Research Paper
Incomplete lineage sorting and secondary admixture results in the paraphyly of Lecanorchis cerina, L. suginoana, and L. thalassica (Orchidaceae) in Taiwan
Shih-Ying Hwang, Yi-Shao Li, Tsan-Piao Lin
Published on: 02 July 2022
Page: 366 - 376
DOI: 10.6165/tai.2022.67.366
Abstract
Inferring the evolutionary history of a group of closely related species can be challenging. Genetic diversity, structure, and multilocus phylogeny were studied to shed light on the evolutionary processes that shapes diversity in three closely related Lecanorchis species (L. cerina, L. suginoana, and L. thalassica). In this study, we surveyed nucleotide and genetic variation, respectively, using nuclear internal transcribed spacer 1 (nrITS1) and amplified fragment length polymorphism (AFLP) in individuals of Lecanorchis species. Both nrITS1 parsimonious and AFLP neighbor-joining trees showed paraphyly indicated that lineage sorting for these species may be incomplete. ITS1 haplotype sharing was found within L. cerina, within L. suginoana, and between L. suginoana and L. thalassica. Higher AFLP diversity was observed in L. cerina than that in L. suginoana and in L. thalassica, indicating larger population size in L. cerina. Two contrasting patterns of AFLP genetic differentiation between geographic neighbors relative to geographic distant populations were observed. Two major AFLP genetic components were found in individuals of Lecanorchis species examined. Individuals of L. cerina and of L. thalassica were classified into either component with high probabilities. Most individuals of L. suginoana were classified into one of these components, but two individuals showed apparent admixture of these components. The evidence of paraphyly, haplotype sharing, higher L. cerina diversity, sharing and admixture of genetic components, and the contrasting patterns of genetic differentiation suggest that both incomplete lineage sorting and secondary gene flow could have occurred in these closely related species, though at different temporal scale.
Keyword: AFLP, incomplete lineage sorting, Lecanorchis, nrITS1, secondary gene flow, Vanilleae, Vanilloideae
Literature Cited
?lvarez, I., J.F. Wendel. 2003. Ribosomal ITS sequences and plant phylogenetic inference. Mol. Phylogenet. Evol. 29(3): 417–434.
DOI: 10.1016/S1055-7903(03)00208-2View Article
Google Scholar
Bates, D., M. Maechler, B. Bolker and S. Walker. 2015. Fitting linear mixed effects models using lme4. J. Stat. Soft. 67(1): 1–48.
DOI: 10.18637/jss.v067.i01View Article
Google Scholar
Bodenhofer, U., E. Bonatesta, C. Horej?-Kainrath and S. Hochreiter. 2015. msa: an R package for multiple sequence alignment. Bioinformatics 31(24): 3997–3999.
DOI: 10.1093/bioinformatics/btv494View Article
Google Scholar
Bonin, A., E. Bellemain, E.P. Bronken, F. Pompanon, C. Brochmann and P. Taberlet. 2004. How to track and assess genotyping errors in population genetics studies. Mol. Ecol. 13(11): 3261–3273.
DOI: 10.1111/j.1365-294X.2004.02346.xView Article
Google Scholar
Clement, M.J., Q. Snell, P. Walke, D. Posada and K.A. Crandall. 2002. TCS: estimating gene genealogies. Proc. 16th Int. Parallel Distrib. Process Symp. 2: 184.
Csill?ry, K., M.G.B. Blum, O.E. Gaggiotti and O. Fran?ois. 2010. Approximate Bayesian computation (ABC) in practice. Trends Ecol. Evol. 25(7): 410–418.
DOI: 10.1016/j.tree.2010.04.001View Article
Google Scholar
Doyle, J.J. and J.L. Doyle. 1987. A rapid DNA isolation procedure from small quantities of fresh leaf material. Phytochem. Bull. 19(1): 11–15.
Dray, S. and A.-B. Dufour. 2007. The ade4 package: implementing the duality diagram for ecologists. J. Stat. Soft. 22(4): 1–20.
