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Type: Article
Published: 2021-08-26
Page range: 237–251
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Species delimitation of the northeastern Anatolian Symphytum (Boraginaceae) taxa

Department of Biology, Faculty of Science and Letters, Eskisehir Osmangazi University, Eskisehir, Turkey
Department of Biology, Faculty of Science, Hacettepe University, Çankaya, Ankara, Turkey
Eudicots Boraginaceae Species Delimitation Symphytum Symphytum asperum aggregate

Abstract

Symphytum is regarded one of the most complicated genera in terms of the classification of its members among the Boraginaceae. In addition to different infrageneric classification methods, several species complex or aggregates have been proposed to deal with the taxonomical problem of genus members. Symphytum asperum aggregate was first introduced by Kurtto, who proposed six taxa within this aggregate. However, according to further studies by different researchers based on morphological data, total number of species of the complex was variable. The number of species was reduced to three, comprising S. asperum, S. savvalense, and S. sylvaticum, after the phylogenetic and morphological studies of Tarıkahya-Hacıoğlu and Erik. However, the taxonomical status of some of these species (i.e., S. savvalense and S. sylvaticum, and S. sepulcrale), which was assigned as a member of this complex by Kurtto, has been regarded as unresolved. To solve this uncertainty, different species delimitation methods were used, including statistical parsimony network analysis (TCS), generalized mixed Yule coalescent (GMYC), and Bayesian Phylogenetics and Phylogeography (BPP) of the ITS, trnL-F and trnS-G sequence data. In addition to members of this complex, S. ibericum, which is phylogenetically nested within the S. asperum aggregate, was also used. The TCS and GMYC analyses demonstrated more complicated clusters, whereas high posterior probabilities of BPP clusters were more compatible with the morphological data. In accordance with the morphological approach of Tarıkahya-Hacıoğlu and Erik, the species delimitation analyses based on molecular data support the recognition of S. asperum, S. ibericum, S. savvalense, and S. sylvaticum as different species.

References

<p>Ayres, D.L., Darling, A., Zwickl, D.J., Beerli, P., Holder, M.T., Lewis, P.O., Huelsenbeck, J.P., Ronquist, F., Swofford, D.L., Cummings, M.P., Rambaut, A. &amp; Suchard, M.A. (2012) BEAGLE: An application programming interface and high-performance computing library for statistical phylogenetics. <em>Systematic Biology </em>61 (1): 170–173.&nbsp; https://doi.org/10.1093/sysbio/syr100</p>
<p>Akaike, H. (1974) A new look at the statistical model identification. IEEE Trans. <em>Automatic Control</em> 19: 716–723.</p>
<p>Bucknall, C. (1913) A revision of the genus Symphytum. <em>Botanical Journal of the Linnean Society</em> 41: 491–556.</p>
<p>Boissier, E. (1875) <em>Flora Orientalis</em>, vol. 3. H. Georg, Genève &amp; Basel, 174 pp.</p>
<p>Camargo, A. &amp; Sites, J. (2013) Species Delimitation: A decade after the renaissance, <em>In</em>: Pavlinov, I. (Ed.) <em>The Species Problem - Ongoing Issues</em>. InTech, New York, NY, pp. 225–247. https://doi.org/10.5772/52664</p>
