Genetic analysis and evaluation of behavioural traits in cattle

Livestock Science 154 (2013) 1–12

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Review article

Genetic analysis and evaluation of behavioural traits in cattle Krzysztof Adamczyk a,n, Joanna Pokorska a, Joanna Makulska a, Bernadette Earley b, Mickael Mazurek b a

´w, Al. Mickiewicza 24/28, Poland University of Agriculture in Krakow, Department of Cattle Breeding, 30-059 Krako Animal and Bioscience Research Department, Animal & Grassland Research and Innovation Centre, Teagasc, Grange, Dunsany, Co. Meath, Ireland

b

a r t i c l e i n f o

abstract

Article history: Received 11 July 2012 Received in revised form 18 January 2013 Accepted 29 January 2013

The behavioural traits of cattle in terms of docility and manageability have traditionally been the main factors that allowed the domestication of, and use of cattle by humans. Behavioural traits have a profound effect on cattle longevity and are very useful in the assessment of animal welfare and determination of ethical limits to animal handling by humans. In this review, we (1) discussed issues relating to the genetics of the behavioural traits of cattle, (2) characterise current status of cattle breeding in terms of behavioural traits, at the level of population and molecular genetics, giving special consideration to high individual variation in behavioural traits and their relatively high correlations with milk and meat performance traits, (3) discuss the present state of knowledge concerning the identification of quantitative trait loci (QTL) for behavioural traits of cattle, (4) characterise major problems that impede breeding progress in cattle behaviour, including great diversity of methods used for the assessment of behavioural traits and the considerable degree of its subjectivity. In summary, we show the need for systematically improving the effectiveness of cattle breeding with a focus on behaviour, including the consistent and uniform definition of behavioural traits and objective measures of their assessment. & 2013 Elsevier B.V. All rights reserved.

Keywords: Cattle Genetics Behavioural traits Breeding programme

Contents 1. 2.

3.

4.

n

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . The main problems in the evaluation of cattle behaviour . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.1. Definition of behavioural traits . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2. A fear as a basic criterion in cattle temperament assessment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.3. Assessment of cattle temperament for breeding purposes. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.4. Objectivity of methods for the assessment of cattle behaviour . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Population genetics and behavioural traits of cattle . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1. Variation in behavioural traits. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2. Heritability of behavioural traits in cattle and their genetic correlations with production traits. . . . . . . . . . . . . . . . . . . 3.3. Breeding for behavioural traits in cattle . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Molecular genetics and behavioural traits in cattle . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.1. Quantitative trait loci affecting behavioural traits in cattle . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.2. Candidate genes for behavioural traits in cattle . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

Corresponding author. Tel./fax: þ48 12 6624162. E-mail address: [email protected] (K. Adamczyk).

1871-1413/$ - see front matter & 2013 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.livsci.2013.01.016

2 2 2 3 3 4 4 4 5 6 7 7 7

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K. Adamczyk et al. / Livestock Science 154 (2013) 1–12

5.

Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9 Conflict of interest . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9

1. Introduction The first cattle that were domesticated were Bos primigenius. People kept cattle for easy access to food, including milk, blood, and meat, and for use as loadbearers and as work animals (e.g. ploughing). Bos taurus cattle were domesticated approximately 8000 years ago (Hirst, 2009). Cattle use their senses to communicate, thus their behaviour will largely depend on their perception. Most forms of communication are related to the important sensory perceptions, for example, vision, sound, smell and touch. The means of communication will have an important impact on the group structure and cohesion (Albright and Arave, 1997; Phillips, 2002). Cattle behaviour is a means of communication between animals and their environment, enabling them to satisfy the needs necessary for survival of the species under different environmental conditions (Phillips, 2002; Fraser and Broom, 1997; Broom and Fraser, 2007). The way an animal will react will most of the time directly depends on its senses, sensory-related behaviour or its sensory environment. Cattle possess the same senses as other mammals: vision, olfaction, hearing, touch and taste. The most important behavioural traits without which animal domestication and breeding would be impossible include: the capacity for a gradual reduction of fearfulness towards humans; the ability to become gradually subordinate to humans as a dominant individual, the ability to learn desired responses and behaviours, the capacity to breed and to rear offspring under human-created conditions; and the capacity to accept feed provided by humans (Keeling and Gonyou, 2001; Jezierski, 2004). Since the behavioural traits of cattle affect their longevity, breeders regard them as workability traits (Boettcher, 2005; Fogh et al., 2009). Thus the process of cattle domestication and their genetic improvement depend on the flexibility of behavioural traits of animals, which have to adapt to the conditions created by humans (Mignon-Grasteau et al., 2005). These traits play an important role in human– animal–environment relationships, which is particularly noticeable in intensified milk and beef production, when behavioural disorders (e.g. lameness, bar-biting, tonguerolling, excessive licking and grooming or the buller steer syndrome) in cattle are especially frequent (Grandin and Deesing, 1998; Phillips, 2002; Broucˇek et al., 2008). Selection towards single purpose breeds induced behavioural changes more especially in the B. taurus species (Burrow, 1997; Von Keyserlingk and Weary, 2007; Hoppe et al., 2008; Cozzi et al., 2009; Prendiville et al., 2010; Titto et al., 2011). Flexibility of behaviour enables animals to cope with their human-created environment and enables breeders, while respecting the behavioural needs of animals, to obtain higher quantity and/or better quality products from them (Price, 2003; Gruber et al., 2010; Sheahan et al., 2011).

