(PDF) Human Social Evolution: Self-Domestication or Self-Control?

HYPOTHESIS AND THEORY published: 14 February 2020 doi: 10.3389/fpsyg.2020.00134 Human Social Evolution: Self-Domestication or Self-Control? Dor Shilton 1* , Mati Breski 1 , Daniel Dor 2 and Eva Jablonka 1,3 1 The Cohn Institute for the History and Philosophy of Science and Ideas, Tel Aviv University, Tel-Aviv, Israel, 2 The Department of Communication, Tel-Aviv University, Tel-Aviv, Israel, 3 Centre for Philosophy of Natural and Social Science (CPNSS), London School of Economics, London, United Kingdom The self-domestication hypothesis suggests that, like mammalian domesticates, humans have gone through a process of selection against aggression – a process that in the case of humans was self-induced. Here, we extend previous proposals and suggest that what underlies human social evolution is selection for socially mediated emotional control and plasticity. In the first part of the paper we highlight general features of human social evolution, which, we argue, is more similar to that of other social mammals than to that of mammalian domesticates and is therefore incompatible with the notion of human self-domestication. In the second part, we discuss the unique aspects of human evolution and propose that emotional control and social motivation in humans evolved during two major, partially overlapping stages. The first stage, which followed the emergence of mimetic communication, the beginnings of musical engagement, and mimesis-related cognition, required socially mediated emotional plasticity and was accompanied by new social emotions. The second stage followed the emergence of Edited by: Antonio Benítez-Burraco, language, when individuals began to instruct the imagination of their interlocutors, and University of Seville, Spain to rely even more extensively on emotional plasticity and culturally learned emotional Reviewed by: control. This account further illustrates the significant differences between humans and Jeremy Van Cleve, domesticates, thus challenging the notion of human self-domestication. University of Kentucky, United States Adam Stanley Wilkins, Keywords: self-domestication hypothesis, human social evolution, language evolution, music evolution, Independent Researcher, Germany emotional control *Correspondence: Dor Shilton

INTRODUCTION Specialty section: The notion that humans are “domesticated” far precedes the notion that humans have evolved. This article was submitted to Since antiquity, scholars have described humans (in general or in reference to their own particular Evolutionary Psychology, culture) as domesticated, which generally referred to their “civility”: their distance from a wild or a section of the journal savage state of being. It was common for writings on the subject to be entangled with various value Frontiers in Psychology judgments, with some considering the superiority of a domesticated state, while others described Received: 15 October 2019 it as a kind of physical and mental degeneration. Coupled with the tradition of differentiating Accepted: 17 January 2020 human cultures on the basis of the extent to which they were “domesticated,” much literature on the Published: 14 February 2020 subject promoted views of social hierarchies in civility, which were later used as a pseudo-scientific Citation: rationale for racist and eugenic political movements (reviewed in Brüne, 2007). This stain on the Shilton D, Breski M, Dor D and Jablonka E (2020) Human Social intellectual history of human domestication theories illustrates the complex social meanings of the Evolution: Self-Domestication or concept, and its consequent ambiguity when used in explaining human evolutionary processes. Self-Control? Front. Psychol. 11:134. It was Darwin who first critically discussed self-domestication from an evolutionary doi: 10.3389/fpsyg.2020.00134 perspective. While he conceded that humans are similar to domesticates in exhibiting extreme Frontiers in Psychology | www.frontiersin.org 1 February 2020 | Volume 11 | Article 134 Shilton et al. Human Social Evolution: Self-Domestication or Self-Control? phenotypic variability, he nonetheless argued that the for about 50 years before the domestication experiment was term domestication would be misapplied in the case of initiated, so the farm foxes do not represent a completely human evolution: wild population (Lord et al., 2019). Most of the foxes were either aggressive, fearful, or aggressively fearful in response to “It is, nevertheless, an error to speak of man, even if we look human contact, but a few displayed less aggressive and more only to the conditions to which he has been exposed, as ‘far exploratory reactions toward the gloved hand (Belyaev, 1979). more domesticated’ [. . . ] man differs widely from any strictly About 10% of the most tame in each generation were selected domesticated animal; for his breeding has never long been (Trut et al., 2009). Several generations later, the experiment controlled, either by methodical or unconscious selection. No race or body of men has been so completely subjugated by other had produced a population of foxes whose reaction to human men, as that certain individuals should be preserved, and thus contact was the opposite of that exhibited by most of the original unconsciously selected, from somehow excelling in utility to their population, with fear and aggression superseded by willful and masters.” (Darwin, 1871, pp. 28–29) positive engagement. As predicted by Belyaev, the behavioral changes were accompanied by physiological and morphological That said, Darwin’s study of domesticated species recognized changes, as well as by changes in mating habits. The foxes the package of traits that many mammalian domesticated species had shortened legs, tails, snouts and upper jaws; floppy ears, share, which includes morphological traits such as skeletal curly tails, and altered coat color patterns; mating became changes (shorter muzzle, decreased heart size, reduced teeth more frequent and no longer strictly seasonal; supernumerary size, short and curly tail, floppy ears), physiological traits such and non-essential B chromosomes became more frequent; the as altered and usually more numerous reproductive cycles, and pattern of inheritance of a pigmentation pattern (a white the retention of many juvenile behavioral features. Decades star on the forehead) was found to be non-Mendelian. At later, Boas (1938) observed that many of these traits were also the hormonal level, which is involved in many behavioral shared by humans, and suggested that this was due to similar changes, the domesticated population exhibited reduced activity selective pressures. Specifically, Boas suggested that in both cases, of the Hypothalamus Adrenal Axis (HPA axis), as well as traits like de-pigmentation, shortening of the face, and the loss higher levels of serotonin and higher activity of key enzymes of reproductive periodicity were partially the result of a more related to serotonin synthesis and degradation, both of which protective environment and a diet of softened, processed food. appear to be critical for the facilitation of tame behavior. Notably, Boas argued that various social laws and prohibitions Interestingly, a line of foxes selected for increased emotional (e.g., marriage regulation, prohibition of infanticide) could also reactivity (enhanced fearful-aggressive behavior) also showed have had selective effects, and was thus anticipating concepts like some characteristics of the domestication syndrome (white cultural niche construction, which would later prove crucial for spotting and changes in stress hormones), suggesting that understanding human evolution. different variations in the regulation of the same developmental In 1959, a still-ongoing experiment on the domestication of pathway may have been under selection in both the tame silver foxes was initiated by Dmitri Belyaev, Lyudmila Trut and and the aggressive lines. The fox selection experiments are their colleagues in Novosibirsk (Belyaev, 1979; Trut, 1999; Trut reviewed in Jablonka and Lamb (1995); Markel and Trut et al., 2006; Dugatkin and Trut, 2017). Belyaev’s experimental (2011), Dugatkin and Trut (2017), Wilkins (2017, 2019), and design has become central to the current formulation of the Lord et al. (2019). self-domestication hypothesis. Belyaev defined domesticated Discussions of self-domestication since the late-20th century behavior as “the ability of animals to have direct contact have centered around Belyaev’s definition of domestication – with man, not to be afraid of man, to obey him, and to in particular, his emphasis on tameness and reduced aggression reproduce under the conditions created by him” (Belyaev, 1979). rather than adaptation to human-made environments. Later The experimenters consequently selected for tameness – the research has put into question the robustness of his definition. degree to which human contact resulted in docile, rather than Lord et al. (2019) argued that the evidence for a widely shared aggressive, behavior. Tameness was estimated through limited suite of traits among animal domesticates, a “domestication human contact: a gloved hand was introduced into a cage syndrome” (DS)1 , is inconclusive: none of the DS traits are shared with a young fox cub, and its reaction was monitored (Trut by all domesticates, although a reduction in brain size, changes in et al., 2009). Importantly, the procedure did not involve any craniofacial characteristics and increased variation in coat color prolonged contact or training, and selection was based purely are observed in most. Nevertheless, in general there is a “family on the perceived propensity toward tame behavior. Belyaev thus resemblance” among domesticated species, which, we believe, separated as best he could the genetic component, and created a renders the notion of DS useful (but see Lord et al., 2019 for a speeded up evolutionary process. It should be stressed, however, dissenting view). that during typical processes of social evolution, including Coppinger and Coppinger (2001) proposed a different route domestication, selection is much more complex and taming to domestication from that of Belyaev. They suggested that includes many additional factors, including priming and learning the domestication of wolves (Canis lupus) into dogs involved processes. In the case of human social evolution, these involve an initial phase in which less nervous members of the group social and cultural interactions within and between groups. It is also important to note that the original fox population 1 The term “domestication syndrome” (DS) was first used to describe the suite of used in Belyaev’s experiments had been bred in captivity characters shared by animal domesticates by Wilkins et al. (2014). Frontiers in Psychology | www.frontiersin.org 2 February 2020 | Volume 11 | Article 134 Shilton et al. Human Social Evolution: Self-Domestication or Self-Control? became better dump-feeders in human habitats, and eventually Homo. However, because of the differences between humans and formed a separate population. During this stage there was “self- domesticates, we take issue with suggestions that human social domestication,” which involved adapting to feeding opportunities evolution, especially early evolution, is best described in terms in and near human habitats (becoming a synanthropic species), of self-domestication. We suggest that the evolution of unique initially without intentional human intervention. human characteristics requires an explanatory framework based Hare and colleagues have suggested that bonobos (Pan on emotional and cognitive plasticity, a framework that goes paniscus) have also undergone self-domestication, meaning, beyond the selection against aggression and for pro-sociality that more generally, that they went through a process in which is described in most characterizations of self-domestication. selection for reduced aggression led to DS traits (Hare et al., Other accounts of HSD stress the similarities in the 2012; Hare, 2017). Citing evidence for reduced aggression and protective environments of humans and their domesticated physiological and morphological differences between bonobos species (Thomas, 2013), emphasizing the effects of relaxed and chimpanzees (e.g., Rilling et al., 2012), Hare and colleagues selection pressures on both human and domesticate evolution proposed a model of bonobo evolution involving the formation (Brüne, 2007). Our approach differs from these accounts by of female coalitions, which thwarted male aggression and (1) focusing on earlier hominin evolution, beginning with male alliances. They called the outcome of this process of Homo erectus, when most human-specific cooperative and selection against aggression “self-domestication.” While reduced morphological traits seem to have already evolved; (2) suggesting aggression (seen in less competitive feeding habits and increased that human social evolution is more similar to the evolution of social tolerance) is emphasized, other critical behavioral factors pro-social behavior in other highly social mammals, which is are also mentioned. These include more stable parties, extended associated with increased sophistication of social structures and female sexual receptivity and a much less significant reduction increased cognitive and emotional plasticity; and (3) emphasizing in relative brain size (when compared to species domesticated the unique social-cultural selective environment of humans, by humans). This raises the question of whether this complex which, we argue, shaped and amplified our species’ cognitive and suite of physiological traits and social behaviors is indeed best affective plasticity. The recent evolution of humans, especially described as an outcome of a “self-domestication” process, rather after the split with Neanderthals, is interpreted as the outcome than as the outcome of selection for cooperation and emotional of intense cultural evolution driven by language, musicking and control that is observed in many other highly social mammals. In other cultural strategies (Heyes, 2018), rather than by selection the case of humans, these questions are particularly pertinent. against aggression. Human self-domestication is usually characterized as a process of selection against aggression, and more recently as selection for pro-sociality. For example, Sánchez-Villagra and SIMILARITIES AND DIFFERENCES van Schaik (2019) characterize the human self-domestication BETWEEN HUMANS AND hypothesis (HSD) thus: “The current version of the HSD DOMESTICATES hypothesis postulates that selection for reduced aggressiveness in human evolution led to physiological, psychological, and The HSD hypothesis is based on the assumption that since behavioral changes, specifically to social tolerance (p. 136).” Hare humans share several (though not all) traits common to many (2017), who recognizes the importance of selection for self- animal domesticates, they have undergone a similar selection control in human evolution, also emphasizes the similarities process (Thomas and Kirby, 2018). In addition to morphological of human social evolution to that of domesticates and stresses and behavioral similarities, there is also some evidence that selection for pro-sociality and against aggression: “The human selection targeted genes in the same developmental pathways, self-domestication hypothesis (HSD) draws on comparative, including genes expressed in neural crest cells. Wilkins et al. developmental, fossil, and neurobiological evidence to show (2014) suggested that gene mutations leading to slightly reduced that late human evolution was dominated by selection for expression of genes in the neural crest underlie the DS and intragroup pro-sociality over aggression (p. 157).” The stress on can explain why so many traits are shared among domesticates. selection against aggression and for docility is also highlighted Neural crest cells are pluripotent embryonic cells, derived from by Francis (2015), and with qualifications, by Wrangham (2018), the neural tube in early embryogenesis. The cells migrate and who focuses on a reduction in reactive, high arousal, non- give rise to neuroendocrine cells, pigment cells, neurons and calculated aggression. glial cells of the sensory, sympathetic, and parasympathetic Hare (2017) underscored the complexity of the changes nervous systems and many of the skeletal and connective tissue undergone by humans and suggested that increased self-control components of the head. Since the structures and processes is the hallmark of human social and cognitive-affective evolution. associated with the neural crest are also related to the DS traits, We agree with this suggestion, which was based on Hare the hypothesis offers a unifying explanation. Genetic variation and Tomasello’s earlier proposal that a reduction in emotional in the regulatory genetic networks (GRNs) of these pathways reactivity was the pre-condition for human cognitive evolution have indeed been shown to characterize several domesticates (Hare and Tomasello, 2005). In the second part of this paper (Simões-Costa and Bronner, 2015; Theofanopoulou et al., 2017; we extend these suggestions and propose that engagement in Wilkins, 2019). Moreover, variation in neural crest genes, as music and in linguistic communication contributed significantly well as variations in genes expressed in cortical regions of to the evolution of cognitive and emotional plasticity in the genus the brain (including the neo-cortex) have been observed in Frontiers in Psychology | www.frontiersin.org 3 February 2020 | Volume 11 | Article 134 Shilton et al. Human Social Evolution: Self-Domestication or Self-Control? neurodevelopmental pathways that affect neural plasticity and 5 genes, 4 showed variations related to neural, behavioral and learning (see Theofanopoulou et al., 2017 for a comparison morphological characteristics related to the DS and to neural focusing on humans, and Wang et al., 2018 for gene expression crest pathways. Two genes seem particularly important: BRAF, in silver foxes). which affects learning and neural plasticity, and GRIK3, which In addition to variations in DNA base sequences, epigenetic affects both learning and cranial characteristics (Theofanopoulou variations may also be