Even though our focus here is on verbal aggression and insult, the benefits of this kind of proto-grammar would have been much broader. This type of proto-grammar would have also provided a convenient strategy for naming animals [*tumbledung; swish-tail* (*bird*)*; stink-bug*], plants (*tumble-weed; catch-fly*), objects, and places, as well as for expressing basic commands (e.g., *Catch fly! Turn snake!*) and statements (e.g., *Bug stink; Monkey see*), not to mention enhanced ways of thinking, because it enables one to create new concepts by merging two pre-existing concepts. They could have also been used for affective purposes between partners or for calming and comforting one's children (e.g., *Baby sleep*), also contributing to alleviating stress and tensions. In addition, according to Progovac (2015, 2016), an important extension of this two-*word* proto-grammar would have been two-*clause* symmetric combinations involving binary formulae (typically AB AC), often expressing wisdoms and observations (e.g., *You seek, you find; You sow, you reap; Easy come, easy go; Come one, come all; First come, first serve(d); Like father, like son; Monkey see, monkey do*) 18. Such symmetric/ paratactic clause combinations, where clauses stand next to each other, would have foreshadowed modern-day subordination/ hypotaxis, where clauses get embedded one within another (e.g., *Those who seek will find*.).

In summary, the postulated approximations of proto-grammar provide continuity with modern syntax in two essential ways: (1) in their binary nature and (2) in their reliance on noun-like and verb-like elements to express predication. Even though it has become customary to reduce syntax to Chomsky's Merge, it is important to emphasize here that the combinatorics of syntax is just one aspect of it, determining how many elements can merge at a time (binarity), and how many times (recursion), and in which manner (flat or hierarchical). Human syntax/language is also undoubtedly designed to express predication, i.e., to express who does what (to whom), by using primarily verbs and nouns. Importantly, the way syntax became complex is not in just any old random way, but in a way that helps express, with more precision, who does what to whom (and when, and where, and how, and why)19. In both of these respects (binary combinatorics, and the focus on who does what to whom), verb-noun compounds are an excellent stepping stone into modern syntax. Importantly for our purposes, the proto-grammar strategy behind these compounds not only provides continuity with complex syntax but also provides a more graceful transition from animal cognition, and particularly, from animal behavior, i.e., their emotional vocalizations, to human behavior, *via* verbal aggression.

## NEUROBIOLOGY OF PHYSICAL AGGRESSION AND REACTIVE LANGUAGE

The limbic system (a group of brain structures supporting emotion, motivation, and long-term memory; see Rolls, 2015 for review), the striatal regions, and parts of the cortex, particularly, the frontal and the temporal cortices (Dolan et al., 2002; Yang et al., 2009; Boccardi et al., 2011) support aggressive behavior. Highly aggressive subjects exhibit enlargement and atypical activation of striatal regions (particularly, the caudate; Gatzke-Kopp et al., 2009; Ducharme et al., 2012; Yang et al., 2017). The striatum has been associated with the dopamine system that governs the regulation of motivated behavior (Mogenson et al., 1980), and which is critically involved in the expression of aggression in animals (Rodriguiz et al., 2004), but it is also crucially involved in language processing (e.g., Krishnan et al., 2016; Viñas-Guasch and Wu, 2017). Domesticated rats exhibit size reductions of the striatal area (Kruska and Schott, 1977), and the limbic system exhibits the highest differences between domesticated animals and their wild conspecifics (reviewed by Kruska, 1988).

Similar brain areas are involved in both reactive and proactive aggression; however, only the latter is associated with a thinner anterior cingulate cortex (Yang et al., 2017), a region involved

17One possibility would be n-ary (as opposed to binary) grammars, with certain designated slots with fixed ordering for tense, subject, verb, object, without grouping these categories into constituents and subconstituents, and without some of these categories exhibiting syntactic dominance over the others. One can also imagine languages that are not obsessed with who does what to whom. There seems to be nothing inevitable about evolving grammars with binary branching based on predication typically expressed by verbs and nouns. 18Such expressions are preserved much better in some languages than others (see Progovac, 2015, 2016 for discussion and references.) For a more theoretical discussion of the relevance of symmetry vs. asymmetry in human language and evolution, see also Citko (2011) and Progovac (2015).

19This is in fact where languages differ profoundly. There are several different strategies for discriminating between subjects/agents from objects/patients, including, but not limited to, ergative-absolutive grammars, split-ergative grammars, nominative-accusative grammars, serial verb grammars, and activestative grammars. These strategies are distinct enough to pose serious challenges for linguistic analysis and description. In this approach, the emergence of transitivity is seen as a later evolutionary development, discovering different solutions to the same problem posed by the limitations of the most rudimentary of grammars.

in the regulation of emotions and social behavior including conflict monitoring and empathy (Devinsky et al., 1995; Botvinick, 2007). The cingulate gyrus, which is part of cingulate cortex, plays a key role in language processing, contributing to speech production *via* its connections with Broca's area (Bernal et al., 2015). Compared to chimpanzees, bonobos (who are less aggressive) exhibit stronger links between the anterior cingulate gyrus and the amygdala, a pathway involved in the inhibition of aggression (Rilling et al., 2012). Likewise, Roth and Strüber (2009) found that reactive aggression is associated with smaller, less active frontal brain structures and amygdala hyperactivity, whereas proactive aggression correlates with reduced response of the amygdala and of cortical regions related to empathic and social behavior. Compared to chimps, bonobos also show an enlarged dorsal amygdala (Rilling et al., 2012). The amygdala is also implicated in the activation of the hypothalamic-pituitary-adrenal (HPA) axis through connections with the hypothalamus (Davis, 1997; Ledoux, 1998). The HPA axis is a major neuroendocrine system encompassing the hypothalamus, the pituitary gland, and the adrenal glands and regulating a great number of bodily functions. A reduced response of the HPA axis to stress has been observed in most domesticated animals (Kruska, 1988; Künzl and Sachser, 1999; Trut et al., 2009). With respect to aggression and cognitive functioning, reactive aggression in humans is associated with lower levels of goal-oriented inhibition and higher levels of flexibility, and proactive aggression is associated with higher levels of working memory (Hecht and Latzman, 2018) 20.

In comparison to other forms of language, the processing of swear words/profanity entails more involvement of the basal ganglia, limbic structures, thalamus, and the right hemisphere (e.g., Code, 2005, 2011; Bergen, 2016). The basal ganglia (i.e., the striatal regions) and the limbic system are also highly implicated in physical aggression. Disorders, which result in uncontrolled swearing/profanity, typically involve a basal-limbic connection dysfunction (discussed further in section "Disorders"). Basal-limbic structures are phylogenetically old, and the aspects of human communication associated with them are considered to be ancient, too (Van Lancker and Cummings, 1999; Bradshaw, 2001; Bergen, 2016), a potentially controversial claim (although see also Lieberman, 2000, 2009 on the ancient nature of basal ganglia). In this respect, Code (2005, p. 317) suggests that these forms of language might represent fossilized clues to the evolutionary origins of human communication. With brain damage affecting inhibitory processes, primitive behaviors (e.g., verbal automatisms) can emerge from primitive regions. In fact, damage to language centers in the brain can obliterate most language but leave swearing and expletives intact (see section "Disorders" for more details).

Differential impairment of reactive language versus intentional language implies that they employ distinct neural bases/pathways (Bergen, 2016, p. 87). The circuit that supports reactive language (including profanity) is evolutionarily far older, dominated by the limbic system, responsible for generating emotions and motor impulses, where the basal ganglia regulates and selectively suppresses such impulses (Bergen, 2016, p. 95). In disorders, such as Tourette's syndrome with coprolalia, there is a failure of this regulatory function of basal ganglia (see section "Disorders"). The relevance of basal ganglia for emotional speech processes, including such basic emotions as fear and disgust, is also established in the work of Paulmann et al. (2009) and Péron et al. (2013). Emotional vocalizations by other primates and mammals also seem to be supported by this kind of pathway, involving the limbic system and the basal ganglia (Robinson, 1967; see also Gruber and Grandjean, 2017), suggesting that emotional, profane language has some continuity with emotional vocalizations in other animals.

In natural use, expletives, especially those that are highly taboo, elicit strong physiological responses (including increased heart rate and sweating; Bergen, 2016). Such words are used for fundamental expression of deep emotion, including fear, pain, frustration, as well as for sex and violence (Code, 2005). The use of profanity is more common in men than in women (Jay, 1980, 1995; Van Lancker and Cummings, 1999, but see section "Aggression, Verbal Behavior, and Sexual Selection" for a possible challenge to this view), and this is true even in language disorders (Code, 1982, 2011; Jankovic and Rohaidy, 1987; Bergen, 2016). Considering that reactive physical aggression is more frequent in men than in women and that self-domestication was primarily subject to sexual selection (see section "Child Development"), this parallelism between physical and verbal aggression reinforces our hypothesis that verbal aggression acts as a proxy/replacement for reactive physical aggression.

Finally, expletive compounds can be highly humorous. One of the main functions of humor is to provide relief from stress and tension, *via* laughter and mirth (Berlyne, 1972; Meyer, 2000; Buijzen and Valkenburg, 2004). Humor serves as a natural stress antagonist in situations of trauma and stress, by decreasing cortisol levels (Vrticka et al., 2013; Bains et al., 2014). Typically, wild animals exhibit a more pronounced cortisol response to stress, compared to their domestic counterparts (Künzl and Sachser, 1999; Künzl et al., 2003; Zipser et al., 2014; Kaiser et al., 2015). As noted above, domestication is associated with a reduction in the function of the HPA axis (Naumenko and Belyaev, 1980; Kruska, 1988; Oskina, 1996; Künzl and Sachser, 1999; Trut et al., 2009). Humor engages a core network of cortical and subcortical structures, including the meso-cortico-limbic dopaminergic system and the amygdala (Vrticka et al., 2013). In addition, humor can often serve as a form of strong assertiveness bordering on aggression, especially in cases of teasing and insult (see section "Child Development"). We therefore argue that humor's dual functions (i.e., stress reduction function and verbal aggression), and its reliance on limbic structures supports our proposition that early forms of language provided relief from stress and tension, as well as a (verbal) alternative to reactive aggression, and thus reinforced the effects of self-domestication.

20In this respect, Wynn and Coolidge (2004) proposed that working memory may have been enhanced in modern humans, compared to Neanderthals, contributing to the capacity for innovation and experimentation. It is also pointed out by Balari et al. (2013) that enhanced working memory may have enabled recursive syntax. Finally, Benítez-Burraco and Kempe (2018) linked the enhancement of working memory to the emergence of languages with expanded vocabularies and more complex syntax, which are purportedly optimized for conveying complex meanings and know-hows to people not sharing a common ground or a common cultural knowledge.

#### Progovac and Benítez-Burraco Language Evolution and Self-Domestication Feedback Loop

## DISORDERS

Of particular relevance to our hypothesis are disorders that exhibit an imbalance between inhibition and disinhibition of verbal aggression. In this section, we consider certain disorders, which imply a dissociation between derogatory language and (more complex) referential language. Some of these conditions have a genetic basis, with candidate genes positively selected in our species.

#### Tourette's Syndrome and Coprophenomena

Tourette's syndrome (TS) is a hereditary tic disorder affecting the basal ganglia and the basolateral amygdala and hippocampal formation, circuitry involved in social decision making (Albin, 2018). It is sometimes accompanied by involuntary obscene speech and derogatory comments (coprolalia). Less commonly, TS patients may also exhibit copropraxia, which involves involuntarily making obscene gestures (Jankovic and Rohaidy, 1987; Singer, 1997; Freeman et al., 2009; Bergen, 2016). Although these coprophenomena and the TS syndrome more generally remain poorly understood, brain imaging, neurophysiological, and post-mortem findings implicate the cortical-striatalthalamocortical pathways in the etiopathology of TS (e.g., Mink, 2003; Singer, 2005; Singer and Minzer, 2005; Ganos et al., 2013). These pathways overlap with striatal-cortical networks implicated in physical aggression (as discussed above) and with the Broca's-basal ganglia network essential for speech and language processing (e.g., Lieberman, 2000, 2009, 2015; Ullman, 2006). TS also tends to include repetitive involuntary eye, facial, and head movements, as well as explosive outbursts (Budman et al., 2008; Kano et al., 2008; Chen et al., 2013; Ganos et al., 2014). Given that the major functional role of eye, face, and head movements is social signaling, Albin (2018) suggested that the coprophenomena associated with TS may be best understood as distortions of reactive, spontaneous social signals, thus possibly implicating the brain areas involved in TS in the evolution of early language. The use of foul reactive language at the early stages of human self-domestication may have strengthened these brain circuits, easing the way into more complex forms of language21.

Patients with TS experience an increase in their tics under stressful conditions, which are accompanied by a sense of discomfort that is relieved by tic performance (e.g., Cohen and Leckman, 1992; Leckman and Peterson, 1993; Evers and van de Wetering, 1994; Jankovic, 1997; Banaschewski et al., 2003; Kwak et al., 2003; Woods et al., 2005; Corbett et al., 2008; Albin, 2018). Importantly, a subset of TS patients exhibits heightened reactivity to stress of the HPA axis (Chappell et al., 1994). Likewise, children with TS show higher cortisol levels in response to stressors, which are indicative of an enhanced HPA responsivity to stress (Corbett et al., 2008). This is relevant to the self-domestication hypothesis of human evolution, because, as noted above, domestication entails reduced response of the HPA axis to stress. In this respect, TS can be seen as exhibiting attenuated features of selfdomestication, positing an intriguing parallelism with autism, also proposed to exhibit some features of a less-domesticated phenotype (Benítez-Burraco et al., 2016).

Rare mutations in selected genes have been identified in some TS patients. One of these genes is *SLITRK1*, which encodes an integral membrane protein involved in neurite outgrowth (Miranda et al., 2009). *SLITRK1* has an evolutionarily conserved expression pattern in projection neurons of the corticostriatal-thalamocortical circuits and cortical pyramidal neurons, contributing to the development of connections between the cortex, the striatum, and the thalamus (Stillman et al., 2009). Incidentally, there is also an ancestral mutation of *SLITRK1* (S330A) that has been related to TS (Ozomaro et al., 2013; Alexander et al., 2016). This SNP is highlighted by Theofanopoulou et al. (2017b) as a sort of window to the "underdomesticated" phenotypes found in other hominins. Overall, these genetic findings suggest that TS is more related to ancestral genomic variants than to derived changes in modern humans.

#### Aphasia and Speech Automatisms

Aphasias, resulting from brain damage, involve disinhibition of speech automatisms, such as counting, rhyming, prayer, but most commonly expletives and modal/auxiliary sentence stem structures (e.g., *I cannot*; *I try*; Code, 2005, 2011; Code et al., 2009). These two most frequent subtypes are also most relevant for evolutionary considerations. For the severest cases of non-fluent aphasia, these automatisms may be the only speech produced (Code, 2011, p. 139). Speaking specifically about derogatory language, Code (2011) points out that naturally occurring expletives emerge from ancient areas of the limbic system (see also Code, 1987; Leckman et al., 1991; Speedie et al., 1993; Van Lancker and Cummings, 1999). On the other hand, in pathology, expletives seem to emerge from disinhibited basal-limbic structures, which are normally under control from prefrontal networks, where basal ganglia damage appears to be essential for the production of an aphasic automatism (Brunner et al., 1982). With aphasias, we witness a loss of the complex compositional language, while the reactive, derogatory language is preserved. According to the so-called last in, first out principle (see e.g., Code, 2005; also Gibson, 2009), what is acquired last is the most shallow/fragile layer

21A reviewer points out that the mainstream view of the evolution of language has shifted away from biological evolution to cultural evolution. While it is true that trends in scientific research often bend in this and then that direction, especially with the questions having to do with nature vs. nurture, our proposal is that both biology and culture are directly involved and that the relevant challenge is to identify phenomena that can be shown to be so intertwined. Our paper presents an attempt in this direction, invoking a complex feedback loop between cultural innovations and biological selection. Importantly, our proposal is detailed enough to allow empirical testing. In this respect, we point out that genetic mutations affecting *FOXP2* and other genes increased synaptic plasticity and neuronal connectivity of the human brain (e.g., Hillert, 2014; Dediu, 2015), particularly in the frontal-striatal network, likely enabling human capacity for more complex language (see also Boeckx and Benítez-Burraco, 2014b). The finding that these networks have a biological foundation, supported by multiple genes, suggests that the emergence of complex syntax/language was not only a cultural invention but also a biological/genetic event.

that is the easiest to lose, and vice versa. In other words, the most recently evolved components of cognition, which certainly include compositional language, are the least robust, and most prone to damage and loss. If true, this provides further evidence of the role of reactive verbal aggression in language evolution.

This raises the question of whether the production of automatisms is associated with a higher degree of stress, and whether such production helps relieve stress. While there are many reports to the effect that aphasics in general experience a lot of stress and anxiety, even anger, specifically in trying to use language (see e.g., Goldstein, 1942; Luria, 1970; Laures-Gore et al., 2007; Cahana-Amitay et al., 2011; Laures-Gore, 2012), we have not come across any reports addressing specifically the production of automatisms in this respect. It would be of interest for future research to determine whether or not the incidence of specifically cursing and derogatory automatisms correlates with the experience of higher stress and anger (and thus higher cortisol levels), as well as whether the uttering of such automatisms helps relieve stress, in a way comparable to the production of tics in TS (section "Tourette's Syndrome and Coprophenomena").

In summary, our discussion of language/cognitive disorders in relation to self-domestication and language evolution supports the view that these disorders can inform on aspects of human domestication. They, moreover, involve patterns of inhibition and disinhibition that seem to be just poles on the continuum of cognitive modes, encompassing also the typically developing cognition. The discussion of disorders also highlights the existence of significant individual variability across all the dimensions relevant for language processing, which, moreover, seems to be genetically influenced. These considerations suggest that the evolution of language cannot be a simple, straightforward step, but rather a complex, multi-faceted, and multi-gene phenomenon, recruiting and coordinating a variety of cognitive systems and functions, with each new development potentially subject to genetic and/or cultural evolution.

## CHILD DEVELOPMENT

While ontogeny does not literally recapitulate phylogeny, there are usually points of comparison (e.g., Ridley, 1993). Here we report on some notable parallels between childhood development and our model of language evolution, with a focus on aggression, verbal (derogatory) behavior, and complex language. First, in the transition from infancy to childhood, when syntax emerges, there are developments in three other relevant areas: the ability to spontaneously coin compounds (Becker, 1994); the tendency to tease and insult, and thus, the onset of humor (McGhee, 1976; Apte, 1985); and the onset of agonistic verbal engagement or verbal dueling (Gossen, 1976; Wyatt, 1995, 1999). Second, as noted by these and other authors, teasing and insulting, as well as verbal dueling, tend to predominate in males, even at the time of their appearance in late infancy or early childhood, pointing to the relevance of sexual selection, and providing further supporting evidence for our proposal.

Regarding the emergence of syntax, children use simpler/ simplified syntactic structures early on, and combinations of just one verb and one noun (intransitive structures) predominate in early child grammars cross-linguistically. It is beyond the scope of this paper to get into different types of theories and controversies behind these omissions/simplifications, as the literature on this topic is vast and varied. Suffice it to note here that, at least on the surface, early children grammars often express only one noun argument per verb (see e.g., Zheng and Goldin-Meadow, 2002; Rakhlin and Progovac, 2017). Children's early utterances also include novel compounds of various kinds, including noun-noun and verb-noun combinations, for example, light-man (electrician); nose-beard (whiskers); and push-ball (a ball for pushing and bouncing; Becker, 1994). Compounding of this type seems to be a rather simple, straightforward strategy for children expressing new concepts.

There are also experiments targeting specifically compounds using verbs and nouns, establishing a clear difference in the order and ease of acquisition between flat verb-noun compounds and their hierarchical counterparts. In their experiment, Clark et al. (1986) prompted children to produce hierarchical -*er* compounds (e.g., *This is a cheese-grater*; *paper-ripper; ballbouncer*). At around three, instead of these targeted compounds, children consistently produced related verb-noun combinations (i.e., *This is a grate-cheese; rip-paper; bounce-ball*). Before reaching the target adult-like stage, many children also experienced another stage, where they produced compounds with misplaced affixes (i.e., *This is dry-hair-er/dry-er-hair* in lieu of *hair-dry-er*) or (*This is a fix-bik-er/fix-er-bike* in lieu of *bike-fix-er*).

Some conclusions from child language studies are important for our hypothesis. First, the stages and struggles in the acquisition of these compounds reinforce the view that -*er* compounds are related to VN compounds, as both rely on the common foundation provided by the flat (paratactic) verbnoun composition. Second, children start with the simpler structures, with the foundation, before they can scaffold to the hierarchical supra-structure, as emphasized by Clark et al. (1986). Third, VN compositions seem to be more primary and simpler than their hierarchical relatives.

With regard to the second area of development, namely, the onset of humor (and the tendency to tease and insult), laughter is one of the first social vocalizations in human infants, with an early onset at approximately 4 months of age (Ruch and Ekman, 2001). Responsive smiling generally develops even earlier, within the first 5 weeks (Kraemer et al., 1999). The earliest form of humor in young children, incongruity-based humor, relies on principles of discrepancy applied to actions, such as clowning and acting silly (McGhee, 1976). This kind of humor has also been reported for other primates (Patterson and Gordon, 1993). McGhee also reports a gender difference emerging at the age of 6–11 years old, but not before that. Specifically, he found that boys laughed more frequently than girls (the girls instead tended to smile), that they initiated humor more often, whether by non-verbal or verbal means, and that they also showed more hostility in their laughter and humor, including ridicule and insult. McGhee concluded that attempts to initiate humor or laughter in the presence of others can be seen as a form of strong assertiveness, especially in the case of hostile humor. This is directly relevant for our hypothesis of verbal aggression (partly) replacing physical aggression, which also predominates in males.

Finally, concerning the third area of development that we wish to highlight (the onset of agonistic verbal engagement or verbal dueling), it has been found that, cross-culturally, boys aged 3–11 engage in rough and tumble play, as well as verbal aggression, significantly more than do girls (Whiting and Edwards, 1973; Apte, 1985, p. 71; but see Björkqvist, 2018, for a possibly different view). Likewise, in many cultures, adolescent boys and men tend to engage in ritual insults (e.g., Apte, 1985, p. 70). Marsh (1978) provides convincing evidence from a variety of situations and cultures that ritual insult exchanges often serve instead of physical violence. This is consistent with our view that verbal aggression provides a different channel to the same goal, involving less risk of physical harm, thus contributing to better survival.

## AGGRESSION, VERBAL BEHAVIOR, AND SEXUAL SELECTION

Self-domestication in humans has been attributed to sexually selective forces, including selection against (physical) aggression, and in favor of pair-bonding beneficial for child rearing (Hare et al., 2012; Stanyon and Bigoni, 2014; Okanoya, 2015; Gleeson, 2018). Likewise, the emergence of early grammars, especially suited to verbal aggression (insult), has been attributed to sexual selection for creative cognitive abilities (Progovac and Locke, 2009; Progovac, 2015). Furthermore, the use of both verbal and physical aggression seems more prevalent in males, revealing a dimorphism characteristic of sexual selection. Starting early on in childhood, and continuing into adulthood, across a variety of cultures, both physical aggression and verbal aggression show significant gender differences in favor of males (Whiting and Edwards, 1973; Apte, 1985), including with language disorders (Code, 1982, 2011; Jankovic and Rohaidy, 1987; Bergen, 2016). This gender discrepancy in both types of aggression suggests that they cluster together and that they have a common underlying cause, consistent with our proposal that verbal aggression served to replace (reactive) physical aggression.

Franks and Rigby (2005) observed that men increase their creativity with language in the presence of both attractive women and male competitors. Creativity is highly correlated with intelligence (Miller, 2000), implicating creative language use in both mate attraction and intra-sexual competition in men. Furthermore, eloquent speakers tend to be granted the highest social status (Tallerman, 2013, p. 95), which in turn is correlated with greater reproductive success (Locke, 2009). Following Gleeson (2018, p. 8), we contend that any increase in language complexity may imply selection forces favoring such complexity (see Progovac, 2019), directly implicating sexual selection in the proliferation of more complex, creative language.

Furthermore, while sexual dimorphism has decreased in humans during the period of self-domestication, it has certainly not been eliminated. In his review article, Gleeson (2018) makes a case for the relevance of sexual selection in the evolution of humans, and he observes that female preferences must have been for moderately masculine males, rather than for extremely non-masculine (domesticated) ones, likely reflecting conflicting forces in sexual selection22. On the one hand, there are female preferences for male investment in pair-bonding, but on the other hand, there are also female preferences for physically stronger, more masculine males, which seem to be contextdependent, and to vary relative to environmental and other circumstances, related to survival (Trivers, 1972; Kruger, 2006; Archer, 2009; Quist et al., 2012). Boothroyd et al. (2017) found that moderately masculine fathers had more surviving offspring than those with both relatively low and relatively high masculinity, suggesting a centralized optimum of masculinity. It is also worth observing that some indicators of masculinity have infiltrated language, including low vocal pitch, as well as the initiation of humor, often analyzed as building and then resolving tension/incongruity, and considered by McGhee (1976) to reveal strong assertiveness, especially given that it involves a risk of failure. Both of these features seem to be subject to female preferences, possibly indirectly contributing to the preservation of (moderate) masculinity.

