Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

The evolution of warning signals

Nature volume 394, pages 882–884 (1998)Cite this article

Abstract

Warning coloration signals are a familiar and conspicuous phenomenon in nature. However, the fundamental question of how warning signals initially evolved remains unanswered. For an unpalatable prey to evolve a signal to indicate its unprofitability, a rare and conspicuous mutant in a population of unpalatable cryptic prey must overcome a double disadvantage: a greater risk of being detected (as a result of being more conspicuous) and of being attacked (because its rarity results in a decreased association with aversion) by a predator1,2. Although the prior evolution of prey gregariousness may help warning signals to evolve3,4,5,6,7,8, such an evolutionary order may not always be the case4,9,10,11. Here we present a theoretical model that describes a mechanism for the evolution of warning signals without having to invoke gregariousness. Specifically, a predator's generalization of stimulus in associative learning, with a ‘peak shift’ towards greater conspicuousness5,12,13,14,15, allows a warning signal to evolve when the prey population density exceeds a threshold. Once a warning signal starts to evolve, it continues to grow; the resulting, evolutionarily stable16 conspicuousness of prey is discontinuously greater than that of the original cryptic prey, drawing an unambiguous distinction in their appearance.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: The stochastic change in the level of associative memories of a predator who randomly searches a prey population consisting of two prey types.
Figure 2: The evolutionary dynamics of the degree x of conspicuousness oftheprey population for the case in which a( y,x,u) = u(0.1 + x)/(1 + x) × exp(−( x − y)2)(1 − 0.5 exp(− y)), u = 1 and p( x) = x/(1 + x).

Similar content being viewed by others

References

  1. Guilford, T. The evolution of conspicuous coloration. Am. Nat. 131 , S7–S21 (1988).

    Article  Google Scholar 

  2. Guilford, T. in Insect Defenses (eds Evans, D. L. & Schmidt, J. O.) 23– 61 (State Univ. New York Press, (1990)).

  3. Fisher, R. A. The Genetical Theory of Natural Selection (Clarendon, Oxford, ( 1930)).

  4. Harvey, P. H., Bull, J. J. & Paxton, R. J. Why some insects look pretty nasty. New Sci. 97, 26–27 ( 1983)).

    Google Scholar 

  5. Leimar, O., Enquist, M. & Sillén-Tullberg, B. Evolutionary stability of aposematic coloration and prey unprofitability: a theoretical analysis. Am. Nat. 128, 469–490 (1986).

    Article  Google Scholar 

  6. Mallet, J. & Singer, M. Individual selection, kin selection, and the shifting balance in the evolution of warning colours: the evidence from butterflies. Biol. J. Linn. Soc. 32, 337–350 (1987).

    Article  Google Scholar 

  7. Gagliardo, A. & Guilford, T. Why do warning-coloured prey live gregariously? Proc. R. Soc. Lond. B 251, 69–74 (1993).

    Article  ADS  Google Scholar 

  8. Alatalo, R. V. & Mappes, J. Tracking the evolution of warning signals. Nature 382, 708– 710 (1996).

    Article  ADS  CAS  Google Scholar 

  9. Sillén-Tullberg, B. Evolution of gregariousness in aposematic butterfly larvae: a phylogenetic analysis. Evolution 42, 293– 305 (1988).

    Article  Google Scholar 

  10. Tullberg, B. S. & Hunter, A. F. Evolution of larval gregariousness in relation to repellent defences and warning coloration in tree-feeding Macrolepidoptera: a phylogenetic analysis based on independent contrasts. Biol. J. Linn. Soc. 57, 253– 276 (1996).

    Article  Google Scholar 

  11. Sillén-Tullberg, B. The effect of biased inclusion of taxa on the correlation between discrete characters in phylogenetic trees. Evolution 47, 1182–1191 (1993).

    Article  Google Scholar 

  12. Weary, D. M., Guilford, T. C. & Weisman, R. G. Aproduct of discriminative learning may lead to female preferences for elaborate males. Evolution 47, 333–336 (1993).

    Article  CAS  Google Scholar 

  13. Leimar, O. & Tuomi, J. Synergistic selection and graded traits. Evol. Ecol. 12, 59–71 (1998).

    Article  Google Scholar 

  14. Gamberale, G. & Tullberg, B. S. Evidence for a peak-shift in predator generalization among aposematic prey. Proc. R& Soc. Lond. B 263, 1329–1334 ( 1996).

    Article  ADS  CAS  Google Scholar 

  15. Hanson, H. M. Effects of discrimination training on stimulus generalization. J. Exp. Psychol. 58, 321–334 (1959).

    Article  CAS  Google Scholar 

  16. Maynard Smith, J. Evolution and the Theory of Games (Cambridge Univ. Press, Cambridge, (1982)).

  17. Gittleman, J. L. & Harvey, P. H. Why are distasteful prey not cryptic? Nature 286, 149– 150 (1980).

    Article  ADS  Google Scholar 

  18. Roper, T. J. & Redston, S. Conspicuousness of distasteful prey affects the strength and durability of one-trail avoidance learning. Anim. Behav. 35, 739–747 (1987).

    Article  Google Scholar 

  19. Owen, R. E. & Owen, A. R. G. Mathematical paradigms for mimicry: recurrent sampling. J. Theor. Biol. 109, 217–247 (1984).

    Article  MathSciNet  Google Scholar 

  20. Guilford, T. Evolutionary pathways of aposematism. Oecologica 11 , 835–841 (1990).

    Google Scholar 

  21. Endler, J. A. Frequency-dependent predation, crypsis and aposematic coloration. Phil. Trans. R. Soc. Lond. B 319, 505– 523 (1988).

    Article  ADS  CAS  Google Scholar 

  22. Karlin, S. A First Course in Stochastic Processes (Academic, New York, ( 1969)).

  23. Schuler, W. & Roper, T. J. Responses to warning coloration in avian predators. Adv. Study Behav. 21, 111–146 (1992).

    Article  Google Scholar 

Download references

Acknowledgements

We thank N. Yamamura for discussions; O. Takeyama for technical advice; and J.Lawton and the NERC Centre for Population Biology for hospitality and discussions offered to M.H. in finalizing the manuscript. This work was supported by an MESSC grant to M.H.

Author information

Authors and Affiliations

  1. Laboratoire d'Ecologie, UMR 7625, Ecole Normale Supérieure, 46 rue d'Ulm, Paris, F-75230 Cedex 05, France

    Shigeo Yachi

  2. Center for Ecological Research, Kyoto University, 606-01, Kyoto, Japan

    Masahiko Higashi

Authors
  1. Shigeo Yachi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Masahiko Higashi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Masahiko Higashi.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Yachi, S., Higashi, M. The evolution of warning signals. Nature 394, 882–884 (1998). https://doi.org/10.1038/29751

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/29751

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing