The taming of the neural crest: a developmental perspective on the origins of morphological covariation in domesticated mammals

Abstract

Studies on domestication are blooming, but the developmental bases for the generation of domestication traits and breed diversity remain largely unexplored. Some phenotypic patterns of human neurocristopathies are suggestive of those reported for domesticated mammals and disrupting neural crest developmental programmes have been argued to be the source of traits deemed the 'domestication syndrome'. These character changes span multiple organ systems and morphological structures. But an in-depth examination within the phylogenetic framework of mammals including domesticated forms reveals that the distribution of such traits is not universal, with canids being the only group showing a large set of predicted features. Modularity of traits tied to phylogeny characterizes domesticated mammals: through selective breeding, individual behavioural and morphological traits can be reordered, truncated, augmented or deleted. Similarly, mammalian evolution on islands has resulted in suites of phenotypic changes like those of some domesticated forms. Many domesticated mammals can serve as valuable models for conducting comparative studies on the evolutionary developmental biology of the neural crest, given that series of their embryos are readily available and that their phylogenetic histories and genomes are well characterized.

Keywords: dog; evolutionary developmental biology; island; modularity; ontogeny; pleiotropy.

Figure 1.

Occurrence of features of the ‘domestication syndrome’ in domesticated mammals ([29,30] and references therein) [–36] and the hypothesized mode of domestication for them [2,31]. The mode of domestication can be of different kinds: along the (i) ‘commensal’ pathway, animals are attracted to and taking advantage of elements of the human niche and subsequently develop social and/or economic bonds with humans. The ‘prey’ and ‘directed’ pathways, on the other hand, are initiated by humans. The species undergoing the (ii) ‘prey’ pathway are usually prey species which are domesticated following continuous stages of game management strategies, herd management strategies, and controlled breeding. The (iii) ‘directed’ pathway is an immediate and fast way of domestication, using established knowledge about previous domestication processes (reviewed in [37]). We refer here to traits hypothesized to have been fixed in the initial process of domestication, and not to ‘improvement traits’ [2,38] present only in a proportion of domesticates. The length of the branches is proportional to time of divergence, based on conservative estimates for the divergence among species from different sources [–43]. A test for the presence of a phylogenetic signal [44,45] for each feature was performed using the Mesquite software [46]. Of the characters hypothesized to have occurred in early domesticated forms, only ‘more frequent oestrus cycles’ shows phylogenetic signal which is statistically significant. C, commensal; D, directed; P, prey pathways; asterisks indicate: ‘*’, thoracic, lumbar; ‘**’, increase or decrease; ‘***’, relatively short limbs.

Figure 2.

Many characteristics of domesticated mammals can also be frequently observed in mammals which evolve, or have evolved, on islands.