Visual predators select for crypticity and polymorphism in virtual prey

Abstract

Cryptically coloured animals commonly occur in several distinct pattern variants. Such phenotypic diversity may be promoted by frequency-dependent predation, in which more abundant variants are attacked disproportionately often, but the hypothesis has never been explicitly tested. Here we report the first controlled experiment on the effects of visual predators on prey crypticity and phenotypic variance, in which blue jays (Cyanocitta cristata) searched for digital moths on computer monitors. Moth phenotypes evolved via a genetic algorithm in which individuals detected by the jays were much less likely to reproduce. Jays often failed to detect atypical cryptic moths, confirming frequency-dependent selection and suggesting the use of searching images, which enhance the detection of common prey. Over successive generations, the moths evolved to become significantly harder to detect, and they showed significantly greater phenotypic variance than non-selected or frequency-independent selected controls.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Figure 1: Samples of digital moths, shown on uniform grey (left) and cryptically textured (right) backgrounds, from the parental population, P0 (a), and from the F100 generations from the non-selected lines (b), the frequency-independent selection lines (c), and the experimental lines selected by the jays (d).
Figure 2: Detection accuracy of blocks of 100 trials as a function of crypticity of the target moth and dissimilarity between the target and the last previous correctly detected moth.
Figure 3: Changes in mean crypticity across successive generations in the three experimental lines (plotted with symbols), contrasted with the distribution of values from the two sets of control lines.
Figure 4: Changes in phenotypic variance of the digital moth population in the three experimental lines (plotted with symbols), contrasted with the distribution of values from the two sets of control lines.

References

  1. 1

    Dearn, J. M. in Biology of Grasshoppers (ed. Chapman, R. F. & Joern, A.) 517–549 (Wiley, New York, 1990).

    Google Scholar 

  2. 2

    Halkka, O. & Halkka, L. Population genetics of the polymorphic meadow spittlebug, Philaenus spumarius (L.). Evol. Biol. 24, 149–191 (1990).

    Google Scholar 

  3. 3

    Edmunds, M. in Insect Defenses (ed. Evans, D. L. & Schmidt, J. O.) 3–21 (SUNY, Albany, New York, 1990).

    Google Scholar 

  4. 4

    Whiteley, D. A. A., Owen, D. F. & Smith, D. A. S. Massive polymorphism and natural selection in Donacilla cornea (Poli, 1791) (Bivalvia: Mesodesmatidae). Biol. J. Linn. Soc. 62, 475–494 (1997).

    Google Scholar 

  5. 5

    Sargent, T. D. Legion of Night: The Underwing Moths (Univ. Massachusetts Press, Amherst, 1976).

    Google Scholar 

  6. 6

    Sargent, T. D. On the maintenance of stability in hindwing diversity among moths of the genus Catocala (Lepidoptera: Noctuidae). Evolution 32, 424–434 (1978).

    Article  Google Scholar 

  7. 7

    Barnes, W. & McDunnough, J. H. Illustrations of the North American species of the genus Catocala. Mem. Am. Mus. Nat. Hist. 3, part 1, 1–47 (1918).

    Google Scholar 

  8. 8

    Owen, D. F. & Whiteley, D. Reflexive selection: Moment's hypothesis resurrected. Oikos 47, 117–1120 (1986).

    Article  Google Scholar 

  9. 9

    Common, I. F. B. A study of the ecology of the adult bogong moth, Agrotis infusa (Boisd.) (Lepidoptera: Noctuidae), with special reference to its behaviour during migration and aestivation. Aust. J. Zool. 2, 223–263 (1954).

    Article  Google Scholar 

  10. 10

    Pruess, K. P. Migration of the army cutworm, Chorizagrotis auxiliaris (Lepidoptera: Noctuidae). I. Evidence for a migration. Ann. Entomol. Soc. Am. 60, 910–920 (1967).

