Human self-domestication: can animal models help to explore the role of epigenetics in vertebrate domestication?

Abstract

Human evolution is characterized by the acquisition of features found in domesticated animals referred to as the self-domestication hypothesis. Features of self-domestication appear altered in people with cognitive diseases, including autism spectrum disorders, schizophrenia and Williams syndrome. The genetic basis of self-domestication has been revealed by non-random associations of animal domestication candidate genes with genes positively selected in recent humans and involved in cognitive disorders. Epigenetic modifications may have also participated in human self-domestication. However, their role is difficult to disentangle unless using animal models because epigenetics have a partly genetic basis and epigenetic patterns are tissue-specific, while only fossil bones are available. Here, we used our published dataset on the early domestication effects on DNA methylation of European sea bass (Dicentrarchus labrax). We mapped 2114 genes related to mammalian domestication to their orthologues in sea bass. We overlapped these with genes differentially methylated between wild and domesticated fish (n = 3, 4 tissues). A set of ~90 orthologues exhibited changes at the early domestication stages in fish. Moreover, we found overlaps with genes selected in anatomically-modern humans and with candidates for human-specific cognitive disorders. Thus, alterations of their methylation status may account in part for some of the human self-domestication phenotypes, and because of the links between self-domestication and cognitive disorders, also for aspects of the etiology of these disorders. Our results suggest that epigenetic modifications can be a general feature involved in vertebrate domestication, and highlight the need to catalogue methylation differences to gain insights into human evolution