Is the domestication syndrome a myth?

In most if not all of my posts on domestication and dedomestication I mentioned the concept of the domestication syndrome that says that domestication works by the same mechanisms and has the same effects in any species that was domesticated. Domestic animals share certain traits, which are that eye-catching that it seems very intuitive that the domestication syndrome as such exists. Parts of my dedomestication hypothesis are based on the assumption that there is a domestication syndrome. However, the concept has been called into question in several works. 

The domestication syndrome is the assumption that all domestic animals, mammals in particular, share certain phenotypic traits, both behavioural and morphological. These include paedomorphy in behaviour and morphology, a reduced brain volume, reduced sexual dimorphism, piebald or spotted coat colour patterns, loss of seasonal adaptions, increased reproductive rate, earlier maturity and others. The hypothesis was expanded in publications discussing the findings of the famous Farm fox experiment, namely that artificial selection on tameness alone produced many of the typically domestic traits as a by-product, suggesting that there is a connecting mechanism working during domestication. You can read my post that I linked above for more detail and literature references on that. 

 

The validity of the Farm fox experiment as evidence for the domestication syndrome is called into question in some sources. For example, the alleged cranial shortening in the foxes selected on tameness is based on anecdotical evidence, it turned out that they are not distinguishable from wild foxes in cranial morphology [1]. A brain volume reduction has not been detected in selected foxes [1]. White spotting in the colour that has been said to be a by-product of the selection on tameness is also found in the control group and the foxes selected on increased aggression [2]. However, the white spotting is more common in the foxes selected on tameness than in the other groups [1]. Nevertheless, a spotted coat colour and a curved tail (the latter trait found in 10% of the foxes selected on tameness), is not associated with increased tameness in the individuals [1]. Lord et al. state that due to the limited population size of the starting population, it is possible that shifts in allele frequency were caused by “chance alone” [1], therefore morphological changes in the selected foxes do not necessarily have to be caused by selection on tameness according to the authors [1]. 

However, there seems to be a weak correlation between tame behaviour and white spotted coat colours in rats and foxes [3]. It has been found, interestingly, that there is no correlation between several physical characters considered symptoms of the domestication syndrome (f.e. floppy ears, spotted coat colours) among each other, and with behaviour among dogs [4]. This seems to be contradictory to what would be expected by a very strict application of the domestication syndrome hypothesis. Also, mutations causing piebald coat colour patterns also appear in wild animals. It is not all that rare in several deer species, for example moose in North America: 

If the piebald coat colour patterns in domestic animals are strongly connected to tameness, it would have to be expected that these moose are also less fearful towards humans than their “normally” coloured conspecifics. This assumption would have to be tested. 

There is a paper by Lord et al. that calls brain volume reduction as a consequence of domestication into question [5]. However, the reduction of brain volume is well-documented for many domesticated species [6], and has recently also been found to be the case in cattle compared to the aurochs [7]. Another problem is that the paper by Lord et al. adopts the premature conclusion by Gaunitz et al. 2018 that the Przewalski’s horse is feral and “not wild in any sense” [6], while they consider the feral European mouflon a wild animal to compare sheep against [6]. So they consider a wild animal feral and a feral animal wild, what is a bit of a problem in the argumentation. 

A major component of the hypothesis that selection on behaviour results in alterations of physical appearance is the proposal that neural crest cell genes are affected by selection on tameness [2,8]. The neural crest is a precursor of many cell types in vertebrates, pigment cells among them. The hypothesis says that if the genes of neural crest cells are affected by selection on tameness, the migration of the precursors of pigment cells is distorted, causing irregular unpigmented areas on the body, resulting in the piebald coat colour that is seen in many domestic animals. A very recent paper compared neural crest genes of domestic animals of several species and compared it to the respective wildtypes or animals related to the wildtype (bison were used to compare with domestic cattle, for example). The result was that evidence for positive selection on neural crest genes was found in nearly all cases [8], providing support for the hypothesis that alterations of the genes of the neural crest played a role in domestication of the species that have been domesticated [8]. Interestingly, in the Farm fox experiment it was noted that crossing two white-marked foxes would occasionally produce offspring that held their head askew [1]. I think it is possible that the allele(s) producing these white markings are connected to factors detrimental for the development of the nervous system, what would support the neural crest hypothesis, although other explanations are plausible as well (f.e. asymmetric development of musculature, abnormities in the vestibular system) – that phenomenon deserves further investigation in my opinion. 

