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Conceptualization, context, and comparison are key to understanding the evolution of fear

Published online by Cambridge University Press:  08 May 2023

Jacob C. Dunn
Affiliation:
Behavioural Ecology Research Group, Anglia Ruskin University, Cambridge CB1 1PT, UK jacob.dunn@aru.ac.uk; caglar.akcay@aru.ac.uk; krishna.balasubramaniam@aru.ac.uk; rh87@aru.ac.uk; claudia.wascher@aru.ac.uk https://www.thepeergroup.org.uk; https://aru.ac.uk/people/caglar-akcay; https://aru.ac.uk/people/krishna-n-balasubramaniam; https://aru.ac.uk/people/rachael-miller-harrison; https://aru.ac.uk/people/claudia-wascher Department of Cognitive Biology, University of Vienna, 1090 Vienna, Austria Biological Anthropology, University of Cambridge, Cambridge CB2 1QH, UK
Rachael Miller
Affiliation:
Behavioural Ecology Research Group, Anglia Ruskin University, Cambridge CB1 1PT, UK jacob.dunn@aru.ac.uk; caglar.akcay@aru.ac.uk; krishna.balasubramaniam@aru.ac.uk; rh87@aru.ac.uk; claudia.wascher@aru.ac.uk https://www.thepeergroup.org.uk; https://aru.ac.uk/people/caglar-akcay; https://aru.ac.uk/people/krishna-n-balasubramaniam; https://aru.ac.uk/people/rachael-miller-harrison; https://aru.ac.uk/people/claudia-wascher Department of Psychology, University of Cambridge, Cambridge CB2 3EB, UK
Krishna Balasubramaniam
Affiliation:
Behavioural Ecology Research Group, Anglia Ruskin University, Cambridge CB1 1PT, UK jacob.dunn@aru.ac.uk; caglar.akcay@aru.ac.uk; krishna.balasubramaniam@aru.ac.uk; rh87@aru.ac.uk; claudia.wascher@aru.ac.uk https://www.thepeergroup.org.uk; https://aru.ac.uk/people/caglar-akcay; https://aru.ac.uk/people/krishna-n-balasubramaniam; https://aru.ac.uk/people/rachael-miller-harrison; https://aru.ac.uk/people/claudia-wascher
Çağlar Akçay
Affiliation:
Behavioural Ecology Research Group, Anglia Ruskin University, Cambridge CB1 1PT, UK jacob.dunn@aru.ac.uk; caglar.akcay@aru.ac.uk; krishna.balasubramaniam@aru.ac.uk; rh87@aru.ac.uk; claudia.wascher@aru.ac.uk https://www.thepeergroup.org.uk; https://aru.ac.uk/people/caglar-akcay; https://aru.ac.uk/people/krishna-n-balasubramaniam; https://aru.ac.uk/people/rachael-miller-harrison; https://aru.ac.uk/people/claudia-wascher
Claudia A. F. Wascher
Affiliation:
Behavioural Ecology Research Group, Anglia Ruskin University, Cambridge CB1 1PT, UK jacob.dunn@aru.ac.uk; caglar.akcay@aru.ac.uk; krishna.balasubramaniam@aru.ac.uk; rh87@aru.ac.uk; claudia.wascher@aru.ac.uk https://www.thepeergroup.org.uk; https://aru.ac.uk/people/caglar-akcay; https://aru.ac.uk/people/krishna-n-balasubramaniam; https://aru.ac.uk/people/rachael-miller-harrison; https://aru.ac.uk/people/claudia-wascher

Abstract

The fearful ape hypothesis proposes that heightened fearfulness in humans is adaptive. However, despite its attractive anthropocentric narrative, the evidence presented for greater fearfulness in humans versus other apes is not sufficient to support this claim. Conceptualization, context, and comparison are strongly lacking in Grossmann's proposal, but are key to understanding variation in the fear response among individuals and species.

Type
Open Peer Commentary
Copyright
Copyright © The Author(s), 2023. Published by Cambridge University Press

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Footnotes

*

These authors contributed equally.