DOI: 10.18637/jss.v022.i04View Article
Google Scholar
Ebersbach, J., J. Schnitzler, A. Favre and A.N. Muellner-Riehl. 2017. Evolutionary radiations in the species-rich mountain genus Saxifraga L. BMC Evol. Biol. 17(1): 119.
DOI: 10.1186/s12862-017-0967-2View 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. 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
Farminh?o, J.N.M., S. Verlynde, E. Kaymak, V. Droissart, M. Simo-Droissart, G. Collobert, F. Martos and T. St?vart. 2021. Rapid radiation of angraecoids (Orchidaceae, Angraecinae) in tropical Africa characterized by multiple karyotypic shifts under major environmental instability. Mol. Phylogenet. Evol. 159: 107105.
DOI: 10.1016/j.ympev.2021.107105View Article
Google Scholar
Farris, J.S. 1989. The retention index and the rescaled consistency index. Cladistics 5(4): 417–419.
DOI: 10.1111/j.1096-0031.1989.tb00573.xView Article
Google Scholar
Felsenstein, J. 1985. Confidence limits on phylogenies: An approach using the bootstrap. Evolution 39(4): 783–791.
DOI: 10.2307/2408678View Article
Google Scholar
Fox, J. and S. Weisberg. 2011. An R Companion to Applied Regression, 2nd ed. Sage, Thousand Oaks, USA.
Frichot, E. and O. Francois. 2015. LEA: an R package for landscape and ecological association studies. Methods Ecol. Evol. 6(8): 925–929.
DOI: 10.1111/2041-210X.12382View Article
Google Scholar
Funk, D.J. and K.E. Omland. 2003. Species-level paraphyly and polyphyly: frequency, causes, and consequences, with insights from animal mitochondrial DNA. Ann. Rev. Ecol. Evol. and Syst. 34(1): 397–423.
DOI: 10.1146/annurev.ecolsys.34.011802.132421View Article
Google Scholar
George, S., J. Sharma and V.L. Yadon. 2009. Genetic diversity of the endangered and narrow endemic Piperia yadonii (Orchidaceae) assessed with ISSR polymorphisms. Amer. J. Bot. 96(11): 2022–2030.
DOI: 10.3732/ajb.0800368View Article
Google Scholar
Goetze, M., C.M. Zanella, C. Palma-Silva, M.V. B?ttow and F. Bered. 2017. Incomplete lineage sorting and hybridization in the evolutionary history of closely related, endemic yellow-flowered Aechmea species of subgenus Ortgiesia (Bromeliaceae). Amer. J. Bot. 104(7): 1073–1087.
DOI: 10.3732/ajb.1700103View Article
Google Scholar
Gow, J.L., C.L. Peichel and E.B. Taylor. 2006. Contrasting hybridization rates between sympatric three spine sticklebacks highlight the fragility of reproductive barriers between evolutionarily young species. Mol. Ecol. 15(3): 739–752.
DOI: 10.1111/j.1365-294X.2006.02825.xView Article
Google Scholar
Hey, J. 2010. Isolation with migration models for more than two populations. Mol. Biol. Evol. 27(4): 905–920.
DOI: 10.1093/molbev/msp296View Article
Google Scholar
Hu, A.-Q., S.W. Gale, Z.-J. Liu, S. Suddee, T.-C. Hsu, G.A. Fischer and R.M.K. Saunders. 2020. Molecular phylogenetics and floral evolution of the Cirrhopetalum alliance (Bulbophyllum, Orchidaceae): Evolutionary transitions and phylogenetic signal variation. Mol. Phylogen. Evol. 143: 106689.
DOI: 10.1016/j.ympev.2019.106689View Article
Google Scholar
Isabel, N., J. Beaulieu, P. Th?riault and J. Bousquet. 1999. Direct evidence for biased gene diversity estimates from dominant random amplified polymorphic DNA (RAPD) fingerprints. Mol. Ecol. 8(3): 477–483.
