbils and seeds. Evol Ecol 24, 1399–1415 (2010). https://doi.org/10.1007/s10682-010-9396-z

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