Unraveling the phenotypic and genomic background of behavioral plasticity and temperament in North American Angus cattle

Abstract

Background: Longitudinal records of temperament can be used for assessing behavioral plasticity, such as aptness to learn, memorize, or change behavioral responses based on affective state. In this study, we evaluated the phenotypic and genomic background of North American Angus cow temperament measured throughout their lifetime around the weaning season, including the development of a new indicator trait termed docility-based learning and behavioral plasticity. The analyses included 273,695 and 153,898 records for yearling (YT) and cow at weaning (CT) temperament, respectively, 723,248 animals in the pedigree, and 8784 genotyped animals. Both YT and CT were measured when the animal was loading into/exiting the chute. Moreover, CT was measured around the time in which the cow was separated from her calf. A random regression model fitting a first-order Legendre orthogonal polynomial was used to model the covariance structure of temperament and to assess the learning and behavioral plasticity (i.e., slope of the regression) of individual cows. This study provides, for the first time, a longitudinal perspective of the genetic and genomic mechanisms underlying temperament, learning, and behavioral plasticity in beef cattle.

Results: CT measured across years is heritable (0.38-0.53). Positive and strong genetic correlations (0.91-1.00) were observed among all CT age-group pairs and between CT and YT (0.84). Over 90% of the candidate genes identified overlapped among CT age-groups and the estimated effect of genomic markers located within important candidate genes changed over time. A small but significant genetic component was observed for learning and behavioral plasticity (heritability = 0.02 ± 0.002). Various candidate genes were identified, revealing the polygenic nature of the traits evaluated. The pathways and candidate genes identified are associated with steroid and glucocorticoid hormones, development delay, cognitive development, and behavioral changes in cattle and other species.

Conclusions: Cow temperament is highly heritable and repeatable. The changes in temperament can be genetically improved by selecting animals with favorable learning and behavioral plasticity (i.e., habituation). Furthermore, the environment explains a large part of the variation in learning and behavioral plasticity, leading to opportunities to also improve the overall temperament by refining management practices. Moreover, behavioral plasticity offers opportunities to improve the long-term animal and handler welfare through habituation.

Fig. 1

Distribution of the age in days for the cow at weaning temperament records (a) and the number of repeated records per cow (b). Vertical dashed-red lines are the thresholds used to cluster the records into nine age groups

Fig. 2

Phenotypic average of temperament across age groups and their significance (a) and the phenotypic average of yearling temperament grouped by age of dam (b)

Fig. 3

Variance, heritability, and repeatability estimates across the years for cow at weaning temperament. ${\mathrm{\sigma }}_{\mathrm{cg}}^2$ is the contemporary group variance; ${\mathrm{\sigma }}_{\mathrm{u}}^2$ is the additive genetic variance; ${\mathrm{\sigma }}_{\mathrm{pe}}^2$ is the permanent environmental variance; ${\mathrm{\sigma }}_{\mathrm{e}}^2$ is the residual variance; ${\mathrm{h}}^2$ is the heritability; and Rep is the repeatability

Fig. 4

Additive genetic (a) and phenotypic (b) correlations among pairs of age group for temperament measured on cows at weaning. Lower diagonal: correlations; upper diagonal: values between parentheses are the standard deviations for the correlations

Fig. 5

Genetic and permanent environment components for the probability of an animal being docile across the years. a GEBV of three sires with habituation (points), sensitization (square), and neutral (triangle) learning and behavioral plasticity. b GEBV of a sire (light blue line) and its daughter that have at least two CT records and have siblings in the same contemporary group. c–e Permanent environment impact (PE) of daughters of a single sire raised in same conditions (same contemporary group). EBV: probability of being docile at a genetic level; PE: impact of the permanent environment on the probability of being docile

Fig. 6

Percentage differences of SNP-window effect across the years for the top 20 genomic regions selected based on the effect for 3, 7, and > 10 years age groups. The liability effect was converted, in which increasing values mean becoming more docile. The SNP-window effect for age group 3-years-old was considered as the baseline for comparison

Fig. 7

Venn diagram for the overlapping genes identified for the top 20 SNP-window based on absolute effect for the cow at weaning temperament and genes identified by Alvarenga et al. [5] for yearling temperament

Fig. 8

Manhattan plot for the average cow temperament measured at weaning (a) and learning and behavioral plasticity (b) components of a random regression model for cow temperament measured at weaning