    Article  Google Scholar 

  11. 11

    Clarke, B. C. in Taxonomy and Geography (ed. Nichols, D.) 47–70 (Systematics Association, Oxford, 1962).

    Google Scholar 

  12. 12

    Allen, J. A. Frequency-dependent selection by predators. Phil. Trans. R. Soc. Lond. B 319, 485–503 (1988).

    ADS  CAS  Article  Google Scholar 

  13. 13

    Poulton, E. B. The Colours of Animals (Appleton, New York, 1890).

    Google Scholar 

  14. 14

    Tinbergen, L. The natural control of insects in pine woods. I. Factors influencing the intensity of predation by songbirds. Arch. Néerlandaises Zool. 13, 265–343 (1960).

    Article  Google Scholar 

  15. 15

    Bond, A. B. & Riley, D. A. Searching image in the pigeon: A test of three hypothetical mechanisms. Ethology 87, 203–224 (1991).

    Article  Google Scholar 

  16. 16

    Reid, P. J. & Shettleworth, S. J. Detection of cryptic prey: Search image or search rate? J. Exp. Psychol. Anim. Behav. Process 18, 273–286 (1992).

    CAS  Article  Google Scholar 

  17. 17

    Langley, C. M. Search images: Selective attention to specific visual features of prey. J. Exp. Psychol. Anim. Behav. Process 22, 152–163 (1996).

    CAS  Article  Google Scholar 

  18. 18

    Bond, A. B. & Kamil, A. C. Searching image in blue jays: Facilitation and interference in sequential priming. Anim. Learn. Behav. 27, 461–471 (1999).

    Article  Google Scholar 

  19. 19

    Bond, A. B. & Kamil, A. C. Apostatic selection by blue jays produces balanced polymorphism in virtual prey. Nature 395, 594–596 (1998).

    ADS  CAS  Article  Google Scholar 

  20. 20

    Rand, A. S. Predator–prey interactions and the evolution of aspect diversity. Atlas Simp. Biota Amazônica 5, 73–83 (1967).

    Google Scholar 

  21. 21

    Ricklefs, R. E. & O'Rourke, K. Aspect diversity in moths: A temperate-tropical comparison. Evolution 29, 313–324 (1975).

    Article  Google Scholar 

  22. 22

    Allen, J. A. Reflexive selection is apostatic selection. Oikos 51, 251–253 (1988).

    Article  Google Scholar 

  23. 23

    Pietrewicz, A. T. & Kamil, A. C. Visual detection of cryptic prey by blue jays (Cyanocitta cristata). Science 195, 580–582 (1977).

    ADS  CAS  Article  Google Scholar 

  24. 24

    Pietrewicz, A. T. & Kamil, A. C. Search image formation in the blue jay (Cyanocitta cristata). Science 204, 1332–1333 (1979).

    ADS  CAS  Article  Google Scholar 

  25. 25

    Kono, H., Reid, P. J. & Kamil, A. C. The effect of background cuing on prey detection. Anim. Behav. 56, 963–972 (1998).

    CAS  Article  Google Scholar 

  26. 26

    Fleishman, L. J., McClintock, W. J., D'Erth, R. B., Brainard, D. M. & Endler, J. A. Colour perception and the use of video playback experiments in animal behaviour. Anim. Behav. 56, 1035–1040 (1998).

    CAS  Article  Google Scholar 

  27. 27

    Robinson, R. Lepidopteran Genetics (Pergamon, Oxford, 1971).

    Google Scholar 

  28. 28

    Nijhout, H. F. The Development and Evolution of Butterfly Wing Patterns (Smithsonian Institution, Washington DC, 1991).

    Google Scholar 

  29. 29

    Carroll, S. B. et al. Pattern formation and eyespot determination in butterfly wings. Science 265, 109–114 (1994).

    ADS  CAS  Article  Google Scholar 

  30. 30

    Brakefield, P. M. et al. Development, plasticity and evolution of butterfly eyespot patterns. Nature 384, 236–242 (1996).

