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Social transmission of avoidance among predators facilitates the spread of novel prey


Warning signals are an effective defence strategy for aposematic prey, but only if they are recognized by potential predators. If predators must eat prey to associate novel warning signals with unpalatability, how can aposematic prey ever evolve? Using experiments with great tits (Parus major) as predators, we show that social transmission enhances the acquisition of avoidance by a predator population. Observing another predator’s disgust towards tasting one novel conspicuous prey item led to fewer aposematic than cryptic prey being eaten for the predator population to learn. Despite reduced personal encounters with unpalatable prey, avoidance persisted and increased over subsequent trials. Next we use a mathematical model to show that social transmission can shift the evolutionary trajectory of prey populations from fixation of crypsis to fixation of aposematism more easily than was previously thought. Therefore, social information use by predators has the potential to have evolutionary consequences across ecological communities.

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Fig. 1: Latency to forage and initial prey choices.
Fig. 2: Relative predation risk for novel conspicuous prey versus the cryptic phenotype.
Fig. 3: An example of the temporal dynamics predicted if social information is available.
Fig. 4: Threshold frequency of aposematic prey necessary for the phenotype to reach fixation.
Fig. 5: Effect of social transmission on the initial population size required for aposematic prey to reach fixation.


  1. Poulton, E. B. The Colours of Animals: Their Meaning and Use Especially Considered in the Case of Insects (Kegan Paul, Trench, Trübner & Co., London, 1890).

  2. Puurtinen, M. & Kaitala, V. Conditions for the spread of conspicuous warning signals: a numerical model with novel insights. Evolution 60, 2246–2256 (2006).

    Article  PubMed  Google Scholar 

  3. Ruxton, G. D. & Sherratt, T. N. Aggregation, defence and warning signals: the evolutionary relationship. Proc. R. Soc. B Biol. Sci. 273, 2417–2424 (2006).

    Article  Google Scholar 

  4. Skelhorn, J., Halpin, C. G. & Rowe, C. Learning about aposematic prey. Behav. Ecol. 27, 955–964 (2016).

    Article  Google Scholar 

  5. Lindström, L., Alatalo, R. V., Mappes, J., Riipi, M. & Vertainen, L. Can aposematic signals evolve by gradual change? Nature 397, 249–251 (1999).

    Article  Google Scholar 

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

    Article  Google Scholar 

  7. Exnerová, A. et al. Avoidance of aposematic prey in European tits (Paridae): learned or innate? Behav. Ecol. 18, 148–156 (2007).

    Article  Google Scholar 

  8. Mappes, J., Kokko, H., Ojala, K. & Lindström, L. Seasonal changes in predator community switch the direction of selection for prey defences. Nat. Commun. 5, 5016 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Longson, C. G. & Joss, J. M. P. Optimal toxicity in animals: predicting the optimal level of chemical defences. Funct. Ecol. 20, 731–735 (2006).

    Article  Google Scholar 

  10. Stevens, M. & Ruxton, G. D. D. Linking the evolution and form of warning coloration in nature. Proc. R. Soc. B Biol. Sci. 279, 417–426 (2012).

    Article  Google Scholar 

  11. Marples, N. M., Kelly, D. J. & Thomas, R. J. Perspective: the evolution of warning coloration is not paradoxical. Evolution 59, 933–940 (2005).

    Article  PubMed  Google Scholar 

  12. Riipi, M., Alatalo, R. V. & Lindström, L. Multiple benefits of gregariousness cover detectability costs in aposematic aggregations. Nature 413, 512–514 (2001).

    Article  CAS  PubMed  Google Scholar 

  13. Marples, N. M. & Mappes, J. Can the dietary conservatism of predators compensate for positive frequency dependent selection against rare, conspicuous prey? Evol. Ecol. 25, 737–749 (2011).

    Article  Google Scholar 

  14. McMahon, K. & Marples, N. Reduced dietary conservatism in a wild bird in the presence of intraspecific competition. J. Avian Biol. 48, 448–454 (2017).

    Article  Google Scholar 

  15. Lindström, L., Alatalo, R. V. & Mappes, J. Reactions of hand-reared and wild-caught predators toward warningly colored, gregarious, and conspicuous prey. Behav. Ecol. 10, 317–322 (1999).

    Article  Google Scholar 

  16. Endler, J. A. & Mappes, J. Predator mixes and the conspicuousness of aposematic signals. Am. Nat. 163, 532–547 (2004).

    Article  PubMed  Google Scholar 

  17. Dall, S. R. X., Giraldeau, L.-A., Olsson, O., McNamara, J. M. & Stephens, D. W. Information and its use by animals in evolutionary ecology. Trends Ecol. Evol. 20, 187–193 (2005).

