Plant Systematics and Evolution

, Volume 284, Issue 3–4, pp 171–185 | Cite as

Extended phylogeny of Aquilegia: the biogeographical and ecological patterns of two simultaneous but contrasting radiations

  • Jesús M. Bastida
  • Julio M. AlcántaraEmail author
  • Pedro J. Rey
  • Pablo Vargas
  • Carlos M. Herrera
Original Article


Studies of the North American columbines (Aquilegia, Ranunculaceae) have supported the view that adaptive radiations in animal-pollinated plants proceed through pollinator specialisation and floral differentiation. However, although the diversity of pollinators and floral morphology is much lower in Europe and Asia than in North America, the number of columbine species is similar in the three continents. This supports the hypothesis that habitat and pollinator specialisation have contributed differently to the radiation of columbines in different continents. To establish the basic background to test this hypothesis, we expanded the molecular phylogeny of the genus to include a representative set of species from each continent. Our results suggest that the diversity of the genus is the result of two independent events of radiation, one involving Asiatic and North American species and the other involving Asiatic and European species. The ancestors of both lineages probably occupied the mountains of south-central Siberia. North American and European columbines are monophyletic within their respective lineages. The genus originated between 6.18 and 6.57 million years (Myr) ago, with the main pulses of diversification starting around 3 Myr ago both in Europe (1.25–3.96 Myr ago) and North America (1.42–5.01 Myr ago). The type of habitat occupied shifted more often in the Euroasiatic lineage, while pollination vectors shifted more often in the Asiatic-North American lineage. Moreover, while allopatric speciation predominated in the European lineage, sympatric speciation acted in the North American one. In conclusion, the radiation of columbines in Europe and North America involved similar rates of diversification and took place simultaneously and independently. However, the ecological drivers of radiation were different: geographic isolation and shifts in habitat use were more important in Europe while reproductive isolation linked to shifts in pollinator specialisation additionally acted in North America.


Adaptive radiation Allopatric speciation Columbines Habitat specialisation Historical contingency Pollination syndromes Sympatric speciation 



We are grateful to the many botanical gardens (listed in Appendix 1) that provided plant material used in this study. Emilio Cano (Real Jardín Botánico de Madrid) generously offered assistance in molecular techniques. This work was supported by the Spanish Ministerio de Educación y Ciencia (projects BOS2003-03979-C02/01-02 and CGL2006-02848). During this work J.M.B. was supported with grant BES-2004-3387 of Spanish MEC. We thank Zhi Duan Chen and Wei Wang for kindly providing the molecular sequences for some of the outgroup taxa used in our study.

Supplementary material

606_2009_243_MOESM1_ESM.doc (73 kb)
Supplementary material 1 (DOC 73 kb)
606_2009_243_MOESM2_ESM.doc (38 kb)
Supplementary material 2 (DOC 37 kb)
606_2009_243_MOESM3_ESM.doc (249 kb)
Supplementary material 3 (DOC 249 kb)


