Abstract
Objectives
The potential differences between phylogenetic threats (e.g., snakes) and ontogenetic threats (e.g., guns) can have a wide-ranging impact on a variety of theoretical and practical issues, from etiology of specific phobias to stimulus selection in psychophysiological studies, yet this line of research has not been systematically reviewed.
Methods
We summarize and synthesize findings from fear conditioning, illusory correlation, attention bias, and neuroimaging studies that have compared these two types of threats to human survival.
Results
While a few brain imaging studies reveal preliminary evidence for different brain networks involved in the processing of phylogenetic and ontogenetic threats, attention bias studies tentatively show faster reaction time for modern threats, illusory correlation bias is evident for both types of threats, and fear conditioning studies are far from conclusive.
Conclusions
The results of behavioral experiments, especially attention bias research, pose a challenge to established theories like biological preparedness and fear module, as they show faster reaction time to modern threats, which is the opposite of what some evolutionary theories predict. We discuss the findings in terms of other theories that might explain the same results and conclude with potential future directions.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Notes
This study has a major technical issue. The authors claim that they have used a wide range of predatory animals (e.g., snakes, spiders, sharks, dogs, and bears) for evolutionary-threatening condition. The id numbers of IAPS photos used in this study and reported in its supplementary material, show they have only picked snakes. The first author did not respond to our emails about this issue.
References
Åhs, F., Rosén, J., Kastrati, G., Fredrikson, M., Agren, T., & Lundström, J. N. (2018). Biological preparedness and resistance to extinction of skin conductance responses conditioned to fear relevant animal pictures: A systematic review. Neuroscience & Biobehavioral Reviews, 95, 430–437. https://doi.org/10.1016/j.neubiorev.2018.10.017
Alpers, P. & Picard, M. (2020a). United States – Gun Facts, Figures and the Law. Retrieved Oct 10, 2020, from https://www.gunpolicy.org/firearms/region/united-states
Alpers, P. & Picard, M. (2020b). India – Gun Facts, Figures and the Law. Retrieved Oct 10, 2020, from https://www.gunpolicy.org/firearms/region/india
Amin, J. M., & Lovibond, P. F. (1997). Dissociations between covariation bias and expectancy bias for fear-relevant stimuli. Cognition & Emotion, 11(3), 273–289. https://doi.org/10.1080/026999397379926
Apicella, C., Norenzayan, A., & Henrich, J. (2020). Beyond WEIRD: A review of the last decade and a look ahead to the global laboratory of the future. Evolution and Human Behavior, 41(5), 319–329. https://doi.org/10.1016/j.evolhumbehav.2020.07.015
Baum, A., Fleming, R., & Davidson, L. M. (1983). Natural disaster and technological catastrophe. Environment and Behavior, 15(3), 333–354.
Behrensmeyer, A. K. (2006). Climate change and human evolution. Science, 311(5760), 476–478.
Blanchette, I. (2006). Snakes, spiders, guns, and syringes: How specific are evolutionary constraints on the detection of threatening stimuli? Quarterly Journal of Experimental Psychology, 59(8), 1484–1504. https://doi.org/10.1080/02724980543000204
Bowles, S., & Choi, J. K. (2013). Coevolution of farming and private property during the early Holocene. Proceedings of the National Academy of Sciences, 110(22), 8830–8835.
Bradley, M. M., & Lang, P. J. (2007). Emotion and motivation. In J. T. Cacioppo, L. G. Tassinary, & G. Berntson (Eds.), Handbook of psychophysiology (pp. 581–607). Cambridge university press.
Bregman, E. O. (1934). An attempt to modify the emotional attitudes of infants by the conditioned response technique. The Pedagogical Seminary and Journal of Genetic Psychology, 45(1), 169–198. https://doi.org/10.1080/08856559.1934.10534254
Brosch, T., & Sharma, D. (2005). The role of fear-relevant stimuli in visual search: A comparison of phylogenetic and ontogenetic stimuli. Emotion, 5(3), 360–364. https://doi.org/10.1037/1528-3542.5.3.360
Brown, C., El-Deredy, W., & Blanchette, I. (2010). Attentional modulation of visual-evoked potentials by threat: Investigating the effect of evolutionary relevance. Brain and Cognition, 74(3), 281–287. https://doi.org/10.1016/j.bandc.2010.08.008
Brun, W. (1992). Cognitive components in risk perception: Natural versus manmade risks. Journal of Behavioral Decision Making, 5(2), 117–132.
