Our commentary addresses the discrepancies pointed out by Grossmann between his fearful ape hypothesis (FAH) and the human self-domestication hypothesis (HSDH). In brief, according to FAH, fearfulness itself was adaptive in the context of cooperative caregiving unique to human group life, resulting in increased caregiving by adults, and ultimately, in increased cooperation with others. On the other hand, according to HSDH, increased cooperation in humans resulted from (sexual) selection for less aggressive partners (e.g., Hare, Reference Hare2017; Hare & Woods, Reference Hare and Woods2020), rather than for fearfulness per se. Grossmann concludes that HSDH is not well-positioned to explain what he identifies as the phenomenon of “increased fearfulness” in humans, given that successful animal domestication leads to a reduction in fearfulness, rather than an increase (Zeder, Reference Zeder2012). Our contention is that certain aspects of FAH may prove incompatible with some features of the human phenotype, which are better accommodated under HSDH, while at the same time, much of FAH, including cautiousness, can actually be accommodated under HSDH. The evidence we use to support these claims includes research on language acquisition and language evolution, as well as neurobiological considerations.
First, FAH relies, to a great extent, on research suggesting that human infants exhibit increased fearful responses to strangers, particularly Herrmann, Hare, Cissewski, and Tomasello's (Reference Herrmann, Hare, Cissewski and Tomasello2011) study. Notably, however, these authors also found that human children behave like bonobos in this respect. But bonobos have been claimed to have gone through a self-domestication process (Hare, Wobber, & Wrangham, Reference Hare, Wobber and Wrangham2012). Also, in the experiment by Herrmann et al., “strangers” are people totally unknown to children. But humans do exhibit reduced fearfulness toward more individuals than, for example, chimps, as our kinship systems go far beyond parent–child ties (Gowlett, Reference Gowlett and Callan2018). Chimps contrast with bonobos in the fact that they have not been self-domesticated. In this sense, it is also noteworthy that hospitality codes, as found in present-day hunter–gatherers, which entail tolerance (i.e., reduced fearfulness) toward strangers, became generalized in our species during Upper Paleolithic (see Nikolsky & Benítez-Burraco, Reference Nikolsky and Benítez-Burraco2022, for discussion), in parallel with an increase in self-domestication features, as attested by the anthropological record (Cieri et al., Reference Cieri, Churchill, Franciscus, Tan and Hare2014). It thus seems to us that FAH is not well-positioned to accommodate some unique elements that characterize humans, which are better accommodated under HSDH, the argument which we will further develop below.
Focusing on language, in particular, research suggests that shyness can impact negatively on language acquisition. For instance, shyer children tend to perform worse on measures of word learning (Hilton, Twomey, & Westermann, Reference Hilton, Twomey and Westermann2019), seemingly because of a less-efficient formation and retention of novel word–object mappings (Hilton & Westermann, Reference Hilton and Westermann2017). Clinical conditions featuring abnormally high fearfulness and avoidance behaviors result in inadequate language acquisition, as is the case with Reactive attachment disorder (Raaska et al., Reference Raaska, Lapinleimu, Sinkkonen, Salmivalli, Matomäki, Mäkipää and Elovainio2012). Accordingly, it might be difficult to reconcile any trend toward increased fearfulness, as claimed by the FAH, with how human children acquire language. More specifically, at the age of 2.5 when children's fearfulness of novelty was compared to that of other primates in Herrmann et al.'s (Reference Herrmann, Hare, Cissewski and Tomasello2011) study, children have already experienced contact with a variety of cultural objects, some dangerous for them, and have already mastered a great deal of language, including being exposed to many warnings of dangers around them. This element in itself, unique to humans, may be contributing to the state of enhanced cautiousness/fearfulness in children, rather than selection for fearfulness itself.
With respect to language evolution, there is extensive research supporting the view that increased self-domestication in humans favoured the potentiation of many of the traits that make language more complex through a cultural mechanism, specifically, learning and shared intentionality (Thomas & Kirby, Reference Thomas and Kirby2018). In our own work, we have emphasized the role of management of aggression in language evolution, in particular reactive aggression, which is a crucial ingredient of HSDH. In this respect, we have proposed that self-domestication favoured the emergence of early grammars, especially suitable for verbal aggression (insult), which in turn contributed to a gradual replacement of reactive physical aggression with verbal/cognitive contest, so that language complexity and self-domestication processes were engaged in a mutually reinforcing feedback loop (Benítez-Burraco & Progovac, Reference Benítez-Burraco and Progovac2020; Progovac & Benítez-Burraco, Reference Progovac and Benítez-Burraco2019). In comparison, it is not clear how increased fearfulness in humans would have resulted in the evolution of sophisticated languages.