References

Birch, L. L. (1995). Research in review. Children's eating: The development of food-acceptance patterns. Young Children, 50(2), 7178.Google Scholar
Blumstein, D. T. (2006). Developing an evolutionary ecology of fear: How life history and natural history traits affect disturbance tolerance in birds. Animal Behaviour, 71(2), 389399. https://doi.org/10.1016/j.anbehav.2005.05.010CrossRefGoogle Scholar
Boissy, A. (1995). Fear and fearfulness in animals. The Quarterly Review of Biology, 70(2), 165191. https://doi.org/10.1086/418981CrossRefGoogle ScholarPubMed
Clutton-Brock, T. H. (2006). Cooperative breeding in mammals. In Kappeler, P. M. & van Schaik, C. P. (Eds.), Cooperation in primates and humans: Mechanisms and evolution (pp. 173190). Springer. https://doi.org/10.1007/3-540-28277-7_10CrossRefGoogle Scholar
Coleman, S. L., & Mellgren, R. L. (1994). Neophobia when feeding alone or in flocks in zebra finches, Taeniopygia guttata. Animal Behaviour, 48(4), 903907. https://doi.org/10.1006/anbe.1994.1315CrossRefGoogle Scholar
Crane, A. L., Brown, G. E., Chivers, D. P., & Ferrari, M. C. O. (2020). An ecological framework of neophobia: From cells to organisms to populations. Biological Reviews, 95(1), 218231. https://doi.org/10.1111/brv.12560CrossRefGoogle ScholarPubMed
Forss, S. I. F., Koski, S. E., & van Schaik, C. P. (2017). Explaining the paradox of neophobic explorers: The social information hypothesis. International Journal of Primatology, 38(5), 799822. https://doi.org/10.1007/s10764-017-9984-7CrossRefGoogle Scholar
Gould, S. J., & Lewontin, R. C. (1979). The spandrels of San Marco and the Panglossian paradigm: A critique of the adaptationist programme. Proceedings of the Royal Society of London. Series B: Biological Sciences, 205(1161), 581598. https://doi.org/10.1098/rspb.1979.0086Google Scholar
Greggor, A. L., Clayton, N. S., Fulford, A. J. C., & Thornton, A. (2016). Street smart: Faster approach towards litter in urban areas by highly neophobic corvids and less fearful birds. Animal Behaviour, 117, 123133. https://doi.org/10.1016/j.anbehav.2016.03.029CrossRefGoogle ScholarPubMed
Greggor, A. L., Thornton, A., & Clayton, N. S. (2015). Neophobia is not only avoidance: Improving neophobia tests by combining cognition and ecology. Current Opinion in Behavioral Sciences, 6, 8289. https://doi.org/10.1016/j.cobeha.2015.10.007CrossRefGoogle Scholar
Henrich, J., Heine, S. J., & Norenzayan, A. (2010). Beyond WEIRD: Towards a broad-based behavioral science. Behavioral and Brain Sciences, 33(2–3), 111135. https://doi.org/10.1017/S0140525X10000725CrossRefGoogle Scholar
Herrmann, E., Hare, B., Cissewski, J., & Tomasello, M. (2011). A comparison of temperament in nonhuman apes and human infants. Developmental Science, 14(6), 13931405. https://doi.org/10.1111/j.1467-7687.2011.01082.xCrossRefGoogle ScholarPubMed
Horn, L., Bugnyar, T., Griesser, M., Hengl, M., Izawa, E.-I., Oortwijn, T., … Massen, J. J. (2020). Sex-specific effects of cooperative breeding and colonial nesting on prosociality in corvids. eLife, 9, e58139. https://doi.org/10.7554/eLife.58139CrossRefGoogle ScholarPubMed
Isbell, L. A. (2006). Snakes as agents of evolutionary change in primate brains. Journal of Human Evolution, 51(1), 135. https://doi.org/10.1016/j.jhevol.2005.12.012CrossRefGoogle ScholarPubMed
Kawai, N., & Koda, H. (2016). Japanese monkeys (Macaca fuscata) quickly detect snakes but not spiders: Evolutionary origins of fear-relevant animals. Journal of Comparative Psychology, 130(3), 299303. https://doi.org/10.1037/com0000032CrossRefGoogle Scholar
Koenig, W. D., & Dickinson, J. L. (Eds.) (2016). Cooperative breeding in vertebrates: Studies of ecology, evolution, and behavior. Cambridge University Press. https://doi.org/10.1017/CBO9781107338357CrossRefGoogle Scholar
König, B. (1997). Cooperative care of young in mammals. Die Naturwissenschaften, 84(3), 95104. https://doi.org/10.1007/s001140050356Google ScholarPubMed
