Hostname: page-component-586b7cd67f-rdxmf Total loading time: 0 Render date: 2024-12-06T05:17:53.465Z Has data issue: false hasContentIssue false

We aren't especially fearful apes, and fearful apes aren't especially prosocial

Published online by Cambridge University Press:  08 May 2023

Raechel Drew
Affiliation:
Department of Psychology, University of British Columbia, Vancouver, BC V6T 1Z4, Canada [email protected] [email protected] [email protected]
Enda Tan
Affiliation:
Department of Human Development and Quantitative Methodology, University of Maryland, College Park, MD 20742-1131, USA Neuroscience and Cognitive Science Program, University of Maryland, College Park, MD 20742-1131, USA [email protected]
Francis Yuen
Affiliation:
Department of Psychology, University of British Columbia, Vancouver, BC V6T 1Z4, Canada [email protected] [email protected] [email protected]
J. Kiley Hamlin
Affiliation:
Department of Psychology, University of British Columbia, Vancouver, BC V6T 1Z4, Canada [email protected] [email protected] [email protected]

Abstract

Grossmann posits that heightened fearfulness in humans evolved to facilitate cooperative caregiving. We argue that three of his claims – that children express more fear than other apes, that they are uniquely responsive to fearful expressions, and that expression and perception of fear are linked with prosocial behaviors – are inconsistent with existing literature or require additional supporting evidence.

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

Are we really fearful apes, and are fearful apes more prosocial?

Grossmann proposes that humans are both more likely to express fear than other ape species and particularly sensitive to conspecifics' fear. This heightened fearfulness and fear detection, then, serves to elicit approach from caregivers, and increases one's own tendency to approach needy conspecifics. These tendencies ultimately ensure that humans receive, and deliver, the nurturance that uniquely characterizes our species. In what follows, we argue that these claims, although interesting and provocative, are currently unsupported by the broader literature in at least three ways. First, the assertion that humans are particularly fearful requires further evidence. Second, infants' sensitivity to fear (“fear bias”) may not actually reflect responsiveness to fear specifically, but rather to a broad range of distress signals. Finally, associations between both the expression and perception of fear and children's own prosocial behaviors are empirically tenuous. We detail our concerns below, ultimately concluding that the “fearful ape” may not be a useful description of the human species.

One aspect of Grossmann's hypothesis is that humans experience and express higher levels of fear than do other nonhuman primates. Support for this assertion comes from a single study (Herrmann, Hare, Cissewski, & Tomasello, Reference Herrmann, Hare, Cissewski and Tomasello2011) in which human infants demonstrated relatively more avoidance toward novel objects and people than did nonhuman ape species. These findings, however, suffer from some important confounds. First, there were significant age differences between the human (2.5 years) and nonhuman (6.4, 6.5, and 6.8 years) primate participants, a difference exacerbated by the faster rate of maturation in nonhumans. These age differences resulted in significant body size differences between participants and experimenters across species. That is, compared with 6.5-year-old nonhuman apes, 2.5-year-old children are much smaller than an adult experimenter, and might have displayed more fear because of the vulnerabilities this size difference entailed. Indeed, although this condition was not without interpretive difficulties, a control condition in which the experimenter was absent from the scene revealed no increased avoidance in humans. Thus, claiming that heightened fearfulness is an essential feature of the human species may be premature.

