Advertisement

Intraspecific floral color variation as perceived by pollinators and non-pollinators: evidence for pollinator-imposed constraints?

  • Kellen C. Paine
  • Thomas E. White
  • Kenneth D. WhitneyEmail author
Natural History Note

Abstract

Pollinator-mediated selection is expected to constrain floral color variation within plant populations, yet populations with high color variation (at least in human visual space) are common in nature. To explore this paradox, we collected floral reflectance spectra for 34 populations of 14 putatively bee-pollinated plant species of north-central New Mexico, USA, and translated them into three different animal visual spaces. We asked, (1) is intrapopulation variation in flower color constrained to be lower than the discrimination threshold of the putative dominant pollinators? And, (2) is perceived intrapopulation variation in flowers higher for non-pollinating animals than it is for the presumed dominant pollinator group? We found evidence consistent with some pollinator-imposed constraints on floral color in our species, with the majority (70.6%) of populations having > 95% of flower–flower or flower-centroid comparisons (where the centroid represents the mean phenotype) estimated to be visually indiscriminable to bees. We also found that perceived floral color variation was significantly greater for two non-pollinating groups—birds and humans—than for bees. Our results suggest that a large portion of human-perceived floral color variation within populations persists because it is effectively invisible to pollinators. In this scenario, human-perceived color may evolve neutrally (via drift) or via indirect selection on correlated characters such as herbivore- or drought-resistance, consistent with previous studies identifying non-pollinator agents of selection on flower color.

Keywords

Plant–pollinator interactions Signalling Reflectance spectra Bee vision Natural selection Color polymorphism 

Notes

Acknowledgements

Thanks to Jennifer A. Rudgers, Diane L. Marshall, Mary C. “Cassie” Stoddard, and members of the Rudgers–Whitney lab group for helpful suggestions on the study and the manuscript. Funding was provided by the University of New Mexico Harry Wayne Springfield Fellowship (to K.C.P.), the Society for the Study of Evolution Rosemary Grant Award (to K.C.P.), and NSF DEB 1257965 (to K.D.W.). The authors declare no conflicts of interest.

Supplementary material

10682_2019_9991_MOESM1_ESM.pdf (1.5 mb)
Supplementary material 1 (PDF 1576 kb)
10682_2019_9991_MOESM2_ESM.pdf (1.2 mb)
Supplementary material 2 (PDF 1225 kb)
10682_2019_9991_MOESM3_ESM.pdf (1.2 mb)
Supplementary material 3 (PDF 1247 kb)