  1. Alfaro ME, Zoller S, Lutzoni F (2003) Bayes or bootstrap: a simulation study comparing the performance of Bayesian Markov Chain Monte Carlo sampling and boostrapping in assessing phylogenetic confidence. Mol Biol Evol 20:255–266CrossRefPubMedGoogle Scholar
  2. Anderson CL, Bremer K, Friis EM (2005) Dating phylogenetically basal eucots using rbcl sequences and multiple fossil reference points. Am J Bot 92:1737–1748CrossRefGoogle Scholar
  3. Arrigoni PV (2006) Flora dell’Isola di Sardegna, vol 1. Carlo Delfino, SassariGoogle Scholar
  4. Bacchetta G, Iiriti G, Mossa L, Pontecorvo C, Serra G (2004) A phytosociological study of the Ostrya carpinifolia Scop. woods in Sardinia (Italy). Fitosociologia 41:67–75Google Scholar
  5. Barrclough TG, Vogler AP, Harvey PH (1998) Revealing the factors that promote speciation. Phil Trans R Soc Lond B 353:241–249CrossRefGoogle Scholar
  6. Beardsly PM, Schoening CB, Whittall JB, Olmstead RG (2004) The radiation of Mimulus in the western North America: systematic, hybridization, chromosomal evolution, cryptic biobiversity, and patterns of rarity. Am J Bot 91:474–489CrossRefGoogle Scholar
  7. Birks HJB, Willis KJ (2008) Alpines, trees and refugia in Europe. Plant Ecol Divers 1:147–160CrossRefGoogle Scholar
  8. Bochenski Z, Bochenski ZM (2008) An old world hummingbird from the Oligocene: a new fossil from Polish Carpathians. J Ornith 149:211–216CrossRefGoogle Scholar
  9. Bollback JP (2006) SIMMAP: stochastic character mapping of discrete traits on phylogenies. Bioinformatics 7:1–17CrossRefGoogle Scholar
  10. Chase VC, Raven PH (1975) Evolutionary and ecological relationship between Aquilegia formosa and Aquilegia pubescens (Ranunculaceae): two perennial plants. Evolution 29:474–486CrossRefGoogle Scholar
  11. Comes HP, Kadereit JW (2003) Spatial and temporal patterns in the evolution of the flora of the European Alpine system. Taxon 52:451–462CrossRefGoogle Scholar
  12. Damerval C, Nadot S (2007) Evolution of perianth and stamen characteristics with respect to floral symmetry in Ranunculales. Ann Bot 100:631–640Google Scholar
  13. Díaz Gonzáles TE (1986) “G. Aquilegia”. In: Castroviejo et al. (eds) Flora Ibérica. Real Jardín Botánico, C.S.I.C, MadridGoogle Scholar
  14. Drummond AJ, Ho SYW, Phillips MJ, Rambaut A (2006) Relaxed phylogentics and dating with confidence. PLoS Biol 4:e88CrossRefPubMedGoogle Scholar
  15. Drumond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214CrossRefGoogle Scholar
  16. Ellis AG, Weis AE, Gaut BS (2006) Evolutionary radiations of “stone plants” in the genus Argyroderma (Aizoaceae): unravelling the effects of landscape, habitat and flowering time. Evolution 60:39–55PubMedGoogle Scholar
  17. Farris JS, Källersjö M, Kluge AG, Bult C (1994) Testing significance of incongruence. Cladistics 10:315–319CrossRefGoogle Scholar
  18. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791CrossRefGoogle Scholar
  19. Felsenstein J (1988) Phylogenies from molecular sequences: inference and reliability. Annu Rev Genet 22:521–565CrossRefPubMedGoogle Scholar
  20. Francisco-Ortega J, Jansen RK, Santos-Guerra A (1996) Chloroplast DNA evidence of colonization, adaptive radiation, and hybridization in the evolution of the Macaronesian flora. Proc Natl Acad Sci USA 93:4085–4090CrossRefPubMedGoogle Scholar
  21. Francisco-Ortega J, Crawford DJ, Santos-Guerra A, Jansen RK (1997) Origin and evolution of Argyranthemum (Asteraceae: Anthemideae) in Macaronesia. In: Givnish TJ, Sytsma KJ (eds) Molecular evolution and adaptive radiation. Cambridge University Press, Cambridge, pp 406–431Google Scholar
