Abstract
Independent gametophyte ferns are unique among vascular plants because they are sporophyteless and reproduce asexually to maintain their populations in the gametophyte generation. Such ferns had been primarily discovered in temperate zone, and usually hypothesized with (sub)tropical origins and subsequent extinction of sporophyte due to climate change during glaciations. Presumably, independent fern gametophytes are unlikely to be distributed in tropics and subtropics because of relatively stable climates which are less affected by glaciations. Nonetheless, the current study presents cases of two independent gametophyte fern species in subtropic East Asia. In this study, we applied plastid DNA sequences (trnL-L-F and matK + ndhF + chlL datasets) and comprehensive sampling (~80%) of congeneric species for molecular identification and divergence time estimation of these independent fern gametophytes. The two independent gametophyte ferns were found belonging to genus Haplopteris (vittarioids, Pteridaceae) and no genetic identical sporophyte species in East Asia. For one species, divergence times between its populations imply recent oversea dispersal(s) by spores occurred during Pleistocene. By examining their ex situ and in situ fertility, prezygotic sterility was found in these two Haplopteris, in which gametangia were not or very seldom observed, and this prezygotic sterility might attribute to their lacks of functional sporophytes. Our field observation and survey on their habitats suggest microhabitat conditions might attribute to this prezygotic sterility. These findings point to consideration of whether recent climate change during the Pleistocene glaciation resulted in ecophysiological maladaptation of non-temperate independent gametophyte ferns. In addition, we provided a new definition to classify fern gametophyte independences at the population level. We expect that continued investigations into tropical and subtropical fern gametophyte floras will further illustrate the biogeographic significance of non-temperate fern gametophyte independence.
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References
Bazinet AL, Zwickl DJ, Cummings MP (2014) A gateway for phylogenetic analysis powered by grid computing featuring GARLI 2.0. Syst Biol 63:812–818
Bouckaert R, Heled J, Kühnert D, et al (2014) BEAST 2: a software platform for Bayesian evolutionary analysis. PLoS Ccomputational Biol 10:e1003537
Chang C-S, Kim H, Chang KS (2014) Provisional checklist of vascular plants for the Korea Peninsula Flora (KPF). Version 1.0
Chen C-W, Huang Y-M, Kuo L-Y et al (2013a) A new vittarioid fern species, Haplopteris heterophylla (Pteridaceae). Syst Bot 38:901–909
Chen C-W, Huang Y-M, Kuo L-Y et al (2013b) TrnL-F is a powerful marker for DNA identification of field vittarioid gametophytes (Pteridaceae). Ann Bot 111:663–673
Chen C-W, Ebihara A, Chiou W-L, Li C-W (2014) Haplopteris yakushimensis (Pteridaceae, Vittarioideae), a new species from Yakushima Island, Japan. Phytotaxa 156:229–234
Dassler CL, Farrar DR (1997) Significance of form in fern gametophytes: clonal, gemmiferous gametophytes of Callistopteris baueriana (Hymenophyllaceae). Int J Plant Sci 158:622–639
Dassler CL, Farrar DR (2001) Significance of gametophyte form in long-distance colonization by tropical, epiphytic ferns. Brittonia 53:352–369
Duffy AM, Stensvold MC, Farrar DR (2015) Independent gametophytes of Hymenophyllum wrightii in North America: not as rare as we thought. Am Fern J 105:45–55
Ebihara A, Farrar DR, Ito M (2008) The sporophyte-less filmy fern of eastern North America Trichomanes intricatum (Hymenophyllaceae) has the chloroplast genome of an Asian species. Am J Bot 95:1645–1651
Ebihara A, Yamaoka A, Mizukami N et al (2013) A survey of the fern gametophyte flora of Japan: frequent independent occurrences of noncordiform gametophytes. Am J Bot 100:735–743
Farrar DR (1967) Gametophytes of four tropical fern genera reproducing independently of their sporophytes in the southern Appalachians. Science 155:1266–1267
Farrar DR (1974) Gemmiferous fern gametophytes-Vittariaceae. Am J Bot 61:146–155
Farrar DR (1978) Problems in the identity and origin of the Appalachian Vittaria gametophyte, a sporophyteless fern of the eastern United States. Am J Bot 65:1–12
Farrar DR (1985) Independent fern gametophytes in the wild. Proc R Soc Edinburgh Sect B Biol Sci 86:361–369
