Identification of QTLs for behavioral reactivity to social separation and humans in sheep using the OvineSNP50 BeadChip

Abstract

Background: Current trends in sheep farming practices rely on animals with a greater level of behavioral autonomy than before, a phenotype that actively contributes to the sustainability of animal production. Social reactivity and reactivity to humans are relevant behavioral traits in sheep, known for their strong gregariousness and weak tolerance to handling, which have previously been reported with moderate to high heritabilities. To identify loci underlying such behaviors, we performed a genome study in Romane lambs.

Results: The experiment was carried out on 934 male and female lambs allocated into 9 half-sib families (average of 103 lambs per family) and reared outside. After weaning, all the lambs were individually exposed to 4 standardized behavioral tests combining social isolation, exposure to humans or handling, confinement and novelty (i.e. arena test, corridor test, isolation box test, shearing test). A broad range of behaviors including vocalizations, locomotion, vigilance and flight distance, as well as the cortisol response to handling, were collected. All lambs were genotyped using the Illumina OvineSNP50 BeadChip. QTL detection was performed by linkage, association and joint linkage and association analyses using the QTLmap software. Five main QTL regions were identified on sheep chromosomes (Ovis Aries Region, OAR) 12, 16, 19, 21 and 23 among many other QTLs with small to moderate effects. The QTLs on OAR12, 16 and 21 showed significant associations with social reactivity. The QTLs on OAR19 and 23 were found to be associated with reactivity to humans. No overlapping QTLs were identified for the different traits measured in the behavioral tests, supporting the hypothesis that different genetic factors influence social reactivity and tolerance to humans.

Conclusion: The results of this study using ovine SNP data suggest that in domestic sheep the behavioral responses to social separation and exposure to humans are under polygenic influence. The most relevant QTLs reported in the present study contain interesting candidate genes previously described to be associated with various emotional and social behaviors in mammals.

Figure 1

Likelihood profiles of the linkage analyses on OAR16 for high bleat vocalization in the isolation box test (IBT-HBLEAT), arena test phase 1 (AT1-HBLEAT), arena test phase 2 (AT2-HBLEAT), corridor test phase 1 (CT1-HBLEAT) and for the synthetic variable ISO-HBLEAT. Horizontal lines indicate average thresholds for the five HBLEAT traits at the 5% chromosome wide threshold (5% CW), 1% chromosome wide threshold (1% CW) and 0.1% genome wide threshold (0.1% GW).

Figure 2

Likelihood profiles of the linkage analyses on OAR21 for low bleat vocalization in the arena test phase 1 (AT1-LBLEAT), arena test phase 2 (AT2-LBLEAT), corridor test phase 1 (CT1-LBLEAT) and for the synthetic variable ISO-LBLEAT. Horizontal lines indicate average thresholds for the four LBLEAT traits at the 1% chromosome wide threshold (1% CW), 5% genome wide threshold (5% GW) and 1% genome wide threshold (1% GW).

Figure 3

Likelihood profiles of the linkage analyses on OAR12 for low bleat vocalization in the arena test phase 1 (AT1-LBLEAT), arena test phase 2 (AT2-LBLEAT), corridor test phase 1 (CT1-LBLEAT) and for the synthetic variable ISO-LBLEAT. Horizontal lines indicate average thresholds for the four LBLEAT traits at the 5% chromosome wide threshold (5% CW), 1% chromosome wide threshold (1% CW) and 5% genome wide threshold (5% GW).

Figure 4

Likelihood ratio test profiles on OAR16 for ISO-HBLEAT with the linkage or association analyses, Likelihood ratio test profiles on OAR16 for AT2-HBLEAT with the linkage or association analyses. A: Horizontal lines indicate the 1% chromosome wide threshold for linkage analysis (1% CW LA) and the 5% genome wide threshold for association analysis (5% GW GWAS) for ISO-HBLEAT. B: Horizontal lines indicate the 0.1% genome wide threshold for linkage analysis (0.1% GW LA) and the 1% genome wide threshold for association analysis (1% GW GWAS) for AT2-HBLEAT.

Figure 5

Likelihood ratio test profiles on OAR12 for ISO-LBLEAT with the linkage or association analyses. Horizontal lines indicate the 5% genome wide threshold for linkage analysis (5% GW LA) and the 1% genome wide threshold for association analysis (1% GW GWAS).

Figure 6

Likelihood ratio test profiles on OAR19 for CORT with the linkage or association analyses. Horizontal lines indicate the 5% chromosome wide threshold for linkage analysis (5% CW LA) and the 5% chromosome wide threshold for association analysis (5% CW GWAS).

Figure 7

Manhattan plot of the likelihood ratio test values obtained for AT2-LOCOM by GWAS. The likelihood ratio test is plotted against SNP haplotype positions (four consecutive SNPs) along the genome (from chromosome one to 26). Horizontal lines indicate the 5% genome wide threshold (5% GW) or the 0.1% genome wide threshold (0.1% GW) for association analysis.