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The "Domestication Syndrome" in Mammals: A Unified Explanation Based on Neural Crest Cell Behavior and Genetics
Abstract and Figures
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 initial selection of tameness is followed by a suite of morphological and physiological traits that mark the domestic state and are shared amongst many species, but not seen in the wild ancestors: changes in coat color, floppy ears, smaller jaws and teeth (signs of neotenization), modified reproductive cycles, altered hormone and neurotransmitter levels. These changes in behaviour and morphology are collectively referred to as domestication syndrome (DS) or domestication phenotype [70][71][72]. In general, two-not mutually exclusive-hypotheses have been proposed underlying the DS. ...
... The neural crest cell (NCC) hypothesis postulates that an initial selection for tameness leads to a reduced function of neural crest-derived tissues relevant for behaviour via mild loss-of-function mutations in neural crest cells (NCCs). Subsequently this neural crest hypofunction produces unselected by-products, such as the morphological changes [70,71]. Genomic support for the NCC hypothesis was found in cats, where genomic regions under selection were associated with NCC survival, neurotransmitters and sensory development [73]. ...
The worldwide dromedary milk production has increased sharply since the beginning of this century due to prolonged shelf life, improved food-safety and perceived health benefits. Scientific confirmation of health claims will expand the market of dromedary milk further. As a result, more and more dromedaries will be bred for one purpose only: the highest possible milk production. However, intensive dromedary farming systems have consequences for animal welfare and may lead to genetic changes. Tighter regulations will be implemented to restrict commercialization of raw milk. Protocols controlling welfare of dromedaries and gene databases of milk-dromedaries will prevent negative consequences of intensive farming. In countries where dromedaries have only recently been introduced as production animal, legislators have limited expertise on this species. This is exemplified by an assessment on behalf of the Dutch government, recommending prohibiting keeping this species from 2024 onwards because the dromedary was deemed to be insufficiently domesticated. Implementation of this recommendation in Dutch law would have devastating effects on existing dromedary farms and could also pave the way for adopting similar measures in other European countries. In this paper it is shown that the Dutch assessment lacks scientific rigor. Awareness of breeders and legislators for the increasing knowledge about dromedaries and their products would strengthen the position of dromedaries as one of the most adapted and sustainable animals.
... In comparison to their wild predecessors, domesticated species exhibit specific health effects depending on the biology of the species and the nature and degree of the domestication process (referred to as domesticated syndrome) (Wilkins et al. 2014). The evolutionary consequences of domestication on cancer development and progression are also discussed . ...
Cancer, a disease due to uncontrolled cell proliferation is as ancient as multicellular organisms. A 255-million-years-old fossilized forerunner mammal gorgonopsian is probably the oldest evidence of cancer, to date. Cancer seems to have evolved by adapting to the microenvironment occupied by immune sentinel, modulating the cellular behavior from cytotoxic to regulatory, acquiring resistance to chemotherapy and surviving hypoxia. The interaction of genes with environmental carcinogens is central to cancer onset, seen as a spectrum of cancer susceptibility among human population. Cancer occurs in life forms other than human also, although their exposure to environmental carcinogens can be different. Role of genetic etiology in cancer in multiple species can be interesting with regard to not only cancer susceptibility, but also genetic conservation and adaptation in speciation. The widely used model organisms for cancer research are mouse and rat which are short-lived and reproduce rapidly. Research in these cancer prone animal models has been valuable as these have led to cancer therapy. However, another rewarding area of cancer research can be the cancer-resistant animal species. The Peto’s paradox and G-value paradox are evident when natural cancer resistance is observed in large mammals, like elephant and whale, small rodents viz. Naked Mole Rat and Blind Mole Rat, and Bat. The cancer resistance remains to be explored in other small or large and long-living animals like giraffe, camel, rhinoceros, water buffalo, Indian bison, Shire horse, polar bear, manatee, elephant seal, walrus, hippopotamus, turtle and tortoise, sloth, and squirrel. Indeed, understanding the molecular mechanisms of avoiding neoplastic transformation across various life forms can be potentially having translational value for human cancer management.
Graphical Abstract
Adapted and Modified from (Hanahan and Weinberg 2011)
... The domestication process affects life history traits due to changes in morphological, physiological, reproductive, behavioural, and immune functions (Mignon-Grasteau et al., 2005;Pulcini et al., 2013; for review in fishes) compared to their wild relatives . Wilkins et al. (2014) suggest that these specific modifications, called domestication syndrome, may be due to mild deficit of neural-crest cells during embryonic development in domesticated animals. In addition, both natural and artificial selection in domesticated species leaves footprints across the genome, known as selection signatures, which can point to regions harboring essential genes for domestication or natural fitness (Dobney & Larson, 2006;. ...
