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The "Domestication Syndrome" in Mammals: A Unified Explanation Based on Neural Crest Cell Behavior and Genetics
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Charles Darwin, while trying to devise a general theory of heredity from the observations of animal and plant breeders, discovered that domesticated mammals possess a distinctive and unusual suite of heritable traits not seen in their wild progenitors. Some of these traits also appear in domesticated birds and fish. The origin of Darwin's "domestication syndrome" has remained a conundrum for more than 140 years. Most explanations focus on particular traits, while neglecting others, or on the possible selective factors involved in domestication rather than the underlying developmental and genetic causes of these traits. Here, we propose that the domestication syndrome results predominantly from mild neural crest cell deficits during embryonic development. Most of the modified traits, both morphological and physiological, can be readily explained as direct consequences of such deficiencies, while other traits are explicable as indirect consequences. We first show how the hypothesis can account for the multiple, apparently unrelated traits of the syndrome and then explore its genetic dimensions and predictions, reviewing the available genetic evidence. The article concludes with a brief discussion of some genetic and developmental questions raised by the idea, along with specific predictions and experimental tests.
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... The domestication of behaviors is specific to animals and represents a unique and challenging aspect to study. Behavioral 'domestication syndromes' (Wilkins et al., 2014), such as reduced fear of humans and tolerance to the stress of the domesticated environment, are the prerequisites for the successful domestication of animals. The brain is the central nervous system that directs and coordinates all parts of the body to carry out complex activities. ...
... The silkworm, Bombyx mori, is the only fully domesticated insect. Like other domesticated animals, there are significant differences between domestic and wild silkworms, including the behavioral 'domestication syndromes' (Wilkins et al., 2014). Compared with mammals and birds, insect brains are much simpler, making them ideal for investigating brain domestication. ...
... Domestication may result in an increased biomass of the whole body, including the brain, but the increase in brain size does not match the increase in body mass (Gonzalez-Voyer et al., 2009;Henriksen et al., 2016;Katajamaa et al., 2018), as is consistently observed in the domestic silkworm B. mori. In the red junglefowl, the reduced brain size has been reported to be associated with a reduced fear of humans (Katajamaa & Jensen, 2020), which is the crucial basis for animal domestication (Wilkins et al., 2014). In the domestic silkworm B. mori, less fear may be reflected as greater endurance to human handling, compared with its wild ancestor B. mandarina. ...
As in other domestic animals, the silkworm Bombyx mori has evolved adaptive behavioral changes compared with its wild ancestor, Bombyx mandarina . Domestication may have significantly impacted the brain of the silkworm, but it remains unclear whether and how the brain has evolved in response to domestication. Here we systematically quantified and compared morphological differences in the brains of domestic and wild silkworms at 7 representative stages during metamorphosis, and revealed that the B. mori brain had a reduced brain area and a reduced degree of fusion compared with the B. mandarina brain. The 2 silkworm species exhibited divergent brain developmental transcriptomic landscapes, implying the reshaping of brain functions during domestication. Genes enriched in nervous system development were generally repressed in the domesticated brain, with a slight upregulation during the wandering stage. An upregulation of Toll and Imd and a disturbance of apoptotic homeostasis were identified in the domestic silkworm brain. Mapping a comprehensive interaction network of these pathways and nervous system‐related processes identified one key gene, Stx1b , and several candidate domestication genes that may have coordinated the developmental changes in the brain of the silkworm during domestication.
... These cells are integral to the formation of various tissues, including those in the skin, adrenal glands, and facial structures. Consequently, variations in NCC development can account for the diverse traits observed in domesticated species (Wilkins et al., 2014, Singh et al., 2017, Lesch et al., 2022, Rubio and Summers, 2022. ...
... Morphological traits: Common physical characteristics associated with domestication include piebald pigmentation, white patches on the fur or feathers, floppy ears or combs, curled tails, and a reduction of craniofacial dimensions. These morphological changes are hypothesised to be linked to alterations in the development of neural crest cells during embryonic development (Wilkins et al., 2014, Singh et al., 2017, Lesch et al., 2022. Physiological changes: Domesticated animals often exhibit modifications in adrenal gland function and brain structure, which is associated with their altered responses to stress and changes in reproductive physiology (Popova, 2017, Gleeson andWilson, 2023). ...
... Research suggests that domesticated animals exhibit downregulated hypothalamic-pituitary-adrenal-axis (HPA-axis) and altered serotonin levels, that also takes longer time to fully develop, making it possible to be exposed to humans for longer as young, without a complete physiological stress response, hence domesticated animals can habituate easier towards humans (Wilkins et al., 2014, Geiger et al., 2018. Studies on the stress response in rats reveals that domesticated, or tame, individuals exhibit lower baseline levels of corticosterone yet demonstrate a more pronounced glucocorticoidmediated response to stress compared to their aggressive counterparts. ...
