Phylogeny and taxonomy of recently diverged groups as exemplified by the genus Rosa

I.A. Schanzer

Proceedings of the Zoological Institute RAS, 2013, 317(Supplement 2):

Abstract

Delimitation of species and establishing their relations in evolutionary young groups often proves to be an uneasy task. In morphological terms this means weak interspecific differentiation, parallel variability, and probable hybrid origin of intermediates. In genetical terms this means the effects of already mentioned hybridization, ancestral polymorphism and incomplete lineage sorting. The genus Rosa may serve as one of the brightest examples of a group where all the mentioned problems occur simultaneously. Such a group appears to be pretty resistant to methods of both traditional taxonomy and molecular cladistics. The use of nuclear and chloroplast haplotype genealogies to reveal the internal structure and phylogenetic relationships in Rosa and similar groups are discussed in the paper. Analyses of nr (ITS1) and cp (trnL-trnF) genealogies enables to reveal with various detail 6 to 9 groups of closely interrelated Rosa species, to much extent coinciding with each other and definite geographically, however, only partly corresponding to traditional sections.

Key words

phylogeny, genealogy, hybridization, incomplete lineage sorting, ITS1, trnL-trnF, Rosa

Published September 16, 2013

References

Абрамсон Н.И. 2007. Филогеография: итоги, проблемы, перспективы. Вестник ВОГиС, 11(2): 307–331.

Хржановский В.Н. 1958. Розы. Филогения и систематика. Спонтанные виды Европейской части СССР, Крыма и Кавказа. Опыт и перспективы использования. Советская Наука, Москва, 497 с.

Шанцер И.А. 2001. Современное состояние таксономической изученности восточноевропейских шиповников (Rosa L.). Бюллетень МОИП. Отдел биологический, 106(2): 43–48.

Шанцер И.А., Вагина А.В. и Остапко В.М. 2011. Критическое исследование шиповников (Rosa L.) заповедника “Хомутовская степь”. Бюллетень МОИП. Отдел биологический, 116(3): 38–49.

Шнеер В.С. 2005. Краткий очерк способов получения, обработки и трактовки данных по последовательности ДНК в систематике растений. Ботанический журнал, 90(3): 304–323.

Avise J.C., Arnold J., Ball R.M., Bermingham E., Lamb T., Neigel J.E., Reeb C.A. and Saunders N.C. 1987. Intraspecific phylogeography: the mitochondrial DNA bridge between population genetics and systematics. Annual Review of Ecology, Evolution and Systematics, 18: 489–522. https://doi.org/10.1146/annurev.es.18.110187.002421

Bandelt H.-J., Forster P. and Röhl A. 1999. Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution, 16(1): 37–48. https://doi.org/10.1093/oxfordjournals.molbev.a026036

Becker H.F. 1963. The fossil record of the genus Rosa. Bulletin of Torrey Botanical Club, 90(2): 99–110. https://doi.org/10.2307/2483008

Bruneau A., Starr J.R. and Joly S. 2007. Phylogenetic relationships in the genus Rosa: new evidence from chloroplast DNA sequences and an appraisal of current knowledge. Systematic Botany, 32(2): 366–378. https://doi.org/10.1600/036364407781179653

Cassens I., van Waerenbeek K., Best P.B., Crespo E.A., Reyes J. and Milinkovitch M.C. 2003. The phylogeography of dusky dolphins (Lagenorhynchus obscurus): a critical examination of network methods and rooting procedures. Molecular Ecology, 12(7): 1781–1792. https://doi.org/10.1046/j.1365-294X.2003.01876.x

Clement M., Posada D. and Crandall K.A. 2000. TCS: a computer program to estimate gene genealogies. Molecular Ecology, 9(10): 1657–1659. https://doi.org/10.1046/j.1365-294x.2000.01020.x

Crandall K.A. and Templeton A.R. 1993. Empirical tests of some predictions from coalescent theory with applications to intraspecific phylogeny reconstruction. Genetics, 134: 959–969. https://doi.org/10.1093/genetics/134.3.959

Degnan J.H. and Rosenberg N.A. 2009. Gene tree discordance, phylogenetic inference and the multispecies coalescence. Trends in Ecology and Evolution, 24(6): 332–340. https://doi.org/10.1016/j.tree.2009.01.009

Doyle J.J. 1992. Gene trees and species trees: molecular systematics as one-character taxonomy. Systematic Botany, 17(1): 144–163. https://doi.org/10.2307/2419070

Eriksson T., Donoghue M.J. and Hibbs M.S. 1998. Phylogenetic analysis of Potentilla using DNA sequences of nuclear ribosomal internal transcribed spacers (ITS), and implications for the classification of Rosoideae (Rosaceae). Plant Systematics and Evolution, 211: 155–179. https://doi.org/10.1007/BF00985357

Fedorova A.V., Schanzer I.A. and Kagalo A.A. 2010. Local differentiation and hybridization in populations of wild roses in W Ukraine. Wulfenia, 17: 99–115.

