A Comparison of Brain Gene Expression Levels in Domesticated and Wild Animals

Abstract

Domestication has led to similar changes in morphology and behavior in several animal species, raising the question whether similarities between different domestication events also exist at the molecular level. We used mRNA sequencing to analyze genome-wide gene expression patterns in brain frontal cortex in three pairs of domesticated and wild species (dogs and wolves, pigs and wild boars, and domesticated and wild rabbits). We compared the expression differences with those between domesticated guinea pigs and a distant wild relative ( Cavia aperea) as well as between two lines of rats selected for tameness or aggression towards humans. There were few gene expression differences between domesticated and wild dogs, pigs, and rabbits (30–75 genes (less than 1%) of expressed genes were differentially expressed), while guinea pigs and C. aperea differed more strongly. Almost no overlap was found between the genes with differential expression in the different domestication events. In addition, joint analyses of all domesticated and wild samples provided only suggestive evidence for the existence of a small group of genes that changed their expression in a similar fashion in different domesticated species. The most extreme of these shared expression changes include up-regulation in domesticates of SOX6 and PROM1, two modulators of brain development. There was almost no overlap between gene expression in domesticated animals and the tame and aggressive rats. However, two of the genes with the strongest expression differences between the rats ( DLL3 and DHDH) were located in a genomic region associated with tameness and aggression, suggesting a role in influencing tameness. In summary, the majority of brain gene expression changes in domesticated animals are specific to the given domestication event, suggesting that the causative variants of behavioral domestication traits may likewise be different.

Author Summary

Over the millennia, humans have turned a range of wild animal species into what we today know as domesticated animals. Domestication has greatly influenced human history and evolution. The changes in the animals are even more drastic. Domesticated animals differ from their wild relatives in appearance, physiology, and behavior. Although these differences are mostly genetically encoded, little is known about which genes contribute to these domestication traits. Changes in gene expression have long been proposed to lead to phenotypic changes in evolution. In this work, we therefore compared gene expression in brains of dogs and wolves, pigs and boars, and domesticated and wild rabbits and guinea pigs. For each of the four domesticated species, we identify gene expression differences that could correlate with behavioral differences compared to wild animals. The majority of expression differences are unique to each domestication event, suggesting that domestication has proceeded through different genetic routes in different species.