Evolutionary Ecology

, Volume 25, Issue 2, pp 237–248 | Cite as

Phenotypic selection on floral scent: trade-off between attraction and deterrence?

  • Florian P. Schiestl
  • Franz K. Huber
  • José M. Gomez
Original Paper


Flowers emit a large variety of floral signals that play a fundamental role in the communication of plants with their mutualists and antagonists. We investigated phenotypic selection on floral scent and floral display using the rewarding orchid species Gymnadenia odoratissima. We found positive directional selection on inflorescence size, as well as positive and negative selection on floral scent compounds. Structural equation modeling showed that “active” compounds, i.e. those that were shown in earlier investigations to be detected by pollinator insects, were positively linked to fitness, whereas “non-active” were negatively linked to fitness. Our results suggest that different patterns of selection impact on different scent compounds, which may relate to the functions of compounds for attracting/deterring insects.


Pollination Floral evolution VOC Plant volatiles Herbivory 



We would like to thanks three anonymous reviewer as well as the handling editor, Arien Biere, for their valuable comments on an earlier version of this manuscript. We also thank Roman Kaiser for his help with identifying scent compounds.


  1. Aragon S, Ackerman JD (2004) Does flower color variation matter in deception pollinated Psychilis monensis (Orchidaceae)? Oecologia 138:405–413CrossRefPubMedGoogle Scholar
  2. Ayasse M, Schiestl FP, Paulus HF, Löfstedt C, Hansson BS, Ibarra F, Francke W (2000) Evolution of reproductive strategies in the sexually deceptive orchid Ophrys sphegodes: how does flower-specific variation of odor signals influence reproductive success? Evolution 54:1995–2006PubMedGoogle Scholar
  3. Baldwin IT, Preston C, Euler M, Gorham D (1997) Patterns and consequences of benzyl acetone floral emissions from Nicotiana attenuata plants. J Chem Ecol 23:2327–2343CrossRefGoogle Scholar
  4. Benitez-Vieyra S, Medina AM, Glinos E, Cocucci AA (2006) Pollinator-mediated selection on floral traits and size of floral display in Cyclopogon elatus, a sweat bee-pollinated orchid. Funct Ecol 20:948–957CrossRefGoogle Scholar
  5. Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical-theoretic approach. Springer, HeidelbergGoogle Scholar
  6. Chess SKR, Raguso RA, LeBuhn G (2008) Geographic divergence in floral morphology and scent in Linanthus dichotomus (Polemoniaceae). Am J Bot 95:1652–1659CrossRefGoogle Scholar
  7. Chittka L, Thomson JD, Waser NM (1999) Flower constancy, insect psychology, and plant evolution. Naturwissenschaften 86:361–377CrossRefGoogle Scholar
  8. Cunningham JP, Moore CJ, Zalucki MP, West SA (2004) Learning, odour preference and flower foraging in moths. J Exp Biol 207:87–94CrossRefPubMedGoogle Scholar
  9. Dötterl S, Jurgens A, Seifert K, Laube T, Weissbecker B, Schutz S (2006) Nursery pollination by a moth in Silene latifolia: the role of odours in eliciting antennal and behavioural responses. New Phytol 169:707–718CrossRefPubMedGoogle Scholar
  10. Galen C (1989) Measuring pollinator-mediated selection on morphometric floral traits. Bumblebees and the alpine sky pilot, Polemonium viscosum. Evolution 43:882–890CrossRefGoogle Scholar
  11. Galen C, Zimmer KA, Newport ME (1987) Pollination in floral scent morphs of Polemonium viscosum—a mechanism for disruptive selection on flower size. Evolution 41:599–606CrossRefGoogle Scholar
  12. Gomez JM (2000) Phenotypic selection and response to selection in Lobularia maritima: importance of direct and correlational components of natural selection. J Evol Biol 13:689–699CrossRefGoogle Scholar