<p>Chacón, J., Luebert, F., Hilger, H.H., Ovchinnikova, S., Selvi, F., Cecchi, L., Guilliams, C.M., Hasenstab-Lehman, K., Sutorı, K., Simpson, M.G. &amp; Weigend, M. (2016) The borage family (Boraginaceae s. str.): A revised infrafamilial classification based on new phylogenetic evidence, with emphasis on the placement of some enigmatic genera. <em>Taxon</em> 65 (3): 523–546. https://doi.org/10.12705/653.6</p>
<p>Chacón, J., Luebert, F. &amp; Weigend, M. (2017) Biogeographic events are not correlated with diaspore dispersal modes in Boraginaceae. <em>Frontiers in Ecology and Evolution</em> 5: 26. https://doi.org/10.3389/fevo.2017.00026</p>
<p>Chase, M.W., Christenhusz, M.J.M., Fay, M.F., Byng, J.W., Judd, W.S., Soltis, D.E., Mabberley, D.J., Sennikov, A.N., Soltis, P.S., Stevens, P.F., Briggs, B., Brockington, S., Chautems, A., Clark, J.C., Conran, J., Haston, E., Möller, M., Moore, M., Olmstead, R., Perret, M., Skog, L., Smith, J., Tank, D., Vorontsova, M. &amp; Weber, A. (2016) An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV. <em>Botanical Journal of the Linnean Society</em> 181: 1–20. https://doi.org/10.1111/boj.12385</p>
<p>Clement, M., Posada, D. &amp; Crandall, K.A. (2000) TCS: A computer program to estimate gene genealogies. <em>Molecular Ecology</em> 9: 1657–1659.&nbsp; https://doi.org/10.1046/j.1365-294x.2000.01020.x</p>
<p>Davis, P.H., Mill, R.R. &amp; Tan, K. (1988) <em>Flora of Turkey</em> Volume 10. Edinburgh University Press, Edinburgh, pp. 186–189.</p>
<p>Drummond, A.J., Ho, S.Y.W., Phillips, M.J. &amp; Rambaut, A. (2006) Relaxed phylogenetics and dating with confidence. <em>PLoS Biology. </em>https://doi.org/10.1371/journal.pbio.0040088</p>
<p>Drummond, A.J., Suchard, M.A., Xie, D. &amp; Rambaut, A. (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. <em>Molecular Biology and Evolution</em> 29: 1969–1973.&nbsp; https://doi.org/10.1093/molbev/mss075</p>
<p>Edgar, R.C. (2004) MUSCLE: Multiple sequence alignment with high accuracy and high throughput. <em>Nucleic Acids Research</em> 32: 1792–1797.&nbsp; https://doi.org/10.1093/nar/gkh340</p>
<p>Ezard, T., Fujisawa, T. &amp; Barraclough, T. (2009) Splits: Species’ Limits by Threshold Statistics. R package version 1.0. URL: [http://R-Forge.R-project. org/projects/splits/]</p>
<p>Fujisawa, T. &amp; Barraclough, T.G. (2013) Delimiting species using single-locus data and the Generalized Mixed Yule Coalescent approach: a revised method and evaluation on simulated data sets. <em>Systematic biology</em> 62 (5): 707–724.&nbsp; https://doi.org/10.1093/sysbio/syt033</p>
<p>Fujita, M.K., Leaché, A.D., Burbrink, F.T., McGuire, J.A. &amp; Moritz, C. (2012) Coalescent-based species delimitation in an integrative taxonomy. <em>Trends in ecology &amp; evolution</em>, 27 (9): 480–488.&nbsp; https://doi.org/10.1016/j.tree.2012.04.012</p>
<p>Gadella, T. W. J. (1972) Cytological and hybridization studies in the genus <em>Symphytum</em>. <em>Symposia Biologica Hungarica</em> (Budapest) 12: 189–199</p>
<p>Gadella, T. W. &amp; Kliphuis, E. (1972) Cytotaxonomic studies in the genus <em>Symphytum</em> IV. Cytogeographic investigations in Symphytum officinale L. <em>Acta botanica neerlandica</em> 21 (2): 169–173. https://doi.org/10.1111/j.1438-8677.1972.tb00761.x</p>