Behavioural traits are therefore helpful in assessing cattle welfare and thus in determining the ethical limits to animal handling by humans (Praks et al., 2007; D’Eath et al., 2009; Nicol, 2011). The considerable role of cattle behaviour from the perspective of milk and beef production resulted in behavioural traits being increasingly used in breeding programs for individual breeds in many countries (Miglior, 2004), although these traits appear to be much more difficult to assess than production traits. This is strictly dependent on the progress of knowledge on cattle behaviour and its genetic and environmental determinants (Morme de, 2005). Therefore, the aim of this paper was to review the key problems in efficient breeding for behavioural traits of cattle, including their phenotypic evaluation, utilisation of population and of molecular genetics in the estimation of genetic parameters and breeding values. Additionally, examples of cattle selection for behavioural traits across countries were reviewed and presented. 2. The main problems in the evaluation of cattle behaviour 2.1. Definition of behavioural traits Cattle behaviour is a function of the whole brain/body and the molecular pathways involved in genetic variability (Herskin et al., 2004; Van Reenen et al., 2004; Morme de, 2005). The plasticity of cattle behaviour and the learning capacities are well developed and are comparable with that of other mammals such as rodents, cats and horses (Kilgour, 1981). Cattle learn by memorising information received by their sensory organs. The information is analysed in the cerebral cortex and learning is made by association, generalisation or discrimination of the stimuli (Albright and Arave, 1997). Robust evaluation of behavioural traits is difficult due to the problems with their definition and subjectivity of measurement. This even applies to such a seemingly well studied trait as cattle temperament. For example, Hurnik et al. (1995) hold that temperament is an animal’s general trait that includes behaviours such as level of physical activity, persistent habits, emotionality, alertness and curiosity. According to the same authors, animal temperament depends on the interaction between excitatory and inhibitory reactions. Meanwhile, Burrow (1997) regarded temperament only as an animal’s behavioural response to handling by humans. Likewise, Phillips (2002) defined this term as an animal’s main personality or mood trait in relation to humans. Sewalem et al. (2011) state that milking temperament is broadly defined as milking behaviour, ease of handling or aggressiveness at feeding. Depending on the definition of cattle temperament different methods of its assessment are used in research and breeding work. Burrow (1997) classified several

K. Adamczyk et al. / Livestock Science 154 (2013) 1–12

dozen methods for assessment of cattle temperament into restrained and non-restrained tests, dairy cow scoring system, dominance tests, free movement test and assessment of maternal temperament. 2.2. A fear as a basic criterion in cattle temperament assessment Temperament is the most important trait of an animal’s personality since it determines their perception and response to different situations (Grandin et al., 1995). This response can be behavioural and/or psychological in nature and can remain constant over time and in different contexts. The visible demonstration of cattle temperament is reactivity (Grignard et al., 2001). Reactivity to humans is mainly be influenced by the previous experience of an animal towards humans and changes depending on the context. In cattle it can be influenced by fear which is defined as a reaction to the perception of an actual danger that threatens the integrity of the individual. Fear is a powerful, emotional state that plays an important role in avoiding potentially dangerous situations (Boissy, 1995). An animal’s response to prepare and cope with danger may be assessed using physiological and behavioural measures (Forkman et al., 2007). Fear reactions are generally triggered by stimuli from the environment that may be associated with a previous negative experience, for example novelty, noise or sudden movements, aggressive handling (Jones, 1997). The main types of reactions that can be observed are: active reactions that can be active defence (threat, attack) and active avoidance (flight, hiding, escape) and passive reactions (immobility, urination, defecation). During challenging situations, it can happen that both active and passive reactions are observed. Other types of behavioural patterns such as postures, facial expressions, calls and emission of pheromones can also be considered as indicating fear (Forkman et al., 2007). Fear is regarded as one of the main psychological determinant factors of cattle temperament, however, it is an emotion thus fleeting, whereas fearfulness is a reflection of the personality of an animal. Therefore, the degree of fearfulness is taken as the major criterion for the assessment of temperament in cattle (Houpt, 2005). Fear seems to be the most important factor influencing the quality of the human–animal relationship (HAR). In order to measure the quality of HAR several tests to assess fear responses or reactivity of cattle, pigs, sheep, poultry and horses have been designed and used (e.g. open field arenas/novel arena tests, novel object tests, forced and voluntary approach tests, restraint tests) (Grignard et al., 2001; Waiblinger et al., 2006; Forkman et al., 2007; Windschnurer et al., 2008, 2009). However, there is a lack of studies investigating the validity of the measures used to assess fear in cattle. Studies have been conducted on dairy cows but little data are available for beef cattle (Munksgaard et al., 2001; Welp et al., 2004; Mazurek et al., 2011a, 2011b). The main problem encountered is that fear responses are very complex mechanisms and fear cannot be measured per se but only evaluated using indicators related to fear