involved in the DS, since it was et al., 2017). However, as Theofanopoulou et al. (2017) point out, shown that the expression of the DNA methyltransferase genes the human data are based on somewhat contested compilations of differs between domesticated and control foxes (Herbeck et al., human genes showing adaptive sweeps. There are also important 2017). There is also evidence of significant and multiple data limitations that complicate interpretation: identification epigenetic differences between jungle fowl and domesticated of adaptive sweeps uncovers selective changes only in protein chickens: selection for fearful and non-fearful behavior in the coding genes, so the regulatory non-coding sequences, which jungle fowl for only five generations led to divergent DNA are probably of the greatest significance in the evolution of the methylation in 22 genomic regions in hypothalamus cells, some relevant regulatory networks, cannot be detected. This means of which were associated with neural functions and cellular both that the number of overlaps is likely to be underestimated, metabolic pathways relevant to the stress response (Bélteky and that the overlaps identified may not be specific to the DS. et al., 2018). A study of very recent domesticates of sea bass, We do not want to downplay the similarities between humans which show no genetic differences from wild fish, found that and domesticated foxes and dogs, nor do we question the these recent domesticates have epimutations (differences in involvement of neural crest mutations in the DS. We believe, patterns of DNA methylation) in various tissues, with about however, that these commonalities can be explained in a way one fifth of the persistent epimutations being in genes that are that is not committed to the HSD hypothesis. The neural crest expressed in embryonic structures, including the neural crest. pathways affect such a large suite of morphological, physiological Furthermore, the epimutated genes coincide with mutated genes and neural phenotypes that we expect that variations in them in established domesticates (Anastasiadi and Piferrer, 2019). It is will be targeted by social selection whenever there is strong therefore plausible that a comparative study of epigenetic (e.g., selection for altered emotional reactivity, mate selection, and methylation) differences among domesticates and humans will social cognition – that is in several social selective contexts. These reveal many more substantial similarities and differences than include selection for domestic, tame characteristics; selection gene-sequence differences, but at present there are only a few reducing stress-related behaviors involving the flight (fear) and comparative studies that address this question. fight (aggression) responses seen in small island populations of Table 1 presents a comparison between human traits that newly introduced animals; sexual selection and social selection correspond to traits that are said to characterize the DS in for pro-sociality in social mammal and bird groups; and social- (i) apes (bonobo compared to chimpanzee), (ii) dogs/wolves cultural selection for human cognition and affect. Sexual selection (feral and domestic dogs compared to the gray wolf), and (iii) and changes in diet and climate can also be underlain by foxes selected for tame behavior and wild, unselected ones. variations in developmental processes that involve the neural A detailed comparison of the traits associated with DS that crest, which lead to cranial modifications such as those seen in includes many other species of domesticates is presented and Neanderthals and Denisovans. discussed in Sánchez-Villagra et al. (2016). The table clearly shows that as well as similarities there The table shows some similarities between humans, bonobos, are also striking differences between humans and domesticates. dogs and tame silver foxes that conform to the characteristics of One important trait that humans do not share with most the DS. The levels of behavior-affecting hormones, most notably (80%) domesticates is reduced brain size – in fact, the opposite elevated levels of serotonin and oxytocin, which are correlated evolutionary trend is often considered as a hallmark of human with reduced emotional reactivity, are increased in humans, evolution. While reduced cranial capacity is in line with other dogs and tame foxes, with tame and wild foxes showing clear pedomorphic traits of domesticates, an increase in hominin differences with regard to the genes involved in these pathways brain size relative to body size has been correlated with changes (Wang et al., 2018). Another similarity is the juvenilization in diet resulting in higher energy intake, increased technical of morphology, the increase in morphological variation, and intelligence, and greater social complexity (Dunbar, 1998; Barton, the prolonged play period in humans and domesticates. These 2012; DeCasien et al., 2017). The retention of juvenile traits similarities are thought to reflect parallel evolution affecting in humans is associated with increased, rather than decreased, the same set of genetic regulatory networks in humans and brain size because the extended human juvenile period involves domesticates, in particular, though not exclusively, in genes a prolongation of neural growth and development (Gould, controlling developmental networks in which neural crest cells 1996). As noted by Spurway (1955) in her seminal paper on are involved. The data, however, are far from conclusive. When domestication, the reduced brain size of domesticates can be genes showing adaptive sweeps in modern humans (742 human explained as the result of selection for the breakdown of social genes) and domesticates (dog, cat, horse, taurine cattle; 691 genes structures. To encourage increased growth and reproduction in total) were compared, 41 were shown to be shared by both in domesticates, humans selected for the slackening of mating humans and one or more domesticated species (15 of the criteria, a shorter period of parental care, reproduction at earlier 41 were shared with the dog), and only 5 of the 41 were ages, unresponsiveness to group hierarchy, less discrimination in shared between humans and several domesticates. Of these the choice of food, less territorial defense, and so on. These traits Frontiers in Psychology | www.frontiersin.org 4 February 2020 | Volume 11 | Article 134 Frontiers in Psychology | www.frontiersin.org Shilton et al. TABLE 1 | Comparison between modern humans, apes, and domesticated and non-domesticated canids (dogs/wolves and tame/wild foxes). Species Modern humans Bonobo/chimpanzee Dog/wolf Domesticated silver evolved factors foxes/unselected foxes Morphology Morphological variability Highly variable Both species less variable than humans Dog breeds highly variable Tame foxes highly variable Mean brain volume (cm3 ) 1239.8; increase in human brain size 345.6/375.11 100.4/139.82 Negligible differences3 throughout most Homo evolution; 10% reduction during the last 10,000 years1 Cranium Evolved globularity emerged in Average bonobo endocranium is more Reduced facial length in dogs Changes in the tame strain are similar H. sapiens lineage4 rounded and less elongated than that compared to wolves6 to changes during dog’s early of the chimpanzee5 domestication7 Sexual dimorphism in body mass 1.161 1.35/1.311 Varies with size of dog breed; 1.27 in 1.2 in wild red fox9 ; no available data (male/female ratio) wolves8 on experimental groups Pigmentation Depigmentation of the sclera is unique Depigmentation of lips and tail tuffs in Depigmentation of coat in dogs12 Depigmentation of coat in tame foxes7 to humans10 bonobos11 Endocrinology Serotonin Receptor expression in the amygdala’s Receptor expression in amygdala’s High levels of variation in serotonin Higher levels of serotonin and serotonin receptor central and accessory basal nuclei is basal nuclei is significantly higher in receptor and transporter genes of the receptors in the brain of tame foxes16 5 significantly higher compared than in bonobos14 dog15 the chimpanzee and bonobo (Pan) genus13 Oxytocin receptor Genetic variation linked with social Fixed genetic variation in both species Genetic variation in dogs related to No available data behavior, empathy and autism17 ; compared with the polymorphisms differences in social behavior20 , was epigenetic changes in oxytocin receptor found in humans; five additional genetic not identified in wolves21 ; epigenetic gene associated with autism and polymorphisms found in chimpanzees differences among dogs associated Human Social Evolution: Self-Domestication or Self-Control? unemotional traits18 but not in bonobos or humans; their with differences in appeasing functional importance has not been behavior22 determined19 Prolactin Adult male prolactin levels rise in Prolactin levels in male chimpanzees Prolactin levels rise in all wolf pack No available data response to infant cries during spike throughout sexual members during pup-rearing period25 , fatherhood and during participation in development24 ; no available data on but are not correlated with paternal sexual acts23 bonobos behavior in male dogs26 February 2020 | Volume 11 | Article 134 Cortisol Cortisol levels are sensitive to Cortisol levels in bonobos, but not in Baseline cortisol levels in wolves Reduced cortisol levels in all tame environmental conditions and are chimpanzees, change during depend on dominance hierarchies29 , strains; highly reduced in pregnancy socially regulated during postnatal competition over food and show a whereas in dogs they are sensitive to and lactation31 development27 greater increase in response to social human caregivers’ personality and stressors28 lifestyle30 (Continued) Frontiers in Psychology | www.frontiersin.org Shilton et al. TABLE 1 | Continued Species Modern humans Bonobo/chimpanzee Dog/wolf Domesticated silver evolved factors foxes/unselected foxes Testosterone levels in males Increase during out-group competition; In male chimpanzees but not bonobos, Increased testosterone in wolves is Lower levels of plasma testosterone in decrease during in-group competition, there is pubertal and adulthood seasonal and tied to reproduction, tame foxes34 pair-bonding and co-sleeping with increases and level-changes during whereas most dog breeds continuously child23 competition over food32 maintain elevated levels 33 Variation in DNA and in gene Humans show many differences when The observed divergence of neural and Overlap among 15 genes that show 150 genes show different patterns of expression compared to apes; there are also social traits in chimpanzees and adaptive sweeps in both modern expression in lines of foxes selected for differences between anatomically bonobos has not been associated with humans and dogs (but not in wolves). aggression and tameness; allele modern humans and archaic humans; differences in protein patterns36 Of these 4 genes show characteristics frequencies at 176 gene loci, including archaic humans do not show adaptive associated with the DS35 genes associated with neural crest sweeps in genes related to DS functioning, are different between the characteristics35 aggressive and tame lines37 Emotional reactivity Aggression Compared to other primates, humans Both proactive and reactive aggression Both species show only rare and weak Tame foxes are very docile and show high propensity for proactive in chimpanzees; reduced proactive aggression among conspecifics40 non-aggressive compared to control aggression and low propensity for aggression and reduced severity of group41 reactive aggression38 reactive aggression in bonobos39 Cooperativeness (pro-sociality) Early onset of cooperative and Cooperation in chimpanzees is limited, Compared to wolves, dogs find it Tame foxes are more interested in 6 pro-social behavior42 and restricted to same-sex pairings difficult to cooperate with conspecifics interacting with humans than are wild whereas bonobos show broader 44 foxes41 cooperation43 Emotional control Humans can either inhibit, modulate or Bonobos are more socially tolerant than Dogs show a higher level of inhibitory Compared to wild foxes, tame foxes mobilize aggressive and other chimpanzees46 control than wolves with regard to show an increase in exploratory emotional responses, depending on humans, and can better suppress their behavior with age, coupled with a ecological conditions, norms etc. 45 immediate drives in favor of delayed substantial decrease in cortisol levels48 rewards47 Human Social Evolution: Self-Domestication or Self-Control? Life History Neotenous features Observed across various anatomical Bonobos have pedomorphic cranium, Dog breeds are underdeveloped to Tame foxes show a trend for faster traits of adult humans49 ; gene white tail-tufts that characterize juvenile varying degrees with regard to physical sexual maturation accompanied by expression indicates neural neoteny in chimpanzees, and play between adults and behavioral traits compared to retarded development of some somatic brain areas involved with social and is similar to adult-juvenile chimpanzee wolves52 traits7 cognitive skills50 play51 February 2020 | Volume 11 | Article 134 Length of female reproductive cycle 3.0553 4.8/5.2–6.654 0.45/0.755 0.5–1/17 (years) Length of juvenile period (years) 13.356 12/7.256 Juvenile period is similar in both Sexual species, but wolves’ sexual maturity maturation in tame foxes occurs a may depend on growth in size and on month earlier on average7 territoriality57 (Continued) Frontiers in Psychology | www.frontiersin.org Shilton et al. TABLE 1 | Continued Species Modern humans Bonobo/chimpanzee Dog/wolf Domesticated silver evolved factors foxes/unselected foxes Social behavior and cognition Developmental timing Long childhood; human brains show an Extended development and The period of socialization in domestic Sensitive period for social development extreme level of postpartum maternal-attachment in bonobo infants, dogs is longer than that observed in in tame foxes is extended from 45 days development, followed by an extended with delayed development of social wild or socialized wolves60 to 12 weeks or longer41 period for synaptic pruning that lasts behavior and cognition relative to until the mid-20’s58 chimpanzees59 Reproductive regulation Mating and child rearing are regulated Reproduction is determined by Reproduction in dogs is controlled by Reproduction of tame foxes controlled by cultural group norms61 ; concealed dominance hierarchies in humans; in wolves, the dominant pair by humans; in ancestral wild species, copulations occur regardless of male chimpanzees54 , whereas in bonobos breeds while other females are female reproduction depends on dominance and status62 male reproductive success is influenced reproductively suppressed, unless food population density, food supply, and by mother’s social status63 is abundant64 social status65 Paternal care Variable across-cultures and associated Similar patterns in both Pan species, Male wolves provide babysitting and Males in wild populations defend and with local ecologies and social but bonobo males engage in more play with infants, whereas provisioning provision pups69 ; no available data on environments66 playful activity with infants, including by male dogs is rare and limited68 experimental groups sociosexual play67 Alloparenting Modern humans in hunter-gatherer Bonobos show more allomaternal care Helpers in wolf packs attend to, and Females act as helpers in wild groups and other social organizations than chimpanzees70 provide for pups64 ; provisioning by populations71 ; no available data on practice alloparenting61 non-maternal female dogs is rare57 experimental groups Infanticide Relatively rare in hunter-gatherer groups Male bonobos assault, but do not Major mechanism used by dominant Not reported for experimental groups; and usually initiated by the mother, attempt to kill, weaned offspring; male feral dog females to suppress in farm conditions, infanticide by vixens when resources are limited or the infant chimpanzees commit infanticide72 reproduction of subordinates; dominant is correlated with more tense and 7 is deformed61 female wolves aggressively prevent insecure behavior74 copulation by subordinates73 Communication and information Polymodal and variable Compared to chimpanzees, bonobos Wolves have better skills with regard to Tame pups more skilled in responding sharing communication; extensive information are more sensitive to human gaze gaze following and imitation vis á vis to human communicative gestures; sharing and early manifestation of direction, use indexical cues in the conspecifics, but only dogs gaze at novel displays of tail wagging, communicative intents and skills75 vegetation when foraging in small human faces for assistance77 ; both submissive posturing and barking in groups, and acquire better linguistic follow human pointing but it appears adult tame foxes79 skills in experimental settings76 earlier in dogs than in wolves78 Human Social Evolution: Self-Domestication or Self-Control? Play Advanced pretend play parallels During juvenile period play-fighting Juvenile play behavior is maintained in Play during adulthood is more common language development80 ; social and becomes longer and more cooperative adult dogs83 in tame foxes84 pretend play in hunter-gatherers are in bonobos, whereas in chimpanzees it used to counteract tendencies toward is more competitive82 dominance81 1 MacLeod et al., 2003; Robson and Wood, 2008; Bednarik, 2014; 2 Comparison taken from dog breed and wolf with similar body masses; see Smith et al., 2018; the variability between different strains should, however, February 2020 | Volume 11 | Article 134 be noted; Lord et al., 2019; 3 Trut et al., 1991 (quoted in Wilkins et al., 2014); 4 Neubauer et al., 2018; 5 Durrleman et al., 2012; 6 Franciscus et al., 2013 (quoted in Cieri et al., 2014); 7 Trut et al., 2004; 8 According to Frynta et al., 2012, Sexual size dimorphism in large breeds is comparable to SSD of wolf; becomes smaller with decreasing body size (see also Moehlman and Hofer, 1997); 9 Voigt, 1987; 10 Tomasello et al., 2007; 11 Kano, 1992; 12 Coppinger and Coppinger, 2001; 13 Lew et al., 2019; 14 Stimpson et al., 2016; 15 van den Berg et al., 2005; 16 Popova et al., 1991; 17 Wu et al., 2005, 2012; Tost