Plant Systematics and Evolution

, Volume 295, Issue 1–4, pp 73–82 | Cite as

Shift towards autogamy in the extremely narrow endemic Aquilegia paui and comparison with its widespread close relative A. vulgaris (Ranunculaceae)

  • M. Carmen MartinellEmail author
  • Ana Rovira
  • Cèsar Blanché
  • Maria Bosch
Original Article


Aquilegia paui is an extremely narrowly endemic species from the northeastern Iberian Peninsula. It is restricted to a few populations with a reduced number of individuals living in summit rock cliffs. It is studied and compared to the widespread Aquilegia vulgaris to assess differences in their breeding system and pollination ecology, expected by their differences in flower morphology and by their habitat divergence. Pollinator exclusion experiments showed the capacity of A. paui to reach a full seed set in the absence of pollinators, whereas A. vulgaris notably reduced its reproductive success under these conditions. At the same time, no insect visits were detected in A. paui, whereas A. vulgaris was frequently visited, mainly by bumblebees and flies. Thus, an evolutionary shift toward autogamy in A. paui is discussed in relation to enhanced reproductive assurance. Additionally, we address reproductive isolation mechanisms that nowadays keep A. paui and A. vulgaris separated in spite of their ability to intercross and the existence of contact areas.


Columbine Ecological differentiation Pollination Endemic species Reproductive isolation Self-pollination Reproductive assurance 



We thank Dr. Julià Molero, Dr. Llorenç Sáez, Joan Carles Baiges and Marta Melé for their assistance in field work as well as Maria Navarro for her aid in the sample analysis. The staff of Els Ports Natural Park helped in the development of this research and partially financed it. This work was also supported by projects FBG-303608 (Generalitat de Catalunya) and CGL2007-60475/BOS (Ministerio de Educación y Ciencia), and by a BRD fellowship (Univeristat de Barcelona) awarded to M. Carmen Martinell.


  1. Aigner PA (2004) Ecological and genetic effects on demographic processes: pollination, clonality and seed production in Dithyrea maritima. Biol Conserv 116:27–34CrossRefGoogle Scholar
  2. Aizen MA, Harder LD (2007) Expanding the limits of the pollen-limitation concept: effects of pollen quantity and quality. Ecology 88:271–281PubMedCrossRefGoogle Scholar
  3. Alcántara JM, Bastida JM, Rey PJ (2010) Linking divergent selection on vegetative traits to environmental variation and phenotypic diversification in the Iberian columbines (Aquilegia). J Evol Biol 23:1216–1233CrossRefGoogle Scholar
  4. Armbruster WS, Mulder CPH, Baldwin BG, Kalisz S, Wessa B, Nute H (2002) Comparative analysis of late floral development and mating-system evolution in tribe Collinsieae (Scrophulariaceae s.l.) 1. Am J Bot 89:37–49PubMedCrossRefGoogle Scholar
  5. Arrigoni PV, Nardi E (1977) Endemic plants of Sardinia, Italy. Part 19–20. Boll Soc Sarda Sci Nat 17:215–226Google Scholar
  6. Barrett SCH (2002) The evolution of plant sexual diversity. Nat Rev Genet 3:274–284PubMedCrossRefGoogle Scholar
  7. Barrett SCH (2008) Major evolutionary transitions in flowering plant reproduction: an overview. Int J Plant Sci 169:1–5CrossRefGoogle Scholar
