Phylogenetic relationships of Erysimum (Brassicaceae) from the Baetic Mountains (SE Iberian Peninsula)
DOI:
https://doi.org/10.3989/ajbm.2377Keywords:
cpDNA, flower colour, nDNA, Erysimum nevadense group, secondary contactAbstract
The Baetic mountains, located in the southern Iberian Peninsula, is a major hotspot of biodiversity in the Mediterranean Basin, constituting one of the most important glacial refugia for vascular plants in Europe. Despite their relatively limited extension, the Baetic Mountains contain almost 50% of the total endemic Erysimum species in the Iberian Peninsula. The broadly distributed Erysimum genus has diversified profusely in the Mediterranean region, with more than a hundred species described in the area, out of a total of c. 200 species included in the genus. We used two plastid DNA regions (ndhF and trnT-L) and one nuclear DNA region (ITS1-5.8S rDNA-ITS2), with 3,556 bp total length, to carry out phylogenetic analysis by Bayesian inference, maximum likelihood and maximum parsimony, in order to explore the evolutionary relationships between the Erysimum species inhabiting these ranges. Analyses of concatenated sequences from the two genomes identified two main clades with no overlap in species composition so that samples from the same species fell within the same major clade. The phylogenetic relationships depicted by those two clades do not give support to the E. nevadense group, previously proposed on taxonomic grounds. In addition, our results indicated recurrent changes in flower colour in the Baetic Erysimum species although, alternatively, reticulate evolution, which is suggested by incongruent position of taxa in the different trees, may have also affected this trait.
Downloads
References
Abdelaziz, M., Lorite, J., Muñoz-Pajares, A.J., Herrador, M.B., Perfectti, F. & Gómez, J.M. 2011. Using complementary techniques to distinguish cryptic species: A new Erysimum (Brassicaceae) species from North Africa. American Journal of Botany 98: 1049-1060. http://dx.doi.org/10.3732/ajb.1000438
Abdelaziz, M. 2013. How species are evolutionarily maintained: Pollinator-mediated divergence and hybridization in Erysimum mediohispanicum and E. nevadense. PhD thesis.
Al-Shehbaz, I.A. 2012. A generic and tribal synopsis of the Brassicaceae (Cruciferae). Taxon 61: 931-954.
Al-Shehbaz, I.A., Beilstein, M.A. & Kellogg, E.A. 2006. Systematics and phylogeny of the Brassicaceae (Cruciferae): An overview. Plant Systematics and Evolution 259: 89-120. http://dx.doi.org/10.1007/s00606-006-0415-z
Ancev, M. 2006. Polyploidy and hybridization in Bulgarian Brassicaceae: Distribution and evolutionary role. Phytologia Balcanica 12: 357-366.
Ball, P.W. 1990. Notes on the genus Erysimum L. in Europe. Botanical Journal of the Linnean Society 103: 200-213.
Blanca, G., Morales C. & Ruiz-Rejón, M. 1992. El género Erysimum L. (CRUCIFERAE) en Andalucía (España). Anales del Jardín Botánico de Madrid 49: 201-214.
Blanca, G., Cueto, M., Martínez-Lirola, M.J. & Molero-Mesa, J. 1998. Threatened vascular flora of Sierra Nevada (Southern Spain). Biological Conservation 86: 269-285. http://dx.doi.org/10.1016/S0006-3207(97)00169-9
Blanca, G., Cabezudo, B., Cueto, M., Fernández López, C. & Morales Torres, C. 2009, eds. Flora vascular de Andalucia Oriental. Vol. 3: Rosaceae-Lentibulariaceae. Consejeria de Medio Ambiente. Junta de Andalucia. Sevilla. Spain
Cansaran, A., Ergen Akaçin, O. & Kandemira, N. 1997. Study on the Morphology, Anatomy and Autecology of Erysimum amasianum Hausskn. & Bornm. (Brassicaceae) Distributed in Central Black Sea Region (Amasya-Turkey). International Journal of Science and Technology 2: 13-24.