Furthermore, males exhibit displays of physical prowess to the formidability of male competitors, as well as characteristics such as facial hair and low vocal pitch, that increase perceptions of dominance (Hill et al., 2017).  Importantly, the specific derogatory compounds, which we argue are reflective of early language, are illustrative of both inter- and intra-sexual selection. Regarding male to male competition, these compounds often describe men in derogatory terms, but even when they seemingly describe women, such compounds are still typically used to derogate men, for a doubly insulting effect (Mihajlović, 1992; Progovac and Locke, 2009) 23. As pointed out by Marsh (1978), the most frequent type of insult among men even today has to do with emasculating one's opponent. Their usefulness in derogating existing rivals and placing prospective rivals on notice (aggressive rivalry), and in demonstrating verbal skills, humor, and quick wittedness simultaneously engages both sides of the sexual selection equation (Progovac and Locke, 2009). Such verbal items would have afforded a particularly useful, low-risk (non-violent) way to compete for status and sex. Of direct relevance for our proposal is Hill et al.'s (2017) conclusion that intra-sexual selection led to enhanced same-sex

22Gleeson and Kushnick (2018) provided evidence in favor of sexual selection *via* female preference for less aggressive males, leading to reduced sexual dimorphism, but only in the societies where females have relatively high social status, high enough to be able to choose. Furthermore, this effect is more robust where food resources are more secure. In the case of food scarcity, even when females can exert a choice, the tendency is toward selecting stronger (more aggressive) males.

23As discussed by Progovac and Locke (2009), even compositions that seem to describe females (*laj-kučka* "bark-bitch," loud, and obnoxious person; *plačipička* "cry-cunt," vulgar version of *crybaby*) are in fact typically used in reference to males.

intimidation, or formidability, instead of actual combat. In this respect, derogatory language can be viewed as the most innovative and creative means of achieving such "formidability," which straddles the boundary between physical and cognitive strength.

According to Card et al.'s (2008) meta-analytic review of 148 studies, there exist clear gender discrepancies favoring boys in direct (reactive) aggression, and only trivial differences favoring girls in indirect aggression (see also Björkqvist, 2018). While Björkqvist (2018) suggests that boys and girls are equally aggressive when it comes to verbal aggression, the evidence for this claim is not provided in this opinion piece, and it contradicts many reports which have found such a difference favoring males in verbal aggression, whether with typical populations [section "Neurobiology of Physical Aggression and Reactive Language"], or impaired populations (section "Disorders"). While reactive physical aggression in humans has seen a decline, as discussed at length in the previous sections, it still exists, and it (still) shows a prominent gender difference. According to, e.g., Archer (2009), the extent and the nature of gender differences in aggression can be better explained by sexual selection, given that they increase with the degree of associated risk, occur early in life, and peak in young adulthood.

There are also gender differences in initiating and perceiving humor. Adolescent and adult females exhibit greater emotional reactivity during humor perception than do males (Vrticka et al., 2013). This supports the fitness indicator hypothesis of humor, related to female preferences. Unlike with humor appreciation, where striatal activation follows or coincides with activation of temporal regions, with humor creation (which exhibits a male bias), the peak striatal activation precedes the peak of temporal activation (Amir and Biederman, 2016). The striatum (basal ganglia) is also implicated in both physical and verbal aggression. Both types of gender differences, those associated with the initiation of humor, and those associated with the appreciation of humor, directly implicate sexual selection in the feedback loop that we propose was critical to the evolution of language and self-domestication.

Three hormones were likely targets for sexual selection with respect to a reduction in physically aggressive behavior: serotonin, testosterone, and oxytocin (Kuepper et al., 2010; Montoya et al., 2012). Low testosterone has been related to male prosociality and parental care (Burnham, 2007). Exogenous serotonin increases harm avoidance and cooperative behavior (Wood et al., 2006; Crockett et al., 2010) and increases in brain levels of serotonin correlate with reduced emotional reactivity and aggression in experimental animal populations selected for friendliness toward humans (Plyusnina et al., 1991; Agnvall et al., 2015). In domesticated animals and bonobos, an increase in serotonin and a reduction in testosterone are associated with facial feminization and reduced cranial capacity (Hare et al., 2012). Although archaic human species had similar sized brains compared to *H. sapiens*, their faces seem to be more masculinized than the oldest modern humans (Churchill, 2014; Hare, 2017). It is also relevant that changes in the brain seem to have predated changes in our face morphology, possibly because of our mild self-domestication at that initial stage. Finally, oxytocin has been claimed to modulate the multimodality that characterizes higher-order linguistic abilities, including the vocal-auditory system, the attentional-memory system, and the socio-interactive system (Theofanopoulou, 2016) because of its regulatory role on the development of specific neural pathways (e.g., Theofanopoulou et al., 2017a on vocal learning).

We thus conclude that sexual selection of self-domestication interacts with sexual selection for verbal aggression, possibly in conflicting ways, which may account for the complicated picture of the expressions of masculinity described above: while the former favored less physically aggressive males, the latter favored verbal behavior/aggression, which, at early stages of language emergence, brought about novelty, creativity, and verbal humor. The net result would converge on selecting those who are not just less aggressive, but who are also better able to use verbal aggression to replace physical aggression, as they would be selected by both processes. This contrasts with the conclusion reached by Stanyon and Bigoni (2014), who argue that it was reduced male competition and increased female choice that favored cognitive evolution. While this is certainly one part of the story, our proposal implies that the continued male competition in the realm of verbal aggression/verbal behavior also contributed substantially to the evolution of cognitive abilities, at least at this early but crucial step in the emergence of language and evolution of self-domestication.

## DISCUSSION AND CONCLUSIONS

Here we proposed that that self-domestication favored the emergence of a phenotype prone to replace reactive physical aggression with verbal aggression. The (partial) transition to verbal aggression and verbal behavior more generally then favored self-domestication, *via* a mutually reinforcing feedback loop, since verbal behavior affords less violence, better survival, and more opportunities for social interactions, ultimately paving the way for the evolution of more complex forms of language. We further proposed that looking at the (gradual) emergence of verbal means of aggression (approximated by protogrammatical compounds) helps illuminate the initial steps of the language evolution/self-domestication feedback loop. The novelty of our approach lies in (1) giving an active role to early forms of language in interacting with self-domestication processes; (2) providing specific details and functions of this early stage of grammar (including creative uses of insult and humor); (3) supplying neurobiological, ontogenetic, and clinical evidence of a link between (reactive) aggression and (reactive) verbal behavior; (4) identifying proxies of the earlier stages in evolution among cognitive disorders; and (5) identifying specific points of contact and mutual reinforcement between these two processes (self-domestication and early language evolution), including reduction in physical aggression and stress/ tension, as well as sexual selection.

One immediate advantage of our proposal is that, as noted, it helps solve the paradox of the two aggression types, reactive and proactive, which the Self-Domestication Hypothesis (SDH) on its own cannot solve. If SDH simply postulates that humans were selected for their friendliness and lack of aggression,

then this discrepancy between the two aggression types is unexpected. But the problem finds a direct solution in correlating early self-domestication processes with the emergence of simple forms of early language/grammar, as per our proposal in this paper, but also in correlating later stages of self-domestication with more complex forms of language, as discussed by Benítez-Burraco and Kempe (2018) and Kissel and Kim (2019). Given that the postulated proto-grammar is particularly suitable for expressing crude and often obscene insults, representing essentially reactive language, this kind of language would have been most useful in countering/replacing reactive aggression, but as such, it would not have affected any existing or emerging proactive aggression.

Several classes of predictions arise from our proposal, yielding specific hypotheses. We single out three such classes: (1) the history of aggression and the fossil record; (2) linguistic proxies (fossils) of the second (proto-grammar) stage in (language) evolution, and their acquisition and processing implications; and (3) Disorders and (verbal) aggression. For each of these classes, we identify some specific hypotheses that are subject to testing and falsification (see also **Figure 2**).

1. The history of aggression and the fossil record.

hypothesis, as collaborative inter-group conflicts became widespread during the Neolithic (Zeng et al., 2018). But further evidence can certainly be sought to better support or falsify this hypothesis. For example, evidence of accelerated proactive aggression in the first or second stages postulated above would falsify our hypothesis and would at least necessitate a reconsideration/revision of the timeline.

	- i. Our first prediction is that the flatter evolutionary proxies will be acquired earlier by children, and with less effort, than their more hierarchical counterparts. As mentioned in Section "Child Development," some experiments with children already established that what we refer to here as "fossil" compounds are acquired earlier, and with more ease, than their hierarchical counterparts (Clark et al., 1986). Such experiments can be replicated with additional language proxies and conducted using additional languages, or even by using artificial grammars.
	- ii. Similar expectations hold for the processing of human language by adults, where the prediction is that the processing of flatter, fossil structures, such as small clauses and compounds, in contrast to their syntactically more layered counterparts, will rely less on the more recently enhanced brain networks. Progovac et al. (2018a,b) report some preliminary results of fMRI experiments along these lines that establish clear processing differences between the two types of structures, but more studies are needed to confirm or disconfirm these results, especially crosslinguistic studies, including a variety of languages. This line of research can help determine what kind of brains are needed for the (effortless) processing of early language vs. modern languages and would potentially tie into the

considerations of the evolution of the human brain and the human skull, as discussed in section "Introduction."

	- i. The anxiolytic (stress and anxiety-relieving) properties of reactive verbal aggression are hypothesized to have contributed to the language emergence/self-domestication feedback loop. While there are proposals in the literature to the effect that tics in TS are anxiolytic (section "Tourette's Syndrome and Coprophenomena"), this should be subjected to further experimental testing. We further predict that tics accompanied by coprolalia (uncontrollable profanity) will provide better stress relief than those without it.
	- ii. We make a similar prediction when it comes to automatisms in aphasia. The production of these automatisms, specifically expletives, seems to be associated with a higher degree of stress, and experiments can be designed to gauge whether such production is anxiolytic.

The truth is that very little is known about swearing and derogatory language, including its processing and genetic basis, whether in typical populations, or in disorders, most probably because this kind of language is often taboo, and typically avoided even in scientific research24. However, once tapped into, these phenomena, including the neuroscience and genetics of the functions and dysfunctions of swearing/

#### REFERENCES

derogatory language, will provide an especially fertile ground for formulating and testing a variety of hypotheses about language evolution and self-domestication, and human evolution more generally.

#### DATA AVAILABILITY STATEMENT

The datasets generated for this study are available on request to the corresponding author.

#### AUTHOR CONTRIBUTIONS

LP and AB-B conceived and wrote the manuscript.

#### FUNDING

This research was funded by the Spanish Ministry of Economy and Competitiveness [grant FFI2016-78034-C2-2-P (AEI/FEDER, UE) to AB-B].

#### ACKNOWLEDGMENTS

We are grateful to the reviewers of this article, who read it carefully, and provided detailed, useful comments. We are also very grateful to the editor, Danielle Sulikowski, for a most thorough editing job. Our paper benefited greatly from their input.

24As pointed out by Freeman et al. (2009) and others, the research on coprophenomena (coprolalia and copropraxia) is very limited and leaves large gaps and many unanswered questions. The same is true of the studies of insult, swearing, and profanity more generally (e.g., Mohr, 2013; Bergen, 2016).

Kayne, R. (1984). *Connectedness and binary branching*. Dordrecht: Foris.

Kissel, M., and Kim, N. C. (2019). The emergence of human warfare: current perspectives. *Am. J. Phys. Anthropol.* 168(Suppl. 67), 141–163. doi: 10.1002/ ajpa.23751

Kitagawa, Y. (1985). Small but clausal. *Chic. Linguist. Soc.* 21, 210–220.

Lieberman, P. (2000). *Human language and our reptilian brain: The subcortical bases of speech, syntax, and thought*. Cambridge, MA: Harvard University Press.

Marsh, P. (1978). *Aggro: The illusion of violence*. London: Dent.

McBrearty, S. (2007). "Down with the revolution" in *Rethinking the human revolution: New behavioral and biological perspectives on the origin and*  *dispersal of modern humans*. eds. P. Mellars, K. Boyle, O. Bar-Yosef, and C. Stringer (Cambridge, UK: McDonald Institute for Archeological Research, University of Cambridge), 133–151.

**Conflict of Interest:** The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

*Copyright © 2019 Progovac and Benítez-Burraco. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.*

 The trait is clearly biological: it is widespread and has a strong additive genetic basis, but how SSSA has evolved remains a subject of debate.  How then did the trait evolve, and how is it maintained in populations? Here we develop a novel argument for the evolution of SSSA that focuses on the likely adaptive social consequences of SSSA. We argue that same sex sexual attraction evolved as just one of a suite of traits responding to strong selection for ease of social integration or prosocial behavior. A strong driver of recent human behavioral evolution has been selection for reduced reactive aggression, increased social affiliation, social communication, and ease of social integration. In many prosocial mammals sex has adopted new social functions in contexts of social bonding, social reinforcement, appeasement, and play. We argue that for humans the social functions and benefits of sex apply to same-sex sexual behavior as well as heterosexual behavior. As a consequence we propose a degree of SSSA, was selected for in recent human evolution for its non-conceptive social benefits.

 While estimates of the population prevalence and distribution of SSSA vary (Bailey et al., 2016) contemporary studies support Kinsey et al.'s (1948, 1953) conclusion that in human populations there is continuous variation in the expression of homosexuality.

#### Edited by:

Antonio Benítez-Burraco, University of Seville, Spain

#### Reviewed by:

Jaroslava Varella Valentova, University of São Paulo, Brazil Rafael Lucas Rodriguez, University of Wisconsin–Milwaukee, United States

> \*Correspondence: Andrew B. Barron<EMAIL_ADDRESS>
#### Specialty section:

This article was submitted to Evolutionary Psychology, a section of the journal Frontiers in Psychology

Received: 11 July 2019 Accepted: 12 December 2019 Published: 16 January 2020

#### Citation:

Barron AB and Hare B (2020) Prosociality and a Sociosexual Hypothesis for the Evolution of Same-Sex Attraction in Humans. Front.  SSSA persists both within and across cultures (Witham and Mathy, 1985; Crompton, 2006) and within families, since sexual orientation has high heritability (Pillard and Bailey, 1998; Mustanski et al., 2005; Santtila et al., 2008; Bailey et al., 2016). Evidence from human twin studies and genome-wide genetic association studies suggest that about one third of the variation in sexual orientation can be attributed to additive genetic factors (Santtila et al., 2008; Bailey et al., 2016; Ganna et al., 2019).  There is expected to be strong selection against genetic factors that contribute to SSSA: how, therefore, can heritable homosexual attractions persist in a population (Kirkpatrick, 2000; Gavrilets and Rice, 2006; Bártová and Valentová, 2012; Rice et al., 2012; Jeffery, 2015)?

Various explanations to this puzzle have been proposed. The prevalence of SSSA is certainly too high for the trait to be maintained by recurrent random mutation (Moran, 1972). Models have consequently been proposed to explain how SSSA could be maintained in a population as a stable genetic polymorphism, but presently there is scant or no evidence to support these theories.

The theory of sexually antagonistic selection proposes that genetic factors contributing to SSSA in one sex could persist in populations if they conferred a strong selective advantage when expressed in the other sex, and various models of this kind have been posed to explain human SSSA (Gavrilets and Rice, 2006; Camperio-Ciani et al., 2008; Rice et al., 2012). Camperio-Ciani et al. (2008) explored whether the female relatives of homosexual males had more offspring than female relatives of heterosexual males, which could be indirect evidence for antagonistic sexual selection.  No study has yet explored whether this theory might apply to human females.

An alternative hypothesis proposes that SSSA and homosexual behavior could be maintained in a population if genetic factors contributing to these traits had pleiotropic effects that conferred a reproductive advantage. Zietsch et al. (2008) explored a version of this hypothesis and reported that psychologically masculine females and psychologically feminine men typically identified as non-heterosexual, but if did self identify as heterosexual they also self-reported a greater number of sexual partners than average for heterosexuals. We note that number of sexual partners is a long way from a measure of reproductive success or fitness. We also note that a critical test of this hypothesis was whether heterosexuals with a non-heterosexual identical twin have more sexual partners than members of heterosexual identical twin pairs. Here, there was a trend in the hypothesized direction but no statistically significant difference in number of sexual partners (Zietsch et al., 2008). Zietsch et al.'s (2008) study is certainly intriguing. The data they present are compatible with a relationship between SSSA, homosexual behavior and increased socio-sexuality – a point we develop later.

Kin-selection theories propose genes promoting SSSA could persist in a population if people expressing SSSA enhanced the reproduction of relatives (Bailey and Zuk, 2009). It is assumed the indirect fitness benefit of more relatives would compensate for the presumed fitness costs associated with SSSA and same-sex sexual behavior. Invoking kin-selection theory to explain human SSSA seems a little odd. The many examples of social and reproductive traits in animals that have evolved as a consequence of kin selection emphasize the evolution of non-reproductives, not same-sex sexual behavior (Kirkpatrick, 2000). In human societies there is very little evidence homosexual people increase the reproductive output of relatives (Bobrow and Bailey, 2001; Rahman and Hull, 2005; Vasey and VanderLaan, 2012; Abild et al., 2014; Prum, 2017) offering weak empirical support to kin selection theories for SSSA. But several studies by Vasey and others have emphasized the avuncularity (defined as altruistic uncle-like behavior) and generosity of transgender males expressing SSSA (Vasey et al., 2007; Vasey and VanderLaan, 2012, 2015; Abild et al., 2014) perhaps indicating a relationship between SSSA and affiliative behavior.

Here we propose a sociosexual hypothesis for the evolution of SSSA that explores possible adaptive social functions of samesex directed attractions and behavior. Benefits of SSSA and same sex sexual behavior for the development and maintenance of same sex social bonds and group affiliation have been proposed previously, most notably by Kirkpatrick (2000) and later by Bártová and Valentová (2012). But here we link the evolution of human SSSA to the suite of traits that evolved as a consequence of selection for ease of social integration (prosocial behavior), within-group tolerance and social affiliation. This has been described as an evolutionary process of human selfdomestication (Eisenberg et al., 1983; Clay and Zuberbühler, 2011; Gleeson, 2016; Hare, 2017; Theofanopoulou et al., 2017; Niego and Benítez-Burraco, 2019; Wrangham, 2019).

Assessing SSSA in non-human animals is not easy, but what is clear is that homosexual behavior is not a human innovation. It is widespread in primates (Sommer and Vasey, 2006) and other animals (Bagemihl, 1999; Bailey and Zuk, 2009), and is certainly ancestral to hominids. Analyses of the contexts of occurrence of homosexual sexual behavior in primate societies suggest the behavior has various diverse functions. These include appeasement, pacification, reinforcement of social dominance structures, juvenile play, social tolerance, stress reduction, and barter (Sommer and Vasey, 2006; Clay and de Waal, 2015).  It appears there has been an expansion of the social functions of sexual interactions (both homosexual and heterosexual) as more

complex societies evolved in primates (Werner, 2006). As a consequence, sexual behavior in primates has been subject to selection for adaptive social functions as well as the obvious reproductive functions.

Social evolutionary processes have been a major driver of recent human cognition and behavior (Eisenberg et al., 1983; Dos Santos and West, 2005); particularly selection for increased intragroup tolerance and reduced intra-group aggression (Bowles and Gintis, 2013; Hare, 2017). Prosocial individuals would have more readily accessed the fitness benefits of cooperative group living (Hare, 2017), and would have gained both greater reproductive success and social mobility (Bowles and Gintis, 2013). Enhanced tolerance also would allow for smoother integration of juveniles that moved from their natal group to a new group – bringing new ideas and technology with them. Selection for prosociality is thought to have driven the recent evolution of bonobos from their chimp-like ancestor, and proto-dogs from their wolf-like ancestor also (Hare, 2017).

In humans, dogs, and bonobos, a common suite of traits has evolved as a consequence of selection for prosociality. These are juvenilization of facial features, extended cognitive developmental periods, reduced social threat responses, reduced aggression, reduced aggressive reactivity, cooperative play behavior, and increased cooperative-communicative capacity and engagement (Hare, 2017; Theofanopoulou et al., 2017; Wrangham, 2019). This set of traits is very similar to those that have arisen from artificial selection on species for reduced aggression and fear of humans in order to domesticate them (Belyaev et al., 1985; Hare, 2017). Consequently, recent human evolution has been described as a process of selfdomestication arising from natural selection for prosocial behavior (Gleeson, 2016; Hare, 2017; Niego and Benítez-Burraco, 2019; Wrangham, 2019).

Across both domesticated species and self-domesticated species it is common to see an increase in expression of same-sex sexual behavior.   While domestication of livestock has not always increased rates of homosexual behavior, there are several well studied examples where domestication has yielded high levels of same-sex sexual behavior among adults (Dagg, 1984; Perkins and Roselli, 2007).

The bonobo has experienced a parallel process to humans of prosocial evolution from a chimp-like ancestor (Hare, 2017; Tan et al., 2017). Like humans, bonobos show a suite of features associated with self-domestication (Hare, 2017). Bonobos exhibit higher levels than chimpanzees of same-sex sexual behavior in contexts of adult play and social affiliation also (Clay and Zuberbühler, 2011; Dixon, 2011; Woods and Hare, 2011; Bailey et al., 2016; Hare and Yamamoto, 2017).

  Sex is a strong reinforcer of pair bonds in all social mammals studied (Young and Wang, 2004). Sexual behavior in social contexts functions as a reinforcer of social bonds also (Kirkpatrick, 2000). Same-sex social bonds are likely to be as important as heterosexual social bonds for any individual operating within a social group (Kirkpatrick, 2000). A degree of SSSA could therefore reasonably confer a selective advantage, by facilitating engagement in sociosexual behavior with the associated benefits of social reinforcement, affiliation, play, appeasement, and conflict resolution (Kirkpatrick, 2000; Bártová and Valentová, 2012). Selective benefits for SSSA could be increased ease of social bonding and reduced intragroup conflict through a willingness to engage in or initiate homosexual sexual play. Human ethnographic evidence points to an adaptive benefit for SSSA in alliance formation and maintenance (Kirkpatrick, 2000; Muscarella et al., 2005).

Mechanistic analyses indicate links between increased prosociality and SSSA. Raghanti et al. (2018) have argued that the neurochemical profile of the human striatum is unique among primates with elevated dopamine, serotonin, and neuropeptide Y signaling. They argue this feature evolved early in hominid evolution and increased sensitivity to social cues to promote empathy and affiliative behavior (Raghanti et al., 2018). Self domestication in both dogs and humans is believed to have caused evolutionary changes in serotonin, oxytocin and androgen systems that regulate affiliative, threat, and aggressive behavior (Hare, 2017), and are involved in chimpanzee social affiliation (Samuni et al., 2017).  In domesticated sheep changes in these neurochemical systems have been considered causal of increased levels of homosexual behavior (Perkins and Roselli, 2007). Taken together, these studies suggest an overlap between the neurochemical systems involved in affiliation and prosocial behavior and those involved in an increased incidence of same-sex sexual behavior in animals.

Prosociality, increased in-group tolerance and increased social affiliation: these are extremely complex traits involving widespread changes in behavior, anatomy, and neurophysiology (Hare, 2017; Theofanopoulou et al., 2017; Raghanti et al., 2018). Genetic changes underlying the evolution of such traits are likely to be complex and highly polygenic. Presently not much is known about the genetic basis of human SSSA, but as we learn more about it, it is clear human SSSA is also highly polygenic and a complex multicomponent trait (Mustanski et al., 2005; Prum, 2017; Sanders et al., 2017; Ganna et al., 2019; Swift-Gallant et al., 2019). The high heritability of human SSSA is caused by a large number of genes each

with individually small effect. These genes likely contribute to different aspects of sexuality which can assort independently (Mustanski et al., 2005; Sanders et al., 2017; Ganna et al., 2019). Genetic models for the evolution of human SSSA should therefore reflect this complexity and be polygenic and multicomponent, rather than positing individual genes of large effect, as has occurred previously (Gavrilets and Rice, 2006; Rice et al., 2012).

A polygenic and additive genetic model of SSSA is compatible with the nature and distribution of SSSA in human populations, which features continuous variation in the degree of SSSA from a majority reporting exclusively heterosexual attractions to a small minority reporting exclusively homosexual attractions (Bailey et al., 2016).  We propose this pattern of variation could have arisen from selection for prosociality increasing the frequency of alleles in a population across multiple loci that contribute to prosocial behavior. This would include alleles contributing to SSSA because of the benefits of sociosexual same-sex behavior for same-sex social bonding and affiliation. If a trait is highly polymorphic and polygenic [as sexual orientation seems to be (Sanders et al., 2017; Ganna et al., 2019)] the random recombination of genes in sexual reproduction would result in a spectrum of heritable variation for strength of SSSA in a population (Prum, 2017).

Given this argument one might ask why SSSA is not more common in human populations. Indeed, Kirkpatrick (2000) wondered that bisexuality might be an adaptive optimum since it would allow for sociosexual affiliative behavior with members of both sexes. Kirkpatrick (2000) proposes that any reproductive disadvantage from a low level of same-sex sexual behavior could be minor or negligible, irrespective of the degree of SSSA associated with the behavior.

To this point we note simply that while individuals reporting exclusive SSSA are rare in most contemporary human populations, SSSA is not. While specific measures vary all studies recognize that males and females reporting some degree of SSSA are relatively common, and not rare (Kinsey et al., 1948, 1953; Kirkpatrick, 2000; Mustanski et al., 2002; Bailey et al., 2016). Bisexuality is more common than homosexuality, but the nature of variation in SSSA is often not well appreciated since experimentalists are prone to force a binary dichotomy across what is in reality continuous and multivariate variation in sexuality (Jordan-Young, 2010). There may also be cultural reasons why the degree of SSSA in populations may go under-reported.