Cao, Z., Zhao, Y., Tan, T., Chen, G., Ning, X., Zhan, L., & Yang, J. (2014). Distinct brain activity in processing negative pictures of animals and objects—The role of human contexts. Neuroimage, 84, 901–910. https://doi.org/10.1016/j.neuroimage.2013.09.064
Carlson, J. M., Fee, A. L., & Reinke, K. S. (2009). Backward masked snakes and guns modulate spatial attention. Evolutionary Psychology, 7(4), 147470490900700404. https://doi.org/10.1177/147470490900700404
Coelho, C. M., Suttiwan, P., Faiz, A. M., Ferreira-Santos, F., & Zsido, A. N. (2019). Are humans prepared to detect, fear, and avoid snakes? The mismatch between laboratory and ecological evidence. Frontiers in Psychology. https://doi.org/10.3389/fpsyg.2019.02094
Cook, E. W., Hodes, R. L., & Lang, P. J. (1986). Preparedness and phobia: Effects of stimulus content on human visceral conditioning. Journal of Abnormal Psychology, 95(3), 195–207. https://doi.org/10.1037/0021-843X.95.3.195
Davey, G. C., & Dixon, A. L. (1996). The expectancy bias model of selective associations: The relationship of judgments of CS dangerousness, CS-UCS similarity and prior fear to a priori and a posteriori covariation assessments. Behaviour Research and Therapy, 34(3), 235–252. https://doi.org/10.1016/0005-7967(96)88487-7
de Jong, P. J., Merckelbach, H., Arntz, A., & Nijmam, H. (1992). Covariation detection in treated and untreated spider phobics. Journal of Abnormal Psychology, 101(4), 724–727. https://doi.org/10.1037/0021-843X.101.4.724
de Jong, P. J., Merckelbach, H., & Arntz, A. (1995). Covariation bias in phobic women: The relationship between a priori expectancy, on-line expectancy, autonomic responding, and a posteriori contingency judgment. Journal of Abnormal Psychology, 104(1), 55–62. https://doi.org/10.1037/0021-843X.104.1.55
de Jong, P. J. (1993). Covariation bias in phobia: Mere resistance to preexperimental expectancies? Behavior Therapy, 24(3), 447–454. https://doi.org/10.1016/S0005-7894(05)80217-5
de Rojas, J., & Kensinger, E. A. (2010). Neural Response to Emotional Stimuli of Phylogenetic and Ontogenetic Significance. Psi Chi Journal of Undergraduate Research. https://doi.org/10.24839/1089-4136.JN15.1.34
Del Giudice, M. (2020). Åhs et al.’s (2018) systematic review on biological preparedness and resistance to extinction: A commentary and reanalysis. Neuroscience and Biobehavioral Reviews, 120, 13–15. https://doi.org/10.1016/j.neubiorev.2020.11.009
Dhum, M., Herwig, U., Opialla, S., Siegrist, M., & Brühl, A. B. (2017). Evolutionary and modern image content differentially influence the processing of emotional pictures. Frontiers in Human Neuroscience, 11. https://doi.org/10.3389/fnhum.2017.00415
Domjan, M. (1997). Behavior systems and the demise of equipotentiality: Historical antecedents and evidence from sexual conditioning. In M. E. Bouton & M. S. Fanselow (Eds.), Learning, motivation, and cognition: The functional behaviorism of Robert C. Bolles (pp. 31–51). American Psychological Association. https://doi.org/10.1037/10223-002
Erlich, N., Lipp, O. V., & Slaughter, V. (2013). Of hissing snakes and angry voices: Human infants are differentially responsive to evolutionary fear-relevant sounds. Developmental Science, 16(6), 894–904. https://doi.org/10.1111/desc.12091
Fang, Z., Li, H., Chen, G., & Yang, J. (2016). Unconscious processing of negative animals and objects: role of the amygdala revealed by fMRI. Frontiers in Human Neuroscience. https://doi.org/10.3389/fnhum.2016.00146