    Article  PubMed  Google Scholar 

  18. Lynn, S. K. Learning to avoid aposematic prey. Anim. Behav. 70, 1221–1226 (2005).

    Article  Google Scholar 

  19. Swynnerton, C. F. M. Birds in relation to their prey: experiments on wood hoopoes, small hornbills and a babbler. J. S. Afr. Ornithol. Union 11, 32–108 (1915).

    Google Scholar 

  20. van de Waal, E., Borgeaud, C. & Whiten, A. Potent social learning and conformity shape a wild primate’s foraging decisions. Science 340, 483–485 (2013).

    Article  CAS  PubMed  Google Scholar 

  21. Landová, E., Hotová Svádová, K., Fuchs, R., Štys, P. & Exnerová, A. The effect of social learning on avoidance of aposematic prey in juvenile great tits (Parus major). Anim. Cogn. 20, 855–866 (2017). 

    PubMed  Google Scholar 

  22. Snowdon, C. T. & Boe, C. Y. Social communication about unpalatable foods in tamarins (Saguinus oedipus). J. Comp. Psychol. 117, 142–148 (2003).

    Article  PubMed  Google Scholar 

  23. Mason, J. R. & Reidinger, R. Observational learning of food aversions in red-winged blackbirds (Agelaius phoeniceus). Auk 99, 548–554 (1982).

    Google Scholar 

  24. Fryday, S. & Greig-Smith, P. The effects of social learning on the food choice of the house sparrow (Passer domesticus). Behaviour 128, 281–300 (1994).

    Article  Google Scholar 

  25. Johnston, A. N. B., Burne, T. H. J. & Rose, S. P. R. Observation learning in day-old chicks using a one-trial passive avoidance learning paradigm. Anim. Behav. 56, 1347–1353 (1998).

    Article  CAS  PubMed  Google Scholar 

  26. Skelhorn, J. Colour biases are a question of conspecifics’ taste. Anim. Behav. 81, 825–829 (2011).

    Article  Google Scholar 

  27. Harvey, P. H., Bull, J. J., Pemberton, M. & Paxton, R. J. The evolution of aposematic coloration in distasteful prey: a family model. Am. Nat. 119, 710–719 (1982).

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  29. Lindström, L., Lyytinen, A., Mappes, J. & Ojala, K. Relative importance of taste and visual appearance for predator education in Müllerian mimicry. Anim. Behav. 72, 323–333 (2006).

    Article  Google Scholar 

  30. Sillén-Tullberg, B. Higher survival of an aposematic than of a cryptic form of a distasteful bug. Oecologia 67, 411–415 (1985).

    Article  PubMed  Google Scholar 

  31. Marchetti, C. & Drent, P. J. Individual differences in the use of social information in foraging by captive great tits. Anim. Behav. 60, 131–140 (2000).

    Article  CAS  PubMed  Google Scholar 

  32. Aplin, L. M. et al. Experimentally induced innovations lead to persistent culture via conformity in wild birds. Nature 518, 538–541 (2015).

    Article  CAS  PubMed  Google Scholar 

  33. Hämäläinen, L., Rowland, H. M., Mappes, J. & Thorogood, R. Can video playback provide social information for foraging blue tits? PeerJ 5, e3062 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  34. Saitou, T. Ecological study of social organization in the great tit, Parus major L. III. Home range of the basic flocks and dominance relationship of the members in a basic flock. J. Yamashina Inst. Ornithol. 11, 149–171 (1979).

    Article  Google Scholar 

  35. Lee, T. J. & Speed, M. P. The effect of metapopulation dynamics on the survival and spread of a novel, conspicuous prey. J. Theor. Biol. 267, 319–29 (2010).

    Article  PubMed  Google Scholar 

  36. Grüter, C. & Leadbeater, E. Insights from insects about adaptive social information use. Trends Ecol. Evol. 29, 177–184 (2014).

    Article  PubMed  Google Scholar 

  37. White, S. L. & Gowan, C. Social learning enhances search image acquisition in foraging brook trout. Environ. Biol. Fishes 97, 523–528 (2014).

    Article  Google Scholar 

  38. Kis, A., Huber, L. & Wilkinson, A. Social learning by imitation in a reptile (Pogona vitticeps). Anim. Cogn. 18, 325–331 (2015).

    Article  PubMed  Google Scholar 

  39. Galef, B. G. & Giraldeau, L.-A. Social influences on foraging in vertebrates: causal mechanisms and adaptive functions. Anim. Behav. 61, 3–15 (2001).