  8. Blanché C, Molero J, Rovira AM, Simon J, Bosch M, Sàez L, López-Pujol J, Orellana MR (2005) Estudi bàsic sobre l’estat de conservació, biologia de poblacions i propostes de protecció per a Aquilegia paui. Memòria del conveni entre el Departament de Medi Ambient i Habitatge de la Generalitat de Catalunya i la Universitat de Barcelona Fundació Bosch i Gimpera (Projecte FBG-303608). BarcelonaGoogle Scholar
  9. Bolòs O, Vigo J (1984) Flora dels Països Catalans. Barcino, BarcelonaGoogle Scholar
  10. Brunet J, Sweet HR (2006) The maintenance of selfing in a population of the rocky mountain columbine. Int J Plant Sci 167:213–219CrossRefGoogle Scholar
  11. Chase VC, Raven PH (1975) Evolutionary and ecological relationships between Aquilegia formosa and Aquilegia pubescens (Ranunculaceae) two perennial plants. Evolution 29:474–486CrossRefGoogle Scholar
  12. Cheptou PO (2004) Allee effect and self-fertilization in hermaphrodites: reproductive assurance in demographically stable populations. Evolution 58:2613–2621PubMedGoogle Scholar
  13. Cruden RW (1977) Pollen-ovule ratios: a conservative indicator of breeding systems in flowering plants. Evolution 31:32–46CrossRefGoogle Scholar
  14. Cruden RW (2000) Pollen grains: why so many? Plant Syst Evol 222:143–165CrossRefGoogle Scholar
  15. Cullen J, Heywood VH (1964) Aquilegia L. In: Tutin TG, Heywood VH, Burges NA, Moore DM, Valentine DH, Walters SM, Webb DA (eds) Flora Europaea, vol 1. Cambridge University Press, Cambridge, pp 238–240Google Scholar
  16. Dafni A, Pacini E, Nepi M (2005) Pollen and stigma biology. In: Dafni A, Kevan PG, Husband BC (eds) Practical pollination biology. Enviroquest, Cambridge, pp 83–146Google Scholar
  17. Dar AR, Dar GH, Reshi Z (2006) Recovery and restoration of some critically endangered endemic angiosperms of the Kashmir Himalaya. J Biol Sci 6:985–991CrossRefGoogle Scholar
  18. Darwin C (1876) The effects of cross- and self-fertilisation in the vegetable kingdom. John Murray, LondonGoogle Scholar
  19. Darwin C (1877) The different forms of flowers on plants of the same species. John Murray, LondonGoogle Scholar
  20. Debussche M, Thompson JD (2003) Habitat differentiation between two closely related Mediterranean plant species, the endemic Cyclamen balearicum and the widespread C. repandum. Acta Oecol 24:35–45CrossRefGoogle Scholar
  21. Delesalle VA, Mazer SJ, Paz H (2008) Temporal variation in the pollen:ovule ratios of Clarkia (Onagraceae) taxa with contrasting mating systems: field populations. J Evol Biol 21:310–323PubMedGoogle Scholar
  22. Díaz-González TE (1986) Aquilegia L. In: Castroviejo S, Laínz M, López-González G, Montserrat P, Muñoz-Garmendia F, Paiva J, Villar L (eds) Flora Ibérica, vol 1. Real Jardín Botánico de Madrid, Madrid, pp 376–387Google Scholar
  23. DOGC (2008) Decret 172/2008, de 26 d’agost, de creació del Catàleg de flora amenaçada de Catalunya. DOGC 5204:65881–65895Google Scholar
  24. Eckert CG, Herlihy CR (2004) Using a cost-benefit approach to understand the evolution of self-fertilization in plants: the perplexing case of Aquilegia canadiensis (Ranunculaceae). Plant Species Biol 19:159–173CrossRefGoogle Scholar
  25. Fenster CB, Marten-Rodriguez S (2007) Reproductive assurance and the evolution of pollination specialization. Int J Plant Sci 168:215–228CrossRefGoogle Scholar
  26. Font X (2008) Mòdul Flora i Vegetació. Banc de Dades de Biodiversitat de Catalunya. Generalitat de Catalunya i Universitat de Barcelona.