Castresana, J. 2000. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular Biology and Evolution 17: 540-552. http://dx.doi.org/10.1093/oxfordjournals.molbev.a026334
Clot, B. 1992. Caryosystématique de quelques Erysimum L. dans le nord de la Péninsule Ibérique. Anales del Jardín Botánico de Madrid 49: 215-229.
Couvreur, T.L.P., Franzke, A., Al-Shehbaz, I.A., Bakker, F.T., Koch, M.A. & Mummenhoff, K. 2010. Molecular Phylogenetics, Temporal Diversification, and Principles of Evolution in the Mustard Family (Brassicaceae). Molecular Biology and Evolution 27: 55-71. http://dx.doi.org/10.1093/molbev/msp202
Davies, K.M., Bloor, S.J., Spiller, G.B. & Deroles, S.C. 1998. Production of yellow colour in flowers: redirection of flavonoid biosynthesis in Petunia. The Plant Journal 13: 259-266. http://dx.doi.org/10.1046/j.1365-313X.1998.00029.x
Dick, C.A., Buenrostro, J., Butler, T., Carlson, M.L., Kliebenstein, D.J. & Whittall, J.B. 2011. Arctic mustard flower color polymorphism controlled by petal-specific down-regulation at the threshold of the anthocyanin biosynthetic pathway. PLoS ONE 6: e18230. http://dx.doi.org/10.1371/journal.pone.0018230
Domínguez, F., Galicia, D., Moreno-Rivero, L., Moreno-Sáiz, J.C. & Saínz-Ollero, H. 1996. Threatened plants in Peninsular and Balearic Spain: a Favarger, C. 1978. Un example de variation cytogeographique: Le complexe de L'Erysimum grandiflorum-sylvestre. Anales del Instituto Botánico A. J. Cavanilles 35: 361-398.
report based on the EU Habitats Directive. Biological Conservation 76: 123-133. http://dx.doi.org/10.1016/0006-3207(95)00107-7
Feliner, G.N. & Rosselló J.A. 2007. Better the devil you know? Guidelines for insightful utilization of nrDNA ITS in species-level evolutionary studies in plants. Molecular Phylogenetics and Evolution 44: 911-919. http://dx.doi.org/10.1016/j.ympev.2007.01.013
Felsenstein, J. 1973. Maximum likelihood and minimum-steps methods for estimating evolutionary trees from data on discrete characters. Systematic Zoology 22: 240-249. http://dx.doi.org/10.2307/2412304
Felsenstein, J. 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39: 783-791. http://dx.doi.org/10.2307/2408678
Gavrilets, S. 2004. Fitness landscapes and the origins of species. Princeton University Press, Princeton, NJ.
Gómez, J.M., Muñoz-Pajares, A.J., Abdelaziz, M., Lorite, J. & Perfectti, F. 2014a. Evolution of pollination niches and floral divergence in the generalist plant Erysimum mediohispanicum. Annals of Botany 113: 237-249. http://dx.doi.org/10.1093/aob/mct186
Gómez, J.M., Perfectti, F. & Klingenber, C. 2014b. The role of pollinators in the evolution of corolla shape integration in a pollination-generalist plant clade. Philosophical Transactions of the Royal Society B 369: 20130257. http://dx.doi.org/10.1098/rstb.2013.0257
Gómez, J.M., Perfectti, F., Abdelaziz, M., Lorite, J., Múñoz-Pajares, A.J. & Valverde J. 2014c. Evolution of pollination niches in a generalist plant clade. New Phytologist 205, 2015: 440-453. http://dx.doi.org/10.1111/nph.13016
Greuter, W., Burdet, H.M. & Long, G. 1986. Med-checklist 3, Dicotyledones (Convolvulaceae-Labiatae). Conservatoire et Jardin botaniques de la Ville de Genève. Genève, Italy.