et al., 2010; 18 Kumsta et al., 2013; 19 Staes et al., 2014; 20 Kis et al., 2014; 21 Oliva et al., 2016; Bence et al., 2017; 22 Cimarelli et al., 2017; 23 Gray et al., 2017; 24 Kondo et al., 2000; 25 Kreeger et al., 1991; Asa, 1997; 26 Corrada et al., 2003; 27 Gunnar and Donzella, 2002; Flinn et al., 2011; 28 Wobber et al., 2010a; 29 Sands and Creel, 2004; 30 Schöberl et al., 2017; 31 Trut et al., 2009; 32 Wobber et al., 2010a, 2013; 33 Asa, 1997; 34 Osadchuk and Shurkalova, 1992; 35 Theofanopoulou et al., 2017; 36 Staes et al., 2019; 37 Wang et al., 2018; 38 Wrangham, 2018; 39 Surbeck et al., 2011; Furuichi, 2011; 40 Range et al., 2015; 41 Trut, 1999; 42 Tomasello, 2009; 43 Surbeck et al., 2017; 44 Feddersen-Petersen, 2007; 45 Hare, 2007; Jablonka et al., 2012; 46 Tan and Hare, 2017; Hare et al., 2007; 47 Gácsi et al., 2009; Marshall-Pescini et al., 2015; 48 Trut, 2001; 49 Skulachev et al., 2017; 50 Bufill et al., 2011; 51 Wrangham, 2002; Palagi, 2006; Lieberman et al., 2007; 52 Udell et al., 2010; 53 Key, 2000; 54 Gruber and Clay, 2016; 55 Jöchle, 1997; 56 Jones et al., 2009; 57 Lord et al., 2013; 58 Zollikofer and Ponce de León, 2010; Casey, 2015; 59 de Lathouwers and Van Elsacker, 2006; Wobber et al., 2010b; 60 Coppinger and Coppinger, 2001; Gácsi et al., 2009; 61 Hrdy, 2009; 62 Ben-Mocha et al., 2018; 63 Surbeck et al., 2019; 64 Montgomery et al., 2018; 65 Macdonald, 1980; 66 Fernandez-Duque et al., 2009; 67 Enomoto, 1990; 68 Kleiman and Malcolm, 1981; Pal, 2005; 69 Macdonald, 1979; 70 Kano, 1992; Furuichi, 2011; 71 Moehlman and Hofer, 1997; 72 Gottfried et al., 2019; 73 Corbett, 1988; 74 Braastad, 1987; Braastad and Bakken, 1993; 75 Tomasello, 2008; 76 Savage-Rumbaugh et al., 1996; Gillespie-Lynch et al., 2014; MacLean and Hare, 2015; 77 Range and Virányi, 2013, 2014; 78 Gácsi et al., 2009; 79 Trut, 1999; Hare et al., 2005; 80 Lewis et al., 2000; Hughes, 2010; 81 Gray, 2009; 82 Palagi, 2006; 83 Goodwin et al., 1997; 84 Trut, 2001; Trut et al., 2004, 2009. Shilton et al. Human Social Evolution: Self-Domestication or Self-Control? are often associated with diminished perceptual acuity and lead (responsive, target-inconsistent, high arousal). However, if self- to a social structure that is impoverished relative to that of their domestication is defined as selection against reactive aggression, wild ancestors, and that is not self-sustaining in the absence of many social mammals, including meerkats and mole rats, should human provisioning (Avital and Jablonka, 2000). be included in the self-domestication category. Furthermore, There is evidence for a reduction in endocranial volume when violence occurs, reactive and proactive aggression are in humans in the past 40,000 years and especially the last often mixed (Allen and Anderson, 2017). Although the decision- 10,000 years (Bednarik, 2014), and it has been suggested that this mechanisms initiating proactive violence are claimed to be points to selection for pro-sociality. Alternatively, the reduction neurally distinct (Blair, 2016), levels of arousal may change may be related to the decrease in overall size, to increased during the act itself – a “coldly” premeditated act of violence sedentism, more reliable food availability and greater safety can be carried out in a state of high arousal. The lower rates of (Hare, 2017; Thomas and Kirby, 2018). It is, however, important within-group violence among humans compared to other great to note that most morphological and behavioral traits that apes (Wrangham, 2018) may in part be a result of violence being are associated with the DS in anatomically modern humans better controlled, both emotionally and socially, rather than the (e.g., increased social cooperation, neoteny, changes in cranial propensity for reactive aggression being simply reduced. morphology, reduced sexual dimorphism) are shared by archaic A third crucial difference between humans and domesticates humans, and so preceded the period in which HSD is supposed relates to the absence, in the case of humans, of subordination to have occurred. to another species, and an increased dependence on other group There are certainly differences in human morphology as well members with regards to foraging, hunting and alloparenting. as in genes when Neanderthals, Denisovans and anatomically Consider the differences in social ecology between wolves and modern humans are compared (Hare, 2017), and some changes dogs: dogs feed primarily on human waste, whereas wolves rely are in genes affecting pathways in which neural crest cells are mostly on group hunting; dog pups are raised mostly by their involved and that lead to changes in the cranium. In a recent mothers (and, in the case of pet dogs, by humans as well), study, Zanlella et al. (2019) showed that there were changes while wolf pups are raised by the entire pack (Marshall-Pescini in the chromatin remodeler BAZ1B in neural crest stem cells et al., 2017a). Recent experiments have clarified the impact of the during the evolution of anatomically modern humans. They different social ecologies on behavior, showing, for example, that found that large-effect mutations in the regulatory region of wolves have greater pro-social tendencies toward pack members this gene lead to DS-like cranial and neural disease-related than do dogs (Dale et al., 2019), that they cooperate better variation in modern humans. More subtle genetic variations with conspecifics than dogs (Marshall-Pescini et al., 2017b), and in the regulatory regions in this gene differ between modern that although wolves and dogs are both capable of cooperating humans, Neanderthals and Denisovans and may be related to with familiar humans, dogs tend to take on more submissive the cranial differences among them. The reduction in average roles (Range et al., 2019). Like wolves, throughout much of brow ridge projection and shortening of the upper facial skeleton their evolutionary history humans relied on group-coordinated from the Middle Pleistocene to recent times has been linked by hunting and participated in alloparenting. Until the onset of Cieri et al. (2014) to a reduction in aggression and increased agriculture, they did not rely on living alongside and being social tolerance. However, the context in which these cranial provisioned by another species, but rather on their intra-group and behavioral changes were selected is not clear, and it pro-social tendencies, which allowed them to cooperate with one has not been established that they are the result of selection another. In other words, humans’ social ecology did not require against aggression rather than, for example, the result of sexual docility toward a domesticator, but rather emotional plasticity selection, or changes in diet or climate. Finally, the data showing that can lead to condition-dependent pro-social behavior among adaptive sweeps in modern humans but not in Neanderthals are group members, as well as highly aggressive behavior, mainly very limited (Theofanopoulou et al., 2017). Nevertheless, it is toward individuals belonging to other social groups. In many possible that, as Sánchez-Villagra et al. (2016) have suggested, ways, human social evolution is more similar to that of wolves once humans had adopted a more sedentary life style, about than to that of dogs.2 15,000 years ago, there was selection for decreased vigilance Finally, unlike animal domesticates and bonobos, humans can similar to that observed in animals that migrate to small create cumulative cultures (Mesoudi, 2011; Laland, 2017). The islands devoid of predators, which often leads to reduced brain cultural learning involved depends on enhanced attention to the size. This may partially account for the recent reduction in actions of others, and this may explain the depigmentation of human brain size. the sclera in humans, which Tomasello et al. (2007) suggested A second important difference between humans and most had evolved to facilitate gaze-following. Uniquely human forms other domesticates is the types of aggression they display. While of communication, engagement, and material technologies point humans can be docile and patient with one another in some to a cognitive and emotional profile that goes well beyond the situations, they can also be extraordinarily violent at others. Wrangham (2018) distinguished between reactive and proactive 2 The observation that modern humans and wolves do not share variations in aggression in order to clarify this apparent oddity. Humans, recently selected human genes (Theofanopoulou et al., 2017) is not surprising given the recent origin of these genes in humans and the far more ancient origin he suggests, share with chimpanzees a high propensity for of wolves, which seem to have diverged from the highly social and cooperative proactive aggression (purposeful, target-consistent, low arousal), coyotes 1.5 million years ago and apparently have not undergone intense social and share with bonobos a low propensity for reactive aggression evolution since then. Frontiers in Psychology | www.frontiersin.org 8 February 2020 | Volume 11 | Article 134 Shilton et al. Human Social Evolution: Self-Domestication or Self-Control? reduced aggression shown in bonobos. The increased emotional Advocates of HSD may argue that selection for emotional plasticity of humans allows the modulation of emotional control and plasticity is not entirely distinct from selection reactions on the basis of social situations and expectations: a against reactive aggression. However, the former is expected norm-sensitive emotional control. to be fundamental to the evolution of social motivation in We believe that incorporating selection for emotional control many highly social animals and does not necessarily lead to a and plasticity can better account for human behavior, affect decrease in overall aggression; it is expected to lead to increased and cognition, than selection for reduced aggression or pro- aggression in some social contexts and to increased cooperative sociality alone. It can also explain why some traits are shared with behaviors in others – patterns of behavior than are seen in domesticates, and others are not. The HPA axis, which affects fear wolves and social mongooses. Since selection for emotional and flight reactions in all vertebrates, is also involved in learning control is likely to involve both the early and late developmental and memory (Sandi and Pinelo-Nava, 2007), so it is likely that pathways that underlie neural development, and since changes mutations and epimutations in this system, and even more so in the early pathways have multiple pleiotropic effects, it is to be in its regulation by higher cortical regions (which are involved expected that the behavioral, social and morphological evolution in executive control) will be found in social mammals including of social vertebrates will be affected by selection for changes bonobos and humans. in these pathways. Mutations affecting neural crest cells are Selection for emotional control could account for the therefore expected to be associated with several different aspects continued increase rather than decrease in brain size for most of social evolution, not just with domestication. We therefore of human evolution. A study of self-control in 36 species of do not find the notion of human self-domestication useful, and mammals and birds found higher levels of control to be best believe that the partial analogy with domesticates focuses too predicted by absolute brain volume, while also being correlated much on the reduction of reactive aggression and too little on with dietary breadth in primates (MacLean et al., 2014). There social organization. With respect to cooperation, selection for are several brain regions (subcortical, cortical and neocortical) emotional control in hominins was essential for alloparental care, implicated in emotional control. These include the cerebellum, cooperative hunting and foraging, and the improvement of lithic which is more broadly involved with attentional control and technologies, all of which had advantages that compensated for social skill-sets Schmahmann (2019), and prefrontal cortical the higher metabolic costs involved with the increase in brain regions that interact with the anterior cingulate cortex to form size and connectivity that is required for improved emotional the executive attention network, which is critical for supporting and executive control. With respect to aggression, selection for the development of emotional regulation (Posner and Fan, emotional control better explains the extraordinary range of 2008). Braunstein et al. (2017) pointed to four control systems human violence: humans are far less impulsive than other apes, that have been strongly implicated in implicit and explicit can better control their aggression in some social conditions, regulation of the emotions: the dorso-lateral prefrontal cortex and are able to amplify their aggression in other conditions, (dlPFC), which is involved in subjective awareness, cognitive leading to extreme cruelty. As we argue below the social-cognitive appraisal and strategic control (Lapate, 2018); the ventrolateral emotional profile of humans, whose underlying developmental prefrontal cortex (vlPFC), which is implicated in the selection pathways lead to the emergence of traits that partially overlap of goals; and the dorsal anterior cingulate cortex (dACC) and those that characterize the DS, is the consequence of selection dorsal medial prefrontal cortex (dmPFC), which are involved for greatly enhanced emotional control and plasticity, which were in monitoring the compatibility or conflict between intended linked with the culture-guided evolution of human capacities. and actual behavioral outcomes and one’s emotional states. In addition, the posterior parietal cortex (PPC) interacts with the dlPFC, exerts top–down, volitional control over attention and HUMAN SOCIAL EVOLUTION working memory processes, and supports perspective taking and spatial processing. Importantly, the PPC is strongly recruited Social Emotions and Emotional Plasticity during reappraisal that involves emotional distancing, suggesting in Pre-linguistic Humans that it regulates perceptions of an emotional stimulus’ relevance Early human evolution was marked by three novel and or proximity (Silvers and Moreira, 2019). A recent phylogenetic increasingly important behaviors: the production of stone tools analysis has found that disproportional increases in the volumes (Laland, 2017), the consumption of meat and marrow (Ferraro of the neocortex and the cerebellum occurred, respectively, at the et al., 2013; Thompson et al., 2019), and, somewhat later, the origins of haplorrhines and of the apes, and not predominantly emergence of alloparenting (Hrdy, 2009). All bear an interesting during the rapid and directional brain evolution observed in relation to emotional control, pro-sociality and communication. hominins. However, the general increase in brain size in humans The use of sharp-edged stones for flesh removal and marrow means that these emotion-related brain regions are nevertheless extraction is found as early as 3.4 Mya (McPherron et al., 2010). larger than expected for a primate of similar body mass (Miller Lithic traditions increased in complexity over time, demanding et al., 2019). We therefore suggest that the genetic and epigenetic that individuals not only have the ability to comprehend long, networks underlying the development of these neocortical hierarchical sequences, but also have the patience and tenacity to regions were major targets of selection during human social work through them (Pargeter et al., 2019). A knapper attempting evolution, and that reduced aggression might be a symptom of to produce a complex tool (e.g., an Acheulian biface) has to keep broader social plasticity and more nuanced social emotions. various sub-goals constantly in mind, and to decide the manner Frontiers in Psychology | www.frontiersin.org 9 February 2020 | Volume 11 | Article 134 Shilton et al. Human Social Evolution: Self-Domestication or Self-Control? in which he should proceed on the basis of the result of each for these skills involved selection for the emotional disposition flake removal. Both emotional and executive control are therefore and communicative abilities that they require. necessary for the production of a complex stone tool (Stout et al., Emotional control and pro-sociality were also likely to 2015). As for the social transmission of the skills and knowledge have been substantially influenced by alloparenting – the care involved, ethnographic and experimental evidence both suggest of young by individuals other than their mother. Extensive that it requires flexible and creative mimetic communication and alloparenting is universal in human societies (Sear and Mace, a high degree of pro-social motivation (Shilton, 2019). Experts 2008), and among the great apes unique to humans (Hrdy, and novices need to spend plenty of time together, to share a 2009). This practice has a proven impact on several other common goal of successful tool production, and to use their factors distinguishing human evolution and psychology, such gestural communication for the purpose of teaching (Laland, as intersubjective abilities, proactive pro-sociality, brain size 2017). Through joint knapping interactions, novices learn to see and altriciality (Hrdy, 2009, 2016; Isler and van Schaik, 2012; the core as the expert does, and become aware of the various Burkart et al., 2014). Alloparenting may have emerged quite visual cues that guide the next striking action (e.g., striking early in the hominin line because (i) cooperative breeding is platforms, step fractures and grain quality). In other words, especially likely to evolve in ecologically unstable environments experts and novices need to establish a common ground based on (Hrdy, 2016); (ii) Australopithecus females were estimated to communicative signals, which many researchers consider to be have given birth to babies who were more than 5% of their the starting point of human-specific communication (Tomasello, adult body mass compared to 3% in chimpanzees and 6% in 2008). The benefits of better stone tools would therefore have modern humans (DeSilva, 2011); and (iii) there is evidence promoted emotional control and plasticity, both for patient tool