Elephants as an animal model for self-domestication.

Humans are unique in their sophisticated culture and societal structures, their complex languages, and their extensive tool use. According to the human self-domestication hypothesis, this unique set of traits may be the result of an evolutionary process of self-induced domestication, in which humans evolved to be less aggressive and more cooperative. However, the only other species that has been argued to be self-domesticated besides humans so far is bonobos, resulting in a narrow scope for investigating this theory limited to the primate order. Here, we propose an animal model for studying self-domestication: the elephant. First, we support our hypothesis with an extensive cross-species comparison, which suggests that elephants indeed exhibit many of the features associated with self-domestication (e.g., reduced aggression, increased prosociality, extended juvenile period, increased playfulness, socially regulated cortisol levels, and complex vocal behavior). Next, we present genetic evidence to reinforce our proposal, showing that genes positively selected in elephants are enriched in pathways associated with domestication traits and include several candidate genes previously associated with domestication. We also discuss several explanations for what may have triggered a self-domestication process in the elephant lineage. Our findings support the idea that elephants, like humans and bonobos, may be self-domesticated. Since the most recent common ancestor of humans and elephants is likely the most recent common ancestor of all placental mammals, our findings have important implications for convergent evolution beyond the primate taxa, and constitute an important advance toward understanding how and why self-domestication shaped humans' unique cultural niche.

Domestication as the evolution of interspecies cooperative breeding.

We propose that domestication is the result of interspecies cooperative breeding. Considering domestication as an outcome of cooperative breeding can explain how domestication occurs in both plants and animals, encompass cases of domestication that do not involve humans, and shed light on why humans are involved in so many domesticatory relationships. We review the cooperative breeding model of human evolution, which posits that care of human infants by alloparents enabled the evolution of costly human brains and long juvenile development, while selecting for tolerance of strangers. We then explore how human cooperation in the protection and provisioning of young plants and animals can explain the evolution of domestication traits such as changes in development; loss of aggressive, defensive, and bet-hedging aspects of the phenotype; and increased fertility. We argue that the importance of cooperative breeding to human societies has made humans especially likely to enter into interspecies cooperative breeding relationships.

Janus faced: The co-evolution of war and peace in the human species.

The human species presents a paradox. No other species possesses the propensity to carry out coalitionary lethal attacks on adult conspecifics coupled with the inclination to establish peaceful relations with genetically unrelated groups. What explains this seemingly contradictory feature? Existing perspectives, the "deep roots" and "shallow roots" of war theses, fail to capture the plasticity of human intergroup behaviors, spanning from peaceful cooperation to warfare. By contrast, this article argues that peace and war have both deep roots, and they co-evolved through an incremental process over several million years. On the one hand, humans inherited the propensity for coalitionary lethal violence from their chimpanzee-like ancestor. Specifically, having first inherited the skills to engage in cooperative hunting, they gradually repurposed such capacity to execute coalitionary killings of adult conspecifics and subsequently enhanced it through tech`nological innovations like the use of weapons. On the other hand, they underwent a process of cumulative cultural evolution and, subsequently, of self-domestication which led to heightened cooperative communication and increased prosocial behavior within and between groups. The combination of these two biocultural evolutionary processes-coupled with feedback loop effects between self-domestication and Pleistocene environmental variability-considerably broadened the human intergroup behavioral repertoire, thereby producing the distinctive combination of conflictual and peaceful intergroup relations that characterizes our species. To substantiate this argument, the article synthesizes and integrates the findings from a variety of disciplines, leveraging evidence from evolutionary anthropology, primatology, archeology, paleo-genetics, and paleo-climatology.

Revisiting Emil Kraepelin's eugenic arguments.