DOI: 10.1046/j.1365-294X.1999.00597.xView Article
Google Scholar
Jacquemyn, H., R. Brys, D. Adriaens, O. Honnay and I. Rold?n-Ruiz. 2009. Effects of population size and forest management on genetic diversity and structure of the tuberous orchid Orchis mascula. Conserv. Genet. 10(1): 161–168.
DOI: 10.1007/s10592-008-9543-zView Article
Google Scholar
Jombart, T. and I. Ahmed. 2011. Adegenet 1.3-1: new tools for the analysis of genome-wide SNP data. Bioinformatics 27(21): 3070–3071.
DOI: 10.1093/bioinformatics/btr521View 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
Kamvar, Z.N., J.C. Brooks and N.J. Gr?nwald. 2015. Novel R tools for analysis of genome-wide population genetic data with emphasis on clonality. Front. Genet. 6: 208.
DOI: 10.3389/fgene.2015.00208View Article
Google Scholar
Kimura, M. 1983. The Neutral Theory of Molecular Evolution. Cambridge Univ. Press, Cambridge, UK.
DOI: 10.1017/CBO9780511623486View Article
Kluge, A.G. and J.S. Farris. 1969. Quantitative phyletics and the evolution of Anurans. Syst. Zool. 18(1): 1–32.
DOI: 10.2307/2412407View Article
Google Scholar
Koopman, W.J.M., V. Wissemann, K. de Cock, J. van Huylenbroeck, J. de Riek, G.J.H Sabatino, D. Visser, B. Vosman, C.M. Ritz, B. Maes, G. Werlemark, H. Nybom, T. Debener, M. Linde and J.M. Smulders. 2008. AFLP markers as a tool to reconstruct complex relationships: A case study in Rosa (Rosaceae). Amer. J. Bot. 95(3): 353–366.
DOI: 10.3732/ajb.95.3.353View Article
Google Scholar
Leigh, J.W. and D. Bryant. 2015. PopART: full-feature software for haplotype network construction. Methods Ecol. Evol. 6(9): 1110–1116.
DOI: 10.1111/2041-210X.12410View Article
Google Scholar
Leimu, R., P. Mutikainen, J. Koricheva and M. Fischer. 2006. How general are positive relationships between plant population size, fitness and genetic variation? J. Ecol. 94(5): 942–952.
DOI: 10.1111/j.1365-2745.2006.01150.xView Article
Google Scholar
Lenth, R. 2018. emmeans: Estimated marginal means, aka least-squares means. R package version 1.3.1. https://CRAN.R-project.org/package=emmeans. Accessed Apr 7. 2018.
Lin, T.P. 2019. The Orchid Flora of Taiwan, a collection of line drawings. NTU Press, Taipei, Taiwan. 1012 pages.
DOI: 10.978.986350/3682View Article
Google Scholar
Linder, C.R. and L.H. Rieseberg. 2004. Reconstructing patterns of reticulate evolution in plants. Amer. J. Bot. 91(10): 1700–1708.
DOI: 10.3732/ajb.91.10.1700View Article
Google Scholar
Mariette, S., V. Le Corre, F. Austerlitz and Kremer, A. 2002. Sampling within the genome for measuring within-population diversity: trade-offs between markers. Mol. Ecol. 11(7): 1145–1156.
DOI: 10.1046/j.1365-294X.2002.01519.xView Article
Google Scholar
Meleshko, O., M.D. Martin, T.S. Korneliussen, C. Schr?ck, P. Lamkowski, J. Schmutz, A. Healey, B.T. Piakowski, A.J. Shaw, D.J. Weston, K.I. Flatberg, P. Sz?v?nyi, K. Hassel and H.K. Sten?ien. 2021. Extensive genome-wide phylogenetic discordance is due to incomplete lineage sorting and not ongoing introgression in a rapidly radiated bryophyte genus. Mol. Biol. Evol. 38(7): 2750–2766.