3

reactions (Boissy et al., 2005). The second problem is that the environment has a large influence on the reactions of cattle. Most of the studies present procedures that can detect differences from one to another and it is a necessary to have more standardized procedures when trying to assess fearfulness of animals (Forkman et al., 2007). Nowadays, there is still a debate among scientists to understand fear, thus the validity of the behavioural and endocrine reactions are under scrutiny. It is therefore important to understand how cattle perceive their environment and their care taker(s). Most of the tests used for cattle (except the ones implicating exposure to humans) were originally designed for laboratory animals and most commonly for rodents (Moberg and Mench, 2000). They were then used for applied ethology but generally without taking the biological significance of farm animals into account (Forkman et al., 2007). Since laboratory species and domestic species live in different environments and placing a rat in an open-field test is very different from its usual environment, whereas cows that are kept in pens or paddocks are already living in an open-field type environment. The motivations of the animals will also change depending on the species (Moberg and Mench, 2000). It is thus important to study animals in their own environment. Since fear responses are very complex it is not possible to measure precisely fear and fear responses. Behavioural and endocrine responses can only be seen as indicators of fear but are not measuring it directly (Boissy, 1998). The validation of the fear responses of cattle should then be investigated by trying to find correlations between the responses using different tests. Another concern is that environmental conditions varies between studies, thus using these tests under different conditions makes interpretation difficult. Kilgour et al. (2006) conducted a study involving several fear tests (11 tests) and observed that the most discriminating responses were the general agitation of the animals and the avoidance of humans. Consequently, the restraint tests, the open-field tests, the fear of humans tests and flight distance were the most appropriate to assess individual responses in cattle. Waiblinger et al. (2006) also showed that forced approach tests would be better to assess the HAR than voluntary approach tests. The forced approach induced more active responses than the voluntary approach and induced more passive responses or no responses could be seen. 2.3. Assessment of cattle temperament for breeding purposes For breeding purposes the assessment of dairy cow temperament generally includes milking behaviour (milking temperament). Different scoring scales are used for this purpose: for example, a scale of 1 to 3 in the Czech Republic, Norway and Poland; a scale of 1 to 5 in Germany, France, Finland and Canada; a scale of 1 to 9 in The Netherlands, Denmark and Sweden. As a rule, the temperament of dairy cattle (first-calf heifers) is assessed directly by the breeder. In countries such as Denmark, Sweden and Finland, the assessment is made every time by the advisor/ classifiers when classification is done or by AI technicians

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K. Adamczyk et al. / Livestock Science 154 (2013) 1–12

when the cow is inseminated for the first time after first calving. Extreme scores are assigned to very calm and slow animals and those that are very nervous and excitable. In some countries (e.g. Canada, Germany, The Netherlands) this assessment is combined with the assessment of milking speed while in other countries temperament is regarded as the general excitability of animals (PFCBDF, 2008; Interbull, 2009; Fogh et al., 2011). The assessment of temperament in beef cattle is most often subjective (based on behavioural observations of animals in their new environment), although more objective methods such as measurement of flight distance, chute exit speed and avoidance distance are also used (Burrow, 1997; Smith et al., 2007; Benhajali et al., 2009; Mazurek et al., 2011a, 2011b). 2.4. Objectivity of methods for the assessment of cattle behaviour For knowledge on cattle behaviour to be used in their husbandry and breeding, it is necessary to assess individual behavioural characteristics using objective measures. Studies reported in the literature show some possibilities in this area. For example, Lanier and Grandin (2002) reported that cannon bone thickness and width in steers differed significantly depending on their temperament. An objective measure of temperament is facial hair whorl position in relation to the eye level of bulls (Randle, 1998; Lanier et al., 2001) or eye white percentage (Core et al., 2009). Relationship between temperament and bulls facial hair whorl position could possibly be attributed to the fact that during embryonic development, skin, its products and the nervous system arise from the same germ layer, or ectoderm (Fletcher and Weber, 2010). Therefore the mentioned traits could serve as precise indicators of cattle temperament and/or perhaps even other behavioural traits. Also, it is expected that in the future, objective methods of temperament assessment will be applied in practice using the latest technical solutions (Huhtala et al., ¨ 2007; Kwong et al., 2009). For example, Konig et al. (2006) suggested that frequency of voluntary entry of dairy cows into an automatic milking system could be used to estimate breeding value for animal temperament. Whereas, Pastell et al. (2006) concluded that measuring the load on each leg of a cow can be used to assess its milking behaviour, including milking temperament. Perhaps this method could be adapted to assess the behaviour of young heifers and bulls. In case of beef cattle, two types of methods for electronic measurement of animal behaviour appear to be practically useful—the assessment of animal reactivity in the mobile cage/chute and the assessment of speed flight (measurement of exit time). These applications indicate that traditional subjective scoring techniques can be replaced with more repeatable objective measures for example, when temperaments are assessed for performance studies (Maffei et al., 2006; Maffei, 2009; Sebastian et al., 2011; Schwartzkopf-Genswein et al., 2012). Technological advances of the last decade have provided tools to develop systems for real-time assessment of cattle

