Note

Development of transferable expressed sequence tag-simple sequence repeat (EST-SSR) markers for delimitating two recently diverged gingers endemic to Taiwan

Yi-Ting Tseng, Min-Xin Luo, Bing-Hong Huang, Pei-Chun Liao

Published on: 14 May 2019

Page: 209 - 216

DOI: 10.6165/tai.2019.64.209

Abstract

Species delimitation may be difficult for recently divergent species, particularly those with few distinguishable morphological characteristics. Zingiber kawagoii and Z. shuanglongensis are two recently divergent species endemic to Taiwan whose extremely similar vegetative characteristics hinder their distinction during non-flowering seasons. Given their recent divergence, the speciation process and introgressions between these two gingers warrant exploration. However, such studies are hampered by the absence of appropriate molecular markers. To solve this dilemma, we developed 20 transferable expressed sequence tag-simple sequence repeat loci (EST-SSR). Seven highly differentiated loci were further identified for rapid species delimitation. A preliminary test using discriminant analysis of principal components (DAPC) validated the effective discrimination of these EST-SSR loci, while Bayesian clustering analysis (BCA) revealed obvious introgression events between species, particularly on positive-outlier loci. These results imply adaptive introgressions between these species. However, more sampling and further experiments are necessary to validate this inference and resolve questions regarding the introgression and speciation mechanisms. The development of genetic markers in this study provides appropriate experimental conditions and a basis for further research.

Keyword: Endemic, FST outliers, Island, Microsatellite DNA, Multilocus marker, Species delimitation, Zingiber

Literature Cited

Alcala, N., D. Streit, J. Goudet and S. Vuilleumier 2013. Peak and persistent excess of genetic diversity following an abrupt migration increase. Genetics 193(3): 953-971.
DOI: 10.1534/genetics.112.147785View Article Google Scholar

Antao, T., A. Lopes, R.J. Lopes, A. Beja-Pereira and G. Luikart 2008. LOSITAN: A workbench to detect molecular adaptation based on a Fst-outlier method. BMC Bioinformatics 9(1): 323.
DOI: 10.1186/1471-2105-9-323View Article Google Scholar

Barrett, R.D. and H.E. Hoekstra 2011. Molecular spandrels: tests of adaptation at the genetic level. Nat. Rev. Genet. 12(11): 767-780.
DOI: 10.1038/nrg3015View Article Google Scholar

Beaumont, M.A. and D.J. Balding 2004. Identifying adaptive genetic divergence among populations from genome scans. Mol. Ecol. 13(4): 969-980.
DOI: 10.1111/j.1365-294X.2004.02125.xView Article Google Scholar

Beaumont, M.A. and R.A. Nichols 1996. Evaluating loci for use in the genetic analysis of population structure. Proc. R. Soc. London Ser. B: Biol. Sc. 263(1377): 1619-1626.
DOI: 10.1098/rspb.1996.0237View Article Google Scholar

Bell, G. 2013. Evolutionary rescue and the limits of adaptation. Philos. T. R. Soc. B 368(1610): 20120080.
DOI: 10.1098/rstb.2012.0080View Article Google Scholar

Bierne, N., J. Welch, E. Loire, F. Bonhomme and P. David 2011. The coupling hypothesis: why genome scans may fail to map local adaptation genes. Mol. Ecol. 20(10): 2044-2072.
DOI: 10.1111/j.1365-294X.2011.05080.xView Article Google Scholar

Blankers, T., S.T. Vilaca, I. Waurick, D.A. Gray, R.M. Hennig, C.J. Mazzoni, F. Mayer and E.L. Berdan 2018. Demography and selection shape transcriptomic divergence in field crickets. Evolution 72(3): 553-567.
DOI: 10.1111/evo.13435View Article Google Scholar

Comeault, A. A. 2018. The genomic and ecological context of hybridization affects the probability that symmetrical incompatibilities drive hybrid speciation. Ecol. Evol. 8(5): 2926-2937.
DOI: 10.1002/ece3.3872View Article Google Scholar

Earl, D.A. and B.M. Vonholdt 2012. STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv. Genet. Resour. 4(2): 359-361.
DOI: 10.1007/s12686-011-9548-7View Article Google Scholar

Edelaar, P. and D.I. Bolnick 2012. Non-random gene flow: an underappreciated force in evolution and ecology. Trends Ecol. Evol. 27(12): 659-665.
DOI: 10.1016/j.tree.2012.07.009View Article Google Scholar

Evanno, G., S. Regnaut and J. Goudet 2005. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol. Ecol. 14(8): 2611-2620.
DOI: 10.1111/j.1365-294X.2005.02553.xView Article Google Scholar

Excoffier, L. and H.E.L. Lischer 2010. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol. Ecol. Resour. 10(3): 564-567.
DOI: 10.1111/j.1755-0998.2010.02847.xView Article Google Scholar

Falush, D., M. Stephens and J.K. Pritchard 2003. Inference of population structure using multilocus genotype data: Linked loci and correlated allele frequencies. Genetics 164(4): 1567-1587.