... A set of phenotypic variations in domestic mammals compared to their wild counterparts roughly speaking includes smaller body shape, thinner bones, changed fur color, smaller teeth, retracted snout and brain mass shrinkage, etc. more docile temperament in terms of behavior, prolonged early childhood, decreased aggression, increased prosocial behavior, etc [2][3][4][5]. Domestication of a set of mammals in terms of behavior, physiology and shape of the phenotypic variant of the state is called "domestication syndrome DS" [2,[6][7][8][9][10][11]. DS in humans has also been further ...
... Some researchers explain the cause of DS from the perspective of changes in neural crest cell function [9]. Such mechanisms should be an intermediate link in the causal sequence from behavioral changes to morphological responses. ...
Early scholars such as Darwin noted that a series of similar trait changes occurred between domesticated mammals and their wild counterparts, and that similar trait changes occurred in humans. Follow-up studies in recent years have further confirmed the findings of earlier scholars. These changes are known as domestication syndrome (DS). Human DS variation occurred over the course of two to three hundred thousand years before and after the formation of Homo sapiens, and is thought to be the result of human self-domestication. The main way to realize human self-domestication has been an important topic in recent years. And more than theoretical explanations have been proposed. In this paper, the main methods of previous research are briefly reviewed, and some related concepts are slightly revised. For example, the attributes and efficacy of selective reproduction in silver fox domestication experiments, the approximate correspondence between DS and the reduction of sexual dimorphism, and the correlation between DS causes and sexual selection. On this basis, this paper proposes a preliminary judgment on the causes of human DS that is different from the past: according to our present knowledge (empirical facts), there are two powerful drivers of DS variation, namely, exogamy and coming-of-age ceremony in tribal institutions. These two systems existed completely before the colonization of Australian tribes. This paper uses the early classical ethnography of Australia by Fison, Howitt, Spencer, and Gillen to analyze and summarize the basic content of these two systems (reconstructing the original state of the system before colonization). Then, its domestication function and efficacy are discussed. Based on this, it is concluded that the joint effect of exogamy and coming-of-age ceremony is the main way for human beings to achieve self-domestication. We are very fortunate to have evidence about the Australian tribes in the early stages of civilization before colonization. We can trace their origins and examine their evolution accordingly. The alliance of two multimale-multifemale (mm-mf) groups through a non-violent approach is the first step in the speciation of Homo sapiens. The tribal system formed in this historical link is the initial process of human civilization and an important foundation for human prosperity to this day
... While boars are typically aggressive and fearful of humans, random genetic mutations can produce tamer individuals with reduced fear responses. These behavioral traits may be associated with deficiencies in neural crest cell development, which has been implicated in the domestication syndrome observed across multiple species ( 65 ). Such tamer individuals would have had an evolutionary advantage, accessing high-quality anthropogenic food resources at lower energetic cost compared to more aggressive counterparts. ...
The domestication of pigs (Sus scrofa) has had profound socioeconomic and ecological consequences. Although pigs are believed to have been independently domesticated in South China, the timing and initial mechanisms of this process remain debated. This study presents a microfossil analysis of pig dental calculus from two early Neolithic sites in the Lower Yangtze River region: Jingtoushan (8,300 to 7,800 cal. BP) and Kuahuqiao (8,200 to 7,000 cal. BP). Analyses of starch, phytolith, and parasite remains indicate that pigs consumed human-associated foods and waste, including cooked starchy plants and human whipworm (Trichuris trichiura) eggs, likely derived from food preparation and fecally contaminated materials. Identified plant taxa include acorns (Fagaceae), rice (Oryza sp.), underground storage organs such as yam (Dioscorea sp.), and wild grasses (Triticeae and Panicoideae), all present in the local botanical assemblages. Coefficients of variation in dental metrics further indicate the coexistence of both domestic and wild populations. Together, these lines of evidence point to multiple modes of human–pig interaction, including early domestic pigs under human management, pigs scavenging near settlements, and free-ranging individuals foraging beyond human influence. Pig domestication in the Lower Yangtze had begun by 8,000 y ago, likely following both commensal and prey pathways, in parallel with the development of rice cultivation and sedentary lifeways. This study also demonstrates the value of dental calculus analysis for revealing early human–animal relationships before the appearance of clear morphological markers of domestication in the archaeological record.