for extended altriciality in Homo erectus (Cofran and DeSilva, production, and to facilitate the kind of cooperative interactions 2015). Strong trust relationships have to be formed in order skill transmission required. for mothers to allow others access to their young: chimpanzee Hunting and foraging skills also became increasingly more mothers, for example, are highly protective. Alloparenting may advanced during human evolution and, like tool-making skills, have developed in ecological conditions that kept mothers in relied on cooperative activity and social learning. Even the close proximity to their familiar and trusted matrilineal kin. more conservative scholars in the hunting vs. scavenging debate Allowing males and less related kin to provision and provide care agree that by 1.5–1.0 Mya hunting was a regular component of is indicative of very high levels of group trust and tolerance. hominin subsistence (Domínguez-Rodrigo and Pickering, 2017). The impact of alloparenting on human psychology is far- The regular consumption of highly nutritious meat, fat and reaching, both for caregivers and infants. Fathers show increased marrow answered the metabolic demands of larger brains. Since oxytocin and decreased testosterone levels compared to non- brain size is hypothesized to be related to self-control (MacLean fathers (Rilling and Mascaro, 2017), and caregivers’ parenting et al., 2014), and since such control would improve the motor behavior is correlated with distinct brain activation patterns, learning and social learning abilities of hominins (which, in turn, including circuitries that support, among other things, emotional require even more self-control), a positive feedback loop might empathy, comprehension of others’ intentions and feelings, have been initiated at some point in human evolutionary history reward and motivation, and anxiety (Glasper et al., 2019). (see also Hare, 2017). These appear to result in structural changes to the brain during A large item of prey that was consumed by many individuals parenting, such as an increase in both mothers and fathers required communicating about it, moving it, guarding it, in gray matter volume in the hypothalamus, amygdala and gathering around it, and eating it together without too striatum (Kim et al., 2014; Kim, 2016). The prolonged brain many squabbles. It has been suggested that the hunting of maturation of human infants means a prolonged influence megafauna, evident since approximately 1.7 Mya, indicates of postnatal environmental and social interactions on neural a concurrent and mutually reinforcing increase in group connectivity (Sakai et al., 2011; Miller et al., 2012). Compared to size and increased cooperative practices (Domínguez-Rodrigo chimpanzees, human infants also show a more rapid increase in and Pickering, 2017). The nature of plant consumption is white matter volume in the prefrontal cortex, a difference that is more difficult to ascertain archaeologically, but studies in the probably related to social interactions (Sakai et al., 2011). Hrdy ∼800,000 years old Acheulian site of Gesher Benot Ya’aqov (2016) contrasts this with the much slower maturation of other provide evidence for the consumption of diverse plant species, brain areas, especially those related to motor coordination and mainly USOs (underground storage organs) and nuts. The mobility, and suggests that it can be partially explained by the extraction and preparation of these require complex procedures greater importance for human infants of assessing the intentions (Melamed et al., 2016) and, as in the case of tool-making, and commitment levels of caregivers and of soliciting care. hunting and foraging skills, they were executed and socially All of the cooperative behaviors we have described both transmitted through collaborative efforts in which visual cues increased the adaptive value of emotional control and in the environment needed to be mutually identified and contributed to the extended pro-sociality of hominins. A life- responded to. USOs, for example, sometimes leave just small style based on toolmaking, hunting, foraging, and alloparenting traces above ground, and digging implements are needed to meant that early hominins were uniquely codependent and other- retrieve the deeper ones (Thomas, 2006). Tracking, which is regarding compared to other great apes. The growing importance essential for hunting, involves recognizing spoors to infer the of cooperative alliances demanded a greater sensitivity to the prey’s location and physical state (Liebenberg, 2013). Selection expectations of others, which led to the emergence of social Frontiers in Psychology | www.frontiersin.org 10 February 2020 | Volume 11 | Article 134 Shilton et al. Human Social Evolution: Self-Domestication or Self-Control? emotions like embarrassment, shame, guilt and pride, all signaled storage organs. Mimetic communication would have enabled by the uniquely human blush (Crozier, 2006). The emergence hominins to coordinate the way they perceived and engaged with of most of these self-evaluating emotions in development is the environment they experienced together – to reduce what thought to occur in the second phase of emotion regulation, Dor (2015) calls “experiential gaps,” the inescapable differences during which children in their third to sixth year of life become in the way different individuals experience their surroundings. capable of an intrapersonal regulation of their emotional actions Mimetic communication, along with social motivation and and reflections (Holodynski and Friedlmeier, 2006). theory of mind, can enable ensuing processes of what Dor calls “experiential mutual identification,” in which hominins direct the attention of their counterparts to elements of interest in Mimesis, Musical Engagement and their immediate environment, attempt to share their attitudes Emotional Control toward them, and construct a mutually-identified collective The method most likely to accommodate hominins’ new view of the environment. This results in the creation of an cooperative behaviors is mimetic communication, or mimesis. intersubjective common ground, enabling flexible coordination Described initially by Donald (1991), the tool-kit of mimesis within the here-and-now. By continually engaging in experiential includes manual and bodily gestures (including the all-important mutual identification, hominins could transmit the diverse gesture of pointing), facial expressions and vocalizations, knowledge and skills they were continually acquiring. Hominin mimicking, pantomime, and early musicking. The entire tool- codependence would create a new evolutionary spiral in kit involves multiple modalities, and represents the goals of which new cooperative behaviors would continuously require individuals and collectives but, unlike language, it is not arbitrary upgrades to the toolkit of mimetic communication, the upgrades and compositional, and is functionally limited to the here- would enable new cooperative behaviors, which would increase and-now of the communication event. It allows for explicit codependence, and so on – an ever extending spiral of positive cooperation at all the relevant levels, from information exchange, feedbacks, one in which humans may be said to be caught up in through explicit teaching of manual skills (in tool-making, to this very day. hunting etc.), all the way to the maintenance of social life We believe that musicking played a crucial role in this process. (through both micro-interactions and collective rituals). The Much has been written on the importance of music in human implications of mimetic communication for the vocal modality evolution, and we can address this literature only briefly (for a in particular are far-reaching. Better executive control would more thorough discussion, see Cross, 2007). It was discussed by have improved vocal learning abilities in humans, increasing the Darwin (1871), who suggested musical behavior, grounded in repertoire of vocalizations and making their use more flexible. the vocal expression of emotions and operating in the context An additional factor affecting vocal flexibility is the relaxation of mating and sexual selection, was a precursor of language. of selection. Studies comparing the birdsong of white rumped After several decades of relative silence on the subject, interest munia to that of its domesticated strain, the Bengalese finch, revived in the 1990s, and was reinvigorated by Pinker’s (1997) show that relaxed selective conditions enable vocal learning provocative and arguably ethnocentric claim that music is an that is less constrained than that observed in the wild and “auditory cheesecake.” This claim, which was based mainly on eventually leads to more complex songs (Okanoya, 2015). This Western habits of passive music consumption, ignored the fact implies that, in addition to the benefits of improved executive that in most of human history and for most human cultures control, extended juvenile periods and more buffered human musicking was and remains a participatory and highly social habitats may have also increased the variability and complexity activity. Mithen (2006), who contributed substantially to the of human vocal communication. A flexible and extensive use of discussion, described musicality as part of the mimetic toolkit and vocal communication in the lives of hominins would have set envisioned a role for it in prehistoric lives. the stage for the elaboration of the vocal modality in musical We agree that musicking is mimetic in essence, but also think engagement and language. that some of its unique qualities merit a separate discussion We agree with Donald that mimetic communication and and special recognition. One such quality is its anticipatory mimetic cognition are sufficient to account for the undoubtedly nature. Music contains tonal and rhythmic elements which are rich, yet in other senses limited, Acheulian cultural complex meant to trigger an embodied anticipation of its continuation. (Shilton, 2017). Although the skills and knowledge required This anticipation relies mainly on rhythmic entrainment and for producing Acheulian stone tools and hunting megafauna repetition. Rhythmic entrainment, or beat-based timing, differs are impressive, their social transmission is dependent mostly from interval-based timing (which has been documented for on cooperative interactions in the here-and-now, and do not some primates) in that movements anticipate the onset of the require the extended functionality of language (described in musical beat, rather than merely corresponding roughly to the the following section). As previously mentioned, the social musical beat period (Merchant and Honing, 2014). Repetition transmission of both tool-making and foraging skills requires is a universal quality of music (Nettl, 1983) and can even that skilled individuals share with novices their way of looking endow speech and random tone sequences with a perceived at and responding to the environment. Recognizing visual cues sense of musicality (Deutsch et al., 2011; Margulis and Simchy- is essential for skills such as finding suitable raw materials for Gross, 2016). Most importantly, repetition triggers more forcibly tools, identifying a good striking platform on a core, spotting the anticipation of the next beat or sound. By supplying an the spoors of prey and predators, and locating underground anticipatory tonal and rhythmic foundation for play interactions Frontiers in Psychology | www.frontiersin.org 11 February 2020 | Volume 11 | Article 134 Shilton et al. Human Social Evolution: Self-Domestication or Self-Control? and group mimetic acts, musicking substantially extends the control, pro-social motivation, as well as good social skills and potential for creating emotional synchrony and rituals of social empathy (Keller et al., 2014; Novembre et al., 2019). Musical bonding. Musicking is different from other forms of mimetic engagement could initially have evolved as a particularly communication (as well as from language) because it establishes engaging form of play and social grooming that was based on simultaneous rather than asynchronous interactions (Cross, synchronous tapping, vocalizations and movements. Based on 2016), as well as carrying highly embodied and ambivalent the ethnography of contemporary African hunter-gatherers, meanings (Langer, 1957; Cross and Tolbert, 2016). Musicking, Lewis (personal communication) suggests that the first critical unlike language, enables big groups to express themselves role of musical engagement was in deterring nocturnal predators. together; and while language excels at displacement, musicking In time, musical engagement began to play a significant is unusually potent in synchronizing the embodied experiences role in many other aspects of social life. Music’s unique of participants, and with it, their arousal and emotional states. properties make it the only form of communication which We consequently suggest that musicking is a technology allows several individuals to express themselves simultaneously of engagement: communicative messages that are designed to as a single group, thus contributing substantially to social strongly compel the receiver to emulate their rhythm and bonding, acculturation and the creation of group identity tonality. Music perception reflects this anticipatory nature of (Lewis, 2016). These contributions were probably adaptive musicking by being highly embodied, predictive and, in a sense, at both the group level (more cohesive groups were more inherently active. Beat perception, for example, is defined by the successful than less cohesive ones) and at the individual level ability to predict the next beat, and engages motor areas of the (individuals who participate in musicking were trusted more brain regardless of any overt movement (Patel and Iversen, 2014). than those who did not). Listening to melodies similarly involves making involuntary Studies on the neurochemistry of music point to its influence predictions about their continuation (Margulis, 2005). Since there on factors related to reducing stress and enhancing social are non-arbitrary relationships between tempo, pitch, timbre bonding (Chanda and Levitin, 2013). A meta-analysis of music and certain emotional states (Juslin and Laukka, 2003), and therapy studies concluded that it is effective in reducing since emotional contagion based on automatic bodily mimicry pain and anxiety (Kühlmann et al., 2018), something which results in emotional convergence (Hatfield et al., 1994), musical appears to be related to reducing levels of cortisol and ACTH synchrony necessarily translates into emotional synchrony. This (adrenocorticotropic hormone). Listening to soothing music was makes musical engagement a potent tool for emotionally uniting found to increase oxytocin levels during post-surgery bed rest humans and for enhancing group cohesion and trust, which is (Nilsson, 2009), and Kreutz (2014) found that, compared to particularly important during cooperative activities like hunting dyadic chatting, group singing increased oxytocin levels, as well big animals or fighting with rival groups. As Darwin (1871) noted, as significantly enhancing perceived psychological well-being. social cohesion and solidarity would have a strong selective value The pleasure derived from listening to music appears to be at the group level. modulated by dopaminergic reward systems (Ferreri et al., 2019), While several species are capable of rhythmic entrainment, and a PET study documented dopamine release in striatal regions so far only parrots have been shown to respond to music during both peak arousal and in anticipation of it (Salimpoor spontaneously and with diverse movements (Keehn et al., 2019). et al., 2011). Tarr et al. (2014) also mention the likely influence This has led Keehn et al. (2019) to suggest five traits that are of musical engagement on the endogenous opioid system, necessary for rhythmic entrainment: complex vocal learning, with exertion-related release of endorphins during musicking a capacity for imitation, an ability to learn complex action promoting social bonding. sequences, a tendency to form social bonds, and attentiveness to Whatever the neurochemical mechanism, the influence of communicative movements. Wilson and Cook (2016) argue that music on social bonding is well documented. Several studies what distinguishes parrots from other animals are two critical have shown that movement synchrony alone promotes pro- factors: social motivation and voluntary motor control. If so, sociality (Cirelli, 2018), with some finding positive effects on peer it suggests that selection for executive control and pro-sociality cooperation (e.g., Rabinowitch and Meltzoff, 2017). Reviewing would have made hominins responsive to rhythmic stimuli. But the interpersonal effects of movement synchrony, Cross et al. whereas parrots spontaneously respond to music with diverse (2019) highlight deindividuation, where the sense of self is movements, they do not make music. For hominins to create and diluted and one comes to feel less separate from others. The develop this new form of communication, two other abilities were general effects of movement synchrony therefore provide the needed. First, proficiency in mimetic communication, which basis for collective emotions, which are intensified by the enables the flexible and intentional production of iconic bodily wide range of feelings embodied and induced through musical signals in a cooperative context; and second, the ability to engagement, and by the creation of musical traditions unique to create and sustain cumulative cultures, thus forming increasingly specific social groups. complex traditions of rhythmic and tonal group engagement. Because musical interactions are based on the synchrony Although it is difficult to establish whether musical of embodied experiences, they can be a powerful tool for engagement was directly or indirectly selected when it first uniting a group in a single, socially mandated “mood,” be it appeared, it seems that the ability to engage in musical calm, joy, grief, anger (directed at another group) or ecstasy. interactions is strongly related to other traits that are likely Musicking continued to diversify alongside the emergence of to provide fitness