  22. Francisco-Ortega J, Fuertes-Aguilar J, Gómez-Campo C, Santos-Guerra A, Jansen RK (1999) ITS sequence phylogeny of Crambe L. (Brassicaceae): molecular data reveal two old world disjunctions. Mol Phyl Evol 11:361–380CrossRefGoogle Scholar
  23. Fu D, Li L, Bartholomew B, Brach AR, Dutton BE, Gilbert MG, Kadota Y, Robinson OR, Tamura M, Warnock MJ, Guanghua Z, Ziman SN (2001) Ranunculaceae. In: Wu Z, Raven PH, Hong D (eds) Flora of China, vol. 6. Missouri Botanical Garden Press, St. Louis, pp 133–148Google Scholar
  24. Fulton M, Hodges SA (1999) Floral isolation between Aquilegia formosa and Aquilegia pubescens. Proc R Soc Lond B 266:2247–2252CrossRefGoogle Scholar
  25. Gafta D, Muncaciu S, Csergö A-M (2006) Morphometric variation in a rare endemic Aquilegia (Ranunculaceae) in the Carpathians. Plant Biosyst 140:297–306CrossRefGoogle Scholar
  26. García-Maroto F, Mañas-Fernández A, Garrido-Cárdenas JA, López Alonso D, Guil-Guerrero JL, Guzmán B, Vargas P (2009) Δ6-Desaturase sequence evidence for explosive Pliocene radiations within the adaptive radiation of Macaronesian Echium (Boraginaceae). Mol Phyl Evol 52:563–574CrossRefGoogle Scholar
  27. Givnish TJ, Montgomery RA, Goldstein G (2004) Adaptive radiation of photosynthetic physiology in the Hawaiian lobeliads: light regimes, static light responses, and whole-plant compensation points. Am J Bot 91:228–246CrossRefGoogle Scholar
  28. Grant V (1993) Origin of floral isolation between ornithophilous and sphingophilous plant species. Proc Natl Acad Sci USA 90:7729–7730CrossRefPubMedGoogle Scholar
  29. Grant V (1994) Historical development of ornithophily in the western North American flora. Proc Natl Acad Sci USA 91:10407–10411CrossRefPubMedGoogle Scholar
  30. Grant V, Grant KA (1965) Flower pollination in the phlox family. Columbia University Press, New YorkGoogle Scholar
  31. Guzmán B, Lledó MD, Vargas P (2009) Adaptive radiation in Mediterranean Cistus. PLoS One 4:1–13CrossRefGoogle Scholar
  32. Hall TA (1999) BioEdit: a user-friendly biological sequence alignmeant edition and analysis program for Windows 95/98/NT. Nucleid Acids Symp Ser 41:95–98Google Scholar
  33. Hamilton MB (1999) Four primers pairs for the amplification of chloroplast intergenic regions with intraspecific variation. Mol Ecol 8:521–523PubMedGoogle Scholar
  34. Herrera CM, García IM, Pérez R (2008) Invisible floral larcenies: microbial communities degrade floral nectar of bumble bee-pollinated plants. Ecology 89:2369–2376CrossRefPubMedGoogle Scholar
  35. Hodges SA (1994) Floral and ecological isolation between Aquilegia formosa and Aquilegia pubescens. Proc Natl Acad Sci USA 91:2493–2496CrossRefPubMedGoogle Scholar
  36. Hodges SA (1997) Floral nectar spurs and diversification. Int J Plant Sci 158:S81–S88CrossRefGoogle Scholar
  37. Hodges SA, Arnold ML (1994) Columbines: a geographically widespread species flock. Proc Natl Acad Sci USA 91:5129–5132CrossRefPubMedGoogle Scholar
  38. Hodges SA, Arnold ML (1995) Spurring plant diversification: are floral nectar spurs a key innovation? Proc R Soc Lond B 262:343–348CrossRefGoogle Scholar
  39. Hodges SA, Fulton M, Yang JY, Whittall JB (2003) Verne Grant and evolutionary studies of Aquilegia. New Phytol 161:113–120CrossRefGoogle Scholar