Laundre, J. W., Hernandez, L., & Ripple, W. J. (2010). The landscape of fear: Ecological implications of being afraid. The Open Ecology Journal, 3, 17. https://benthamopen.com/ABSTRACT/TOECOLJ-3-3-1CrossRefGoogle Scholar
Mettke-Hofmann, C., Winkler, H., & Leisler, B. (2002). The significance of ecological factors for exploration and neophobia in parrots. Ethology, 108(3), 249272. https://doi.org/10.1046/j.1439-0310.2002.00773.xCrossRefGoogle Scholar
Miller, K. A., Garner, J. P., & Mench, J. A. (2006). Is fearfulness a trait that can be measured with behavioural tests? A validation of four fear tests for Japanese quail. Animal Behaviour, 71(6), 13231334. https://doi.org/10.1016/j.anbehav.2005.08.018CrossRefGoogle Scholar
Miller, R., Bugnyar, T., Pölzl, K., & Schwab, C. (2015). Differences in exploration behaviour in common ravens and carrion crows during development and across social context. Behavioral Ecology and Sociobiology, 69(7), 12091220. https://doi.org/10.1007/s00265-015-1935-8CrossRefGoogle ScholarPubMed
Miller, R., Lambert, M. L., Frohnwieser, A., Brecht, K. F., Bugnyar, T., Crampton, I., … Clayton, N. S. (2022). Socioecological correlates of neophobia in corvids. Current Biology, 32(1), 7485.e4. https://doi.org/10.1016/j.cub.2021.10.045CrossRefGoogle ScholarPubMed
Mobbs, D., Hagan, C. C., Dalgleish, T., Silston, B., & Prévost, C. (2015). The ecology of human fear: Survival optimization and the nervous system. Frontiers in Neuroscience, 9, 55. https://doi.org/10.3389/fnins.2015.00055CrossRefGoogle ScholarPubMed
Moretti, L., Hentrup, M., Kotrschal, K., & Range, F. (2015). The influence of relationships on neophobia and exploration in wolves and dogs. Animal Behaviour, 107, 159173. https://doi.org/10.1016/j.anbehav.2015.06.008CrossRefGoogle ScholarPubMed
Öhman, A. (2009). Of snakes and faces: An evolutionary perspective on the psychology of fear. Scandinavian Journal of Psychology, 50(6), 543552. https://doi.org/10.1111/j.1467-9450.2009.00784.xCrossRefGoogle ScholarPubMed
Paul, E. S., Harding, E. J., & Mendl, M. (2005). Measuring emotional processes in animals: The utility of a cognitive approach. Neuroscience & Biobehavioral Reviews, 29(3), 469491. https://doi.org/10.1016/j.neubiorev.2005.01.002CrossRefGoogle ScholarPubMed
Pellman, B. A., & Kim, J. J. (2016). What can ethobehavioral studies tell us about the brain's fear system? Trends in Neurosciences, 39(6), 420431. https://doi.org/10.1016/j.tins.2016.04.001CrossRefGoogle ScholarPubMed
Safryghin, A., Hebesberger, D. V., & Wascher, C. A. F. (2019). Testing for behavioral and physiological responses of domestic horses (Equus caballus) across different contexts – Consistency over time and effects of context. Frontiers in Psychology, 10, 849. https://doi.org/10.3389/fpsyg.2019.00849CrossRefGoogle ScholarPubMed
Schaffer, A., Caicoya, A. L., Colell, M., Holland, R., von Fersen, L., Widdig, A., & Amici, F. (2021). Neophobia in 10 ungulate species – A comparative approach. Behavioral Ecology and Sociobiology, 75(7), 102. https://doi.org/10.1007/s00265-021-03041-0CrossRefGoogle ScholarPubMed
Takola, E., Krause, E. T., Müller, C., & Schielzeth, H. (2021). Novelty at second glance: A critical appraisal of the novel object paradigm based on meta-analysis. Animal Behaviour, 180, 123142. https://doi.org/10.1016/j.anbehav.2021.07.018CrossRefGoogle Scholar
Vernouillet, A., & Kelly, D. M. (2020). Individual exploratory responses are not repeatable across time or context for four species of food-storing corvid. Scientific Reports, 10(1), 394. https://doi.org/10.1038/s41598-019-56138-yCrossRefGoogle ScholarPubMed
Webster, M. M., & Rutz, C. (2020). How STRANGE are your study animals? Nature, 582(7812), 337340. https://doi.org/10.1038/d41586-020-01751-5CrossRefGoogle ScholarPubMed
Webster, S. J., & Lefebvre, L. (2000). Neophobia by the lesser-Antillean bullfinch, a foraging generalist, and the bananaquit, a nectar specialist. The Wilson Bulletin, 112(3), 424427. https://doi.org/10.1676/0043-5643(2000)112[0424:NBTLAB]2.0.CO;2CrossRefGoogle Scholar