    ADS  CAS  Article  Google Scholar 

  31. 31

    Guilford, T. & Dawkins, M. S. Search images not proven: A reappraisal of recent evidence. Anim. Behav. 35, 1838–1845 (1987).

    Article  Google Scholar 

  32. 32

    Endler, J. A. in Behavioural Ecology 3rd edn (eds Krebs, J. R. & Davies, N. B.) 169–196 (Blackwell Scientific, Oxford, 1991).

    Google Scholar 

  33. 33

    Bond, A. B. Visual search and selection of natural stimuli in the pigeon: The attention threshold hypothesis. J. Exp. Psychol. Anim. Behav. Process 9, 292–306 (1983).

    CAS  Article  Google Scholar 

  34. 34

    Wallace, A. R. Darwinism: An Exposition of the Theory of Natural Selection with Some of its Applications (MacMillan, London, 1891).

    Google Scholar 

  35. 35

    Endler, J. A. A predator's view of animal color patterns. Evol. Biol. 11, 319–364 (1978).

    Google Scholar 

  36. 36

    Cott, H. B. Adaptive Coloration in Animals (Methuen, London, 1957).

    Google Scholar 

  37. 37

    Robinson, M. H. Defenses against visually hunting predators. Evol. Biol. 3, 225–259 (1969).

    Google Scholar 

  38. 38

    Endler, J. A. Natural selection on color patterns in Poecilia reticulata. Evolution 34, 76–91 (1980).

    Article  Google Scholar 

  39. 39

    Ford, E. B. in Insect Polymorphism: Symposia of the Royal Entomological Society of London (ed. Kennedy, J. S.) Vol. 1, 11–19 (Royal Entomological Society, London, 1961).

    Google Scholar 

  40. 40

    Moment, G. B. Reflexive selection: a possible answer to an old puzzle. Science 136, 262–263 (1962).

    ADS  CAS  Article  Google Scholar 

  41. 41

    Nabours, R. K., Larson, I. & Hartwig, N. Inheritance of color patterns in the grouse locust Acrydium arenosum Burmeister (Tettigidae). Genetics 18, 159–171 (1933).

    CAS  PubMed  PubMed Central  Google Scholar 

  42. 42

    Plaisted, K. C. & Mackintosh, N. J. Visual search for cryptic stimuli in pigeons: implications for the search image and search rate hypotheses. Anim. Behav. 50, 1219–1232 (1995).

    Article  Google Scholar 

  43. 43

    Darlington, C. D. & Mather, K. The Elements of Genetics (Macmillan, New York, 1950).

    Google Scholar 

  44. 44

    Bäck, T. Evolutionary Algorithms in Theory and Practice (Oxford Univ. Press, New York, 1996).

    Google Scholar 

  45. 45

    Endler, J. A. Progressive background matching in moths, and a quantitative measure of crypsis. Biol. J. Linn. Soc. 22, 187–231 (1984).

    Article  Google Scholar 

  46. 46

    Kaufman, L. & Rousseeuw, P. J. Finding Groups in Data (Wiley, New York, 1990).

    Google Scholar 

  47. 47

    Sneath, P. H. A. & Sokal, R. R. Numerical Taxonomy (Freeman, San Francisco, 1973).

    Google Scholar 

Download references

Acknowledgements

We thank J. Allen, R. Balda, J. Endler, T. Getty, L. Harshman, S. Louda, D. Pilson and S. Shettleworth for their comments and suggestions. This research was supported by a grant from the National Science Foundation.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Alan B. Bond.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Bond, A., Kamil, A. Visual predators select for crypticity and polymorphism in virtual prey. Nature 415, 609–613 (2002). https://doi.org/10.1038/415609a

Download citation

Further reading

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

Quick links

Sign up for the Nature Briefing newsletter for a daily update on COVID-19 science.
Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing