The “Domestication Syndrome” in Mammals: A Unified Explanation Based on Neural Crest Cell Behavior and Genetics
Open accessAbstract
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 genetic architecture of domestication is by necessity pleiotropic, with variants in genes affecting neural crest development and distribution causing multiple domestication traits.
“This implies that the genetic architecture of domestication is by necessity pleiotropic, with variants in genes affecting neural crest development and distribution causing multiple domestication traits.”
From The neural crest cell hypothesis: no unified explanation for domestication (2021) · cites this paper as Wilkins et al. (2014)
The ‘Conclusions regarding morphological changes’ section says most neural-crest genes are pleiotropic and that multiple neural-crest-affecting mutations can jointly produce domestication-syndrome traits. But the paper presents this as a hypothesis and says in its Conclusions that the precise genetic basis still needs elucidation; it does not establish that domestication’s genetic architecture is necessarily pleiotropic. (LLM, conf=0.86)
Experimental — accuracy not yet measuredThe neural crest cell hypothesis entails that a reduction in neural crest cell proliferation and migration is a core genetic mechanism of early domestication.
“The hypothesis entails that a reduction in neural crest cell proliferation and migration is a core genetic mechanism of early domestication.”
From The neural crest cell hypothesis: no unified explanation for domestication (2021) · cites this paper as Wilkins et al. (2014)
In “The Hypothesis: A Critical Role for the Neural Crest,” the paper proposes genetically driven neural crest cell deficits following initial selection for tameness. It lists reduced cell formation, impaired migration, and decreased proliferation at destination sites as possible routes, rather than saying that reductions in both proliferation and migration are required. (LLM, conf=0.85)
Experimental — accuracy not yet measuredThe characters affected by Dlx5/6 in mouse (sociability, vocalization, skull, and brain shape) overlap those affected in the domestication syndrome.
“The characters affected by Dlx5/6 in the mouse (sociability, vocalization, skull, and brain shape…) overlap those affected in the “domestication syndrome”.”
From <i>DLX5/6</i> GABAergic Expression Affects Social Vocalization: Implications for Human Evolution (2021) · cites this paper as Wilkins, et al. 2014
The paper’s sections on morphological and behavioral components of the domestication syndrome describe craniofacial changes, tameness, and changes in brain size. They do not establish that Dlx5/6 affects these traits in mice or identify vocalization as part of the overlap (searched: Dlx5/6, vocalization, sociability). (LLM, conf=0.83)
Experimental — accuracy not yet measuredNeural crest cell function is polygenic, affected by many genetic variants with individually small effects.
“The authors also suggest that neural crest cell function is polygenic, affected by many genetic variants with individually small effects.”
From The neural crest cell hypothesis: no unified explanation for domestication (2021) · cites this paper as Wilkins et al. (2014)
The neural-crest cell hypothesis of domestication assumes that a process of domestication leads to depigmentation rather than an intensification of pigmentation.
“the neural-crest cell hypothesis of domestication assumes that a process of domestication leads to depigmentation rather than an intensification of pigmentation [40,41].”
From Are dark-eyed dogs favoured by humans? Domestication as a potential driver of iris colour difference between dogs and wolves (2023) · cites this paper as [40]
There is some evidence that a common mechanism related to crest cell function might be at least partially a cause of commonalities in domesticated animals.
“The concept of”
From Ecological validity of social interaction tests in rats and mice (2019) · cites this paper as [48]
Feminization is associated with reduced reactivity of the hypothalamus-pituitary-adrenal axis, a physiological trait thought to be critical for domestication.
“The process of ‘feminization’ (reduction of androgen levels and rise in estrogen levels [21]) is often associated with reduced reactivity of the hypothalamus-pituitary-adrenal axis [26], a physiological trait thought to be critical for domestication [17, 27].”
From Self-domestication in Homo sapiens: Insights from comparative genomics (2017) · cites this paper as [17]
Hirschsprung disease affects the neural crest, which is associated with domestication syndrome.
“This disease is very relevant in the context of domestication, as it affects the neural crest, associated with domestication syndrome [17, 38].”
From Self-domestication in Homo sapiens: Insights from comparative genomics (2017) · cites this paper as [17]
The overlaps listed in S1 and S2 Tables and the associated functions and pathways converge to a large extent with what is expected from the neural crest-based hypothesis.
“we find the overlaps listed in S1 and S2 Tables and the associated functions and pathways discussed in the Results section all the more relevant, especially because they converge to a large extent with what is to be expected from the neural crest-based hypothesis [17] put forth to capture the common mechanistic basis of domestication events.”
From Self-domestication in Homo sapiens: Insights from comparative genomics (2017) · cites this paper as [17]
A disruption in neural crest developmental programs might be the source of changes spanning multiple organ systems and morphological structures.