Flykt, A., Esteves, F., & Öhman, A. (2007). Skin conductance responses to masked conditioned stimuli: Phylogenetic/ontogenetic factors versus direction of threat? Biological Psychology, 74(3), 328–336. https://doi.org/10.1016/j.biopsycho.2006.08.004
Fox, E., Griggs, L., & Mouchlianitis, E. (2007). The detection of fear-relevant stimuli: Are guns noticed as quickly as snakes? Emotion, 7(4), 691–696. https://doi.org/10.1037/1528-3542.7.4.691
Gao, H., & Jia, Z. (2017). Detection of threats under inattentional blindness and perceptual load. Current Psychology, 36(4), 733–739. https://doi.org/10.1007/s12144-016-9460-0
Garcia, J., & Koelling, R. A. (1966). Relation of cue to consequence in avoidance learning. Psychonomic Science, 4(1), 123–124. https://doi.org/10.3758/BF03342209
Guex, R., Méndez-Bértolo, C., Moratti, S., Strange, B. A., Spinelli, L., Murray, R. J., Sander, D., Seeck, M., Vuilleumier, P., & Domínguez-Borràs, J. (2020). Temporal dynamics of amygdala response to emotion-and action-relevance. Scientific Reports, 10(1), 1–16. https://doi.org/10.1038/s41598-020-67862-1
Hall, G. S. (1897). A study of fears. The American Journal of Psychology, 8(2), 147–249. https://doi.org/10.2307/1410940
Hebb, D. O. (1946). On the nature of fear. Psychological Review, 53(5), 259–276. https://doi.org/10.1037/h0061690
Heffner, R. S. (1997). Comparative study of sound localization and its anatomical correlates in mammals. Acta Oto-Laryngologica, 117(sup532), 46–53. https://doi.org/10.3109/00016489709126144
Heffner, R. S., & Heffner, H. E. (1992). Evolution of sound localization in mammals. In The evolutionary biology of hearing (pp. 691–715). Springer. https://doi.org/10.1007/978-1-4612-2784-7_43
Honeybourne, C., Matchett, G., & Davey, G. C. (1993). Expectancy models of laboratory preparedness effects: A UCS-expectancy bias in phylogenetic and ontogenetic fear-relevant stimuli. Behavior Therapy, 24(2), 253–264. https://doi.org/10.1016/S0005-7894(05)80267-9
Hugdahl, K., & Kärker, A. C. (1981). Biological vs experiential factors in phobic conditioning. Behaviour Research and Therapy, 19(2), 109–115. https://doi.org/10.1016/0005-7967(81)90034-6
Hugdahl, K., & Johnsen, B. H. (1989). Preparedness and electrodermal fear-conditioning: Ontogenetic vs phylogenetic explanations. Behaviour Research and Therapy, 27(3), 269–278. https://doi.org/10.1016/0005-7967(89)90046-6
Isbell, L. A. (2006). Snakes as agents of evolutionary change in primate brains. Journal of Human Evolution, 51(1), 1–35. https://doi.org/10.1016/j.jhevol.2005.12.012
Kennedy, S. J., Rapee, R. M., & Mazurski, E. J. (1997). Covariation bias for phylogenetic versus ontogenetic fear-relevant stimuli. Behaviour Research and Therapy, 35(5), 415–422. https://doi.org/10.1016/S0005-7967(96)00128-3
LeDoux, J. E. (1992). Emotion and the amygdala. In J. P. Aggleton (Ed.), The amygdala: Neurobiological aspects of emotion, memory, and mental dysfunction (p. 339–351). Wiley-Liss.
LeDoux, J. (2014). Rethinking the Emotional Brain. In Dębiec, J., Heller, M., Brożek, B., LeDoux, J. (Eds.), The Emotional Brian Revisited (pp. 13–83) Copernicus Center Press. https://doi.org/10.1016/j.neuron.2012.02.004
LeDoux, J. (1998). The emotional brain: The mysterious underpinnings of emotional life. Simon and Schuster.