<p>Gadella, T.W.J., Kliphuis, E. &amp; Perring, F.H. (1974) Cytotaxonomic studies in the genus <em>Symphytum</em>. VI. Some notes on <em>Symphytum</em> in Brıtain. <em>Acta Botanica Neerlandica</em> 23: 433–437.&nbsp; https://doi.org/10.1111/j.1438-8677.1974.tb00960.x</p>
<p>Greuter, W., Burdet, H. &amp; Long, G. (1984) <em>Med-Checklist I. </em>Genéve and Berlin.</p>
<p>Gviniašvili, C.N. (1976) <em>Kavkazskie predstaviteli roda Symphytum</em> L. Boraginaceae Jus, Tbilisi.</p>
<p>Hacıoğlu, B.T. &amp; Erik, S. (2011) Phylogeny of <em>Symphytum</em> L. (Boraginaceae) with special emphasis on Turkish species. <em>African Journal of Biotechnology </em>10: 15483–15493. https://doi.org/10.5897/AJB11.1094</p>
<p>Hamilton, M.B. (1999) Four primer pairs for the amplification of chloroplast intergenic regions with intraspecific variation. <em>Molecular Ecology</em> 8: 521–523.</p>
<p>Hassanpour, H., Zare-Maivan, H., Sonboli, A., Kazempour-Osaloo, S., Wagner, F., Tomasello, S. &amp; Oberprieler, C. (2018) Phylogenetic species delimitation unravels a new species in the genus Sclerorhachis (Rech.f.) Rech.f. (Compositae, Anthemideae). <em>Plant Systematics and Evolution</em> 304: 185–203. https://doi.org/10.1007/s00606-017-1461-4</p>
<p>Hilger, H.H., Selvi, F., Papini, A. &amp; Bigazzi, M. (2004) Molecular systematics of boraginaceae tribe boragineae based on ITS1 and trnL sequences, with special reference to Anchusa s.l. <em>Annals of Botany</em> 94: 201–212.&nbsp; https://doi.org/10.1093/aob/mch132</p>
<p>Ho, S.Y.W. (2007) Calibrating molecular estimates of substitution rates and divergence times in birds. <em>Journal of Avian Biology </em>38: 409–414.&nbsp; https://doi.org/10.1111/j.2007.0908-8857.04168.x</p>
<p>Hu, H., Al-Shehbaz, I.A., Sun, Y., Hao, G., Wang, Q. &amp; Liu, J. (2015) Species delimitation in Orychophragmus (Brassicaceae) based on chloroplast and nuclear DNA barcodes. <em>Taxon</em> 64: 714–726.&nbsp; https://doi.org/10.12705/644.4</p>
<p>Irimia, R.E., Pérez-Escobar, O.A. &amp; Gottschling, M (2015) Strong biogeographic signal in the phylogenetic relationships of <em>Rochefortia</em> Sw.(Ehretiaceae, Boraginales). <em>Plant Systematics and Evolution</em> 301 (5): 1509–1516.</p>
<p>Jackson, N.D., Carstens, B.C., Morales, A.E. &amp; O’Meara, B.C. (2017) Species delimitation with gene flow. <em>Systematic biology</em> 66 (5): 799–812.</p>
<p>Kay, K.M., Whittall, J.B. &amp; Hodges, S.A. (2006) A survey of nuclear ribosomal internal transcribed spacer substitution rates across angiosperms: An approximate molecular clock with life history effects. <em>BMC Ecology and Evolution</em> 6: 36. https://doi.org/10.1186/1471-2148-6-36</p>
<p>Kobrlová, L., HroneŠ, M., Kouteckı, P., Štech, M. &amp; Trávníček, B. (2016) <em>Symphytum tuberosum</em> complex in central Europe: Cytogeography, morphology, ecology and taxonomy. <em>Preslia</em> 88: 77–112.</p>
<p>Kobrlová, L., Mandáková, T. &amp; Hroneš, M. (2018) Taxonomic status and typification of a neglected name <em>Symphytum leonhardtianum</em> from the <em>symphytum tuberosum</em> complex (Boraginaceae). <em>Phytotaxa</em> 349 (3): 225–236.&nbsp; https://doi.org/10.11646/phytotaxa.349.3.3</p>
<p>Kurtto, A. (1982) Taxonomy of the <em>Symphytum asperum</em> aggregate (Boraginaceae), especially in Turkey. <em>Annales Botanici Fennici</em> 22: 319–331.</p>