Farrar DR (1990) Species and evolution in asexually reproducing independent fern gametophytes. Syst Bot 15:98–111
Farrar DR (1992) Trichomanes intricatum: the independent Trichomanes gametophyte in the eastern United States. Am Fern J 82:68–74
Farrar DR (2016) Vittaria appalachiana continues to provide insight into the biology of ferns: a commentary on two studies recently published in American. J Bot Am J Bot 103:593–595
Farrar DR, Mickel JT (1991) Vittaria appalachiana: a name for the “Appalachian gametophyte”. Am Fern J 81:69–75
Gillespie RG, Baldwin BG, Waters JM et al (2012) Long-distance dispersal: a framework for hypothesis testing. Trends Ecol Evol 27:47–56
Harrison SP, Yu G, Takahara H, Prentice IC (2001) Diversity of temperate plants in East Asia. Nature 413:129–130
Hatusima S (1991) Flora of the Northern Ryukyus. Asahiinsatsushoseki, Kagoshima, Japan
Iwatsuki K, Kato M, Yamazaki T (1995) Flora of Japan. Volume I Pteridophyta and gymnospermae. KODANSHA LTD., Tokyo
Knapp R (2014) Index to ferns and fern allies of Taiwan. KBCC Press, Taiwan
Kuo L-Y, Li F-W, Chiou W-L, Wang C-N (2011) First insights into fern matK phylogeny. Mol Phylogenet Evol 59:556–566
Kuo L-Y, Tang D-Y, Huang Y-M et al (2014) Cryptic species diversity on field fern gametophytes flora in Fushan (Taiwan). In: the 6th Asian fern symposium. Bali, Indonesia
Kuo L-Y, Chang Y-H, Glowienka JMO et al (2016) A revised framework of Dryopteris subg. Nothoperanema (Dryopteridaceae) inferred from phylogenetic evidence, with descriptions of two new sections. Syst Bot 41:596–605
Osozawa S, Shinjo R, Armid A et al (2012) Palaeogeographic reconstruction of the 1.55 Ma synchronous isolation of the Ryukyu Islands, Japan, and Taiwan and inflow of the Kuroshio warm current. Int Geol Rev 54:1369–1388
Pinson JB, Schuettpelz E (2016) Unraveling the origin of the Appalachian gametophyte, Vittaria appalachiana. Am J Bot 103:668–676
Qiu Y-X, Fu C-X, Comes HP (2011) Plant molecular phylogeography in China and adjacent regions: tracing the genetic imprints of Quaternary climate and environmental change in the world’s most diverse temperate flora. Mol Phylogenet Evol 59:225–244
Raine CA, Farrar DR, Sheffield E (1991) A new Hymenophyllum species in the Appalachians represented by independent gametophyte colonies. Am Fern J 81:109–118
Rumsey FJ, Jermey AC (1998) The independent gametophytic stage of Trichomanes speciosum Willd. (Hymenophyllaceae), the Killarney Fern and its distribution in the British Isles. Watsonia 22:1–19
Rumsey FJ, Sheffeld E (1996) Inter-generational ecological niche separation and the “independent gametophyte” phenomenon. In: Camus JM, Gibby M, John RJ (eds) Pteridology in perspective. Royal Botanic Gardens, Kew, pp 563–570
Sato T, Sakai A (1981) Cold tolerance of gametophytes and sporophytes of some cool temperate ferns native to Hokkaido. Can J Bot 59:604–608
Schuettpelz E, Pryer KM (2009) Evidence for a Cenozoic radiation of ferns in an angiosperm-dominated canopy. Proc Natl Acad Sci USA 106:11200–11205
Schuettpelz E, Chen C-W, Kessler M et al (2016) A revised generic classification of vittarioid ferns (Pteridaceae) based on molecular, micromorphological, and geographic data. Taxon 65:708–722
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
Zhang X-C, Gilbert MG (2013) Haplopteris. In: Wu ZY, Raven PH, Hong DY (eds) Flora of China, vol 2–3 (pteridophytes). Science Press, Beijing, pp 252–255
Acknowledgements
The authors thank Joel Nitta and Jerald Pinson for providing comments on the manuscript; Mr. Daniel P. Chamberlin for helping English editing; Kaede Mizukoshi, Hiroko Sakuragi, Louzamira Bivaqua, Sabilah Tahir, and Shizuka Fuse for the assistance of gametophyte survey in Yakushima; Hui Wang, Pi-Fong Lu, Ralf Knapp, Tian-Chuan Hsu, Wayne Takeuchi, and Zhao-Rong He for the sample collecting.
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Li-Yaung Kuo and Cheng-Wei Chen have contributed equally to this work.
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Kuo, LY., Chen, CW., Shinohara, W. et al. Not only in the temperate zone: independent gametophytes of two vittarioid ferns (Pteridaceae, Polypodiales) in East Asian subtropics. J Plant Res 130, 255–262 (2017). https://doi.org/10.1007/s10265-016-0897-x
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DOI: https://doi.org/10.1007/s10265-016-0897-x