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.

The genomic landscape of mammal domestication might be orchestrated by selected transcription factors regulating brain and craniofacial development.

Domestication transforms once wild animals into tamed animals that can be then exploited by humans. The process entails modifications in the body, cognition, and behavior that are essentially driven by differences in gene expression patterns. Although genetic and epigenetic mechanisms were shown to underlie such differences, less is known about the role exerted by trans-regulatory molecules, notably transcription factors (TFs) in domestication. In this paper, we conducted extensive in silico analyses aimed to clarify the TF landscape of mammal domestication. We first searched the literature, so as to establish a large list of genes selected with domestication in mammals. From this list, we selected genes experimentally demonstrated to exhibit TF functions. We also considered TFs displaying a statistically significant number of targets among the entire list of (domestication) selected genes. This workflow allowed us to identify 5 candidate TFs (SOX2, KLF4, MITF, NR3C1, NR3C2) that were further assessed in terms of biochemical and functional properties. We found that such TFs-of-interest related to mammal domestication are all significantly involved in the development of the brain and the craniofacial region, as well as the immune response and lipid metabolism. A ranking strategy, essentially based on a survey of protein-protein interactions datasets, allowed us to identify SOX2 as the main candidate TF involved in domestication-associated evolutionary changes. These findings should help to clarify the molecular mechanics of domestication and are of interest for future studies aimed to understand the behavioral and cognitive changes associated to domestication.

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.

Enrichment of self-domestication and neural crest function loci in the heritability of neurodevelopmental disorders.

Self-domestication could contribute to shaping the biology of human brain and consequently the predisposition to neurodevelopmental disorders. Leveraging genome-wide data from the Psychiatric Genomics Consortium, we tested the enrichment of self-domestication and neural crest function loci with respect to the heritability of autism spectrum disorder, schizophrenia (SCZ in East Asian and European ancestries, EAS and EUR, respectively), attention-deficit/hyperactivity disorder, obsessive-compulsive disorder, and Tourette's syndrome (TS). Considering only self-domestication and neural-crest-function annotations in the linkage disequilibrium score regression (LDSC) model, our partitioned heritability analysis revealed statistically significant enrichments across all disorders investigated. The estimates of the heritability enrichments for self-domestication loci were similar across neurodevelopmental disorders, ranging from 0.902 (EAS SCZ, p = 4.55 × 10-20) to 1.577 (TS, p = 5.85 × 10-5). Conversely, a wider spectrum of heritability enrichment estimates was present for neural crest function with the highest enrichment observed for TS (enrichment = 3.453, p = 2.88 × 10-3) and the lowest for EAS SCZ (enrichment = 1.971, p = 3.81 × 10-3). Although these estimates appear to be strong, the enrichments for self-domestication and neural crest function were null once we included additional annotations related to different genomic features. This indicates that the effect of self-domestication on the polygenic architecture of neurodevelopmental disorders is not independent of other functions of human genome.

The human fear paradox turns out to be less paradoxical when global changes in human aggression and language evolution are considered.

Our commentary focuses on the interaction between Grossmann's fearful ape hypothesis (FAH) and the human self-domestication hypothesis (HSDH), also taking into account language acquisition and evolution. Although there is considerable overlap between the two hypotheses, there are also some discrepancies, and our goal is to consider the extent to which HSDH can explain the phenomena identified by FAH without invoking fearfulness as directly adaptive.

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.

Human-specific changes in two functional enhancers of FOXP2.

FOXP2 is a gene involved in language development and function. Neanderthals and humans share the same coding region of the gene, although the formers are thought to have exhibited less sophisticated language abilities. In this paper, we report on several human-specific changes in two functional enhancers of FOXP2. Two of these variants are located within the binding sites for the transcription factors POLR2A and SMARCC1, respectively. Interestingly, SMARCC1 is involved in brain development and vitamin D metabolism. We hypothesize that the human specific change in this position might have resulted in a different regulation pattern of FOXP2 expression in our species compared to extinct hominins, with a potential impact on our language abilities.