Domestication goes hand in hand with an increase of deleterious alleles as a result of mutation accumulation since natural selection plays no or only a minor role in domesticates. This phenomenon is described as the “costs of domestication” [9]. Mutation accumulation might be an alternative explanation for why piebald coat colour patterns are found in all domesticated species. Rather than being connected to behavioural aspects that get selected for during domestication, it is possible that these piebald patterns showed up due to spontaneous mutations that also appear in wild populations, and humans tended to favour these deviant colour variants in their breeding regime. In fact, piebald patterns are only one type of novel colours that appear in domestic populations. Many domesticated species show melanism (found in cattle, dogs, horses, cats and others), erythricism, leucism and albinism as much as completely novel coat colours, yet nobody suggested that these pigment modifications are a common consequence of domestication and possibly connected to behavioural traits (with the exception of melanism, which has been linked to increased aggression in the past). Piebald patterns even exist in “domesticated” fish such as the goldfish, and as far as I know goldfish were never particularly selected for tameness. The fact that white markings are more common in the foxes selected on tameness than in the other lineages can also be due to genetic drift or the loci regulating those markings being coincidentally genetically linked with those regulating tameness on the same chromosome. Therefore, white spots do not necessarily have to be a consequence of behavioural modifications during domestication.

While white spotted patterns are not a good example for the connection between physical characteristics and behaviour and the role of this possible connection in domestication, I would not give up that hypothesis. We should not forget that paedomorphy and a reduced brain volume are very common among domestic animals, and that changes in hormone productions likely played a role in domestication. Thyroid hormones have a major role in postnatal growth, pigmentation, brain development, adrenal gland function and development of the gonads [10]. Selection on tameness is, to a certain degree, selection on paedomorphic behaviour as the fear response of juvenile mammals is much less intense than that of fully grown ones. Therefore, selection on tameness might have influenced the overall development, causing the expression of hormones relevant in adulthood to be delayed. This would lead to an overall paedomorphy because it would affect thyroid hormones, among others (corticosteroids might play a role as well). If the consequence is a shortage in thyroid production, this would have a dramatic influence on the morphology of the animals. For example, hypothyroidic rats are smaller, have a shorter snout and floppy ears – they have paedomorphic, domestic characters. Hypothyroidism is also known to cause cretinism in humans, which includes symptoms such as shortened extremities, reduced body size and lowered cognitive abilities. This is what we see in many domestic animals. I also think that hormonal changes are responsible for the brain volume reduction, perhaps even the thyroid hormones, rather than the fact that a domestic life is less cognitively demanding than a life in the wild, what is usually offered as explanation for the smaller brains of domesticates. We should also not forget that the neural crest genes of domesticates show signs of positive selection as outlined above, although pleiotropic effects leading to a change in physical appearance have not been proven directly yet. 

I think the domestication syndrome concept would be invalidated if there was a domesticated species that is completely devoid of any traits that are considered symptoms of the domestication syndrome such as paedomorphy, reduced brain volume and others, yet still behaves completely domestic, i.e. has a very moderate fear response, reduced aggression and increased tameness compared to its wildtype, trainability and agreeableness. Sixteen mammal species have been domesticated, yet there is no such case. This indicates to me that the domestication syndrome is a valid concept, although piebald colour patterns possibly have to be excluded from the list of symptoms considering the weak to absent correlation between them and tameness. 

 

Literature

 

[1] Lord et al.: The history of Farm foxes undermines the animal domestication syndrome. 2019. 

[2] Wilkins: A striking example of developmental bias in an evolutionary process: the “domestication syndrome”. 2019 

[3] Wilkins et al.: The “domestication syndrome” in mammals: A unified explanation based on neural crest cell behaviour and genetics. 2014

[4] Wheat et al.: Morphology does not covary with predicted behavioral correlations of the domestication syndrome in dogs. 2020. 

[5] Lord et al.: Brain size does not rescue domestication syndrome. 2020. 

[6] Balcarcel et al.: The mammalian brain under domestication: discovering patterns after a century of old and new analyses. 2021. 

[7] Balcarcel et al.: Intensive human contact correlates with smaller brains: differential brain size reduction in cattle types. 2021. 

[8] Rubio: Neural crest cell genes and the domestication syndrome: A comparative analysis of selection. 2022. 

[9] Moyers et al: Genetic costs of domestication and improvement. 2017. 

[10] Dobney & Larson: Genetics and animal domestication: new windows on an elusive process. 2005