Domestication involves raising animals in a different environment from their natural habitat, which ends up modifying their behaviour and physical appearance. Charles Darwin was the first to realize that domestic animals were not only more docile, but had common characteristics such as a shorter snout, drooping ears and lack of skin pigmentation in some areas. These changes are known as the "domestication syndrome".
Domestication involves raising animals in a different environment from their natural habitat, which ends up modifying their behaviour and physical appearance. Charles Darwin was the first to realize that domestic animals were not only more docile, but had common characteristics such as a shorter snout, drooping ears and lack of skin pigmentation in some areas. These changes are known as the "domestication syndrome". However, the processes involved at the initial stages of domestication and its contribution to the acquisition of a domesticated phenotype, have been an enigma for 150 years.
Five years ago, Adam Wilkins (Humboldt University, Germany), Richard Wrangham (Harvard University, USA) and Tecumseh Fitch (University of Vienna, Austria) proposed "the neural crest cell deficit" hypothesis, suggesting that the domestication syndrome was essentially due to slight deficits in the number of cells of the neural crest during embryonic development. The neural crest is a vertebrates-exclusive structure formed in the early stages of development. The neural crest cells migrate throughout the body generating certain structures and cells. For example, melanocytes, cells that produce melanin in the skin, and jaws derive from the neural crest.
Now, the study by researchers Dafni Anastasiadi and Francesc Piferrer, from the Institut de Ciències del Mar (Institute of Marine Sciences, CSIC), confirms the neural crest cell deficit hypothesis and, in addition, shows how the domestication syndrome mechanism works. Their results are published in the journal Molecular Biology and Evolution.
"Darwin described the domestication syndrome ("what"), the researchers Wilkins, Wrangham and Fitch proposed the reason "why" (deficits in neural crest cells), but the mechanisms ("how") was missing. And this last question is what our work resolves ", explain the ICM-CSIC scientists.
Wild and domesticated seabass
The ICM-CSIC scientists thought that changes underlying the "domestication syndrome" must originate very early in the domestication process. Therefore, they compared wild seabass from Medes Islands Natural Reserve, with farmed seabass from a farm located in the same area, and at the initial stages of domestication. The work demonstrates that the "domestication syndrome" occurs through epigenetic changes in DNA methylation of early-development genes and, specifically, of the neural crest. No study before had addressed the participation of epigenetics changes during early development in the first steps of domestication, before the appearance of genetic differences.
Methylation is a chemical modification of DNA that, without modifying its nucleotide sequence, regulates the expression and silencing of genes. It is a so-called 'epigenetic' mechanism. Thus, a wild animal and a domestic animal may have genes with identical genetic sequences, but the environmental conditions can cause changes in DNA methylation, which in turn modifies gene expression and, thus, the phenotype.
Persistence of epigenetic changes
The ICM-CSIC scientists observed that changes in DNA methylation during embryonic development persist into adulthood and affect the expression of genes responsible of some domestication phenotypes, such as jaw deformities or change in pigmentation.
However, the most relevant finding is that the genes with changes in DNA methylation coincide with genes presenting genetic variants (SNP) in captive seabass from a 25-year genetic selection program. Since DNA methylation increases the likelihood of mutation, these results suggest that after several generations these epigenetic changes can be assimilated into the genome. In addition "many of the genes that present these epigenetic changes coincide with the same variants in mammals and domestic birds such as the dog, cat, horse, rabbit, duck, among others", says Francesc Piferrer.
Among these genes there is Adamts9, a gene coding an enzyme involved in the control of organ formation during development, and several genes in the glutamate receptor family. Glutamate is the main neurotransmitter in vertebrates, and glutamate receptor genes have undergone positive selection in all domesticated animals without exception. "Changes in glutamate receptor may be related to an attenuation of the stress response, a key aspect in the development of docility during domestication," say the scientists.
This work constitutes the first empirical demonstration including epigenetic mechanisms that support the neural crest hypothesis to explain the appearance of Darwin's domestication syndrome, and suggest a conserved process valid for all vertebrates.
Original article: Anastasiadi, D., Piferrer, F. 2019. Epimutations in developmental genes underlie the onset of domestication in farmed European sea bass. Molecular Biology and Evolution. Doi: 10.1093/molbev/msz153
Press Release: Delegació CSIC Catalunya