  27. Font Quer P (1920) Contribució al coneixement de la flora catalana occidental. Treb Mus Hist Nat Barcelona v. ser Bot 3:193–223Google Scholar
  28. Fulton M, Hodges SA (1999) Floral isolation between Aquilegia formosa and Aquilegia pubescens. Proc R Soc Lond Ser B Biol Sci 266:2247–2252CrossRefGoogle Scholar
  29. Gómez JM (2002) Self-pollination in Euphrasia willkommii Freyn (Scrophulariaceae), an endemic species from the alpine of the Sierra Nevada (Spain). Plant Syst Evol 232:63–71CrossRefGoogle Scholar
  30. Goodwillie C, Kalisz S, Eckert CG (2005) The evolutionary enigma of mixed mating systems in plants: occurrence, theoretical explanations, and empirical evidence. Annu Rev Ecol Evol Syst 36:47–79CrossRefGoogle Scholar
  31. Grant V (1952) Isolation and hybridization between Aquilegia formosa and Aquilegia pubescens. Aliso 2:341–360Google Scholar
  32. Grant V (1971) Plant speciation. Columbia University Press, New YorkGoogle Scholar
  33. Grant V (1993) Origin of floral isolation between ornithophilous and sphingophilous plant species. Proc Natl Acad Sci USA 90:7729–7733PubMedCrossRefGoogle Scholar
  34. Guinochet M, Vilmorin R (1984) Flore de France. Éditions du Centre national de la recherche scientifique, ParisGoogle Scholar
  35. Heywood VH (1954) Critical notes on the flora of Spain. I. Bull Br Mus Nat Hist Bot 1:81–122Google 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 91:5129–5132PubMedCrossRefGoogle Scholar
  38. Hodges SA, Arnold ML (1995) Spurring plant diversification: are floral nectar spurs a key innovation? Proc. R Soc Lond Ser B Biol Sci 262:343–348CrossRefGoogle Scholar
  39. Hodges SA, Whittall JB, Fulton M, Yang JY (2002) Genetics of floral traits influencing reproductive isolation between Aquilegia formosa and Aquilegia pubescens. Am Nat 159:S51–S60PubMedCrossRefGoogle Scholar
  40. Hodges SA, Fulton M, Yang JY, Whittall JB (2003) Verne Grant and evolutionary studies of Aquilegia. New Phytol 161:113–120CrossRefGoogle Scholar
  41. Huang SQ, Tang LL, Yu Q, Guo YH (2004) Temporal floral sex allocation in protogynous Aquilegia yabeana contrasts with protandrous species: support for the mating environment hypothesis. Evolution 58:1131–1134PubMedGoogle Scholar
  42. Igic B, Kohn JR (2006) The distribution of plant mating systems: study bias against obligately outcrossing species. Evolution 60:1098–1103PubMedGoogle Scholar
  43. Jahandiez E, Maire R (1932) Catalogue des Plantes du Maroc. Ed. Minerva, AlgerGoogle Scholar
  44. Jain SK (1976) The evolution of inbreeding in plants. Annu Rev Ecol Evol Syst 7:469–495CrossRefGoogle Scholar
  45. Jürgens A, Witt T, Gottsberger G (2002) Pollen grain numbers, ovule numbers and pollen-ovule ratios in Caryophylloideae: correlation with breeding system, pollination, life form, style number, and sexual system. Sex Plant Reprod 14:279–289CrossRefGoogle Scholar
  46. Kalisz S, Vogler DW (2003) Benefits of autonomous selfing under unpredictable pollinator environments. Ecology 84:2928–2942CrossRefGoogle Scholar
  47. Kearns CA, Inouye DW (1993) Techniques for pollination biologists. University Press of Colorado, NiwotGoogle Scholar
  48. Kennedy BF, Elle E (2008) The reproductive assurance benefit of selfing: importance of flower size and population size. Oecologia 155:469–477PubMedCrossRefGoogle Scholar
  49. Kephart S, Reynolds RJ, Rutter MT, Fenster CB, Dudash MR (2006) Pollination and seed predation by moths on Silene and allied Caryophyllaceae: evaluating a model system to study the evolution of mutualisms. New Phytol 169:667–680PubMedCrossRefGoogle Scholar
  50. Kreyer D, Oed A, Walther-Hellwig K, Frankl R (2004) Are forests potential landscape barriers for foraging bumblebees? Landscape scale experiments with Bombus terrestris agg. and Bombus pasquorum (Hymenoptera, Apidae). Biol Conserv 116:111–118CrossRefGoogle Scholar