  40. Huelsenbeck JP, Nielsen R, Bollback JP (2003) Stochastic mapping of morphological characters. Syst Biol 52:113–158Google Scholar
  41. Hughes C, Eastwood R (2006) Island radiation on a continental scale: exceptional rates of plant diversification after uplift of the Andes. Proc Natl Acad Sci USA 103:10334–10339CrossRefPubMedGoogle Scholar
  42. Jalas J, Suominen J (1989) Atlas Florae Europaeae. Distribution of vascular plants in Europe. 8. Nymphaceae to Ranunculaceae. The Committee for Mapping the Flora of Europe and Societas Biologica Fennica Vanamo, HelsinkiGoogle Scholar
  43. Johnson LA, Soltis DE (1994) MatK DNA and phylogenetic reconstruction in Saxifragaceae s. str. Syst Bot 19:143–156CrossRefGoogle Scholar
  44. Kay KM, Whittall JB, Hodges SA (2006) A survey of nuclear ribosomal internal transcribed spacer substitution rates across angiosperms: an approximate molecular clock with life history effects. BCM Evol Biol 6:36CrossRefGoogle Scholar
  45. Kelchner SA (2000) The evolution of non-coding chloroplast DNA and its applications on plant systematics. Ann Mo Bot Gard 87:482–498CrossRefGoogle Scholar
  46. Knobloch E, Mai DH (1986) Monographie der Früchte und Samen in der Kreide von Mitteleuropa. Rozpravy ústredního ústavu geologickénho Praha 47:1–219Google Scholar
  47. Knuth P (1906-09) Handbook of flower pollination. Clarendon, OxfordGoogle Scholar
  48. LaRoche G (1978) An experimental study of population differences in leaf morphology of Aquilegia canadensis. Am Midl Nat 100:341–349CrossRefGoogle Scholar
  49. LaRoche G (1980) The effects of restricting root growing space, decreasing nutrient supply and increasing water stress on the phenetics of Aquilegia canadensis L. (Ranunculaceae). Bull Torrey Bot Club 107:220–222CrossRefGoogle Scholar
  50. Lavergne S, Thompson JD, Garnier E, Debussche M (2004) The biology and ecology of narrow endemic and widespread plants: a comparative study of trait variation in 20 congeneric pairs. Oikos 107:505–518CrossRefGoogle Scholar
  51. Lavergne S, Debussche M, Thompson JD (2005) Limitations on reproductive success in endemic Aquilegia viscosa (Ranunculaceae) relative to its widespread congener Aquilegia vulgaris: the interplay of herbivory and pollination. Oecologia 142:212–220CrossRefPubMedGoogle Scholar
  52. Lavin M, Herendeen P, Wojciechowski MF (2005) Evolutionary rates analysis of Leguminosae implicates a rapid diversification of lineages during the Tertiary. Syst Biol 54:530–549CrossRefGoogle Scholar
  53. Louchart A, Tourment N, Carrier J, Roux T, Mourer-Chauviré C (2008) Hummingbird with modern feathering: an exceptionally well-preserved Oligocene fossil from southern France. Naturwissenschaften 95:171–175CrossRefPubMedGoogle Scholar
  54. Marincovich L Jr, Gladenkov AY (2001) New evidence for the age of Bering Strait. Quaternary Sci Rev 20:329–335CrossRefGoogle Scholar
  55. Matthiessen J, Knies J, Vogt C, Stein R (2009) Pliocene palaeoceanography of the Arctic Ocean and subarctic seas. Phil Trans R Soc A 367:21–48CrossRefPubMedGoogle Scholar
  56. Mayr G (2004) Old World fossil record of modern—type hummingbirds. Science 304:810–811CrossRefGoogle Scholar
  57. Medrano M, Castellanos MC, Herrera CM (2007) Comparative floral and vegetative differentiation between two European Aquilegia taxa along a narrow contact zone. Plant Syst Evol 262:209–224CrossRefGoogle Scholar