Guindon, S. & Gascuel, O. 2003. A simple, fast and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52: 696-704. http://dx.doi.org/10.1080/10635150390235520
Hall, T.A. 1999. BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41: 95-98.
Heywood, V.H. 1954. Notulae criticae ad floram hispaniae pertinentes, I. Bulletin of the British Museum (Natural History), Botany 1: 81-122.
Kevan, P.G. 1972. Floral colors in the high arctic with reference to insect-flower relations and pollination. Canadian Journal of Botany 50: 2289- 2316. http://dx.doi.org/10.1139/b72-298
Koch, M.A. & Al-Shehbaz, I.A. 2008. Molecular systematics and evolution of "wild" crucifers (Brassicaceae or Cruciferae). In P. K. Gupta [ed.], Biology and breeding of crucifers. 1-19. Taylor and Francis, London, UK.
Larkin, M.A., Blackshields, G., Brown, N.P., Chenna, R., McGettigan, P.A., McWilliam, H., Valentin, F., Wallace, I.M., Wilm, A., Lopez, R., Thompson, J.D., Gibson, T.J. & Higgins, D.G. 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947-2948. http://dx.doi.org/10.1093/bioinformatics/btm404
Lavergne, S., Hampe, A. & Arroyo, J. 2012. In and out of Africa: how did the Strait of Gibraltar affect plant species migration and local diversification? Journal of Biogeography 39: 204-214.
Legendre, P. & Lapointe, F.J. 2004. Assessing the congruence among distance matrices: single malt Scotch whiskies revisited. Australian and New Zealand Journal of Statistics 46: 615-629. http://dx.doi.org/10.1111/j.1467-842X.2004.00357.x
Linder, C.R. & Rieseberg L.H. 2004. Reconstructing patterns of reticulate evolution in plants. American Journal of Botany 91: 1700-1708. http://dx.doi.org/10.3732/ajb.91.10.1700
Lonergan, L. & White, N. 1997. Origin of the Betic-Rif mountain belt. Tectonics 16: 504-522. http://dx.doi.org/10.1029/96TC03937
Marhold, K. & Lihová, J. 2006. Polyploidy, hybridization and reticulate evolution: lessons from the Brassicaceae. Plant Systematics and Evolution 259: 143-174. http://dx.doi.org/10.1007/s00606-006-0417-x
Médail, F. & Diadema, K. 2009. Glacial refugia influence plant diversity patterns in the Mediterranean basin. Journal of Biogeography 36: 1222-1345. http://dx.doi.org/10.1111/j.1365-2699.2008.02051.x
Médail, F. & Quézel, P. 1999. Biodiversity Hotspots in the Mediterranean Basin: Setting Global Conservation Priorities. Conservation Biology 13: 1510-1513. http://dx.doi.org/10.1046/j.1523-1739.1999.98467.x
Medina-Cazorla, J.M., Garrido-Becerra, J.A., Mendoza Fernández, A., Pérez-García, F.J., Salmerón, E., Gil, C. & Mota Poveda, J.F. 2010. Biogeography of the Baetic mountains (SE Spain): A historical approach using cluster and parsimony analyses of endemic dolomitophytes. Plant Biosystems 144: 111-120. http://dx.doi.org/10.1080/11263500903367983
Moazzeni, H., Zarre, S., Pfeil, B.E., Bertrand, Y., German, D.A., Al-Shehbaz, I. A., Mummenhoff, K. & Oxekman, B. 2014. Phylogenetic perspectives on diversification, biogeography and character evolution in the species-rich genus Erysimum (Erysimeae; Brassicaceae) based on a densely sampled ITS approach. Botanical Journal of the Linnean Society 175: 497-522. http://dx.doi.org/10.1111/boj.12184
Muñoz-Pajares, A.J. 2013. Erysimum mediohispanicum at the evolutionary crossroad: Phylogeography, phenotype, and pollinators. PhD thesis.