We emphasize that our hypothesis is not that homosexual people are domesticated, or even more prosocial than the population average. Rather, we recognize that self-domestication has been an important process in the recent evolution of our species as a whole. SSSA has increased in frequency in humans as a consequence of the self-domestication syndrome experienced by our species. If correct, this sociosexual hypothesis comprehends the phenomenon of human SSSA as part of broader adaptive prosocial changes in recent human cognitive and social evolution (Burkart et al., 2009, 2014; Hare, 2017).

Two other authors have remarked on a link between SSSA and selection for prosociality: Prum (2017) and Wrangham (2019). Prum (2017) argues that for humans female dispersal was the ancestral condition, with females rather than males leaving their natal group. He proposes that female SSSA could evolve as part of selection for female prosociality to aid female introgression into a new social group and strengthen female-female social bonds (Prum, 2017, p. 508).  Females may have preferred males that show a degree of SSSA since this male trait would lessen the intensity and investment of males in sexual and social control of females, and would subsequently have fostered the evolution of prosocial males and more cooperative male–male and female– male relationships (Prum, 2017, p. 509).

Wrangham (2019) has also recognized an association between prosociality and homosexuality, but Wrangham proposes a very different hypothesis for why this association might be so. Wrangham (2019, p. 189) suggests human homosexuality is a maladaptive by product of selection against reactive aggression in humans. Wrangham (2019) argues that selection for reduced reactive aggression reduced prenatal testosterone levels in males, which resulted in a maladaptive expression of homosexuality in a minority of males.

Models of human evolution are naturally hard, if not impossible, to prove or disprove, but here we note that Wrangham's explanation for an association between homosexuality and prosociality does not, and cannot, explain homosexuality in women. By contrast, prosocial benefits of SSSA would be expected to apply to both female–female social relationships and male–male social relationships (Kirkpatrick, 2000). Prum's (2017) evolutionary argument is interesting in many ways, not least of which is because it proposes different (but interacting) selective pressures for the evolution of male and female SSSA in humans. Here we have argued a link between prosocial evolution and SSSA. Prum (2017) recognizes this selective force for females, but considers female mate choice the primary driver of human male SSSA, with prosociality in human males an outcome of female mate choice. This hypothesized evolutionary scenario is perhaps more complex than ours, but that does not mean it is less likely. If non-prosocial species could be found in which female mate choice had lead to the evolution of male SSSA this would lend strong support to Prum's (2017) model for social evolution.

Wrangham's reasoning and evidence draw on the endocrine hypothesis for human homosexuality, which has been strongly refuted (Jordan-Young, 2010). There are many variants of the endocrine hypothesis, but they all propose that SSSA is caused by some malfunction or gendered misexpression of endocrine systems considered responsible for establishing gender-typical behavioral differences between heterosexual males and heterosexual females (Mustanski et al., 2002; Balthazart, 2011; Rice et al., 2012; Bailey et al., 2016). Hypotheses vary as to when or how in development a change in endocrine systems

could result in SSSA. Arguments in support of the endocrine hypothesis come from a range of experimental manipulations of mammals, including primates, which demonstrate a role for androgens in the organization and development of male and female typical sexual and social behavior, and also show that severe manipulations of endocrine systems in early development can result in males showing femaletypical sexual behavior and vice-versa (Balthazart, 2011; Poiani, 2011).

The endocrine hypothesis does not, however, fit well to features of human SSSA (Jordan-Young, 2010). The example of female congenital adrenal hyperplasia (CAH) is often cited as evidence supporting an endocrine basis of human SSSA (Balthazart, 2011). This disorder causes prenatal hypertrophy of the adrenal gland, and consequently the developing fetus is exposed to higher than normal levels of testosterone. Females with CAH report a higher incidence of adult homosexual orientation than that of the population as a whole, but most females with CAH report exclusively heterosexual attraction (Meyer-Bahlburg et al., 2008; Jordan-Young, 2010). This would suggest that for women there is not a simple relationship between elevated prenatal testosterone and SSSA. Further, in both animal studies and the human cases of CAH pre- or perinatal endocrine manipulations have consequences for the development of anatomical secondary sexual characteristics and genital morphology. Female rhesus monkeys given testosterone postnatally develop an enlarged clitoris (Pfaff, 1999; Dixson, 2013) and some females with CAH also develop partially masculinized genitalia (Bailey et al., 2016). There is no evidence that homosexual people (male or female) have intersex genital development (Jordan-Young, 2010; Bailey et al., 2016) suggesting it is unlikely an endocrine imbalance pre or perinatally is causal of human SSSA.

Rice and Gavrilets (Rice et al., 2012) argued that a misexpressed epigenetic modifier of testosterone sensitivity or insensitivity that affected development of the brain only and not the body and genitals might possibly explain why homosexual people show SSSA but do not have intersex bodies. This is an interesting theory, but there is currently no evidence such a precise epigenetic modifier of testosterone sensitivity exists in either humans or other animals.

  These views of homosexuality have long since been rejected by clinical and social psychology because in clinical psychology they have been found to be inaccurate, unsupported, and unconstructive (Haumann, 1995; Jordan-Young, 2010; Bailey et al., 2016). We argue that it is time for evolutionary psychology to also question the veracity of the endocrine hypothesis for human homosexuality.

 It would not require that SSSA be masculinelike for females or feminine-like for males. Rather, consideration of both an additive genetic model for SSSA and selection on SSSA in prosocial contexts would predict a diversity of expression of SSSA in both males and females.

We have argued that SSSA evolves as part of selection for increased prosociality. This hypothesis is testable. If it is correct there should be a detectable benefit to SSSA in contexts of within-group cohesion or cooperative tasks. Some evidence already points to a relationship between affiliation and SSSA in humans. Kirkpatrick (2000) documents ethnographic examples of SSSA and homosexual behavior strengthening important social affiliations in both males and females and SSSA supporting long term supportive social bonds. Human males self-reported a higher level of homoerotic motivation if they were primed with words related to friendship than if they were primed with words related to sex (Fleischman et al., 2015). This suggests that for males social affiliation is a greater releaser of SSSA than a sexual context (Fleischman et al., 2015). Whether within-group SSSA enhances cooperation and group performance to provide individual selective benefits remains to be tested, however.

Animal models could provide a powerful resource to explore these questions. We have described how homosexual behavior is more common in highly prosocial species than non-prosocial close relatives. We would predict homosexual behavior to enhance cooperation, group cohesion and performance and ultimately increase the reproductive success of individuals that are part of a high-functioning group in animals also. Comparing the consequences of homosexual behavior in bonobos and chimpanzees for group function would be a test of this hypothesis (Moscovice et al., 2019).

If the sociosexual hypothesis of SSSA evolution is correct we would expect to see an introgression of systems causal of human SSSA and social and affiliative behavior at both genetic and physiological levels of analysis. As we have discussed above, current evidence is compatible with this hypothesis, but significant gaps remain in our understanding of the genomic and neurophysiological basis of human sexual orientation and much work remains to be done.

Exploration of human SSSA has thus far been dominated by assumptions that the trait must be maladaptive (Bell et al., 1981; King et al., 2005; Wrangham, 2019). It may be timely and beneficial to explore alternatives that consider the sociosexual adaptive functions of same sex attraction and sexual behavior, and the full spectra of expression of SSSA.

## AUTHOR CONTRIBUTIONS

AB and BH conceptualized and wrote the manuscript.

## REFERENCES

fpsyg-10-02955 January 10, 2020 Time: 9:34 # 6

Pillard, R. C., and Bailey, M. J. (1998).  Hum. Biol. 70, 347–365.

**Conflict of Interest:** The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Copyright © 2020 Barron and Hare. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

# Prehistoric Perspectives on "Others" and "Strangers"

Anna Belfer-Cohen1 \* † and Erella Hovers1,2 \* †

1 The Institute of Archaeology, The Hebrew University of Jerusalem, Jerusalem, Israel, 2 Institute of Human Origins, Arizona State University, Tempe, AZ, United States

Social "connectivity" through time is currently considered as one of the major drivers of cultural transmission and cultural evolution. Within this framework, the interactions within and between groups are impacted by individuals' distinction of social relationships. In this paper, we focus on changes in a major aspect of social perceptions, "other" and "stranger." As inferred from the archaeological record, this perception among human groups gained importance during the course of the Pleistocene. These changes would have occurred due to the plasticity of cognitive mechanisms, in response to the demands on behavior along the trajectory of human social evolution. The concepts of "other" and "stranger" have received little attention in the archaeological discourse, yet they are fundamental in the perception of social standing. The property of being an "other" is defined by one's perception and is inherent to one's view of the world around oneself; when shared by a group it becomes a social cognitive construct. Allocating an individual the status of a "stranger" is a socially-defined state that is potentially transient. We hypothesize that, while possibly entrenched in deep evolutionary origins, the latter is a relatively late addition to socio-cognitive categorization, associated with increased sedentism, larger groups and reduced territorial extent as part of the process of Neolithization. We posit that "others" and "strangers" can be approached from contextual archaeological data, with inferences as regards the evolution of cognitive social categories. Our analysis focused on raw material studies, observations on style, and evidence for craft specialization. We find that contrary to the null hypothesis the archaeological record implies earlier emergence of complex sociocognitive categorization. The cognitive, cultural and social processes involved in the maintenance and distinction between "others" and "strangers" can be defined as "self-domestication" that is still an on-going process.

Keywords: social behavior, paleolithic archaeology, socio-cognitive construct, social stereotypes, inter-group relationships, material culture proxies

"No man is an island entire of itself; every man is a piece of the continent, a part of the main;" MEDITATION XVII, Devotions upon Emergent Occasions (John Donne)

## INTRODUCTION

While much research focused on the question of the emergence of "modern" cognition – a vague concept that is variably understood and therefore variably recognized (see, e.g., Belfer-Cohen and Hovers, 2010) – there is a growing realization that rudimentary forms of human cognition can be traced into deep prehistoric times (e.g., Deacon, 1989; Laland, 2017 and references therein).

#### Edited by:

Antonio Benítez-Burraco, University of Seville, Spain

#### Reviewed by:

Thomas Wynn, University of Colorado Colorado Springs, United States Mark Collard, Simon Fraser University, Canada Masami Izuho, Tokyo Metropolitan University, Japan

#### \*Correspondence:

Anna Belfer-Cohen<EMAIL_ADDRESS>Erella Hovers<EMAIL_ADDRESS>
#### †ORCID:

Anna Belfer-Cohen orcid.org/0000-0003-3072-667 Erella Hovers orcid.org/0000-0002-7855-6573

#### Specialty section:

This article was submitted to Evolutionary Psychology, a section of the journal Frontiers in Psychology

Received: 29 July 2019 Accepted: 26 December 2019 Published: 21 January 2020

#### Citation:

Belfer-Cohen A and Hovers E (2020) Prehistoric Perspectives on "Others" and "Strangers". Front. Psychol. 10:3063. doi: 10.3389/fpsyg.2019.03063

**75**

Research into human biological and social evolution has attempted to identify the role played by various cognitive aspects (e.g., Donald, 1993; Richerson and Boyd, 2000; van Schaik and Pradhan, 2003; Dunbar and Shultz, 2007; Andersson, 2011; Wynn and Coolidge, 2011, 2016; Grove, 2012; Jaffers, 2014; Dennett, 2016; Lombard and Gardenfors, 2017). Archaeologists of early prehistory directed their attention to the production and use of stone tools, focusing on planning depth, dexterity, and forms of teaching and learning. At the same time, primatologists, prehistorians, and paleoanthropologists developed lines of inquiry that focused on the capacity of the hominin brain to create, maintain and augment social relationships (e.g., Delagnes and Roche, 2005; Stout et al., 2008, 2011, 2019; Nowell and Davidson, 2010; Vaesen, 2012; Dunbar et al., 2014; Tomasello, 2014; Tomasello and Call, 2014; Dunbar and Shultz, 2017; Gärdenfors and Högberg, 2017; Herzlinger et al., 2017).

Plasticity of cognitive mechanisms is implicated as a major factor responsible for behavioral and cultural trajectories, as it both influences and is influenced by the way those have evolved over the course of prehistoric time. In fact, it seems unlikely that culture could have evolved without affecting cognition. Colagè and d'Errico (2018):4) argued that " . . .the brain [modifies] physiological, functional, and/or structural features as a consequence of experience and practice without any concomitant change at the genetic level" (see also discussion in Lotem et al., 2017).

In this context, the emergence of human sociality (Barrett et al., 2012) draws our attention to "social cognition" (SC) which emerges as an important element that influenced the structure, economy and culture of Paleolithic groups (e.g., Davies, 2016). SC constitutes people's subjective interpretations of social situations as well as the concepts and cognitive processes whereby they were shaped (Korman et al., 2015; and see Thompson et al., 2016). Because of the assumed link between culture and SC, we also speculate that changes in cognitive social concepts, and thus in social relations, can be inferred from the cultural record of the Pleistocene.