DOI: 10.1093/molbev/msab063View Article
Google Scholar
Muir, G. and C. Schl?tterer. 2005. Evidence for shared ancestral polymorphism rather than recurrent gene flow at microsatellite loci differentiating two hybridizing oaks (Quercus spp.) Mol. Ecol. 14(2): 549–561.
DOI: 10.1111/j.1365-294X.2004.02418.xView Article
Google Scholar
Nei, M. 1978. Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89(3): 583–590.
DOI: 10.1093/genetics/89.3.583View Article
Google Scholar
Nei, M. 1987. Molecular Evolutionary Genetics. Columbia University Press, New York, USA. 512 pp.
DOI: 10.7312/nei-92038View Article
Nielsen, R. and J. Wakeley. 2001. Distinguishing migration from isolation. A Markov chain Monte Carlo approach. Genetics 158(2): 885–896.
DOI: 10.1093/genetics/158.2.885View Article
Google Scholar
Paradis, E. and K. Schliep. 2019. ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics 35(3): 526–528.
DOI: 10.1093/bioinformatics/bty633View Article
Google Scholar
Pease, J.B., D.C. Haak, M.W. Hahn and L.C. Moyle. 2016. Phylogenomics reveals three sources of adaptive variation during a rapid radiation. PLoS Biol. 14(2): e1002379.
DOI: 10.1371/journal.pbio.1002379View Article
Google Scholar
P?rez-Excobar, O.A., G. Chomicki, F.L. Condamine, A.P. Karremans, D. Bogarin, N.J. Matxke, D. Silvestro and A. Antonelli. 2017. Recent origin and rapid speciation of Neotropical orchids in the world’s richest plant biodiversity hotspot. New Phytol. 215(2): 891–905.
DOI: 10.1111/nph.14629View Article
Google Scholar
Petit, R.J. and L. Excoffier. 2009. Gene flow and species delimitation. Trends Ecol. Evol. 24(7): 386–393.
DOI: 10.1016/j.tree.2009.02.011View Article
Google Scholar
Pritchard, J.K., M. Stephens and P. Donnelly. 2000. Inference of population structure using multilocus genotype data. Genetics 155(2): 945–959.
DOI: 10.1093/genetics/155.2.945View Article
Google Scholar
Qu, Y.H., X. Luo, R.Y. Zhang, G. Song, F.S. Zou and F.M. Lei. 2011. Lineage diversification and historical demography of a montane bird Garrulax elliotii—implications for the Pleistocene evolutionary history of the eastern Himalayas. BMC Evol. Biol. 11(1): 174.
DOI: 10.1186/1471-2148-11-174View Article
Google Scholar
R Development Core Team. 2020. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing. Vienna, Austria.
Rokas, A. and S.B. Carroll. 2006. Bushes in the tree of life. PLoS Biol. 4(11): e352.
DOI: 10.1371/journal.pbio.0040352View Article
Google Scholar
Rozas, J., A. Ferrer-Mata, J.C. S?nchez-DelBarrio, S. Guirao-Rico, P. Librado, S.E. Ramos-Onsins and A. S?nchez-Gracia. 2017. DnaSP 6: DNA sequence polymorphism analysis of large datasets. Mol. Biol. Evol. 34(12): 3299–3302.
DOI: 10.1093/molbev/msx248View Article
Google Scholar
Schliep, K.P. 2011. phangorn: phylogenetic analysis in R. Bioinformatics 27(4): 592–593.
DOI: 10.1093/bioinformatics/btq706View Article
Google Scholar
Sten?ien, H.K., A.J. Shaw, B. Shaw, K. Hassel and U. Gunnarsson. 2011. North American origin and recent European establishments of the amphi-Atlantic peat moss Sphagnum angermanicum. Evolution 65(4):1181–1194.
DOI: 10.1111/j.1558-5646.2010.01191.xView Article
Google Scholar
Suetsugu, K., S. Kaida, H. Fukunaga and S. Sawa. 2020. A new form of the mycoheterotrophic plant Lecanorchis japonica (Orchidaceae) from Japan. Acta Phytotax. Geobot. 71(3): 243–248.
