Skip to main content
SpringerLink
Log in

Are pollinators and seed predators selective agents on flower color in Gentiana lutea?

  • Original Paper
  • Published:
Evolutionary Ecology Aims and scope Submit manuscript

Abstract

Animals which interact with plants often cause selective pressures on plant traits. Flower color variation within a species might be shaped by the action of animals feeding on the plant species. Pollinators might exert natural selection on color if flower color is related to their foraging efficiency. For example, some pollinator species might require more time to detect particular colors. If that is the case, flower color might have evolved as a pollination exploitation barrier—ensuring that flowers are more visited by the most efficient pollinators. In addition, non-pollinator agents such as predispersal seed predators may select on flower color, if color indicates food resources (seeds) or if color is related to deterrent compounds. We address selection on flower color in a population of Gentiana lutea where color varies among individuals from yellow to orange. We hypothesize that opposed selection from mutualists (pollinators) and antagonists (predispersal seed predators) maintains flower color variation in this population. By means of path analysis we addressed the role of both interactors in flower color selection. We found that selection acts on flower color, mediated by both pollinators and seed predators. Both agents favored yellow-flowered individuals, thus selection by pollinators and seed predators does not maintain flower color variation in this population.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Arista M, Talavera M, Berjano R, Ortiz PL (2013) Abiotic factors may explain the geographical distribution of flower colour morphs and the maintenance of colour polymorphism in the scarlet pimpernel. J Ecol 101:1613–1622

    Article  Google Scholar 

  • Armbruster W (2002) Can indirect selection and genetic context contribute to trait diversification? a transition probability study of blossom colour evolution in two genera. J Evol Biol 15:468–486

  • Bradshaw H, Schemske DW (2003) Allele substitution at a flower colour locus produces a pollinator shift in monkeyflowers. Nature 426:176–178

    Article  CAS  PubMed  Google Scholar 

  • Briscoe AD, Chittka L (2001) The evolution of color vision in insects. Annu Rev Entomol 46:471–510

    Article  CAS  PubMed  Google Scholar 

  • Campbell DR (2009) Using phenotypic manipulations to study multivariate selection of floral trait associations. Ann Bot 103:1557–1566

    Article  PubMed Central  PubMed  Google Scholar 

  • Carlson JE, Holsinger KE (2013) Direct and indirect selection on floral pigmentation by pollinators and seed predators in a color polymorphic South African shrub. Oecologia 171:905–919

    Article  PubMed  Google Scholar 

  • Caruso CM, Scott SL, Wray JC, Walsh CA (2010) Pollinators, herbivores, and the maintenance of flower color variation: a case study with Lobelia siphilitica. Int J Plant Sci 171(9):1020–1028

    Article  Google Scholar 

  • Chittka L, Waser NM (1997) Why red flowers are not invisible to bees. Isr J Plant Sci 45:169–183

    Article  Google Scholar 

  • CIE (2004) 15: 2004 Colorymetry. CIE Central Bureau, Vienna

    Google Scholar 

  • Eckhart VM (1992) Spatio-temporal variation in abundance and variation in foraging behaviour of the pollinators of gynodioecious Phacelia linearis (Hydrophyllaceae). Oikos 64:573–586

    Article  Google Scholar 

  • Fenster CB, Armbruster WS, Wilson P, Dudash MR, James D (2004) Pollination syndromes and floral specialization. Annu Rev Ecol Evol Syst 35:375–403

    Article  Google Scholar 

  • Fineblum WL, Rausher MD (1997) Do floral pigmentation genes also influence resistance to enemies? The W locus in Ipomoea purpurea. Ecology 78(6):1646–1654

    Article  Google Scholar 

  • Frey FM (2004) Opposing natural selection from herbivores and pathogens may maintain floral-color variation in Claytonia virginica (Portulacaceae). Evolution 58(11):2426–2437

    Article  PubMed  Google Scholar 

  • Gómez J (2000) Phenotypic selection and response to selection in Lobularia maritima: importance of direct and correlational components of natural selection. J Evol Biol 13:689–699

    Article  Google Scholar 

  • Grace JB (2006) Structural equation modeling and natural systems. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Green B, Durnford D (1996) The chlorophyll-carotenoid proteins of oxygenic photosynthesis. Annu Rev Plant Biol 47:685–714

    Article  CAS  Google Scholar 

  • Irwin RE, Strauss SY, Storz S, Emerson A, Guibert G (2003) The role of herbivores in the maintenance of a flower color polymorphism in wild radish. Ecology 84:1733–1743

    Article  Google Scholar 

  • Jones KM, Reithel JS (2001) Pollinator-mediated selection on a flower color polymorphism in experimental populations of Antirrhinum (Scrophulariaceae). Am J Bot 88:447–454

