Reticulate evolution in the apogamous Dryopteris varia complex (Dryopteridaceae, subg. Erythrovariae, sect. Variae) and its related sexual species in Japan

Abstract

Apogamous fern species are often difficult to distinguish from related species because of their continuous morphological variations. To clarify the genetic relationships among the members of the Dryopteris varia complex, we analyzed the nucleotide sequences of the plastid gene rbcL and the nuclear gene PgiC. We also analyzed the diploid sexual species D. caudipinna and D. chinensis, which have not been included in the complex, but were recently shown to be closely related to the complex in a molecular phylogenetic study. The PgiC sequences of the diploid sexual species, D. varia, D. saxifraga, D. sp. ‘protobissetiana’ (undescribed diploid sexual species), D. caudipinna, and D. chinensis, were well differentiated and hence designated A, B, C, D, and E, respectively. Thus, the PgiC constitution of apogamous species in the complex was as follows: D. bissetiana, B + C; D. kobayashii, B + C + E); D. pacifica, A + C, A + B + C, or A + C + D; D. sacrosancta, A + C + E; and D. saxifragivaria, B + C. These results suggest that these apogamous species are formed by hybridizations of species including not only the three diploid sexual species of the D. varia complex (A, B, and C) but also the two diploid sexual species D. caudipinna (D) and D. chinensis (E), which do not belong to the complex.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. Adjie B, Masuyama S, Ishikawa H, Watano Y (2007) Independent origins of tetraploid cryptic species in the fern Ceratopteris thalictroides. J Plant Res 120:129–138

    PubMed  Article  CAS  Google Scholar 

  2. Braithwaite AF (1964) A new type of apogamy in ferns. New Phytol 63:293–305

    Article  Google Scholar 

  3. Darnaedi D, Kato M, Iwatsuki K (1990) Electrophoretic evidence for the origin of Dryopteris yakusilvicola (Dryopteridaceae). Bot Mag Tokyo 103:1–10

    Article  Google Scholar 

  4. Döpp W (1939) Cytologische und genetische Untersuchungen innerhalb der Gattung Dryopteris. Planta 29(4):481–533

    Article  Google Scholar 

  5. Doyle JA, Doyle JL (1990) Isolation of plant DNA from fresh tissue. Focus 12:13–15

    Google Scholar 

  6. Dyer RJ, Savolaainen V, Schneider H (2012) Apomixis and reticulate evolution in the Asplenium monanthes fern complex. Ann Bot 110:1515–1529

    PubMed  Article  PubMed Central  Google Scholar 

  7. Dyer RJ, Pellicer J, Savolainen V, Leitch IJ, Schneider H (2013) Genome size expansion and the relationship between nuclear DNA content and spore size in the Asplenium monanthes fern complex (Aspleniaceae). BMC Plant Biol 2013:219

    Article  Google Scholar 

  8. Ebihara A (2011) RbcL phylogeny of Japanese pteridophyte flora and implications on intrafamilial systematics. Bull Natl Mus Nat Sci B 37:63–74

    Google Scholar 

  9. Ebihara A, Ishikawa H, Matsumoto S, Lin S-J, Iwatsuki K, Takamiya M, Watano Y, Ito M (2005) Nuclear DNA, chloroplast DNA, and ploidy analysis clarified biological complexity of the Vandenboschia radicans complex (Hymenophyllaceae) in Japan and adjacent areas. Am J Bot 92:1535–1547

    PubMed  Article  CAS  Google Scholar 

  10. Ebihara A, Matsumoto S, Kato M (2012) Origin of Dryopteris shibipedis (Dryopteridaceae), a fern species extinct in the wild. J Plant Res 125:499–505

    PubMed  Article  Google Scholar 

  11. Ebihara A, Nakato N, Matsumoto S, Chao YS, Kuo LY (2014) Cytotaxonomic studies on thirteen ferns of Taiwan. Bull Natl Mus Nat Sci B (in press)

  12. Fraser-Jenkins CR (1986) A classification of the genus Dryopteris (Pteridophyta: Dryopteridaceae). Bull Br Mus Nat Hist (Bot) 14:183–218

    Google Scholar 

  13. Gastony GJ, Yatskievych G (1992) Maternal inheritance of the chloroplast and mitochondrial genomes in cheilanthoid ferns. Am J Bot 79:716–722

    Article  CAS  Google Scholar 

  14. Grusz AL, Windham MD, Pryer KM (2009) Deciphering the origins of apomictic polyploids in the Cheilanthes yavapensis complex (Pteridaceae). Am J Bot 96:1636–1645

    PubMed  Article  CAS  Google Scholar 

  15. Hasebe M, Omori T, Nakazawa M, Sano T, Kato M, Iwatsuki K (1994) RbcL gene sequences provide evidence for the evolutionary cytotypes of leptosporangiate ferns. Proc Natl Acad Sci USA 91:5730–5734

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  16. Hirabayashi H (1966) Chromosome numbers in Japanese species of Dryopteris (1). J Jpn Bot 41:11–13

