The Journal of Heredity 2001:92(3)
© 2001 The American Genetic Association 92:290-292
Brief Communication |
A QTL Study of Cattle Behavioral Traits in Embryo Transfer Families
From the Department of Animal and Poultry Science (Schmutz, Winkelman-Sim, and Buchanan) and the Department of Herd Medicine and Theriogenology (Stookey and Waltz), University of Saskatchewan, Saskatoon, Canada, and Bova Can Labs, Saskatchewan Research Council, Saskatoon, Canada (Plante).
Address correspondence to Sheila Schmutz, Department of Animal and Poultry Science, 51 Campus Dr., University of Saskatchewan, Saskatoon S7N 58A, Canada, or e-mail: schmutz;casask.usask.ca.
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Abstract |
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Two behavioral traits, temperament and habituation, were measured in 130 calves from 17 full-sib families which comprise the Canadian Beef Cattle Reference Herd. Using variance components, heritability was calculated as 0.36 for temperament and 0.46 for habituation. Genotyping of 162 microsatellites at approximately 20 cM intervals allowed the detection of six quantitative trait loci (QTL) for behavior traits on cattle chromosomes 1, 5, 9, 11, 14, 15.
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Introduction |
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The inheritance of behaviors in domestic animals is of considerable interest to livestock producers, but it has been the focus of relatively few studies. In part, this may be because of the difficulty of assessing or quantifying a behavior for statistical analyses. For example, most studies with cattle rely on a subjective scoring scale to assess temperament during some handling procedure (Dickson et al. 1970; Hearnshaw and Morris 1984; Tulloh 1961; Voisinet et al. 1997). Temperament of an animal can be defined as "an animal's behavioral responses to handling by humans" (Burrow et al. 1997), including its excitatory or inhibitory reactions, level of motor activity, persistent habits, emotionality, alertness, etc. (Hurnik et al. 1995), and as such is not easily quantified. However, certain aspects of temperament such as excitability and the level of motor activity during handling have been quantified (Burrow and Dillon 1997; Stookey et al. 1994) and proven to be persistent over time (Grandin 1993). In addition, these objective measurements have been correlated to at least one physiological response—heart rate (Piller et al. 1999; Waynert et al. 1999). Because selection for certain behaviors is considered to be useful to humans and/or to the animal (Schmutz and Schmutz 1998) it would be beneficial to establish that such behaviors are inherited and therefore could potentially be mapped.
Some studies in humans have been conducted to evaluate relationships between behavior and specific candidate genes, often chosen on the basis of neurochemical properties. Polymorphisms in type 4 dopamine receptor (DRD4) (Ekelund et al. 1999) and in dopamine receptor type 2 (Noble et al. 1998) have been associated with novelty seeking as assessed by the temperament and character inventory (Ekelund et al. 1999). This same assessment was used by Kumarkiri et al. (1999) to conclude that alleles in the serotonin transporter transcriptional control region were associated with cooperativeness. An intronic polymorphism in tryptophan hydroxylase was used as a marker to show it appears to be associated with antagonistic behavior (Manuck et al. 1999).
Quantitative trait loci (QTL) mapping is being used in humans and mice for complex traits, and some of these include behaviors. We report here on a study that attempts to map two behavioral traits using a QTL approach in beef cattle: the response to isolation during handling (which we believe to be a reflection of temperament) and habituation to the handling procedure.
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Methods |
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Animals
A herd of 17 families composed of 130 embryo transfer calves was used in this study. The calves were raised by surrogate mothers or recipient dams, as opposed to their biological mothers. As is typical of cow herds, the sires were not in contact with their calves either. The calves were weaned from their recipient dams at 6 months of age and trucked for approximately 2 h from the ranch where they were born to the University of Saskatchewan Beef Research Station. The newly weaned calves arrived in six groups of a few families each over a period of 4 months. The calves were unloaded from the trucks and group penned until each was individually weighed and measured within the next hour.
Behavior Measurements
Each group was assessed upon arrival at the feedlot and again on a single day when they ranged in age from 8 to 12 months. The difference between the initial score at weaning and this later measurement, we call "habituation," since the animals had been weighed in this same building, and therefore held briefly in this same device, every other week since weaning.
During the behavioral assessment, cattle were moved single file through an indoor handling facility and held individually on an electronic platform scale for 1 min. Solid sliding doors and sides prevented the animal from seeing other cattle. The amount of movement made by the animal during the 1-min test was quantified by an electronic movement measuring device (MMD) attached to the load cells of the weight scale (Stookey et al. 1994). The MMD samples the analogue voltage signal at 122 discrete time intervals per second. Any movement by the animal on the scale causes the signal to fluctuate. A peak is recorded whenever a trend of increasing or decreasing voltage is reversed. The number of peaks recorded is correlated to the amount of movement that can be detected by video analysis (Stookey et al. 1994). We call this response to isolation "temperament," in the sense that agitation and movement during handling can be thought of as a reflection of an animal's temperament.
Heritability Calculation
Heritability was calculated from variance components obtained from analysis of variance (ANOVA) using a nested design with biological dams nested within sires, since each sire was mated to more than one dam and hence had more than one full-sib family.
Genotyping
One hundred and sixty-two microsatellites were selected at approximately 20 cM intervals throughout the genome. We chose microsatellites that had six or more alleles whenever these were available, at approximately 20 cM intervals. Polymerase chain reaction (PCR) was used to genotype all parents and calves from DNA extracted from blood (Buchanan et al. 1994). Genotypes were scored twice independently and discrepancies were resolved or the samples were retyped.