benefits, such as improved vocal and motor language and more complex social structures, being utilized Frontiers in Psychology | www.frontiersin.org 12 February 2020 | Volume 11 | Article 134 Shilton et al. Human Social Evolution: Self-Domestication or Self-Control? for a variety of social functions. Cross-culturally, musical collective effort of experiential mutual-identification that has engagement appears in broadly similar social practices, already been established in the mimetic period. The crucial notably dance, ritual, religious ceremonies, processions, upgrade is that every point of experiential mutual-identification mourning, healing and infant care (Mehr et al., 2019). is symbolically marked by a mutually identified sign – lexical, These diverse utilizations of musical communication in morphological or syntactic. This symbolic signification allows contexts that are critical for harmonious social life confirm speakers to translate what they want to communicate into its importance as a tool for modulating the emotions formally arranged symbolic codes and transmit the codes involved in collective activities and in responding to social to their interlocutors. The interlocutors analyze the codes, demands. Musical engagement, made possible by a selection retrieve from their memories the relevant experiences that for emotional and executive control and pro-sociality, are associated with the signs, and construct their own became a potent tool for promoting further pro-sociality, imagined experiences. improving executive control, and inducing socially prescribed Language thus revolutionized hominin life. For the first emotional states. time, individuals could begin to take into account things they themselves have never experienced, things they only heard Language and Emotional Control about. Communities could begin to explicitly negotiate collective Mimesis could maintain the various cooperative behaviors we conceptualizations of the world, norms of social conduct, and have described to a level that was probably sufficient for more plans for future collaborative activities, all of which in the than a million and half years. However, as codependency mimetic period could only be implicitly and indirectly negotiated in hominin groups increased, it gradually required a system through perceptible behavior (Dor, 2019). Stories (both factual of communication that could break the boundaries of the and fictional) became a crucial mode of information transfer, here-and-now of the communication event, and allow the identity synchronization and negotiation of social behavior and communication of experiences, norms, skills and worldviews norms (Smith et al., 2017; Boyd, 2018), and conversations allowed beyond what was possible through mimesis. The new system explicit complaints and criticism (Wiessner, 2014). of communication was language. It was built on the basis of As we see it, once in place, the evolution of language must have mimesis, with the first prototypes of language appearing around entailed profound alterations to hominins’ emotional profiles a half a million years ago (Dediu and Levinson, 2013), and and in their capacities for emotional control. At the most continued to evolve in a process of culturally driven, gene- foundational level, the emergence of a linguistic communication culture coevolution until it acquired its fully fledged form technology that transcends individuals’ immediate experiences (Dor and Jablonka, 2014). of the here-and-now required them to develop increasing levels All the tools of communication that we share with our ape of trust and the control of affect-related drives and triggers relatives, and the toolkit of mimesis that is uniquely human, of action. When told about things beyond what they could share a basic functional strategy: they enable communicators perceive by themselves, whether dangerous or beneficial to them, to target their interlocutors’ senses, and present them with individuals had to imagine those things while either inhibiting, communicative materials to perceive. As Dor (2015) shows, modulating or mobilizing the appropriate emotional response. the functional uniqueness of language lies in the fact that They also had to face new problems: they needed to reduce the language abandons this strategy – it allows speakers to dangers of false memories and distinguish between what they communicate directly with their interlocutors’ imaginations. It recalled on the basis of their own experiences and what they permits speakers to intentionally and systematically instruct their recalled on the basis of stories told by others. These dynamics interlocutors in the process of imagining the intended meaning led, among other things, to the evolution of the human-specific instead of experiencing it. Speakers provide interlocutors with phenomenon of distinguishing between thought and feeling a code, a structured list of the basic co-ordinates of their (Jablonka et al., 2012). experience, which the interlocutors then use as a scaffold for The instruction of imagination, which is what language their own imagination. Following the code, the interlocutors enables, has another problematic aspect: it revolutionized raise past experiences from their own memories, and then deception and enabled the uniquely human phenomenon of reconstruct and recombine them to produce novel, imagined the lie. Many evolutionary-oriented scholars argue that this experiences. Language is thus the only system that allows new capacity for lying was a major obstacle to the emergence the communication of meanings that cannot be presented and stabilization of language itself (Boyd et al., 2003; Knight, to the senses. This includes experiences from the past and 2007; Mercier and Sperber, 2011; Tomasello, 2016). Their from other places (this is Hockett’s displacement: reference argument is based on the idea that linguistic communication to things remote or “displaced” in time and space), but also, requires trust: if everybody lies to everybody else, the trust and as importantly, a very wide variety of inner experiences breaks down, and language itself follows suit. As Dor (2017) that are very difficult to present, even if they refer to the shows, however, this line of reasoning is based on a series here-and-now. The fact that the communicator is worried, of unrealistic assumptions. It concentrates on a single type for example, may show itself on his or her face, but if of lying, where an individual lies with an explicit exploitative the object of worry is not directly available for perception, intention, and the lying carries real detrimental consequences it will remain uncommunicable without language. Language for the community, but this is far from representing the makes it communicable, and it does so on the basis of the functions of lying in linguistic communication. Individuals Frontiers in Psychology | www.frontiersin.org 13 February 2020 | Volume 11 | Article 134 Shilton et al. Human Social Evolution: Self-Domestication or Self-Control? very often lie with non-exploitative intentions, sometimes with can be used to regulate emotional responses to external pro-social intentions (‘white lies’), and such lying actually stimuli (Engen and Singer, 2018). For example, an emotion contributes to social cohesion. Potentially detrimental and word such as “anger,” when used in the context of a exploitative lies are effectively policed and punished in small conflict with an out-group member, could help mobilize an groups, so exploitative lying is unlikely to destroy linguistic aggressive response. communication. Moreover, language is not restricted to the Hare (2017) cites evidence that the widening of the transfer of propositional information. It is necessary for developmental window enables human children to reach, around collective action and collective identity, so the multiple functions age 6, levels of self-control that exceed those of non-human apes. of language compensated for its occasional and inevitable It is around this same age that children begin to internalize detrimental effects. Especially relevant to our current discussion means of emotion regulation including speech signs, so audible is the fact that lying, both exploitative and non-exploitative, taunts and curses become silent ones, a visible smile becomes an requires more sophisticated capacities at the cognitive, emotional inner smile, and on the linguistic level, audible speech becomes and social levels, than honest communication. It did not inner speech (Holodynski and Friedlmeier, 2006). Symbolic harm the overall capacity of the community to cooperate, strategies are increasingly employed by caregivers to instruct the but made the social negotiation of community life more children under their care, teaching the children why and how nuanced and broader in scope. Lying requires higher levels they should control and express their emotions (Holodynski and of emotional control of behavioral expressions – bodily, facial Friedlmeier, 2006). Such a dynamic puts the individual child’s and vocal – than honest communication (Dor, 2017); efficient unique emotional profile and its expression under collective lying requires a poker face and the ability to express pretended pressure, making him comply with shared cultural norms and emotions. Language, therefore, would have added to the selective reflect on his emotional state and its regulation. pressures for better mimesis-related emotional control, rather The emergence of language in hominin evolution added to than reducing the need for it. A similar dynamic would have shared cultural norms a gradually increasing subset of language- occurred at the underlying physio-anatomical level of adapting specific norms of communication, such as conventionalized to language, as the appearance of the modern vocal apparatus conversational styles. This would have placed additional selective made the human face highly mobile and controllable, thus pressures on individuals’ capacities for emotional control. Living increasing the repertoire of facial expressions and their voluntary among egalitarian, coordinated groups requires a heightened control (Donald, 1991; Wilkins, 2017). In addition, language sensitivity to the motives and emotional states of others, was arguably able to provide its own means for emotional especially while negotiating smooth interactions between group control, whether for lying or other purposes. Neuroimaging members. As data from modern hunter-gatherer societies show, studies show that stimulus reappraisal, a widely acknowledged these requirements may result in pervasive conversational styles cognitive process of emotion regulation (Ertl et al., 2013), is of surface courtesy, which are achieved through a conspicuous correlated with activity in brain areas that are involved with and conventionalized politeness (Brown, 2004; Groark, 2008). the representation of semantic knowledge and its retrieval The effects of these or other norms of linguistic communication (Wagner et al., 2001; Satpute et al., 2014). Although semantic on the emotional lives of their speakers may vary according to knowledge is not necessarily linguistic, its digitization and how different linguistic groups (and different group members massive expansion during the emergence and development of within them) view the relations between language and experience language (Dor, 2015) could have allowed hominins living in (Dor, 2015). For example, in Tenejapa Mayans, conspicuous linguistic groups to better categorize, appraise and reappraise politeness, which includes politeness utterances, serves to convey emotion-provoking stimuli, and thus better control their agreement, empathy, and positive affect (Brown, 2004), thereby responses to them. promoting pro-sociality. In Tzotzil Mayans, on the other hand, In addition, the mutual identification, categorization and aggression has been transferred from the physical level (assaults signification of emotional experiences led to the emergence and murders are relatively uncommon) to the symbolic-linguistic of a semantic field of emotion – sets of semantically related level. Ill-wishing utterances are believed to possess a sorcerous words and expressions referring to mutually identified emotions. quality when uttered within the privacy of one’s residency, often Emotion-words enable affect labeling, a language-specific during the night, i.e., away from everyday social interaction and technique of emotion regulation, which can modulate its linguistic norms of politeness (Groark, 2008).3 an emotional experience, its accompanying physiological Language has also led to the cultural construction of response and the resulting behavior, in accordance with novel categories of feelings (or emotions; we use the terms the emotion-word used for categorizing the initial affective interchangeably here). For example, feelings of certainty, response. For example, a stress response can be categorized by an emotion-word as either exciting or fearful, and this 3 The symbolic norms regulating human behavior, which are culturally learned and alters the resulting emotional experience, the physiological culturally evolved, make it possible to argue that humans are “domesticated” by correlates and the behavioral responses of the individual externally imposed symbolic social conventions (and by an internally constructed, that utters or responds to the emotion-word (Jamieson norm-binding “super-ego”). This notion of HSD, which goes back to the old and misleading idea of humans being tamed by “civilization,” is very different from et al., 2013). Another possible contribution of emotion- the current one. Moreover, the regulation of human life by symbolic norms and words for emotional control is in their use as scaffolds for conventions has little in common with the taming of domesticates, or with the endogenous emotion generation, a process which in itself social evolution of bonobos and other social mammals. Frontiers in Psychology | www.frontiersin.org 14 February 2020 | Volume 11 | Article 134 Shilton et al. Human Social Evolution: Self-Domestication or Self-Control? suspicion and doubt derive from issues of truth and falsity as structures (Spurway, 1955), social structures in humans became properties of the relationship between a linguistic message – more complex. Second, in most domesticates there is a reduction arbitrary and displaced – and the experiential world (Jablonka in brain size whereas brain size increased during most of human et al., 2012). Other existing, prelinguistic feelings came to be evolution. It is possible that in humans the last 10,000 years of mutually identified and reconceptualized in ways that align with sedentary life led to small-island-like conditions, which could the values, myths and the shared worldview of a linguistic group’s arguably explain the recent reduction in human brain size semantic landscape. As Myers (1988) shows in his conceptual (Sánchez-Villagra et al., 2016). Generally, however, although analysis of ‘compassion’ and ‘anger’ in the culture and language of selection for reduced emotional reactivity was involved in both Pintupi Aborigines, these emotion-words refer to the acceptance socially impoverished domesticates and socially sophisticated or rejection of relatedness. “Compassion” refers to the acceptance humans, the differences between the two types of pro-social of relatedness and “anger” to its rejection. Generally, once evolution mean that their inclusion under the same umbrella people construct overall shared worldviews through language and term of “domestication” is misleading. myth, their linguistic emotion-concepts will come to reflect this Third, the evolution of all cooperative and sophisticated “deep structure.” social animals, including humans, was inevitably entwined with At the simplest level, the sharing of experiences through changes in their emotional dispositions. We observe, on the language has allowed individuals to expand their private one hand, context-sensitive reduced aggression and displays of experiential knowledge, including emotional knowledge affection toward some group members. Notable examples are (Jablonka and Ginsburg, 2012). This sharing of emotional teaching the young by non-parents in meerkats, alloparenting knowledge could have been achieved by the use of metonyms in wolves, and sophisticated, hierarchical social structure and and metaphors (e.g., the “head” of the group; having the reduced aggression of mole rats (Skulachev et al., 2017). On upper “hand”), which derive from the shared anatomy and the other hand, in some of the same cooperative species we physiological functioning of the human body and appear to be find increased aggression toward group members, mainly in the a universal tool for cultural-specific content (Kövecses, 2000). context of status-related conflicts. For example, the offspring Linguistically constructed emotion concepts that are combined of a subordinate meerkat females that have become pregnant together further elaborate the semantic emotional knowledge are killed by the dominant female, and such subordinates of individuals (Barrett, 2017). They bring together diverse are often evicted from the group; in addition, subordinates bodily sensations, thoughts, feelings, and social contexts in may engage in infanticide activities, though to a significantly unique configurations. lesser degree (Clutton-Brock et al., 1998). Proactive violence against other groups is also evident in meerkats and other cooperative species. What is striking about these and most CONCLUSION AND FUTURE other examples of social behavior in cooperative taxa is the DIRECTIONS increased context-sensitivity of both pro-social and aggressive behaviors, which points to an altered emotional responsiveness. Domestication is the longest and the most systematic We therefore expect that comparing humans with other social evolutionary experiment that humans have ever conducted. mammals will be as fruitful as comparing them to domesticates. It was used by Darwin (1872) to explain evolutionary change We anticipate that future research will uncover similarities in through natural selection and assortative mating, and in the the executive control of emotions among humans and other Variation in Animals and Plants under Domestication (Darwin, highly social mammals, which will only