L’amélioration génétique de populations de truites arc-en-ciel a permis d’accroître l’efficacité de la production, mais à contribuer à une forte diminution de la variabilité génétique. Cette perte de diversité génétique peut causer de la dépression de consanguinité mais aussi mettre en péril le progrès génétique à long terme et l’adaptation des populations aux changements environnementaux. Les niveaux de consanguinité observés (via des indicateurs génomiques) au sein de nos populations de truites françaises, nous interrogent sur les causes et les impacts de tels niveaux de consanguinité. Ces interrogations font l’objet des travaux de thèse présentés. Au-delà des effets de la sélection et de la dérive génétique liée à la faible taille des populations en élevage, la perte de diversité génétique au sein des populations de truite arc-en-ciel s’explique aussi par des déséquilibres de contribution des mères à la génération suivante associés à une surmortalité embryonnaire observée de la fécondation à l’éclosion dans les descendances de certaines mères. L’étude des effets locaux de la consanguinité sur les performances de taille, reproduction et survie de la truite, montre que localisée dans certaines parties du génome, la consanguinité peut avoir des effets notables, sans que l’on observe forcément un effet à l’échelle de tout le génome. Si, ces effets locaux peuvent être négatifs, ils sont toutefois positifs dans certaines zones du génome. Le principal phénomène observé est un impact négatif de la consanguinité récente, expliqué par l’accumulation d’allèles récessifs dont les effets sont défavorables, en lien direct avec l’estimation d’effets de dominance importants sur les caractères de reproduction et de survie. Cependant la consanguinité, en particulier accumulée dans des générations passées, engendre aussi des effets positifs. Ainsi neuf régions d’homozygotie forte ont été identifiées sous sélection positive commune à trois lignées de truites françaises et une population américaine. Les gènes annotés dans ces régions sont liés à la domestication (fonctions de croissance, reproduction, comportement et immunité) ainsi qu’à la fitness naturelle en lien avec la survie des individus (embryogenèse, organisation cellulaire). C’est pourquoi, comprendre l’impact et le rôle de la diversité génétique locale est essentiel, afin de mieux la gérer dans les programmes de sélection. L’utilisation d’indicateurs génomiques de la consanguinité permettra aux sélectionneurs de mieux maîtriser les compromis entre valeurs génétiques des reproducteurs et effets indésirables de la consanguinité de leur progéniture. Cela permettra aussi d’exploiter les effets d’hétérosis, et ainsi améliorer durablement les performances des cheptels de production.
... Ce résultat surprend car chez les Artiodactyles, les taxons domestiques sont généralement plus petits que les taxons sauvages(Tchernov et Horwitz, 1991). On suppose traditionnellement que cette réduction de taille est liée à la sélection d'individus moins agressifs, à certains comportements sexuels et changements dans le cycle de vie(Clutton-Brock, 1999;Hongo et al., 2009 ;Vigne et al., 2005a ;Wilkins et al., 2014 ;Zeder, 2006a). Or comme l'ont déjà soulevéBalcarcel et al. 2021, le phénomène de la réduction de taille est observée chez des taxons tels que les chèvres, moutons ou porcs pour lesquels il existe des races particulièrement grandes(Ekarius, 2008) et qui ont une trajectoire de domestication différente des CSA. ...