    Google Scholar 

  17. Hirabayashi H (1967) Chromosome numbers in Japanese species of Dryopteris (2). J Jpn Bot 42:44–48

    Google Scholar 

  18. Hirabayashi H (1969) Chromosome numbers in Japanese species of Dryopteris (3). J Jpn Bot 44:85–95

    Google Scholar 

  19. Hirabayashi H (1970) Chromosome numbers in Japanese species of Dryopteris (4). J Jpn Bot 45:11–19

    Google Scholar 

  20. Hirabayashi H (1974) Cytogeographic studies on Dryopteris of Japan. Hara Shobo, Tokyo

    Google Scholar 

  21. Huber KT, Oxelman B, Lott M, Moulton V (2006) Reconstructing the evolutionary history of polyploids from multilabeled trees. Mol Biol Evol 23:1784–1791

    PubMed  Article  CAS  Google Scholar 

  22. Ishikawa H, Watano Y, Kano K, Ito M, Kurita S (2002) Development of primer sets for PCR amplification of the PgiC gene in ferns. J Plant Res 115:65–70

    PubMed  Article  CAS  Google Scholar 

  23. Iwatsuki K, Yamazaki T, Boufford DE, Ohba H (1995) Flora of Japan, vol I. Kodansha, Tokyo

    Google Scholar 

  24. Jaruwattanaphan T, Matsumoto S, Watano Y (2013) Reconstructing hybrid speciation events in the Pteris cretica group (Pteridaceae) in Japan and adjacent regions. Syst Bot 38:15–27

    Article  Google Scholar 

  25. Kurata S (1966) Notes on Japanese ferns (39). J Geobot 14:82–86

    Google Scholar 

  26. Kurita S (1961) Chromosome numbers of some Japanese ferns (2). Bot Mag Tokyo 74:395–401

    Article  Google Scholar 

  27. Lee S-J, Park C-W (2013) Relationships and origins of the Dryopteris varia (L.) Kuntze species complex (Dryopteridaceae) in Korea inferred from nuclear and chloroplast DNA sequences. Biochem Syst Ecol 50:371–382

    Article  CAS  Google Scholar 

  28. Lee S-J, Kim Y-D, Suh Y, Lee S-K, Park C-W (2006) Morphological and chromosomal variation of the Dryopteris varia (L.) Kuntze complex (Dryopteridaceae) in Korea. Plant Syst Evol 262:37–52

    Article  Google Scholar 

  29. Lin S-J, Kato M, Iwatsuki K (1992) Diploid and triploid offspring of triploid agamosporous fern Dryopteris pacifica. J Plant Res 105:443–452

    Google Scholar 

  30. Lin S-J, Kato M, Iwatsuki K (1995) Electrophoretic variation of the apogamous Dryopteris varia group (Dryopteridaceae). J Plant Res 108:451–456

    Article  Google Scholar 

  31. Lin S–J, Kato M, Iwatsuki K (2003) Morphological and cytological variations of Japanese Dryopteris Varia group (Dryopteridaceae). In: Pteridology in the new millennium, pp 217–231

  32. Liu HM, Dyer RJ, Guo ZY, Meng Z, Li JH, Schneider H (2012) The evolutionary dynamics of apomixis in ferns: a case study from polystichoid ferns. J Bot ID 510478

  33. Lott M, Spillner A, Huber KT, Petri A, Oxelman B, Moulton V (2009a) Inferring polyploid phylogenies from multiply-labeled gene trees. BMC Evol Biol 9:216

    PubMed  Article  PubMed Central  Google Scholar 

  34. Lott M, Spillner A, Huber KT, Moulton V (2009b) PADRE: a package for analyzing and displaying reticulate evolution. Bioinformatics 25:1199–1200

    PubMed  Article  CAS  Google Scholar 

  35. Lovis JD (1978) Evolutionary patterns and processes in ferns. Adv Bot Res 4:229–415

    Article  Google Scholar 

  36. Manton I (1950) Problems of cytology and evolution in the Pteridophyta. Cambridge University Press, Cambridge

    Google Scholar 

  37. Mitui K (1965) Chromosome studies on Japanese ferns (1). J Jpn Bot 40:117–124

    Google Scholar 

  38. Mitui K (1966) Chromosome studies on Japanese ferns (2). J Jpn Bot 41:60–64

    Google Scholar 

  39. Mitui K (1968) Chromosomes and speciation in fern. Sci Rep Tokyo Kyoiku Daigaku Sect B 13:285–333

    Google Scholar 

  40. Mitui K (1975) Chromosome numbers of Japanese pteridophytes. Bull Nippon Dent Coll Gen Educ 4:221–271

    Google Scholar 

  41. Nakai T (1942) Notulae ad plantas Asiae orientalis (XX). J Jpn Bot 18:281–292

    Google Scholar 

  42. Nakato N, Kato M, Liu BD (1995) A cytotaxonomic study of some ferns from Jiangsu and Zhejiang provinces, China. J Jpn Bot 70:194–204

    Google Scholar 

  43. Narayan RK (1987) Nuclear DNA changes, genome differentiation and evolution in Nicotiana (Solanaceae). Plant Syst Evol 157:161–180

