Bidirectional natural hybridization between sympatric Ligularia vellerea and L. subspicata

doi:10.1016/j.pld.2017.07.001

Abstract

Abstract: Natural hybridization has been regarded as a crucial pathway of speciation and provides the raw materials for the evolution of biodiversity. The interspecific natural hybridization of the genus Ligularia Cass. is universal and has been considered to be an important factor driving the high diversity of Ligularia species in the Hengduan Mountains, China. Although the natural hybridization between L. vellerea and L. subspicata was reported previously, the direction of hybridization was uncertain due to the limitation of sampling. Thus, in this study, we sampled more individuals and increased two fragments of chloroplast DNA on the basis of the previous study to further verify the natural hybridization between L. vellerea and L. subspicata and confirm the direction of hybridization. Based on DNA sequences (atpBrbcL, trnL-rpl32, trnQ-5'rps16, and nuclear ribosomal internal transcribed spacer region) data, we concluded that putative hybrids were primary products of hybridization between L. vellerea and L. subspicata and the hybridization was bidirectional. Moreover, sympatric L. tongolensis was not apparently involved in the hybridization. Surprisingly, some pure L. subspicata individuals showed the disaccordance between morphology and DNA data, which might indicate that introgression occurs between L. vellerea and L. subspicata.

Key words: Ligularia, Natural hybridization, Introgression, cpD

Huai Ning, Jiaojun Yu, Xun Gong. Bidirectional natural hybridization between sympatric Ligularia vellerea and L. subspicata[J]. Plant Diversity, 2017, 39(04): 214-220.