Les lamas (Lama glama Linnaeus, 1758) et les alpagas (Vicugna pacos Linnaeus, 1758) ont été domestiqués à partir de deux espèces sauvages : les guanacos (Lama guanicoe Müller, 1776) et les vigognes (Vicugna vicugna Molina, 1782). Les camélidés domestiques ont joué un rôle économique et symbolique majeur dans le développement des sociétés préhispaniques. Cependant, la documentation du processus de domestication des camélidés sud-américains (CSA) reste un défi. Pour obtenir de nouvelles informations sur ce processus, nous nous sommes concentrés sur la zone des Andes centrales et le site de Telarmachay (Puna de Junín, Pérou). Sur la longue séquence chronologique de ce site, de 7000 à 150 av. J.-C., des preuves de contrôle/management ont été suggérées vers 3000-1800 av. J.-C., proposant un processus de domestication des CSA antérieur de 2000 ans aux autres centres de domestication de la zone andine. Afin d'explorer l’intensification des interactions entre sociétés humaines et camélidés, nous avons produit de nouvelles datations 14C des ossements de CSA et utilisé une approche multicritère associant des profils de mortalité, la morphométrie morphométrique 3D du talus et une analyse des teneurs en isotopes stables du carbone et de l’azote (δ13C et δ15N) du collagène de l’os. Nos résultats nous permettent d’étayer l’hypothèse d’un processus ancien de domestication des CSA in situ à Telarmachay dès le 5ème millénaire, entre 5106/4851 et 4328/4129 av. J.-C. La morphométrie géométrique 3D du talus nous permettant de suivre l’évolution phénotypique des deux lignées de camélidés le long de la séquence chronologique du site, nous avons pu observer, dès cette période, la présence de formes hybrides de taille intermédiaire entre les vigognes et les guanacos. Ces premiers changements de la diversité phénotypique sont associés à des profils de mortalité témoignant d’une phase de changement d’exploitation des camélidés avec la forte représentation des camélidés ayant entre 0 et 3 mois. C’est à la phase suivante, entre 4270/4060 à 3626/3054 av. J.-C, que l’on observe un changement marqué de la variabilité du talus, interprété comme la conséquence d’une contrainte plus forte sur la mobilité des vigognes avec potentiellement une mise en captivité, comme le suggère la présence d’enclos empierrés à proximité du site. Enfin, si la réduction de la mobilité des guanacos semble moins claire, des modifications squelettiques ont quand même été mises en évidence dès le 5ème millénaire. D’après les valeurs du δ13C et δ15N, les camélidés de Telarmachay ont vécu dans la puna autour du site et n’ont pas subi de changement majeur dans leur alimentation et leur environnement durant 4000 ans. En revanche, une légère variation a été mise en évidence dès le 3ème millénaire, entre 3179/2495 et 2226/1854 av. J.-C., qui pourrait concorder avec le contrôle de la mobilité des camélidés. Ainsi, l’accroissement du contrôle culturel des CSA à partir du 5ème millénaire av. J.-C. soutient l’hypothèse de l’ancienneté du processus de domestication des camélidés andins dans la région de Junín. Nous proposons que l’écosystème de la Puna du Junin fût un écosystème particulièrement propice à l’intensification des interactions entre les sociétés de chasseurs-cueilleurs et celles des camélidés à l’Holocène.
... Probably the most comprehensive definition of animal domestication, by Zeder (2015, p. 3191), defines it as "a sustained multigenerational, mutualistic relationship in which one organism assumes a significant degree of influence over the reproduction and care of another organism in order to secure a more predictable supply of a resource of interest, and through which the partner organism gains advantage over individuals that remain outside this relationship, thereby benefitting and often increasing the fitness of both the domesticator and the target domesticate." Traditional archaeological approaches to domestication have focused largely on aspects of reproductive control by searching for morphological characteristics associated with the domestication syndrome, which is a set of morphological, physiological, and behavioral features linked to domestication, probably via changes in neural crest development (Wilkins et al. 2014). These morphological characteristics such as craniofacial changes and reduction in body size (e.g., Arbuckle and Makarewicz 2009;Clutton-Brock 1992, pp. ...
Animal domestication is a profound change for human societies, economies, and worldviews. The shifting definitions of animal domestication reflect its varying and process-like nature. Reindeer is one of the species whose domestication is not easily pinned down using standard definitions and research methodologies of animal domestication. In recent years, advances in archaeological methodology and the conceptual understanding of animal domestication have opened new avenues for research on this topic. This review summarizes recent research on the archaeology of reindeer domestication among the Indigenous Sámi of northern Fennoscandia. It compiles a chronological framework of reindeer domestication with an emphasis on the development of reindeer-herding practices and human–reindeer relationships. I argue that while a major transition to reindeer herding occurred among the Sámi from the 15th century onward, small-scale reindeer herding characterized by interspecies sociality, cooperation, and care developed earlier during the Late Iron Age, with regional variations in the timing and details of the events. By focusing on reindeer-herding practices and the human–reindeer relationships embedded in them, I also argue that reindeer domestication, and animal domestication in general, is a relationship constructed and constantly renegotiated in everyday interactions with the animals.
... Such findings have important implications for understanding mechanisms by which large phenotypic shifts occur within species, the potentially outsized significance of certain cell types in such processes, and the implications of artificial selection aimed at potential master-regulators of phenotype. [84][85][86][87] Our findings are consistent with the inefficient nature of selective pressure aimed at complex behavioral traits in comparison with readily observable or even quantifiable aesthetic or morphological phenotypes, particularly those controlled by one or a few high-impact loci. 13, [88][89][90] As such, we propose a model of canine behavioral diversification that largely predates modern breed formation, in which behavioral traits conducive to lineageassociated occupations (e.g., sled-pulling and herding) arose as a result of selective breeding for certain tasks over thousands of years within relatively geographically isolated populations (e.g., a need for livestock guardians in the Near East and sled dogs in the Arctic). ...
