Genetic population structure of Osmunda japonica, rheophilous Osmunda lancea and their hybrids

Abstract

Rheophilous Osmunda lancea often hybridizes with a dryland ally, Osmunda japonica, to produce O. × intermedia, forming zonation in riverbanks and the adjacent dryland along flooding frequency clines. This study examined the genetic structure of populations consisting of O. × intermedia and the two parental species by analyzing ten nuclear DNA markers [six cleaved amplified polymorphic sequence (CAPS) markers and three simple sequence repeat (SSR) markers developed from an expressed sequence tag (EST) library, and the sequence of the glyceraldehyde-3-phosphate dehydrogenase gene GapCp] and chloroplast DNA sequences. The results suggest that the nuclear genes of O. japonica and O. lancea are genetically differentiated despite shared polymorphism in their chloroplast DNA sequences. This discrepancy may be attributable to natural selection and recent introgression, although it is not evident if introgression occurs between O. japonica and O. lancea in the examined populations. Our findings of putative F2 hybrids in O. × intermedia support its partial reproducibility, and also suggest that formation of later-generation hybrids generates morphological variation in O. × intermedia. O. lancea plants collected from geographically distant localities were genetically very similar, and it is suggested that O. lancea originated monotopically.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

References

  1. Altshul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z (1997) Gapped Blast and PSI-BlAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  Google Scholar 

  2. Anderson EC, Thompson EA (2002) A model-based method for identifying species hybrids using multilocus genetic data. Genetics 160:1217–1229

    CAS  PubMed  Google Scholar 

  3. Bowcock AM, Ruiz-Linares A, Tomfohrde J, Minch E, Kidd JR, Cavalli-Sforza LL (1994) High resolution of human evolutionary trees with polymorphic microsatellites. Nature 368:455–457

    Article  CAS  PubMed  Google Scholar 

  4. Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587

    CAS  PubMed  Google Scholar 

  5. Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376

    Article  CAS  PubMed  Google Scholar 

  6. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Article  Google Scholar 

  7. Funk DJ, Omland KE (2003) Species-level paraphyly and polyphyly: frequency, causes, and consequences, with insights from animal mitochondrial DNA. Annu Rev Ecol Evol Syst 34:397–423

    Article  Google Scholar 

  8. Gottlieb LD (1972) Levels of confidence in analysis of hybridization in plants. Ann Mo Bot Gard 59:435–446

    Article  Google Scholar 

  9. Hasebe M, Oumori T, Nakazawa M, Iwatsuki K, Kato M (1994) rbcL gene sequences gave new clue to evolutionary lineage for leptosporangiate ferns. Proc Natl Acad Sci USA 91:5730–5734

    Article  CAS  PubMed  Google Scholar 

  10. Heiser CB (1973) Introgression re-examined. Bot Rev 39:347–366

    Article  Google Scholar 

  11. Hey J, Won YJ, Sivasundar A, Nielsen R, Markert JA (2004) Using nuclear haplotypes with microsatellites to study gene flow between recently separated Cichlid species. Mol Ecol 13:909–919

    Article  CAS  PubMed  Google Scholar 

  12. Imaichi R, Kato M (1992) Comparative leaf development of Osmunda lancea and O. japonica (Osmundaceae): heterochronic origin of rheophytic stenophylly. Bot Mag Tokyo 105:199–213

    Article  Google Scholar 

  13. Kato M (2007) Distribution of Osmundaceae. Bull Natl Mus Nat Sci Ser B 33:81–90

    Google Scholar 

  14. Lexer C, Kremer A, Petit RJ (2006) Shared alleles in sympatric oaks: recurrent gene flow is a more parsimonious explanation than ancestral polymorphism. Mol Ecol 15:2007–2012

    Article  CAS  PubMed  Google Scholar 

  15. Martinsen GD, Whitham TG, Turek RJ, Keim P (2001) Hybrid populations selectively filter gene introgression between species. Evolution 55:1325–1335

    CAS  PubMed  Google Scholar 

  16. Metzgar JS, Skog JE, Zimmer EA, Pryer KM (2008) The paraphyly of Osmunda is confirmed by phylogenetic analyses of seven plastid loci. Syst Bot 33:31–36