Furthermore, we find that other outcomes of HSDH can account for the increased protective behavior toward children by adults, which is at the core of FAH, without a need to invoke selection for fearfulness. One such outcome is prolonged childhood/juvenile period, that is, helplessness, which, in itself, can be the cause of more adult caring and attention, including enhanced co-parenting, as children would have demanded more attention during longer periods and from more people (Bogins, Reference Bogins1999). Moreover, HSDH is associated with a reduction in sexual dimorphism, which in humans manifests itself as males becoming more like females (Gleeson & Kushnick, Reference Gleeson and Kushnick2018). If females on average are more cautious, that is, less bold or reckless than males (e.g., McLean & Anderson, Reference McLean and Anderson2009), and if fearfulness responses are also inversely correlated to physical strength (e.g., Manson et al., Reference Manson, Chua, Rodriguez, Barlev, Durkee and Lukaszewski2022), then this feminization brought about by self-domestication could by itself have contributed to the human fearfulness (or cautiousness) phenotype, without a need to invoke any direct selection for fearfulness.
Finally, we wish also to note that most if not all the neurobiological mechanisms involved in fearful responses and invoked to provide support for FAH are indeed impacted by (self-)domestication, from the dopamine system to the oxytocin system. Accordingly, changes in the dopamine system have been extensively documented in domesticated animals (e.g., Komiyama et al., Reference Komiyama, Iwama, Osada, Nakamura, Kobayashi, Tateno and Gojobori2014; Sato et al., Reference Sato, Rafati, Ring, Younis, Feng, Blanco-Aguiar and Andersson2020). Likewise, in humans, oxytocin has been identified as a target of sexual selection contributing to a reduction in physically aggressive behavior (Hare, Reference Hare2017). In our opinion, this further reinforces our argument that HSDH can account for many aspects of the human distinctive phenotype, including fearfulness/cautiousness, weakening the case for FAH.
Our commentary addresses the discrepancies pointed out by Grossmann between his fearful ape hypothesis (FAH) and the human self-domestication hypothesis (HSDH). In brief, according to FAH, fearfulness itself was adaptive in the context of cooperative caregiving unique to human group life, resulting in increased caregiving by adults, and ultimately, in increased cooperation with others. On the other hand, according to HSDH, increased cooperation in humans resulted from (sexual) selection for less aggressive partners (e.g., Hare, Reference Hare2017; Hare & Woods, Reference Hare and Woods2020), rather than for fearfulness per se. Grossmann concludes that HSDH is not well-positioned to explain what he identifies as the phenomenon of “increased fearfulness” in humans, given that successful animal domestication leads to a reduction in fearfulness, rather than an increase (Zeder, Reference Zeder2012). Our contention is that certain aspects of FAH may prove incompatible with some features of the human phenotype, which are better accommodated under HSDH, while at the same time, much of FAH, including cautiousness, can actually be accommodated under HSDH. The evidence we use to support these claims includes research on language acquisition and language evolution, as well as neurobiological considerations.
First, FAH relies, to a great extent, on research suggesting that human infants exhibit increased fearful responses to strangers, particularly Herrmann, Hare, Cissewski, and Tomasello's (Reference Herrmann, Hare, Cissewski and Tomasello2011) study. Notably, however, these authors also found that human children behave like bonobos in this respect. But bonobos have been claimed to have gone through a self-domestication process (Hare, Wobber, & Wrangham, Reference Hare, Wobber and Wrangham2012). Also, in the experiment by Herrmann et al., “strangers” are people totally unknown to children. But humans do exhibit reduced fearfulness toward more individuals than, for example, chimps, as our kinship systems go far beyond parent–child ties (Gowlett, Reference Gowlett and Callan2018). Chimps contrast with bonobos in the fact that they have not been self-domesticated. In this sense, it is also noteworthy that hospitality codes, as found in present-day hunter–gatherers, which entail tolerance (i.e., reduced fearfulness) toward strangers, became generalized in our species during Upper Paleolithic (see Nikolsky & Benítez-Burraco, Reference Nikolsky and Benítez-Burraco2022, for discussion), in parallel with an increase in self-domestication features, as attested by the anthropological record (Cieri et al., Reference Cieri, Churchill, Franciscus, Tan and Hare2014). It thus seems to us that FAH is not well-positioned to accommodate some unique elements that characterize humans, which are better accommodated under HSDH, the argument which we will further develop below.