Another facet of Grossmann's hypothesis posits that infants are particularly sensitive to others' fear. We propose, instead, that the literature is more consistent with a general sensitivity to distress (Decety et al., Reference Decety, Bartal, Uzefovsky and Knafo-Noam2016; de Waal & Preston, Reference de Waal and Preston2017). While human infants do demonstrate sensitivity to fear (Leppänen & Nelson, Reference Leppänen and Nelson2012), they are also highly receptive to distress signals, including pain and sadness (Addabbo, Bolognini, & Turati, Reference Addabbo, Bolognini and Turati2021; Davidov et al., Reference Davidov, Paz, Roth-Hanania, Uzefovsky, Orlitsky, Mankuta and Zahn-Waxler2021; Dondi, Simion, & Caltran, Reference Dondi, Simion and Caltran1999). The fear bias literature typically compares infants' responses to fear solely with anger and happiness (Grossmann, Missana, & Krol, Reference Grossmann, Missana and Krol2018; Peltola, Leppänen, Mäki, & Hietanen, Reference Peltola, Leppänen, Mäki and Hietanen2009; Xie, McCormick, Westerlund, Bowman, & Nelson, Reference Xie, McCormick, Westerlund, Bowman and Nelson2019); these comparisons do not distinguish the “fearful ape” from the “distressed ape.” Indeed, some studies have shown that infants respond comparably and/or inconsistently to any arousing and/or threatening emotions (fear, anger, pain) relative to happy/neutral stimuli (Cheng, Lee, Chen, Wang, & Decety, Reference Cheng, Lee, Chen, Wang and Decety2012; Hunnius, de Wit, Vrins, & von Hofsten, Reference Hunnius, de Wit, Vrins and von Hofsten2011; Vanderwert et al., Reference Vanderwert, Westerlund, Montoya, McCormick, Miguel and Nelson2015). Thus, more evidence is required to show that infants are uniquely sensitive to fear.

Further, Grossmann suggests that the enhanced experience and privileged perception of fear make humans more caring and cooperative. To support the link between heightened fearfulness and prosociality, he draws from evidence suggestive that heightened fearfulness enhances children's guilt proneness, which in turn reduces rule violation (Kochanska, Gross, Lin, & Nichols, Reference Kochanska, Gross, Lin and Nichols2002). He also cites research showing that heightened fearfulness in children is associated with enhanced theory-of-mind skills (Wellman, Lane, LaBounty, & Olson, Reference Wellman, Lane, LaBounty and Olson2011), thought to be important for cooperation (Tomasello, Carpenter, Call, Behne, & Moll, Reference Tomasello, Carpenter, Call, Behne and Moll2005). Although guilt proneness and social-cognitive competencies are clearly relevant to prosociality, they are at best indirect measures. Further, direct evidence seems to contradict Grossmann's claims. For example, shyness is a core dimension of fearfulness traits (Henderson, Reference Henderson2010; Poole, Tang, & Schmidt, Reference Poole, Tang, Schmidt, Pérez-Edgar and Fox2018). Many studies have shown that higher levels of shyness is associated with reduced, rather than enhanced, prosocial behavior (Beier, Terrizzi, Woodward, & Larson, Reference Beier, Terrizzi, Woodward and Larson2017; Eisenberg et al., Reference Eisenberg, Fabes, Karbon, Murphy, Carlo and Wosinski1996; Karasewich, Kuhlmeier, Beier, & Dunfield, Reference Karasewich, Kuhlmeier, Beier and Dunfield2019; Tan, Mikami, Luzhanska, & Hamlin, Reference Tan, Mikami, Luzhanska and Hamlin2021; Young, Fox, & Zahn-Waxler, Reference Young, Fox and Zahn-Waxler1999), presumably because prosocial behavior requires social interaction with unfamiliar others. In addition, exhibiting fearfulness and inhibited responses early in life has consistently been associated with less adaptive social functioning (e.g., fewer close friends, higher loneliness, less prosocial behavior) and greater risk for developing social anxiety later in life (Clauss & Blackford, Reference Clauss and Blackford2012; Eisenberg, Spinrad, Taylor, & Liew, Reference Eisenberg, Spinrad, Taylor and Liew2019; Liew et al., Reference Liew, Eisenberg, Spinrad, Eggum, Haugen, Kupfer and Baham2011; Sandstrom, Uher, & Pavlova, Reference Sandstrom, Uher and Pavlova2020; Tang et al., Reference Tang, Crawford, Morales, Degnan, Pine and Fox2020). Thus, rather than promoting prosociality, enhanced fearfulness appears to have a negative impact on prosocial behavior specifically and social functioning broadly.