<p>Kuznecov, N. (1910) Kavkazskie vidy roda <em>Symphytum tourn</em> L. iznacÌŒenie ich v istorii razvitija flory Kavkaza N[ikolaj] I[vanovicÌŒ] Kuznecov. S 2 tabl. ris. i 2 kart. <em>Memories l’Academie Imp. des Sci. St. Petersbg. ser. 8. Physical Review Materials </em>25: 91–94.</p>
<p>Leigh, J.W. &amp; Bryant, D. (2015) PopART: Full-feature software for haplotype network construction. <em>Methods in Ecology and Evolution</em> 6 (9): 1110–1116.&nbsp; https://doi.org/10.1111/2041-210X.12410</p>
<p>Lepechin, I.I. (1805) Symphyti asperi nova species. <em>Nova Acta Academiae Scientiarum Imperialis Petropolitanae. Praecedit Historia ejusdem Academiae </em>14 (2): 442–444.</p>
<p>Lindman, C.A.M. (1911) Über <em>Symphytum orientale</em> L. und <em>Symphytum uplandicum</em> <em>Nym. Botaniska Notiser</em>: 71–77.</p>
<p>Linnaeus, C. (1753) <em>Species Plantarum</em>. Volume 1. L. Salvius, Stockholm, 560 pp.</p>
<p>Lohse, K. (2009) Can mtDNA be used to delimit species? A response to Pons <em>et al.</em> (2006). <em>Systematic Biology </em>58: 439–442. https://doi.org/10.1093/sysbio/syp039</p>
<p>Matos-Maraví, P., Wahlberg, N., Antonelli, A. &amp; Penz, C.M. (2019) Species limits in butterflies (Lepidoptera: Nymphalidae): Reconciling classical taxonomy with the multispecies coalescent. <em>Systematic Entomology</em> 44: 745–756.&nbsp; https://doi.org/10.1111/syen.12352</p>
<p>Mayr E. (1976) Species Concepts and Definitions. <em>Topics in the Philosophy of Biology</em>. <em>Boston Studies in the Philosophy of Science</em>, vol 27. Springer, Dordrecht. pp. 353–371.&nbsp; https://doi.org/10.1007/978-94-010-1829-6_16</p>
<p>Mayr, E. (2000) The biological species concept. <em>In</em>: Wheeler, Q.D. &amp; Meier, R. (Eds.) <em>Species concepts and phylogenetic theory: a debate</em>. Columbia University Press, New York, pp. 17–29.</p>
<p>Monaghan, M.T., Wild, R., Elliot, M., Fujisawa, T., Balke, M., Inward, D.J.G., Lees, D.C., Ranaivosolo, R., Eggleton, P., Barraclough, T.G. &amp; Vogler, A.P. (2009) Accelerated species Inventory on Madagascar using coalescent-based models of species Delineation. <em>Systematic Biology</em> 58: 298–311. https://doi.org/10.1093/sysbio/syp027</p>
<p>Murín, A. &amp; Májovskı, J. (1982) Die Bedeutung der Polyploidie in der Entwicklung der in der Slowakei wachsenden Arten der Gattung Symphytum L. <em>acta botanica universitatis comenianae</em> 29: 1–25.</p>
<p>Nazaire, M., Wang, X.Q. &amp; Hufford, L. (2014) Geographic origins and patterns of radiation of Mertensia (Boraginaceae). <em>American Journal of Botany</em> 101: 104–118. https://doi.org/10.3732/ajb.1300320</p>
<p>Pawłowski B. (1961) Uwagi o żywokostach–observationes ad genus <em>Symphytum</em> L. pertinentes. <em>Fragmenta Floristica et Geobotanica Polonica</em> 7: 327–356.</p>
<p>Pawłowski, B. (1971) Symphyta mediteranea nova vel minus cognita. <em>Fragmenta Floristica et Geobotanica Polonica </em>7: 2–38.</p>
<p>Pawłowski, B. (1972) <em>Symphytum</em> L. <em>In</em>: Tutin, T.G., Heywood, V.H., Burges, N.A., Moore, D.M., Valentine, D.H., Walters, S.M. &amp; Webb, D.A. (Eds.) <em>Flora Europaea</em>. Volume 3. Cambridge University Press, Cambridge, pp. 103–105.</p>