Nieto Feliner, G. 1991. Breeding systems and related floral traits in several Erysimum (Cruciferae). Canadian Journal of Botany 69 : 2515-2521. http://dx.doi.org/10.1139/b91-313
Nieto Feliner, G. 1992a. Los Erysimum orófilos nevadenses de flor amarilla y purpureo-violácea: ¿son coespecíficos? Anales delJardín Botánico de Madrid 50: 272-274.
Nieto Feliner, G. 1992b. Life-form and systematics in the Iberian Erysimum (Cruciferae). Anales del Jardín Botánico de Madrid 49: 303-308.
Nieto Feliner, G. 1992c. Multivariate and cladistic analyses of the purpleflowered species of Erysimum (Cruciferae) from the Iberian Peninsula. Plant Systematics and Evolution 180: 15-28. http://dx.doi.org/10.1007/BF00940395
Nieto Feliner, G. 1993. Erysimum L. In: Castroviejo, S. & al. (eds.), Flora iberica. Vol. IV. Cruciferae-Monotropaceae: 48-76. Real Jardín Botánico, CSIC. Madrid.
Nylander, J.A.A. 2004. MrModeltest v2 [computer program]. Evolutionary Biology Center, Uppsala University, Uppsala, Sweden.
Olmstead, R.G. & Sweere, J.A. 1994. Combining data in phylogenetic systematics: An empirical approach using three molecular data sets in the Solanaceae. Systematic Biology 43: 467-481. http://dx.doi.org/10.1093/sysbio/43.4.467
Ono, E., Fukuchi-Mizutani, M., Nakamura, N., Fukui, Y., Yonekura-Sakakibara, K., Yamaguchi, M., Nakayama, T., Tanaka, T., Kusumi, T. & Tanaka, Y. 2006. Yellow flowers generated by expression of the aurone biosynthetic pathway. Proceeding of the National Academy of Sciences, USA 103: 11075-11080. http://dx.doi.org/10.1073/pnas
Paradis, E., Claude, J. & Strimmer, K. 2004. APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20: 289-290. http://dx.doi.org/10.1093/bioinformatics/btg412
Polatschek, A. 1975. Die Gattung Erysimum auf den Kapverden, Kanaren und Madeira. Annalen des Naturhistorisches Museum inWien 80: 93-103.
Polatschek, A. 1982. Erysimum. - In Pignatti, S., (ed.): Flora d'Italia 1: 382-389. Bologna: Edagricole. Italy.
Polatschek, A. 1986. Erysimum. In A. Strid [ed.], Mountain flora of Greece, l: 239-247. Cambridge University Press, Cambridge, UK.
Polatschek, A. 2010. Revision der Gattung Erysimum (Cruciferae)-Teil 1-Russland, die Nachfolgestaaten der USSR (excl. Georgien, Armenien, Azerbaidzan), China, Indien, Pakistan, Japan und Korea. Annalen des Naturhistorisches Museum inWien. 111: 181-275.
Polatschek, A. 2011. Revision der gattung Erysimum (Cruciferae), Teil 2: Georgien, Armenien, Azerbaidzan, Türkei, Syrien, Libanon, Israel, Jordanien, Irak, Iran, Afghanistan. Annalen des Naturhistorisches Museum inWien 112: 369-497.
Posada, D. & Crandall, K.A. 1998. MODELTEST: Testing the model of DNA substitution. Bioinformatics 14: 817-818. http://dx.doi.org/10.1093/bioinformatics/14.9.817
Quézel, P., & Médail, P. 1995. La région circum-méditerranéene, centre mondial majeur de biodiversité végétale. Actes des 6èmes rencontres de L′Agence Régionale pour L′Environnmentn Provence-Alpes-Côte D′Azur. Colloque Scientifique Internationale BioMes.