partially overlap the 1868) to shed light on the generation of heritable variations. early developmental pathways that are affected in the DS. It has profoundly changed the history of humans, being a It would be of particular interest to study the correlations necessary condition for the agricultural revolution (Diamond, between neoteny, increase in brain size and alloparenting 1997), and is used today as an example of evolutionary change practices in humans and other highly social mammals, and that highlights the need to incorporate multiple modes of compare the developmental networks that underlie these information transmission (genetic, epigenetic, behavioral cooperative behaviors. and cultural) when considering cumulative evolution (Zeder, More specifically, we expect that the developmental pathways 2018). The social evolution of humans and bonobos has been and the genetic and epigenetic networks underlying cooperative interpreted as a special variant of domestication – as a self- behavior, neoteny and other features related to pro-sociality domestication process. While this analogy has led to productive in humans and other social mammals will include neural research because it focused attention on the commonalities of crest-related gene networks. These networks underpin cranial humans and domesticates, we believe that the social evolution differences and other important morphological and physiological of humans is better explained in terms of selection for pro-social changes that are involved in domestication and have been motivation and self-control, which are guided by symbolic targeted by selection during the social evolution of humans. communication and representation rather than as a process of However, we predict that in humans, changes in the GRNs self-domestication. underlying the HPA axis and pathways associated with learning In this paper we have emphasized the differences between the and with the control of emotions, will be even more prominent. evolution of domesticates and the social evolution of humans. The nature of the changes in the cognition and emotionality First, while in domesticates there is a breakdown of social of humans suggests that pathways controlling metacognition Frontiers in Psychology | www.frontiersin.org 15 February 2020 | Volume 11 | Article 134 Shilton et al. Human Social Evolution: Self-Domestication or Self-Control? (e.g., complex decision-making and regulation of affect), which to be shared by modern humans and their Neanderthal and are controlled by neo-cortical regions, were important targets Denisvoan cousins. of selection. These pathways are also expected to underlie the The second stage that we identified in human evolution social evolution of other mammals that became socially organized involved a further increase in emotional and cognitive plasticity and cooperative with regard to tasks such as foraging, hunting, that was driven by the instruction of imagination through group defense and alloparenting. Hence we predict that genetic language. We therefore expect, and find, a strong cultural and epigenetic changes in the GRNs underlying the development influence on the expression of emotions, including the ability to of these pathways will prove to be of major importance in suppress emotions under some social and intellectual conditions. the evolution of highly social mammals and to be especially We also expect, and find, that the new adaptations in the prominent in human evolution. ability of humans to represent and to communicate have Extending Hare’s (2017) suggestion, we have argued that led to a huge increase in the ability to deceive and to the the evolution of emotional self-control is the hallmark of problem of distinguishing between false and true memories, human social evolution, and that self-control is part of the problems that were partially solved by cultural evolution cognitive-affective evolved make-up of humans. We identified of social norms and the development of autobiographical two overlapping stages in the process, one preceding the memory (Jablonka, 2017; Dor, 2019). More culture-specific emergence of language and the second following it. The first changes in the control and effects of emotions can also be stage involved the initial development of the hominin life-style: explained within this framework. Sapolsky (1999), for example, hunting and foraging, toolmaking, and alloparenting. Each of discusses the case of individuals with repressive personalities these practices both profited from and promoted an increase whose “unemotional” lives of discipline and conformity are in emotional control and pro-sociality. As argued elsewhere actually characterized by markedly elevated basal cortisol (Dor and Jablonka, 2010, 2014; Dor, 2015), the evolution levels and hyper-reactive sympathetic stress-responses. These of all forms of uniquely human communication – including findings are notable because repressive personalities are not mimesis, musical engagement and language – was driven by exposed to irregular amounts of stress with which they cultural evolution. (For extensive discussion of human cultural are coping maladaptively, but rather are highly stressed by evolution see Richerson and Boyd, 2005; Mesoudi, 2011; Jablonka the process of constructing a world without any stressors. and Lamb, 2014; Henrich, 2016; Laland, 2017.) The evolution We see this case as illustrative of the ways in which of human communication was initiated by cultural practices human-specific emotional control and emotional plasticity, that shaped the plastic human brain through learning-based mediated by language and other uniquely human cultural adjustments, followed by the partial genetic accommodation of practices, may modulate and mold human physiology, and in elements enabling ever more complex communication. Hence, doing so lead to a phenotype that partially resembles that culturally evolved communication not only adapted to the of domesticates. brains and minds of individual communicators, but the brains In summary, we regard the social, gene-cultural evolution and minds of the communicators became adapted to the of humans as more similar to the social evolution of other culturally evolving communication systems, thereby generating, highly social mammals that display enhanced cognitive and through positive feedbacks, an ever-widening co-evolutionary affective plasticity and sophisticated social structures, than to spiral. We have argued that the evolution of pro-sociality the evolution of socially impoverished domesticates. These and cooperation in pre-linguistic humans was a major part similarities however, pale in comparison to the unique features of this spiraling evolutionary process. Among other things, of human social evolution, which has been guided by cumulative it entailed the evolution of increased emotional control cultural changes that led to increased cognitive and affective and mimetic communication, including rhythmically entrained plasticity, allowing feats of saintly cooperation and sadistic mimetic acts that are the seed of musical engagement. cruelty that go far beyond those of any other animal. Building on the foundation of rhythmic and tonal anticipation, musical activities became a powerful technology of engagement, capable of inducing high levels of emotional synchrony and AUTHOR CONTRIBUTIONS promoting pro-social behavior. Because of this, we expect to find that limbic regions involved in emotional reactions All authors listed have made a substantial, direct and intellectual became specialized during human evolution, as were the contribution to the work, and approved it for publication. neo-cortical regions controlling them (for some indications that this may indeed be the case, see Barger et al., 2014.) According to our argument, the basic social emotions of ACKNOWLEDGMENTS embarrassment, shame, guilt and pride evolved in this context. We expect that once the developmental genetic networks We are grateful to Marion Lamb for her constructive and detailed underlying them (and the blush, which is their outward comments on a previous draft of this article, and to the reviewers expression) are identified, the relevant variations will be found of this article for their useful comments and suggestions. Frontiers in Psychology | www.frontiersin.org 16 February 2020 | Volume 11 | Article 134 Shilton et al. Human Social Evolution: Self-Domestication or Self-Control? REFERENCES Cieri, R., Churchill, S., Franciscus, R., Tan, J., and Hare, B. (2014). Craniofacial feminization, social tolerance, and the origins of behavioral modernity. Curr. Allen, J. J., and Anderson, C. A. (2017). “General aggression model,” in The Anthropol. 55, 419–443. doi: 10.1086/677209 International Encyclopedia of Media Effects, eds P. Rössler, C. A. Hoffner, and Cimarelli, G., Virányi, Z., Turcsán, B., Rónai, Z., Sasvári-Székely, M., and Bánlaki, L. Zoonen, (Hoboken, NJ: Wiley), doi: 10.1002/9781118783764.wbieme0078 Z. (2017). Social behavior of pet dogs is associated with peripheral OXTR Anastasiadi, D., and Piferrer, F. (2019). Epimutations in developmental genes methylation. Front. Psychol. 8:549. doi: 10.3389/fpsyg.2017.00549 underlie the onset of domestication in farmed European sea bass. Mol. Biol. Cirelli, L. K. (2018). How interpersonal synchrony facilitates early prosocial Evol. 36, 2252–2264. doi: 10.1093/molbev/msz153 behavior. Curr. Opin. Psychol. 20, 35–39. doi: 10.1016/j.copsyc.2017.08.009 Asa, C. (1997). “Hormonal and experiential factors in the expression of social and Clutton-Brock, T. H., Brotherton, P. N. M., Smith, R., McIlrath, G. M., Kansky, R., parental behavior in canids,” in Cooperative Breeding in Mammals, eds N. G. Gaynor, D., et al. (1998). Infanticide and expulsion of females in a cooperative Salomon, and J. A. French, (Cambridge: Cambridge University Press), 129–150. mammal. Proc. R. Soc. Lond. Ser. B Biol. Sci. 265, 2291–2295. doi: 10.1098/rspb. Avital, E., and Jablonka, E. (2000). Animal Traditions: Behavioural Inheritance in 1998.0573 Evolution. Cambridge: Cambridge University Press. Cofran, Z., and DeSilva, J. M. (2015). A neonatal perspective on homo erectus brain Barger, N., Hanson, K. L., Teffer, K., Schenker-Ahmed, N. M., and Semendeferi, growth. J. Hum. Evol. 81, 41–47. doi: 10.1016/j.jhevol.2015.02.011 K. (2014). Evidence for evolutionary specialization in human limbic structures. Coppinger, R., and Coppinger, L. (2001). Dogs: A Startling New Understanding of Front. Hum. Neurosci. 8:277. doi: 10.3389/fnhum.2014.00277 Canine Origins, Behavior, and Evolution. New York, NY: Scribner. Barrett, L. F. (2017). How Emotions are Made: The Secret Life of the Brain. Corbett, L. K. (1988). Social dynamics of a captive dingo pack: population New York, NY: Houghton Mifflin Harcourt. regulation by dominant female infanticide. Ethology 78, 177–198. doi: 10.1111/ Barton, R. A. (2012). Embodied cognitive evolution and the cerebellum. Philos. j.1439-0310.1988.tb00229.x Trans. R. Soc. B Biol. Sci. 367, 2097–2107. doi: 10.1098/rstb.2012.0112 Corrada, Y., Castex, G., Sosa, Y., and Gobello, C. (2003). Secretory patterns of Bednarik, R. G. (2014). Doing with less: hominin brain atrophy. HOMO J. Compar. prolactin in dogs: circannual and ultradian rhythms. Reprod. Domest. Anim. Hum. Biol. 65, 433–449. doi: 10.1016/j.jchb.2014.06.001 38, 219–223. doi: 10.1046/j.1439-0531.2003.00432.x Bélteky, J., Agnvall, B., Bektic, L., Höglund, A., Jensen, P., and Guerrero-Bosagna, Cross, I. (2007). “Music and cognitive evolution,” in Oxford Handbook of C. (2018). Epigenetics and early domestication: differences in hypothalamic Evolutionary Psychology, eds R. I. M. Dunbar, and L. Barrett, (Oxford: Oxford DNA methylation between red junglefowl divergently selected for high or low University Press), 649–667. fear of humans. Genet. Select. Evol. 50:13. Cross, I. (2016). “The nature of music and its evolution,” in The Oxford Handbook Belyaev, D. K. (1979). Destabilizing selection as a factor in domestication. of Music Psychology, eds S. Hallam, I. Cross, and M. Thaut, (Oxford: Oxford J. Heredity 70, 301–308. doi: 10.1093/oxfordjournals.jhered.a109263 University Press). Bence, M., Marx, P., Szantai, E., Kubinyi, E., Ronai, Z., and Banlaki, Z. (2017). Cross, I., and Tolbert, E. (2016). “Music and meaning,” in The Oxford Handbook Lessons from the canine Oxtr gene: populations, variants and functional of Music Psychology, eds S. Hallam, I. Cross, and M. Thaut, (Oxford: Oxford aspects. Genes Brain Behav. 16, 427–438. doi: 10.1111/gbb.12356 University Press). Ben-Mocha, Y., Mundry, R., and Pika, S. (2018). Why hide? Concealed sex in Cross, L., Turgeon, M., and Atherton, G. (2019). How moving together binds dominant Arabian babblers (Turdoides squamiceps) in the wild. Evol. Hum. us together: the social consequences of interpersonal entrainment and group Behav. 39, 575–582. doi: 10.1016/j.evolhumbehav.2018.05.009 processes. Open Psychol. 1, 273–302. doi: 10.1515/psych-2018-0018 Blair, R. J. (2016). The neurobiology of impulsive aggression. J. Child Adolesc. Crozier, W. R. (2006). Blushing and the Social Emotions. Basingstoke: Macmillan Psychopharmacol. 26, 4–9. doi: 10.1089/cap.2015.0088 Palgrave. Boas, F. (1938). The Mind of Primitive Man. New York, NY: Macmillan. Dale, R., Palma-Jacinto, S., Marshall-Pescini, S., and Range, F. (2019). Wolves, Boyd, B. (2018). The evolution of stories: from mimesis to language, from fact to but not dogs, are prosocial in a touch screen task. PLoS One 14:e0215444. fiction. Cogn. Sci. 9:e1444. doi: 10.1002/wcs.1444 doi: 10.1371/journal.pone.0215444 Boyd, R., Gintis, H., Bowles, S., and Richerson, P. J. (2003). The evolution of Darwin, C. (1868). The Variation of Animals and Plants under Domestication. altruistic punishment. Proc. Natl. Acad. Sci. U.S.A. 100, 3531–3535. London: Murray. Braastad, B. (1987). Abnormal behaviour in farmed silver fox vixens (Vulpes vulpes Darwin, C. (1871). The Descent of Man, and Selection in Relation to Sex. London: L.): tail-biting and infanticide. Appl. Anim. Behav. Sci. 17, 376–377. doi: 10. Murray. 1016/0168-1591(87)90171-7 Darwin, C. (1872). The Origin of Species, 6th Edn, London: Murray. Braastad, B. O., and Bakken, M. (1993). Maternal infanticide and periparturient de Lathouwers, M., and Van Elsacker, L. (2006). Comparing infant and juvenile behaviour in farmed silver foxes Vulpes vulpes. Appl. Anim. Behav. Sci. 36, behavior in bonobos (Pan paniscus) and chimpanzees (Pan troglodytes): a 347–361. doi: 10.1016/0168-1591(93)90132-9 preliminary study. Primates 47, 287–293. doi: 10.1007/s10329-006-0179-7 Braunstein, L. M., Gross, J. J., and Ochsner, K. N. (2017). Explicit and implicit DeCasien, A. R., Williams, S. A., and Higham, J. P. (2017). Primate brain size is emotion regulation: a multi-level framework. Soc. Cogn. Affect. Neurosci. 12, predicted by diet but not sociality. Nat. Ecol. Evol. 1:112. doi: 10.1038/s41559- 1545–1557. doi: 10.1093/scan/nsx096 017-0112 Brown, P. (2004). Learning the social graces: socializing affect through play in Dediu, D., and Levinson, S. C. (2013). On the antiquity of language: the a mayan community. Paper Presented at the UCLA-Sloan Center on Working reinterpretation of neandertal linguistic capacities and its consequences. Front. Families Workshop “Emotional Meaning in Social Interaction: Toward an Psychol. 4:397. doi: 10.3389/fpsyg.2013.00397 Integration of the Subjective and the Social,” Department of Anthropology, (Los DeSilva, J. M. (2011). A shift toward birthing relatively large infants early in Angeles: University of California), 29–30. human evolution. Proc. Natl. Acad. Sci. U.S.A. 108, 1022–1027. doi: 10.1073/ Brüne, M. (2007). On human self-domestication, psychiatry, and eugenics. Philos. pnas.1003865108 Ethics Hum. Med. 2:21. doi: 10.1186/1747-5341-2-21 Deutsch, D., Henthorn, T., and Lapidis, R. (2011). Illusory transformation from Bufill, E., Agustí, J., and Blesa, R. (2011). Human neoteny revisited: the case of speech to song. J. Acoust. Soc. Am. 129, 2245–2252. doi: 10.1121/1.3562174 synaptic plasticity. Am. J. Hum. Biol. 23, 729–739. doi: 10.1002/ajhb.21225 Diamond, J. (1997). Guns, Germs, and Steel: The Fates of Human Societies. Burkart, J. M., Allon, O., Amici, F., Fichtel, C., Finkenwirth, C., Heschl, A., et al. New York, NY: Random House. (2014). The evolutionary origin of human hyper-cooperation. Nat. Commun. Domínguez-Rodrigo, M., and Pickering, T. R. (2017). The meat of the matter: an 5:4747. doi: 10.1038/ncomms5747 evolutionary perspective on human carnivory. Azania 52, 4–32. doi: 10.1080/ Casey, B. J. (2015). Beyond simple models of self-control to circuit-based accounts 0067270x.2016.1252066 of adolescent behavior. Annu. Rev. Psychol. 66, 295–319. doi: 10.1146/annurev- Donald, M. (1991). The Origin of the Modern Mind: Three Stages in the Evolution of psych-010814-015156 Culture and Cognition. Cambridge, MA: Harvard University Press. Chanda, M. L., and Levitin, D. J. (2013). The neurochemistry of music. Trends Dor, D. (2015). The Instruction of Imagination: Language as a Social Cogn. Sci. 17, 179–193. doi: 10.1016/j.tics.2013.02.007 Communication technology. Oxford: Oxford University Press. Frontiers in Psychology | www.frontiersin.org 17 February 2020 | Volume 11 | Article 134 Shilton et al. Human Social Evolution: Self-Domestication or Self-Control? Dor, D. (2017). The role of the lie in the evolution of human language. Lang. Sci. Goodwin, D., Bradshaw, J. W. S., and Wickens, S. M. (1997). Paedomorphosis 63, 44–59. doi: 10.1016/j.cub.2017.01.020 affects agonistic visual signals of domestic dogs. Anim. Behav. 53, 297–304. Dor, D. (2019). Language and innovation: comment on “replication and emergence doi: 10.1006/anbe.1996.0370 in cultural transmission” by Monica Tamariz. Phys. Life Rev. 30, 77–79. Gottfried, H., Vigilant, L., Mundry, R., Behringer, V., and Surbeck, M. (2019). Dor, D., and Jablonka, E. (2010). “Canalization and plasticity in the evolution of Aggression by male bonobos against immature individuals does not fit linguistic communication,” in The Evolution of Human Language, eds R. K. with predictions of infanticide. Aggres. Behav. 