To support the assertion that sensitivity to fear facilitates children's prosociality, Grossmann offers limited evidence that children who exhibit a fear bias are more helpful and generous (Grossmann et al., Reference Grossmann, Missana and Krol2018; Rajhans, Altvater-Mackensen, Vaish, & Grossmann, Reference Rajhans, Altvater-Mackensen, Vaish and Grossmann2016). However, different means of measuring fear bias across these studies (e.g., latency to fixate, duration of first look) make this argument less convincing. Further, it seems that responsiveness to distress signals generally, not fear specifically, elicits caring behavior (Davidov, Zahn-Waxler, Roth-Hanania, & Knafo, Reference Davidov, Zahn-Waxler, Roth-Hanania and Knafo2013; Decety, Reference Decety, Bartal, Uzefovsky and Knafo-Noam2016). For instance, individual differences in 3–10-month-olds' empathic concern for peers and adults feigning injury (i.e., pained, not fearful) predicts caring responses at 12–18 months (Davidov et al., Reference Davidov, Paz, Roth-Hanania, Uzefovsky, Orlitsky, Mankuta and Zahn-Waxler2021; Roth-Hanania, Davidov, & Zahn-Waxler, Reference Roth-Hanania, Davidov and Zahn-Waxler2011), suggesting a role for processing others' pain in facilitating prosocial responses. Even past work from Grossmann's own lab suggests that viewing painful (vs. angry) expressions activates approach mechanisms during infancy (i.e., left hemisphere activation; Missana, Grigutsch, & Grossmann, Reference Missana, Grigutsch and Grossmann2014). Thus, evidence supporting a unique relationship between responsiveness to fear and caring behaviors appears tenuous at best.

Although Grossmann's hypothesis is intriguing, it contradicts existing work or requires further evidence to support three of its major claims: That humans are particularly fearful, highly receptive to fear, and that these tendencies promote prosociality. Instead, it is more likely that human caregiving and prosocial behavior result from the expression of, and sensitivity to, a broad range of distress cues.

Financial support

RD was supported by a Joseph-Armand Bombardier Canada Graduate Scholarship under award 767-2019-2852. ET was supported by a Social Sciences and Humanities Research Council of Canada (SSHRC) Postdoctoral Fellowship under award 756-2022-0589. JKH was supported by an SSHRC Insight Grant under award F18-04495.

Competing interest

None.

