Extending and refining the fearful ape hypothesis

Abstract

The fearful ape hypothesis (FAH) presents an evolutionary-developmental framework stipulating that in the context of cooperative caregiving, unique to human great ape group life, heightened fearfulness was adaptive. This is because from early in human ontogeny fearfulness expressed and perceived enhanced care-based responding and cooperation with mothers and others. This response extends and refines the FAH by incorporating the commentaries' suggestions and additional lines of empirical work, providing a more comprehensive and nuanced version of the FAH. Specifically, it encourages and hopes to inspire cross-species and cross-cultural, longitudinal work elucidating evolutionary and developmental functions of fear in context. Beyond fear, it can be seen as a call for an evolutionary-developmental approach to affective science.

R1. Introduction

The novel evolutionary-developmental framework presented herein – the fearful ape hypothesis (FAH) – suggests that, in the context of the strong interdependence reflected in cooperative caregiving and provisioning unique to human great ape group life, enhanced fearfulness traits serve adaptive functions. The central hypothesis supported by the reviewed body of empirical research is that, starting early in human ontogeny, fearfulness traits facilitate care-based responding and provisioning from, while concurrently increasing cooperation with, mothers and others. Within this framework, enhanced fearfulness is assumed to be of adaptive value because of its functions in facilitating cooperative care across the lifespan, improving survival and reproduction in human evolution.

From a cultural perspective, enhanced fearfulness traits can thus be considered adaptive in interdependent human societies primarily build on cooperative care and success, whereas enhanced fearfulness has become maladaptive in independent human societies build more strongly on individual success and less so on cooperative care. The new synthesis based on the fearful ape hypothesis, stands in contrast to existing clinical work relying on Western, educated, industrialized, rich, and democratic (WEIRD) samples, conceptualizing heightened fearfulness as a predominately maladaptive trait increasing the risk of developing anxiety and depression. Viewing fearfulness traits through a WEIRD lens focused on risk conflicts with the presumed social environment that interdependent human group life evolved in and is adapted to. According to the fearful ape hypothesis, enhanced fear is considered an evolved adaptive trait that enhances cooperative care and success, which emerged in and is maintained by highly interdependent and supportive human societies. When viewed through this evolutionary lens, a radically different picture arises, painting an image of humans as fearful apes, trading off a risk for anxiety and depression with the affective foundations for cooperative care.

This response extends and refines the FAH by incorporating the conceptual and empirical points brought forward in the commentaries. Specifically, this response will address the following issues in turn. First, what kind of adaptation does the FAH invoke? Second, how can the FAH be extended by considering the roles of development, context, and learning? Third, how specific is the proposed affective/emotional adaptation to fear or may it extend more generally to suffering, distress, and anxiety? Fourth, how can the FAH be reconciled with research linking positive emotion to cooperation? Fifth, does responding to novelty (and cognitive control) rather than responding to fear account for the link between fear processing and cooperation? Sixth, what role does culture and caregiving play in what makes enhanced fear (mal)adaptive? Finally, this response discusses previously overlooked research indicating that enhanced fear may have direct adaptive benefits as it is linked to reproductive success. Together, this is aimed at providing a more comprehensive and nuanced version of the FAH in the hope to inspire cross-species and cross-cultural, longitudinal approaches to studying the evolutionary and developmental functions of fear in context.

R2. Enhanced fear: What kind of adaptation is it?

Before delving into the specific points made regarding the ontogenetic and phylogenetic evidence and reasoning behind the fearful ape hypothesis (FAH), it appears critical to address the important conceptual question raised by Bjorklund & Hernández Blasi, namely, what kind of adaptation is purported in the FAH? Specifically, Bjorklund & Hernández Blasi emphasize that one needs to distinguish between ontogenetic adaptations and deferred adaptations. According to Bjorklund & Hernández Blasi, ontogenetic adaptations are evolutionary solutions to specific problems with an immediate function in early development, whereas deferred adaptations represent an evolutionary solution to a problem beginning early in life and serving the same or at least a similar function later in development. Bjorklund & Hernández Blasi then argue that the adaptation invoked by the FAH likely represents an ontogenetic adaptation and is as such similar to other ontogenetic adaptations such as other evolved infantile traits that elicit care such as neotenous facial features (Kindchenschema), smiles and laughs, coos and cries, which do not play a role beyond early ontogeny/infancy. However, the notion that the FAH may represent an ontogenetic adaptation is at odds with a body of research attesting to the important role that enhanced fear continues to play in adolescence and adulthood (Marsh, 2015). In fact, in their commentary, Marsh presents a strong case based on research with adults to conclude that humans are not only fearful apes but also caring apes endowed with a multitude of social cues to convey our fear to concerned others providing help. In this context, it is important to mention that human infants, similar to adults, have been shown to detect not only facial expression of fear but also bodily expressions of fear and vocal signals of distress (Missana, Altvater-Mackensen, & Grossmann, 2017; Missana, Atkinson, & Grossmann, 2015; Missana, Rajhans, Atkinson, & Grossmann, 2014; Rajhans, Jessen, Missana, & Grossmann, 2016), supporting Marsh's point regarding the multitude of social cues used to express and respond to fear.

Intriguingly, a newly published study relying on longitudinal data from the Finn Brain Birth Cohort study (Kataja et al., 2022) lends some credence to Bjorklund & Hernández Blasi's ontogenetic adaptation point, as this study shows that fear bias decreases (linearly) with age from 8 months to 60 months (5 years). Therefore, based on these novel insights, not available at the time the target article was written, enhanced fear might be most pronounced in early ontogeny. It is worth noting, however, that even though the fear bias was found to decrease with age, there still is a fear bias at 5 years of age. It is also important to mention that this study assessed the fear bias by measuring the disengagement probability when presenting an emotional face in the center of a screen and by assessing how quickly they disengage from the center image to a (non-emotional) distractor image located at the flanks of the screen (Kataja et al., 2022). This form of disengagement likely requires attentional processes related to cognitive control, which show a protracted development beyond infancy associated with the maturation of lateral prefrontal cortex (Holmboe, Bonneville-Roussy, Csibra, & Johnson, 2018). In any case, as summarized in the target article, the fear bias (in perception) does not exist among great apes (Kret, Jaasma, Bionda, & Wijnen, 2016; Kret, Muramatsu, & Matsuzawa, 2018), therefore, the species-level differences remain. It will also be important to see whether the decline in fear bias during early development observed in the Finnish sample generalizes across cultures. More specifically, enhanced fear might be tolerated less in Western (individualistic) societies but may even be promoted in Eastern (collectivistic) societies and cultural learning may play an important role in the developmental trajectory characteristics of the fear bias (see also, Kitayama & Rossmaier).

R3. Extending the FAH by considering development, context, and learning

From an ontogenetic perspective, Hepach & Gerdemann extend the FAH by proposing that enhanced fear may continue to play a critical role in regulating cooperation beyond infancy. Specifically, they suggest that with the widening of the children's social networks and relationships during preschool years, the increased complexity of peer interactions and the emergence of the capacity for reputation management, social emotions such as shame emerge that reflect children's concern for and perhaps even a fear of others' evaluation. Within this proposal the stipulated continued (adaptive) influence of enhanced fear beyond infancy stands in contrast to Bjorklund & Hernández Blasi's critique and classification of enhanced fear as an ontogenetic adaptation limited to infancy. Evidence that enhanced fearful temperament is linked to greater expression of social emotions – especially – guilt was already included and discussed by us in the target article (Kochanska, Gross, Lin, & Nichols, 2002). This might be seen as tentatively supporting Hepach & Gerdemann's proposal. Nonetheless, as proposed by Hepach & Gerdemann, future work adopting a longitudinal approach mapping human fear and its effects on social emotions and cooperation is needed to directly test this developmental extension of the FAH.

Related to Hepach & Gerdemann's suggestions, MacGowan, Karasewich, & Kuhlmeier stress that it is important to differentiate between social and nonsocial fears. However, as clearly outlined in the target article, enhanced fear among humans was seen across social and nonsocial contexts (Herrmann, Hare, Cissewski, & Tomasello, 2011). Therefore, the species-comparison and phylogenetic argument was based on fear across contexts. There obviously is much need for additional research especially at the phylogenetic level which examines fearfulness across species in nonsocial and social contexts. Regarding enhanced fearful behavior in social contexts or shyness, it is important to acknowledge research suggesting an adaptive subtype of shyness referred to as positive shyness, which is characterized by the expression of shy behavior in social interactions (e.g., gaze aversion, avoidance) in combination with positive affect (e.g., smiling) (Poole & Schmidt, 2020). Positive shyness is argued to be an adaptive phenotype that helps the shy individual modulate arousal in social contexts, which may protect the shy individual from maladjustment. Moreover, cultural context may play an important role in determining whether shyness among children is considered adaptive. In societies that endorse collectivistic values and norms, shyness in children and adolescents is viewed favorable by parents and others (Gurr et al., 2020; Yiu, Choi, & Chen, 2020). These suggestions and considerations can be seen as largely in agreement with the view put forward within the FAH as they also point to the potential adaptive and culture-sensitive nature of enhanced fearfulness.

Dwyer & Heyes see enhanced fearfulness as an important addition to what they call the “starter kit” for distinctively human minds and demand to further explicate the role that learning (and perception–action coupling) may play in the development of enhanced fearfulness during infancy. More specifically, within their framework, heightened fear is argued to provide critical learning opportunities by enhancing (a) emotional displays of fear co-occurring with the internal emotional experience of fear, (b) caregiver imitation and mirroring of fear, and (c) alignment of fear responses to external stimuli or events with others. Fear enhanced perception–action coupling and learning clearly plays an important role in the acquisition of fearful behavior in the developing individual and should thus be seen as a critical proximate mechanism within the FAH. However, as acknowledged by Dwyer & Heyes, heightened fearfulness is a part of the foundational “starter kit” and is thus needed to get learning off the ground rather than learning being the ultimate origin of the evolutionary trait itself.

Olsen & Selbing also stress the importance of social learning and mention a host of studies supporting the notion of vicarious social learning of fears including work with children, which might indeed represent another facet of the adaptive value of enhanced fearfulness in humans. However, Olsen & Selbing propose that social (observational) learning itself serves as the primary (ultimate) mechanism and care-based cooperation is only a byproduct of domain-general social learning capacities. Similar to the notion put forward in Dwyer & Heyes' commentary, we agree that (social) learning likely plays an important role in understanding enhanced fearfulness and the FAH needs to be extended by incorporating social learning as a critical proximate mechanism, yet it is not clear how this general social learning mechanism can explain the fear-specific effects seen in the phylogenetic and ontogenetic empirical evidence reviewed to support the FAH.

R4. Evolutionary test and behavioral economic extension of the FAH

In their commentary, Burkart & de Oliveira Terceiro point out that the FAH leads to strong predictions in callitrichids, who are the only other cooperative breeding primates. They then present work that may indeed support the FAH by showing that callitrichids display more distress than independently breeding monkeys and are also more likely to respond to distress signals with approach and affiliation. Similarly, Dunn, Miller, Balasubramaniam, Akçay, & Wascher point to research with corvids showing that enhanced fearfulness, especially neophobia, tracks with levels of cooperative care (Horn et al., 2020; Miller et al., 2022). These findings from cooperative breeders provide further evidence for the notion that cooperative breeding may have indeed provided a precondition, which allowed for the emergence of enhanced fearfulness in humans, who are the only cooperatively breeding great apes. Nonetheless, a much broader and systematic comparative analysis is needed to better characterize and understand the evolution of enhanced fearfulness traits and the role of socioecological variables more generally.

Barkan & Lahav present a rational behavioral economic analysis from two mixed-motive games with strong interdependence, which support and complement the FAH. More specifically, their game theoretical analysis shows that weakness elicits cooperative, caring responses from a stronger player leading to an equilibrium, even in sequential games. This is an important extension into the realm of behavioral economics and presents a critical test of a novel prediction generated based on the FAH.

Halevy points out that research on social decision-making with adults shows that states of fear can also be associated with aggressive or competitive behavior, which seemingly undermines the FAH. Regarding this criticism, it is important to re-emphasize something already stressed in the target article. Namely, the FAH stipulates that a human-specific link between heightened fear and cooperation exists in addition to fight (and flight) responses shared with many other animals when experiencing fear. Moreover, the FAH explicitly refers to fearfulness as an affective trait and thereby distinguishes it from affective state as used in the social decision-making research mentioned by Halevy. Therefore, Halevy's criticism does not directly undermine the FAH but rightly alerts us to a need for more systematic decision-making and behavior economics research including measures of affective traits to test the FAH.

R5. Beyond fear: Humans as suffering, distressed, or anxious apes?

Steinkopf argues that the FAH should be considered as only one facet of a more general “suffering ape hypothesis” (see Barclay, Yerman, & Twardus; Clark, Adkins, Hirsch, Elizbeth, and Reed, for similar argument), suggesting that humans are more likely to experience all sorts of negative emotions, aversive symptoms, and self-harming behavior, because they elicit caring which then provides fitness benefits. In response to this comment, it is important to clarify and stress that the FAH never claimed that fear is the only emotion enhanced or changed over the course of human evolution. For example, we already discussed the self-domestication hypothesis (Hare, 2017) at length, which shows that other affective traits such as social tolerance and aggression have changed during human evolution. More specifically, with respect to Steinkopf's specific suggestions, it might well be the case that other facets of human affective life are different from other great apes, however, to our knowledge, there currently is no direct evidence from comparative (phylogenetic) work supporting the notion of human-specific suffering responses as outlined by Steinkopf. Therefore, a more general human suffering hypothesis currently lacks empirical support.

Similar to Steinkopf's criticism, Drew, Tan, Yuen, & Hamlin (Drew et al.) suggest that humans, rather than being uniquely fearful apes, might instead be more generally “distressed apes.” This argument is based on research showing that responsiveness to distress signals generally, not fear specifically, elicits caring behavior (Davidov et al., 2021; Davidov, Zahn-Waxler, Roth-Hanania, & Knafo, 2013; Roth-Hanania, Davidov, & Zahn-Waxler, 2011). In response to this comment, it is important to note that we already emphasize that within the FAH framework, expression of fear is thought to convey distress rather than threat as has often been claimed (see also Marsh's commentary). We also previously acknowledged work linking increased levels of fearfulness to greater levels of crying as a vocal signal of distress (Kagan & Snidman, 2004). In fact, Davidov et al.'s (2021) most recent study and prior work from this group (Roth-Hanania et al., 2011) explicitly used a video stimulus of an infant peer crying (when separated from her mother during the strange situation) when measuring infants' concern, which is linked to emotional helping behavior in these longitudinal studies. Therefore, Drew et al.'s comment implies a narrowness of the FAH that is not at all intended by the theoretical proposal put forward, which explicitly assigns a role to distress signaling in accounting for enhanced fearfulness in humans.

Relatedly, Mercadante, Witkower, Hohm, & Tracy (Mercadante et al.) suggest extending the FAH by including additional emotions beyond fear. Specifically, they argue for the FAH to be extended by including so-called supplication emotions, referring to a group of emotions that comprises not only fear but also sadness, disappointment, distress, and worry and appeasement emotions such as shame, guilt, and regret, which are all presumed to serve cooperative functions in human interactions and relationships. As noted above, the FAH is already explicit about the inclusion of distress and may have room to accommodate other supplication emotions in the framework. However, as noted by Mercadante et al., species comparisons are currently lacking, and it remains to be seen whether the human-specific effects obtained for fear (and distress) extend to other supplication emotions. With respect to the appeasement emotions mentioned, they all fall within the category of moral or social emotions, which since Darwin have been argued to be specific to humans (Darwin, 1872). Critically, these moral emotions have been shown to display relatively distinct comparative, developmental, cognitive, and brain characteristics from the supplication emotions (Tomasello & Vaish, 2013; Zahn, de Oliveira-Souza, & Moll, 2020), rendering it unlikely that they emerged through similar processes in human evolution as enhanced fearfulness. Nonetheless, it should be noted that we already explicitly mention work by Kochanska et al. (2002), showing that children who are more fearful in temperament are more likely to experience guilt listed as one of the appeasement emotions by Mercadante et al.

Kurth argues that a distinction should be drawn between fear as a reaction to immediate danger or threat resulting in freeze, fight, or flight responses, and anxiety as reflecting a distinct set of processes seen when facing uncertain threats. Kurth further suggests that anxiety rather than fear is at play in the FAH. To clarify, fear rather than anxiety was explicitly chosen in the FAH framework because it: (1) stands in contrast to the clinical, pathological, diagnostic meaning often associated with anxiety, (2) draws attention to natural variability on a dimension of fearfulness rather than a categorical difference (fear vs. anxiety), and (3) allows for continuity between species, whereby fear is shared with other apes and enhanced fear in humans represents a quantitative, gradual difference, and evolutionary modification. To further clarify, it is also important to stress that enhanced fear within the FAH refers to an evolved trait, which is linked to but not the same as the state of fear in the moment.

R6. Beyond fear continued: Humans as happy apes?

Another criticism put forward across several commentaries was based on evidence linking positive affect, smiling, and laughing with human cooperation (see daSilva & Bertenthal; Drew et al.; Herbert, Condry, & Sutton; Riddell, Kret, Zijlstra, & Nikolic [Riddell et al.]; Yang). This evidence is then used to argue that, in contrast to the FAH, humans are instead happy apes (Yang) and fear is not “human-unique” (Riddell et al.). In this context, it is important to reiterate that the FAH did not claim that fear is the only emotion changed/modified over the course of human evolution and further the FAH never suggested that fear is the only route to human cooperation. Importantly, human cooperation is highly complex and multi-determined (Rand & Nowak, 2013; Tomasello & Vaish, 2013), allowing for several psychological processes to be (simultaneously) linked to cooperation. In other words, links between enhanced fear and cooperation and increased happiness/positive affect and cooperation are not mutually exclusive. Nonetheless, it is critical to emphasize that empirical evidence discussed in the FAH review clearly demonstrates that, in human infancy, brain and attentional responses to fear, but not happiness, are linked to cooperative behavior. Specifically, in a longitudinal study, brain and attentional responses to fearful faces, but not to angry or happy faces, at 7 months of age predicted helping behavior at 14 months of age (Grossmann, Missana, & Krol, 2018). Another longitudinal study with infants at similar ages also failed to find evidence that infant positive emotion was linked to cooperative helping behavior (Davidov et al., 2021). Moreover, positive emotion has been shown to be the result of and hence follows rather than precedes cooperative behavior in toddlers, whereas concern for others precedes and more directly motivates cooperative behavior (Grossmann, 2018). For example, in a series of studies, concern for others, as reflected in sympathetic arousal, preceded helping behavior in toddlers, whereas elevated body posture, as an index of positive affect, followed helping behavior (Hepach, Vaish, Muller, & Tomasello, 2019; Hepach, Vaish, & Tomasello, 2012, 2017).

Relatedly, daSilva & Bertenthal raised the issue that biobehavioral synchrony and positive dyadic engagement with the caregiver rather than fear is at the origin of human cooperative care. Again, the FAH did not claim that fear is exclusive in this sense and that other factors cannot play a role in the emergence of human cooperative care. From an empirical perspective, however, it is important to mention that infants' responding to fearful faces selectively predicted their cooperative behavior even when controlling for positive maternal engagement measured during dyadic interactions (Grossmann et al., 2018), suggesting that the link between fearful face processing and cooperative behavior exists independent of positive maternal engagement. In fact, recent research suggests that positive maternal engagement only affects infants' brain responses to angry facial expressions, signaling direct threat, but did not affect infants' responses to fearful or happy facial expressions (Thrasher, Krol, & Grossmann, 2021).

R7. Novelty versus fear

Kelsey proposes an alternative explanation by arguing that rather than being specific to fear, infant responses to fear are driven by novelty and links between fear processing and cooperation may thus be mediated by greater cognitive control processes when facing novelty. Regarding this point, it is critical to mention that novelty is unlikely to account for the experimentally observed effects, because the study Kelsey is pointing to also used angry facial expressions, which are equally novel to infants, but did not predict cooperative behavior longitudinally (Grossmann et al., 2018). Moreover, in this study, when processing fear greater engagement of dorso-lateral prefrontal cortex, as one of the key brain regions implicated in cognitive control, was associated with reduced rather than enhanced levels of cooperative behavior. This is in line with other work showing that: (1) fear processing is automatic and occurs without conscious perception (Jessen & Grossmann, 2014, 2015, 2020) and (2) enhanced cognitive control (inhibitory control) is associated with reduced levels of cooperative behavior in infants (Grossmann, Missana, & Vaish, 2020). Therefore, cognitive control is an unlikely candidate for explaining early cooperative behavior. Similarly, research with adults also suggests that at least some cooperative behaviors are intuitive (implicit) rather than deliberative (explicit) in nature (Rand, 2016; Zaki & Mitchell, 2013) and that the link between fear and cooperative behavior is underpinned by implicit processes as it is seen during subliminal priming with fearful faces and linked to subcortical (amygdala) processes (Marsh, 2015).

R8. Culture matters

Ogren, Barrett, Hoemann, & LoBue (Ogren et al.) make the point that fearfulness is associated with negative long-term outcomes (see also Krstić for another commentary suggesting that fear is maladaptive). This is correct but exclusively based on data from WEIRD cultures. Even the cross-cultural work referred to by Ogren et al. as indicating negative developmental outcomes stems from WEIRD samples, Netherlands, and South Africa (Howard, Muris, Loxton, & Wege, 2017; Vreeke, Muris, Mayer, Huijding, & Rapee, 2013). Here it is important to reiterate that the FAH does not deny that extreme fearfulness is associated with negative outcomes (primarily in WEIRD samples), but rather tries to draw attention to the possibility that enhanced fearfulness evolved in the context of inter-dependent (collectivistic) group life. The FAH thus generates the proposal that it is important to study effects of cultural context, especially with respect to differences between cultures emphasizing collectivistic (interdependent) values and practices, and cultures emphasizing individualistic (independent) values and practices.

Indeed, Kitayama & Rossmaier present a whole line of research indicating that in collectivistic cultures but not in individualistic cultures, increased neuroticism, which links to the enhanced fearfulness traits invoked by the FAH, is associated with a whole host of positive (adaptive) outcomes. Kitayama & Rossmaier's commentary thus largely provides additional support for the ideas put forward in the FAH. However, Kitayama & Rossmaier also raised the criticism that the FAH falsely points to small-scale societies as the cultural context matching the enhanced fearfulness profile, because enhanced fearfulness (or more specifically neuroticism) is still adaptive in current large-scale societies characterized by collectivism/interdependence. In response to this point, we would like to clarify that the proposal was that enhanced fearfulness likely first evolved in small-scale groups of ancestral humans characterized by interdependence, but FAH never entailed that it is not adaptive (or cannot be associated with positive outcomes) in current large-scale societies, which also rely on interdependence (collectivism). In fact, when discussing the implications of the FAH, we explicitly refer to work from Eastern (collectivistic) countries showing that developmental outcomes are largely positive in this cultural context. We also raise the possibility that increased rates of anxiety and depression in WEIRD societies may represent a mismatch disease. Regarding the potential mismatch, Kitayama & Rossmaier present an important factor interacting with neuroticism, which is behavioral adjustment. Neuroticism is argued to be adaptive in the context of high behavioral adjustment in interdependent cultures, which positively sanction behavioral adjustment. Behavioral adjustment and social/cultural learning thus appear to represent an important proximate mechanism that may help explain the effects of enhanced fearfulness in varying cultural contexts.

R9. Caregiving matters

Another issue raised by Ogren et al. is that caregivers respond to all affective behaviors not just those perceived as fearful. Regarding this point, it seems critical to stress that the FAH never made any claims as to how fearful behavior is the only way to elicit care, but rather intends to put enhanced fearfulness “on the map” as a potential early-developing affective trait that serves such functions. In fact, other commentaries acknowledge this contribution of the FAH by noting that enhanced fearfulness may be added to other adaptations to elicit care. A further criticism is based on work showing that caregiver responsiveness reduces fear in the infant/child (see also Shteynberg). In fact, we explicitly mention research along these lines, in order to support our argument that displays of fear elicit care and protection, which makes it a functional adaptation. Within the FAH, reducing infant fear in any given instance through caregiver responsiveness is seen as a functional outcome rather than evidence undermining the notion that human infants and children display enhanced fear. Relatedly, the FAH conceives of enhanced fearfulness as a trait, whereas the reduction of fear as a function of caregiver responsiveness focuses on the state. Concerning caregiver responding, Parsons & Skewes point out that excessive infant crying has also been associated with maladaptive responses in caregivers, specifically shaking and in severe instances of physical abuse. The existence of extreme parental responses such as physical abuse being associated with excessive crying is important to acknowledge, but does not directly undermine the FAH, whereby fearfulness traits – enhanced in comparison to our closest living primate relatives – are thought to elicit increased caring behavior. Within any of these species, there is a range of infant fearfulness and a range of parental/caregiver responsiveness that at the extreme ends of the distribution may then be related to maladaptive behaviors and outcomes.

R10. Sex differences may exist

Veit & Browning see the FAH largely in agreement with their own theoretical framework (Veit & Browning, 2022) and suggest that one potential application or extension may be the consideration of sex differences in affective traits (see also Benítez-Burraco and Progovac). Specifically, they make the argument that greater self-protection among human females should be considered as an adaptive rather than pathological trait that evolved as an optimal life-history strategy. Therefore, greater fearfulness, depression, and anxiety among human females than human males as is commonly reported across studies, may represent one manifestation of this greater self-protection strategy in human female life history. This notion is compatible with the FAH and further strengthened by taking into account cross-cultural evidence showing greater involvement of mothers than fathers in cooperative child care (Kramer, 2019). Studying and understanding sex differences in fearfulness can thus be seen as an important extension of the FAH.

R11. Does enhanced fear have direct adaptive benefits?

Regarding the issue concerning enhanced fear's adaptiveness, there exists evidence that enhanced fearfulness is associated with higher rates of reproductive success. Specifically, a large three-generational analysis (N = 2,657), previously not mentioned in the target article, shows that heightened levels of anxiety when assessed along a continuum is associated with greater reproductive success across three generations as indexed by a significantly greater number of children, grandchildren, and great-grandchildren (Jacobson & Roche, 2018). This raises the possibility that, rather than through or in addition to cooperative care as stipulated in the FAH, enhanced fearfulness may even have direct fitness benefits. This possibility and extension of the FAH requires explicit examination and close attention in future research.

R12. Conclusion

To conclude, the thoughtful commentaries have provided the platform to further refine, specify, test, and extend the FAH. We have seen that enhanced fear in humans possesses characteristics that speak for it being a developmental adaptation with deferred or better continued adaptive benefits. Evidence from cooperative breeders and from employing formal behavioral economic analysis support the notion that enhanced fearfulness may have emerged as a function of cooperative care. Whether or not other emotions signaling suffering, distress, and/or positive emotion have undergone similar changes over the course of human evolution remains to be seen. The extension of the FAH outlined herein has particularly benefitted from research evidence on neuroticism and its adaptive versus maladaptive effects as a function of cultural context. This line of evidence not only further stresses the importance of culture when studying enhanced fear in humans but also suggests that enhanced fear, which is thought to have evolved in small-scale interdependent group life, may continue to serve adaptive functions in concurrent large-scale interdependent societies. In turn, maladaptive effects of enhanced fear may indeed represent a mismatch resulting from independent societal structures in WEIRD cultures.

In summary, incorporating the suggestions from the numerous commentaries, this response provides an extended and refined picture of the FAH and its complexity. As with any novel theoretical framework many of the predictions generated by the FAH need to be explicitly tested. There is a strong need for cross-species and cross-cultural, longitudinal approaches to study the evolutionary and developmental functions of fear in context. More broadly, the time is ripe for a comprehensive evolutionary-developmental approach to human affective science.