Radiative evolution of polyploid races of the Iberian carnation Dianthus broteri (Caryophyllaceae).
*The micro-evolutionary mechanisms that drive large-scale radiations are not completely understood, partly because of a shortage of population-level studies aimed at identifying putative causes of rapid evolutionary change. The Dianthus broteri complex, representing the largest polyploid series known to date for any species in the genus (2x, 4x, 6x and 12x cytotypes), belongs to a lineage that was recently found to have diversified at unusually rapid rates. *We used a combination of genome sequencing (internal transcribed spacer (ITS), plus chloroplast DNA (cpDNA) regions trnH-psbA, psbA-trnK and trnK-matK) and amplified fragment length polymorphism (AFLP) fingerprinting in 25 populations to infer the evolutionary history of extant polyploid races. *The haplotype, ribotype and AFLP reconstructions showed a star-shaped arrangement suggesting a pattern of radiative evolution. The major, widespread haplotype occurred at all ploidy levels, whereas 20 minor haplotypes were restricted to single populations and cytotypes. In addition, AFLP analyses retrieved well-supported cytogeographic groups: six clades were clearly differentiated in terms of ploidy level and geography. Molecular data indicate that gene flow among different cytotypes is rare or nonexistent. *Our study supports a scenario of rapid diversification in carnations in which autopolyploidy and allopolyploidy, in interaction with geography and/or isolation, have played prominent roles.
Balao
Francisco
F
Departamento de Biología Vegetal y Ecología, Universidad de Sevilla, Apdo. 1095, E-41080 Sevilla, Spain.
Valente
Luis M
LM
Real Jardín Botánico de Madrid, CSIC, Plaza de Murillo 2, 28014 Madrid, Spain.
Vargas
Pablo
P
Real Jardín Botánico de Madrid, CSIC, Plaza de Murillo 2, 28014 Madrid, Spain.
Herrera
Javier
J
Departamento de Biología Vegetal y Ecología, Universidad de Sevilla, Apdo. 1095, E-41080 Sevilla, Spain.
Talavera
Salvador
S
Departamento de Biología Vegetal y Ecología, Universidad de Sevilla, Apdo. 1095, E-41080 Sevilla, Spain.
D054458:Amplified Fragment Length Polymorphism Analysis; D001499:Bayes Theorem; D005075:Biological Evolution; D029748:Caryophyllaceae / Q000235:genetics*; D018742:DNA, Chloroplast / Q000235:genetics; D021901:DNA, Intergenic / Q000235:genetics; D014644:Genetic Variation; D005828:Genetics, Population; D005843:Geography; D006239:Haplotypes / Q000235:genetics; D011123:Polyploidy; D011174:Portugal; D025341:Principal Component Analysis; D013030:Spain
D018742:DNA, Chloroplast; D021901:DNA, Intergenic
Balao F, Casimiro-Soriguer R, Talavera M, Herrera J, Talavera S. 2009. Distribution and diversity of cytotypes in Dianthus broteri as evidenced by genome size variations. Annals of Botany 104: 965-973.
Barrier M, Baldwin B, Robichaux R, Purugganan M. 1999. Interspecific hybrid ancestry of a plant adaptive radiation: allopolyploidy of the Hawaiian silversword alliance (Asteraceae) inferred from floral homeotic gene duplications. Molecular Biology and Evolution 16: 1105-1113.
Blöch C, Weiss-Schneeweiss H, Schneeweiss GM, Barfuss MHJ, Rebernig CA, Villaseñor JL, Stuessy TF. 2009. Molecular phylogenetic analyses of nuclear and plastid DNA sequences support dysploid and polyploid chromosome number changes and reticulate evolution in the diversification of Melampodium (Millerieae, Asteraceae). Molecular Phylogenetics and Evolution 53: 220-233.
Bruvo R, Michiels NK, D’Souza TG, Schulenburg H. 2004. A simple method for the calculation of microsatellite genotype distances irrespective of ploidy level. Molecular Ecology 13: 2101-2106.