It is widely recognized that Emil Kraepelin explicitly advocated for eugenic ideas in his academic works. Given the renewed interest in related concepts such as self-domestication and neo-Lamarckism in different contexts, this article revisits his eugenic arguments by scrutinizing a section of his seminal work, the 8th edition of his textbook published in 1909. Our analysis reveals that Kraepelin's arguments consisted of multiple theories and ideas prevalent at the time (i.e. self-domestication hypothesis, neo-Lamarckism, degeneration theory, social Darwinism, racism and ethnic nationalism), each of which presented individual fundamental claims. Nevertheless, Kraepelin amalgamated them into one combined narrative, which crystallized into an anti-humanistic psychiatry in the next generation. This paper cautions that a similar 'packaging of ideas' might be emerging now.

Abnormal features of human self-domestication in bipolar disorder.

Bipolar disorder (BD) is a severe mental condition characterized by episodes of elevated mood and depression. Being a heritable condition, it features a complex genetic architecture, although it is not still clear how genes contribute to the onset and course of the disease. In this paper, we adopted an evolutionary-genomic approach to this condition, focusing on changes occurred during human evolution as a source of our distinctive cognitive and behavioural phenotype. We show clinical evidence that the BD phenotype can be construed as an abnormal presentation of the human self-domestication phenotype. We further demonstrate that candidate genes for BD significantly overlap with candidates for mammal domestication and that this common set of genes is enriched in functions that are important for the BD phenotype, especially neurotransmitter homeostasis. Finally, we show that candidates for domestication are differentially expressed in brain regions involved in BD pathology, particularly, the hippocampus and the prefrontal cortex, which have been subject to recent changes in our species. Overall, this link between human self-domestication and BD should facilitate a better understanding of the BD etiopathology.

Shared reproductive disruption, not neural crest or tameness, explains the domestication syndrome.

Altered neural crest cell (NCC) behaviour is an increasingly cited explanation for the domestication syndrome in animals. However, recent authors have questioned this explanation, while others cast doubt on whether domestication syndrome even exists. Here, we review published literature concerning this syndrome and the NCC hypothesis, together with recent critiques of both. We synthesize these contributions and propose a novel interpretation, arguing shared trait changes under ancient domestication resulted primarily from shared disruption of wild reproductive regimes. We detail four primary selective pathways for 'reproductive disruption' under domestication and contrast these succinct and demonstrable mechanisms with cryptic genetic associations posited by the NCC hypothesis. In support of our perspective, we illustrate numerous important ways in which NCCs contribute to vertebrate reproductive phenotypes, and argue it is not surprising that features derived from these cells would be coincidentally altered under major selective regime changes, as occur in domestication. We then illustrate several pertinent examples of Darwin's 'unconscious selection' in action, and compare applied selection and phenotypic responses in each case. Lastly, we explore the ramifications of reproductive disruption for wider evolutionary discourse, including links to wild 'self-domestication' and 'island effect', and discuss outstanding questions.

The gradual coevolution of syntactic combinatorics and categorization under the effects of human self-domestication: a proposal.

The gradual emergence of syntax has been claimed to be engaged in a feedback loop with Human Self-Domestication (HSD), both processes resulting from, and contributing to, enhanced connectivity in selected cortico-striatal networks, which is the mechanism for attenuating reactive aggression, the hallmark of HSD, but also the mechanism of cross-modality, relevant for syntax. Here, we aim to bridge the gap between these brain changes and further changes facilitated by the gradual complexification of grammars. We propose that increased cross-modality would have enabled and supported, more specifically, a feedback loop between categorization abilities relevant for vocabulary building and the gradual emergence of syntactic structure, including Merge. In brief, an enhanced categorization ability not only brings about more distinct categories, but also a critical number of tokens in each category necessary for Merge to take off in a systematic and productive fashion; in turn, the benefits of expressive capabilities brought about by productive Merge encourage more items to be categorized, and more categories to be formed, thus further potentiating categorization abilities, and with it, syntax again. We support our hypothesis with evidence from the domains of language development and animal communication, but also from biology, neuroscience, paleoanthropology, and clinical linguistics.