QTL Analysis
It was necessary to use an analysis that could summarize information about each marker-QTL linkage (Knott and Haley 1992) across several small full-sib families. We used a modified identical-by-descent analysis procedure. Each sib pair within a family (i.e., a family of 5 sibs would constitute 10 sib pairs) was designated as being like or unlike in their genotype at a given marker. An unpaired t test was used to test the absolute differences in the phenotypes (i.e., MMD score) of like versus unlike groups within each family. The t-test values were squared and summed across all the families and the probability was determined using a chi-squared distribution (Xu and Atchley 1995) with degrees of freedom equal to the number of families (Weller et al. 1990). A P 
.00156 was considered significant (Knott et al. 1996).
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Results |
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The movement score, as a response to isolation, had a mean of 89 ± 5.9 at weaning, with a standard deviation of 56. The movement scores ranged from 21 to 284. The difference between this score and the score several months later, or habituation, had a mean decrease of 17 ± 6 (SD = 70). The range was 267 more to 232 less, indicating that some cattle were more agitated in the first measurement while others were more agitated during the second. In his review, Burrow (1997) states that most studies show temperament improved with age and increased handling.
The heritability of temperament at weaning was calculated as 0.36 and of habituation as 0.46. Several QTL were detected for one and/or both of these traits. Chromosomal locations for QTL detected for both behaviors are shown in Table 1.
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Of anecdotal interest, one night a pen of heifers was scared by something and two animals became so agitated they ran into a post in their corral and each broke their jaw. Both were members of a single family and had high scores (119 and 149) detected during their behavioral measurements. We suggest this exemplifies the problem such a temperament can cause an animal.
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Discussion |
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We found a slightly higher heritability for temperament than most other studies. However, most studies, including ours, agree that temperament is of moderate heritability in beef cattle. Fordyce et al. (1996) studied Shorthorn cross beef cattle in Australia and found a heritability of 0.08–0.014 for their temperament score but 0.32–0.70 for flight distance. Le Neindre et al. (1995) reported a heritability of 0.22 for a docility score based on a Limousin heifer's reactions to being limited to a corner of a pen by a handler. Morris et al. (1994) used a subjective scale of 1–8 for assessing cows during weighing and 1–5 to rate temperament in terms of ease of handling during herding into pens by stockmen in Angus and Hereford beef cattle. They report low to moderate heritabilities with wide standard errors. Mourao et al. (1998) estimate the heritability of temperament as 0.27 using dam-daughter regression analysis of subjective scores between 1 and 5 based on aggressiveness. Using a restraint test in a chute of weaned calves, Stricklin et al. (1980) reported a higher heritability, similar to that found in this study, of 0.44–0.48 which was calculated using paternal half-sib correlations. This measurement of temperament, although subjectively scored, was obtained from the test situation most similar to that used in our study.
In the present study, the embryo transfer protocol used to produce the families created a unique group of individuals deprived of the opportunity to imitate their biological dams' behavior during rearing. Each calf was carried to term and reared by a surrogate mother making it possible to study innate behavioral tendencies with the confounding effects of maternal influence on early experience somewhat diluted. The high heritabilities of behavioral traits that we report may be a reflection of having equalized some of the effects of early environmental (maternal) influences.
The modification in our analysis from the more typical scoring of zero, one, or two alleles shared was done because most families had only one or the other parent heterozygous at a marker instead of both heterozygous, as shown in Figure 1. Some families had both parents heterozygous, but they had the same genotype and the offspring were thus uninformative. A few had neither parent heterozygous. Therefore we did consider the more typical IBD approach, but we did not feel it suited our dataset as well as one might expect. Although we might miss some QTL using only "like or unlike," we believed that this approach was conservative.
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We report six QTL localizations where both of these related behavioral traits were detected. Relatively few coding genes are yet mapped in cattle, but we attempted to look for candidate genes in the regions near these QTL. Cannabinoid receptor (CNR1) was previously mapped by in situ hybridization to the region of chromosome 9 (Pfister-Genskow et al. 1997), where one QTL was found. This gene was mapped in humans to chromosome 6q14-15 (Hoehe et al. 1991). Type 2 and 4 dopamine receptors (DRD2 and DRD4) are localized to human chromosome 11p15.5. DRD2 is mapped to cattle chromosome 15 (Amarente et al. 1999).
Although few studies have attempted QTL mapping of behavioral traits in animals, Turri et al. (1999) reported three localizations for "emotionality" in mice, chromosomes 1, 12, and 15. Their behavior measurements for this trait were the total distance a mouse traversed in an open field arena in 5 mm and the number of fecal boli during this 5-min time period. The region on mouse 1, from 92 to 105 cM, is homologous to the upper third of cattle chromosome 16. The area on mouse chromosome 15, at approximately 43 cM, in which they found a QTL, is homologous to cattle chromosome 14 in the region where a QTL was found in this study.
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Acknowledgments |
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The authors are grateful for the financial support provided by the Canadian Cattlemen's Association, Alberta Cattle Commission, and Natural Science and Engineering Research Council (NSERC). The Saskatchewan Agricultural Development Fund provided support for the development and use of the device (M.M.D.) for quantifying animal movement. The help provided by the staff of the Termuende Farm and the University of Saskatchewan Beef Research Facility was also greatly appreciated.
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Footnotes |
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Corresponding Editor: Bruce S. Weir
Received May 5, 2000
Accepted January 16, 2001
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References |
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