The “Domestication Syndrome” in Mammals: A Unified Explanation Based on Neural Crest Cell Behavior and Genetics

Abstract

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.

Revisiting two hypotheses on the “domestication syndrome” in light of genomic data

“…Wilkins et al (2014) proposed that all the "phenes" (single phenotypic traits) of the DS might be explained by relatively small deficits of neural crest cells in their final locations -relative to the progenitor wild breeds -after these cells have migrated in early embryonic development from the dorsal side of the neural tube. In this view, selection for docility and tameness -presumably the initial step in domestication -entails selection for those properties produced as a consequence of mild neural crest cell deficiencies in development.…”

“…In this view, selection for docility and tameness -presumably the initial step in domestication -entails selection for those properties produced as a consequence of mild neural crest cell deficiencies in development. They further suggested that docility in the early stages of domestication specifically reflected smaller adrenal glands (which derive in part from neural crest cells) producing lower concentrations of adrenocorticotropic hormones, leading to delayed and/or reduced "fight-or-flight" responses (Wilkins et al, 2014). (Domesticated rats and foxes, in fact, have smaller adrenal glands than their wild counterparts and produce lower concentrations of adrenocorticotropic hormones.)…”

“…Although many genes are known that affect and are required for neural crest cell formation, migration or correct cellular differentiation of the cells that form from them, there are no known singlegene mutations in any species in this set of genes that create the DS, although a number of single gene mutations in this group of genes generate some features of the DS, especially pigmentation changes and mild alterations in craniofacial features (Wilkins et al, 2014). While severe loss-of-function mutations in these genes tend to produce lethality or neurocristopathies, mild loss-of-function mutations should, in principle, be viable.…”

“…) This condition has been dubbed the "domestication syndrome", abbreviated here as the DS. The term itself appears to have been first used in connection with a parallel set of observed commonalities amongst domesticated plants (Hammer, 1984) but was later applied to animals (Larson et al, 2014;Wilkins et al, 2014). (Some authors, however, prefer the term "domesticated phenotype" to avoid the implication of illness associated with the word "syndrome", e. g. (Leach, 2003).)…”

Domestication and early experiences in chickens: Behavior, stress and gene expression

“…Behavioral differences observed include more tame and docile individuals, with lower fearfulness. Physiological changes are also present, including an attenuated physiological stress response and altered reproduction cycles (Wilkins et al, 2014).…”