An evolutionary account of impairment of self in cognitive disorders.

Recent research has proposed that certain aspects of psychosis, as experienced in, e.g., schizophrenia (SCZ), but also aspects of other cognitive conditions, such as autism spectrum disorders (ASD) and synesthesia, can be related to a shattered sense of the notion of self. In this paper, our goal is to show that altered processing of self can be attributed to an abnormal functioning of cortico-striatal brain networks supporting, among other, one key human distinctive cognitive ability, namely cross-modality, which plays multiple roles in human cognition and language. Specifically, our hypothesis is that this cognitive mechanism sheds light both on some basic aspects of the minimal self and on some aspects related to higher forms of self, such as the narrative self. We further link the atypical functioning in these conditions to some recent evolutionary changes in our species, specifically, an atypical presentation of human self-domestication (HSD) features. In doing so, we also lean on previous work concerning the link between cognitive disorders and language evolution under the effects of HSD. We further show that this approach can unify both linguistic and non-linguistic symptoms of these conditions through deficits in the notion of self. Our considerations provide further support for the hypothesis that SCZ and ASD are diametrically opposed cognitive conditions, as well for the hypothesis that their etiology is associated with recent human evolution, leading to a deeper understanding of the causes and symptoms of these disorders, and providing new cues, which can be used for an earlier and more accurate diagnostics.

DLX5/6 GABAergic Expression Affects Social Vocalization: Implications for Human Evolution.

DLX5 and DLX6 are two closely related transcription factors involved in brain development and in GABAergic differentiation. The DLX5/6 locus is regulated by FoxP2, a gene involved in language evolution and has been associated with neurodevelopmental disorders and mental retardation. Targeted inactivation of Dlx5/6 in mouse GABAergic neurons (Dlx5/6VgatCre mice) results in behavioral and metabolic phenotypes notably increasing lifespan by 33%. Here, we show that Dlx5/6VgatCre mice present a hyper-vocalization and hyper-socialization phenotype. While only 7% of control mice emitted more than 700 vocalizations/10 min, 30% and 56% of heterozygous or homozygous Dlx5/6VgatCre mice emitted more than 700 and up to 1,400 calls/10 min with a higher proportion of complex and modulated calls. Hyper-vocalizing animals were more sociable: the time spent in dynamic interactions with an unknown visitor was more than doubled compared to low-vocalizing individuals. The characters affected by Dlx5/6 in the mouse (sociability, vocalization, skull, and brain shape…) overlap those affected in the "domestication syndrome". We therefore explored the possibility that DLX5/6 played a role in human evolution and "self-domestication" comparing DLX5/6 genomic regions from Neanderthal and modern humans. We identified an introgressed Neanderthal haplotype (DLX5/6-N-Haplotype) present in 12.6% of European individuals that covers DLX5/6 coding and regulatory sequences. The DLX5/6-N-Haplotype includes the binding site for GTF2I, a gene associated with Williams-Beuren syndrome, a hyper-sociability and hyper-vocalization neurodevelopmental disorder. The DLX5/6-N-Haplotype is significantly underrepresented in semi-supercentenarians (>105 years of age), a well-established human model of healthy aging and longevity, suggesting their involvement in the coevolution of longevity, sociability, and speech.

Two types of aggression in human evolution.

