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The Neuroscience of Domestication

Abstract:


From being hunter-gatherers, humans switched to agriculture about 12,000 years ago. This new age saw an increase in plant and animal breeding catering to diverse human needs. Different animals were domesticated for different purposes. However, Darwin noticed that all domesticated animals had similar features. So how are all these animals belonging to unrelated species showing the same traits? Is their motivation to approach and interact with humans influenced by specific genes? This article shall highlight recent studies that aim to answer these questions.


 

Charles Darwin heavily relied on the observations drawn from plant and animal breeding to explain his theory of inheritance. His, then controversial, findings drew a parallel between domestication (artificial selection) and natural selection. He believed that identifying the mechanism of domestication might help in understanding evolution by natural selection(1).

Darwin observed that the domesticated animals displayed certain features that set them apart from their wild counterparts. This list of features includes tameness, depigmentation of coat colour, floppy ears, smaller snout, non-seasonal oestrus cycle, prolonged juvenile behaviour and reduced tooth & brain size. The appearance of this ensemble of characters is called domestication syndrome (DS)(2–4). These features have been seen in various animals domesticated based on a different selective pressure. Some of these features are even seen in birds and fish. Hence, it can be concluded that the appearance of this set of features is not a coincidence(3).


Despite being a key piece in understanding evolution, the genetic basis of domestication is not well known. One popular theory that tries to explain the domestication syndrome is the neural crest theory.


What is the neural crest theory?

During the early embryogenesis stage, Neural Crest cells (NC) arise from the dorsal margins of the neural tube. These stem cells then migrate throughout the body and differentiate into different cell types. The broad range of neural crest derivatives include melanocytes which control pigmentation of coat, odontoblasts (tooth precursor cells) and secretory cells in adrenal glands which produces dopamine, epinephrine and non-epinephrine. NCs are also a source of dopaminergic neurons in substantia nigra, the brain region responsible for learning and reward processing. Studies show that NCs, in mammals, tightly regulate transcription factors crucial for induction, differentiation and mineralisation of skeletal features.


Hence, the abnormal differentiation, migration and/or survival of neural crest cells might lead to DS traits that consistently occur together. It is, thus, hypothesised that mild neurocristopathy leads to the appearance of an ensemble of characters that are actually unselected by-products in domesticated animals(3,4).


However, there are some observations this theory is yet to explain. For example, different dogs have varying degrees of aggression and display a mixture of DS features. Some extremely aggressive breeds like Staffordshire bull terriers have a short rostrum, de-pigmented coat and half pricked ears. However, dogs like Border collie that show increased tameness have longer head and erect ears. In addition, studies on domesticated rats and dogs show no correlation between tameness and coat pigmentation(4).


Hence, it is crucial to address the genetic basis of the DS features and the decoupling of some of these features due to varying selection pressures.


Is there a genetic basis to tameness?

One of the most common traits selected for domestication is tameness. It is a measure of animals’ response to human interaction. Domesticated animals can be divided into two groups based on tameness: actively tamed (motivation to approach humans) and passively tamed (reluctance to avoid humans). Dr Koide and the group designed three behavioural tests to identify the degree of tameness among 17 inbred mice strains comprising both wild-derived and domesticated mice. Interestingly, the domesticated mice exhibited passive tameness, showing no motivation to approach or interact with humans. The study found the heritability of the tame characteristics seen during the tests ranged from 0.15 to 0.79, indicating that tameness has a genetic basis(5).


The group further went on to establish a line of mice selectively bred for active tameness. They identified two loci named ATR1 and ATR2 in chromosome 11 to have genes associated with active tameness. Studies on dogs that are actively tamed have reported that specific regions in their genome are selected during domestication. Comparative analysis of these regions with ATR1 and ATR2 loci indicates three candidate genes that might be responsible for tameness. These genes are already known to be associated with anxiety, aggression, sociability and stress response(6).


Tameness is a complex trait under the control of multiple loci. Several studies on tamed fox, dogs, rats and mice have identified many potential genes responsible for tameness, aggression and other hallmark traits of domesticated animals(6,7). But how these genes influence the behaviour of a tamed animal is yet to be explored. Understanding the genetic mechanisms underlying tameness in not only important in understanding domestication syndrome but, at large, will help in deciphering evolution by natural selection.


Hence, our pet’s behaviour towards us are under the influence of these complex neurogenetic mechanisms. So next time, while showering your pet(s) with love, take a moment to think and appreciate the neuroscience behind all of it.



REFERENCES


1. Gregory TR. Artificial Selection and Domestication: Modern Lessons from Darwin’s Enduring Analogy. Evol Educ Outreach [Internet]. 2009 Mar 14;2(1):5–27. Available from: https://evolution-outreach.biomedcentral.com/articles/10.1007/s12052-008-0114-z


2. Ahmad HI, Ahmad MJ, Jabbir F, Ahmar S, Ahmad N, Elokil AA, et al. The Domestication Makeup: Evolution, Survival, and Challenges. Front Ecol Evol [Internet]. 2020 May 8;8. Available from: https://www.frontiersin.org/article/10.3389/fevo.2020.00103/full


3. Wilkins AS, Wrangham RW, Tecumseh Fitch W. The “domestication syndrome” in mammals: A unified explanation based on neural crest cell behavior and genetics. Genetics. 2014;197(3):795–808.


4. Sánchez-Villagra MR, Geiger M, Schneider RA. The taming of the neural crest: A developmental perspective on the origins of morphological covariation in domesticated mammals. R Soc Open Sci. 2016;3(6).


5. Goto T, Tanave A, Moriwaki K, Shiroishi T, Koide T. Selection for reluctance to avoid humans during the domestication of mice. Genes, Brain Behav [Internet]. 2013 Nov 7;12(8):760–70. Available from: https://onlinelibrary.wiley.com/doi/10.1111/gbb.12088


6. Matsumoto Y, Goto T, Nishino J, Nakaoka H, Tanave A, Takano-Shimizu T, et al. Selective breeding and selection mapping using a novel wild-derived heterogeneous stock of mice revealed two closely-linked loci for tameness. Sci Rep [Internet]. 2017 Dec 4;7(1):4607. Available from: http://www.nature.com/articles/s41598-017-04869-1


7. Matsumoto Y, Nagayama H, Nakaoka H, Toyoda A, Goto T, Koide T. Combined change of behavioral traits for domestication and gene-networks in mice selectively bred for active tameness. Genes, Brain Behav. 2020;(August 2020):1–18.

 

About the author



Author: Bharathi Venkatachalam

Author Bio: I am an alumna of SASTRA University and CSIR-CCMB, Hyderabad. I am interested in studying neural circuits underlying behaviour. I strongly believe in ‘science for all’ and hope to be more involved in science communication.

Twitter: @VenkatBharathy


Editor: Dr. Harsh Srivastava

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