  58. Miller RB, Willard CL (1983) The pollination ecology of Aquilegia micrantha (Ranunculaceae) in Colorado. Southw Nat 28:157–164CrossRefGoogle Scholar
  59. Müller H (1883) The fertilization of flowers. MacMillan, LondonGoogle Scholar
  60. Munz PA (1946) Aquilegia: the cultivated and wild columbines. In: Bailey LH (eds) Gentes Herbarium 7:1-50Google Scholar
  61. Nielsen R (2002) Mutations mapping on phylogenies. Syst Biol 51:729–732CrossRefPubMedGoogle Scholar
  62. Nold R (2003) Columbines. Aquilegia, Paraquilegia and Semiaquilegia. Timber Press, CambridgeGoogle Scholar
  63. Paradis E (2008) Asymmetries in phylogenetic diversification and character change can be untangled. Evolution 62:241–247PubMedGoogle Scholar
  64. Paradis E, Claude J, Strimmer K (2004) APE: analysis of phylogenetics and evolution in R language. Bioinformatics 20:289–290CrossRefPubMedGoogle Scholar
  65. Patterson TB, Givnish J (2003) Geographic cohesion, chromosomal evolution, parallel adaptive radiations, and consequent floral adaptations in Calochortus (Calochortaceae): evidence from a cpDNA phylogeny. New Phytol 161:253–264CrossRefGoogle Scholar
  66. Pignatti S (1982) Flora d`Italia. Edagricole, BolognaGoogle Scholar
  67. Polyakova MA, Dits LY, Ermakov NB (2008) Studies on biological features of band pine forests in the intermontane Minusinsk depression by methods of gradient analysis. Russ J Ecol 39:238–245CrossRefGoogle Scholar
  68. Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817–818CrossRefPubMedGoogle Scholar
  69. Rambaut A, Drummond AJ (2007) Tracer v.1.4.1.
  70. Ro K-E, McPheron B (1997) Molecular phylogeny of the Aquilegia group (Ranunculaceae) based on internal transcribed spacers and 5.8S nuclear ribosomal DNA. Biochem Syst Ecol 25:445–461CrossRefGoogle Scholar
  71. Ro K-E, Keener CS, McPheron BA (1997) Molecular phylogenetic study of the Ranunculaceae: utility of the nuclear 26S ribosomal DNA in inferring intrafamilial relationships. Mol Phyl Evol 8:117–127CrossRefGoogle Scholar
  72. Robichaux RH, Carr GD, Liebman M, Pearcy RW (1990) Adaptive radiation of the Hawaiian silversword alliance (Compositae-Madiinae): ecological, morphological and physiological diversity. Ann Mo Bot Gard 77:64–72CrossRefGoogle Scholar
  73. Rodríguez F, Oliver JF, Marín A, Medina JR (1990) The general stochastic model of nucleotide substitution. J Theor Biol 142:485–501CrossRefPubMedGoogle Scholar
  74. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574CrossRefPubMedGoogle Scholar
  75. Sanderson MJ (1998) Estimating rate and time in molecular phylogenies: beyond the molecular clock? In: Soltis PS, Soltis DE, Doyle JJ (eds) Molecular systematics of plants II: DNA sequencing. Kluwer, New York, pp 242–264Google Scholar
  76. Sang T, Crawford DJ, Stuessy TF (1997) Chloroplast DNA phylogeny, reticulate evolution and biogeography of Paeonia (Paeoniaceae). Am J Bot 84:1120–1136CrossRefGoogle Scholar
  77. Schluter D (1996) Ecological causes of adaptive radiation. Am Nat 148:S40–S64CrossRefGoogle Scholar
  78. Schluter D (2000) The ecology of adaptive radiation. Oxford Series in Ecology and Evolution. Oxford University Press, New YorkGoogle Scholar
  79. Schönswetter P, Popp M, Brochmann C (2006) Central Asian origin of and strong genetic differentiation among populations of the rare and disjunct Carex atrofusca (Cyperaceae) in the Alps. J Biogeogr 33:948–956CrossRefGoogle Scholar