Rambaut, A. & Drummond, A.J. 2007. Tracer v1.4 [computer program]. URL: http://beast.bio.ed.ac.uk/Tracer
R Development Core Team. 2011. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available at http://www.R-project.org
Rodríguez-Sánchez, F., Pérez-Barrales, R., Ojeda, F., Vargas, P. & Arroyo, J. 2008. The Strait of Gibraltar as a melting pot for plant biodiversity. Quaternary Science Reviews 27: 2100-2117. http://dx.doi.org/10.1016/j.quascirev.2008.08.006
Ronquist, F. & Huelsenbeck, J. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572-1574. http://dx.doi.org/10.1093/bioinformatics/btg180
Sainz-Ollero, H. & Hernández-Bermejo, J.E. 1985. Sectorización fitogeográfica de la Península Ibérica e Islas Baleares: la contribución de su endemoflora como criterio de semejanza. Candollea 40: 485-508.
Swofford, D.L. 2002. PAUP*: Phylogenetic analysis using parsimony (*and other methods), beta version 4.0. Sinauer, Sunderland, Massachusetts, USA.
Taberlet, P., Gielly, L., Pautou, G. & Bouvet, J. 1991. Universal primers for amplification of three non-coding regions of chloroplast DNA. Plant Molecular Biology 17: 1105-1109. http://dx.doi.org/10.1007/BF00037152
Taiyan, Z., Lianli, L., Guang, Y., Dorofeyev, V. I. & Al-Shehbaz, I. A. 2001. Erysimum. Flora of China 8: 163-169.
Tamura, K., Dudley, J., Nei, M. & Kumar, S. 2007. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24: 1596-1599. http://dx.doi.org/10.1093/molbev/msm092
Thompson, J.D., Higgins, D.G. & Gibson, T.J. 1994. CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment trough sequence weighting, position specific gap penalties and weight matrix choice. Nucleic Acids Research 22: 4673-4680. http://dx.doi.org/10.1093/nar/22.22.4673
Turner, B.L. 2006. Taxonomy and nomenclature of the Erysimum asperum-E. capitatum complex (Brassicaceae). Phytologia 88: 279-287.
Van Oppen, M.J.H., McDonald, B.J., Willis, B. & Miller, D.J. 2001. The Evolutionary History of the Coral Genus Acropora (Scleractinia, Cnidaria) Based on a Mitochondrial and a Nuclear Marker: Reticulation, Incomplete Lineage Sorting, or Morphological Convergence? Molecular Biology and Evolution 18: 1315-1329. http://dx.doi.org/10.1093/oxfordjournals.molbev.a003916
Warwick, S.I., Francis, A. & Al-Shehbaz, I.A. 2006. Brassicaceae: Species checklist and database on CD-ROM. Plant Systematics and Evolution 259: 249-258. http://dx.doi.org/10.1007/s00606-006-0421-1
White, T.J., Bruns, T., Lee, S. & Taylor, J.W. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In M.A. Innis, D.H. Gelfand, J.J. Sninsky, and T.J. White [eds.], PCR protocols: A guide to methods and applications. San Diego Academic Press, San Diego, California, USA.
Yang, Z. & Rannala, B. 1997. Bayesian phylogenetic inference using DNA sequences: A Markov chain Monte Carlo method. Molecular Biology and Evolution 14: 717-724. http://dx.doi.org/10.1093/oxfordjournals.molbev.a025811
Downloads
Published
How to Cite
Issue
Section
License
Copyright (c) 2014 Consejo Superior de Investigaciones Científicas (CSIC)

This work is licensed under a Creative Commons Attribution 4.0 International License.
© CSIC. Manuscripts published in both the print and online versions of this journal are the property of the Consejo Superior de Investigaciones Científicas, and quoting this source is a requirement for any partial or full reproduction.
All contents of this electronic edition, except where otherwise noted, are distributed under a Creative Commons Attribution 4.0 International (CC BY 4.0) licence. You may read the basic information and the legal text of the licence. The indication of the CC BY 4.0 licence must be expressly stated in this way when necessary.
Self-archiving in repositories, personal webpages or similar, of any version other than the final version of the work produced by the publisher, is not allowed.