Garza, J.C. and E.G. Williamson 2001. Detection of reduction in population size using data from microsatellite loci. Mol. Ecol. 10(2): 305-318.
DOI: 10.1046/j.1365-294x.2001.01190.xView Article Google Scholar

Huang, B.-H., Y.-C. Lin, C.-W. Huang, H.-P. Lu, M.-X. Luo and P.-C. Liao 2018. Differential genetic responses to the stress revealed the mutation-order adaptive divergence between two sympatric ginger species. BMC Genomics 19(1): 692.
DOI: 10.1186/s12864-018-5081-3View Article Google Scholar

Hubisz, M. J., D. Falush, M. Stephens and J.K. Pritchard 2009. Inferring weak population structure with the assistance of sample group information. Mol. Ecol. Resour. 9(5): 1322-1332.
DOI: 10.1111/j.1755-0998.2009.02591.xView Article Google Scholar

Jombart, T. 2008. adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24(11): 1403-1405.
DOI: 10.1093/bioinformatics/btn129View Article Google Scholar

Jombart, T., S. Devillard and F. Balloux 2010. Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genet. 11(1): 94.
DOI: 10.1186/1471-2156-11-94View Article Google Scholar

Khodwekar, S. and O. Gailing 2017. Evidence for environment-dependent introgression of adaptive genes between two red oak species with different drought adaptations. Am. J. Bot. 104(7): 1088-1098.
DOI: 10.3732/ajb.1700060View Article Google Scholar

Kofler, R., C. Schlotterer and T. Lelley 2007. SciRoKo: a new tool for whole genome microsatellite search and investigation. Bioinformatics 23(13): 1683-1685.
DOI: 10.1093/bioinformatics/btm157View Article Google Scholar

Lin, Y.-C. 2017. Taxonomic Study of Zingiber Mill. (Zingiberaceae) in Taiwan. Department of Forestry. Master Degree: 136, National Chung Hsing University. Taichung, Taiwan.

Lotterhos, K.E. and M.C. Whitlock 2014. Evaluation of demographic history and neutral parameterization on the performance of FST outlier tests. Mol. Ecol. 23(9): 2178-2192.
DOI: 10.1111/mec.12725View Article Google Scholar

Manel, S., O.E. Gaggiotti and R.S. Waples 2005. Assignment methods: matching biological questions techniques with appropriate. Trends Ecol. Evol. 20(3): 136-142.
DOI: 10.1016/j.tree.2004.12.004View Article Google Scholar

Martin, N.H., A.C. Bouck and M.L. Arnold 2005. Loci affecting long-term hybrid survivorship in Louisiana irises: Implications for reproductive isolation and introgression. Evolution 59(10): 2116-2124.
DOI: 10.1554/05-139.1View Article Google Scholar

Martin, N.H., A.C. Bouck and M.L. Arnold 2006. Detecting adaptive trait introgression between Iris fulva and I. brevicaulis in highly selective field conditions. Genetics 172(4): 2481-2489.
DOI: 10.1534/genetics.105.053538View Article Google Scholar

Ohta, T. and M. Kimura 1973. A model of mutation appropriate to estimate the number of electrophoretically detectable alleles in a finite population. Genet. Res. 22(2): 201-204.
DOI: 10.1017/S0016672300012994View Article Google Scholar

Osozawa, S., R. Shinjo, A. Armid, Y. Watanabe, T. Horiguchi and J. Wakabayashi 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(12): 1369-1388.
DOI: 10.1080/00206814.2011.639954View Article Google Scholar

R Core Team 2015. R: A language and environment for statistical computing, R Foundation for Statistical Computing. Vienna, Austria.

Ravinet, M., R. Faria, R.K. Butlin, J. Galindo, N. Bierne, M. Rafajlovic, M.A.F. Noor, B. Mehlig and A.M. Westram 2017. Interpreting the genomic landscape of speciation: a road map for finding barriers to gene flow. J. Evol. Biol. 30(8): 1450-1477.
DOI: 10.1111/jeb.13047View Article Google Scholar

Schuelke, M. 2000. An economic method for the fluorescent labeling of PCR fragments. Nat. Biotech. 18(2): 233-234.
DOI: 10.1038/72708View Article Google Scholar

Sibuet, J.-C. and S.-K. Hsu 1997. Geodynamics of the Taiwan arc-arc collision. Tectonophysics 274(1-3): 221-251.
DOI: 10.1016/S0040-1951(96)00305-8View Article Google Scholar

Stork, N. E. 2010. Re-assessing current extinction rates. Biodivers. Conserv. 19(2): 357-371.
DOI: 10.1007/s10531-009-9761-9View Article Google Scholar

Taylor, S. A. and E. L. Larson 2019. Insights from genomes into the evolutionary importance and prevalence of hybridization in nature. Nat. Ecol. Evol. 3(2): 170-177.
DOI: 10.1038/s41559-018-0777-yView Article Google Scholar

Yeh, C.-L., S.-W. Chung, Y.-W. Kuo, T.-C. Hsu, C.-S. Leou, S.-J. Hong and C.-R. Yeh 2012. A new species of Zingiber (Zingiberaceae) from Taiwan, China, based on morphological and molecular data. J. Syst. Evol. 50(2): 163-169.
DOI: 10.1111/j.1759-6831.2011.00179.xView Article Google Scholar

Yuan, X.-Y., Y.-W. Sun, X.-R. Bai, M. Dang, X.-J. Feng, S. Zulfiqar and P. Zhao 2018. Population structure, genetic diversity, and gene introgression of two closely related walnuts (Juglans regia and J. sigillata) in Southwestern China revealed by EST-SSR markers. Forests 9(10): 646.
DOI: 10.3390/f9100646View Article Google Scholar

Zhang, D., T. Xia, M. Yan, X. Dai, J. Xu, S. Li and T. Yin 2014. Genetic introgression and species boundary of two geographically overlapping pine species revealed by molecular markers. PLOS ONE 9(6): e101106.
DOI: 10.1371/journal.pone.0101106View Article Google Scholar

Zhang, L. Y., M. Bernard, P. Leroy, C. Feuillet and P. Sourdille 2005. High transferability of bread wheat EST-derived SSRs to other cereals. Theor. Appl. Genet. 111(4): 677-687.
DOI: 10.1007/s00122-005-2041-5View Article Google Scholar