LeDoux, J. E., Cicchetti, P., Xagoraris, A., & Romanski, L. M. (1990). The lateral amygdaloid nucleus: Sensory interface of the amygdala in fear conditioning. Journal of Neuroscience, 10(4), 1062–1069. https://doi.org/10.1523/JNEUROSCI.10-04-01062.1990
LoBue, V., & Adolph, K. E. (2019). Fear in infancy: Lessons from snakes, spiders, heights, and strangers. Developmental Psychology, 55(9), 1889–1907. https://doi.org/10.1037/dev0000675
Lonsdorf, T. B., Menz, M. M., Andreatta, M., Fullana, M. A., Golkar, A., Haaker, J., ... & Drexler, S. M. (2017). Don’t fear ‘fear conditioning’: Methodological considerations for the design and analysis of studies on human fear acquisition, extinction, and return of fear. Neuroscience & Biobehavioral Reviews, 77, 247–285. https://doi.org/10.1016/j.neubiorev.2017.02.026
Lovibond, P. F., Hanna, S. K., Siddle, D. A., & Bond, N. W. (1994). Electrodermal and subjective reactions to fear-relevant stimuli under threat of shock. Australian Journal of Psychology, 46(2), 73–80. https://doi.org/10.1080/00049539408259476
Luck, C. C., Patterson, R. R., & Lipp, O. V. (2020). “Prepared” fear or socio-cultural learning? Fear conditioned to guns, snakes, and spiders is eliminated by instructed extinction in a within-participant differential fear conditioning paradigm. Psychophysiology, 57(4), e13516. https://doi.org/10.1111/psyp.13516
Mallan, K. M., Lipp, O. V., & Cochrane, B. (2013). Slithering snakes, angry men and out-group members: What and whom are we evolved to fear? Cognition & Emotion, 27(7), 1168–1180. https://doi.org/10.1080/02699931.2013.778195
Marks, I. M. (1969). Fears and phobias. Academic Press.
Marks, I. M. (1970). The classification of phobic disorders. The British Journal of Psychiatry, 116(533), 377–386. https://doi.org/10.1192/bjp.116.533.377
McNally, R. J. (2016). The legacy of Seligman’s "phobias and preparedness" (1971). Behavior Therapy, 47(5), 585–594. https://doi.org/10.1016/j.beth.2015.08.005
McNally, R. J. (1987). Preparedness and phobias: A review. Psychological Bulletin, 101(2), 283–303. https://doi.org/10.1037/0033-2909.101.2.283
McNally, R. J., & Heatherton, T. F. (1993). Are covariation biases attributable to a priori expectancy biases? Behaviour Research and Therapy, 31(7), 653–658. https://doi.org/10.1016/0005-7967(93)90118-E
Mineka, S., & Sutton, S. K. (1992). Cognitive biases and the emotional disorders. Psychological Science, 3(1). https://doi.org/10.1111/j.1467-9280.1992.tb00260.x
Morris, J. S., deBonis, M., & Dolan, R. J. (2002). Human amygdala responses to fearful eyes. Neuroimage, 17(1), 214–222. https://doi.org/10.1006/nimg.2002.1220
Mobbs, D., Adolphs, R., Fanselow, M. S., Barrett, L. F., LeDoux, J. E., Ressler, K., & Tye, K. M. (2019). Viewpoints: Approaches to defining and investigating fear. Nature Neuroscience, 22(8), 1205–1216. https://doi.org/10.1038/s41593-019-0456-6
Muris, P., De Jong, P. J., Meesters, C., & Waterreus, B. (2005). An experimental study of spider-related covariation bias in 8-to 13-year-old children. Child Psychiatry and Human Development, 35(3), 185–201. https://doi.org/10.1007/s10578-004-6457-y
Muris, P., Huijding, J., Mayer, B., den Breejen, E., & Makkelie, M. (2007). Spider fear and covariation bias in children and adolescents. Behaviour Research and Therapy, 45(11), 2604–2615. https://doi.org/10.1016/j.brat.2007.06.002