behaviour. For this purpose, use is made of knowledge concerning applied ethology, animal psychology or chronobiology, which examines periodic biological phenomena in animals under different environmental conditions (Balzer et al., 2009). At the same time, current knowledge and technological solutions ‘‘work’’ together. Today, cattle behaviour can be studied using the Global Positioning System (GPS) and the Geographic Information System (GIS) in open spaces (e.g. pastures), or using tracking and monitoring systems (x-, y-, z-positioning in 3D and 2D space) in barns. In many cases, these systems are still being improved and adapted for use in research and breeding practice. One of the major limitations to the use of these systems on a wide scale has been the cost of purchase and installation (Turner et al., 2000; Neisen, 2005; Gygax et al., 2006; Swain et al., 2010; Helmreich et al., 2011). It is believed that in the future, the methods reported above could serve to assess temperament and other behavioural traits in cattle of different ages maintained under different conditions, while minimising the effect of anthropomorphic interpretations of animal behaviour and taking into account the importance of positive/negative states experienced by animals during their lives. 3. Population genetics and behavioural traits of cattle 3.1. Variation in behavioural traits Cattle behavioural traits are characterised by considerably high individual variation, despite the fact that for example, cows, being gregarious by nature, perform many activities during the same time, using similar patterns of behaviour. This variation increases as animals are allowed to freely demonstrate their behaviours (e.g. in pasture and loose-housing systems) and concerns especially those behavioural traits that did not play a key role in cattle domestication and breeding. When studying the behavioural responses of dairy cows to weaning of calves, Hopster et al. (1995) found no clear similarities in the behaviour of multiparous cows. The authors analysed physiological and behavioural parameters such as plasma cortisol levels before and after separation, heart rate, continuity of food intake and vocalisations. Meanwhile, Cooper et al. (2008) observed high variation in cows’ behaviour associated with feeding behaviour, lying, and order of entry into the milking parlour. Adamczyk et al. (2011) reported high individual variation (V) in daily physical activity (V ¼37–78%) of Holstein–Friesian cows within particular technological/treatment groups raised under welfare conditions in a free-stall barn. During the study period, no animal diseases and no occurrence of oestrus were observed, and no additional procedures (e.g. artificial insemination, pregnancy checks) were performed. Barrozo et al. (2011) also found high variation in temperament of Nellore cattle (V ¼41.15%) using fourpoint scale. Similarly Cafe et al. (2011) assessed the temperament of young Brahman and Angus cattle based on measurements of flight speed (FS) and crush score (CS), found that despite using tests with different degrees of scoring objectivity, animals of both breeds were characterised by equally high individual variation, as evidenced

K. Adamczyk et al. / Livestock Science 154 (2013) 1–12

by the variation coefficients of 33–49% (FS for Brahman), 25–42% (FS for Angus), 26–43% (CS for Brahman) and 30– 40% (CS for Angus). 3.2. Heritability of behavioural traits in cattle and their genetic correlations with production traits It is generally accepted that cattle behavioural traits are inherited as quantitative traits influenced by additive gene effects. They are much less frequently associated with single gene effect as exemplified by the relationship between excitability and the muscle hypertrophy gene in beef cattle (Holmes et al., 1972; Holmes et al., 1973; Newman, 1994; Phillips, 2002). Of all behavioural traits in cattle, temperament has received the most attention. Burrow (1997) showed that the coefficients of heritability for temperament, estimated within similar production systems and using the same assessment method, varied considerably (h2 ¼0.00–0.67) according to the age of animals and their genotype.

5

Relatively the smallest differences (h2 ¼0.32–0.70) were noted when temperament was assessed by measuring flight speed. Likewise, Schutz and Pajor (2001) demonstrated high variation in the coefficients of heritability for dairy cow temperament (h2 ¼0.00–0.52). Visscher and Goddard (1995) and Lassen and Mark (2008) estimated this parameter to be 0.18–0.22 in Holstein–Friesian cattle and 0.25 in the Jersey breed. Meanwhile, the coefficients of heritability for beef cattle temperament ranged from 0.00 to 0.61 (Gauly et al., 2001) and from 0.11 to 0.31 (Benhajali et al., 2010) (Table 1). Robinson and Oddy (2004) showed relatively high coefficients of heritability for feeding behaviour in feedlot finished B. taurus and Bos indicus crossbreds (h2 ¼0.36 for time spent eating, h2 ¼ 0.44 for number of eating sessions, h2 ¼0.51 for eating rate). The other behavioural traits in cattle such as social behaviour or reproductive behaviour generally have medium or low heritability (Schutz and Pajor, 2001; Boissy et al., 2005; Løvendahl and Chagunda, 2009; Berry and McCarthy, 2012).

Table 1 Heritability of cattle temperament (data for the last 30 years). h2 7 s.e.

No. animals

No. sires

Type of cattle

Age

Model used

References

0.227 0.03 0.257 0.06 0.00–0.19 70.05–0.12

14,596 4695 259

334 125 –n

24.5mo 24.4mo 238d

Multivariate REML with sire model Multivariate REML

Visscher and Goddard (1995) Gauly et al. (2001)

TRc

0.00–0.61 70.05–0.24

259

TSb TRc Tmultid

0.00–0.38 70.05–0.26 0.00–0.59 70.05–0.21 0.08–0.35 7 

206 206 5313

Holstein cows Jersey cows German Angus calves German Angus calves Simmental calves Simmental calves Bullfighting cattle

Multivariate REML

Silva et al. (2002)

MTe

0.187 0.04

30,190

(AI)–REML

0.177 0.07 0.317 0.09

1032 1142

54 51

Lassen and Mark (2008) Prayaga et al. (2009)