References

Addabbo, M., Bolognini, N., & Turati, C. (2021). Neural time course of pain observation in infancy. Developmental Science, 24(4), e13074. https://doi.org/10.1111/desc.13074CrossRefGoogle ScholarPubMed
Beier, J. S., Terrizzi, B. F., Woodward, A. M., & Larson, E. G. (2017). Shyness and social conflict reduce young children's social helpfulness. Child Development, 88(6), 19221929. https://doi.org/10.1111/cdev.12681CrossRefGoogle ScholarPubMed
Cheng, Y., Lee, S. Y., Chen, H. Y., Wang, P. Y., & Decety, J. (2012). Voice and emotion processing in the human neonatal brain. Journal of Cognitive Neuroscience, 24(6), 14111419. https://doi.org/10.1162/jocn_a_00214CrossRefGoogle ScholarPubMed
Clauss, J. A., & Blackford, J. U. (2012). Behavioral inhibition and risk for developing social anxiety disorder: A meta-analytic study. Journal of the American Academy of Child & Adolescent Psychiatry, 51(10), 10661075. e1061. https://doi.org/10.1016/j.jaac.2012.08.002CrossRefGoogle ScholarPubMed
Davidov, M., Paz, Y., Roth-Hanania, R., Uzefovsky, F., Orlitsky, T., Mankuta, D., & Zahn-Waxler, C. (2021). Caring babies: Concern for others in distress during infancy. Developmental Science, 24(2), e13016. https://doi.org/10.1111/desc.13016CrossRefGoogle ScholarPubMed
Davidov, M., Zahn-Waxler, C., Roth-Hanania, R., & Knafo, A. (2013). Concern for others in the first year of life: Theory, evidence, and avenues for research. Child Development Perspectives, 7(2), 126131. https://doi.org/10.1111/cdep.12028CrossRefGoogle Scholar
Decety, J., Bartal, I. B. A., Uzefovsky, F., & Knafo-Noam, A. (2016). Empathy as a driver of prosocial behaviour: Highly conserved neurobehavioural mechanisms across species. Philosophical Transactions of the Royal Society B: Biological Sciences, 371(1686), 20150077. https://doi.org/10.1098/rstb.2015.0077CrossRefGoogle ScholarPubMed
de Waal, F., & Preston, S. D. (2017). Mammalian empathy: Behavioural manifestations and neural basis. Nature Reviews Neuroscience, 18(8), 498509. https://doi.org/10.1038/nrn.2017.72CrossRefGoogle ScholarPubMed
Dondi, M., Simion, F., & Caltran, G. (1999). Can newborns discriminate between their own cry and the cry of another newborn infant?. Developmental Psychology, 35(2), 418426. https://doi.org/10.1037/0012-1649.35.2.418CrossRefGoogle ScholarPubMed
Eisenberg, N., Fabes, R. A., Karbon, M., Murphy, B. C., Carlo, G., & Wosinski, M. (1996). Relations of school children's comforting behavior to empathy-related reactions and shyness. Social Development, 5, 330351. https://doi.org/10.1111/j.1467-9507.1996.tb00089.xCrossRefGoogle Scholar
Eisenberg, N., Spinrad, T. L., Taylor, Z. E., & Liew, J. (2019). Relations of inhibition and emotion-related parenting to young children's prosocial and vicariously induced distress behavior. Child Development, 90(3), 846858.CrossRefGoogle ScholarPubMed
Grossmann, T., Missana, M., & Krol, K. M. (2018). The neurodevelopmental precursors of altruistic behavior in infancy. PLoS Biology, 16(9), e2005281. https://doi.org/10.1371/journal.pbio.2005281CrossRefGoogle ScholarPubMed
Henderson, H. A. (2010). Electrophysiological correlates of cognitive control and the regulation of shyness in children. Developmental Neuropsychology, 35(2), 177193. https://doi.org/10.1080/87565640903526538CrossRefGoogle ScholarPubMed
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
Hunnius, S., de Wit, T. C., Vrins, S., & von Hofsten, C. (2011). Facing threat: Infants’ and adults’ visual scanning of faces with neutral, happy, sad, angry, and fearful emotional expressions. Cognition & Emotion, 25(2), 193205. https://doi.org/10.1080/15298861003771189mCrossRefGoogle ScholarPubMed
Karasewich, T. A., Kuhlmeier, V. A., Beier, J. S., & Dunfield, K. A. (2019). Getting help for others: An examination of indirect helping in young children. Developmental Psychology, 55(3), 606611. https://doi.org/10.1037/dev0000654CrossRefGoogle ScholarPubMed
