Comparison of village dog and wolf genomes highlights the role of the neural crest in dog domestication

Abstract

BackgroundDomesticated from gray wolves between 10 and 40 kya in Eurasia, dogs display a vast array of phenotypes that differ from their ancestors, yet mirror other domesticated animal species, a phenomenon known as the domestication syndrome. Here, we use signatures persisting in dog genomes to identify genes and pathways possibly altered by the selective pressures of domestication.ResultsWhole-genome SNP analyses of 43 globally distributed village dogs and 10 wolves differentiated signatures resulting from domestication rather than breed formation. We identified 246 candidate domestication regions containing 10.8 Mb of genome sequence and 429 genes. The regions share haplotypes with ancient dogs, suggesting that the detected signals are not the result of recent selection. Gene enrichments highlight numerous genes linked to neural crest and central nervous system development as well as neurological function. Read depth analysis suggests that copy number variation played a minor role in dog domestication.ConclusionsOur results identify genes that act early in embryogenesis and can confer phenotypes distinguishing domesticated dogs from wolves, such as tameness, smaller jaws, floppy ears, and diminished craniofacial development as the targets of selection during domestication. These differences reflect the phenotypes of the domestication syndrome, which can be explained by alterations in the migration or activity of neural crest cells during development. We propose that initial selection during early dog domestication was for behavior, a trait influenced by genes which act in the neural crest, which secondarily gave rise to the phenotypes of modern dogs.Electronic supplementary materialThe online version of this article (10.1186/s12915-018-0535-2) contains supplementary material, which is available to authorized users.

Evaluating the self‐domestication hypothesis of human evolution

“…Domestication of course involves genetic changes . Regulatory regions were found to differ much more than coding sequences in genomic studies of domestication in rabbits and dogs . Genomic tools are being used to test whether domestication features “resulted from a relaxation of selection as animals exited the wild environment or, alternatively, from positive selection resulting from conscious or unconscious human preference” (Larson and Fuller, p. 127–128).…”

“…Many of these features derive from the neural crest, discussed below . Indeed, inspired by the suggestion of neural crest as a driver of morphological patterns associated with domestication, several recent genomic studies of the domestication of dogs, cats, rabbits, and horses reported evidence for positive selection on genes involved in neural crest “development programs.” In addition, hormonal changes—potentially related to the neural crest—have been at the center of the HSD hypothesis. Cieri et al hypothesized an enhanced social tolerance since the Middle Pleistocene, physiologically caused by a reduction in average androgen reactivity and morphologically expressed in craniofacial feminization.…”

The role of common ancestry and gene flow in the evolution of human‐directed play behaviour in dogs

“…Such a secondary effect can occur if human-directed play behaviour is a component of the domestication syndromes(Darwin, 1868;Wheat, Fitzpatrick, Rogell, & Temrin, 2019;Wilkins, Wrangham, & Fitch, 2014) whereby an entire suite of traits enhancing the bond between owners and their dogs are genetically linked and thus collectively respond to existing artificial selection on function. Wolf-dog hybrids are considerably less playful with humans than dogs in general indicating that the human-directed playfulness was not or little expressed in the undomesticated wild ancestors(Burghardt, 2005;Pendleton et al, 2018;Wheat et al, 2018). However, several ancient breeds that likely reflect early states of domestication(Wheat et al, 2019) were characterized by intermediate average scores for human-directed playfulness (e.g.…”

Masculinity and the mechanisms of human self-domestication

“…At present, modified NCC functioning provides the most widely supported explanation for the observed link between selection for reduced aggression and the wider syndrome of domesticated traits (Geiger et al, 2018;Montague et al, 2014;Pendleton et al, 2018;Wilkins, 2017;Wilkins et al, 2014;Zeder, 2017). Wilkins et al (2014) proposed that hypoplasia of the NCC-derived adrenal medulla dampens behavioural reactivity prompted by the Hypothalamic-Pituitary-Adrenal (HPA) axis.…”