The general question as to how prehistoric hominins structured their social relations is not a new one. Two fundamental, widely-discussed concepts in paleoanthropological research are those of "group" and "population" (e.g., Birdsell, 1958; Zhou et al., 2005; Gamble et al., 2014; White, 2017; Casari and Tagliapietra, 2018; and references therein). Attention was devoted to the variable forms of the organization of individuals into groups as the mechanisms that enabled rich and complex social configurations in extant and past hunter-gatherers (e.g., Grove, 2010; Hill et al., 2011; Grove et al., 2012; Bird et al., 2019; Domínguez-Rodrigo et al., 2019; Herzlinger and Goren-Inbar, 2019; Malinsky-Buller and Hovers, 2019).

In particular, shifts in group size and intra- and inter-group connectivity are currently considered as significant drivers of cultural transmission and cultural change (e.g., Premo and Scholnick, 2011; Derex et al., 2014, 2018; Stout, 2018; Greenbaum et al., 2019). The interactions within- and between- groups are complex processes that are impacted by the social roles of the individuals that comprise those units (Jenkins et al., 2018; Cacault and Grieder, 2019). These encompass the self-recognized place of an individual within her group, which in turn shapes ". . . the processes of formation of groups and changing membership of groups." (Festinger, 1954: 135).

Here we discuss the SC concepts of "other" and "stranger," fundamental in defining social interfaces within and between groups of hunter-gatherers, as they have shaped, to considerable degree, economic, mobility and territorial behaviors that can be inferred from the archaeological record. Yet, these concepts have rarely been addressed in archaeological discussion.

In the modern (and, mainly, post-modern. . .) discourse, "other" and "stranger," are often used alternately. However, they are not synonymous. Dictionary definitions run:

"Other" – refers to a person or thing that is different or distinct from one already mentioned or known about1 .

"Stranger" – a person who does not know a particular place or community or is not known in a particular place or community2 .

Addressed from contextual archaeological data, our exploration is preliminary and inherently speculative, with inferences as regards the evolution of human sociality. As a caveat to the discussion we must add that the nature of prehistoric evidence clearly impedes archaeologists from discussing the socio-cultural process defined by cultural anthropologists and sociologists as "othering" or the concept of "The Other".

The human social cognition system reflects the history of the genus Homo, potentially as far back as Homo erectus (∼1.8 million years ago), during which SC played a major part in constructing the human unique "niche" of adaptation to the external world (Laland et al., 2014; Davies, 2016).  The latter would include shared social norms, predispositions and prejudices, being aware that "we are differently located in a shared world." (ibid.). The active role of culture in shaping the social landscape of humans, in conjunction with genetic dictates and sometimes over-riding them, constitutes what one might define as "self-domestication."

The property of "otherness" is inherent to one's view of the surrounding world and to a large degree defines oneself (see definition above). In evolutionary terms the notion of being an "other" is an innate trait of human sociality, and is immutable. At a group-level, when a number of individuals consider themselves as "one," vis-à-vis individuals or groups that do not belong to the "one," "others" becomes a social cognitive construct. Still, there are degrees of social "otherness" that can be perceived within and between groups. Hunter-gatherer kinship terminologies (Chapais, 2014) make it psychologically possible to embrace nonkin members of one's residential or task group, with whom one shares common history and beliefs, in order to accept them as kin. For example, Bird et al. (2019: 102), describing the Martu in the Western desert of Australia, state: "Many of the compound families in the 2005 census were actually multigenerational extended "classificatory kin" (e.g., older and younger "sisters"

1https://en.oxforddictionaries.com/definition/other

2https://en.oxforddictionaries.com/definition/stranger

who share the same fictive kinship section, and are thus parallel "cousins", but may have no close biological relationship)."

The concept of "stranger"is a trait of a complex society, an emergent social construct that is transient, since it depends on changeable cultural perceptions. In the words of Korman et al. (2015: 31), "This constant and reflexive updating of mental states presents a significant computational challenge, and people's ability to conduct such rich and dynamic social interactions is one of the greatest achievements of human cognition."

## A SUGGESTED DIACHRONIC SCENARIO

Some non-human primates appear to present behaviors that suggest that they may differentiate between "others" and "strangers." To wit, the viability of a chimpanzee genetic pool (which is ≤300 individuals) is maintained by the relocation of fertile females among groups. When chimpanzees from those groups ("kin" or "others" in our terminology) encounter each other, the outcomes vary from skirmishes to friendship (see Tokuyama et al., 2019 for a recent discussion). This contrasts with encounters of groups from a different breeding pool ("strangers"), who fight until annihilation of one of the groups, including productive females.

Even when leaving aside the question of how deep the evolutionary roots of ape/chimpanzee aggression behavior might be (e.g., Ferguson, 2011; Sussman, 2013), there are a number of compelling arguments to support the view that the survival of human groups depended on the existence of social groupings of non-kin, even beyond "classificatory kinship" relationship. Viable mating networks, constituting some hundreds of individuals, are perhaps the most obvious such social units, within which interactions among "others" took place. Additional incentives for interacting with non-kin "others" may have involved the need to outcompete carnivores and gain safety through numbers. In many ecological contexts, low carrying capacity would preclude protracted and/or large aggregations, such that early hominins spent most of their time in small residential groups within an overall larger, even if mostly virtual, social structures (e.g., "extended groups," Gamble, 1999). The latter constituted the pool for the "daily" grouping, enabling a flexible fission-fusion social structure, which was in turn constrained by ecology, technology and demography (Grove et al., 2012). Cautiously drawing inferences from extant populations, it is reasonable to assume that aggregations, namely large meetings that provided networking opportunities, were not random, as they had to be part of a basic behavioral routine, for example seasonal/annual aggregations, obligate exchange, etc. (e.g., Hovers, 1990; Bar-Yosef, 1997; Pearce and Moutsiou, 2014).

The frequencies of large group gatherings were dictated by population densities, such that lower densities would require more frequent aggregations. These meetings would have been of a limited duration. The reasons could be shortage of resources to sustain relatively large numbers of people. Since the meetings were scheduled, of a short duration and in an agreed-upon territory, there would be fewer opportunities for encroachment on the resources of the respective groups taking part in the aggregation. In ethnographic contexts, the fissioning of the aggregation stems from rising social tensions rather than environmental stress. When asked how people knew when to break up an aggregation, a !Kung informant replied that it happened when the women had no further information to share and started quarreling at the communal water hole (Konner, 2002).

Under these circumstances members of a particular group were likely aware of "us" or "we", i.e., their own group members, as opposed to "others" with whom they had relatively brief social interactions. Under Paleolithic conditions (of sparse populations, spread over extensive territories) there would be only "us" and "others," because every person, with whom one had any kind of interaction, belonged by default to the same reproductive network, even if not of the same basic social unit (extended family, kin and classificatory kin, residential unit). At all times, these social interactions involved kin and "others" but not "strangers."

Because of the strong influence of culture on SC, changes in economic, demographic, spatial (and other) aspects of human culture introduced changes in perceptions of social relationship, i.e., in SC. Through time, one can observe a rise in residential group size and a reduction in territory sizes – both linked to improved means of production and associated demographic changes (Hayden, 1981; Gilman, 1984; Hamilton et al., 2007a,b). A larger group could serve as a viable genetic pool nearly on its own, without the need to meet members of other groups on a regular basis. Moreover, evolving complex societies would become more tethered to their geographic locations and more protective of their bounded resources and, in later periods, their surpluses. Encounters with individuals that did not belong to the same group would be less crucial for survival, and therefore would not be pre-scheduled or repetitive. On the other hand, when such encounters occurred, potential causes for inter-personal tensions would stem from economic interests, related to the availability, ownership and sharing of resources. Such encounters occurred between "strangers," i.e., individuals or groups that did not share common history, cultural traditions, or behavioral patterns.

With the increase of global and local population sizes and change of economic mode, with the introduction of farming/agriculture, boundaries became less defined by clearcut geographic features. Instead, "crowding" (e.g., by sedentism ensuing increased population densities) led to the emergence of socially constructed barriers. The definition of "strangers" lost its dependency on rare, random encounters. People came to consider as strangers also individuals they could meet on a daily basis but belonged on the other side of the social barrier.

The perception of "strangers" became even more nuanced through time. As networks of exchange (of both commodities and information) expanded, the rate of encounters with strangers increased, being beneficial to both sides. Under this premise some strangers, whose expertise and fields of knowledge complemented the ones present within a group, would be favored and would be more often tolerated by, if not accepted into, a given community. This differentiation became most obvious with the introduction of craft specialization and market economy. Hence it is in these

later periods that we expect to find indications for "strangers" in the archaeological record.

The scenario presented above relies on theoretical, sociological and ethnographic knowledge, all engaged by researchers in attempts to structure a narrative of the evolution of human society and sociability. We find similarities with the question of children's visibility in the archaeological record, a topic that, once raised, has burgeoned into a prolific field of inquiry (see, for example, Hammond and Hammond, 1981; Shea, 2006; Baxter, 2008; Chappell et al., 2013). The challenge herewith would be to evaluate the feasibility of archaeology to provide evidence based on the material culture record for the suggested scenario of the diachronic transformation of SC as regards "others" and "strangers." On the evolutionary scale of prehistory, our questions should be formulated at the group rather than individual level.

## THE ARCHAEOLOGICAL EVIDENCE

An obvious question is which archaeological proxies can be used in addressing such questions. Given the scenario above, we suggest investigating aspects of the archaeological record that are often understood as markers of personal and group boundaries and alliances. Prominent among these are elements that denote territoriality, social identities, and within- and between-group relationship. Here we address examples from pertinent behaviors identified archaeologically.

The types of **raw materials** and their distributions within and between regions speak to the modes of procurement and transport and help to understand spatial dimensions of group interactions. At least in some instances, it is possible to discern between direct procurement (i.e., when a person/group traveled to the source and brought material back to a site) and forms of exchange. Each of these behaviors potentially bears implications for the type of interactions between groups in a given geographic space, namely, contacts with "others" or with "strangers."

**Stylistic variations** within various categories of material objects have been argued to represent social identities at personal, group and regional levels. In some instances, stylistic variability can be tied to the fission-fusion social structure dynamic, specifically to the phase of aggregation when many "others" come together. It is sometimes possible to identify stylistic particularities that were used consciously as emblems, specifying group or population identities. By default, the absence of a shared emblem would denote one's state of "stranger."

The phenomenon of **craft specialization** pertains to differences in both style and production technology. Whereas experts perform with high levels of both conceptual and practical (savoire-faire) knowledge, average or novice practitioners possess the theoretical knowledge that is embedded in their material culture traditions, but would implement it poorly. Hence these two (broad) categories of skill are identified archaeologically (e.g., Karlin et al., 1993).

In a number of published case studies, the signature of local experts, who adhere to the raw materials, technological practices and styles of their group, has been recognized. Conversely (in particular during later prehistory) there are instances when the material record suggests that an artisan was not local, as expressed by the use of technology and style that had emerged and developed elsewhere. This would suggest a different type of social standing within the group, that of a "stranger."

As our archaeological experience lies mainly within the Levantine record, we discuss some of the implications of the above scenario by looking closely at the details of selected case studies from the Levant. Our insights from the regional record are then contextualized into a broader geographic scope in the Discussion.

## Raw Material

In the Levant (**Figure 1**), flint is the nearly exclusive raw material used for making stone tools (Goring-Morris et al., 2009). Its ubiquity on the landscape suggests that throughout time the optimal behavior of Levantine hominins was that of local procurement from nearby sources of suitable flint, embedded in their subsistence system. This pattern characterizes many Eurasian Paleolithic groups (e.g., Geneste, 1985; Féblot-Augustins, 1993, 2009). It has even been suggested that the same raw material sources/quarries had been recognized and utilized over tens of thousands of years (Gopher and Barkai, 2014; Finkel et al., 2019). If that scenario holds, it would suggest that (for each period) such locations may have served as places of meeting between "others," i.e., individuals that belonged in a single mating system.

However, studies of raw material-related behaviors among Middle Paleolithic (MP; ca. 250,000–50,000 years ago) groups in the Levant suggest that hominins (both Neanderthals and modern humans) did not always opt for a "least effort" solutions for raw material requirements. At times, they obtained a variable (across sites) fraction of the raw material from additional, diverse sources, some of which were located at relatively long distances from the habitation sites. At Amud Cave (**Figure 1**; ca. 68,000–55,000 years ago), for example, this entailed a relatively significant, though non-systematic, transport from numerous, different sources located at distances of over 60 km. Notably, the techno-typological traits and the way of using the "exotic" raw material do not differ from those of the local flint, suggesting that the same people used the local and non-local sources (Ekshtain et al., 2017). Unexpectedly, the existence of a "buffer zone" in the central Galilee, located midrange between the local and the most distant outcrops, was revealed by this analysis. This zone remained unexploited by the Amud hominins, even though it contained many flint outcrops of reasonable quality (Ekshtain, 2015). The appearance and distribution of non-local raw material behavior in the Amud Cave assemblages can be interpreted as the outcome of direct procurement from distant sources. This would potentially entail encounters with groups of "others" within the same mating system. It would constitute an example of permeable social boundaries and the inclusion of the "other" within the economic and cognitive realm of the group. However, the presence of a "buffer zone" possibly demarcates a rigid boundary between groups that perceived each other as "strangers."