<p>Pease, J.B. &amp; Hahn, M.W. (2013) More accurate phylogenies inferred from low-recombination regions in the presence of incomplete lineage sorting. <em>Evolution</em> 67 (8): 2376–2384.&nbsp; https://doi.org/10.1111/evo.12118</p>
<p>Pons, J., Barraclough, T.G., Gomez-Zurita, J., Cardoso, A., Duran, D.P., Hazell, S., Kamoun, S., Sumlin, W.D. &amp; Vogler, A.P. (2006) Sequence-based species delimitation for the DNA taxonomy of undescribed insects. <em>Systematic Biology </em>55: 595–609. https://doi.org/10.1080/10635150600852011</p>
<p>Posada, D. (2008) jModelTest: Phylogenetic model averaging. <em>Molecular Biology and Evolution </em>25 (7): 1253–1256.&nbsp; https://doi.org/10.1093/molbev/msn083</p>
<p>Prebble, J.M. (2016) <em>Species delimitation and the population genetics of rare plants: a case study using the New Zealand native pygmy forget-me-not group (Myosotis; Boraginaceae)</em>, a thesis presented in partial fulfilment of the requirements for the degree of Doctor of Philosophy in Plant Biology at Massey University, Manawatű, New Zealand, 269 pp.</p>
<p>Prebble, J.M., Meudt, H.M., Tate, J.A. &amp; Symonds, V.V. (2019) Comparing and co-analysing microsatellite and morphological data for species delimitation in the New Zealand native Myosotis pygmaea species group (Boraginaceae). <em>Taxon</em> 68 (4): 731–750.&nbsp; https://doi.org/10.1002/tax.12096</p>
<p>R Core Team (2020) <em>R: A language and environment for statistical computing. R A Lang. Environ. Stat. Comput. R Found. Stat. Comput. </em>Vienna, Austria.</p>
<p>Rambaut, A. &amp; Drummond, A.J. (2009) <em>Tracer v 1.5. </em>[http://beast.bio.ed.ac.uk/Tracer]</p>
<p>Rannala, B. &amp; Yang, Z. (2003) Bayes estimation of species divergence times and ancestral population sizes using DNA sequences from multiple loci. <em>Genetics </em>164: 1645–1656. https://doi.org/10.1093/genetics/164.4.1645</p>
<p>Runemark, H. (1967) Studies in the Aegean Flora XI Procopiana (Boraginaceae) included into Symphytum. <em>Botaniska Notiser</em> 120: 85–94.</p>
<p>Sandbrink, J.M., Van Brederode, J. &amp; Gadella, T.W.J. (1990) Phylogenetic relationships in the genus <em>Symphytum</em> L. (Boraginaceae). <em>Proceedings, Koninklijke Nederlandse Akademie van Wetenschappen</em> 93: 295–334.</p>
<p>Spooner, D.M. (2016) Species delimitations in plants: Lessons learned from potato taxonomy by a practicing taxonomist. <em>Journal of Systematics and Evolution</em> 54: 191–203. https://doi.org/10.1111/jse.12203</p>
<p>Suchard, M.A., Lemey, P., Baele, G., Ayres, D.L., Drummond, A.J. &amp; Rambaut, A. (2018) Bayesian phylogenetic and phylodynamic data integration using BEAST 1.10. <em>Virus Evolution </em>4: 1–5.&nbsp; https://doi.org/10.1093/ve/vey016</p>
<p>Steven, C. (1851) Observationes in Asperifolias taurico-caucasicas. <em>Bulletin de la Société Imperiale des Naturalistes de Moscou</em> 24: 558–609.</p>
<p>Taberlet, P., Gielly, L., Pautou, G. &amp; Bouvet, J. (1991) Universal primers for amplification of three non-coding regions of chloroplast DNA. <em>Plant Molecular Biology</em> 17: 1105–1109.&nbsp; https://doi.org/10.1007/BF00037152</p>
<p>Talavera, G., Dincă, V. &amp; Vila, R. (2013) Factors affecting species delimitations with the GMYC model: insights from a butterfly survey. <em>Methods in Ecology and Evolution</em> 4 (12): 1101–1110. https://doi.org/10.1111/2041-210X.12107</p>