  51. Lavergne S (2003) Les espèces végétales rares ont-elles des caractéristiques écologiques et biologiques qui leur sont propres? Applications à la conservation de la flore en Languedoc-Rousssillon. PhDThesis. Academie de Montpellier. Ecole Nationale Superieure Agronomique de Montpellier, MontpellierGoogle Scholar
  52. Lavergne S, Garnier E, Debussche M (2003) Do rock endemic and widespread plant species differ under the leaf-height-seed plant ecology strategy scheme? Ecol Lett 6:398–404CrossRefGoogle Scholar
  53. 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
  54. 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 142:212–220PubMedCrossRefGoogle Scholar
  55. Lloyd DG, Schoen DJ (1992) Self-fertilization and cross-fertilization in plants, 1. Functional dimensions. Int J Plant Sci 153:358–369CrossRefGoogle Scholar
  56. Macior LW (1966) Foraging behavior of Bombus (Hymenoptera: Apidae) in relation of Aquilegia pollination. Am J Bot 53:302–309CrossRefGoogle Scholar
  57. Martinell MC (2010) Biología de la conservación de especies de área de distribución restringida en Cataluña. PhD Thesis. Universitat de BarcelonaGoogle Scholar
  58. Martinell MC, Sàez L, Molero J (2007) Taxonomic assessment of the critically endangered narrow endemic Aquilegia paui Font Quer. XII Optima meeting, PisaGoogle Scholar
  59. Martinell MC, López-Pujol J, Bosch M, Blanché C (2010) Low genetic variability in the rare, recently differentiated Aquilegia paui (Ranunculaceae). Biochem Syst Ecol 38:390–397CrossRefGoogle Scholar
  60. Martinell MC, López-Pujol J, Blanché C, Molero J, Sáez L (2011) Conservation assessment of Aquilegia paui (Ranunculaceae): a case study of an extremely narrow endemic. Oryx 45:187–190Google Scholar
  61. Medrano M, Castellanos MC, Herrera CM (2006) Comparative floral and vegetative differentiation between two European Aquilegia taxa along a narrow contact zone. Plant Syst Evol 262:209–224CrossRefGoogle Scholar
  62. Micheneau C, Fournel J, Gauvin-Bialecki A, Pailler T (2008) Auto-pollination in a long-spurred endemic orchid (Jumellea stenophylla) on Reunion Island (Mascarene Archipelago, Indian Ocean). Plant Syst Evol 272:11–22CrossRefGoogle Scholar
  63. Montalvo A (1992) Relative success of self and outcross pollen comparing mixed- and single donor pollinations in Aquilegia caerulea. Evolution 46:1181–1198CrossRefGoogle Scholar
  64. Moody-Weis JM, Heywood JS (2001) Pollination limitation to reproductive success in the Missouri evening primrose, Oenothera macrocarpa (Onagraceae). Am J Bot 88:1615–1622PubMedCrossRefGoogle Scholar
  65. Morgan JW (1999) Effects of population size on seed production and germinability in an endangered, fragmented grassland plant. Conserv Biol 13(2):266–273Google Scholar
  66. Munz PA (1946) Aquilegia. Gentes Herb 7:1–150Google Scholar
  67. Niet T, Johnson SD, Linder HP (2006) Macroevolutionary data suggest a role for reinforcement in pollination system shifts. Evolution 60:1596–1601PubMedCrossRefGoogle Scholar
  68. Nold R (2003) Columbines: Aquilegia, Paraquilegia and Semiaguilegia. Timber Press, PortlandGoogle Scholar
  69. Ornduff R (1969) Reproductive biology in relation to systematics. Taxon 18:1–33CrossRefGoogle Scholar
  70. Parsons K, Hermanutz L (2006) Conservation of rare, endemic Braya species (Brassicaceae): breeding system variation, potential hybridization and human disturbance. Biol Conserv 128:201–214CrossRefGoogle Scholar
  71. Pedersen HÆ, Ehlers BK (2000) Local evolution of obligate autogamy in Epipactis helleborine subsp. neerlandica (Orchidaceae). Plant Syst Evol 223:173–183CrossRefGoogle Scholar
