Abstract

In the past decade the number of studies investigating temperament in farm animals has increased greatly because temperament has been shown not only to affect handling but also reproduction, health and economically important production traits. However, molecular pathways underlying temperament and molecular pathways linking temperament to production traits, health and reproduction have yet to be studied in full detail. Here we report the results of metabolite profiling of the prefrontal cortex and serum of cattle with distinct temperament types that were performed to further explore their molecular divergence in the response to the slaughter procedure and to identify new targets for further research of cattle temperament. By performing an untargeted comprehensive metabolite profiling, 627 and 1097 metabolite features comprising 235 and 328 metabolites could be detected in the prefrontal cortex and serum, respectively. In total, 54 prefrontal cortex and 51 serum metabolite features were indicated to have a high relevance in the classification of temperament types by a sparse partial least square discriminant analysis. A clear discrimination between fearful/neophobic-alert, interested-stressed, subdued/uninterested-calm and outgoing/neophilic-alert temperament types could be observed based on the abundance of the identified relevant prefrontal cortex and serum metabolites. Metabolites with high relevance in the classification of temperament types revealed that the main differences between temperament types in the response to the slaughter procedure were related to the abundance of glycerophospholipids, fatty acyls and sterol lipids. Differences in the abundance of metabolites related to C21 steroid metabolism and oxidative stress indicated that the differences in the metabolite profiles of the four extreme temperament types could be the result of a temperament type specific regulation of molecular pathways that are known to be involved in the stress and fear response.

Highlights

  • Temperament in cattle can be defined as the consistent behavioral and physiological difference observed between individuals in response to a stressor or environmental challenge and is used to describe the relatively stable difference in the behavioral predisposition of an animal, which can be related to psychobiological mechanisms [1,2,3]

  • principal component analysis (PCA) of the complete prefrontal cortex metabolite data and plotting of the principal components (PC)-scores for the first two PCs indicated temperament type specific difference based on the abundance of prefrontal cortex metabolite features at least for the distinct temperament types (Fig 1A), whereas no obvious differentiation could be observed for the serum data (Fig 1B)

  • By applying the variable important in the projection (VIP)-algorithm 54 prefrontal cortex and 51 serum metabolite features were identified to have a high relevance in the classification of temperament types (VIPscore > 1) (Table A and Table B in S3 File)

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Summary

Introduction

Temperament in cattle can be defined as the consistent behavioral and physiological difference observed between individuals in response to a stressor or environmental challenge and is used to describe the relatively stable difference in the behavioral predisposition of an animal, which can be related to psychobiological mechanisms [1,2,3]. The animals that had lower exit times had lower milk yields when milked in a novel environment [2], overall indicating that animals with more excitable temperaments seem to have higher baseline cortisol levels and are more prone to losses in productivity. Studies in mice and rat have shown that the selection for a specific behavior phenotype, like the learned helplessness model of depression in rats [11,12] or the high and low anxiety-related behavior model in mice [13,14], is possible, and several studies in cattle have identified quantitative trait loci for behavior related and temperament related traits [15,16,17,18,19] overall indicating a genetic background of behavior. It is assumed that the selection for temperament types that are well suited for specific production systems will improve productivity and overall animal welfare [6,20,21]

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