0.147 0.08 0.117 0.07 0.227 0.08 0.207 0.08 0.317 0.10 0.287 0.09 0.177 0.07 0.197 0.07

1113 1113 1113 1113 1271 1271 1271 1271

73 73 73 73 65 65 65 65

Items T5 TS

TF

a

b

f

TNMWg TRMWh TNMHi TRMHj TNMWg TRMWh TNMHi TRMHj a

– – – 230

–

Danish Holstein cows Brahman heifers Tropical composite heifers Limousin calves Limousin calves Limousin calves Limousin calves Limousin calves Limousin calves Limousin calves Limousin calves

(average for both breeds) 2-year-old females, 3-4year-old males 579-1,379d 300d 300d

REML

80-179d 80-179d 80-179d 80-179d 180-280d 180-280d 180-280d 180-280d

(AI)-REML

Benhajali et al. (2010)

Temperament scoring: five-point scale (1—good temperament, 5—bad temperament). Temperament scoring during separation tests based on the following traits: total separation times, signs of aggression, separation success and vocalisation. c Temperament scoring related to restraint tests on the following traits: Before handling period (60 s): time spent running before and during handling in the restraint yard and time spent running in the restraint yard; During handling period (180 s): time until animal reached the corner, number of times the animal tried to escape during the test, signs of aggression, time spent in the corner, stroking the animal for a maximum period of 30 s at the back, defecation and/or urination, vocalisation; Five-point scale (1– calm, 5– very excited). d Temperament scored based concurrently on the following traits: aggressiveness, ferocity, fixedness, involvement, mobility, enters in a gallop, falling, homing instinct, development, distance, hiding of the face, straightforwardness, rhythm, nobility e Milking temperament scoring: nine-point scale (36% herds in tie stalls, 64% herds in free stall). f Temperament scored based on flight time (sec.  102). g Total number of movements during weighing. h Number of rush movements during weighing. i Total number of movements during exposure to the human. j Number of rush movements during exposure to the human. n no data available. b

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K. Adamczyk et al. / Livestock Science 154 (2013) 1–12

Research shows that cow temperament is a behavioural trait most correlated to dairy performance, in particular milk yield and milking speed (rg ¼ 0.11–  0.40 and 0.36–0.57, respectively) (Foster et al., 1988; Lawstuen et al., 1988; Erf et al., 1992; Visscher and Goddard, 1995). In a population of Canadian dairy cattle (Holstein–Friesian, Jersey and Ayrshire), Sewalem et al. (2010) reported that longevity decreases with increasing nervousness. This is mainly due to the systematic selection of bulls (since 2001) for milking temperament using the Lifetime Profit Index and giving preference to calm animals during mating. Feeding behaviour and temperament are mostly correlated with meat performance traits. Robinson and Oddy (2004) found high genetic correlations between the following traits assessed in beef cattle crosses: time spent eating and feed conversion ratio (rg ¼0.78), eating rate and feed conversion ratio (rg ¼  0.83), eating rate and weight gains (rg ¼0.53), number of eating sessions and feed conversion ratio (rg ¼0.49). Nkrumah et al. (2007) noted slightly lower correlations between the temperament of beef cattle sired by Angus, Charolais, or Hybrid bulls and traits such as carcass weight (rg ¼  0.54), carcass meat percentage (rg ¼0.33) or average daily gain (rg ¼ 0.25). Phocas et al. (2006) demonstrated relatively high genetic correlations between docility and fertility in Limousin heifers (rg ¼0.55). 3.3. Breeding for behavioural traits in cattle Among cattle behavioural traits, most attention is given by breeders to temperament. Long-term culling of aggressive animals caused a marked increase in the

proportion of cattle with a calm temperament. This concerns both dairy and beef cattle populations. For example, the results of the evaluation of dairy cattle population in Canada indicated that temperament of more than 90% milk-recorded cows can be described as an average, calm and very calm (Interbull, 2010). Also, in Canadian Limousine cattle a noticeable genetic improvement of docility was observed—from about 1.00 EPD in 1985 to above 14.00 EPD in 2006 (CLA, 2007). Similarly good results are achieved when selecting cattle with more aggressive traits. An example of empirical selection for aggressiveness in bullfighting cattle was given by Silva et al. (2002), who found a distinct increase of mean breeding value for this trait in 1980–99. Breeding value for temperament of dairy breed bulls, based on daughters, has been estimated internationally since 2009. This was pioneered by Canada, Germany, The Netherlands, Switzerland and Scandinavia for the Holstein–Friesian; by Canada, The Netherlands and Scandinavia for Red cattle; and by Canada, The Netherlands and Scandinavia for the Jersey. The first data for 2009 showed a high consistency of results across some countries. For example, in Scandinavian countries it was 79– 96% (Red breeds) and 83–91% (Holstein–Friesian). The highest breeding value (BV) for temperament of Holstein– Friesian bulls was estimated in Canada (BV ¼104.2) and Finland (BV ¼103.2), and the lowest in the Netherlands (BV ¼98.6). In the case of Red cattle the highest and the lowest scores were given to Danish (BV ¼107.5) and Canadian (BV ¼95.1) bulls, respectively (Fogh et al., 2009). Among the countries reported above, special mention should be given to breeding work on dairy cattle temperament in Denmark. This trait is evaluated in