“A disruption in neural crest developmental programs might be the source of changes spanning multiple organ systems and morphological structures [17]”
From Self-domestication in Homo sapiens: Insights from comparative genomics (2017) · cites this paper as [17]
A biological hypothesis for the production of domestication syndromes has received important support, including evidence that genetic variants underlying self-domestication occur in H. sapiens but not in H. neanderthalensis or Denisovans.
“Furthermore a biological hypothesis for the production of domestication syndromes (Wilkins et al., 2014) has received important support (Wilkins, 2017; Pendleton et al., 2018), including evidence that genetic variants underlying self-domestication occur in H. sapiens but not in H. neanderthalensis or Denisovans (Theofanopoulou et al., 2017).”
From Hypotheses for the Evolution of Reduced Reactive Aggression in the Context of Human Self-Domestication (2019) · cites this paper as Wilkins et al., 2014
The first formulation of the neurocristopathic hypothesis of domestication included BAZ1B among the genes influencing neural crest development.
“(iii) the first formulation of the neurocristopathic hypothesis of domestication, which included BAZ1B among the genes influencing NC development (5);”
Mild neural crest deficits have been put forth as a unifying explanatory framework for the defining features of domestication syndrome, with BAZ1B listed among putative underlying genes because of its previously reported role in the neural crest of model organisms.
“Mild NC deficits have been put forth as a unifying explanatory framework for the defining features of the so-called domestication syndrome, with BAZ1B listed among the putative underlying genes because of its previously reported role in the NC of model organisms (5, 10, 11).”
Neural crest changes have been implicated in domestication syndrome.
“since NC changes have been implicated in the domestication syndrome (5)”
Mild neural crest deficits are a central and unifying functional layer underlying domestication.
“The first problem was tackled by the recent proposition of mild NC deficits as a central and unifying functional layer underlying domestication (5).”
The investigation provides the first experimental evidence for the neurocristopathic hypothesis that had been put forth to explain the domestication syndrome and had pointed to BAZ1B as one of the candidates underlying this syndrome.
“Third, our investigation provides the first experimental evidence for the neurocristopathic hypothesis that had been put forth to explain the domestication syndrome and had pointed to BAZ1B as one of the candidates underlying this syndrome (5).”
Hypofunction of the HPA axis has been proposed as a key mechanism in the development of tame behaviors in domesticates.
“the hypofunction of which has been proposed as a key mechanism in the development of tame behaviors in domesticates (Trut et al., 2009;Wilkins et al., 2014).”
From Glutamate receptors in domestication and modern human evolution (2020) · cites this paper as Wilkins et al., 2014
Alterations to the HPA axis are considered to be essential for the emergence of tameness in different theories of domestication.
“Alterations to the HPA axis are considered to be essential for the emergence of tameness in different (indeed competing) theories of domestication (Wilkins et al., 2014;Belyaev, 1979).”
From Glutamate receptors in domestication and modern human evolution (2020) · cites this paper as Wilkins et al., 2014
The genetic signals from this analysis fall in line with the predictions of the domestication syndrome hypothesis.
“The genetic signals from this analysis fall in line with the predictions of the domestication syndrome hypothesis (50), which posits that the morphological and physiological traits modified by mammalian domestication are explained by direct and indirect consequences of mild neural crest cell deficits during embryonic development.”
From Comparative analysis of the domestic cat genome reveals genetic signatures underlying feline biology and domestication (2014) · cites this paper as [50]
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- Authors
- Wilkins, A. S., Wrangham, R. W., & Fitch, W. T.
- Affiliations
- Stellenbosch University (ZA)
- Harvard University (US)
- University of Vienna (AT)
- Corresponding author
- Wilkins, Adam S
- Venue
- Genetics
- Publisher
- Oxford University Press (OUP)
- Published
- 2014-07-01
- Volume
- 197
- Issue
- 3
- Pages
- 795-808
- ISSN
- 0016-6731 (ISSN-L)
- 1943-2631
- PMC
- PMC4096361
- OpenAlex
- W2165155571
- Cited by
- 751
- References
- 114
- Citations by year
- 2026: 35 · 2025: 60 · 2024: 87 · 2023: 113 · 2022: 81 · 2021: 76 · 2020: 77 · 2019: 72 · 2018: 45 · 2017: 45 · 2016: 40 · 2015: 14 · 2014: 4
- FWCI
- 22.49
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model (vor)
- Locations
- Genetics (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Digital Access to Scholarship at Harvard (DASH) (Harvard University) (submittedVersion, cc-by)
- Funders
- FP7 Ideas: European Research Council (230604)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic and phenotypic traits in livestock
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Human-Animal Interaction Studies
- Physical Sciences › Mathematics › Geometry and Topology › Morphological variations and asymmetry
- Keywords
- domestication syndrome, neural crest cells, embryonic development, developmental genetics, heritable traits
- MeSH terms
- Animals, Animals, Domestic, Behavior, Animal, Mammals, Models, Genetic, Neural Crest, Syndrome, Epigenesis, Genetic
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