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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 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]. ...
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... 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 . ...
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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;. ...
Thesis
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... 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. ...
Thesis
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. ...
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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). ...
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