Carolin RC. 1957. Cytological and hybridization studies in the genus Dianthus. New Phytologist 56: 81-97.
Cavalli-Sforza LL, Edwards AWF. 1967. Phylogenetic analysis: models and estimation procedures. Evolution 21: 550-570.
Clement M, Posada D, Crandall KA. 2000. TCS: a computer program to estimate gene genealogies. Molecular Ecology 9: 1657-1659.
Corander J, Marttinen P. 2006. Bayesian identification of admixture events using multilocus molecular markers. Molecular Ecology 15: 2833-2843.
Coyne JA, Orr H. 2004. Polyploidy and hybrid speciation. In: Coyne J, Orr H, eds. Speciation. Sunderland, MA, USA: Sinauer Associates, 321-351.
De Silva HN, Hall AJ, Rikkerink E, McNeilage MA, Fraser LG. 2005. Estimation of allele frequencies in polyploids under certain patterns of inheritance. Heredity 95: 327-334.
Demesure B, Sodzi N, Petit R. 1995. A set of universal primers for amplification of polymorphic non-coding regions of mitochondrial and chloroplast DNA in plants. Molecular Ecology 4: 129-131.
Dixon CJ. 2006. A means of estimating the completeness of haplotype sampling using the Stirling probability distribution. Molecular Ecology Notes 6: 650-652.
Doyle JJ, Doyle JL. 1987. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochemistry Bulletin 19: 11-15.
Drummond A, Ashton B, Cheung M, Heled J, Kearse M, Moir R, Stones-Havas S, Thierer T, Wilson A. 2009. Geneious v4.7. Available from http://www.geneious.com/.
Efron B, Tibshirani R. 1986. Bootstrap methods for standard errors, confidence intervals, and other measures of statistical accuracy. Statistical Science 1: 54-75.
Ehrich D. 2006. AFLPDAT: a collection of R functions for convenient handling of AFLP data. Molecular Ecology Notes 6: 603-604.
Escudero M, Vargas P, Valcarcel V, Luceño M. 2008. Strait of Gibraltar: an effective gene-flow barrier for wind-pollinated Carex helodes (Cyperaceae) as revealed by DNA sequences, AFLP, and cytogenetic variation. American Journal of Botany 95: 745-755.
Excoffier L. 2004. Patterns of DNA sequence diversity and genetic structure after a range expansion: lessons from the infinite-island model. Molecular Ecology 13: 853-864.
Excoffier L, Laval G, Schneider S. 2005. Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online 1: 47-50.
Felsenstein J. 2005. PHYLIP (Phylogeny Inference Package) version 3.6. Seattle, WA, USA: Department of Genome Sciences, University of Washington.
Gallego MJ. 1986. Una nueva especie de Dianthus del litoral del SW de España. Lagascalia 14: 71-72.
Gaudeul M. 2006. Disjunct distribution of Hypericumn nummularium L. (Hypericaceae): molecular data suggest bidirectional colonization from a single refugium rather than survival in distinct refugia. Biological Journal of the Linnean Society 87: 437-447.
Gaudeul M, Taberlet P, Till-Bottraud I. 2000. Genetic diversity in an endangered alpine plant, Eryngium alpinum L. (Apiaceae), inferred from amplified fragment length polymorphism markers. Molecular Ecology 9: 1625-1637.
Gómez A, Lunt D. 2006. Refugia within refugia: patterns of phylogeographic concordance in the Iberian Peninsula. In: Weiss S, Ferrand N, eds. Phylogeography in southern European refugia: evolutionary perspectives on the origins and conservation of European biodiversity. Dordrecht, the Netherlands: Springer, 155-182.
Guo Y-P, Saukel J, Mittermayr R, Ehrendorfer F. 2005. AFLP analyses demonstrate genetic divergence, hybridization, and multiple polyploidization in the evolution of Achillea (Asteraceae-Anthemideae). New Phytologist 166: 273-290.
Halverson K, Heard SB, Nason JD, Stireman JO. 2008. Origins, distribution, and local co-occurrence of polyploid cytotypes in Solidago altissima (Asteraceae). American Journal of Botany 95: 50-58.