References

Aanderson, E., 1949. Introgressive Hybridization. Wiley, New York.
Arnold, M.L., 1992. Natural hybridization as an evolutionary process. Annu. Rev.Ecol. Syst. 237-261.
Arnold, M.L., Hodges, S.A., 1995. Are natural hybrids fit or unfit relative to their parents? Trends Ecol. Evol. 10, 67-71.
Arnold, M.L., 1997. Natural Hybridization and Evolution. Oxford University Press, New York.
Arnold, M.L., 2006. Evolution through Genetic Exchange. Oxford University Press, New York.
Abbott, R.J., Ritchie, M.G., Hollingsworth, P.M., 2008. Introduction. Speciation in plants and animals:pattern and process. Philos. Trans. R. Soc. B Biol. Sci. 363, 2965-2969.
Abbott, R.J., Hegarty, M.J., Hiscock, S.J., et al., 2010. Homoploid hybrid speciation in action. Taxon 59, 1375-1386.
Burland, T.G., 1999. DNASTAR's Lasergene sequence analysis software. Methods Mol.Biol. 132, 71-91.
Buerkle, C.A., Morris, R.J., Asmussen, M.A., et al., 2000. The likelihood of homoploid hybrid speciation. Heredity 84, 441-451.
Burke, J.M., Arnold, M.L., 2001. Genetics and the fitness of hybrids. Annu. Rev. Genet. 35, 31-52.
Chiang, T.Y., Schaal, B.A., Peng, C.I., 1998. Universal primers for amplification and sequencing a non-coding spacer between the atpB and rbcL genes of chloroplast DNA. Botanical Bull. Acad. Sinica 39, 245-250.
Comes, H.P., Abbott, R.J., 2001. Molecular phylogeography, reticulation, and lineage sorting in Mediterranean Senecio sect. Senecio (Asteraceae). Evolution 55, 1943-1962.
Coyne, J.A., Orr, H.A., 2004. Speciation. Sinauer Associates Sunderland, M.A.
Cao, Y., Ma, R.J., Wang, G.X., 2008. The breeding system of three species of genus Ligularia in the east of Qinghai-Tibet Plateau. Guihaia 28, 302-306.
Chase, M.W., Paun, O., Fay, M.F., 2010. Hybridization and speciation in angiosperms:a role for pollinator shifts? BMC Biol. 8, 45.
Doyle, J.J., Doyle, J.L., 1987. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem. Bull. 19, 11-15.
Davis, J.I., Simmons, M.P., Stevenson, D.W., et al., 1998. Data decisiveness, data quality, and incongruence in phylogenetic analysis:an example from the monocotyledons using mitochondrial atpA sequences. Syst. Biol. 47, 282-310.
Desplanque, B.F., Viard, F., Bernard, J., et al., 2000. The linkage disequilibrium between chloroplast DNA and mitochondrial DNA haplotypes in Beta vulgaris ssp.maritima (L.):the usefulness of both genomes for population genetic studies.Mol. Ecol. 9, 141-154.
Heiser, C.B., 1947. Hybridization between the sunflower species Helianthus annuus and H. petiolaris. Evolution 1, 249-262.
Harrison, R.G., 1986. Pattern and process in a narrow hybrid zone. Heredity 56, 337-349.
Harrison, R.G., 1990. Hybrid zones:windows on evolutionary process. Oxf. Surv.Evol. Biol. 7, 69-128.
Hall, T.A., 1999. Bioedit:a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. 41, 95-98.
He, W.Y., Pan, Y.Z., 2015. Study on DNA barcoding of genus Ligularia Cass. (Asteraceae). Plant Divers. Resour. 37, 693-703.
Koch, M.A., Dobes, C., Mitchell-Olds, T., 2003. Multiple hybrid formation in natural populations:concerted evolution of the internal transcribed spacer of nuclear ribosomal DNA (ITS) in North American Arabis divaricarpa (Brassicaceae). Mol.Biol. Evol. 20, 338-350.
Liu, S.W., 1989. Compositae-senecioneae. In:Ling, Y., Liu, S.W. (Eds.), Flora Reipublicae Popularis Sinicae. Science Press, Beijing, pp. 4-115.
Liu, Z.J., 2002. Life History Strategies of Ligularia virgaurea, an Advantage Toxic Forb in Degradative Rangland of Alpine Meadow (Doctor Degree). Lanzhou University China, Lanzhou.
Liao, R.L., Ma, Y.P., Gong, W.C., et al., 2015. Natural hybridization and asymmetric introgression at the distribution margin of two Buddleja species with a large overlap. BMC Plant Biol. 15 (1), 146.
Martin, N.H., Bouck, A.C., Arnold, M.L., 2006. Detecting adaptive trait introgression between Iris fulva and I. brevicaulis in highly selective field conditions. Genetics 172, 2481-2489.
Mallet, J., 2007. Hybrid speciation. Nature 446, 279-283.
Nolte, A.W., Tautz, D., 2010. Understanding the onset of hybrid speciation. Trends Genet. 26, 54-58.
Nishiwaki, A., Mizuguti, A., Kuwabara, S., et al., 2011. Discovery of natural Miscanthus (Poaceae) triploid plants in sympatric populations of Miscanthus sacchariflorus and Miscanthus sinensis in southern Japan. Am. J. Bot. 98, 154-159.