References

  1. Bennett ATD, Théry M (2007) Avian color vision and coloration: multidisciplinary evolutionary biology. Am Nat 169:S1–S6CrossRefGoogle Scholar
  2. Briscoe AD, Chittka L (2001) The evolution of color vision in insects. Annu Rev Entomol 46:471–510CrossRefGoogle Scholar
  3. Buchmann SL (1985) Bees use vibration to aid pollen collection from non-poricidal flowers. J Kansas Entomol Soc 58:517–525Google Scholar
  4. Campbell DR, Bischoff M, Lord JM, Robertson AW (2012) Where have all the blue flowers gone: pollinator responses and selection on flower colour in New Zealand Wahlenbergia albomarginata. J Evol Biol 25:352–364CrossRefGoogle Scholar
  5. 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 171:1020–1028CrossRefGoogle Scholar
  6. Chittka L (1992) The colour hexagon: a chromaticity diagram based on photoreceptor excitations as a generalized representation of colour opponency. J Comp Physiol A 170:533–534Google Scholar
  7. Chittka L, Kevan PG (2005) Flower colors as advertisement. In: Dafni A, Kevan PG, Husband B (eds) Practical Pollination Biology. Enviroquest, Cambridge, Canada, pp 157–196Google Scholar
  8. Cockerell TDA (1906) The bees of New Mexico. Trans Am Entomol Soc 32:289–314Google Scholar
  9. Cuthill IC, Bennett ATD, Partridge JC, Maier EJ (1999) Plumage reflectance and the objective assessment of avian sexual dichromatism. Am Nat 153:183–200CrossRefGoogle Scholar
  10. Dalrymple RL, Hui FKC, Flores-Moreno H et al (2015) Roses are red, violets are blue—so how much replication should you do? An assessment of variation in the colour of flowers and birds. Biol J Linn Soc 114:69–81CrossRefGoogle Scholar
  11. De Ibarra NH, Vorobyev M, Menzel R (2014) Mechanisms, functions and ecology of colour vision in the honeybee. J Comp Physiol A 200:411–433CrossRefGoogle Scholar
  12. Dyer AG (2006) Discrimination of flower colours in natural settings by the bumblebee species Bombus terrestris (Hymenoptera: Apidae). Entomol Gen 28:257–268CrossRefGoogle Scholar
  13. Dyer AG (2012) The mysterious cognitive abilities of bees: why models of visual processing need to consider experience and individual differences in animal performance. J Exp Biol 215:387–395CrossRefGoogle Scholar
  14. Dyer AG, Chittka L (2004) Fine colour discrimination requires differential conditioning in bumblebees. Naturwissenschaften 91:224–227CrossRefGoogle Scholar
  15. Dyer AG, Neumeyer C (2005) Simultaneous and successive colour discrimination in the honeybee (Apis mellifera). J Comp Physiol A 191:547–557CrossRefGoogle Scholar
  16. Dyer AG, Boyd-Gerny S, McLoughlin S et al (2012) Parallel evolution of angiosperm colour signals: common evolutionary pressures linked to hymenopteran vision. Proc R Soc B Biol Sci 279:3606–3615CrossRefGoogle Scholar
  17. Eaton MD (2005) Human vision fails to distinguish widespread sexual dichromatism among sexually “monochromatic” birds. Proc Natl Acad Sci 102:10942–10946CrossRefGoogle Scholar
  18. Eckhart VM, Rushing NS, Hart GM, Hansen JD (2006) Frequency-dependent pollinator foraging in polymorphic Clarkia xantiana ssp. xantiana populations: implications for flower colour evolution and pollinator interactions. Oikos 112:412–421CrossRefGoogle Scholar
  19. Endler JA, Mielke PW (2005) Comparing entire colour patterns as birds see them. Biol J Linn Soc 86:405–431CrossRefGoogle Scholar
  20. Fairchild MD (2013) Color appearance models, 3rd edn. Wiley, ChichesterCrossRefGoogle Scholar
  21. Fenster CB, Armbruster W, Wilson P et al (2004) Pollination syndromes and floral specialization. Annu Rev Ecol Evol Syst 35:375–403CrossRefGoogle Scholar
