Incomplete lineage sorting and secondary admixture results in the paraphyly of Lecanorchis cerina, L. suginoana, and L. thalassica (Orchidaceae) in Taiwan

10.6165/tai.2022.67.366

Shih-Ying HWANG；Yi-Shao LI；Tsan-Piao LIN

AFLP ； incomplete lineage sorting ； Lecanorchis ； nrITS1 ； secondary gene flow ； Vanilleae ； Vanilloideae

TAIWANIA

67卷3期（2022 / 09 / 01）

366 - 376+s1-2

英文

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.

1. Álvarez, I., J.F. Wendel. 2003. Ribosomal ITS sequences and plant phylogenetic inference. Mol. Phylogenet. Evol. 29(3): 417–434.
   連結：
2. Bates, D., M. Maechler, B. Bolker and S. Walker. 2015. Fitting linear mixed effects models using lme4. J. Stat. Soft. 67(1): 1–48.
   連結：
3. Bodenhofer, U., E. Bonatesta, C. Horejš-Kainrath and S. Hochreiter. 2015. msa: an R package for multiple sequence alignment. Bioinformatics 31(24): 3997–3999.
   連結：
4. 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.
   連結：
5. Csilléry, K., M.G.B. Blum, O.E. Gaggiotti and O. François. 2010. Approximate Bayesian computation (ABC) in practice. Trends Ecol. Evol. 25(7): 410–418.
   連結：
6. Dray, S. and A.-B. Dufour. 2007. The ade4 package: implementing the duality diagram for ecologists. J. Stat. Soft. 22(4): 1–20.
   連結：
7. 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.
   連結：
8. 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.
   連結：
9. 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.
   連結：
10. Farminhão, J.N.M., S. Verlynde, E. Kaymak, V. Droissart, M. Simo-Droissart, G. Collobert, F. Martos and T. Stévart. 2021. Rapid radiation of angraecoids (Orchidaceae, Angraecinae) in tropical Africa characterized by multiple karyotypic shifts under major environmental instability. Mol. Phylogenet. Evol. 159: 107105.
    連結：
11. Farris, J.S. 1989. The retention index and the rescaled consistency index. Cladistics 5(4): 417–419.
    連結：
12. Felsenstein, J. 1985. Confidence limits on phylogenies: An approach using the bootstrap. Evolution 39(4): 783–791.
    連結：
13. Frichot, E. and O. Francois. 2015. LEA: an R package for landscape and ecological association studies. Methods Ecol. Evol. 6(8): 925–929.
    連結：
14. 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.
    連結：
15. 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.
    連結：
16. Goetze, M., C.M. Zanella, C. Palma-Silva, M.V. Büttow 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.
    連結：
17. 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.
    連結：
18. Hey, J. 2010. Isolation with migration models for more than two populations. Mol. Biol. Evol. 27(4): 905–920.
    連結：
19. 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.
    連結：
20. Isabel, N., J. Beaulieu, P. Thériault 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.
    連結：
21. Jacquemyn, H., R. Brys, D. Adriaens, O. Honnay and I. Roldán-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.
    連結：
22. 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.
    連結：
23. 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.
    連結：
24. Kamvar, Z.N., J.C. Brooks and N.J. Grünwald. 2015. Novel R tools for analysis of genome-wide population genetic data with emphasis on clonality. Front. Genet. 6: 208.
    連結：
25. Kimura, M. 1983. The Neutral Theory of Molecular Evolution. Cambridge Univ. Press, Cambridge, UK.
    連結：
26. Kluge, A.G. and J.S. Farris. 1969. Quantitative phyletics and the evolution of Anurans. Syst. Zool. 18(1): 1–32.
    連結：
27. 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.
    連結：
28. Leigh, J.W. and D. Bryant. 2015. PopART: full-feature software for haplotype network construction. Methods Ecol. Evol. 6(9): 1110–1116.
    連結：
29. 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.
    連結：
30. Lin, T.P. 2019. The Orchid Flora of Taiwan, a collection of line drawings. NTU Press, Taipei, Taiwan. 1012 pages.
    連結：
31. Linder, C.R. and L.H. Rieseberg. 2004. Reconstructing patterns of reticulate evolution in plants. Amer. J. Bot. 91(10): 1700–1708.
    連結：
32. 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.
    連結：
33. Meleshko, O., M.D. Martin, T.S. Korneliussen, C. Schröck, P. Lamkowski, J. Schmutz, A. Healey, B.T. Piakowski, A.J. Shaw, D.J. Weston, K.I. Flatberg, P. Szövényi, K. Hassel and H.K. Stenøien. 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.
    連結：
34. Muir, G. and C. Schlötterer. 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.
    連結：
35. Nei, M. 1978. Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89(3): 583–590.
    連結：
36. Nei, M. 1987. Molecular Evolutionary Genetics. Columbia University Press, New York, USA. 512 pp.
    連結：
37. Nielsen, R. and J. Wakeley. 2001. Distinguishing migration from isolation. A Markov chain Monte Carlo approach. Genetics 158(2): 885–896.
    連結：
38. Paradis, E. and K. Schliep. 2019. ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics 35(3): 526–528.
    連結：
39. 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.
40. 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.
41. Fox, J. and S. Weisberg. 2011. An R Companion to Applied Regression, 2nd ed. Sage, Thousand Oaks, USA.
42. 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.