Communication deficits in a case of a deletion in 7q31.1-q31.33 encompassing FOXP2.

Copy number variants (CNVs) found in individuals with communication deficits provide a valuable window to the genetic causes of problems with language and, more generally, to the genetic foundation of the human-specific ability to learn and use languages. This paper reports on the language and communication problems of a patient with a microduplication in 22q11.23 and a microdeletion in 7q31.1-q1.33 encompassing FOXP2. The proband exhibits severe speech problems and moderate comprehension deficits, whereas her pragmatic abilities are a relative strength, as she uses gestures quite competently to compensate for her expressive issues. This profile is compatible with the deficiencies found in patients with similar CNVs, particularly with people bearing microdeletions in 7q31.1-q31.33.

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.

Evolutionary linguistics can help refine (and test) hypotheses about how music might have evolved.

Both the music and social bonding (MSB) hypothesis and the music as a credible signal hypothesis emerge as solid views of how human music and human musicality might have evolved. Nonetheless, both views could be improved (and tested in better ways) with the consideration of the way in which human language(s) might have evolved under the effects of our self-domestication.

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.

Language impairment with a microduplication in 1q42.3q43.

Deletions and duplications of the distal region of the long arm of chromosome 1 are associated with brain abnormalities and developmental delay. Because duplications are less frequent than deletions, no detailed account of the cognitive profile of the affected people is available, particularly, regarding their language (dis)abilities. In this paper we report on the cognitive and language capacities of a girl with one of the smallest interstitial duplications ever described in this region, affecting to 1q42.3q43 (arr[hg19] 1q42.3q43(235,963,632-236,972,276)x3), and advance potential candidate genes for the observed deficits. The proband's speech is severely impaired, exhibiting dysarthric-like features, with speech problems also resulting from a phonological deficit boiling down to a verbal auditory memory deficit. Lexical and grammatical knowledge are also impaired, impacting negatively on both expressive and receptive abilities, seemingly as a consequence of the phonological deficit. Still, her pragmatic abilities seem to be significantly spared, granting her a good command on the principles governing conversational exchanges. Genetic analyses point to several genes of interest. These include one gene within the duplicated region (LYST), one predicted functional partner (CMIP), and three genes outside the 1q42.3q43 region, which are all highly expressed in the cerebellum: DDIT4 and SLC29A1, found strongly downregulated in the proband compared to her healthy parents, and CNTNAP3, found strongly upregulated. The genes highlighted in the paper emerge as potential candidates for the phonological and speech deficits exhibited by the proband and ultimately, for her problems with 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.

Functional characterization of two enhancers located downstream FOXP2.

BACKGROUND: Mutations in the coding region of FOXP2 are known to cause speech and language impairment. However, it is not clear how dysregulation of the gene contributes to language deficit. Interestingly, microdeletions of the region downstream the gene have been associated with cognitive deficits. METHODS: Here, we investigate changes in FOXP2 expression in the SK-N-MC neuroblastoma human cell line after deletion by CRISPR-Cas9 of two enhancers located downstream of the gene. RESULTS: Deletion of any of these two functional enhancers downregulates FOXP2, but also upregulates the closest 3' gene MDFIC. Because this effect is not statistically significant in a HEK 293 cell line, derived from the human kidney, both enhancers might confer a tissue specific regulation to both genes. We have also found that the deletion of any of these enhancers downregulates six well-known FOXP2 target genes in the SK-N-MC cell line. CONCLUSIONS: We expect these findings contribute to a deeper understanding of how FOXP2 and MDFIC are regulated to pace neuronal development supporting cognition, speech and language.

Differences in the Neanderthal BRCA2 gene might be related to their distinctive cognitive profile.