Table 2 Coefficients of correlation between breeding values for temperament of dairy breed bulls used in different countries (adapted from Bagnato et al., 2007). Countrya

AUS

CAN

CHE

DEA

DFS

GBR

JPN

NLD

NZL

AUS

1.00

–n

–

–

–

0.64d  0.09e 0.15d – 0.60d – 0.72d 0.73e 0.65d – 0.68d – 0.72d 0.97e 0.76d 0.83e

–

–

–

–

0.99f

–

– 0.67c – 0.94c –

–

CAN

 0.05b 0.72c 1.00

–

–

–

0.33b 0.77c 0.92b 0.58c –

1.00

–

–

–

–

–

0.89d – 0.73d – 0.81d – 0.88d – 0.58d –

1.00

–

–

–

0.82d – 0.85d – 0.89d 0.53e 0.65d 0.47e

1.00

–

–

– 0.51c –

1.00

–

–

0.79d – 0.59d –

1.00

–

0.74d 0.87e

1.00

CHE DEU DFS GBR JPN NLD NZL

0.03d – 0.97d – 0.87d 0.62e 0.65d – 0.79d – 0.88d  0.34e 0.57d  0.24e

1.00 d

0.20 – 0.15d – 0.46d – 0.34d – 0.21d – 0.22d –

d

0.75 – 0.73d – 0.52d –

a Abbreviation for country name: AUS–Australia, CAN–Canada; CHE–Switzerland; DEA–Germany and Austria; DFS–Denmark, Finland and Sweden; GBR–United Kingdom and Ireland; ITA–Italy; JPN–Japan; NLD–The Netherlands and Flanders; NZL–New Zealand. Abbreviations for breed types. b Guernsey. c Red Dairy Cattle. d Holstein–Friesian. e Jersey. f Brown Swiss. n no data available.

K. Adamczyk et al. / Livestock Science 154 (2013) 1–12

primiparous cows of all milk-recorded dairy breeds (Holstein-Friesian, Jersey, Danish Red). According to Interbull data, heritability of temperament in Danish dairy cattle is 0.05 for Danish Jersey, 0.13 for Red Holstein and Danish Holstein, and 0.20 for Danish Red. By analogy with the coefficients of heritability, the weights for cow temperament in the Danish selection index Nordic Total Merit (NTM) are 0.02 (Danish Jersey), 0.03 (Red Holstein), 0.04 (Danish Holstein), and 0.10 (Danish Red). It is notable that the NTM index is also used in Sweden and Finland, which facilitates comparison of animal breeding value among these countries (Interbull, 2003; Fogh et al., 2011). The diversity of methods for assessment of dairy cattle temperament makes it difficult to compare the breeding value of bulls from different countries. This was pointed out by Bagnato et al. (2007), who calculated correlations between breeding values for dairy breed bulls, estimated using the Multiple Across Country Evaluation method. These authors reported the following values of correlation coefficients according to country of origin of the bulls: 0.05–0.92 for Guernsey;  0.34–0.97 for Jersey; 0.03– 0.89 for Holstein–Friesian; 0.51–0.94 for Red Dairy Cattle and 0.99 for Brown Swiss (Table 2). 4. Molecular genetics and behavioural traits in cattle 4.1. Quantitative trait loci affecting behavioural traits in cattle To date, 6305 QTLs for 416 different cattle traits have been mapped (Hu et al., 2007; AnimalQTLdb, 2013). In comparison, the search for QTLs affecting behavioural traits has been much less successful. So far most studies in this area were conducted with other species of animals, mainly mice (Willis-Owen and Flint, 2006), in farmed animals, including poultry (Buitenhuis et al., 2005) and pigs (Reiner et al., 2009). Among the research results published on the identification of QTLs for behavioural traits in cattle, special consideration should be given to the studies by Fisher et al. (2001), Schmutz et al. (2001), Hiendleder et al. (2003), Wegenhoft (2005), Boldt (2008) and Gutierrez-Gil et al. (2008). This topic was also addressed by authors investigating the genetic determinants of production traits in dairy cattle and their milking temperament (Spelman et al., 1999; Schrooten et al., 2000; Hiendleder et al., 2003). Of the behavioural traits in cattle, researchers generally focused on temperament and capacity for habituation. To date, approximately 44 QTLs located on most chromosomes except numbers 2, 13, 17, 22, 23, 24 and 27 were identified for these traits (Table 3). Most QTLs for the traits mentioned above were mapped on chromosomes 1, 4, 9, 16, 19 and 29. This significant dispersion of bovine genome regions that determine the behaviour of animals may be largely due to using different research methods within a given trait. Preliminary genome scanning results also indicate the need for increasing the density of genetic markers to improve the applicability of studies aimed at finding candidate genes for cattle behaviour traits in the future.