Gurushidze M., Fritsch R.M. and Blattner F.R. 2010. Species-level phylogeny of Allium subgenus Melanocrommyum: Incomplete lineage sorting, hybridization and trnF gene duplication. Taxon, 59(3): 829–840. https://doi.org/10.1002/tax.593012

Hein J., Scheirup M.H. and Wiuf C. 2005. Gene genealogies, variation and evolution. A primer in coalescent theory. Oxford University Press, New York, 276 p.

Helfgott D.M., Francisco-Ortega J., Santos-Guerra A., Jansen R.K. and Simpson B.B. 2000. Biogeography and breeding system evolution of the woody Bencomia alliance (Rosaceae) in Macaronesia based on ITS sequence data. Systematic Botany, 25(1): 82–97. https://doi.org/10.2307/2666675

Hudson R.R. 1991. Gene genealogies and the coalescent process. Oxford Surveys in Evolutionary Biology, 7: 1–44.

Huson D.H. 1998. Splits Tree: A program for analyzing and visualizing evolutionary data. Bioinformatics, 14(10): 68–73. https://doi.org/10.1093/bioinformatics/14.1.68

Huson D.H. and Bryant D. 2006. Application of phylogenetic networks in evolutionary studies. Molecular Biology and Evolution, 23(2): 254–267. https://doi.org/10.1093/molbev/msj030

Iwata H., Kato T. and Ohno S. 2000. Triparental origin of Damask roses. Gene, 259(1–2): 53–59. https://doi.org/10.1016/S0378-1119(00)00487-X

Jacob S.S. and Blattner F.R. 2006. A chloroplast genealogy of Hordeum (Poaceae): long-term persisting haplotypes, incomplete lineage sorting, regional extinction, and the consequences for phylogenetic inference. Molecular Bioliology and Evolution, 23(8): 1602–1612. https://doi.org/10.1093/molbev/msl018

Joly S., Starr J.R., Lewis W.H. and Bruneau A. 2006. Polyploid and hybrid evolution in roses east of the Rocky Mountains. American Journal of Botany, 93: 412–425. https://doi.org/10.3732/ajb.93.3.412

Khaitova L., Werlemark G., Nybom H. and Kovarik A. 2010. Frequent silencing of rDNA loci on the univalent-forming genomes contrasts with their stable expression on the bivalent-forming genomes in polyploid dogroses (Rosa sect. Caninae). Heredity, 104(1): 113–120. https://doi.org/10.1038/hdy.2009.94

Kingman J.F.C. 1982. On the genealogy of large populations. Journal of Applied Probability, 19: 27–43. https://doi.org/10.2307/3213548

Kingman J.F.C. 2000. Origins of the coalescent: 1974–1982. Genetics, 156: 1461–1463. https://doi.org/10.1093/genetics/156.4.1461

Koopman W.J.M., Wissemann V., De Cock K., van Huylenbroeck J., De Riek J., Sabatino G.J.H., Visser D., Vosman B., Ritz C.M., Maes B., Werlemark G., Nybom H., Debener T., Linde M. and Smulders M.J.M. 2008. AFLP markers as a tool to reconstruct complex relationships: a case study in Rosa (Rosaceae). American Journal of Botany, 95(3): 353–366. https://doi.org/10.3732/ajb.95.3.353

Kovarik A., Werlemark G., Leitch A.R., Souckova-Skalicka K., Lim Y.K., Khaitova L., Koukalova B. and Nybom H. 2008. The asymmetric meiosis in pentaploid dogroses (Rosa sect. Caninae) is associated with a skewed distribution of rRNA gene families in the gametes. Heredity, 101(4): 359–367. https://doi.org/10.1038/hdy.2008.63

Matsumoto S., Kouchi M. and Fukui H. 2000. Phylogenetic analyses of the subgenus Eurosa using the ITS nrDNA sequence. Acta Horticulturae, 521: 193–202. https://doi.org/10.17660/ActaHortic.2000.521.21

Matsumoto S., Nishio H., Ueda Y. and Fukui H. 2001. Phylogenetic analyses of genus Rosa: polyphyly of section Pimpinellifoliae and origin of Rosa x fortuniana Lindl. Acta Horticulturae, 547: 357–363. https://doi.org/10.17660/ActaHortic.2001.547.43