Suetsugu, K., S. Kaida, T.-C. Hsu and S. Sawa. 2019. Lecanorchis moritae (Orchidaceae, Vanilloideae), a new mycoheterotrophic species from Amamai-Oshima Island, Japan based on morphological and molecular data. Phytotaxa 404(4): 137–145.
DOI: 10.11646/phytotaxa.404.4.2View Article
Google Scholar
Suetsugu, K., C. Shimaoka, H. Fukunaga and S. Sawa. 2018. The taxonomic identity of three varieties of Lecanorchis nigricans (Vanilleae, Vanilloideae, Orchidaceae) in Japan. PhytoKeys 92: 17–35.
DOI: 10.3897/phytokeys.92.21657View Article
Google Scholar
Sunn?ker, M., A.G. Busetto, E. Numminen, J. Corander, M. Foll and C. Dessimoz. 2013. Approximate Bayesian computation. PLoS Comput. Biol. 9(1): e1002803.
DOI: 10.1371/journal.pcbi.1002803View Article
Google Scholar
Szczeci?ska, M., G. Sramk?, K. Wolosz and J. Sawwicki. 2016. Genetic diversity and population structure of the rare and endangered plant species Pulsatilla patens (L.) Mill in East Central Europe. PLoS One 11(3): e0151730.
DOI: 10.1371/journal.pone.0151730View Article
Google Scholar
Sz?v?nyi, P., S. Terracciano, M. Ricca, S. Giordano and A.J. Shaw. 2008. Recent divergence, intercontinental dispersal and shared polymorphism are shaping the genetic structure of amphi-Atlantic peatmoss populations. Mol Ecol. 17(24): 5364–5377.
DOI: 10.1111/j.1365-294X.2008.04003.xView Article
Google Scholar
Takashima, M., Y. Yamashita, A. Kinoshita, M. Ohta and T. Yukawa. 2019. Taxonomic status of Lecanorchis suginoana (Tuyama) Seriz. (Orchidaceae). Bull. Natl. Mus. Nat. Sci. Ser. B. 45(3): 119–129.
Thompson, J.D., D.G. Higgins and T.J. Gibson. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucl. Acids Res. 22(22): 4673–4680.
DOI: 10.1093/nar/22.22.4673View Article
Google Scholar
Vekemans, X., T. Beauwens, M. Lemaire and I. Rold?n-Ruiz. 2002. Data from amplified fragment length polymorphism (AFLP) markers show indication of size homoplasy and of a relationship between degree of homoplasy and fragment size. Mol. Ecol. 11(1): 139–151.
DOI: 10.1046/j.0962-1083.2001.01415.xView Article
Google Scholar
Vos, P., R. Hogers, M. Bleeker, M. Reijans, T. van der Lee, M. Hornes, A. Friters, J. Pot, J. Paleman, M. Kuiper and M. Zabeau. 1995. AFLP: a new technique for DNA fingerprinting. Nucl. Acids Res. 23(21): 4407–4414.
DOI: 10.1093/nar/23.21.4407View Article
Google Scholar
WCVP. 2022, World Checklist of Vascular Plants, version 2.0. Facilitated by the Royal Botanic Gardens, Kew. Published on the Internet; http://wcvp.science.kew.org. Accessed 11 Mar. 2022.
Zhivotovsky, L.A. 1999. Estimating population structure in diploids with multilocus dominant DNA markers. Mol. Ecol. 8(6): 907–913.
DOI: 10.1046/j.1365-294x.1999.00620.xView Article
Google Scholar
Zhou, Y., L. Duvaux, G. Ren, L. Zhang, O. Savolainen and J. Liu. 2017. Importance of incomplete sorting and introgression in the origin of shared genetic variation between two closely related pines with overlapping distributions. Heredity 118(3): 211–220.
DOI: 10.1038/hdy.2016.72View Article
Google Scholar