The unique divergence of the BRCA2 gene in Neanderthals compared to modern humans has been hypothesized to account for a differential susceptibility to cancer. However, the role of the gene in brain development and its connection with autism suggest that these differences might be (also) related to the more encapsulated nature of the Neanderthal cognition and their (inferred) autistic-like features.

Schizophrenia and Human Self-Domestication: An Evolutionary Linguistics Approach.

Schizophrenia (SZ) is a pervasive neurodevelopmental disorder that entails social and cognitive deficits, including marked language problems. Its complex multifactorial etiopathogenesis, including genetic and environmental factors, is still widely uncertain. SZ incidence has always been high and quite stable in human populations, across time and regardless of cultural implications, for unclear reasons. It has been hypothesized that SZ pathophysiology may involve the biological components that changed during the recent human evolutionary history, and led to our distinctive mode of cognition, which includes language skills. In this paper we explore this hypothesis, focusing on the self-domestication of the human species. This has been claimed to account for many human-specific distinctive traits, including aspects of our behavior and cognition, and to favor the emergence of complex languages through cultural evolution. The "domestication syndrome" in mammals comprises the constellation of traits exhibited by domesticated strains, seemingly resulting from the hypofunction of the neural crest. It is our intention to show that people with SZ exhibit more marked domesticated traits at the morphological, physiological, and behavioral levels. We also show that genes involved in domestication and neural crest development and function comprise nearly 20% of SZ candidates, most of which exhibit altered expression profiles in the brain of SZ patients, specifically in areas involved in language processing. Based on these observations, we conclude that SZ may represent an abnormal ontogenetic itinerary for the human faculty of language, resulting, at least in part, from changes in genes important for the domestication syndrome and primarily involving the neural crest.

Linguistic correlates of societal variation: A quantitative analysis.

Traditionally, many researchers have supported a uniformitarian view whereby all languages are of roughly equal complexity, facilitated by internal trade-offs between complexity at different levels, such as morphology and syntax. The extent to which the speakers' societies influence the trade-offs has not been well studied. In this paper, we focus on morphology and syntax, and report significant correlations between specific linguistic and societal features, in particular those relating to exoteric (open) vs. esoteric (close-knit) society types, characterizable in terms of population size, mobility, communication across distances, etc. We conduct an exhaustive quantitative analysis drawing upon WALS, D-Place, Ethnologue and Glottolog, finding some support for our hypothesis that languages spoken by exoteric societies tend towards more complex syntaxes, while languages spoken by esoteric societies tend towards more complex morphologies.

Revisiting the hypothesis of language retrogenesis from an evolutionary perspective.

OBJECTIVE: In this article, we reexamine the hypothesis of language retrogenesis, that is, the assumption that language change over healthy ageing mirrors, albeit inversely, language acquisition by the child. We additionally question whether this inverse pattern can as well be observed at the cognitive and neurobiological levels, and whether it can be informative (and a consequence, in fact) of how language evolved in humans. METHOD: We compare the language strengths and weaknesses signifying language acquisition and its eventual decay in healthy ageing. We further compare age-related cognitive and neurobiological readjustments during each of these two developmental stages, with a focus on brain areas involved in language processing. Finally, we delve into the evolutionary changes experienced by these areas. RESULTS: We present evidence supporting the hypothesis of retrogenesis in two domains of language: the lexicon (lexical access, understanding of nonliteral meanings, and resolution of lexical competition) and syntax (understanding and production of complex sentences). Additionally, we show evidence that the brain areas supporting these complex tasks are late-myelinated in childhood and early-demyelinated during ageing. Finally, we show that some of these areas (such as the inferior frontal gyrus) are phylogenetically newer. CONCLUSIONS: Language acquisition in children and language degradation/loss in healthy ageing follow the principle of retrogenesis, but mostly in domains that are cognitively demanding and that depend on recently evolved brain devices. Putting this differently, the components of language that emerged more recently appear to be more, and earlier, affected during ageing, as well as developed later over childhood. (PsycInfo Database Record (c) 2023 APA, all rights reserved).