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Analysis of the brain transcriptome in lines of laying hens divergently selected for feather pecking.

ABSTRACT: BACKGROUND:Feather pecking (FP) in laying hens reduces animal welfare and leads to economic losses for the layer industry. FP is considered a heritable condition that is influenced by dysregulation of neurotransmitter homeostasis, the gut microbiome, and the immune system. To identify genes and biological pathways responsible for FP behavior we compared the brain transcriptomes of 48 hens divergently selected for FP. In addition, we tested if high feather peckers (HFP) and low feather peckers (LFP) respond differently to light since light has been shown to trigger FP behavior. RESULTS:Of approximately 48 million reads/sample an average of 98.4% were mapped to the chicken genome (GRCg6a). We found 13,070 expressed genes in the analyzed brains of which 423 showed differential expression between HFP and LFP. Genes of uncertain function and non-coding RNAs were overrepresented among those transcripts. Functional analyses revealed the involvement of cholinergic signaling, postsynaptic activity, membrane channels, and the immune system. After the light stimulus, 28 genes were found to be differentially expressed. These included an interaction cluster of core components of the circadian clock. However, differences in the response to light between HFP and LFP were not detectable. CONCLUSIONS:Genes involved in cholinergic signaling, channel activity, synaptic transmission, and immune response were found to be involved in FP behavior. We propose a model in which the gut microbiota modulates the immune system, which in turn affects cholinergic signaling. This might have an influence on monoamine signaling with possible involvement of GABA or glutamate signaling.

SUBMITTER: Falker-Gieske C

PROVIDER: S-EPMC7457272 | biostudies-literature | 2020 Aug

REPOSITORIES: biostudies-literature

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Analysis of the brain transcriptome in lines of laying hens divergently selected for feather pecking.

Falker-Gieske Clemens C Mott Andrea A Preuß Siegfried S Franzenburg Sören S Bessei Werner W Bennewitz Jörn J Tetens Jens J

BMC genomics 20200827 1

<h4>Background</h4>Feather pecking (FP) in laying hens reduces animal welfare and leads to economic losses for the layer industry. FP is considered a heritable condition that is influenced by dysregulation of neurotransmitter homeostasis, the gut microbiome, and the immune system. To identify genes and biological pathways responsible for FP behavior we compared the brain transcriptomes of 48 hens divergently selected for FP. In addition, we tested if high feather peckers (HFP) and low feather pe ...[more]

PMID: 32854615

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Project description:Feather pecking in chickens is a damaging behavior, seriously impacting animal welfare and leading to economic losses. Feather pecking is a complex trait, which is partly under genetic control. Different hypotheses have been proposed to explain the etiology of feather pecking and notably, several studies have identified similarities between feather pecking and human mental disorders such as obsessive-compulsive disorder and schizophrenia. This study uses transcriptomic and phenotypic data from 167 chickens to map expression quantitative trait loci and to identify regulatory genes with a significant effect on this behavioral disorder using an association weight matrix approach. From 70 of the analyzed differentially expressed genes, 11,790 genome wide significantly associated variants were detected, of which 23 showed multiple associations (≥15). These were located in proximity to a number of genes, which are transcription regulators involved in chromatin binding, nucleic acid metabolism, protein translation and putative regulatory RNAs. The association weight matrix identified 36 genes and the two transcription factors: SP6 (synonym: KLF14) and ENSGALG00000042129 (synonym: CHTOP) as the most significant, with an enrichment of KLF14 binding sites being detectable in 40 differentially expressed genes. This indicates that differential expression between animals showing high and low levels of feather pecking was significantly associated with a genetic variant in proximity to KLF14. This multiallelic variant was located 652 bp downstream of KLF14 and is a deletion of 1-3 bp. We propose that a deletion downstream of the transcription factor KLF14 has a negative impact on the level of T cells in the developing brain of high feather pecking chickens, which leads to developmental and behavioral abnormalities. The lack of CD4 T cells and gamma-Aminobutyric acid (GABA) receptors are important factors for the increased propensity of laying hens to perform feather pecking. As such, KLF14 is a clear candidate regulator for the expression of genes involved in the pathogenic development. By further elucidating the regulatory pathways involved in feather pecking we hope to take significant steps forward in explaining and understanding other mental disorders, not just in chickens.

Project description:BackgroundFeather pecking (FP) is a maladaptive behavior in laying hens that is associated with numerous physiological traits, including those involving the central neurotransmitter system and the immune system, which have been identified in many species as being regulated by the gut microbiota via the "microbiota-gut-brain" (MGB) axis. Yet, it is unknown whether and how gut microbiota influences FP by regulating multiple central neurotransmission systems and immune system.MethodsThis study was measured the prevalence of severe FP (SFP) in the commercial layer farm. The chicken flock with the highest frequency of SFP were selected for FP phenotype identification. Nontargeted metabolomics was performed to investigated the differences in the peripheral and central metabolites and 16S rDNA sequencing was performed to investigated the differences in gut microbiome of laying hens with different FP phenotypes. Correlation analysis was performed to determine the potential mechanism by which the disturbed gut microbiota may modulate host physiology and behavior.ResultsThe results showed that pullets (12 weeks of age) showed significantly higher SFP frequencies than chicks (6 weeks of age) and adults (22 weeks of age; p < 0.05). Compared to neutrals (N), peckers (P) exhibited the stress-induced immunosuppression with the increased plasma levels of corticosterone and norepinephrine, and the decreased plasma levels of IgA, IL-1, IL-6 and tumor necrosis factor α (p < 0.05). In the cecum, the relative abundances of Bacteroides and Gemmiger were higher in the P group, while Roseburia, Ruminococcus2, Anaerostipes, Lachnospiracea_incertae_sedis and Methanobrevibacter were more enriched in the N group. Moreover, increased plasma levels of L-tryptophan, beta-tyrosine and L-histidine were found in the P group (p < 0.05). Notably, in the P group, hippocampal levels of L-tryptophan, xanthurenic acid, L-histidine and histamine were improved and showed a positive association with L-glutamic acid levels. Plasma levels of L-tryptophan, beta-tyrosine and L-histidine were both positively correlated with Bacteroides abundance but negatively correlated with Methanobrevibacter abundance.ConclusionOverall, these findings suggest that the development of FP may be affected by the gut microbiota, which regulates the central glutamatergic nerve system by altering the metabolism of tryptophan, histidine and tyrosine.

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Analysis of the brain transcriptome in lines of laying hens divergently selected for feather pecking.

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Analysis of the brain transcriptome in lines of laying hens divergently selected for feather pecking.

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