Pan, Y.Z., Shi, S.H., Gong, X., et al., 2008. A natural hybrid between Ligularia paradoxa and L. duciformis (Asteraceae, Senecioneae) from Yunnan, China. Ann. Missouri Botanical Gard. 95, 487-494.
Rieseberg, L.H., Brunsfeld, S.J., 1992. Molecular Evidence and Plant Introgression.Molecular Systematics of plants, Springer US, pp. 151-176.
Rieseberg, L.H., Ellstrand, N.C., 1993. What can molecular and morphological markers tell us about plant hybridization? Crit. Rev. Plant Sci. 12, 213-241.
Rieseberg, L.H., Wendel, J.F., 1993. Introgression and its consequences in plants. In:Harrison, R.G. (Ed.), Hybrid Zones and the Evolutionary Process. Oxford University Press, New York, pp. 70-109.
Rieseberg, L.H., 1997. Hybrid origins of plant species. Annu. Rev. Ecol. Syst. 28, 359-389.
Rieseberg, L.H., Baird, S.J.E., Gardner, K.A., 2000. Hybridization, introgression, and linkage evolution. Plant Mol. Biol. 42, 205-224.
Rieseberg, L.H., Raymond, O., Rosenthal, D.M., et al., 2003. Major ecological transitions in wild sunflowers facilitated by hybridization. Science 301, 1211-1216.
Rozas, J., S anchez-DelBarrio, J.C., Messeguer, X., et al., 2003. DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19, 2496-2497.
Rieseberg, L.H., Willis, J.H., 2007. Plant speciation. Science 317, 910-914.
Soltis, D.E., Soltis, P.S., 1999. Polyploidy:recurrent formation and genome evolution.Trends Ecol. Evol. 14, 348-352.
Swofford, D.L., 2002. PAUP:Phylogenetic Analysis Using Parsimony version 4.0 b10.
Sinauer Associates, Sunderland.Shaw, J., Lickey, E.B., Schilling, E.E., et al., 2007. Comparison of whole chloroplast genome sequences to choose noncoding regions for phylogenetic studies in angiosperms:the tortoise and the hare Ⅲ. Am. J. Bot. 94, 275.
Soltis, P.S., Soltis, D.E., 2009. The role of hybridization in plant speciation. Annu. Rev.Plant Biol. 60, 561-588.
Saito, Y., Hattori, M., Iwamoto, Y., et al., 2011. Overlapping chemical and genetic diversity in Ligularia lamarum and Ligularia subspicata. Isolation of ten new eremophilanes and a new seco-bakkane compound. Tetrahedron 67, 2220-2231.
Tsukaya, H., Fukuda, T., Yokoyama, J., 2003. Hybridization and introgression between Callicarpa japonica and C. mollis (Verbenaceae) in central Japan, as inferred from nuclear and chloroplast DNA sequences. Mol. Ecol. 12, 3003-3011.
Tate, J.A., Soltis, D.E., Soltis, P.S., 2005. Polyploidy in plants. In:Gregory, T.R. (Ed.), The Evolution of the Genome. Elsevier Science and Technology, Academic Press, San Diego, CA, pp. 371-426.
Tamura, K., Dudley, J., Nei, M., et al., 2007. MEGA:molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24, 1596-1599.
Tripathi, A.M., Tyagi, A., Kumar, A., et al., 2013. The internal transcribed spacer (ITS)region and trnH-psbA are suitable candidate loci for DNA barcoding of tropical tree species of India. PLoS One 8, e57934.
Wolfe, K.H., Li, W.H., Sharp, P.M., 1987. Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs. Proc. Natl. Acad. Sci.U. S. A. 84, 9054-9058.
White, T.J., Bruns, T., Lee, S., et al., 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR Protoc. A Guide Methods Appl. 18, 315-322.
Yatabe, Y., Tsutsumi, C., et al., 2009. Genetic population structure of Osmunda japonica, rheophilous Osmunda lancea and their hybrids. J. Plant Res. 122, 585-595.
Yu, J.J., Kuroda, C., Gong, X., 2011. Natural hybridization and introgression in sympatric Ligularia species (Asteraceae, Senecioneae). J. Syst. Evol. 49, 438-448.
Yan, L.J., Gao, L.M., Li, D.Z., 2013. Molecular evidence for natural hybridization between Rhododendron spiciferum and R. spinuliferum (Ericaceae). J. Syst. Evol. 51, 426-434.
Yu, J.J., Pan, L., Pan, Y.Z., Gong, X., 2014a. Natural hybrids between Ligularia vellerea and L. subspicata (Asteraceae:Senecioneae). Plant Biodivers. Resour. 36, 219-226.
Yu, J.J., Kuroda, C., Gong, X., 2014b. Natural hybridization and introgression between Ligularia cymbulifera and L. tongolensis (Asteraceae, Senecioneae) in four different locations. PLoS One 9 (12), e115167.
Zhang, Q., Liu, Y., Sodmergen, 2003. Examination of the cytoplasmic DNA in male reproductive cells to determine the potential for cytoplasmic inheritance in 295 angiosperm species. Plant Cell Physiol. 44, 941-951.
Zhang, W.Y., Kuo, L.Y., Li, F.W., et al., 2014. The hybrid origin of Adiantum meishanianum (Pteridaceae):a rare and endemic species in Taiwan. Syst. Bot. 39, 1034-1041.

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