  22. Frey FM (2004) Opposing natural selection from herbivores and pathogens may maintain floral-color variation in Claytonia virginica (Portulacaceae). Evolution 58:2426–2437CrossRefGoogle Scholar
  23. Frey FM, Dunton J, Garland K (2011) Floral color variation and associations with fitness-related traits in Malva moschata (Malvaceae). Plant Spec Biol 26:235–243CrossRefGoogle Scholar
  24. Fry JD, Rausher MD (1997) Selection on a floral color polymorphism in the tall morning glory (Ipomoea purpurea): transmission success of the alleles through pollen. Evolution 51:66–78Google Scholar
  25. Garcia JE, Spaethe J, Dyer AG (2017) The path to colour discrimination is S-shaped: behaviour determines the interpretation of colour models. J Comp Physiol A 203:983–997CrossRefGoogle Scholar
  26. Garcia JE, Shrestha M, Dyer AG (2018) Flower signal variability overwhelms receptor-noise and requires plastic color learning in bees. Behav Ecol 29:1286–1297Google Scholar
  27. Gegear RJ, Laverty TM (2001) The effect of variation among floral traits on the flower constancy of pollinators. In: Chittka L, Thomson JD (eds) Cognitive ecology of pollination. Cambridge University Press, Cambridge, pp 1–20Google Scholar
  28. 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
  29. Gray M, Stansberry MJ, Lynn JS et al (2018) Consistent shifts in pollinator-relevant floral coloration along Rocky Mountain elevation gradients. J Ecol 106:1910–1924CrossRefGoogle Scholar
  30. Hannan GL (1981) Flower color polymorphism and pollination biology of Platystemon californicus Benth. (Papaveraceae). Am J Bot 68:233CrossRefGoogle Scholar
  31. Hart NS (2001) The visual ecology of avian photoreceptors. Prog Retin Eye Res 20:675–703CrossRefGoogle Scholar
  32. Hersch EI, Roy BA (2007) Context-dependent pollinator behavior: an explanation for patterns of hybridization among three species of indian paintbrush. Evolution 61:111–124CrossRefGoogle Scholar
  33. Hessing MB (1988) Geitonogamous pollination and its consequences in Geranium caespitosum. Am J Bot 75:1324–1333CrossRefGoogle Scholar
  34. Hurd PD Jr, LaBerge WE, Linsley EG (1980) Principal sunflower bees of North America with emphasis on the Southwestern United States (Hymenoptera, Apoidea). Smithsonian Contributions to Zoology 310:1–158CrossRefGoogle Scholar
  35. Irwin RE, Strauss SY (2005) Flower color microevolution in wild radish: evolutionary response to pollinator-mediated selection. Am Nat 165:225–237Google Scholar
  36. Irwin RE, Strauss SY, Emerson A, Guibert G (2003) The role of herbivores in the maintenance of a flower-color polymorphism in wild radish. Ecology 84:1733–1743CrossRefGoogle Scholar
  37. Jones KN (1996) Fertility selection on a discrete floral polymorphism in Clarkia (Onagraceae). Evolution 50:71–79CrossRefGoogle Scholar
  38. Kantsa A, Raguso RA, Dyer AG, Sgardelis SP, Olesen JM, Petanidou T (2017) Community-wide integration of floral colour and scent in a Mediterranean scrubland. Nat Ecol Evol 1:1502–1510CrossRefGoogle Scholar
  39. Keasar T, Gerchman Y, Lev-Yadun S (2016) A seven-year study of flower-color polymorphism in a Mediterranean annual plant. Basic Appl Ecol 17:741–750CrossRefGoogle Scholar
  40. Kelber A, Vorobyev M, Osorio D (2003) Animal colour vision—behavioural tests and physiological concepts. Biol Rev Camb Philos 78:81–118CrossRefGoogle Scholar
  41. Kemp DJ, Herberstein ME, Fleishman LJ et al (2015) An integrative framework for the appraisal of coloration in nature. Am Nat 185:705–724CrossRefGoogle Scholar
  42. King C, Ballantyne G, Willmer PG (2013) Why flower visitation is a poor proxy for pollination: measuring single-visit pollen deposition, with implications for pollination networks and conservation. Methods Ecol Evol 4:811–818CrossRefGoogle Scholar