    Article  Google Scholar 

  17. Muir G, Schlotterer C (2005) Evidence for shared ancestral polymorphism rather than recurrent gene flow at microsatellite loci differentiating two hybridizing oaks (Quercus spp.). Mol Ecol 14:549–561

    Article  CAS  PubMed  Google Scholar 

  18. Ohwi J (1957) Flora of Japan. Pteridophyta. Shibundo, Tokyo

    Google Scholar 

  19. Patterson N, Richter DJ, Gnerre S, Lander ES, Reich D (2006) Genetic evidence for complex speciation of humans and chimpanzees. Nature 441:1103–1108

    Article  CAS  PubMed  Google Scholar 

  20. Petersen J, Brinkmann H, Cerff R (2003) Origin, evolution, and metabolic role of a novel glycolytic GAPDH enzyme recruited by land plant plastids. J Mol Evol 57:16–26

    Article  CAS  PubMed  Google Scholar 

  21. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    CAS  PubMed  Google Scholar 

  22. Rieseberg LH, Wendel J (1993) Introgression and its consequences in plants. In: Harrison R (ed) Hybrid zones and the evolutionary process. Oxford University Press, Oxford, pp 70–114

    Google Scholar 

  23. Rieseberg LH, Whitton J, Linder CR (1996) Molecular marker incongruence in plant hybrid zones and phylogenetic trees. Acta Bot Neerl 45:243–262

    CAS  Google Scholar 

  24. Shimura Y (1964) Observations on the fertile fronds of Osmunda lancea var. latipinnula. J Jpn Bot 39:242–246

    Google Scholar 

  25. Shimura Y (1972) Study of reproduction of Osmunda × intermedia Sugimoto. J Geobot 20:38–42

    Google Scholar 

  26. Shimura Y, Matsumoto S (1977) On the chromosome association in meiosis of Osmunda × intermedia. J Jpn Bot 52:377–378

    Google Scholar 

  27. Swofford DL (2002) PAUP*. Phylogenetic Analysis Using Parsimony (*and other methods), version 4. Sinauer Associates, Sunderland

    Google Scholar 

  28. 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

    Article  CAS  PubMed  Google Scholar 

  29. Tagawa M (1959) Colored illustrations of the Japanese Pteridophyta. Hoikusha, Osaka

    Google Scholar 

  30. Tsutsumi C, Kato M (2005) Molecular phylogenetic study on Davalliaceae. Fern Gaz 17:147–162

    Google Scholar 

  31. van Steennis CGGJ (1981) Rheophytes of the World. Sijthoff & Noordhoff, Alphen aan den Rijn

    Google Scholar 

  32. van Steennis CGGJ (1987) Rheophytes of the world: supplement. Allertonia 4:267–330

    Google Scholar 

  33. Yatabe Y, Nishida H, Murakami N (1999) Phylogeny of Osmundaceae inferred from rbcL nucleotide sequences and comparison to the fossil evidence. J Plant Res 112:397–404

    Article  CAS  Google Scholar 

  34. Yatabe Y, Murakami N, Iwatsuki K (2005) Claytosmunda; a new subgenus of Osmunda (Osmundaceae). Acta Phytotax Geobot 56:127–128

    Google Scholar 

Download references

Acknowledgments

We thank S. Akiyama, A. Ebihara, G. Kokubugata, S. Matsumoto and T. Minamitani for providing materials used in this study. We also thank N. Katayama and S. Koi for their collaborative field work and, M. Takamiya, M. Tanaka and S. Kobayashi for information on localities of Osmunda × intermedia and O. lancea. This study was supported by grants-in-aid numbers 1806295 (to Y.Y.) and 20247006 (to M.K.) from the Japan Society for the Promotion of Science.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Yoko Yatabe.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Yatabe, Y., Tsutsumi, C., Hirayama, Y. et al. Genetic population structure of Osmunda japonica, rheophilous Osmunda lancea and their hybrids. J Plant Res 122, 585 (2009). https://doi.org/10.1007/s10265-009-0254-4

Download citation

Keywords

  • Rheophyte
  • Osmunda
  • Hybrid
  • Expressed sequence tag
  • Simple sequence repeat
  • Cleaved amplified polymorphic sequence
  • Genetic population structure