    Article  Google Scholar 

  • Kawecki TJ, Ebert D (2004) Conceptual issues in local adaptation. Ecol Lett 7(12):1225–1241

    Article  Google Scholar 

  • Kingsolver JG, Hoekstra HE, Hoekstra JM, Berrigan D, Vignieri SN, Hill CE, Hoang A, Gibert P, Beerli P (2001) The strength of phenotypic selection in natural populations. Am Nat 157(3):245–261

    Article  CAS  PubMed  Google Scholar 

  • Kohlein F (1991) Gentians. Timber Press Inc, Portland

    Google Scholar 

  • Kolb A, Ehrlén J, Eriksson O (2007) Ecological and evolutionary consequences of spatial and temporal variation in pre-dispersal seed predation. Perspect Plant Ecol Evol Syst 9(2):79–100

    Article  Google Scholar 

  • Kugler H (1943) Hummeln als Blütenbesucher. Ergebnisse der Biologie 19:323

    Google Scholar 

  • Kunze J, Gumbert A (2001) The combined effect of color and odor on flower choice behavior of bumblebees in flower mimicry systems. Behav Ecol 12(4):447–456

    Article  Google Scholar 

  • Lande R, Arnold SJ (1983) The measurement of selection on correlated characters. Evolution 37:1210–1226

    Article  Google Scholar 

  • Lev-Yadun S, Gould KS (2009) Role of anthocyanins in plant defence. In: Gould K, Davies K, Winefield C (eds) Anthocyanins: biosynthesis, functions, and applications. Springer, New York, pp 21–48

    Google Scholar 

  • Moehs CP, Tian L, Osteryoung KW, DellaPenna D (2001) Analysis of carotenoid biosynthetic gene expression during marigold petal development. Plant Mol Biol 45:281–293

    Article  CAS  PubMed  Google Scholar 

  • Ninyerola M, Roure JM, Fernández XP (2005) Atlas climático digital de la Península Ibérica: metodología y aplicaciones en bioclimatología y geobotánica. Universidad Autónoma de Barcelona, Bellaterra

    Google Scholar 

  • Peitsch D, Fietz A, Hertel H, de Souza J, Ventura DF, Menzel R (1992) The spectral input systems of hymenopteran insects and their receptor-based colour vision. J Comp Physiol A 170:23–40

    Article  CAS  PubMed  Google Scholar 

  • Ploquin EF, Herrera JM, Obeso JR (2013) Bumblebee community homogenization after uphill shifts in montane areas of northern Spain. Oecologia 173:1649–1660

    Article  PubMed  Google Scholar 

  • Price MV, Waser NM, Irwin RE, Campbell DR, Brody AK (2005) Temporal and spatial variation in pollination of a montane herb: a seven-year study. Ecology 86(8):2106–2116

    Article  Google Scholar 

  • Rausher MD (2008) Evolutionary transitions in floral color. Int J Plant Sci 169(1):7–21

    Article  CAS  Google Scholar 

  • Rodríguez-Gironés MA, Santamaría L (2004) Why are so many bird flowers red? PLoS Biol 2:e350

    Article  PubMed Central  PubMed  Google Scholar 

  • Rodríguez-Gironés MA, Santamaría L (2005) Resource partitioning among flower visitors and evolution of nectar concealment in multi-species communities. Proc Biol Sci 272:187–192

    Article  PubMed Central  PubMed  Google Scholar 

  • Rossi M (2011) Taxonomy, phylogeny and reproductive ecology of Gentiana lutea L. Dissertation. Universitá degli studi di Bologna, Bologna

    Google Scholar 

  • Schemske DW, Bierzychudek P (2007) Spatial differentiation for flower color in the desert annual Linanthus parryae: was Wright right? Evolution 61:2528–2543

    Article  PubMed  Google Scholar 

  • Spaethe J, Tautz J, Chittka L (2001) Visual constraints in foraging bumblebees: flower size and color affect search time and flight behavior. Proc Natl Acad Sci USA 98:3898–3903

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • StatSoft Inc. (2001) STATISTICA (data analysis software system), version 6. StatSoft Inc., Tulsa

    Google Scholar 

  • Strauss SY, Irwin RE (2004) Ecological and evolutionary consequences of multispecies plant–animal interactions. Annu Rev Ecol Evol Syst 35:435–466

    Article  Google Scholar 

  • Strauss SY, Whittall JB (2006) Non-pollinator agents of selection on floral traits. In: Harder LD, Barret SCH (eds) Ecology and evolution of flowers. Oxford University Press, New York, pp 120–138

    Google Scholar 

  • Strauss SY, Irwin RE, Lambrix VM (2004) Optimal defence theory and flower petal colour predict variation in the secondary chemistry of wild radish. J Ecol 92:132–141

    Article  Google Scholar 

  • Streisfeld MA, Kohn JR (2005) Contrasting patterns of floral and molecular variation across a cline in Mimulus aurantiacus. Evolution 59:2548–2559