... While we have amassed considerable knowledge about the behavioral, physiological, and morphological differences between domesticated and wild mammals 12 and posed specific evolutionary hypotheses for how those changes came about 13,14 , the extent to which this is paralleled in the nonmammalian realm is understudied. In this work, we address this gap in knowledge by investigating the genetic basis of the domesticated phenotype in the Bengalese finch. ...
Many domesticated animals share a syndromic phenotype marked by a suite of traits that include more variable patterns of coloration, reduced stress, aggression, and altered risk-taking and exploratory behaviors relative to their wild counterparts. Roughly 150 years after Darwin’s pioneering insight into this phenomenon, reasonable progress has been made in understanding the evolutionary and biological basis of the so-called domesticated phenotype in mammals. However, the extent to which these processes are paralleled in non-mammalian domesticates is scant. Here, we address this knowledge gap by investigating the genetic basis of the domesticated phenotype in the Bengalese finch, a songbird frequently found in pet shops and a popular animal model in the study of learned vocal behaviors. Using whole-genome sequencing and population genomic approaches, we identify strain-specific selection signals in the Bengalee finch and its wild munia ancestor. Our findings suggest that, like in mammals, the evolution of the domestication syndrome in avian species involves a shift in the selective regime, capable of altering brain circuits favoring the dynamic modulation of motivation and reward sensitivity over augmented aggression and stress responses.
... There is a consensus that the key to dog domestication lies in changes in the rate of developmental phases, and due to genetic effects, dogs retain paedomorphic features (Geiger et al., 2017;Goodwin et al., 1997). It is hypothesised that the domestication syndrome results from mild neural crest cell deficits during embryonic development (Pendleton et al., 2018;Wilkins et al., 2014). ...
While many societies worldwide are experiencing demographic transitions characterized by declining birth rates and shrinking kinship networks, the rise in pet ownership, particularly dog keeping, is most pronounced in Western and East Asian urbanized societies, where pets increasingly fulfill companionship roles. Dogs, one of the most often kept pets, are largely considered integral members of the human family. An increasing number of owners have even begun to regard their dogs as their children. This phenomenon can be explained by cultural evolutionary hypotheses, which suggest that due to changes in their environment, humans have culturally redirected their biological needs to nurture and care for children towards animals. Why are dogs good candidates for this child-like role in Western societies? The aim of this theoretical review is to describe the child-like morphological, behavioural and physiological features of pet dogs and explore the similarities and differences in dog and child parenting. We also examine the motivations behind “dog parenting” and conclude that “dog parents” constitute a heterogeneous group of people who attribute child-like roles to their dogs to various degrees and for various reasons. Both are highly dependent on socio-cultural contexts, among other factors. While some owners might see their dog as a child surrogate to spoil, others actively choose to have dogs and not children, bearing in mind that they have species-specific characteristics and needs. Dog parenting can also coexist with child parenting, enhancing the idea that humans might have evolved to care for others regardless of species.
Neural crest cells (NCCs) are a key component of the vertebrate body plan and contribute to a variety of different traits. However, their dynamic migratory behavior and spatiotemporal heterogeneity in the developing embryo pose significant challenges for their identification and isolation. Consequently, most studies of NCCs have been confined to model organisms with established transgenic tools. To overcome this limitation, we present a novel approach that combines antibody labelling with fluorescence activated cell sorting to enrich for NCCs and we demonstrate the approach in the common wall lizard ( Podarcis muralis ). Through microscopy, reverse transcription quantitative polymerase chain reaction and single-cell RNA sequencing, we show that the method enriches for NCCs as efficiently as methods relying on transgenic animals. Using this technique, we successfully characterise transcriptional profiles of NCCs in wall lizard embryos. We anticipate that this method can be applied to a wide range of vertebrates that lack transgenic tools, enabling deeper insights into the roles that neural crest cells are playing in developmental and evolution.
Domestication involves huge phenotypic shifts via strong directional selection. The resulting changes, often termed the Domestication Syndrome, typically encompass numerous traits; however, the most universal of these are changes in reduced fear of humans (tameness) and brain composition. To assess how early domestication selection may have focused on tameness and its interaction with brain composition, a Red Junglefowl ( Gallus gallus ) population (the wild progenitor of the domestic chicken) was used to create two lines bidirectionally selected for fear of humans over eight generations of selection. These selection lines were then used to make an intercross population. Using a combination of genome‐wide mapping in the intercross and between‐line analysis of the selection lines, we show that the genetic loci for tameness co‐localise with genetic loci for brain composition and anxiety behaviour. Furthermore, the detected loci for brain composition also co‐localise with brain composition loci identified in a separate wild × domestic intercross. These results indicate that tameness and brain composition are either pleiotropic or genetically linked, and that tameness selection appears to recapitulate the same loci that have been selected by domestication itself. Therefore, selection for increased tameness could be the initial selection pressure driving the core of the domestication syndrome.
