Genetic structure and demographic history of Cycas chenii (Cycadaceae), an endangered species with extremely small populations

doi:10.1016/j.pld.2016.11.003

Abstract

Abstract: Geological activities and climate oscillations during the Quaternary period profoundly impacted the distribution of species in Southwest China. Some plant species may be harbored in refugia, such as the dry-hot valleys of Southwest China. Cycas chenii X. Gong & W. Zhou, a critically endangered cycad species, which grows under the canopy in subtropical evergreen broad-leaved forests along the upstream drainage area of the Red River, is endemic to this refugium. In this study, 60 individuals of C. chenii collected from six populations were analyzed by sequencing two chloroplast intergenic spacers (cpDNA: psbA-trnH and trnL-trnF) and two nuclear genes (PHYP and RBP-1). Results showed high genetic diversity at the species level, but low within-population genetic diversity and high interpopulation genetic differentiation. A Bayesian phylogenetic tree based on cpDNA showed that five chloroplast haplotypes were clustered into two clades, which corresponds to the division of the western and eastern bank of the Red River. These data indicate a possible role for the Red River as a geographic barrier to gene flow in C. chenii. Based on our findings, we propose appropriate in situ and ex situ conservation strategies for C. chenii.

Key words: Cycas chenii, Genetic variation, Phylogeography, Conservation

Rui Yang, Xiuyan Feng, Xun Gong. Genetic structure and demographic history of Cycas chenii (Cycadaceae), an endangered species with extremely small populations[J]. Plant Diversity, 2017, 39(01): 44-51.

