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. 2012 Sep;8(9):e1002962.
doi: 10.1371/journal.pgen.1002962. Epub 2012 Sep 27.

A comparison of brain gene expression levels in domesticated and wild animals

Frank W Albert  1 , Mehmet Somel, Miguel Carneiro, Ayinuer Aximu-Petri, Michel Halbwax, Olaf Thalmann, Jose A Blanco-Aguiar, Irina Z Plyusnina, Lyudmila Trut, Rafael Villafuerte, Nuno Ferrand, Sylvia Kaiser, Per Jensen, Svante Pääbo
Affiliations

A comparison of brain gene expression levels in domesticated and wild animals

Frank W Albert et al. PLoS Genet. 2012 Sep.

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.

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Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

Figure 1
Figure 1. Gene expression in domesticated and wild animals.
Cortical gene expression in four domesticated animal species is compared to their wild relatives (blue arrows), followed by comparisons between the four domestication events (red arrows). Next to each domesticated/wild pair, a heatmap shows expression levels of all respective DE genes (Table 1). Genes were individually normalized and sorted by DE p-value, separately for genes up- and downregulated in domestication. Red (blue): lower (higher) expression. Due to the high number of DE genes, gene names are omitted for the guinea pig comparison. See Dataset S2 for details on the DE genes.
Figure 2
Figure 2. Expression differences between domesticated and wild animals.
A. Pairwise expression differences. Plotted for each comparison is in black on the left the mean variance explained by domestication, along with 95% confidence intervals (box whiskers) based on 10,000 bootstraps across genes. On the right in light blue is the null distribution of mean variance explained by domestication based on permutations of the domestication factor (box whiskers comprise 95% of the distribution, central horizontal bar is the median). B. For each comparison, the mean variance explained by domestication across genes is plotted as a function of sequence divergence expressed as the median fraction of nucleotides that differ between any two domesticated and wild animals in that comparison.
Figure 3
Figure 3. Gene expression across domesticated species.
A and B) For each of three models, the figure shows the number of genes that match or exceed the p-value for the domestication factor and that are expressed in the same direction in domesticated animals. The thick black line shows the real data. Each grey line shows the result from one of the possible extreme permutations (see Note S1 for details). p = 1 is included to show the effect of only requiring genes to be expressed in the same direction, irrespective of significance. vsd: variance stabilized data. A) joint analyses of dogs, pigs and rabbits. B) As in A, but including guinea pigs.
Figure 4
Figure 4. Expression levels of four genes with common expression in domesticated dogs, pigs, rabbits, and guinea pigs.
Blue: domesticated animals, red: wild animals. Shown are the four genes with the lowest p-values for the domestication factor across dogs, pigs and rabbits, and with expression change in the same direction in these three species as well as guinea pigs. Expression levels are from variance stabilized data, separately normalized to the median in each species pair.
Figure 5
Figure 5. Expression differences between tame and aggressive rats.
A. Heatmap showing expression levels of DE genes. Genes were individually normalized and sorted by DE p-value, separately for genes up- and downregulated in domestication. Red (blue): lower (higher) expression. B. A QTL for tameness is located on chromosome one . The x-axis shows the genetic position along chromosome one in centiMorgan (cM). The F-value is a measure of the likelihood of the presence of a QTL. The dashed horizontal line is the genome-wide significance threshold. See for details. C. Expression differences in the tameness QTL region. Top panel: significance and location for each gene. P-values were signed so that positive (negative) values correspond to genes with higher expression in aggressive (tame) rats. Dashed lines: genome-wide 10% FDR threshold, dotted lines: p = 0.05. Lower panel: fold changes. Red: genes with FDR<10%, orange: genes with p<0.05. D: positions of Dll3 and Dhdh (green vertical lines) compared to patterns of DNA polymorphism in the founder animals of the QTL pedigree used to identify the tameness QTL . Blue (red) line: nucleotide diversity in the tame (aggressive) founder animals.
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This work was funded by the Max Planck Society and a European Research Council grant (233297, TWOPAN) to SP. FWA is supported by a grant from the German Science Foundation (DFG grant AL 1525/1-1). MS was supported by a CAS young scientists fellowship (2009Y2BS12) and a National Science Foundation of China research grant (31010022). JAB-A is supported by fellowship (SFRH/BPD/65464/2009). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.