Two major types of aggression, proactive and reactive, are associated with contrasting expression, eliciting factors, neural pathways, development, and function. The distinction is useful for understanding the nature and evolution of human aggression. Compared with many primates, humans have a high propensity for proactive aggression, a trait shared with chimpanzees but not bonobos. By contrast, humans have a low propensity for reactive aggression compared with chimpanzees, and in this respect humans are more bonobo-like. The bimodal classification of human aggression helps solve two important puzzles. First, a long-standing debate about the significance of aggression in human nature is misconceived, because both positions are partly correct. The Hobbes-Huxley position rightly recognizes the high potential for proactive violence, while the Rousseau-Kropotkin position correctly notes the low frequency of reactive aggression. Second, the occurrence of two major types of human aggression solves the execution paradox, concerned with the hypothesized effects of capital punishment on self-domestication in the Pleistocene. The puzzle is that the propensity for aggressive behavior was supposedly reduced as a result of being selected against by capital punishment, but capital punishment is itself an aggressive behavior. Since the aggression used by executioners is proactive, the execution paradox is solved to the extent that the aggressive behavior of which victims were accused was frequently reactive, as has been reported. Both types of killing are important in humans, although proactive killing appears to be typically more frequent in war. The biology of proactive aggression is less well known and merits increased attention.

Recent selection of candidate genes for mammal domestication in Europeans and language change in Europe: a hypothesis.

BACKGROUND AND AIM: Human evolution resulted from changes in our biology, behaviour, and culture. One source of these changes has been hypothesised to be our self-domestication (that is, the development in humans of features commonly found in domesticated strains of mammals, seemingly as a result of selection for reduced aggression). Signals of domestication, notably brain size reduction, have increased in recent times. METHODS: In this paper, we compare whole-genome data between the Late Neolithic/Bronze Age individuals and modern Europeans. RESULTS: We show that genes associated with mammal domestication and with neural crest development and function are significantly differently enriched in nonsynonymous single nucleotide polymorphisms between these two groups. CONCLUSION: We hypothesise that these changes might account for the increased features of self-domestication in modern humans and, ultimately, for subtle recent changes in human cognition and behaviour, including language.

Mental time travel, language evolution, and human self-domestication.

Human self-domestication might have contributed to the evolutionary changes in the hippocampus accounting for our enhanced mental travel abilities, and ultimately for our sophisticated language.

Playing with language, creating complexity: Has play contributed to the evolution of complex language?

We argue that enhanced play may have contributed to the emergence of complex language systems in modern humans (Homo sapiens). To support this idea, we first discuss evidence for an expansion of playing behavior connected to the extended childhood of modern human children, and the potential of this period for the transmission of complex cultural traits, including language. We then link two of the most important functions of play-exploration and innovation-to the potential for cumulative cultural evolution in general and for the emergence of complex language in particular. If correct, the shorter childhood of Neanderthals-involving restrictions on time to experiment and innovate-may have restricted their language (and other symbolic) system/s. Consequently, fully investigating the role that play may have had in the transmission of language and the development of symbolic cultures in both modern humans and Neanderthals provides a new avenue of research for Paleolithic archaeology and related disciplines.

Wild bonobo and chimpanzee females exhibit broadly similar patterns of behavioral maturation but some evidence for divergence.

OBJECTIVES: Primates exhibit variation in rates of growth and development. Variation in female growth and development across ape species appears to be explained by the Ecological Risk Aversion Hypothesis (ERAH). Indeed, existing data on variation in somatic growth and reproductive maturation between humans' closest living ape relatives, bonobos and chimpanzees, appear to be consistent with this hypothesis. However, existing data on behavioral maturation between the two species appear to contradict this hypothesis. We present novel behavioral data on infant and juvenile females from wild populations of both species in order to further evaluate predictions of the ERAH as it relates to the speed of behavioral maturation. MATERIALS AND METHODS: We analyzed 3 years of behavioral data on 17 female bonobos (<8 years of age) from LuiKotale, Democratic Republic of the Congo and 40 years of behavioral data on 30 age-matched female chimpanzees from Gombe, Tanzania. We compared the timing of (a) the attainment of independence from mothers and (b) the development of social skills using the following proxies: proximity between females and their mothers and the time that females spent engaged in eating, suckling, social play, social grooming, and riding on their mothers. RESULTS: We did not find species differences in the proportion of time that females spent in contact with their mothers or engaged in eating, suckling, social play, or social grooming. Female bonobos spent more time riding on their mothers than did female chimpanzees. Female bonobos spent more time at distances greater than 5 m from their mothers during the ages of 3-8 years, but females did not differ during the ages of 0-3 years. DISCUSSION: Behavioral maturation is largely similar between females of the two species based on the ages and proxies considered herein. We propose alternative explanations for the differences that we found in proximity and riding that do not invoke differences in underlying rates of maturation.

