Abstract
Hybridization with alien species can affect the reproduction and persistence of native species. Native Oxalis corniculata and alien O. dillenii are distributed in human-made habitats in Japan, and they coexist with their putative hybrid. We examined the origin of the putative hybrid and the possibility of introgression and reproductive interference between these species by analyzing their morphological, cytological, genetic, and reproductive characteristics. The flower morphology of the putative hybrid was similar to the alien species. The chromosome complement and the amount of nuclear DNA of the putative hybrid were intermediate between the two species. Genotyping of the nuclear ITS region showed the putative hybrid was invariably heterozygous for native and alien alleles. Haplotyping of the chloroplast trnS–trnG region showed that 22 and four hybrids had their maternal origin in the alien and native species, respectively. The ovules of the putative hybrid were sterile. When pollen of the putative hybrid was applied to flowers of the parental species, the fruit set was very low, suggesting that their pollen is only marginally viable. Based on these results, we conclude that the putative hybrid is an F1 hybrid between native and alien Oxalis species. The hybrid is virtually sterile, indicating that hybridization led to a waste of gametes and may result in reproductive interference between the two parental species. The capacity for selfing and/or asexual reproduction may weaken reproductive interference between the species; alternatively, their apparent coexistence may be maintained by dispersal from different parental habitats.
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References
Allendorf FW, Leary RF, Spruell P, Wenburg JK (2001) The problems with hybrids: setting conservation guidelines. Trends Ecol Evol 16:613–622. https://doi.org/10.1016/S0169-5347(01)02290-X
Amano M (2001) Oxalidaceae. In: Iwatsuki K, Boufford ED, Ohba H (eds) Flora of Japan IIb. Angiospermae, Dicotyledoneae, Archichlamydeae (b). Kodansha, Tokyo, pp 283–286
Bleeker W, Schmitz U, Ristow M (2007) Interspecific hybridisation between alien and native plant species in Germany and its consequences for native biodiversity. Biol Conservation 137:248–253. https://doi.org/10.1016/j.biocon.2007.02.004
Brys R, van Cauwenberghe J, Jacquenmyn H (2016) The importance of autonomous selfing in preventing hybridization in three closely related plant species. J Ecol 104:601–610. https://doi.org/10.1111/1365-2745.12524
Burgess KS, Morgan M, Husband BC (2008) Interspecific seed discounting and the fertility cost of hybridization in an endangered species. New Phytol 177:276–284. https://doi.org/10.1111/j.1469-8137.2007.02244.x
Doust LL, Doust JL, Cvers PB (1981) Fertility relationships in closely related taxa of Oxalis, section Corniculatae. Canad J Bot 59:2603–2609. https://doi.org/10.1139/b81-312
Doust LL, MacKinnon A, Doust JL (1985) Biology of Canadian weeds. 71. Oxalis stricta L., O. corniculata L., O. dillenii Jacq. ssp. dillenii and O. dillenii Jacq. ssp filipes (Small) Eiten. Canad J Pl Sci 65:691–709. https://doi.org/10.4141/cjps85-090
Eiten G (1963) Taxonomy and regional variation of Oxalis section Corniculatae. I. Introduction, keys, and synopsis of the species. Amer Midl Naturalist 69:257–309. https://doi.org/10.2307/2422912
Fukuda T, Naiki A, Nagamasu H (2007) Karyotypic analysis of Skimmia japonica (Rutaceae) and related species. J Plant Res 120:113–121. https://doi.org/10.1007/s10265-006-0033-4
Gröning J, Hochkirch A (2008) Reproductive interference between animal species. Quart Rev Biol 83:257–282. https://doi.org/10.1086/590510
Hamilton MB (1999) Four primer pairs for the amplification of chloroplast intergenic regions with intraspecific variation. Molec Ecol 8:521–523. https://doi.org/10.1046/j.1365-294X.1999.00510.x
Johnston JS, Bennett MD, Rayburn AL, Galbraith DW, Price HJ (1999) Reference standards for determination of DNA content of plant nuclei. Amer J Bot 86:609–613. https://doi.org/10.2307/2656569
Kubešová M, Moravcová L, Suda J, Jarosšik V, Pysšek P (2011) Naturalized plants have smaller genomes than their non-invading relatives: a flow cytometric analysis of the Czech alien flora. Preslia 82:81–96
Lourteig A (1979) Oxalidaceae extra—Austroamericanae. II. Oxalis L. sectio Corniculatae DC. Phytologia 42:57–198
Mathew PM (1958) Cytology of Oxalidaceae. Cytologia 23:200–210
Mitsuyuki C, Hoya A, Shibaike H, Watanabe M, Yahara T (2014) Formation of a hybrid triploid agamosperm on a sexual diploid plant: evidence from progeny tests in Taraxacum platycarpum Dahlst. Pl Syst Evol 300:863–870. https://doi.org/10.1007/s00606-013-0925-4
Mooney HA, Cleland EE (2001) The evolutionary impact of invasive species. Proc Natl Acad Sci USA 98:5446–5451. https://doi.org/10.1073/pnas.091093398
Murata G (1967) A new invasive species of Oxalidaceae. Acta Phytotax Geobot 22:194 (in Japanese)
Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucl Acids Res 8:4321–4326
Nesom GL (2009) Again: taxonomy of yellow-flowered caulescent Oxalis (Oxalidaceae) in eastern North America. J Bot Res Inst of Texas 3:727–738