Mühlberger, A., Wiedemann, G., Herrmann, M. J., & Pauli, P. (2006). Phylo-and ontogenetic fears and the expectation of danger: Differences between spider-and flight-phobic subjects in cognitive and physiological responses to disorder-specific stimuli. Journal of Abnormal Psychology, 115(3), 580. https://doi.org/10.1037/0021-843X.115.3.580
National Institute for Occupational Safety and Health. (2020). Venomous Snakes. Center for Disease Control and Prevention. Retrieved on Oct 10, 2010 from https://www.cdc.gov/niosh/topics/snakes/default.html
Neumayer, E., & Plümper, T. (2007). The gendered nature of natural disasters: The impact of catastrophic events on the gender gap in life expectancy, 1981–2002. Annals of the Association of American Geographers, 97(3), 551–566. https://doi.org/10.1111/j.1467-8306.2007.00563.x
Öhman, A. (1986). Face the beast and fear the face: Animal and social fears as prototypes for evolutionary analyses of emotion. Psychophysiology, 23(2), 123–145. https://doi.org/10.1111/j.1469-8986.1986.tb00608.x
Öhman, A., & Mineka, S. (2001). Fears, phobias, and preparedness: Toward an evolved module of fear and fear learning. Psychological Review, 108(3), 483. https://doi.org/10.1037/0033-295X.108.3.483
Öhman, A., Flykt, A., & Esteves, F. (2001). Emotion drives attention: Detecting the snake in the grass. Journal of Experimental Psychology: General, 130(3), 466. https://doi.org/10.1037/0096-3445.130.3.466
Öhman, A., & Mineka, S. (2003). The malicious serpent: Snakes as a prototypical stimulus for an evolved module of fear. Current Directions in Psychological Science, 12(1), 5–9. https://doi.org/10.1111/1467-8721.01211
Ouimet, A. J., Gawronski, B., & Dozois, D. J. (2009). Cognitive vulnerability to anxiety: A review and an integrative model. Clinical Psychology Review, 29(6), 459–470. https://doi.org/10.1016/j.cpr.2009.05.004
Penning, D. A., Sawvel, B., & Moon, B. R. (2016). Debunking the viper's strike: Harmless snakes kill a common assumption. Biology Letters, 12(3), 20160011. https://doi.org/10.1098/rsbl.2016.0011
Pessoa, L., & Adolphs, R. (2010). Emotion processing and the amygdala: From a 'low road' to 'many roads' of evaluating biological significance. Nature Reviews Neuroscience, 11(11), 773–782. https://doi.org/10.1038/nrn2920
Sander, D., Grafman, J., & Zalla, T. (2003). The human amygdala: An evolved system for relevance detection. Reviews in the Neurosciences, 14(4), 303–316. https://doi.org/10.1515/REVNEURO.2003.14.4.303
Seligman, M. E. (1970). On the generality of the laws of learning. Psychological Review, 77(5), 406–418. https://doi.org/10.1037/h0029790
Seligman, M. E. (1971). Phobias and preparedness. Behavior Therapy, 2(3), 307–320. https://doi.org/10.1016/S0005-7894(71)80064-3
Siegrist, M., & Sütterlin, B. (2014). Human and nature-caused hazards: The affect heuristic causes biased decisions. Risk Analysis, 34(8), 1482–1494.
Stjepanović, D., & LaBar, K. S. (2018). The cognitive neuroscience of fear learning. Stevens' Handbook of Experimental Psychology and Cognitive Neuroscience, 1, 1–39.
Subra, B., Muller, D., Fourgassie, L., Chauvin, A., & Alexopoulos, T. (2018). Of guns and snakes: Testing a modern threat superiority effect. Cognition and Emotion, 32(1), 81–91. https://doi.org/10.1080/02699931.2017.1284044
Suraweera, W., Warrell, D., Whitaker, R., Menon, G., Rodrigues, R., Fu, S. H., Begum, R., Sati, P., & Piyasena, K. (2020). Trends in snakebite deaths in India from 2000 to 2019 in a nationally representative mortality study. Elife, 9, e54076.