Article Domestic dog lineages reveal genetic drivers of behavioral diversification Graphical abstract Highlights d High-dimensional data analysis reveals canine lineages, resolving breed relationships d Canine behavioral diversification predates modern breed formation d Ancient non-coding variation drives working role-related dog behaviors d Canine genetic diversity is associated with neurodevelopmental gene co-expression A framework for understanding the relationships between canine breeds allows for the identification of genetic drivers of the behaviors that define them. SUMMARY Selective breeding of domestic dogs has generated diverse breeds often optimized for performing specialized tasks. Despite the heritability of breed-typical behavioral traits, identification of causal loci has proven challenging due to the complexity of canine population structure. We overcome longstanding difficulties in identifying genetic drivers of canine behavior by developing a framework for understanding relationships between breeds and the behaviors that define them, utilizing genetic data for over 4,000 domestic, semi-feral, and wild canids and behavioral survey data for over 46,000 dogs. We identify ten major canine genetic line-ages and their behavioral correlates and show that breed diversification is predominantly driven by non-coding regulatory variation. We determine that lineage-associated genes converge in neurodevelopmental co-expression networks, identifying a sheepdog-associated enrichment for interrelated axon guidance functions. This work presents a scaffold for canine diversification that positions the domestic dog as an unparalleled system for revealing the genetic origins of behavioral diversity.
A central question in the evolution of human language is how it emerged. Based on recent research across disciplines, we identified three processes proposed as potential driving factors behind the evolution of ‘modern’ language phenotype: i) a reduction in reactive aggression entailing a boost in prosociality and cooperation, ii) a change in early brain growth trajectory that impacted structures like the cerebellum and striatum, and thus likely impacted the (procedural) memory circuits these regions support, and iii) a demographic expansion of H. sapiens during the Middle Pleistocene. While extensively researched on their own, the interaction between these three processes has yet to be investigated systematically. We develop an abstract agent-based model to interrogate the relationship between these three factors and how they influence transmission of information within a population, which we take to be the essence of language. The model abstracts linguistic capacity to an ‘array of skills’ and investigates under what conditions the number of skills increases. The results demonstrate that there is an optimal degree of cooperation and memory capacity at which the amount of transmitted information is the highest. Our model also shows that separate linguistic communities arise under circumstances where individuals have high levels of memory capacity and there is at least a certain degree of non-cooperation. In contrast, we find no significant direct effects for population size in the process of linguistic community formation. Taken together, these results highlight the explanatory benefits of combining insights from cognitive science, archaeology, and computational modelling.
The study of human evolution should teach us that we are unusual primates, but not exceptional. We are subject to the same natural laws and constraints as any other species and suffer the same consequences. By following our instincts to control the resources we need and to reproduce, we are now threatened with global catastrophe from climate change and overpopulation. The fossil record should be a reminder that we are not safe from extinction. Humans are not finished evolving. It is easiest to observe at the molecular level in a continual struggle to find a harmony with the microbes around and within us. Individuals who cannot do so succumb to disease. Natural selection continues and will always be present.
We aimed to clarify the changes in facial morphology of cats in relation to their interactions with humans. In Study 1, we compared the facial morphology of cats (feral mixed breed, owned domestic mixed breed, and owned domestic purebreds) with that of African wildcats. After collecting 3295 photos, we found that owned domestic cats’ noses were significantly shorter than those of African wildcats and feral mixed breed, and there were no significant differences between the latter two. The eye angles were significantly more gradual in owned domestic purebreds than in the other groups. In Study 2, we examined the correlation between facial morphology and years with the owner, and found that the former is not affected by the latter. This suggests that changes in facial morphology are possibly transgenerational changes. The difference in facial morphology between wildcats and owned cats might be caused by domestication, and that between feral cats and owned cats might be due to feralization. In Study 3, we investigated whether cats’ facial features affect cuteness ratings. We asked human participants to evaluate the cuteness of cats’ face images and found that faces with shorter nose lengths were considered cuter. This suggests that owned domestic cats’ facial morphology is preferred by humans.
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.
MWS is a multiple congenital anomaly syndrome, first clinically delineated by Mowat et al in 1998. Over 45 cases have now been reported. All patients have typical dysmorphic features in association with severe intellectual disability, and nearly all have microcephaly and seizures. Congenital anomalies, including Hirschsprung disease (HSCR), congenital heart disease, hypospadias, genitourinary anomalies, agenesis of the corpus callosum, and short stature are common. The syndrome is the result of heterozygous deletions or truncating mutations of the ZFHX1B (SIP1) gene on chromosome 2q22.