    Article  PubMed  Google Scholar 

  40. Heyes, C. M. Social learning in animals: categories and mechanisms. Biol. Rev. 69, 207–231 (1994).

    Article  CAS  PubMed  Google Scholar 

  41. Skelhorn, J. & Rowe, C. Taste-rejection by predators and the evolution of unpalatability in prey. Behav. Ecol. Sociobiol. 60, 550–555 (2006).

    Article  Google Scholar 

  42. Olsson, A. & Phelps, E. A. Social learning of fear. Nat. Neurosci. 10, 1095–1102 (2007).

    Article  CAS  PubMed  Google Scholar 

  43. Sasvári, L. & Hegyi, Z. How mixed-species foraging flocks develop in response to benefits from observational learning. Anim. Behav. 55, 1461–1469 (1998).

    Article  PubMed  Google Scholar 

  44. Farine, D. R., Garroway, C. J. & Sheldon, B. C. Social network analysis of mixed-species flocks: exploring the structure and evolution of interspecific social behaviour. Anim. Behav. 84, 1271–1277 (2012).

    Article  Google Scholar 

  45. Nokelainen, O., Valkonen, J., Lindstedt, C. & Mappes, J. Changes in predator community structure shifts the efficacy of two warning signals in arctiid moths. J. Anim. Ecol. 83, 598–605 (2014).

    Article  PubMed  Google Scholar 

  46. Farine, D. R., Montiglio, P. & Spiegel, O. From individuals to groups and back: the evolutionary implications of group phenotypic composition. Trends Ecol. Evol. 30, 609–621 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  47. Beckmann, C., Crossland, M. R. & Shine, R. Responses of Australian wading birds to a novel toxic prey type, the invasive cane toad Rhinella marina. Biol. Invasions 13, 2925–2934 (2011).

    Article  Google Scholar 

  48. Cremona, T., Spencer, P., Shine, R. & Webb, J. K. Avoiding the last supper: parentage analysis indicates multi-generational survival of re-introduced ‘toad-smart’ lineage. Conserv. Genet. 18, 1475–1480 (2017).

    Article  Google Scholar 

  49. Thorogood, R. & Davies, N. B. Cuckoos combat socially transmitted defenses of reed warbler hosts with a plumage polymorphism. Science 337, 578–580 (2012).

    Article  CAS  PubMed  Google Scholar 

  50. Pruitt, J. N. et al. Behavioral hypervolumes of predator groups and predator–predator interactions shape prey survival rates and selection on prey behavior. Am. Nat. 189, 254–266 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  51. Orell, M. Population fluctuations and survival of great tits Parus major dependent on food supplied by man in winter. Ibis 131, 112–127 (1989).

    Article  Google Scholar 

  52. Snijders, L., Naguib, M. & van Oers, K. Dominance rank and boldness predict social attraction in great tits. Behav. Ecol. 28, 398–406 (2017).

    Google Scholar 

  53. Guillette, L. M. & Healy, S. D. The roles of vocal and visual interactions in social learning zebra finches: a video playback experiment. Behav. Process. 139, 43–49 (2017).

    Article  Google Scholar 

  54. R Development Core Team R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, Vienna, 2017).

  55. Bates, D., Mächler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48 (2015).

    Article  Google Scholar 

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We are grateful to N. Boogert for suggesting the video playback method, D. Abondano Almeida, S. Burdillat and M. Brain for help with the experiments, J. Valkonen for valuable technical help, V. Franks for providing illustrations, and H. Nisu and staff at the Konnevesi Research Station for hosting the experiments and caring for the birds. P. Klopfer provided helpful discussion and the manuscript was improved by comments from N. Boogert, L. Hämäläinen and M. Puurtinen. R.T. was funded by an Independent Research Fellowship from the Natural Environment Research Council (NE/K00929X/1). J.M. and H.K. were supported by the Academy of Finland Centre of Excellence in Biological Interactions (project number 252411) and H.K. was additionally supported by the Swiss National Foundation.

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Authors and Affiliations



R.T. conceived the project and designed and conducted the experiments and analyses. J.M. designed the experiments and assisted with the analyses. H.K. conceived and conducted the modelling. All authors wrote the manuscript.

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Correspondence to Rose Thorogood.

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Supplementary Information

Supplementary Methods, Supplementary References, Supplementary Figures 1–3, and Supplementary Tables 1–2.

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Supplementary Video 1

Example of social information treatment from validation experiment.

Supplementary Video 2

Example of control from validation experiment.

Supplementary Video 3

Example of social information treatment from predation experiment.

Supplementary Video 4

Example of control from predation experiment.

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Thorogood, R., Kokko, H. & Mappes, J. Social transmission of avoidance among predators facilitates the spread of novel prey. Nat Ecol Evol 2, 254–261 (2018).

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