FIGURE 1 | Map showing the location of sites mentioned in the text. Base map from Google Earth.

The notion that the construct of "strangers" was activated in the social cognition of MP hominins gains support from another case study at the open-air site of 'Ein Qashish (**Figure 1**; ca.70,000–60,000 years ago). Lithic raw materials were imported into the site from both local and more distant sources. Interestingly, the site's occupants seem to have avoided exploiting available, good-quality sources located east of the site (Ekshtain et al., 2014). This pattern could not be explained through strictly economic aspects of raw material organization. Thus, Ekshtain et al. (2014) suggested that the decision of 'Ein Qashish hominins to avoid exploitation of these sources speaks to social/cultural constraints imposed by territorial boundaries (e.g., Wilson, 2007) between groups identifying themselves as "strangers" to each other.

The different implications for social cognitive distinctions, associated with direct transport vs. indirect procurement through exchange, may be best considered when dealing with raw materials from distinct geographic sources. In the Levantine record, this can be done by looking at marine shells. Such items are known from MIS 5 (ca. 120,000–90,000 years ago) in Qafzeh and Skhul caves (**Figure 1**; Vanhaeren et al., 2006; Bar-Yosef Mayer et al., 2009) as well as in the later open-air site of 'Ein Qashish (70,000–60,000 years ago) (Ekshtain et al., 2019). The relative proximity of the sites to the Mediterranean shorelines of their respective times of occupation and the sporadic appearance of shells in the relevant assemblages likely reflect direct transport rather than exchange (Bar-Yosef Mayer et al., 2009; Hovers, 2009), seemingly within the territory of a mating network (i.e., "others").

A later example from the Epi-Paleolithic (24,000–11,500 years ago) site of Urkan e-Rubb IIa (**Figure 1**; ca. 17,000 years ago; Hovers and Marder, 1991) requires a more nuanced consideration. Located in the Jordan Valley, this site was a place of bead production, to which shells of selected genera and species were brought unmodified, cut and made into beads in situ. Because of the distance from the contemporaneous shoreline of the time (some 70 km to the west), and because of the large number of shells found in Urkan, this situation could be construed as indicative of exchange between groups, reflecting contacts with "strangers" beyond the group's habitual territory. Two lines of evidence suggest differently: first, among the shells that reached the site very few belong to species that were not part of the repertoire of Epi-Paleolithic groups (Hovers et al., 1988; Bar-Yosef Mayer, 2005). These shells seem to have been collected due to mistaken identification. If the Urkan shells were retrieved by exchange, it is likely that the mistake would be

discovered during negotiations. Thus, these specimens reflect collectors' error, indicating that the site's occupants themselves traveled to the shores of the Mediterranean. Moreover, the lithic assemblage of Urkan bears striking similarities to those from sites located in a specific part of the east Mediterranean coast (Hovers et al., 1988; Hovers and Marder, 1991). In the present context of discussion, the archaeology seems to imply that the occupants traveled to the shoreline within their own territory, and that they encountered "others," rather than "strangers."

#### Style

Stylistic characteristics are widely accepted as expressions of individual or group identity (Sackett, 1990; Hegmon, 1992; McElreath et al., 2003; McGuire and Hildebrandt, 2018; see papers in Wobst, 1977; Stark, 1998). To bear on the cognitive differentiation between "other" and "stranger" at the population level, we turn to a striking example of its expression in the Levantine record.

The "Levantine Aurignacian" is a short-lived (37,000– 34,000 years ago) cultural entity that existed only in the northern part of modern Israel and along the Lebanese coast. It is a unique phenomenon in the Upper Paleolithic (UP; 48,000– 24,000 years ago) sequence of the Levant in that it shows greater similarity to the West European "classic Aurignacian" cultural entity (dated there to ca. 40,000–27,000 years ago) than to the local archaeological entities that immediately precede or follow it (Belfer-Cohen and Goring-Morris, 2014). This similarity is seen in both its chipped stone typo-technology and its non-lithic objects. Among the latter are personal ornaments such as tooth pendants as well as bone and antler worked items (Goring-Morris and Belfer-Cohen, 2006). Both the European Aurignacian and the Levantine Aurignacian shared complex technical concepts of antler working as opposed to simpler bone-working technologies.

A unique feature of the Levantine Aurignacian is the occurrence of notched bones (n = 15; typically, gazelle scapulae as well as a single hyoid bone) from the Aurignacian levels of Hayonim, Manot, Kebara (and possibly Emireh) caves (**Figure 1**), all located in northern Israel. Contrary to European Aurignacian sites, where similar items were reported as sporadic finds per site/assemblage, the assemblage from Hayonim Cave is relatively large (n = 9; Tejero et al., 2018). A careful technological analysis demonstrated that the notches constitute intentional markings. Whereas other modified bone objects in the same assemblages, mainly awls and "chisels" intended probably for mundane use, were minimally modified, the notched scapulae were shaped through a complex and specific technique, rarely observed in the Aurignacian techno-complex in Europe.

The difference between the Levant and Europe vis-a-vis notched items is expressed in the selected animal taxa, the raw materials and anatomical elements used, and in the types of "decorated" objects. In the European Aurignacian notches were made on bone, antler and ivory pieces deriving from reindeer, red deer, bovid, and mammoth; the marks occur on antler, bone splinters, personal ornaments and on "utilitarian" tools such as polishers. In contrast, notched pieces in the Levantine Aurignacian are highly uniform and homogenous, with gazelles being the only animal species selected and with an almost exclusive use of a single anatomical element, the scapula.

The standardization of their production procedures as well as their relative concentration in Levantine Aurignacian assemblages indicate that these items were unique features of the regional record. It was suggested that they served as an emblem of the Levantine Aurignacian (Tejero et al., 2018). Such items possibly reflect the strong ties between various Levantine Aurignacian communities by serving as a marker of "us" and "others" (i.e., biological and "classificatory" kin), differentiating them from the surrounding population of "strangers" (e.g., the native Ahmarian cultural entity)3 , who did not share the social and cultural worldviews expressed through this particular cultural item.

Tooth pendants, recovered from the very same sites of the short-lived Levantine Aurignacian, illuminate another facet of the social cognitive distinctions between "others" and "strangers." By way of example, we use the assemblage from the same layers at Hayonim Cave (Belfer-Cohen and Bar-Yosef, 1981). In contrast to the notched pieces, tooth pendants were never made on gazelle teeth, but on the vestigial canines of (mostly) male red deer (Cervus elaphus), and were shaped by a particular technique. Both the manufacture marks and the use-wear signs point toward personal ornaments. Some of the modification processes differed from those observed in other Levantine Aurignacian sites (Tejero et al., submitted).

In the European Aurignacian record, the exploitation of mammal teeth – including in some cases human teeth – became a common practice, probably playing a role in the symbolic sphere of these hunter-gatherer groups. Different teeth (incisors, canines, premolars and molars) of a large spectrum of herbivores (e.g., reindeer, red deer, horse, bison, goat) and carnivore (e.g., bear, wolf, fox) species were selected for the manufacture of these ornaments. The flexibility seen in the techniques employed for ornament production is expressed by the emergence of region-specific (albeit interconnected) characteristics (Vanhaeren and d'Errico, 2006).

The use-wear of the Levantine and European Aurignacian pierced teeth implies identical utilization of the objects, suggesting shared symbolic practices. The in situ production of the pendants, demonstrated at least for some of the Hayonim items, reinforces this suggestion. This contrasts significantly with the archaeological manifestations of the locally-rooted Ahmarian techno-complex. Thus, accepting that the pendants were markers of the Aurignacians, their similarity in the Levant and in Europe is striking. It lends support to the notion of the Levantine Aurignacian as an incursion from Europe that is linked to its geographic origins through cultural tradition. The pendants therefore suggest that the Aurignacian populations were "others" within a Mediterranean meta-population, with a shared history that arose before the "migration" of Aurignacian groups into the Levant, and which defined them as "strangers" to the local Ahmarian groups of the eastern Mediterranean coast. Thus, the

3The Ahmarian differs from the Aurignacian mainly in its characteristic flint tools and the near absence of bone and antler artifacts. It is dated to 46,000–30,000 years and accordingly is contemporaneous with the Levantine Aurignacian (Alex et al., 2017; Goring-Morris and Belfer-Cohen, 2018).

differentiation was not necessarily constrained or dictated by geographic distance. For the Levantine Aurignacian, "otherness" and "strangeness" seem to have been first and foremost constructs of social cognition.

## Craft Specialization

We hypothesized (see above) that encounters with strangers should become more apparent in the archaeological record of later periods. We also suggested that their presence can be detected through identification of the products of expert artisans bringing with them knowledge that is new to the local groups.

Although expert lithic knappers may have existed in the Levant as early as the Acheulian, it is of note that their activities are understood as those of local artisans acting within the context of a (sometimes large) residential group (Herzlinger and Goren-Inbar, 2019) of kin (in the extended sense of Bird et al., 2019). Comparable evidence is lacking for most of the Levantine Paleolithic record (possibly due to research/preservation constraints), yet the presence of expert knappers has been recognized in other Paleolithic records, such as the UP Magdalenian culture (ca. 15,000 years ago), in Etiolles, France (Pigeot, 1990 and references therein). There, too, expert knapping occurred within a residential context, and experts are regarded as models for novice knappers.

The context of activities of expert knappers in the Levant seems to have changed in the Pre-Pottery Neolithic B (ca. 10,500–8,400 years ago), possibly as part of the Neolithization processes. The "naviform" mode of flaking stone, designed for the production of long and thin blades, was a pan-Levantine phenomenon (Bar-Yosef and Belfer-Cohen, 1989). Naviform products (arrowheads and sickle blades) expertly produced on non-local raw material, were found together with items sharing the same regional conceptual knowledge yet crudely knapped on local raw material (Barzilai and Goring-Morris, 2007; Khalaily et al., 2007, 2013; Barzilai, 2010; Mitki, 2015). A common explanation of this phenomenon is that the well-made items were introduced into the local communities from outside the region. We maintain that those were produced by expert knappers rather than traded, because of the presence at the sites of production debris besides the finished products (ibid.). The material cultural record shows that naviform technology first emerged and evolved in the northern Levant (e.g., current-day central and eastern Turkey, northern Syria), and that its craftsmanship in the north was overall more refined than in the southern Levant. We therefore posit that, heralding from the northern Levant, the expert knappers of naviform items would be perceived as "strangers" by the local communities.

## DISCUSSION

Chimpanzees and humans both appear to harbor concepts of "strangers," which may be attributed to a shared evolutionary origin. The encounters of chimpanzee groups with "strangers" are rare, and were reported rather sparsely (e.g., Goodall, 2010; Wilson et al., 2014), because the spatial packing of chimpanzee groups on the landscape typically does not bring groups from different breeding networks into contact. Based on current evidence (which is incomplete for Pleistocene hominins due to the vagaries of time), in human society this SC construct has changed from that of the chimps (and presumably, an early ancestor) during the course of the Pleistocene. We identify the main changes in that the notion of "strangers" is enacted upon constantly in the context of large social networks, and in that it is fluid and transient.

Nearly all researchers agree that hominins, unlike perhaps other species, have found cognitive and social scaffoldings that enable them to operate within very large groups, crossculturally. It is also clear that at some point in human cultural and social evolution, one's recognition of "group size" shifted from census numbers to a social perception. Notwithstanding any biological limitations on group size, humans acquired a cognitive flexibility that enabled them to first, enlarge the biological and social perception of kin and, secondly, to categorize their social world as one of stable ("kin"/"classificatory kin"/"others") and transient relationships ("strangers"). The latter could be remodeled contextually (i.e., politically, economically or culturally) according to shifting circumstances. Already Isaac (1972) wrote that once culture became more complex and comprehensive and social rules became more structured, it was more likely that internal isolating mechanisms would develop. Gilman (1984) specifically related to shifting circumstances when explaining the difference between the MP vs. UP social interactions. "Thus, as technique improved, relations between groups would become more problematical. [In the earlier periods] the give-and-take of mutual aid would have been so essential that it would have known no social boundaries. . ." (Gilman, 1984:122). In contrast, in the cultural world of the UP, improved technology led to higher group densities, such that more neighbors became available yet there were fewer occasions on which help from neighboring groups would be required to mitigate environmental risks. "The clear solution to this shift in the balance of a group's interests would be to restrict the scope of its alliances." (ibid.). Similar to Stiner and Kuhn (2006), we interpret the UP pattern to suggest higher degrees of connectivity between groups belonging to the same cultural environment, yet we propose that such connectivity was structured differentially across geographic space, with "strangers" located more distally to a given group than were "others." We argue that these large UP groups could not have formed without the emergence of the SC construct of "strangers."