Survival of the Friendliest: Homo sapiens Evolved via Selection for Prosociality.

The challenge of studying human cognitive evolution is identifying unique features of our intelligence while explaining the processes by which they arose. Comparisons with nonhuman apes point to our early-emerging cooperative-communicative abilities as crucial to the evolution of all forms of human cultural cognition, including language. The human self-domestication hypothesis proposes that these early-emerging social skills evolved when natural selection favored increased in-group prosociality over aggression in late human evolution. As a by-product of this selection, humans are predicted to show traits of the domestication syndrome observed in other domestic animals. In reviewing comparative, developmental, neurobiological, and paleoanthropological research, compelling evidence emerges for the predicted relationship between unique human mentalizing abilities, tolerance, and the domestication syndrome in humans. This synthesis includes a review of the first a priori test of the self-domestication hypothesis as well as predictions for future tests.

Female status, food security, and stature sexual dimorphism: Testing mate choice as a mechanism in human self-domestication.

OBJECTIVES: Humans exhibit multiple anatomical and behavioral signatures of domestication syndrome, leading evolutionary-minded scholars to suggest Homo sapiens is a "self-domesticated" species. We examined one of three mechanisms proposed to explain human self-domestication-that is, intersexual selection against reactive aggression. We hypothesized that this process has been, at least in part, caused by context-dependent female preferences for less-aggressive males. We predicted that societies where women have higher social status will show relatively elevated signs of self-domestication-as indicated by lower stature sexual dimorphism (SSD)-and that this relationship should be mediated by food security. MATERIALS AND METHODS: To test our prediction, we used male and female stature data for 28 societies from the Standard Cross-Cultural Sample. We applied multivariate regression to examine our hypothesis while controlling for theoretically important confounders. RESULTS: We found convincing support for the prediction that the relationship between SSD and female status is mediated by food security. As predicted, higher female status was associated with less sexual dimorphism and the effect is stronger when food resources are secure. DISCUSSION: Context-dependent female mate choices significantly contribute to lower SSD, suggesting female mate choice is likely to have played an influential role in human self-domestication. Future research on this theme will benefit by including more of the expected symptoms of human self-domestication and examining other potential drivers of this process.

Differences in expression of male aggression between wild bonobos and chimpanzees.

Researchers investigating the evolution of human aggression look to our closest living relatives, bonobos (Pan paniscus) and chimpanzees (Pan troglodytes), as valuable sources of comparative data.1,2 Males in the two species exhibit contrasting patterns: male chimpanzees sexually coerce females3,4,5,6,7,8 and sometimes kill conspecifics,9,10,11,12 whereas male bonobos exhibit less sexual coercion13,14 and no reported killing.13 Among the various attempts to explain these species differences, the self-domestication hypothesis proposes negative fitness consequences of male aggression in bonobos.2,15,16 Nonetheless, the extent to which these species differ in overall rates of aggression remains unclear due to insufficiently comparable observation methods.17,18,19,20,21,22,23 We used 14 community-years of focal follow data-the gold standard for observational studies24-to compare rates of male aggression in 3 bonobo communities at the Kokolopori Bonobo Reserve, Democratic Republic of Congo, and 2 chimpanzee communities at Gombe National Park, Tanzania. As expected, given that females commonly outrank males, we found that bonobos exhibited lower rates of male-female aggression and higher rates of female-male aggression than chimpanzees. Surprisingly, we found higher rates of male-male aggression among bonobos than chimpanzees even when limiting analyses to contact aggression. In both species, more aggressive males obtained higher mating success. Although our findings indicate that the frequency of male-male aggression does not parallel species difference in its intensity, they support the view that contrary to male chimpanzees, whose reproductive success depends on strong coalitions, male bonobos have more individualistic reproductive strategies.25.