Hudson RR. 2000. A new statistic for detecting genetic differentiation. Genetics 155: 2011-2014.
Johnson L, Soltis D. 1994. matK DNA sequences and phylogenetic reconstruction in Saxifragaceae s. str. Systematic Botany 19: 143-156.
Jombart T. 2008. adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24: 1403-1405.
Jordon-Thaden I, Koch M. 2008. Species richness and polyploid patterns in the genus Draba (Brassicaceae): a first global perspective. Plant Ecology & Diversity 1: 255-263.
Kadereit JW, Uribe-Convers S, Westberg E, Comes HP. 2006. Reciprocal hybridization at different times between Senecio flavus and Senecio glaucus gave rise to two polyploid species in north Africa and south-west Asia. New Phytologist 169: 431-441.
Kalinowski ST. 2004. Counting alleles with rarefaction: private alleles and hierarchical sampling designs. Conservation Genetics 5: 539-543.
Kalinowski ST. 2005. HP-RARE 1.0: a computer program for performing rarefaction on measures of allelic richness. Molecular Ecology Notes 5: 187-189.
Koch MA, Kiefer C, Ehrich D, Vogel J, Brochmann C, Mummenhoff K. 2006. Three times out of Asia Minor: the phylogeography of Arabis alpina L. (Brassicaceae). Molecular Ecology 15: 825-839.
Lammerts W. 1931. Interspecific hybridization in Nicotiana. XII. The amphidiploid rustica-paniculata hybrid; its origin and cytogenetic behavior. Genetics 16: 191.
Leitch AR, Leitch IJ. 2008. Genomic plasticity and the diversity of polyploid plants. Science 320: 481-483.
Librado P, Rozas J. 2009. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25: 1451-1452.
Linder HP. 2008. Plant species radiations: where, when, why? Philosophical Transactions of the Royal Society B: Biological Sciences 363: 3097-3105.
Liston A, Robinson W, Oliphant J, Alvarez-Buylla E. 1996. Length variation in the nuclear ribosomal DNA internal transcribed spacer region of non-flowering seed plants. Systematic Botany 21: 109-120.
Marhold K, Lihová J. 2006. Polyploidy, hybridization and reticulate evolution: lessons from the Brassicaceae. Plant Systematics and Evolution 259: 143-174.
Médail F, Diadema K. 2009. Glacial refugia influence plant diversity patterns in the Mediterranean Basin. Journal of Biogeography 36: 1333-1345.
Obbard DJ, Harris SA, Pannell JR. 2006. Simple allelic-phenotype diversity and differentiation statistics for allopolyploids. Heredity 97: 296-303.
Oksanen J, Blanchet FG, Kindt R, Legendre P, O’Hara RG, Simpson GL, Solymos P, Henry M, Stevens H, Wagner H. 2010. vegan: community ecology package. R package version 1.17-2. Available from http://CRAN.R-project.org/package=vegan/.
Ortiz MA, Tremetsberger K, Talavera S, Stuessy T, Garcia-Castano JL. 2007. Population structure of Hypochaeris salzmanniana DC. (Asteraceae), an endemic species to the Atlantic coast on both sides of the Strait of Gibraltar, in relation to Quaternary sea level changes. Molecular Ecology 16: 541-552.
Otto SP. 2007. The evolutionary consequences of polyploidy. Cell 131: 452-462.
Parisod C, Holderegger R, Brochmann C. 2010. Evolutionary consequences of autopolyploidy. New Phytologist 186: 5-17.
Paun O, Forest F, Fay MF, Chase MW. 2009. Hybrid speciation in angiosperms: parental divergence drives ploidy. New Phytologist 182: 507-518.
Paun O, Schönswetter P, Winkler M, Tribsch A, Intrabiodiv Consortium. 2008. Historical divergence vs. contemporary gene flow: evolutionary history of the calcicole Ranunculus alpestris group (Ranunculaceae) in the European Alps and the Carpathians. Molecular Ecology 17: 4263-4275.
Paun O, Stuessy TF, Horandl E. 2006. The role of hybridization, polyploidization and glaciation in the origin and evolution of the apomictic Ranunculus cassubicus complex. New Phytologist 171: 223-236.
Petit RJ, Brewer S, Bordács S, Burg K, Cheddadi R, Coart E, Cottrell J, Csaikl UM, van DamB, Deans JD et al. 2002. Identification of refugia and post-glacial colonisation routes of European white oaks based on chloroplast DNA and fossil pollen evidence. Forest Ecology and Management 156: 49-74.
R Development Core Team. 2008. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
Ramsey J, Robertson A, Husband B. 2008. Rapid adaptive divergence in new world Achillea, an autopolyploid complex of ecological races. Evolution 62: 639-653.
Ramsey J, Schemske DW. 1998. Pathways, mechanisms, and rates of polyploid formation in flowering plants. Annual Reviews in Ecology and Systematics 29: 467-501.
Ramsey J, Schemske DW. 2002. Neopolyploidy in flowering plants. Annual Review of Ecology and Systematics 33: 589-639.
Ray N, Currat M, Excoffier L. 2003. Intra-deme molecular diversity in spatially expanding populations. Molecular Biology and Evolution 20: 76-86.
Rogers A, Harpending H. 1992. Population growth makes waves in the distribution of pairwise genetic differences. Molecular Biology and Evolution 9: 552-569.
Salvador L, Alía R, Agúndez D, Gil L. 2000. Genetic variation and migration pathways of maritime pine (Pinus pinaster Ait) in the Iberian Peninsula. Theoretical and Applied Genetics 100: 89-95.
Schönswetter P, Tribsch A. 2005. Vicariance and dispersal in the alpine perennial Bupleurum stellatum L. (Apiaceae). Taxon 54: 725-732.
Segraves KA, Thompson JN, Soltis PS, Soltis DE. 1999. Multiple origins of polyploidy and the geographic structure of Heuchera grossulariifolia. Molecular Ecology 8: 253-262.
Soltis DE, Albert VA, Leebens-Mack J, Bell CD, Paterson AH, Zheng C, Sankoff D, dePamphilis CW, Wall PK, Soltis PS. 2009. Polyploidy and angiosperm diversification. American Journal of Botany 96: 336-348.
Soltis DE, Soltis PS. 1999. Polyploidy: recurrent formation and genome evolution. Trends in Ecology & Evolution 14: 348-352.
Soltis PS, Soltis DE. 2000. The role of genetic and genomic attributes in the success of polyploids. Proceedings of the National Academy of Sciences, USA 97: 7051-7057.
Soltis PS, Soltis DE. 2009. The role of hybridization in plant speciation. Annual Review of Plant Biology 60: 561-588.
Valente LM, Savolainen V, Vargas P. 2010. Unparalleled rates of species diversification in Europe. Proceedings of the Royal Society B: Biological Sciences 277: 1489-1497.
Vekemans X, Beauwens T, Lemaire M, Roldan-Ruiz I. 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. Molecular Ecology 11: 139-151.
Verheyen E, Salzburger W, Snoeks J, Meyer A. 2003. Origin of the superflock of cichlid fishes from Lake Victoria, East Africa. Science 300: 325-329.
Weiss H, Dobes C, Schneeweiss GM, Greimler J. 2002. Occurrence of tetraploid and hexaploid cytotypes between and within populations in Dianthus sect. Plumaria (Caryophyllaceae). New Phytologist 156: 85-94.
White T, Bruns T, Lee S, Taylor J. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis M, Gelfand D, Sninsky J, White T, eds. PCR protocols: a guide to methods and applications. San Diego, CA, USA: Academic Press, 315-322.
Wood TE, Takebayashi N, Barker MS, Mayrose I, Greenspoon PB, Rieseberg LH. 2009. The frequency of polyploid speciation in vascular plants. Proceedings of the National Academy of Sciences, USA 106: 13875-13879.