7

4.2. Candidate genes for behavioural traits in cattle The construction of genetic maps for different species of farm animals and efforts to improve their welfare in different production systems has increased the number of studies on the genetic background of animal behaviour. Identification of the molecular mechanisms of behaviour may contribute to a better understanding of behavioural problems widespread in many fields of livestock production, such as animal handling, susceptibility to stress, or adaptability to different production conditions (Morme de, 2005; Jensen et al., 2008). It is supposed that the identification of QTLs for behavioural traits in cattle makes it possible to determine candidate genes located near genetic markers that have the largest influence on a given trait. However, this procedure is not sufficiently effective due to the high complexity of the expression of individual animal behaviours and their interaction with the environment (Schmutz et al., 2001; Gutierrez-Gil et al., 2008). To date, only several published studies determined genes that may affect cattle temperament, feeding behaviour and reproductive behaviour. These studies concern the location and polymorphism of genes related to regulation of the stress hormone, neuropeptide and neurotransmitter levels. For example, Boldt (2008) found no relationship between cattle temperament and four genes, bone morphogenetic protein 1 (BMP1), bridging integrator 3 (BIN3), farnesyl-diphosphate-farnesyltransferase 1 (FDFT1) and cathepsin B (CTSB), localised on bovine chromosome 8 close to QTL associated with temperament understood as disposition, this QTL being previously identified by Wegenhoft (2005). Studies in humans, mice and monkeys revealed a relationship between genetic variants of the neurotransmitter monoamine oxidase (MAOA) and the level of individual aggression (Brunner et al., 1993; Popova ¨ et al., 2001; Karere et al., 2009), whereas Luhken et al. (2010) found no significant relationships between MAOA gene polymorphism and behavioural traits in beef breeds of cattle. Moreover, Glenske et al. (2011) reported a low relationship between the dopamine receptor D4 (DRD4) gene located near QTL for behavioural traits on chromosome 29, and temperament of German Angus cattle. A study using the expression of the leucocyte heat shock protein (Hsp) gene for early detection of the subclinical signs of bovine respiratory disease complex (BRD) confirmed that this gene is associated with stress response of animals (Eitam et al., 2010). Preliminary results of a study (Alam et al., 2012) on the polymorphism of bovine neuropeptide Y5 receptor gene (NPY5R) suggest that it potentially modifies the action of neuropeptide Y by modulating its effect, and thus may play an important role in the regulation of appetite and feeding behaviour in beef cattle. Similar results of research on using the polymorphism of the melanocortin 4 receptor gene (MC4R) as a genetic marker of economic traits in Korean Hanwoo cattle suggest its possible effect on feed intake capacity and feeding behaviour in cattle (Seong et al., 2011). A study aimed at determining genes that affect reproductive behaviour in cows showed a significant

8

Table 3 Quantitative trait loci for temperamenta and habituation abilityb of cattle. Traitc

Trait-associated marker

Chromosome position (cM)

Genotype

Literature

1

habituationþtemperament temperament habituation

BMS574 DIK70-PIT17B7 BM6438 BMS4044

15,42 37 1,78 141

beef breed cattle from ET Bos taurus (Angus)  Bos indicus (Brahman, Nellore) Charolais  Holstein–Friesian

Schmutz et al. (2001) Wegenhoft (2005) Gutierrez-Gil et al. (2008)

3

temperament

BM7225-ILSTS64

45

Bos taurus (Angus)  Bos indicus (Brahman, Nellore)

Boldt (2008)

4

temperament habituation

TEXAN17-MAF50 MAF50-DIK026

28–51 51,21–86,23

Bos taurus (Angus)  Bos indicus (Brahman, Nellore) Charolais  Holstein–Friesian

Wegenhoft (2005) Gutierrez-Gil et al. (2008)

5

habituationþtemperament

RM103

29,42

beef breed cattle from ET

Schmutz et al. (2001)

6

habituation temperament

DIK5076-BM1329 CSSM22-CSM34

4,51–35,39 1

Charolais  Holstein–Friesian Bos taurus (Angus)  Bos indicus (Brahman, Nellore)

Gutierrez-Gil et al. (2008) Boldt (2008)

7

habituation

RM006-BM1853

25,39–85,32

Charolais  Holstein–Friesian

Gutierrez-Gil et al. (2008)

8

temperament habituation

BMS1864-BM3419 CSSM047

0 115,2

Bos taurus (Angus)  Bos indicus (Brahman, Nellore) Charolais  Holstein–Friesian

Wegenhoft (2005) Gutierrez-Gil et al. (2008)

9

habituationþtemperament temperament temperament habituation

ILSTS013 BM6436-BM4208 BM2504-UWCA9 BM888-CSRM60

48,73 72 30,92–49,99 59,98–77,81

beef breed cattle from ET Bos taurus (Angus)  Bos indicus (Brahman, Nellore) Charolais  Holstein–Friesian

Schmutz et al. (2001) Wegenhoft (2005) Gutierrez-Gil et al. (2008)

10

habituation

BMS528-TGLA378

24,01–43,65

Charolais  Holstein–Friesian

Gutierrez-Gil et al. (2008)

11

habituationþtemperament habituation

LISTS036 ILSTS100-IDVGA-3

61,57 59,11–81,8

beef breed cattle from ET Charolais  Holstein–Friesian

Schmutz et al. (2001) Gutierrez-Gil et al. (2008)

12

temperament

BMS2252-RM094

20 I 22

Bos taurus (Angus)  Bos indicus (Brahman, Nellore)

Boldt (2008)

14

habituationþtemperament

RM180-ILSTS008

33,31–50,91

beef breed cattle from ET

Schmutz et al. (2001)

15

habituationþtemperament

ADCY2

22,67

beef breed cattle from ET

Schmutz et al. (2001)