Kochanska, G., Gross, J. N., Lin, M.-H., & Nichols, K. E. (2002). Guilt in young children: Development, determinants, and relations with a broader system of standards. Child Development, 73(2), 461482. https://doi.org/10.1111/1467-8624.00418CrossRefGoogle ScholarPubMed
Leppänen, J. M., & Nelson, C. A. (2012). Early development of fear processing. Current Directions in Psychological Science, 21(3), 200204. https://doi.org/10.1177/0963721411435841CrossRefGoogle Scholar
Liew, J., Eisenberg, N., Spinrad, T. L., Eggum, N. D., Haugen, R. G., Kupfer, A., … Baham, M. E. (2011). Physiological regulation and fearfulness as predictors of young children's empathy-related reactions. Social Development, 20(1), 111134. https://doi.org/10.1111/j.1467-9507.2010.00575.xCrossRefGoogle ScholarPubMed
Missana, M., Grigutsch, M., & Grossmann, T. (2014). Developmental and individual differences in the neural processing of dynamic expressions of pain and anger. PLoS One, 9(4), e93728. https://doi.org/10.1371/journal.pone.0093728CrossRefGoogle ScholarPubMed
Peltola, M. J., Leppänen, J. M., Mäki, S., & Hietanen, J. K. (2009). Emergence of enhanced attention to fearful faces between 5 and 7 months of age. Social Cognitive and Affective Neuroscience, 4(2), 134142. https://doi.org/10.1093/scan/nsn046CrossRefGoogle ScholarPubMed
Poole, K. L., Tang, A., & Schmidt, L. A. (2018). The temperamentally shy child as the social adult: An exemplar of multifinality. In Pérez-Edgar, K. & Fox, N. A. (Eds.), Behavioral inhibition (pp. 185212). Springer.CrossRefGoogle Scholar
Rajhans, P., Altvater-Mackensen, N., Vaish, A., & Grossmann, T. (2016). Children's altruistic behavior in context: The role of emotional responsiveness and culture. Scientific Reports, 6(1), 16. https://doi.org/10.1038/srep24089CrossRefGoogle ScholarPubMed
Roth-Hanania, R., Davidov, M., & Zahn-Waxler, C. (2011). Empathy development from 8 to 16 months: Early signs of concern for others. Infant Behavior & Development, 34(3), 447458. https://doi.org/10.1016/j.infbeh.2011.04.007CrossRefGoogle ScholarPubMed
Sandstrom, A., Uher, R., & Pavlova, B. (2020). Prospective association between childhood behavioral inhibition and anxiety: A meta-analysis. Journal of Abnormal Child Psychology, 48(1), 5766. https://doi.org/10.1007/s10802-019-00588-5Google ScholarPubMed
Tan, E., Mikami, A. Y., Luzhanska, A., & Hamlin, J. K. (2021). The homogeneity and heterogeneity of moral functioning in preschool. Child Development, 92(3), 959975. https://doi.org/10.1111/cdev.13458CrossRefGoogle ScholarPubMed
Tang, A., Crawford, H., Morales, S., Degnan, K. A., Pine, D. S., & Fox, N. A. (2020). Infant behavioral inhibition predicts personality and social outcomes three decades later. Proceedings of the National Academy of Sciences, 117(18), 201917376. https://doi.org/10.1073/pnas.1917376117CrossRefGoogle ScholarPubMed
Tomasello, M., Carpenter, M., Call, J., Behne, T., & Moll, H. (2005). Understanding and sharing intentions: The origins of cultural cognition. Behavioral and Brain Sciences, 28(5), 675691. https://doi.org/10.1017/S0140525X05000129CrossRefGoogle ScholarPubMed
Vanderwert, R. E., Westerlund, A., Montoya, L., McCormick, S. A., Miguel, H. O., & Nelson, C. A. (2015). Looking to the eyes influences the processing of emotion on face-sensitive event-related potentials in 7-month-old infants. Developmental Neurobiology, 75(10), 11541163. https://doi.org/10.1002/dneu.22204CrossRefGoogle Scholar
Wellman, H. M., Lane, J. D., LaBounty, J., & Olson, S. L. (2011). Observant, nonaggressive temperament predicts theory-of-mind development. Developmental Science, 14(2), 319326. https://doi.org/10.1111/j.1467-7687.2010.00977.xCrossRefGoogle ScholarPubMed
Xie, W., McCormick, S. A., Westerlund, A., Bowman, L. C., & Nelson, C. A. (2019). Neural correlates of facial emotion processing in infancy. Developmental Science, 22(3), e12758. https://doi.org/10.1111/desc.12758CrossRefGoogle ScholarPubMed
Young, S. K., Fox, N. A., & Zahn-Waxler, C. (1999). The relations between temperament and empathy in 2-year-olds. Developmental Psychology, 35, 11891197. https://doi.org/10.1037/0012-1649.35.5.1189CrossRefGoogle ScholarPubMed