References

Arenas, M., Ray, N., Currat, M., et al, 2012. Consequences of range contractions and range shifts on molecular diversity. Mol. Biol. Evol. 29. 207-218.
Burban, C., Petit, R.J., Carcreff, E., et al, 1999. Rangewide variation of the maritime pine bast scale Matsucoccus feytaudi Duc. (Homoptera: Matsucoccidae) in relation to the genetic structure of its host. Mol. Ecol. 8. 1593-1602.
Calonje, M., Stevenson, D.W., Stanberg, L., 2016. The World List of Cycads, online edition. Available from: http://www.cycadlist.org.
Chiang, Y., Hung, K., Moore, S., et al, 2009. Paraphyly of organelle DNAs in Cycas Sect. Asiorientales due to ancient ancestral polymorphisms. BMC Evol. Biol. 9. 1-19.
Doyle, J., 1991. DNA Protocols for Plants–CTAB Total DNA Isolation. Molecular Techniques in Taxonomy. Springer, Berlin.
Drummond, A.J., Rambaut, A., 2004. Tracer-MCMC Trace Analysis Tool. University of Oxford, UK.
Drummond, A.J., Rambaut, A., 2007. BEAST: bayesian evolutionary analysis by sampling trees. BMC Evol. Biol. 7. 1-8.
Excoffier, L., Smouse, P.E., Quattro, J.M., 1992. Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131. 479-491.
Excoffier, L., Laval, G., Schneider, S., 2005. Arlequin version. 3.0: an integrated software package for population genetics data analysis. Evol. Bioinform 1. 47-50.
Feng, X.Y., Wang, Y.H., Gong, X., 2014. Genetic diversity, genetic structure and demographic history of Cycas simplicipinna (Cycadaceae) assessed by DNA sequences and SSR markers. BMC Plant Biol. 14. 1-16.
Forster, M., Forster, P., Watson, J., 2007. NETWORK (version 4.2. 0.1): A Software for Population Genetics Data Analysis. Fluxus Technology Ltd, Clare.
Fu, Y.X., 1997. Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147. 915-925.
Gong, Y.Q., Zhan, Q.Q., Nguyen, K.S., et al, 2015. The Historical Demography and Genetic Variation of the Endangered Cycas multipinnata (Cycadaceae) in the Red River Region, Examined by Chloroplast DNA Sequences and Microsatellite Markers. PLoS One 10. e0117719.
Graur, D., Li, W.H., Dynamics of genes in populations. Fundam. Mol. Evol. 58.
Guan, Z.T., Zhou, L., 1996. Cycads of China. Sichuan Science and Technology Press, Chengdu.
Hall, T.A., 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 41. 95-98.
Hamrick, J.L., Godt, M.J.W., 1990. Allozyme Diversity in Plant Species. Plant Population Genetics, Breeding and Genetic Resources. Sinnaur Associates Inc, Sunderland.
Hill, K., 2008. The genus Cycas (Cycadaceae) in China. Telopea 12. 71-118.
Hoffmann, M., Hilton-Taylor, C., Angulo, A., et al, 2010. The impact of conservation on the status of the world's vertebrates. Science 330. 1503-1509.
Huang, S., Hsieh, H.-T., Fang, K., et al, 2004. Patterns of genetic variation and demography of Cycas taitungensis in Taiwan. Botanical Rev. 70. 86-92.
Jian, S.G., Zhong, Y., Liu, N., et al, 2006. Genetic variation in the endangered endemic species Cycas fairylakea (Cycadaceae) in China and implications for conservation. Biodivers. Conserv. 15. 1681-1694.
Li, Y.G., He, D.M., Ye, C.Q., 2008. Spatial and temporal variation of runoff of Red River Basin in Yunnan. J. Geogr. Sci. 18. 308-318.
Liu, J., Moeller, M., Provan, J., et al, 2013. Geological and ecological factors drive cryptic speciation of yews in a biodiversity hotspot. New Phytol. 199. 1093-1108.
Liu, J., Zhou, W., Gong, X., 2015. Species delimitation, genetic diversity and population historical dynamics of Cycas diannanensis (Cycadaceae) occurring sympatrically in the Red River region of China. Front. Plant Sci. 6. 696.
Mousadik, A., Petit, R.J., 1996. Chloroplast DNA phylogeography of the argan tree of Morocco. Mol. Ecol. 5. 547-555.
Peakall, R.O.D., Smouse, P.E., 2006. GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol. Ecol. Notes 6. 288-295.
Petit, R.J., Duminil, J., Fineschi, S., et al, 2005. Invited review: comparative organization of chloroplast, mitochondrial and nuclear diversity in plant populations. Mol. Ecol. 14. 689-701.
Ronquist, F., Teslenko, M., Mark, v.d.P., 2012. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61. 539-542.
Royden, L.H., Burchfiel, B.C., van der Hilst, R.D., 2008. The geological evolution of the Tibetan Plateau. Science 321. 1054-1058.
Rozas, J., Sánchez-DelBarrio, J.C., Messeguer, X., et al, 2003. DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19. 2496-2497.
Schneider, S., Roessli, D., Excoffier, L., 2000. Arlequin: a software for population genetics data analysis. User Man. Ver. 2. 2496-2497.
Shaw, J., Lickey, E.B., Beck, J.T., et al, 2005. The tortoise and the hare Ⅱ: relative utility of 21 noncoding chloroplast DNA sequences for phylogenetic analysis. Am. J. Bot. 92. 142-166.
Swindell, S.R., Plasterer, T.N., 1997. SEQMAN. Sequence Data Analysis Guidebook. 75-89.
Swofford, D.L., 2002. PAUP*: Phylogenetic Analysis Using Parsimony (and other methods), Version 4.0b10. Massachusetts. Sinauer Associates, Inc, Sunderland.
Taberlet, P., Gielly, L., Pautou, G., et al, 1991. Universal primers for amplification of three non-coding regions of chloroplast DNA. Plant Mol. Biol. 17. 1105-1109.
Tajima, F., 1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123. 585-595.
Tamura, K., Stecher, G., Peterson, D., et al, 2013. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 30. 2725-2729.
Thompson, J.D., Gibson, T.J., Plewniak, F., et al, 1997. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25. 4876-4882.
Walters, T.W., Decker-Walters, D.S., 1991. Patterns of allozyme diversity in the West Indies cycad Zamia pumila (Zamiaceae). Am. J. Bot. 78. 436-445.
Wang, F.X., Liang, H.B., Chen, T.Q., et al, 1996. Cycads in China. Guangdong Science and Technology Press, Guangzhou.
Xiao, L.Q., Ge, X.J., Gong, X., et al, 2004. ISSR variation in the endemic and endangered plant Cycas guizhouensis (Cycadaceae). Ann. Bot. 94. 133-138.
Yang, S.L., Meerow, A.W., 1996. The Cycas pectinata (Cycadaceae) complex: genetic structure and gene flow. Int. J. Plant Sci. 157. 468-483.
Zhan, Q.Q., Wang, J.F., Gong, X., et al, 2011. Patterns of chloroplast DNA variation in Cycas debaoensis (Cycadaceae): conservation implications. Conserv. Genet. 12. 959-970.
Zheng, Y., Liu, J., Gong, X., 2016. Tectonic and climatic impacts on the biota within the Red River Fault, evidence from phylogeography of Cycas dolichophylla (Cycadaceae). Sci. Rep. 6. 33540.
Zhong, Z.R., Li, N., Qian, D., et al, 2011. Maternal inheritance of plastids and mitochondria in Cycas L. (Cycadaceae). Mol. Genet. Genomics 286. 411-416.
Zhou, S.Z., Wang, X.L., Wang, J., et al, 2006. A preliminary study on timing of the oldest Pleistocene glaciation in Qinghai–Tibetan Plateau. Quat. Int. 154. 44-51.
Zhou, W., Guan, M.M., Gong, X., 2015. Cycas chenii (Cycadaceae), a new species from China, and its phylogenetic position. J. Syst. Evol. 53. 489-498.

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