Nishida S, Kanaoka MM, Hashimoto K, Takakura KI, Nishida T (2014) Pollen-pistil interactions in reproductive interference: mechanism driving the exclusive distribution of alien and native species of Taraxacum. Funct Ecol 28:450–457. https://doi.org/10.1111/1365-2435.12165
Nishida S, Hashimoto K, Hashimoto MM, Takakura KI, Nishida T (2017) Variation in the strength of reproductive interference from an alien congener to a native species in Taraxacum. J Pl Res 130:125–134. https://doi.org/10.1007/s10265-016-0865-5
Ogawa K (1979) Distributions of native and introduced dandelions in the Tokyo metropolitan area, Japan. In: Miyawaki A, Okuda S (eds) Vegetation und landschaft Japans. Maruzen, Tokyo, pp 417–421
Ogawa K, Mototani I (1985) Invasion of the introduced dandelions and survival of the native ones in the Tokyo metropolitan area of Japan. Jap J Ecol 33:443–452
Ornduff R (1972) The breakdown of trimorphic incompatibility in Oxalis section Corniculatae. Evolution 26:52–65
Praça-Fontes MM, Carvalho CR, Clarindo WR, Cruz CD (2011) Revisiting the DNA C-values of the genome size-standards used in plant flow cytometry to choose the “best primary standards”. Pl Cell Rep 30:1183–1191. https://doi.org/10.1007/s00299-011-1026-x
Runquist RB, Stanton ML (2013) Asymmetric and frequency-dependent pollinator-mediated interactions may influence competitive displacement in two vernal pool plants. Ecol Lett 16:183–190. https://doi.org/10.1111/ele.12026
Sato K, Enomoto R, Kumagai D, Yamazaki T, Iwatsubo Y (2008) Chromosome numbers of three species of Oxalis (Oxalidaceae) in Japan. J Jap Bot 83:239–245
Shibaike H, Ishiguri Y, Kawano S (1995) Reproductive biology of Oxalis corniculata (Oxalidaceae): style length polymorphisms and breeding systems of Japanese populations. Pl Spec Biol 10:83–93. https://doi.org/10.1111/j.1442-1984.1995.tb00126.x
Sorensson CT, Brewbaker JL (1994) Interspecific compatibility among 15 Leucaena species (Leguminosae: Mimosoidea) via artificial hybridizations. Amer J Bot 81:240–247. https://doi.org/10.1002/j.1537-2197.1994.tb15435.x
Takakura KI (2013) Two-way but asymmetrical reproductive interference between an invasive Veronica species and a native congener. Amer J Pl Sci 4:535–642. https://doi.org/10.4236/ajps.2013.43069
Takakura KI, Nishida T, Matsumoto T, Nishida S (2009) Alien dandelion reduces the seed-set of a native congener through frequency-dependent and one-sided effects. Biol Invas 11:973–981. https://doi.org/10.1007/s10530-008-9309-z
Takakura KI, Matsumoto T, Nishida T, Nishida S (2011) Effective range of reproductive interference exerted by an alien dandelion, Taraxacum officinale, on a native congener. J Pl Res 124:269–276. https://doi.org/10.1007/s10265-010-0368-8
Tiffin P, Olson MS, Moyle LC (2001) Asymmetrical crossing barriers in angiosperms. Proc Roy Soc B 268:861–867. https://doi.org/10.1098/rspb.2000.1578
Vaio M, Gardner A, Emshwiller E, Guerra M (2013) Molecular phylogeny and chromosome evolution among the creeping herbaceous Oxalis species of sections and Ripariae (Oxalidaceae). Molec Phylogen Evol 68:199–211. https://doi.org/10.1016/j.ympev.2013.03.019
Vallejo-Marín M, Hiscock JS (2016) Hybridization and hybrid speciation under global change. New Phytol 211:1170–1187. https://doi.org/10.1111/nph.14004
Vilà M, Weber E, Antonio CM (2000) Conservation implications of invasion by plant hybridization. Biol Invas 2:207–217
White TJ, Bruns TD, Lee SB, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and application, pp 315–322
Xu BS, Weng RF, Zhang MZ (1992) Chromosome numbers of Shanghai plants I. Invest Stud Nat 12:48–65
Yasumoto AA, Yahara T (2006) Post-pollination reproductive isolation between diurnally and nocturnally flowering daylilies, Hemerocallis fulva and Hemerocallis citrina. J Pl Res 119:617–623. https://doi.org/10.1007/s10265-006-0028-1
Acknowledgments
We thank T. Sugawara, A. Iwamoto, and T. Fukuda for their advice with the cytological experiments, M. Kimura and other members of the laboratory of TGU for their help in fieldwork, and Y. Takami for his valuable comments based on critical readings of manuscript. We also thank the National BioResource Project Lotus/Glycine for providing the seeds of L. japonicus Gifu B-129. This work was supported by the Tokyu Foundation for a Better Environment, Nissei Foundation, and the Grant-in-Aid for Scientific Research from Japan Society for the Promotion of Science (15K12255).
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Handling editor: Jorg Fuchs.
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Online Resource 1. Localities and presence of Oxalis species used in this study.
Online Resource 2. Measured parts in flowers for principal component analysis.
Online Resource 3. Eigenvectors of the first two principal components based on the floral morphology of Oxalis species.
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Fukatsu, M., Horie, S., Maki, M. et al. Hybridization, coexistence, and possible reproductive interference between native Oxalis corniculata and alien O. dillenii in Japan. Plant Syst Evol 305, 127–137 (2019). https://doi.org/10.1007/s00606-018-1557-5
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DOI: https://doi.org/10.1007/s00606-018-1557-5