The domestication of plants and animals permitted the development of cities and social hierarchies, as well as fostering cultural changes that ultimately led humanity into the modern world. Despite the importance of this set of related evolutionary phenomena, scholars have not reached a consensus on what the earliest steps in the domestication process looked like, how long the seminal portions of the process took to unfold, or whether humans played a conscious role in parts or all of it. Likewise, many scholars find it difficult to disentangle the cultural processes of cultivation from the biological processes of domestication. Over the past decade, the prevailing views among scholars have begun to shift towards unconscious and protracted models of early domestication; however, the nomenclature used to discuss these changes has been stagnant. Discussions of early domestication remain bound up in prevailing definitions and preconceived ideas of what the process looked like. In this paper, we seek to break down definitions of domestication and to construct a definition that serves equal utility regardless of the views that researchers hold about the process.
This article is part of the theme issue ‘Unravelling domestication: multi-disciplinary perspectives on human and non-human relationships in the past, present and future’.
Early experience permanently alters behavior and physiology. These effects are, in part, mediated by sustained alterations in gene expression in selected brain regions. The critical question concerns the mechanism of these environmental “programming” effects. We examine this issue with an animal model that studies the consequences of variations in mother-infant interactions on the development of individual differences in behavioral and endocrine responses to stress in adulthood. Increased levels of pup licking/grooming by rat mothers in the first week of life alter DNA structure at a glucocorticoid receptor gene promoter in the hippocampus of the offspring. Differences in the DNA methylation pattern between the offspring of high- and low-lickinglgrooming mothers emerge over the first week of life; they are reversed with cross-fostering; they persist into adulthood; and they are associated with altered histone acetylation and transcription factor (nerve growth factor-induced clone A [NGFIA]) binding to the glucocorticoid receptor promoter. DNA methylation alters glucocorticoid receptor expression through modifications of chromatin structure. Pharmacological reversal of the effects on chromatin structure completely eliminates the effects of maternal care on glucocorticoid receptor expression and hypothalamic-pituitary-adrenal (HPA) responses to stress, thus suggesting a causal relation between the maternally induced, epigenetic modification of the glucocorticoid receptor gene and the effects on stress responses in the offspring. These findings demonstrate that the structural modifications of the DNA can be established through environmental programming and that, in spite of the inherent stability of this epigenomic marker, it is dynamic and potentially reversible.
This 1999 edition of The Neural Crest contains comprehensive information about the neural crest, a structure unique to the vertebrate embryo, which has only a transient existence in early embryonic life. The ontogeny of the neural crest embodies the most important issues in developmental biology, as the neural crest is considered to have played a crucial role in evolution of the vertebrate phylum. Data that analyse neural crest ontogeny in murine and zebrafish embryos have been included in this revision. This revised edition also takes advantage of recent advances in our understanding of markers of neural crest cell subpopulations, and a full chapter is now devoted to cell lineage analysis. The major research breakthrough since the first edition has been the introduction of molecular biology to neural crest research, enabling an elucidation of many molecular mechanisms of neural crest development. This book is essential reading for students and researchers in developmental biology, cell biology, and neuroscience.
Neural Crest Cells: Evolution, Development and Disease summarizes discoveries of historical significance and provides in-depth, current analyses of the evolution of neural crest cells, their contribution to embryo development, and their roles in disease. In addition, prospects for tissue engineering, repair and regeneration are covered, offering a timely synthesis of the current knowledge in neural crest cell research. A comprehensive resource on neural crest cells for researchers studying cell biology, developmental biology, stem cells and neurobiology, Neural Crest Cells: Evolution, Development and Disease provides foundational information needed for students , practicing physicians and dentists treating patients with craniofacial defects. Provides timely, comprehensive synthesis of the current knowledge of neural crest cells. Covers the evolution and development of neural crest cells. Includes content on applications for tissue engineering, repair and regeneration
The genomic program for development operates primarily by the regulated expression of genes encoding transcription factors and components of cell signaling pathways. This program is executed by cis-regulatory DNAs (e.g., enhancers and silencers) that control gene expression. The regulatory inputs and functional outputs of developmental control genes constitute network-like architectures. In this PNAS Special Feature are assembled papers on developmental gene regulatory networks governing the formation of various tissues and organs in nematodes, flies, sea urchins, frogs, and mammals. Here, we survey salient points of these networks, by using as reference those governing specification of the endomesoderm in sea urchin embryos and dorsal-ventral patterning in the Drosophila embryo.
