Can we pin the fluffy tails of our pet dogs on neural crest cells?

Domest­ic­ated anim­als share sim­il­ar fea­tures, such as floppy ears, curly tails, and smal­ler brains. A new study pub­lished in Evol­u­tion Let­ters chal­lenges the most pop­u­lar explan­a­tion for how these fea­tures arose. Lead author Dr Laura Wilson tells us more.

Charles Dar­win was first to notice that dif­fer­ent domest­ic anim­als share sim­il­ar char­ac­ter­ist­ics des­pite not being closely related. These fea­tures (see Fig­ure 1), called the domest­ic­a­tion syn­drome, have long puzzled evol­u­tion­ary bio­lo­gists – what causes them to devel­op and how?

Fig­ure 1. Left, fea­tures that are com­mon among domest­ic­ated anim­als, referred to as the ‘domest­ic­a­tion syn­drome’. The domest­ic­a­tion syn­drome has been hypo­thes­ized to be caused by neur­al crest cell defi­cits. We assessed mor­pho­lo­gic­al evid­ence for this by invest­ig­at­ing the pat­tern­ing of shape in the skull, focus­ing on its embryon­ic tis­sues ori­gins (meso­derm, red; neur­al crest, blue). 

In 2014, genet­i­cists pro­posed a com­pel­ling explan­a­tion: selec­tion on tame­ness dur­ing the early phases of domest­ic­a­tion has led to dis­rup­tions in the devel­op­ment of neur­al crest cells, thereby caus­ing the domest­ic­a­tion syn­drome. Many tis­sues in the body – such as car­til­age, bone, and con­nect­ive tis­sue – form from neur­al crest cells, and this hypo­thes­is gained much trac­tion in the lit­er­at­ure, with sup­port­ing evid­ence sur­fa­cing from gen­om­ic data. 

In our study, we set out to provide the mor­pho­lo­gic­al piece of the puzzle, ask­ing wheth­er there was evid­ence for the neur­al crest hypo­thes­is among dif­fer­ent pairs of wild and domest­ic mammals. 

We used advanced 3D quant­it­at­ive approaches to record vari­ation in the shape of cra­ni­al bones, con­trast­ing those bones of the cra­ni­um that form from neur­al crest (the facial region) with those that derive from meso­derm ori­gins (the vault region) (Fig­ure 1). We com­pared six pairs of domest­ic­ated mam­mals with their wild rel­at­ives using over 500 spe­ci­mens from his­tor­ic­al col­lec­tions world­wide, includ­ing pigs and boars, dogs and wolves, goats and bezoar, llama (Fig­ure 2) and guanaco, among oth­ers. These rep­res­ent examples for each of the dif­fer­ent path­ways that human-anim­al inter­ac­tions have taken (e.g. com­pan­ion­ship, pro­vi­sion of food).

Fig­ure 2. Lama glama, one of the forms stud­ied by Wilson et al. Photo taken by Laura Wilson in Puna, Peru – the ‘birth­place’ of South Amer­ic­an camelid domestication.


We hypo­thes­ized that, if the neur­al crest hypo­thes­is was respons­ible for changes asso­ci­ated with domest­ic­a­tion, in domest­ic forms we would recov­er 1) dif­fer­ences in trait inter­ac­tions among neur­al crest bones com­pared to meso­derm bones and 2) great­er vari­ation in shape among neur­al crest bones. 

By adopt­ing the ana­lyt­ic­al frame­works of mod­u­lar­ity and integ­ra­tion, we con­duc­ted a suite of mor­pho­lo­gic­al-based tests of shape vari­ation. We did not find strong evid­ence for our pre­dic­tions under the neur­al crest hypo­thes­is. Instead, we showed that domest­ic forms had great­er shape vari­ation in both meso­derm and neur­al crest bones com­pared to their wild coun­ter­parts (Fig­ure 3), and that neur­al crest bones differed in integ­ra­tion mag­nitudes (a meas­ure of con­nec­ted­ness) com­pared to meso­derm bones, but again this was not exclus­ive to domest­ic forms. 

Fig­ure 3. Vari­ation in cra­ni­al shape among bones derived from neur­al crest (NC: blue) and meso­derm (MD: red) ori­gins, con­trast­ing domest­ic (filled boxes) and wild (open boxes) forms.

From the per­spect­ive of cra­ni­al trait inter­ac­tions, our res­ults sug­gest­ing that the domest­ic­a­tion pro­cess has co-opted under­ly­ing rela­tion­ships and that the astound­ing amount of cra­ni­al vari­ation that has been gen­er­ated (e.g. pugs, poodles, great danes) does not appear exclus­ive to neur­al crest derived bones.

The valid­ity of the domest­ic­a­tion syn­drome, and the con­di­tions under which its expect­a­tions are met, con­tin­ue to be a sub­ject of con­tro­versy. Our res­ults add to the nar­rat­ive that domest­ic­a­tion is not a ‘one size fits all’ process.

Dr Laura Wilson is an Aus­trali­an Research Coun­cil Future Fel­low and Head of Bio­lo­gic­al Anthro­po­logy at the Aus­trali­an Nation­al University.