Furthermore, the archaeological evidence allows us to identify earlier-than-expected trends in the emergence of the social cognitive constructs related to inter-personal/intra-group and inter-group behaviors. There is indirect evidence that large social groupings, with their implied categorization of social relationships, emerged earlier than the UP, thus our null hypothesis must be rejected.

We have focused our archaeological discussion on Levantine case studies, using information from lithic raw material, bone tools and personal ornaments. When contextualized against the broader archaeological records of the respective periods outside of the Levant, archaeological data provide insights of

similar social cognitive constructs. For example, larger transport distances of raw material entailed, almost by default, awareness and recognition of "strangers." Long transport distances of obsidian in eastern Africa (>200 km and sometimes >300 km; Blegen, 2017; Merrick et al., 1994; Negash and Shackley, 2006) are reported from the early Middle Stone Age (MSA; ca. 320,000–50/40,000 years ago) onward. These data could be interpreted to reflect large home ranges of "others" acting within a social/cultural group, interacting directly at the obsidian sources. More likely, this pattern should be attributed to indirect procurement (e.g., Merrick et al., 1994; Tryon and Faith, 2013) through the agency of "strangers." Indeed, it has been argued that this very pattern reflects the increase in spatial extent of the social networks, as is the case with modern hunter-gatherers (Pearce, 2014; Pearce and Moutsiou, 2014). Similar behaviors may explain the distances of obsidian transport in the Caucasus (see discussion in Doronicheva and Shackley, 2014), which in some cases were >500 km during the late MP and the UP (Frahm et al., 2019). The late MP in Eurasia may be the first time when "strangers" become an element of the social structure, within networks of partial connectivity greatly contributing to the growth and evolution of human culture at large (Derex and Boyd, 2016; Premo, 2016; Derex et al., 2018). In fact, this may be the continuation of a trend that had started in the Middle Pleistocene (e.g., Rolland, 2004; Kuhn and Stiner, 2019) and gradually increased through time, as indicated by the Eurasian UP record in general (Stiner and Kuhn, 2006), and the Levant specifically (see above).

A known phenomenon in the south Levant, of sites dating to Late UP [Epipalaeolithic] and Neolithic times, is that of obsidian sourced to central and northern Anatolia. This is parsimoniously explained as evidence of down-the-line trade or exchange (see Ammerman, 1979 for a case study outside the Levant) involving "others" and/or "strangers," which grew in scope with the process of Neolithization. Indeed, the evidence for the activities of

#### REFERENCES

non-local expert knappers in south Levantine Early Neolithic villages corroborates such interpretations. In fact, this may be the culmination of a trend that had started ca. 400,000 years ago, in the late Middle Pleistocene (e.g., Kuhn and Stiner, 2019) and gradually increased through time, as indicated by the Eurasian UP record in general (Stiner and Kuhn, 2006; and see above).

As we understand it, the trend is consistent with Isaac (1972) and Gilman (1984) insights that as economy and technology became more complex, it required constant evaluation of social cognitive rules and their ongoing restructuring within the respective cultural contexts. The separation between "us" and "others" vis-a-vis "strangers" would be instrumental in alleviating "scalar stress" (as defined by Johnson, 1982) within a large group. The breaking down of larger and growing social units into smaller, conceptually "manageable" ones, would require the creation of social stereotypes that one could allude to (see also Cohen, 1985). This is a process that has been observed in historical and extant societies and apparently is still ongoing. A historical example is the ancient Greek worldview, by which a social universe was divided almost by default into two: "us" (and all related "others"), meaning familiar, Greekspeaking individuals/political entities; and the rest of the world populations, "strangers," i.e., unfamiliar individuals/political entities that did not speak the language, all of them stereotyped as "Barbarians." In fact, to this day group identity creates cognitive social and economic biases and stereotypes that affect venues of modern life (e.g., Cacault and Grieder, 2019). In this sense, SC constructs that have emerged in deep prehistoric times affect many aspects of our modern lives, in an ongoing process of self-domestication.

## AUTHOR CONTRIBUTIONS

Both authors perceived and wrote the manuscript.

**Conflict of Interest:** The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Copyright © 2020 Belfer-Cohen and Hovers. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

# Why Care: Complex Evolutionary History of Human Healthcare Networks

#### Sharon E. Kessler1,2 \*

1 Department of Psychology, Faculty of Natural Sciences, University of Stirling, Stirling, United Kingdom, 2 Department of Anthropology, Durham University, Durham, United Kingdom

One of the striking features of human social complexity is that we provide care to sick and contagious individuals, rather than avoiding them. Care-giving is a powerful strategy of disease control in human populations today; however, we are not the only species which provides care for the sick. Widespread reports occurring in distantly related species like cetaceans and insects suggest that the building blocks of care for the sick are older than the human lineage itself. This raises the question of what evolutionary processes drive the evolution of such care in animals, including humans. I synthesize data from the literature to evaluate the diversity of care-giving behaviors and conclude that across the animal kingdom there appear to be two distinct types of care-behaviors, both with separate evolutionary histories: (1) social care behaviors benefitting a sick individual by promoting healing and recovery and (2) community health behaviors that control pathogens in the environment and reduce transmission within the population. By synthesizing literature from psychology, anthropology, and biology, I develop a novel hypothesis (Hominin Pathogen Control Hypothesis) to explain how these two distinct sets of behaviors evolved independently then merged in the human lineage. The hypothesis suggests that social care evolved in association with offspring care systems whereas community health behaviors evolved as a type of niche construction. These two types of behaviors merged in humans to produce complex, multi-level healthcare networks in humans. Moreover, each type of care increases selection for the other, generating feedback loops that selected for increasing healthcare behaviors over time. Interestingly, domestication processes may have contributed to both social care and community health aspects of this process.

Keywords: care-giving, illness, disease, social cognition, self-domestication, human evolution, niche construction, eusocial

## WHAT ARE HEALTHCARE BEHAVIORS?

Human healthcare, including biomedical care, has enabled our species to exert an unprecedented amount of control over the pathogens which affect our species (Ferguson et al., 2003; Kessler et al., 2017, 2018). We synthesize medications, track the evolution and outbreak of novel diseases (Jones et al., 2008), and have even eradicated pathogens using vaccines (Ferguson et al., 2003). While these activities are clearly unique to our species, once healthcare behaviors are separated from medical technologies, we see intriguing continuities and convergences in healthcare behaviors across the animal kingdom. It is these patterns of care-giving behaviors that offer the opportunity to examine

#### Edited by:

Antonio Benítez-Burraco, University of Seville, Spain

#### Reviewed by:

Mikael Puurtinen, University of Jyväskylä, Finland Kai Hiraishi, Keio University, Japan Paul Gilbert, NHS England, United Kingdom

> \*Correspondence: Sharon E. Kessler<EMAIL_ADDRESS>
#### Specialty section:

This article was submitted to Evolutionary Psychology, a section of the journal Frontiers in Psychology

Received: 23 September 2019 Accepted: 28 January 2020 Published: 13 February 2020

#### Citation:

Kessler SE (2020) Why Care: Complex Evolutionary History of Human Healthcare Networks. Front. Psychol. 11:199. doi: 10.3389/fpsyg.2020.00199

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the underlying evolutionary processes driving them, including when, how, and why, care-giving in health contexts got scaled up in our species.

Here, I define healthcare behaviors as a group of behaviors which can control diseases. Because the outcomes of individual infections influence transmission dynamics within a community, this definition includes both behaviors that can control disease progression within infected individuals and behaviors that can control transmission through communities.

This definition means that healthcare behaviors can be paradoxical. Some behaviors promote recovery when given to diseased individuals, i.e., provisioning or guarding animals that might not survive otherwise, whereas other behaviors are harmful to diseased individuals, but protective for the community. For example, termites cannibalizing nest-mates which have been infected with a fungal pathogen do not benefit the infected individuals, but if the cannibalization deactivates the fungal propagules as they pass through the cannibalizer's digestive tract, it does protect other nest-mates from exposure (Octavio Lopez-Riquelme and Luisa Fanjul-Moles, 2013). In addition, some healthcare behaviors, like grooming, are widespread across taxa (Lehmann et al., 2007; Octavio Lopez-Riquelme and Luisa Fanjul-Moles, 2013; Bush and Clayton, 2018), while others are restricted to only a few relevant species. For example, lifting a sick conspecific to breathe at the surface of a body of water (Bearzi et al., 2018) is only necessary in aquatic mammals. Understanding the complex transmission dynamics produced by different types of behaviors and their distribution across species is central to understanding how healthcare behaviors evolve.

In the next section, I examine healthcare behaviors observed in non-human animals while paying particular attention to who the beneficiary is (a specific individual vs. the community in general) and the implications of the behavior for disease transmission. I use healthcare behaviors as an umbrella term which encompasses both healthcare behaviors directed toward an individual [social care, hereafter, also referred to as conspecific care or social support in the anthropological literature (DeGusta, 2003; Hublin, 2009; Turner et al., 2014)] and healthcare behaviors which benefit the community (community health behaviors, hereafter, to reflect the division between medical care for patients and public health in humans today). I deal with these two types of healthcare behaviors separately because a central goal of this paper is to further our understanding of how these two processes may have interacted during human evolution. Notably, these definitions exclude self-directed care and other forms of care, like parental care, which are not specific to health contexts.

Because animals (including humans) may have difficulty determining when a conspecific has an infectious vs. noninfectious condition (injury, disability, non-contagious diseases, etc.), social care for individuals with infectious and noninfectious conditions are unlikely to have evolved independently. As it is more costly to provide care to infectious individuals (one might contract the disease), if animals are unable to accurately distinguish infectious from non-infectious individuals, yet still provide care, non-infectious individuals will lower the costs of providing care when averaged over many care-giving events. Over an evolutionary scale, this may be relevant to understanding how social care could be perpetuated in populations, despite the risks that they pose for the carer. Therefore, I include responses to noncontagious conditions as well. Similarly, I also include responses to dead individuals because (1) care behaviors may start before death and continue afterward (Anderson et al., 2010; Bearzi et al., 2018) and (2) corpses are potential sources of pathogens (Octavio Lopez-Riquelme and Luisa Fanjul-Moles, 2013; Cremer et al., 2018; Porter et al., 2019).

To my knowledge, this is the first review which integrates the biological literature (animal behavior, citations below) with the psychological and anthropological literature [e.g., compassion (Gilbert, 2017; Seppälä et al., 2017) and attachment theory (Fogel and Melson, 1986; Preston, 2013; Cassidy and Shaver, 2016), fossil evidence of social care during human evolution (Dettwyler, 1991; Lebel et al., 2001; DeGusta, 2003; Hublin, 2009; Spikins, 2015; Spikins et al., 2018, 2019)] to produce a new hypothesis explaining the integration of social care and community health behaviors. These healthcare behaviors are part of the behavioral immune system (Schaller and Park, 2011) but focus on a specific subset of the behavioral immune system – the contexts in which individuals suppress disgust, fear, and avoidance responses to engage in behaviors that benefit others (Peng et al., 2013; Preston, 2013). While this review aims to provide a broad overview, I pay particular attention to primates for their evolutionary relationship to humans, cetaceans, and birds for their convergences with humans in cognition, and eusocial insects (Hymenoptera: ants, bees, wasps, and Isoptera: termites) for their convergences with humans without complex cognition. While the selection of species may appear an unsystematic collection of anecdotes, this is largely a reflection of the discipline at present; these are the taxa which have received the most attention, first as anecdotal reports by field researchers and then, with taxa specific reviews (e.g., Bearzi et al., 2018; Bush and Clayton, 2018; Reggente et al., 2018; Watson and Matsuzawa, 2018). This has had the unintended effect of making the discipline fairly "siloed." One of the goals of this paper is to look across taxa and behaviors to identify patterns and start building a broader theoretical framework for understanding the evolution of healthcare behaviors. I hope that this will lay the foundation for future work which can test this theoretical framework.

## SOCIAL CARE: BEHAVIORS BENEFITTING AN INFECTED INDIVIDUAL

#### Grooming

Allogrooming is widespread across the animal kingdom [i.e., primates (Lehmann et al., 2007), birds (Bush and Clayton, 2018), ungulates (Hart and Hart, 2018), and insects (Octavio Lopez-Riquelme and Luisa Fanjul-Moles, 2013)]. This includes removing ectoparasites with hands (Lehmann et al., 2007), bills (Bush and Clayton, 2018), teeth (Hart and Hart, 2018), or mouthparts (Octavio Lopez-Riquelme and Luisa Fanjul-Moles, 2013). Although many species appear to tolerate some ectoparasites (Hart, 2011), they may also be vectors of other