  80. Semerikov VL, Zang HQ, Sun M, Lascoux M (2003) Conflicting phylogenies of Larix (Pinaceae) based on cytoplasmatic and nuclear DNA. Mol Phyl Evol 27:173–184CrossRefGoogle Scholar
  81. Simmons MP, Ochotorena H (2000) Gaps as characters in sequence-based phylogenetic analyses. Syst Biol 49:369–381CrossRefPubMedGoogle Scholar
  82. Stebbins GL (1970) Adaptive radiation of reproductive characteristics in angiosperms. I. Pollination mechanisms. Annu Rev Ecol Syst 1:307–326CrossRefGoogle Scholar
  83. Strand AE, Brook GM, Pruit CS (1996) Are populations island? Analysis of chloroplast DNA variation in Aquilegia. Evolution 50:1822–1829CrossRefGoogle Scholar
  84. Sun Y, Skinner DZ, Liang GH, Hulbert SH (1994) Phylogenetic analysis of sorghum and related taxa using internal transcribed spacer of nuclear ribosomal DNA. Theor Appl Gen 89:26–32CrossRefGoogle Scholar
  85. Swofford DL (2002) PAUP*: phylogenetic analysis using parsimony, version 4.010b. Sinauer Associates, SunderlandGoogle Scholar
  86. Tang L-L, Yu Q, Sun J-F, Huang S-Q (2007) Floral traits and isolation of three sympatric Aquilegia species in the Qinling Mountains, China. Plant Syst Evol 267:121–128CrossRefGoogle Scholar
  87. Tucker SC, Hodges SA (2005) Floral ontogeny of Aquilegia, Semiaquilegia, and Enemion (Ranunculaceae). Int J Plant Sci 166(4):557–574CrossRefGoogle Scholar
  88. Verboom GA, Linder HP, Stock W (2003) Phylogenetics of the grass genus Ehrharta: evidence for adaptive radiation in the summer-arid zone of the South African Cape. Evolution 57:1008–1021PubMedGoogle Scholar
  89. Verboom GA, Linder HP, Stock WD (2004) Testing the adaptive nature of radiation: growth form and life history divergence in the African grass genus Ehrharta (Poaceae: Ehrhartoideae). Am J Bot 91:1364–1370CrossRefGoogle Scholar
  90. Wang W, Chen Z-D (2007) Generic level phylogeny of Thalictroideae (Ranunculaceae) implications for the status of Paropyrum and petal evolution. Taxon 56:811–821CrossRefGoogle Scholar
  91. Weber WA (2003) The Middle Asian element in the southern Rocky Mountain flora of the western United States: a critical biogeographical review. J Biogeog 30:649–685CrossRefGoogle Scholar
  92. Whittall JB (2005) Ecological speciation and convergent evolution in the North American columbine radiation (Aquilegia, Ranunculaceae). PhD Thesis, UC Santa Barbara, Santa BarbaraGoogle Scholar
  93. Whittall JB, Hodges SA (2007) Pollinator shifts drive increasingly long nectar spurs in columbine flowers. Nature 447:706–710CrossRefPubMedGoogle Scholar
  94. Whittemore AT (1997) Aquilegia. In: Morin NR (ed) Flora of North America. Oxford University Press, New YorkGoogle Scholar
  95. Wikström N, Savolainen V, Chase M (2001) Evolution of angiosperms: calibrating the family tree. Proc R Soc Lond B 268:2211–2222CrossRefGoogle Scholar
  96. Wolfe AD, Randle CP, Datwyler SL, Morawetz JJ, Arguedas N, Díaz J (2006) Phylogeny, taxonomic affinities, and biogeography of Penstemon (Plantaginaceae) based on ITS and cpDNA sequence data. Am J Bot 93:1699–1713CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Jesús M. Bastida
    • 1
  • Julio M. Alcántara
    • 1
    Email author
  • Pedro J. Rey
    • 1
  • Pablo Vargas
    • 2
  • Carlos M. Herrera
    • 3
  1. 1.Departamento de Biología Animal, Biología Vegetal y EcologíaUniversidad de JaénJaénSpain
  2. 2.Real Jardín BotánicoC.S.I.C.MadridSpain
  3. 3.Estación Biológica de DoñanaC.S.I.CSevillaSpain

Personalised recommendations