Focusing on language, in particular, research suggests that shyness can impact negatively on language acquisition. For instance, shyer children tend to perform worse on measures of word learning (Hilton, Twomey, & Westermann, Reference Hilton, Twomey and Westermann2019), seemingly because of a less-efficient formation and retention of novel word–object mappings (Hilton & Westermann, Reference Hilton and Westermann2017). Clinical conditions featuring abnormally high fearfulness and avoidance behaviors result in inadequate language acquisition, as is the case with Reactive attachment disorder (Raaska et al., Reference Raaska, Lapinleimu, Sinkkonen, Salmivalli, Matomäki, Mäkipää and Elovainio2012). Accordingly, it might be difficult to reconcile any trend toward increased fearfulness, as claimed by the FAH, with how human children acquire language. More specifically, at the age of 2.5 when children's fearfulness of novelty was compared to that of other primates in Herrmann et al.'s (Reference Herrmann, Hare, Cissewski and Tomasello2011) study, children have already experienced contact with a variety of cultural objects, some dangerous for them, and have already mastered a great deal of language, including being exposed to many warnings of dangers around them. This element in itself, unique to humans, may be contributing to the state of enhanced cautiousness/fearfulness in children, rather than selection for fearfulness itself.
With respect to language evolution, there is extensive research supporting the view that increased self-domestication in humans favoured the potentiation of many of the traits that make language more complex through a cultural mechanism, specifically, learning and shared intentionality (Thomas & Kirby, Reference Thomas and Kirby2018). In our own work, we have emphasized the role of management of aggression in language evolution, in particular reactive aggression, which is a crucial ingredient of HSDH. In this respect, we have proposed that self-domestication favoured the emergence of early grammars, especially suitable for verbal aggression (insult), which in turn contributed to a gradual replacement of reactive physical aggression with verbal/cognitive contest, so that language complexity and self-domestication processes were engaged in a mutually reinforcing feedback loop (Benítez-Burraco & Progovac, Reference Benítez-Burraco and Progovac2020; Progovac & Benítez-Burraco, Reference Progovac and Benítez-Burraco2019). In comparison, it is not clear how increased fearfulness in humans would have resulted in the evolution of sophisticated languages.
Furthermore, we find that other outcomes of HSDH can account for the increased protective behavior toward children by adults, which is at the core of FAH, without a need to invoke selection for fearfulness. One such outcome is prolonged childhood/juvenile period, that is, helplessness, which, in itself, can be the cause of more adult caring and attention, including enhanced co-parenting, as children would have demanded more attention during longer periods and from more people (Bogins, Reference Bogins1999). Moreover, HSDH is associated with a reduction in sexual dimorphism, which in humans manifests itself as males becoming more like females (Gleeson & Kushnick, Reference Gleeson and Kushnick2018). If females on average are more cautious, that is, less bold or reckless than males (e.g., McLean & Anderson, Reference McLean and Anderson2009), and if fearfulness responses are also inversely correlated to physical strength (e.g., Manson et al., Reference Manson, Chua, Rodriguez, Barlev, Durkee and Lukaszewski2022), then this feminization brought about by self-domestication could by itself have contributed to the human fearfulness (or cautiousness) phenotype, without a need to invoke any direct selection for fearfulness.
Finally, we wish also to note that most if not all the neurobiological mechanisms involved in fearful responses and invoked to provide support for FAH are indeed impacted by (self-)domestication, from the dopamine system to the oxytocin system. Accordingly, changes in the dopamine system have been extensively documented in domesticated animals (e.g., Komiyama et al., Reference Komiyama, Iwama, Osada, Nakamura, Kobayashi, Tateno and Gojobori2014; Sato et al., Reference Sato, Rafati, Ring, Younis, Feng, Blanco-Aguiar and Andersson2020). Likewise, in humans, oxytocin has been identified as a target of sexual selection contributing to a reduction in physically aggressive behavior (Hare, Reference Hare2017). In our opinion, this further reinforces our argument that HSDH can account for many aspects of the human distinctive phenotype, including fearfulness/cautiousness, weakening the case for FAH.
Financial support
This research was funded by the Spanish Ministry of Science and Innovation (grant PID2020-114516GB-I00 funded by MCIN/AEI/10.13039/501100011033 and by “ERDF A way of making Europe” to ABB).
Competing interest
None.