  13. Gomez JM, Bosch J, Perfectti F, Fernandez JD, Abdelaziz M, Camacho JPM (2008) Spatial variation in selection on corolla shape in a generalist plant is promoted by the preference patterns of its local pollinators. Proc R Soc Lond B Biol Sci 275:2241–2249CrossRefGoogle Scholar
  14. Goyret J, Pfaff M, Raguso RA, Kelber A (2008) Why do Manduca sexta feed from white flowers? Innate and learnt colour preferences in a hawkmoth. Naturwissenschaften 95:569–576CrossRefPubMedGoogle Scholar
  15. Grace JB (2006) Structural equation modeling and natural systems. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  16. Hair JF, Black WC, Babin BJ, Anderson RE (2009) Multivariate data analysis, 7th edn. Prentice Hall, Englewood CliffsGoogle Scholar
  17. Herrera CM, Castellanos MC, Medrano M (2006) Geographical context of floral evolution: towards an improved research programme in floral diversification. In: Harder LD, Barrett SCH (eds) Ecology and Evolution of flowers. Oxford University Press, Oxford, pp 278–294Google Scholar
  18. Huber FK, Kaiser R, Sauter W, Schiestl FP (2005) Floral scent emission and pollinator attraction in two species of Gymnadenia (Orchidaceae). Oecologia 142:564–575CrossRefPubMedGoogle Scholar
  19. Ibrahim MA, Kainulainen P, Aflatuni A, Tiilikkala K, Holopainen JK (2001) Insecticidal, repellent, antimicrobial activity and phytotoxicity of essential oils: with special reference to limonene and its suitability for control of insect pests. Agric Food Sci Finl 10:243–259Google Scholar
  20. Johnson SD (2006) Pollinator driven speciation in plants. In: Harder LD, Barrett SCH (eds) Ecology and evolution of flowers. Oxford University Press, Oxford, pp 295–310Google Scholar
  21. Junker RJ, Blüthgen N (2010) Floral scents repel facultative flower visitors, but attract obligate ones. Ann Bot (in press)Google Scholar
  22. Kessler D, Gase K, Baldwin IT (2008) Field experiments with transformed plants reveal the sense of floral scents. Science 321:1200–1202CrossRefPubMedGoogle Scholar
  23. Knudsen JT, Eriksson R, Gershenzon J, Stahl B (2006) Diversity and distribution of floral scent. Bot Rev 72:1–120CrossRefGoogle Scholar
  24. Lande R, Arnold SJ (1983) The measurement of selection on correlated characters. Evolution 37:1210–1226CrossRefGoogle Scholar
  25. Maad J (2000) Phenotypic selection in hawkmoth-pollinated Platanthera bifolia: targets and fitness surfaces. Evolution 54:112–123PubMedGoogle Scholar
  26. Maad J, Alexandersson R (2004) Variable selection in Platanthera bifolia (Orchidaceae): phenotypic selection differed between sex functions in a drought year. J Evol Biol 17:642–650CrossRefPubMedGoogle Scholar
  27. Mant J, Peakall R, Schiestl FP (2005) Does selection on floral odor promote differentiation among populations and species of the sexually deceptive orchid genus Ophrys? Evolution 59:1449–1463PubMedGoogle Scholar
  28. Melendez-Ackerman E, Campbell DR (1998) Adaptive significance of flower color and inter-trait correlations in an Ipomopsis hybrid zone. Evolution 52:1293–1303CrossRefGoogle Scholar
  29. Melendez-Ackerman E, Campbell DR, Waser NM (1997) Hummingbird behavior and mechanisms of selection on flower color in Ipomopsis. Ecology 78:2532–2541Google Scholar
  30. O’Connell ML, Johnston MO (1998) Male and female pollination success in a deceptive orchid, a selection study. Ecology 79:1246–1260Google Scholar
  31. O’Reilly-Wapstra JM, Iason GR, Thoss V (2007) The role of genetic and chemical variation of Pinus sylvestris seedlings in influencing slug herbivory. Oecologia 152:82–91CrossRefPubMedGoogle Scholar
  32. Ômura H, Honda K, Hayashi N (2000) Floral scent of Osmanthus fragrans discourages foraging behavior of cabbage butterfly, pieris rapae. J Chem Ecol 26:655–666CrossRefGoogle Scholar