    Article  CAS  Google Scholar 

  44. Nei M, Kumar S (2000) Molecular evolution and phylogenetics. Oxford University Press, New York

    Google Scholar 

  45. Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256

    PubMed  Article  CAS  Google Scholar 

  46. Rambaut A, Drummond AJ (2009) Tracer v1.5. Computer program. http://tree.bio.ed.ac.uk/software/tracer/. Accessed 13 Aug 2001

  47. Ronquist F, Teslenko M, Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542

    PubMed  Article  PubMed Central  Google Scholar 

  48. Serizawa S (2009) Dryopteris kobayashii Kitagawa and D. sacrosancta Koidz. Shidekobushi 1:97–99 (in Japanese)

    Google Scholar 

  49. Sessa EB, Zimmer EA, Givnish TJ (2012) Reticulate evolution on a global scale: a nuclear phylogeny for New World Dryopteris (Dryopteridaceae). Mol Phylogenet Evol 64:563–581

    PubMed  Article  Google Scholar 

  50. Suzuki T, Iwatsuki K (1990) Genetic variation in agamosporous fern Pteris cretica L. in Japan. Heredity 65:221–227

    Article  Google Scholar 

  51. Tagawa M (1959) Coloured Illustrations of the Japanese Pteridophyta. Hoikusha, Osaka (in Japanese)

    Google Scholar 

  52. Takamiya M (1996) Index to chromosomes of Japanese Pteridophyta (1910–1996). Japan Pteridological Society, Tokyo

    Google Scholar 

  53. Takamiya M, Ohta N, Yatabe Y, Murakami N (2001) Cytological, morphological, genetic, and molecular phylogenetic studies on intraspecific differentiations within Diplazium doederleinii (Woodsiaceae: pteridophyta). Int J Plant Sci 162:625–636

    Article  CAS  Google Scholar 

  54. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  55. Tanaka K (1999) Variation of Dryopteris pacifica in the western part of Kanagawa Prefecture. J Nippon Fern Club 3:1–7 (in Japanese)

    Google Scholar 

  56. Tsai JL, Shie WC (1975) Chromosome numbers of the family Aspidiaceae (Sensu Copland) in Taiwan (1). J Sci Eng 12:321–334

    Google Scholar 

  57. Tsai JL, Shieh WC (1985) A cytotaxonomic survey of the fern family Aspidiaceae (Sensu Copeland) in Taiwan. J Sci Eng 22:121–144

    Google Scholar 

  58. Wagner WH Jr (1954) Reticulate evolution in the Appalachian Asplenium. Evolution 7:103–118

    Article  Google Scholar 

  59. Walker TG (1958) Hybridization in some species of Pteris L. Evolution 12:82–92

    Article  Google Scholar 

  60. Watano Y, Iwatsuki K (1988) Genetic variation in the ‘Japanese apogamous form’ of the fern Asplenium unilaterale Lam. Bot Mag Tokyo 101:213–222

    Article  Google Scholar 

Download references

Acknowledgments

We are grateful to the following persons for their assistance in collecting plant material: Chun-Ming Chen of the Koo Botanic Conservation Center (Taiwan); Li-Yaung Kuo of the Taiwan Forestry Research Institute; W. Shinohara of Kagawa University; J. Yamashita of Okayama University; S. J. Lin of Shimane University; S. Tagane of Kyushu University; S. Saito and S. Kariyama of the Kurashiki Museum of Natural History; and S. Fujimoto, Y. Inoue, T. Kuramata, S. Mitani, K. Mizote, K. Mizunashi, K. Ohora, T. Oka, H. Takae, T. Tamaru, K. Tanaka, and I. Yamazumi of the Nippon Fernist Club. We are also grateful to S. Nakamura, T. Sugawara, H. Kato, and Y. Kakugawa of the Makino Herbarium, Tokyo Metropolitan University; S. Serizawa and S. Tsuneki of the Aichi University of Education; and K. Yamamoto of the National Museum of Nature and Science, Japan for their valuable suggestions and advice during the course of this study. This study is partly supported by Grants-in-Aid for Scientific Research No. 25291089 and by the Environment Research and Technology Development Fund (S-9) of the Ministry of the Environment, Japan for N. Murakami. We would like to thank Enago (http://www.enago.jp) for the English language review.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Kiyotaka Hori.

Appendices

Appendix 1

See Table 3

Table 3 Voucher specimens examined in this study

Appendix 2

See Table 4

Table 4 DNA data accession numbers of the obtained nucleotide sequences in this study

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Hori, K., Tono, A., Fujimoto, K. et al. Reticulate evolution in the apogamous Dryopteris varia complex (Dryopteridaceae, subg. Erythrovariae, sect. Variae) and its related sexual species in Japan. J Plant Res 127, 661–684 (2014). https://doi.org/10.1007/s10265-014-0652-0

Download citation

Keywords

  • Apogamy
  • Fern
  • PgiC
  • rbcL
  • Reticulate evolution
  • Single-strand conformation polymorphism (SSCP)