45, 300–309. doi: 10.1002/ab. Larson, V. Deprez, and H. Yamakido, (Cambridge: Cambridge University 21819 Press), 135–147. doi: 10.1017/cbo9780511817755.010 Gould, S. J. (1996). The Mismeasure of Man. New York, NY: Norton. Dor, D., and Jablonka, E. (2014). “‘Why we need to move from gene-culture co- Gray, P. (2009). Play as a foundation for hunter-gatherer social existence. Am. J. evolution to culturally driven co-evolution’,” in The Social Origins of Language: Play 1, 476–522. Studies in the Evolution of Language, eds D. Dor, C. Knight, and J. Lewis, Gray, P. B., McHale, T. S., and Carré, J. M. (2017). A review of human male (Oxford: Oxford University Press), 15–30. field studies of hormones and behavioral reproductive effort. Horm. Behav. 91, Dugatkin, L. A., and Trut, L. N. (2017). How to Tame a Fox (and Build A Dog). 52–67. doi: 10.1016/j.yhbeh.2016.07.004 Chicago: University of Chicago Press. Groark, K. P. (2008). Social opacity and the dynamics of empathic in-sight among Dunbar, R. I. M. (1998). The social brain hypothesis. Evol. Anthropol. 6, 178–190. the Tzotzil Maya of chiapas, Mexico. ETHOS 36, 427–448. doi: 10.1111/j.1548- Durrleman, S., Pennec, X., Trouvé, A., Ayache, N., and Braga, J. (2012). 1352.2008.00025.x Comparison of the endocranial ontogenies between chimpanzees and bonobos Gruber, T., and Clay, Z. (2016). A comparison between bonobos and chimpanzees: via temporal regression and spatiotemporal registration. J. Hum. Evol. 62, a review and update. Evol. Anthropo. Issues News Rev. 25, 239–252. doi: 10.1002/ 74–88. doi: 10.1016/j.jhevol.2011.10.004 evan.21501 Engen, H. G., and Singer, T. (2018). “Fighting fire with fire: endogenous emotion Gunnar, M. R., and Donzella, B. (2002). Social regulation of the cortisol levels generation as a means of emotion regulation,” in The Nature of Emotion, 2nd in early human development. Psychoneuroendocrinology 27, 199–220. doi: 10. Edn, eds R. Davidson, A. Shackman, A. Fox, and R. Lapate, (New York, NY: 1016/s0306-4530(01)00045-2 Oxford University Press), 172–177. Hare, B. (2007). From nonhuman to human mind: what changed and why? Curr. Enomoto, T. (1990). Social play and sexual behavior of the bonobo (Pan paniscus) Dir. Psychol. Sci. 16, 60–64. doi: 10.1111/j.1467-8721.2007.00476.x with special reference to flexibility. Primates 31, 469–480. doi: 10.1007/ Hare, B. (2017). Survival of the friendliest: homo sapiens evolved via selection bf02382531 for prosociality. Annu. Rev. Psychol. 68, 155–186. doi: 10.1146/annurev-psych- Ertl, M., Hildebrandt, M., Ourina, K., Leicht, G., and Mulert, C. (2013). Emotion 010416-044201 regulation by cognitive reappraisal — The role of frontal theta oscillations. Hare, B., Melis, A. P., Woods, V., Hastings, S., and Wrangham, R. (2007). Tolerance Neuroimage 81, 412–421. doi: 10.1016/j.neuroimage.2013.05.044 allows bonobos to outperform chimpanzees on a cooperative task. Curr. Biol. Feddersen-Petersen, D. U. (2007). “Social behaviour of dogs and related canids,” in 17, 619–623. doi: 10.1016/j.cub.2007.02.040 The Behavioural Biology of Dogs, ed. P. Jensen (Wallingford: CABI Publishing), Hare, B., Plyusnina, I., Ignacio, N., Schepina, O., Stepika, A., Wrangham, R., et al. 105–119. doi: 10.1079/9781845931872.0105 (2005). Social cognitive evolution in captive foxes is a correlated byproduct of Fernandez-Duque, E., Valeggia, C. R., and Mendoza, S. P. (2009). the biology of experimental domestication. Curr. Biol. 15, 226–230. doi: 10.1016/j.cub.2005. paternal care in human and nonhuman primates. Ann. Rev. Anthropol. 38, 01.040 115–130. doi: 10.1016/j.pnpbp.2010.09.017 Hare, B., and Tomasello, M. (2005). The emotional reactivity hypothesis and Ferraro, J. V., Plummer, T. W., Pobiner, B. L., Oliver, J. S., Bishop, L. C., Braun, cognitive evolution: reply to Miklósi and Topál. Trends Cogn. Sci. 9, 464–465. D. R., et al. (2013). Earliest archaeological evidence of persistent hominin doi: 10.1016/j.tics.2005.08.010 carnivory. PLoS One 8:e62174. doi: 10.1371/journal.pone.0062174 Hare, B., Wobber, V., and Wrangham, R. (2012). The self-domestication Ferreri, L., Mas-Herrero, E., Zatorre, R. J., Ripollés, P., Gomez-Andres, A., Alicart, hypothesis: evolution of bonobo psychology is due to selection against H., et al. (2019). Dopamine modulates the reward experiences elicited by music. aggression. Anim. Behav. 83, 573–585. doi: 10.1016/j.anbehav.2011. Proc. Natl. Acad. Sci. U.S.A. 116, 3793–3798. doi: 10.1073/pnas.1811878116 12.007 Flinn, M. V., Nepomnaschy, P. A., Muehlenbein, M. P., and Ponzi, D. (2011). Hatfield, E., Cacioppo, J. T., and Rapson, R. L. (1994). Emotional Contagion. Evolutionary functions of early social modulation of hypothalamic-pituitary- New York, NY: Cambridge University Press. adrenal axis development in humans. Neurosci. Biobehav. Rev. 35, 1611–1629. Henrich, J. (2016). The Secret of Our Success: How Culture is Driving Human doi: 10.1016/j.neubiorev.2011.01.005 Evolution, Domesticating Our Species, and Making Us Smarter. Oxford: Francis, R. C. (2015). Domesticated: Evolution in a Man-Made World. New York, Princeton University Press. NY: W.W. Norton and Co. Herbeck, Y., Khantemirova, A., Antonov, V., Goncharova, N., Gulevich, R. G., Franciscus, R. G., Maddux, S. D., and Schmidt, K. W. (2013). Anatomically Shepeleva, D., et al. (2017). Expression of the DNA methyltransferase genes modern humans as a “self-domesticated” species: Insights from ancestral wolves in silver foxes experimentally selected for domestication. Russ. J. Genet. 53, and descendant dogs. Presented at the 82nd annual meeting of the American 483–489. doi: 10.1134/s1022795417040056 Association of Physical Anthropologists, Knoxville, TN. Heyes, C. (2018). Cognitive Gadgets. The Cultural Evolution of Thinking. Frynta, D., Baudyšová, J., Hradcová, P., Faltusová, K., and Kratochvíl, L. (2012). Cambridge, MA: Harvard University Press. Allometry of sexual size dimorphism in domestic dog. PLoS One 7:e46125. Holodynski, M., and Friedlmeier, W. (2006). Development of Emotions and doi: 10.1371/journal.pone.0046125 Emotion Regulation. New York, NY: Springer. Furuichi, T. (2011). Female contributions to the peaceful nature of bonobo society. Hrdy, S. B. (2009). Mothers and Others: The Evolutionary Origins Of Joint Evol. Anthropol. 20, 131–142. doi: 10.1002/evan.20308 Understanding. Cambridge, MA: Harvard University Press. Gácsi, M., Gyoöri, B., Virányi, Z., Kubinyi, E., Range, F., Belényi, B., et al. (2009). Hrdy, S. B. (2016). “‘Development plus social selection in the emergence Explaining dog wolf differences in utilizing human pointing gestures: selection of “emotionally modern” humans’,” in Childhood: Origins, Evolution, and for synergistic shifts in the development of some social skills. PLoS One 4:e6584. Implications, eds C. L. Meehan, and A. N. Crittenden, (Santa Fe: School for the doi: 10.1371/journal.pone.0006584 Advanced Research Press), 11–44. Gillespie-Lynch, K., Savage-Rumbaugh, S., and Lyn, H. (2014). “Language learning Hughes, F. P. (2010). Children, Play, and Development. Thousand Oaks, CA: Sage in non-human primates,” in Encyclopedia of Language Development, eds Publications. P. J. Brooks, and V. Kempe, (Thousand Oaks, CA: SAGE Publications), Isler, K., and van Schaik, C. P. (2012). Allomaternal care, life history and brain size 334–337. evolution in mammals. J. Hum. Evol. 63, 52–63. doi: 10.1016/j.jhevol.2012.03. Glasper, E. R., Kenkel, W. M., Bick, J., and Rilling, J. K. (2019). More than 009 just mothers: the neurobiological and neuroendocrine underpinnings of Jablonka, E. (2017). Collective narratives, false memories and the origins of allomaternal caregiving. Front. Neuroendocrinol. 53:100741. doi: 10.1016/j. autobiographical memory. Biol. Philos. 32, 839–853. doi: 10.1007/s10539-017- yfrne.2019.02.005 9593-z Frontiers in Psychology | www.frontiersin.org 18 February 2020 | Volume 11 | Article 134 Shilton et al. Human Social Evolution: Self-Domestication or Self-Control? Jablonka, E., and Ginsburg, S. (2012). Scaffolding emotions and evolving language. Lapate, R. C. (2018). “Regulatory benefits of conscious awareness: insights from Behav. Brain Sci. 35, 154–155. doi: 10.1017/S0140525X1100152X the emotion misattribution paradigm and a role for lateral prefrontal cortex,” in Jablonka, E., Ginsburg, S., and Dor, D. (2012). The co-evolution of language and The Nature of Emotion: Fundamental Questions, 2nd Edn, eds A. S. Fox, R. C. emotions. Philos. Trans. R. Soc. Lond. B Biol. Sci. 367, 2152–2159. doi: 10.1098/ Lapate, A. J. Shackman, and R. J. Davidson, (New York, NY: Oxford University rstb.2012.0117 Press). Jablonka, E., and Lamb, M. J. (1995). Epigenetic Inheritance and Evolution. The Lew, C. H., Hanson, K. L., and Groeniger, K. M. (2019). Serotonergic innervation Lamarckian Dimension. Oxford: Oxford University Press. of the human amygdala and evolutionary implications. Am. J. Phys. Anthropol. Jablonka, E., and Lamb, M. J. (2014). Evolution in Four Dimensions: Genetic, 170, 351–360. doi: 10.1002/ajpa.23896 Epigenetic, Behavioral and Symbolic variations in the History of Life, 2nd Edn, Lewis, J. (2016). “‘Play, music, and taboo in the reproduction of an egalitarian Cambridge, MA: MIT Press. society’,” in Social Learning and Innovation in Contemporary Hunter-Gatherers, Jamieson, J. P., Mendes, W. B., and Nock, M. K. (2013). Improving acute stress eds H. Terashima, and B. S. Hewlett, (Tokyo: Springer), 147–158. doi: 10.1007/ responses: the power of reappraisal. Curr. Dir. Psychol. Sci. 22, 51–56. doi: 978-4-431-55997-9_12 10.1177/0963721412461500 Lewis, V., Boucher, J., Lupton, L., and Watson, S. (2000). ‘Relationships between Jöchle, W. (1997). Prolactin in canine and feline reproduction. Reprod. Domest. symbolic play, functional play, verbal and non-verbal ability in young children’. Anim. 32, 183–193. doi: 10.1111/j.1439-0531.1997.tb01280.x Int. J. Lang. Commun. Disord. 35, 117–127. doi: 10.1080/136828200247287 Jones, K. E., Bielby, J., Cardillo, M., Fritz, S. A., O’Dell, J., Orme, C. D. L., Liebenberg, L. (2013). The Origin of Science. Cape Town: CyberTracker. et al. (2009). PanTHERIA: a species-level database of life history, ecology, Lieberman, D., Carlo, J., Ponce de Leon, M., and Zollikofer, C. (2007). A geometric and geography of extant and recently extinct mammals: ecological archives morphometric analysis of heterochrony in the cranium of chimpanzees and E090-184. Ecology 90, 2648–2648. doi: 10.1890/08-1494.1 bonobos. J. Hum. Evol. 52, 647–662. doi: 10.1016/j.jhevol.2006.12.005 Juslin, P. N., and Laukka, P. (2003). Communication of emotions in vocal Lord, K., Feinstein, M., Smith, B., and Coppinger, R. (2013). Variation in expression and music performance: different channels, same code? Psychol. reproductive traits of members of the genus Canis with special attention to Bull. 129:770. doi: 10.1037/0033-2909.129.5.770 the domestic dog (Canis familiaris). Behav. Proces. 92, 131–142. doi: 10.1016/ Kano, T. (1992). The Last Ape: Pygmy Chimpanzee Behavior and Ecology. Stanford: j.beproc.2012.10.009 Stanford University Press. Lord, K. A., Larson, G., Coppinger, R. P., and Karlsson, E. K. (2019). The history of Keehn, R. J. J., Iversen, J. R., Schulz, I., and Patel, A. D. (2019). Spontaneity farm foxes undermines the animal domestication syndrome. Trends Ecol. Evol. and diversity of movement to music are not uniquely human. Curr. Biol. 29, doi: 10.1016/j.tree.2019.10.011 [Epub ahead of print]. R621–R622. doi: 10.1016/j.cub.2019.05.035 Macdonald, D. W. (1979). Helpers in fox society. Nature 282, 69–71. Keller, P. E., Novembre, G., and Hove, M. J. (2014). Rhythm in joint action: Macdonald, D. W. (1980). “Social factors affecting reproduction amongst red psychological and neurophysiological mechanisms for real-time interpersonal foxes,” in The Red Fox. Biogeographica, ed. E. Zimen, (Dordrecht: Springer). coordination. Philos. Trans. R. Soc. B Biol. Sci. 369:20130394. doi: 10.1098/rstb. MacLean, E. L., and Hare, B. (2015). Bonobos and chimpanzees exploit helpful 2013.0394 but not prohibitive gestures. Behaviour 152, 493–520. doi: 10.1163/1568539x- Key, C. A. (2000). The evolution of human life history. World Archaeol. 31, 00003203 329–350. MacLean, E. L., Hare, B., Nunn, C. L., Addessi, E., Amici, F., Anderson, R. C., Kim, P. (2016). Human maternal brain plasticity: adaptation to parenting. New Dir. et al. (2014). The evolution of self-control. Proc. Natl. Acad. Sci. U.S.A. 111, Child Adolesc. Dev. 2016, 47–58. doi: 10.1002/cad.20168 E2140–E2148. doi: 10.1073/pnas.1323533111 Kim, P., Rigo, P., Mayes, L. C., Feldman, R., Leckman, J. F., and Swain, J. E. MacLeod, C. E., Zilles, K., Schleicher, A., Rilling, J. K., and Gibson, K. R. (2003). (2014). Neural plasticity in fathers of human infants. Soc. Neurosci. 9, 522–535. Expansion of the neocerebellum in Hominoidea. J. Hum. Evol. 44, 401–429. doi: 10.1080/17470919.2014.933713 doi: 10.1016/S0047-2484(03)00028-9 Kis, A., Bence, M., Lakatos, G., Pergel, E., Turcsán, B., Pluijmakers, J., et al. (2014). Margulis, E. H. (2005). A model of melodic expectation. Music Percept. 22, Oxytocin receptor gene polymorphisms are associated with human directed 663–714. doi: 10.1525/mp.2005.22.4.663 social behavior in dogs (Canis familiaris). PLoS One 9:e83993. doi: 10.1371/ Margulis, E. H., and Simchy-Gross, R. (2016). Repetition enhances the musicality journal.pone.0083993 of randomly generated tone sequences. Music Percept. 33, 509–514. doi: 10. Kleiman, D. G., and Malcolm, J. (1981). “The evolution of male parental investment 1525/mp.2016.33.4.509 in mammals,” in Parental Care in Mammals, eds D. J. Gubernick, and P. H. Markel, A. L., and Trut, L. N. (2011). Behavior, stress, and evolution in light of Klopfer, (New York, NY: Plenum Press), 347–387. doi: 10.1007/978-1-4613- the Novosibirsk selection experiments. Transform. Lamarckism 461, 171–180. 3150-6_9 doi: 10.7551/mitpress/9780262015141.003.0017 Knight, C. (2007). Language co-evolved with the rule of law. Mind Soc. 7, 109–128. Marshall-Pescini, S., Cafazzo, S., Viranyi, Z., and Range, F. (2017a). Integrating doi: 10.1007/s11299-007-0039-1 social ecology in explanations of wolf–dog behavioral differences. Curr. Opin. Kondo, M., Udono, T., Jin, W., Shimizu, K., Funakoshi, M., Itoh, M., et al. (2000). Behav. Sci. 16, 80–86. doi: 10.1016/j.cobeha.2017.05.002 Changes in plasma concentrations of inhibin A and inhibin B throughout sexual Marshall-Pescini, S., Schwarz, J. F., Kostelnik, I., Virányi, Z., and Range, F. (2017b). maturation in the male chimpanzee. Endocr. J. 47, 707–714. doi: 10.1507/ Importance of a species’ socioecology: wolves outperform dogs in a conspecific endocrj.47.707 cooperation task. Proc. Natl. Acad. Sci. U.S.A. 114, 11793–11798. doi: 10.1073/ Kövecses, Z. (2000). Metaphor and Emotion: Language, Culture, and the Body in pnas.1709027114 Human Feeling. Cambridge: Cambridge University Press. Marshall-Pescini, S., Virányi, Z., and Range, F. (2015). The effect of domestication Kreeger, T. J., Seal, U. S., Cohen, Y., Plotka, E. D., and Asa, C. S. (1991). on inhibitory control: wolves and dogs compared. PLoS one 10:e0118469. doi: Characterization of prolactin secretion in gray wolves (Canis lupus). Can. J. 10.1371/journal.pone.0118469 Zool. 69, 1366–1374. doi: 10.1139/z91-192 McPherron, S. P., Alemseged, Z., Marean, C. W., Wynn, J. G., Reed, D., Geraads, Kreutz, G. (2014). Does singing facilitate social bonding. Music Med. 6, 51–60. D., et al. (2010). Evidence for stone-tool-assisted consumption of animal tissues Kühlmann, A. Y. R., De Rooij, A., Kroese, L. F., van Dijk, M., Hunink, M. G. M., before 3.39 million years ago at Dikika, Ethiopia. Nature 466:857. doi: 10.1038/ and Jeekel, J. (2018). Meta-analysis evaluating music interventions for anxiety nature09248 and pain in surgery. Br. J. Surg. 105, 773–783. doi: 10.1002/bjs.10853 Mehr, S. A., Singh, M., Knox, D., Ketter, D. M., Pickens-Jones, D., Atwood, S., Kumsta, R., Hummel, E., Chen, F. S., and Heinrichs, M. (2013). Epigenetic et al. (2019). Universality and diversity in human song. Science 366:eaax0868. regulation of the oxytocin receptor gene: implications for behavioral doi: 10.1126/science.aax0868 neuroscience. Front. Neurosci. 7:83. doi: 10.3389/fnins.2013.00083 Melamed, Y., Kislev, M. E., Geffen, E., Lev-Yadun, S., and Goren-Inbar, N. (2016). Laland, K. (2017). Darwin’s Unfinished Symphony: How Culture Made The Human The plant component of an Acheulian diet at gesher benot Ya ‘aqov, Israel. Proc. Mind. Princeton: Princeton University Press. Natl. Acad. Sci. U.S.A. 113, 14674–14679. doi: 10.1073/pnas.1607872113 Langer, S. K. (1957). Philosophy in a New Key: A Study In The Symbolism Of Reason, Merchant, H., and Honing, H. (2014). Are non-human primates capable Rite, and Art. Cambridge, MA: Harvard University Press. of rhythmic entrainment? Evidence for the gradual audiomotor Frontiers in Psychology | www.frontiersin.org 19 February 2020 | Volume 11 | Article 134 Shilton et al. Human Social Evolution: Self-Domestication or Self-Control? evolution hypothesis. Front. Neurosci. 7:274. doi: 10.3389/fnins.2013. Range, F., Marshall-Pescini, S., Kratz, C., and Virányi, Z. (2019). Wolves lead 00274 and dogs follow, but they both cooperate with humans. Scie. Rep. 9:3796. Mercier, H., and Sperber, D. (2011). Why do humans reason? Arguments for an doi: 10.1038/s41598-019-40468-y argumentative theory. Behav. Brain Sci. 34, 57–111. Range, F., Ritter, C., and Virányi, Z. (2015). Testing the myth: tolerant dogs and Mesoudi, A. (2011). Cultural Evolution: How Darwinian Theory Can Explain aggressive wolves. Proc. R. Soc. B Biol. Sci. 282:20150220. doi: 10.1098/rspb. Human Culture and Synthesize the Social Sciences. Chicago, IL: University of 2015.0220 Chicago Press. Range, F., and Virányi, Z. (2013). Social learning from humans or conspecifics: Miller, D. J., Duka, T., Stimpson, C. D., Schapiro, S. J., Baze, W. B., McArthur, M. J., differences and similarities between wolves and dogs. Front. Psychol. 4:868. et al. (2012). Prolonged myelination in human neocortical evolution. Proc. Natl. doi: 10.3389/fpsyg.2013.00868 Acad. Sci. U.S.A. 109, 16480–16485. doi: 10.1073/pnas.1117943109 Range, F., and Virányi, Z. (2014). Wolves are better imitators of conspecifics than Miller, I. F., Barton, R. A., and Nunn, C. L. (2019). Quantitative uniqueness of dogs. PLoS One 9:e86559. doi: 10.1371/journal.pone.0086559 human brain evolution revealed through phylogenetic comparative analysis. Richerson, P. J., and Boyd, R. (2005). Not by Genes Alone: How Culture Transformed eLife 8:e41250. doi: 10.7554/eLife.41250 Human Evolution. Chicago, IL: University of Chicago Press. Mithen, S. J. (2006). The Singing Neanderthals: The Origins of Music, Language, Rilling, J. K., and Mascaro, J. S. (2017). The neurobiology of fatherhood. Curr. Opin. Mind, and Body. Cambridge, MA: Harvard University Press. Psychol. 