  33. Pellmyr O (1986) Three pollination morphs in Cimicifuga simplex; incipient speciation due to inferiority competition. Oecologia 68:304–307CrossRefGoogle Scholar
  34. Plepys D, Ibarra F, Lofstedt C (2002) Volatiles from flowers of Platanthera bifolia (Orchidaceae) attractive to the silver y moth, Autographa gamma (Lepidoptera : Noctuidae). Oikos 99:69–74CrossRefGoogle Scholar
  35. Raguso RA (2008) Wake up and smell the roses: the ecology and evolution of floral scent. Annu Rev Ecol Evol Syst 39:549–569CrossRefGoogle Scholar
  36. Salzmann CC, Cozzolino S, Schiestl FP (2007a) Floral scent in food-deceptive orchids: Species specificity and sources of variability. Plant Biol 9:720–729CrossRefPubMedGoogle Scholar
  37. Salzmann CC, Nardella AM, Cozzolino S, Schiestl FP (2007b) Variability in floral scent in rewarding and deceptive orchids: the signature of pollinator-imposed selection? Ann Bot 100:757–765CrossRefPubMedGoogle Scholar
  38. Schiestl FP (2004) Floral evolution and pollinator mate choice in a sexually deceptive orchid. J Evol Biol 17:67–75CrossRefPubMedGoogle Scholar
  39. Schiestl FP (2010) The evolution of floral scent and insect chemical communication. Ecol Lett 13:643–656CrossRefPubMedGoogle Scholar
  40. Schiestl FP, Roubik DW (2003) Odor compound detection in male euglossine bees. J Chem Ecol 29:253–257CrossRefPubMedGoogle Scholar
  41. Schiestl FP, Schlüter PM (2009) Floral isolation, specialized pollination, and pollinator behavior in orchids. Annu Rev Entomol 54:425–446CrossRefPubMedGoogle Scholar
  42. Schiestl FP et al (2003) The chemistry of sexual deception in an orchid-wasp pollination system. Science 302:437–438CrossRefPubMedGoogle Scholar
  43. Steinebrunner F, Schiestl FP, Leuchtmann A (2008) Ecological role of volatiles produced by epichloe: differences in antifungal toxicity. FEMS Microbiol Ecol 64:307–316CrossRefPubMedGoogle Scholar
  44. Streisfeld MA, Kohn JR (2007) Environment and pollinator-mediated selection on parapatric floral races of Mimulus aurantiacus. J Evol Biol 20:122–132CrossRefPubMedGoogle Scholar
  45. Theis N (2006) Fragrance of canada thistle (Cirsium arvense) attracts both floral herbivores and pollinators. J Chem Ecol 32:917–927CrossRefPubMedGoogle Scholar
  46. Theis N, Kesler K, Adler LS (2009) Leaf herbivory increases floral fragrance in male but not female Curcubita pepo subsp. texana (Cucurbitaceae) flowers. Am J Bot 96:897–903CrossRefGoogle Scholar
  47. Tremblay RL, Ackerman JD, Zimmerman JK, Calvo RN (2005) Variation in sexual reproduction in orchids and its evolutionary consequences: a spasmodic journey to diversification. Biol J Linn Soc 84:1–54CrossRefGoogle Scholar
  48. Vereecken NJ, Schiestl FP (2008) The evolution of imperfect floral mimicry. Proc Natl Acad Sci USA 105:7484–7488CrossRefPubMedGoogle Scholar
  49. Waelti MO, Mühlemann JK, Widmer A, Schiestl FP (2008) Floral odour and reproductive isolation in two species of Silene. J Evol Biol 21:111–121PubMedGoogle Scholar
  50. Waelti MO, Page PA, Widmer A, Schiestl FP (2009) How to be an attractive male: floral dimorphism and attractiveness to pollinators in a dioecious plant. BMC Evol Biol 9Google Scholar
  51. Wiemer AP, More M, Benitez-Vieyra S, Cocucci AA, Raguso RA, Sersic AN (2009) A simple floral fragrance and unusual osmophore structure in Cyclopogon elatus (Orchidaceae). Plant Biol 11:506–514CrossRefPubMedGoogle Scholar
  52. Williams NH, Dodson CH (1972) Selective attraction of male euglossine bees to orchid floral fragrances and its importance in long distance pollen flow. Evolution 26:84–95CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Florian P. Schiestl
    • 1
  • Franz K. Huber
    • 1
  • José M. Gomez
    • 2
  1. 1.Institute of Systematic BotanyUniversity of ZürichZurichSwitzerland
  2. 2.Dpto EcologíaUniversidad de GranadaGranadaSpain

Personalised recommendations