  43. LaDuke JC (1985) A new species of Sphaeralcea (Malvaceae). Southwest Nat 30:433CrossRefGoogle Scholar
  44. Levin DA, Kerster HW (1967) Natural selection for reproductive isolation in Phlox. Evolution 21:679–687CrossRefGoogle Scholar
  45. Lewis MB, Schupp EW (2014) Reproductive ecology of the endangered Utah endemic Hesperidanthus suffrutescens with implications for conservation. Am Midl Nat 172:236–251CrossRefGoogle Scholar
  46. Lowe AD, Foltz-Sweat JL (2017) Effect of floral diversity and urbanization on bee species community composition in Phoenix, Arizona. J Arizona Nevada Acad Sci 47:6–18CrossRefGoogle Scholar
  47. Maia R, White TE (2018) Comparing colors using visual models. Behav Ecol 29:649–659CrossRefGoogle Scholar
  48. Maia R, Gruson H, Endler JA, White TE (2019) pavo 2: new tools for the spectral and spatial analysis of colour in R. Methods Ecol Evol Early View.  https://doi.org/10.1111/2041-210X.13174 Google Scholar
  49. Miller RB (1981) Hawkmoths and the geographic patterns of floral variation in Aquilegia caerulea. Evolution 35:763–774CrossRefGoogle Scholar
  50. Mu J, Li G, Niklas KJ, Sun S (2011) Difference in floral traits, pollination, and reproductive success between white and blue flowers of Gentiana leucomelaena (Gentianaceae) in an alpine meadow. Arct Antarct Alp Res 43:410–416CrossRefGoogle Scholar
  51. Ng L, Garcia JE, Dyer AG (2018) Why colour is complex: evidence that bees perceive neither brightness nor green contrast in colour signal processing. Facets 3:800–817CrossRefGoogle Scholar
  52. Olsson P, Lind O, Kelber A (2017) Chromatic and achromatic vision: parameter choice and limitations for reliable model predictions. Behav Ecol 29:273–282CrossRefGoogle Scholar
  53. Ortiz PL, Berjano R, Talavera M et al (2015) Flower colour polymorphism in Lysimachia arvensis: How is the red morph maintained in Mediterranean environments? Perspect Plant Ecol 17:142–150CrossRefGoogle Scholar
  54. Papiorek S, Rohde K, Lunau K (2013) Bees’ subtle colour preferences: how bees respond to small changes in pigment concentration. Naturwissenschaften 100:633–643CrossRefGoogle Scholar
  55. Peitsch D, Fietz A, Hertel H et al (1992) The spectral input systems of hymenopteran insects and their receptor-based colour vision. J Comp Physiol A 170:23–40CrossRefGoogle Scholar
  56. Pendery BM, Rumbaugh MD (1993) Globemallows. Rangelands 15:127–130Google Scholar
  57. R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  58. Rausher MD (2008) Evolutionary transitions in floral color. Int J Plant Sci 169:7–21CrossRefGoogle Scholar
  59. Rausher MD, Fry JD (1993) Effects of a locus affecting floral pigmentation in Ipomoea purpurea on female fitness components. Genetics 134:1237–1247Google Scholar
  60. Renoult JP, Thomann M, Schaefer HM, Cheptou P-O (2013) Selection on quantitative colour variation in Centaurea cyanus: the role of the pollinator’s visual system. J Evol Biol 26:2415–2427CrossRefGoogle Scholar
  61. Renoult JP, Kelber A, Schaefer HM (2017) Colour spaces in ecology and evolutionary biology. Biol Rev 92:292–315CrossRefGoogle Scholar
  62. Rozen JG Jr, Rozen BL (1986) Bionomics of crepuscular bees associated with the plant Psorothamnus scoparius (Hymenoptera: Apoidea). J New YorkEntomol S 94:472–479Google Scholar
  63. Ruxton GD, Schaefer HM (2016) Floral colour change as a potential signal to pollinators. Curr Opin Plant Biol 32:96–100CrossRefGoogle Scholar
  64. Schemske DW, Bierzychudek P (2001) Perspective: evolution of flower color in the desert annual Linanthus parryae: wright revisited. Evolution 55:1269–1282CrossRefGoogle Scholar
  65. Schemske DW, Bierzychudek P (2007) Spatial differentiation for flower color in the desert annual Linanthus parryae: was wright right? Evolution 61:2528–2543CrossRefGoogle Scholar