15, 26–32. doi: 10.1016/j.copsyc.2017.02.013 Moehlman, P. D., and Hofer, H. (1997). “Cooperative breeding, reproductive Rilling, J. K., Scholz, J., Preuss, T. M., Glasser, M. F., Errangi, B. K., and Behrens, suppression, and body mass in canids,” in Cooperative Breeding in Mammals, T. E. (2012). Differences between chimpanzees and bonobos in neural systems eds N. G. Solomon, and J. A. French, (New York, NY: Cambridge University supporting social cognition. Soc. Cogn. Affect. Neurosci. 7, 369–379. doi: 10. Press), 76–128. doi: 10.1017/cbo9780511574634.005 1093/scan/nsr017 Montgomery, T. M., Pendleton, E. L., Jennifer, E., and Smith, J. E. (2018). Robson, S. L., and Wood, B. (2008). Hominin life history: reconstruction and Physiological mechanisms mediating patterns of reproductive suppression and evolution. J. Anat. 212, 394–425. doi: 10.1111/j.1469-7580.2008.00867.x alloparental care in cooperatively breeding carnivores. Physiol. Behav. 193, Sakai, T., Mikami, A., Tomonaga, M., Matsui, M., Suzuki, J., Hamada, Y., et al. 167–178. doi: 10.1016/j.physbeh.2017.11.006 (2011). Differential prefrontal white matter development in chimpanzees and Myers, F. (1988). The logic and meaning of anger among pintupi aborigines. Man humans. Curr. Biol. 21, 1397–1402. doi: 10.1016/j.cub.2011.07.019 23, 589–610. doi: 10.2307/2802595 Salimpoor, V. N., Benovoy, M., Larcher, K., Dagher, A., and Zatorre, R. J. (2011). Nettl, B. (1983). The Study of Ethnomusicology: Twenty-Nine Issues and Concepts. Anatomically distinct dopamine release during anticipation and experience of Urbana, IL: University of Illinois Press. peak emotion to music. Nat. Neurosci. 14:257. doi: 10.1038/nn.2726 Neubauer, S., Hublin, J.-J., and Gunz, P. (2018). The evolution of modern human Sánchez-Villagra, M. R., Geiger, M., and Schneider, R. A. (2016). The taming of brain shape. Sci. Adv. 4:eaao5961. doi: 10.1126/sciadv.aao5961 the neural crest: a developmental perspective on the origins of morphological Nilsson, U. (2009). Soothing music can increase oxytocin levels during bed rest covariation in domesticated mammals. R. Soc. Open Sci. 3:160107. doi: 10.1098/ after open-heart surgery: a randomised control trial. J. Clin. Nurs. 18, 2153– rsos.160107 2161. doi: 10.1111/j.1365-2702.2008.02718.x Sánchez-Villagra, M. R., and van Schaik, C. (2019). Evaluating the self- Novembre, G., Mitsopoulos, Z., and Keller, P. E. (2019). Empathic perspective domestication hypothesis of human evolution. Evol. Anthropol. 28, 133–143. taking promotes interpersonal coordination through music. Sci. Rep. 9, 1–12. doi: 10.1002/evan.21777 doi: 10.1038/s41598-019-48556-9 Sandi, C., and Pinelo-Nava, M. T. (2007). Stress and memory: behavioral effects Okanoya, K. (2015). Evolution of song complexity in Bengalese finches could and neurobiological mechanisms. Neural Plast. 2007:78970. mirror the emergence of human language. J. Ornithol. 156, 65–72. doi: 10.1007/ Sands, J. L., and Creel, S. (2004). Social dominance, aggression and fecal s10336-015-1283-5 glucocorticoid levels in a wild population of wolves Canis lupus. Anim. Behav. Oliva, J. L., Wong, Y. T., Rault, J. L., Appleton, B., and Lill, A. (2016). The oxytocin 67, 387–396. doi: 10.1016/j.anbehav.2003.03.019 receptor gene, an integral piece of the evolution of Canis familaris from Canis Sapolsky, R. M. (1999). “Hormonal correlates of personality and social contexts: lupus. Pet Behav. Sci. 2, 1–15. from non-human to human primates,” in Hormones, Health, and Behavior: Osadchuk, L. V., and Shurkalova, T. A. (1992). The testosterone level in the testes A Socio-Ecological and Lifespan Perspective, eds C. Panter-Brick, and C. M. of silver foxes during prenatal development. Ontogenez 23, 385–389. Worthman, (New York, NY: Cambridge University Press), 18–46. doi: 10.1017/ Pal, S. K. (2005). Parental care in free-ranging dogs, Canis familiaris. Appl. Anim. cbo9780511623462.002 Behav. Sci. 90, 31–47. doi: 10.1016/j.applanim.2004.08.002 Satpute, A. B., Badre, D., and Ochsner, K. N. (2014). Distinct regions of prefrontal Palagi, E. (2006). Social play in bonobos (Pan paniscus) and chimpanzees cortex are associated with the controlled retrieval and selection of social (Pan troglodytes): implications for natural social systems and interindividual information. Cereb. Cortex 24, 1269–1277. doi: 10.1093/cercor/bhs408 relationships. Am. J. Phys. Anthropol. 129, 418–426. doi: 10.1002/ajpa.20289 Savage-Rumbaugh, E. S., Williams, S. L., Furuichi, T., and Kano, T. (1996). Pargeter, J., Khreisheh, N., and Stout, D. (2019). Understanding stone tool-making “Language perceived: pan paniscus branches out,” in Great Ape Societies, eds skill acquisition: experimental methods and evolutionary implications. J. Hum. C. Mcgrew, L. F. Marchant, and T. Nishida, (Cambridge: Cambridge University Evol. 133, 146–166. doi: 10.1016/j.jhevol.2019.05.010 Press), 173–184. doi: 10.1017/cbo9780511752414.015 Patel, A. D., and Iversen, J. R. (2014). The evolutionary neuroscience of Schmahmann, J. D. (2019). The cerebellum and cognition. Neurosci. Lett. 688, musical beat perception: the action simulation for auditory prediction (ASAP) 62–75. doi: 10.1016/j.neulet.2018.07.005 hypothesis. Front. Syst. Neurosci. 8:57. doi: 10.3389/fnsys.2014.00057 Schöberl, I., Wedl, M., Beetz, A., and Kotrschal, K. (2017). Psychobiological factors Pinker, S. (1997). How the Mind Works. New York, NY: Norton. affecting cortisol variability in human-dog dyads. PLoS One 12:e0170707. doi: Popova, N. K., Voitenko, N. N., Kulikov, A. V., and Avgustinovich, D. F. 10.1371/journal.pone.0170707 (1991). Evidence for the involvement of central serotonin in mechanism of Sear, R., and Mace, R. (2008). Who keeps children alive? A review of the effects of domestication of silver foxes. Pharmacol. Biochem. Behav. 40, 751–756. doi: kin on child survival. Evol. Hum. Behav. 29, 1–18. doi: 10.1016/j.evolhumbehav. 10.1016/0091-3057(91)90080-l 2007.10.001 Posner, M. I., and Fan, J. (2008). “Attention as an organ system,” in Neurobiology of Shilton, D. (2017). The Communication Technology at the Acheulian Site of Gesher Perception and Communication: From Synapse to Society. The IVth De Lange Benot Ya’aqov. Master’s thesis, Tel Aviv University, Tel Aviv. Conference, ed. J. Pomerantz, (Cambridge, England: Cambridge University Shilton, D. (2019). Is language necessary for the social transmission of Lithic Press). technology? J. Lang. Evol. 4, 124–133. doi: 10.1093/jole/lzz004 Rabinowitch, T. C., and Meltzoff, A. N. (2017). Synchronized movement Silvers, J. A., and Moreira, J. F. G. (2019). Capacity and tendency: a neuroscientific experience enhances peer cooperation in preschool children. J. Exp. Child framework for the study of emotion regulation. Neurosci. Lett. 693, 35–39. Psychol. 160, 21–32. doi: 10.1016/j.jecp.2017.03.001 doi: 10.1016/j.neulet.2017.09.017 Frontiers in Psychology | www.frontiersin.org 20 February 2020 | Volume 11 | Article 134 Shilton et al. Human Social Evolution: Self-Domestication or Self-Control? Simões-Costa, M., and Bronner, M. E. (2015). Establishing neural crest identity: Tomasello, M., Hare, B., Lehmann, H., and Call, J. (2007). Reliance on head versus a gene regulatory recipe. Development 142, 242–257. doi: 10.1242/dev. eyes in the gaze following of great apes and human infants: the cooperative 105445 eye hypothesis. J. Hum. Evol. 52, 314–320. doi: 10.1016/j.jhevol.2006. Skulachev, V. P., Holtze, S., Vyssokikh, M. Y., Bakeeva, L. E., Skulachev, M. V., 10.001 Markov, A. V., et al. (2017). Neoteny, prolongation of youth: from naked Tost, H., Kolachana, B., Hakimi, S., Lemaitre, H., Verchinski, B. A., Mattay, mole rats to “Naked Apes” (Humans). Physiol. Rev. 97, 699–720. doi: 10.1152/ V. S., et al. (2010). A common allele in the oxytocin receptor gene (OXTR) physrev.00040.2015 impacts prosocial temperament and human hypothalamic-limbic structure and Smith, B., Lucas, T., Norris, R., and Henneberg, M. (2018). Brain size/body weight function. Proc. Natl. Acad. Sci. U.S.A. 107, 13936–13941. doi: 10.1073/pnas. in the dingo (Canis dingo): comparisons with domestic and wild canids. Austr. 1003296107 J. Zool. 65, 292–301. Trut, L. N. (1999). Early canid domestication: the farm-fox experiment. Am. Sci. Smith, D., Schlaepfer, P., Major, K., Dyble, M., Page, A. E., Thompson, J., et al. 87, 160–169. (2017). Cooperation and the evolution of hunter-gatherer storytelling. Nat. Trut, L. N. (2001). “‘Experimental studies of early canid domestication’,” in The Commun. 8:1853. doi: 10.1038/s41467-017-02036-8 Genetics of the Dog, eds A. Ruvinsky, and J. Sampson, (New York, NY: CABI Spurway, H. (1955). The causes of domestication: an attempt to integrate some Publishing), 15–43. ideas of Konrad Lorenz with evolution theory. J. Genet. 53, 325–362. doi: Trut, L. N., Dzerzhinsky, F. J., and Nikolsky, V. S. (1991). Intracranial allometry 10.1007/bf02993986 and morphological changes in silver foxes (Vulpes vulpes) under domestication. Staes, N., Smaers, J. B., Kunkle, A. E., Hopkins, W. D., Bradley, B. J., and Sherwood, Genetika 27, 1605–1611. C. C. (2019). Evolutionary divergence of neuroanatomical organization and Trut, L. N., Kharlamova, A., Kukekova, A., Acland, G., Carrier, D., Chase, related genes in chimpanzees and bonobos. Cortex 118, 154–164. doi: 10.1016/ K., et al. (2006). “Morphology and behavior: are they coupled at the j.cortex.2018.09.016 genome level?,” in The Dog and its Genome, eds E. Ostrander, U. Ginger, Staes, N., Stevens, J. M., Helsen, P., Hillyer, M., Korody, M., and Eens, M. (2014). and K. Lindblad-Toh, (New York, NY: Cold Spring Harbor Laboratory Oxytocin and vasopressin receptor gene variation as a proximate base for inter- Press), 81e93. and intraspecific behavioral differences in bonobos and chimpanzees. PLoS One Trut, L. N., Oskina, I., and Kharlamova, A. (2009). Animal evolution during 9:e113364. doi: 10.1371/journal.pone.0113364 domestication: the domesticated fox as a model. Bioessays 31, 349–360. doi: Stimpson, C. D., Barger, N., Taglialatela, J. P., Gendron-Fitzpatrick, A., Hof, 10.1002/bies.200800070 P. R., Hopkins, W. D., et al. (2016). Differential serotonergic innervation of Trut, L. N., Plyusnina, I. Z., and Oskina, I. N. (2004). An experiment on fox the amygdala in bonobos and chimpanzees. Soc. Cogn. Affect. Neurosci. 11, domestication and debatable issues of evolution of the dog. Russ. J. Genet. 413–422. doi: 10.1093/scan/nsv128 40:644. doi: 10.1023/B:RUGE.0000033312.92773.c1 Stout, D., Hecht, E., Khreisheh, N., Bradley, B., and Chaminade, T. (2015). Udell, M. A., Dorey, N. R., and Wynne, C. D. (2010). What did domestication do Cognitive demands of Lower Paleolithic toolmaking. PLoS One 10:e0121804. to dogs? A new account of dogs’ sensitivity to human actions. Biol. Rev. 85, doi: 10.1371/journal.pone.0121804 327–345. doi: 10.1111/j.1469-185X.2009.00104.x Surbeck, M., Boesch, C., Crockford, C., Thompson, M. E., Furuichi, T., Fruth, B., van den Berg, L., Kwant, L., Hestand, M. S., van Oost, B. A., and Leegwater, P. A. J. et al. (2019). Males with a mother living in their group have higher paternity (2005). Structure and variation of three canine genes involved in serotonin success in bonobos but not chimpanzees. Curr. Biol. 29, R354–R355. doi: 10. binding and transport: the serotonin receptor 1A gene (htr1A), serotonin 1016/j.cub.2019.03.040 receptor 2A gene (htr2A), and serotonin transporter gene (slc6A4). J. Heredity Surbeck, M., Boesch, C., Girard-Buttoz, C., Crockford, C., Hohmann, G., and 96, 786–796. doi: 10.1093/jhered/esi108 Wittig, R. M. (2017). Comparison of male conflict behavior in chimpanzees Voigt, D. R. (1987). “Red fox’,” in Wild Furbearer Management and Conservation (Pan troglodytes) and bonobos (Pan paniscus), with specific regard to coalition in North America, eds M. Novak, J. A. Baker, M. E. Obbard, and B. Malloch, and post-conflict behavior. Am. J. Primatol. 79:e22641. doi: 10.1002/ajp. (Ontario: Ministry of Natural Resources), 378–392. 22641 Wagner, A. D., Pare-Blagoev, E. J., Clark, J., and Poldrack, R. A. (2001). Recovering Surbeck, M., Mundry, R., and Hohmann, G. (2011). Mothers matter! maternal meaning: left prefrontal cortex guides controlled semantic retrieval. Neuron 31, support, dominance status and mating success in male bonobos (Pan paniscus). 329–338. Proc. R. Soc. B Biol. Sci. 278, 590–598. doi: 10.1098/rspb.2010.1572 Wang, X., Pipes, L., Trut, L. N., Herbeck, Y., Vladimirova, A. V., Gulevich, R. G., Tan, J., and Hare, B. (2017). “Prosociality among non-kin in bonobos and et al. (2018). Genomic responses to selection for tame/aggressive behaviors in chimpanzees compared,” in Bonobos: Unique in Mind, Brain, and Behavior, the silver fox (Vulpes vulpes). Proc. Natl. Acad. Sci. U.S.A. 115, 10398–10403. eds B. Hare, and S. Yamamoto, (New York, NY: Oxford University Press), doi: 10.1073/pnas.1800889115 140–153. Wiessner, P. W. (2014). Embers of society: firelight talk among the Ju/’hoansi Tarr, B., Launay, J., and Dunbar, R. I. (2014). Music and social bonding:“self- bushmen. Proc. Natl. Acad. Sci. U.S.A. 111, 14027–14035. doi: 10.1073/pnas. other” merging and neurohormonal mechanisms. Front. Psychol. 5:1096. doi: 1404212111 10.3389/fpsyg.2014.01096 Wilkins, A. S. (2017). Making Faces: The Evolutionary Origins of the Human Face. Theofanopoulou, C., Gastaldon, S., O’Rourke, T., Samuels, B. D., Messner, A., Cambridge, MA: Harvard University Press. Martins, P. T., et al. (2017). Self-domestication in Homo sapiens: insights Wilkins, A. S. (2019). A striking example of developmental bias in an evolutionary from comparative genomics. PLoS One 12:e0185306. doi: 10.1371/journal.pone. process: the “domestication syndrome”. Evol. Dev. 2019:e12319. doi: 10.1111/ 0185306 ede.12319 Thomas, E. M. (2006). The Old Way: A Story of the First People. New York, NY: Wilkins, A. S., Wrangham, R. W., and Fitch, W. T. (2014). The “domestication Farrar, Straus, Giroux. syndrome” in mammals: a unified explanation based on neural crest cell Thomas, J. (2013). Self-Domestication and Language Evolution. Ph.D. thesis, The behavior and genetics. Genetics 197, 795–808. doi: 10.1534/genetics.114. University of Edinburgh, Edinburgh. 165423 Thomas, J., and Kirby, S. (2018). Self domestication and the evolution of language. Wilson, M., and Cook, P. F. (2016). Rhythmic entrainment: why humans Biol. Philos. 33:9. want to, fireflies can’t help it, pet birds try, and sea lions have to be Thompson, J. C., Carvalho, S., Marean, C., and Alemseged, Z. (2019). Origins of the bribed. Psychonom. Bull. Rev. 23, 1647–1659. doi: 10.3758/s13423-016-1 human predatory pattern: the transition to large-animal exploitation by early 013-x hominins. Curr. Anthropol. 60, 1–23. doi: 10.1086/701477 Wobber, V., Hare, B., Lipson, S., Wrangham, R., and Ellison, P. (2013). Tomasello, M. (2008). Origins of Human Communication. Cambridge, MA: MIT Different ontogenetic patterns of testosterone production reflect divergent Press. male reproductive strategies in chimpanzees and bonobos. Physiol. Behav. 116, Tomasello, M. (2009). Why We Cooperate. Cambridge, MA: MIT Press. 44–53. doi: 10.1016/j.physbeh.2013.03.003 Tomasello, M. (2016). A Natural History of Human Morality. Cambridge, MA: Wobber, V., Hare, B., Maboto, J., Lipson, S., Wrangham, R., and Ellison, P. T. Harvard University Press. (2010a). Differential changes in steroid hormones before competition in Frontiers in Psychology | www.frontiersin.org 21 February 2020 | Volume 11 | Article 134 Shilton et al. Human Social Evolution: Self-Domestication or Self-Control? bonobos and chimpanzees. Proc. Natl. Acad. Sci. U.S.A. 107, 12457–12462. [Preprint]. Available at: https://www.biorxiv.org/content/10.1101/570036v1. doi: 10.1073/pnas.1007411107 abstract (accessed January 2020). Wobber, V., Wrangham, R., and Hare, B. (2010b). Bonobos exhibit delayed Zeder, M. A. (2018). Why evolutionary biology needs anthropology: development of social behavior and cognition relative to chimpanzees. Curr. evaluating core assumptions of the extended evolutionary synthesis. Biol. 20, 226–230. doi: 10.1016/j.cub.2009.11.070 Evol. Anthropol. Issues News Rev. 27, 267–284. doi: 10.1002/evan. Wrangham, R. (2002). “The cost of sexual attraction: is there a trade-off in female 21747 pan between sex appeal and received coercion?,” in Behavioral Diversity in Zollikofer, C. P. E., and Ponce de León, M. S. (2010). The evolution of hominin Chimpanzees and Bonobos, eds C. Boesch, G. Hohmann, and L. Marchant, ontogenies. Semin. Cell Dev. Biol. 21, 441–452. doi: 10.1016/j.semcdb.2009. (Cambridge, MA: Cambridge University Press), 204–215. 10.012 Wrangham, R. W. (2018). Two types of aggression in human evolution. Proc. Natl. Acad. Sci. U.S.A. 115, 245–253. doi: 10.1073/pnas.1713611115 Conflict of Interest: The authors declare that the research was conducted in the Wu, N., Li, Z., and Su, Y. (2012). The association between oxytocin receptor absence of any commercial or financial relationships that could be construed as a gene polymorphism (OXTR) and trait empathy. J. Affect. Disord. 138, 468–472. potential conflict of interest. doi: 10.1016/j.jad.2012.01.009 Wu, S., Jia, M., Ruan, Y., Liu, J., Guo, Y., Shuang, M., et al. (2005). Positive Copyright © 2020 Shilton, Breski, Dor and Jablonka. This is an open-access article association of the oxytocin receptor gene (OXTR) with autism in the Chinese distributed under the terms of the Creative Commons Attribution License (CC BY). Han population. Biol. Psychiatry 58, 74–77. doi: 10.1016/j.biopsych.2005.03.013 The use, distribution or reproduction in other forums is permitted, provided the Zanlella, M., Vitriolo, A., Andirko, A., Martins, P. T., Sturm, S., O’Rourke, T., original author(s) and the copyright owner(s) are credited and that the original et al. (2019). 7q11. 23 syndromes reveal BAZ1B as a master regulator of the publication in this journal is cited, in accordance with accepted academic practice. No modern human face and validate the self-domestication hypothesis. bioRxiv use, distribution or reproduction is permitted which does not comply with these terms. Frontiers in Psychology | www.frontiersin.org 22 February 2020 | Volume 11 | Article 134