  72. Porcher E, Lande R (2005) The evolution of self-fertilization and inbreeding depression under pollen discounting and pollen limitation. J Evol Biol 18:497–508PubMedCrossRefGoogle Scholar
  73. Pramzo W (1965) Cytogenetic studies on the genus Aquilegia. IV. Fertility relationships among the Aquilegia species. Acta Soc Bot Pol 34:667–685Google Scholar
  74. Preston RE (1986) Pollen-ovule ratios in the Cruciferae. Am J Bot 73:1732–1740CrossRefGoogle Scholar
  75. Richards AJ (1986) Plant breeding systems. George Allen & Unwin, LondonGoogle Scholar
  76. Routley MB, Mavraganis K, Eckert CG (1999) Effect of population size on the mating system in a self-compatible, autogamous plant, Aquilegia canadensis (Ranunculaceae). Heredity 82:518–528PubMedCrossRefGoogle Scholar
  77. Sàez L, Rosselló JA, Vigo J (1998) Catàleg de plantes vasculars endèmiques, rares o amenaçades de Catalunya. I. Tàxons endèmics. Acta Bot Barc 45:309–321Google Scholar
  78. Sakai AK, Weller SG, Wagner WL, Nepokroeff M, Culley TM (2006) Adaptative radiation and evolution of breeding systems in Schiedea (Caryophyllaceae), an endemic Hawaiian genus. Ann Mo Bot Gard 93:49–63CrossRefGoogle Scholar
  79. Stebbins GL (1974) Flowering plants: evolution above the species level. Belknap Press, HarvardGoogle Scholar
  80. Steven JC, Waller DM (2004) Reproductive alternatives to insect pollination in four species of Thalictrum (Ranunculaceae). Plant Species Biol 19:73–80CrossRefGoogle Scholar
  81. Tang LL, Yu Q, Sun JF, Huang SQ (2007) Floral traits and isolation of three sympatric Aquilegia species in the Qinling Mountains, China. Plant Syst Evol 267:121–128CrossRefGoogle Scholar
  82. Thompson JD (2001) How do visitation patterns vary among pollinators in relation to floral display and floral design in a generalist pollination system? Oecologia 126:386–394CrossRefGoogle Scholar
  83. Thompson JD, Lavergne S, Affre L, Gaudeul M, Debussche M (2005) Ecological differentiation of Mediterranean endemic plants. Taxon 54:967–976CrossRefGoogle Scholar
  84. Torres L (1989) Flora del Massís del Port. Publicaciones de la Diputació de Tarragona, TarragonaGoogle Scholar
  85. Valdés B, Rejdali M, el Kadmiri AA (2002) Catalogue des plantes vasculaires du nord du Maroc. CSIC, MadridGoogle Scholar
  86. Walther-Hellwig K, Frankl R (2000) Foraging habitats and foraging distances of bumblebees, Bombus spp. (Hymenoptera, Apidae), in an agricultural landscape. J Appl Entomol 124:299–306CrossRefGoogle Scholar
  87. Whittall JB, Medina-Marino A, Zimmer EA, Hodges SA (2006) Generating single-copy nuclear gene data for a recent adaptive radiation. Mol Phylogenet Evol 39:124–134PubMedCrossRefGoogle Scholar
  88. Wyatt R (1984) The evolution of self-pollination in granite outcrop species of Arenaria (Caryophyllaceae), I: morphological correlates. Evolution 38:804–816CrossRefGoogle Scholar
  89. Yu Q, Huang SQ (2006) Flexible stigma presentation assists context-dependent pollination in a wild columbine. New Phytol 169:237–241PubMedCrossRefGoogle Scholar
  90. Yu Q, Guo YH, Huang SQ (2005) Characters of stigma in three Aquilegia species. Acta Phytotaxon Sin 43:513–516CrossRefGoogle Scholar
  91. Zhang L, Barrett SCH, Gao JY, Chen J, Cole WW, Liu Y, Bai ZL, Li QJ (2005) Predicting mating patterns from pollination syndromes: the case of “sapromyiophily” in Tacca chantrieri (Taccaceae). Am J Bot 92:517–524PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • M. Carmen Martinell
    • 1
    Email author
  • Ana Rovira
    • 1
  • Cèsar Blanché
    • 1
  • Maria Bosch
    • 1
  1. 1.BioC, GReB, Laboratori de Botànica, Facultat de FarmàciaUniversitat de BarcelonaBarcelonaSpain

Personalised recommendations