Tomarken, A. J., Mineka, S., & Cook, M. (1989). Fear-relevant selective associations and covariation bias. Journal of Abnormal Psychology, 98(4), 381–394. https://doi.org/10.1037/0021-843X.98.4.381
Tomarken, A. J., Sutton, S. K., & Mineka, S. (1995). Fear-relevant illusory correlations: What types of associations promote judgmental bias? Journal of Abnormal Psychology, 104(2), 312–326. https://doi.org/10.1037/0021-843X.104.2.312
Tooby, J., & Cosmides, L. (1990). The past explains the present: Emotional adaptations and the structure of ancestral environments. Ethology and Sociobiology, 11(4–5), 375–424. https://doi.org/10.1016/0162-3095(90)90017-Z
Valentine, C. W. (1930). The innate bases of fear. The Journal of Genetic Psychology, 37, 394–420. https://doi.org/10.1080/00221325.1991.9914710
Vida, M. D., & Behrmann, M. (2017) Subcortical Facilitation of Behavioral Responses to Threat. Scientific Reports. https://doi.org/10.1038/s41598-017-13203-8
Watson, J. B., & Rayner, R. (1920). Conditioned emotional reactions. Journal of Experimental Psychology, 3(1), 1–14. https://doi.org/10.1037/h0069608
World Health Organization. (2018a). The Top Ten Causes of Death. Retrieved Oct 10, 2020, from https://www.who.int/news-room/fact-sheets/detail/the-top-10-causes-of-death
World Health Organization. (2018b). Animal Bites. Retrieved Oct 10, 2020, from https://www.who.int/news-room/fact-sheets/detail/animal-bites
Wiemer, J., & Pauli, P. (2016). Fear-relevant illusory correlations in different fears and anxiety disorders: A review of the literature. Journal of Anxiety Disorders, 42, 113–128. https://doi.org/10.1016/j.janxdis.2016.07.003
Wardenaar, K. J., Lim, C. C., Al-Hamzawi, A. O., Alonso, J., Andrade, L. H., Benjet, C., … Gureje, O. (2017). The cross-national epidemiology of specific phobia in the world mental health surveys. Psychological Medicine, 47(10), 1744. https://doi.org/10.1017/S0033291717000174
Yang, J., Wang, A., Yan, M., Zhu, Z., Chen, C., & Wang, Y. (2012). Distinct processing for pictures of animals and objects: Evidence from eye movements. Emotion, 12(3), 540–551. https://doi.org/10.1037/a0026848
Young, S. G., Brown, C. M., & Ambady, N. (2012). Priming a natural or human-made environment directs attention to context-congruent threatening stimuli. Cognition & Emotion, 26(5), 927–933. https://doi.org/10.1080/02699931.2011.625399
Zhang, S., & Guo, Q. (2019). Superiority effect in detecting phylogenetic threats under Unattentional condition: A visual mismatch negativity study. Psychology Research, 9(9), 353–370. https://doi.org/10.17265/2159-5542/2019.09.002
Zsido, A. N., Deak, A., & Bernath, L. (2019a). Is a snake scarier than a gun? The ontogenetic–phylogenetic dispute from a new perspective: The role of arousal. Emotion, 19(4), 726. https://doi.org/10.1037/emo0000478
Zsido, A. N., Deak, A., Losonci, A., Stecina, D., Arato, A., & Bernath, L. (2018). Investigating evolutionary constraints on the detection of threatening stimuli in preschool children. Acta Psychologica, 185, 166–171. https://doi.org/10.1016/j.actpsy.2018.02.009
Zsido, A. N., Csatho, A., Matuz, A., Stecina, D. T., Arato, A., Inhof, O., & Darnai, G. (2019b). Does threat have an advantage after all?–proposing a novel experimental design to investigate the advantages of threat-relevant cues in visual processing. Frontiers in Psychology, 10, 2217. https://doi.org/10.3389/fpsyg.2019.02217
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of Interest
The authors declare that they have no conflict of interest.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Shapouri, S., Martin, L.L. Snakes vs. Guns: a Systematic Review of Comparisons Between Phylogenetic and Ontogenetic Threats. Adaptive Human Behavior and Physiology 8, 131–155 (2022). https://doi.org/10.1007/s40750-021-00181-5
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s40750-021-00181-5