    Article  CAS  PubMed  Google Scholar 

  • Streisfeld MA, Kohn JR (2007) Environment and pollinator-mediated selection on parapatric floral races of Mimulus aurantiacus. J Evol Biol 20:122–132

    Article  CAS  PubMed  Google Scholar 

  • Struwe L, Albert VA (2002) Gentianaceae: systematics and natural history. Cambridge University Press, Cambridge

    Google Scholar 

  • Tanaka Y, Ohmiya A (2008) Seeing is believing: engineering anthocyanin and carotenoid biosynthetic pathways. Curr Opin Biotechnol 19:190–197

    Article  CAS  PubMed  Google Scholar 

  • Tanaka Y, Sasaki N, Ohmiya A (2008) Biosynthesis of plant pigments: anthocyanins, betalains and carotenoids. Plant J 54:733–749

    Article  CAS  PubMed  Google Scholar 

  • Veiga T, Galetto L, Machado I (2013) Nectar regulation in Euphorbia tithymaloides L., a hummingbird pollinated Euphorbiaceae. Plant Biol 15:910–918

  • Zhu C, Yamamura S, Koiwa H, Nishihara M, Sandmann G (2002) cDNA cloning and expression of carotenogenic genes during flower development in Gentiana lutea. Plant Mol Biol 48:277–285

    Article  CAS  PubMed  Google Scholar 

  • Zhu C, Yamamura S, Nishihara M, Koiwa H, Sandmann G (2003) cDNAs for the synthesis of cyclic carotenoids in petals of Gentiana lutea and their regulation during flower development. Biochim Biophys Acta 1625:305–308

    Article  CAS  PubMed  Google Scholar 

  • Zhu C, Bai C, Sanahuja G, Yuan D, Farré G, Naqvi S, Shi L, Capell T, Christou P (2010) The regulation of carotenoid pigmentation in flowers. Arch Biochem Biophys 504:132–141

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors thank P. Domínguez for field assistance and E. Ploquin for bumblebees identification. Two anonymous reviewers and M. A. Rodríguez-Gironés made useful comments on a previous version of this manuscript. This work was financed by the Plan Nacional de I+D+I (2008–2011), CGL2009-08959 Ministerio de Ciencia. T.V. was supported by a PhD grant from the Plan Galego de Investigación e Crecemento 2011/2015 (Plan I2C), Consellería de Cultura, Educación e Ordenación Universitaria.

Author information

Authors and Affiliations

  1. Department of Botany, University of Santiago de Compostela, Santiago de Compostela, 15782, Galicia, Spain

    Tania Veiga, Javier Guitián & Pablo Guitián

  2. Area of Ecology, University of Santiago de Compostela, Santiago de Compostela, 15782, Galicia, Spain

    José Guitián

  3. Department of Biology, Stanford University, 385 Serra Mall, Stanford, CA, 94305, USA

    Mar Sobral

Authors
  1. Tania Veiga
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Javier Guitián
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Pablo Guitián
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. José Guitián
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mar Sobral
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Tania Veiga.

Appendix

Appendix

UV light reflectance

UV light may influence pollinator choices but, if there are no differences on the UV light among orange and yellow flowering plants, we might conclude that pollinators may not distinguish the orange-flowered plants from the yellow-flowered plants due to UV light. So, we studied the UV reflectance variation among individuals associated to flower color in this species. We randomly selected 100 plants belonging to nine monomorphic populations (five orange and four yellow populations). Details of the procedure to obtain the spectra measures are identical to those described in “Materials and methods” section. We considered reflectance between 300 and 400 nm at each 10 nm intervals. Thus, UV color of each plant was described by 11 reflectance variables. We reduced those variables by means of a principal components analysis (PCA) to a single variable (which explained 75 % of the variance) describing UV reflectance. We run an analysis of variance with the first PCA component (UV reflectance) as the dependent variable. Color (orange or yellow) and population nested in color (since populations were monomorphic), were the independent variables.

None of those factors were statistically significant (F7,91 = 1.77, P = 0.10; F1,91 = 1.54, P = 0.22; respectively for population and color), which indicates that orange and yellow-flowered plants do not differ in the UV pattern of reflectance (Fig. 3) that there are not differences in the UV reflectance among populations.

Fig. 3
figure 3

Average spectra reflectance for yellow (grey line) and orange-flowered plants (black line). Data come from 100 plants selected randomly from four yellow and five orange populations

Full size image

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Veiga, T., Guitián, J., Guitián, P. et al. Are pollinators and seed predators selective agents on flower color in Gentiana lutea?. Evol Ecol 29, 451–464 (2015). https://doi.org/10.1007/s10682-014-9751-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10682-014-9751-6

Keywords

Search

Navigation