16

temperament temperament temperament

INRA013-BMS462 INRA48-BM3509 HUJ625 ETH11-BM719 BM121

79 70 100.2 54.07–77.57 26.4

Bos taurus (Angus)  Bos indicus (Brahman, Nellore) Bos taurus (Angus)  Bos indicus (Brahman, Nellore) Charolais  Holstein–Friesian

Wegenhoft (2005) Boldt (2008) Gutierrez-Gil et al. (2008)

18

temperament

BL1016-BM8151 IDVGA-31-ABS013

18 0–15.75

Bos taurus (Angus)  Bos indicus (Brahman, Nellore) Charolais  Holstein–Friesian

Wegenhoft (2005) Gutierrez-Gil et al. (2008)

19

temperament habituation

CSSM065–ETH3 BMS2142-CSSM065

69.83–90.04 43.31–69.83

Charolais  Holstein–Friesian

Gutierrez-Gil et al. (2008)

20

temperament

DIK015-BM5004

52.49–71.80

Charolais  Holstein–Friesian

Gutierrez-Gil et al. (2008)

21

habituation

HEL10-TGLA337

65

Charolais  Holstein–Friesian

Gutierrez-Gil et al. (2008)

25

temperament

BM737-INRA222

31.59–53.37

Charolais  Holstein–Friesian

Gutierrez-Gil et al. (2008)

26

temperament

ABS012-HEL11 IDVGA59-HEL11

9.9 33

Charolais  Holstein–Friesian Bos taurus (Angus)  Bos indicus (Brahman, Nellore)

Gutierrez-Gil et al. (2008) Boldt (2008)

habituation

K. Adamczyk et al. / Livestock Science 154 (2013) 1–12

BTA chromosome

Gutierrez-Gil et al. (2008) Charolais  Holstein–Friesian habituation

Temperament was measured once by the degree of animal nervousness in changed/new environmental conditions for the animal, with the assessed animal being most often separated. Habituation was defined by the authors as adaptability of animals to novel environmental conditions in a given time period. Temperament and habituation were assessed by the following methods: separation test during weighing according to the method of Stookey et al. (1994) (in: Schmutz et al., 2001), assessment on a 5-point scale (1-calm animal, 5-animal defined as ‘‘crazy’’) during blood collection and on a 9-point scale (1-non-aggressive animal, 9-extremely aggressive animal) based on disposition assessment accounting for the following behaviours: aggressiveness, nervousness, flightiness, gregariousness (in: Wegenhoft, 2005; Boldt, 2008), assessment of milking temperament on a 9-point scale made by breeder (in: Hiendleder et al., 2003), assessment of animal fearfulness (flight from feeder) on a 6-point scale and separation test according to the methods of Martin and Bateson (1993) and Ball (2004) (in: Gutierrez-Gil et al., 2008). c

b

a

Hiendleder et al. (2003) Boldt (2008) Holstein–Friesian cows Bos taurus (Angus)  Bos indicus (Brahman, Nellore)

11.29–21.11 40.16–69.73 21 24.48–33.51 temperament 29

BMS764-BMC8012 DIK094-MNB101 BMC3224-BMS764 RM044-MNB166

Gutierrez-Gil et al. (2008) 10.89 temperament 28

BP23

Charolais  Holstein–Friesian

K. Adamczyk et al. / Livestock Science 154 (2013) 1–12

9

relationship between the expression genes in the ventral tegmental area and the intensity of oestrus expression by high-yielding Holstein–Friesian cows (Wyszyn´ska-Koko et al., 2011). Furthermore, Kommadath et al. (2011) demonstrated a significant effect of the expression of several brain neurotransmitter and neurotransmitter receptor genes (OXT, AVP, POMC, MCHR1) on oestrous behaviour of dairy cows such as socio-sexual anxiety, stress and feeding motivation. It follows from the studies cited above that no candidate genes with a substantial effect on cattle behavioural traits have been identified to date, regardless of the breed and the environment that modulates them. One of the reasons for this could be the complexity of cattle behaviour and lack of phenotypic data used to characterise the behavioural traits. 5. Conclusions Identification of cattle behaviour is necessary for efficient production of milk and beef under welfarefriendly conditions. Unfortunately, our understanding of the neurohormonal and genetic determinants of cattle behaviour warrants further investigation. Because these traits are essential for cattle breeding, they have been increasingly incorporated in breeding programs in recent years. It appears that because behavioural traits still show considerable variation and correlate favourably to production traits, the prospects for their improvement are promising with regard to both population genetics and molecular genetics. However, for behavioural genetic studies to achieve applied use, it is necessary to provide unambiguous phenotypic definitions of individual behavioural traits of cattle and to use objective methods for their assessments in order to compare breeding values in production systems within and between countries. Conflict of interest There is no conflict of interest in this manuscript. References Adamczyk, K., Gil, Z., Felenczak, A., Skrzyn´ski, G., Zapletal, P., Choroszy, Z., 2011. Relationship between milk yield of cows and their 24-hour walking activity. Anim. Sci. Pap. Rep, 29, 185–195. Alam, T., Bahar, B., Waters, S.M., McGee, M., Sweeney, T., 2012. Analysis of multiple polymorphisms in the bovine neuropeptide Y5 receptor gene and structural modelling of the encoded protein. