Is there a human fear paradox? A more thorough use of comparative data to test the fearful ape hypothesis

Abstract

Grossmann's intriguing proposal can benefit from a more thorough integration of the primate literature, particularly on neophobia. Moreover, it directly leads to strong predictions in callitrichids, the only other cooperatively breeding primates beyond humans, which may indeed be met: Being more likely to signal distress than independently breeding monkeys, and responding to such signals with approach and affiliation.

Grossmann proposes that humans are particularly fearful apes, and more likely to react to signals of fearfulness in others not only with fight and flight reactions, but also with approaching distressed individuals which can result in providing comfort, support, or even help. The hypothesis that this may be linked to our reliance on allomaternal care fits well with the cooperative breeding model of human evolution (Burkart, Hrdy, & van Schaik, 2009; Hrdy, 2009; Hrdy & Burkart, 2020), and is carefully elaborated regarding the ontogenetic patterns in humans and underlying brain mechanisms.

Grossmann's comparative evidence is taken from Herrmann, Hare, Cissewski, and Tomasello (2011), who showed that 2.5-year-old human toddlers indeed have a more fearful temperament than adult orangutans, bonobos, and chimpanzees. However, because fearfulness (i.e., enhanced reactivity to, and inhibited approach of, novel situations, objects and people; target article, sect. 2, para. 1) is well known to change dramatically during ontogeny in primates, as well as with settings (wild vs. zoo), the conclusion that humans are more fearful than other apes requires further evidence. Immature primates are remarkably neophobic. For instance, Forss, Motes-Rodrigo, Hrubesch, and Tennie (2019) report higher neophobia in immature nonhuman apes than adults in captivity. Unfortunately, the younger age classes directly comparable to the 2.5-year-old human toddlers from Herrmann et al. (2011) were not part of this sample. Immatures are also more neophobic in the wild (e.g., orangutans: van Schaik et al., 2016; capuchin monkeys: Perry, 2020) and some, including the marmoset monkeys, who notably are cooperative breeders like humans, are so neophobic as young immatures that they may not even touch novel food unless they can first observe that adult group members are accepting it (Voelkl, Schrauf, & Huber, 2006). By adolescence, however, the pattern changes and individuals go through a period of low neophobia and high risk-taking (Taylor et al., 2022; van Schaik et al., 2016), which likewise resembles human developmental patterns. Without taking this systematic age-based trajectory into account and thus only comparing subjects at the same developmental stage, a meaningful comparison of fearfulness in humans and other primates is impossible. This comparison is further hampered by captivity effects which can remarkably decrease neophobia, for instance in orangutans who even as adults will avoid novel objects in the wild for months, but happily interact with the same novel objects in captivity immediately (Forss, Schuppli, Haiden, Zweifel, & van Schaik, 2015; van Schaik et al., 2016; see Forss, Motes-Rodrigo, Dongre, Mohr, & van de Waal [2021] for vervet monkeys). These setting effects strongly suggest that also for humans, fearfulness needs to be assessed cross-culturally, and not only based on Western, educated, industrialized, rich, and democratic (WEIRD) populations. The jury for whether humans, and in particular human infants, are indeed more fearful may thus still be out.

Grossmann's proposal directly leads to additional evolutionary predictions. First, the comparative evidence does not have to be restricted to comparing human and nonhuman apes. Through broad phylogenetic analyses, we can test in a wider range of species whether interspecific variation in fearfulness is indeed correlated with variation in allomaternal care. Phylogenetic tests can also be more targeted (MacLean, 2016) and focus on specific contrasts, in this case not only the contrast between humans and other apes, but also the one between callitrichid monkeys (i.e., marmosets and tamarins), which are the only cooperatively breeding primates beyond humans, and their closest, but independently breeding sister taxa, the cebids (capuchin monkeys and squirrel monkeys). Additional contrasts targeting the role of cooperative breeding can be found outside primates, for instance in voles (see below).

Second, evolutionary predictions can be made not only for fearfulness. Signaling fearfulness may well be only part of a larger package in cooperative breeders to more readily signal affective states to others (Burkart et al., 2022), because in tightly knit interdependent groups, this will facilitate behavioral coordination, and immatures are under selection pressure to attract helpers, for example, by signaling their neediness. A comparative analysis of relative neuropil fraction of the facial nucleus indeed suggests a link between allomaternal care and facial dexterity which can facilitate communication and coordination (Cerrito & DeCasien, 2021). Moreover and in line with this comparative evidence, when callitrichids ingest non-palatable food, they often produce gag faces that group members can use to learn to avoid this type of food (Snowdon & Boe, 2003). Perhaps most impressively, immature callitrichids engage in conspicuous babbling behavior, loudly announcing their neediness and vigor (Snowdon, 2001). These behaviors appear shared between humans and callitrichid monkeys, but have not been reported in other primates.

But do callitrichid monkeys also react with approach when group members signal their affective states? Some evidence suggests they do. When infants are babbling, adults are more likely to approach and interact with them, highlighting that one function of babbling is indeed the attraction of caregivers (Snowdon, 2001). When adults can observe how infants unsuccessfully struggle to open a specific apparatus to reach the food inside, they are more likely to share food that they have to extract from this apparatus than food that is freely handed over, suggesting some flexible adjustment to infant need (Martins & Burkart, 2013; Sehner & Burkart, 2022). Among adults, marmosets observing the fear-related signal “piloerection of the tip of the tail” in others showed higher rates of affiliative behaviors (de Boer, Overduin-de Vries, Louwerse, & Sterck, 2013). In a follow-up study, de Oliveira Terceiro, Willems, Araújo, and Burkart (2021) found that naïve marmosets who encountered a group member displaying this fear signal preferentially approached this distressed individual even when not aroused themselves. Intriguingly, a similar pattern was also found in voles and could directly be linked to cooperative breeding and oxytocin. Burkett et al. (2016) reported that within pairs of the cooperatively breeding prairie voles (Microtus ochrogaster), an unstressed partner increased its grooming of a stressed partner; an oxytocin receptor antagonist infused into the anterior cingulate cortex abolished this partner-directed response. In contrast, the closely related, independently breeding meadow voles (M. pennsylvanicus) did not show this consolation behavior at all.

In line with Grossmann's proposal, these results suggest that in cooperative breeders, internal affective states may be more readily signaled to group members, and perceiving others in distress may indeed elicit affiliative approach. However, to what extent the fearful ape hypothesis, or which elements of it, will stand the test of time has to await more systematic comparisons of directly comparable data, in the context of broader phylogenetic analyses or targeted comparisons (MacLean, 2016).