McNutt P.M., Dehart M.J. and Matej L.A. 2007. Characterization of the 16S-23S internal transcribed spacer among 34 higher plants: suitability for interspecific plastid transformation. Plant Cell Reports, 26(1): 47–60. https://doi.org/10.1007/s00299-006-0203-9

Mort M.E., Archibald J.K., Randle C.P., Levsen N.D., O’Leary T.R., Topalov K., Wiegand C.M. and Crawford D.J. 2007. Inferring phylogeny at low taxonomic levels: utility of rapidly evolving cpDNA and nuclear ITS loci. American Journal of Botany, 94(2): 173–183. https://doi.org/10.3732/ajb.94.2.173

Page R.D. and Charleston M.A. 1997. From gene to organismal phylogeny: reconciled trees and the gene tree/species tree problem. Molecular Phylogenetics and Evolution, 7(2): 231–240. https://doi.org/10.1006/mpev.1996.0390

Posada D. and Crandall K.A. 2001. Intraspecific gene genealogies: trees grafting into networks. Trends in Ecology and Evolution, 16(1): 37–45. https://doi.org/10.1016/S0169-5347(00)02026-7

Potter D., Eriksson T., Evans R.C., Oh S., Smedmark J.E.E., Morgan D.R., Kerr M., Robertson K.R., Arsenault M., Dickinson T.A. and Campbell C.S. 2007. Phylogeny and classification of Rosaceae. Plant Systematics and Evolution, 266: 5–43. https://doi.org/10.1007/s00606-007-0539-9

Ritz C.M. and Wissemann V. 2003. Male correlated non-matroclinal character inheritance in reciprocal hybrids of Rosa section Caninae (DC.) Ser. (Rosaceae). Plant Systematics and Evolution, 241: 213–221. https://doi.org/10.1007/s00606-003-0058-2

Ritz C.M., Schmuths H. and Wissemann V. 2005. Evolution by reticulation: European dogroses originated by multiple hybridization across the genus Rosa. Journal of Heredity, 96(1): 4–14. https://doi.org/10.1093/jhered/esi011

Rosenberg N.A. and Nordborg M. 2002. Genealogical trees, coalescent theory and the analysis of genetic polymorphisms. Nature reviews. Genetics, 3: 380–390. https://doi.org/10.1038/nrg795

Taberlet P., Gielly L., Pautou G. and Bouvet J. 1991. Universal primers for amplification of three non-coding regions of chloroplast DNA. Plant Molecular Biology, 17: 1105–1109. https://doi.org/10.1007/BF00037152

Templeton A.R. 1998. Nested clade analyses of phylogeographic data: testing hypotheses about gene flow and population history. Molecular Ecology, 7: 381–397. https://doi.org/10.1046/j.1365-294x.1998.00308.x

Templeton A.R. 2001. Using phylogeographic analyses of gene trees to test species status and processes. Molecular Ecology, 10: 779–791. https://doi.org/10.1046/j.1365-294x.2001.01199.x

Templeton A.R. and Sing C.F. 1993. A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. IV. Nested analysis with cladogram uncertainty and recombination. Genetics, 134: 659–669. https://doi.org/10.1093/genetics/134.2.659

Templeton A.R., Boerwinkle E. and Sing C.F. 1987. A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping. I. Basic theory and an analysis of alcohol dehydrogenase activity in Drosophila. Genetics, 117: 343–351. https://doi.org/10.1093/genetics/117.2.343

Templeton A.R., Crandall K.A. and Sing C.F. 1992. A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation. Genetics, 132: 619–633. https://doi.org/10.1093/genetics/132.2.619

Wissemann V. and Ritz C. 2005. The genus Rosa (Rosoideae, Rosaceae) revisited: molecular analysis of nrITS-1 and atpB-rbcL intergenic spacer (IGS) versus conventional taxonomy. Botanical Journal of the Linnean Society, 147: 275–290. https://doi.org/10.1111/j.1095-8339.2005.00368.x

Woolley S.M., Posada D. and Crandall K.A. 2008. A comparison of phylogenetic network methods using computer simulation. PLoS ONE, 3(4): e1913. https://doi.org/10.1371/journal.pone.0001913

Wu S., Ueda Y., Nishihara S. and Matsumoto S. 2001. Phylogenetic analysis of Japanese Rosa species using DNA sequences of nuclear ribosomal internal transcribed spacers (ITS). Journal of Horticultural Science and Biotechnology, 76: 127–132. https://doi.org/10.1080/14620316.2001.11511338

Zieliński J. 1985. Studia nad rodzajem Rosa L. – Systematyka sekcji Caninae DC. em. Christ. Arboretum Kórnickie, 30: 3–109.