The evolutionary neuroscience of domestication.

How does domestication affect the brain? This question has broad relevance. Domesticated animals play important roles in human society, and substantial recent work has addressed the hypotheses that a domestication syndrome links phenotypes across species, including Homo sapiens. Surprisingly, however, neuroscience research on domestication remains largely disconnected from current knowledge about how and why brains change in evolution. This article aims to bridge that gap. Examination of recent research reveals some commonalities across species, but ultimately suggests that brain changes associated with domestication are complex and variable. We conclude that interactions between behavioral, metabolic, and life-history selection pressures, as well as the role the role of experience and environment, are currently largely overlooked and represent important directions for future research.

Scleral appearance is not a correlate of domestication in mammals.

Numerous hypotheses try to explain the unusual appearance of the human eye with its bright sclera and transparent conjunctiva and how it could have evolved from a dark-eyed phenotype, as is present in many non-human primates. Recently, it has been argued that pigmentation defects induced by self-domestication may have led to bright-eyed ocular phenotypes in humans and some other primate lineages, such as marmosets. However, it has never been systematically studied whether actual domesticated mammals consistently deviate from wild mammals in regard to their conjunctival pigmentation and if this trait might therefore be part of a domestication syndrome. Here, we test this idea by drawing phylogenetically informed comparisons from a photographic dataset spanning 13 domesticated mammal species and their closest living wild relatives (n ≥ 15 photos per taxon). We did not recover significant differences in scleral appearance or irido-scleral contrast between domesticated and wild forms, suggesting that conjunctival depigmentation, unlike cutaneous pigmentation disorders, is not a general correlate of domestication. Regardless of their domestication status, macroscopically depigmented conjunctivae were observed in carnivorans and lagomorphs, whereas ungulates generally displayed darker eyes. For some taxa, we observed pronounced intraspecific variation, which should be addressed in more exhaustive future studies. Based on our dataset, we also present preliminary evidence for a general increase of conjunctival pigmentation with eye size in mammals. Our findings suggest that conjunctival depigmentation in humans is not a byproduct of self-domestication, even if we assume that our species has undergone such a process in its recent evolutionary history.

Female cooperative labour networks in hunter-gatherers and horticulturalists.

Cooperation in food acquisition is a hallmark of the human species. Given that costs and benefits of cooperation vary among production regimes and work activities, the transition from hunting-and-gathering to agriculture is likely to have reshaped the structure of cooperative subsistence networks. Hunter-gatherers often forage in groups and are generally more interdependent and experience higher short-term food acquisition risk than horticulturalists, suggesting that cooperative labour should be more widespread and frequent for hunter-gatherers. Here we compare female cooperative labour networks of Batek hunter-gatherers of Peninsular Malaysia and Tsimane forager-horticulturalists of Bolivia. We find that Batek foraging results in high daily variation in labour partnerships, facilitating frequent cooperation in diffuse networks comprised of kin and non-kin. By contrast, Tsimane horticulture involves more restricted giving and receiving of labour, confined mostly to spouses and primary or distant kin. Tsimane women also interact with few individuals in the context of hunting/fishing activities and forage mainly with spouses and primary kin. These differences give rise to camp- or village-level networks that are more modular (have more substructure when partitioned) among Tsimane horticulturalists. Our findings suggest that subsistence activities shape the formation and extent of female social networks, particularly with respect to connections with other women and non-kin. We discuss the implications of restricted female labour networks in the context of gender relations, power dynamics and the adoption of farming in humans. This article is part of the theme issue 'Cooperation among women: evolutionary and cross-cultural perspectives'.