<p>Tamura, K., Stecher, G., Peterson, D., Filipski, A. &amp; Kumar, S. (2013) MEGA6: Molecular evolutionary genetics analysis version 6.0. <em>Molecular Biology and Evolution</em> 30 (12): 2725–2729. https://doi.org/10.1093/molbev/mst197</p>
<p>Tarıkahya, B. &amp; Erik, S. (2010) Taxonomy of <em>Symphytum asperum</em> Lepech and <em>S. sylvaticum</em> Boiss (Boraginaceae) based on macro- and micro-morphology. <em>Hacettepe Journal of Biology and Chemistry</em> 38: 47–61.</p>
<p>Tarıkahya, B. (2009) <em>The revision of Turkish Symphytum L. (Boraginaceae) genus</em>. Hacettepe University.</p>
<p>Tarıkahya-Hacıoğlu, B. &amp; Erik, S. (2013) Türkiye’de yetişen <em>Symphytum</em> (Boraginaceae) taksonlarının revizyonu. <em>Ot Sistematik Botanik Dergisi </em>20: 23–72.</p>
<p>Templeton, A.R., Crandall, K.A. &amp; Sing, C.F. (1992) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation. <em>Genetics</em> 132: 619–633. https://doi.org/10.1093/genetics/132.2.619</p>
<p>WFO (2021) World Flora Online. Available from: http://www.worldfloraonline.org (accessed 5 August 2021)</p>
<p>Tutin, T.G. (1956) The genus Symphytum in Britain. <em>Watsonia</em> 3: 280–281.</p>
<p>Valdés, B. (2011) Euro+Med Plantbase - the information resource for Euro-Mediterranean plant diversity.</p>
<p>White, T.J., Bruns, T., Lee, S. &amp; Taylor, J. (1990) Amplifications and direct sequencing offungal ribosomal RNA genes for phylogenetics, <em>In</em>: Innis, M.A., Gelfand, D.H., Sninsky, J.J. &amp; White, T.J. (Eds.) <em>PCR Protocols: A Guide to Methods and Applications.</em> Academic Press, Inc., New York, pp. 315–322. https://doi.org/10.1016/B978-0-12-372180-8.50042-1</p>
<p>Wickens, G.E. (1969) Revision of <em>Symphytum</em> L. in Turkey and adjacent areas. <em>Notes from the Royal Botanic Garden, Edinburgh </em>24: 157–180.</p>
<p>Wickens, G.E. (1978) <em>Symphytum</em> L. <em>In</em>: Davis, P.H. (Ed.) <em>Flora of Turkey and the East Aegean Islands</em>, IV. Edinburgh, pp. 378–386.</p>
<p>Yang, Z. (2002) Likelihood and Bayes estimation of ancestral population sizes in hominoids using data from multiple loci. <em>Genetics</em> 162: 1811–1823. https://doi.org/10.1093/genetics/162.4.1811</p>
<p>Yang, Z. (2015) The BPP program for species tree estimation and species delimitation. <em>Current Zoology </em>61 (5): 854–865. https://doi.org/10.1093/czoolo/61.5.854</p>
<p>Yang, Z. &amp; Rannala, B. (2010) Bayesian species delimitation using multilocus sequence data. <em>Proceedings of the National Academy of Sciences</em> 107: 9264–9269.&nbsp; https://doi.org/10.1073/pnas.0913022107</p>
<p>Yang, Z. &amp; Rannala, B. (2014) Unguided species delimitation using DNA sequence data from multiple loci. <em>Molecular Biology and Evolution</em> 31: 3125–3135. https://doi.org/10.1093/molbev/msu279</p>
<p>Yule, G.U. (1925) A mathematical theory of evolution based on the conclusions of Dr. J.C. Willis, F.R.S. <em>Journal of the Royal Statistical Society</em> 213: 21–87. https://doi.org/10.2307/2341419</p>
<p>Zhang, C., Zhang, D.X., Zhu, T. &amp; Yang, Z. (2011) Evaluation of a Bayesian coalescent method of species delimitation. <em>Systematic biology</em> 60 (6): 747–761. https://doi.org/10.1093/sysbio/syr071</p>