  66. Schiestl FP, Johnson SD (2013) Pollinator-mediated evolution of floral signals. Trends Ecol Evol 28:307–315CrossRefGoogle Scholar
  67. Schoen DJ, Giannasi DE, Ennos RA, Clegg MT (1984) Stem color and pleiotropy of genes determining flower color in the common morning glory. J Hered 75:113–116CrossRefGoogle Scholar
  68. Shrestha M, Dyer AG, Boyd-Gerny S et al (2013) Shades of red: bird-pollinated flowers target the specific colour discrimination abilities of avian vision. New Phytol 198:301–310CrossRefGoogle Scholar
  69. Smithson A (2001) Pollinator preference, frequency dependence, and floral evolution. In: Chittka L, Thomson JD (eds) Cognitive ecology of pollination. Cambridge University Press, Cambridge, pp 237–258CrossRefGoogle Scholar
  70. Stanton ML, Snow AA, Handel SN, Bereczky J (1989) The impact of a flower-color polymorphism on mating patterns in experimental populations of wild radish (Raphanus raphanistrum L.). Evolution 43:335–346CrossRefGoogle Scholar
  71. 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 92:132–141CrossRefGoogle Scholar
  72. Sussman RW, Raven PH (1978) Pollination by lemurs and marsupials: an archaic coevolutionary system. Science 200:731–736CrossRefGoogle Scholar
  73. Tang XX, Liu HL, Zhang C et al (2016) Flower colour polymorphism in Geranium nepalense (Geraniaceae): adaptation to non-pollinator agents. Pol J Ecol 64:526–533CrossRefGoogle Scholar
  74. Tyrl RJ, Erteeb FB, Bruner JL et al (1984) A biosystematic study of the relationship of Nama hispidum and Nama stevensii (Hydrophyllaceae). Southwest Nat 29:367CrossRefGoogle Scholar
  75. Vaidya P, McDurmon A, Mattoon E et al (2018) Ecological causes and consequences of flower color polymorphism in a self-pollinating plant (Boechera stricta). New Phytol 218:380–392CrossRefGoogle Scholar
  76. Veiga T, Guitián J, Guitián P et al (2015) Are pollinators and seed predators selective agents on flower color in Gentiana lutea? Evol Ecol 29:451–464CrossRefGoogle Scholar
  77. Vorobyev M, Osorio D (1998) Receptor noise as a determinant of colour thresholds. Proc R Soc B Biol Sci 265:351–358CrossRefGoogle Scholar
  78. Warren J, Mackenzie S (2001) Why are all colour combinations not equally represented as flower-colour polymorphisms? New Phytol 151:237–241CrossRefGoogle Scholar
  79. Waser NM, Price MV (1981) Pollinator choice and stabilizing selection for flower color in Delphinium nelsonii. Evolution 35:376–390CrossRefGoogle Scholar
  80. Waser NM, Price MV (1983) Pollinator behaviour and natural selection for flower colour in Delphinium nelsonii. Nature 302:422–424CrossRefGoogle Scholar
  81. White TE, Dalrymple RL, Noble DWA et al (2015) Reproducible research in the study of biological coloration. Anim Behav 106:51–57CrossRefGoogle Scholar
  82. Wolfe LM (1993) Reproductive consequences of a flower color polymorphism in Hydrophyllum appendiculatum. Am Midl Nat 129:405–408CrossRefGoogle Scholar
  83. Wolfe LM (2001) Associations among multiple floral polymorphisms in Linum pubescens (Linaceae), a heterostylous plant. Int J Plant Sci 162:335–342CrossRefGoogle Scholar
  84. Wolfe LM, Sellers SE (1997) Polymorphic floral traits in Linaria canadensis (Scrophulariaceae). The Am Midl Nat 138:134–139CrossRefGoogle Scholar
  85. Wyszecki G, Stiles WS (2000) Color science: concepts and methods, quantitative data and formulae, 2nd edn. Wiley, New YorkGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Department of Biology, MSC03 2020University of New MexicoAlbuquerqueUSA
  2. 2.School of Life and Environmental SciencesThe University of SydneySydneyAustralia

Personalised recommendations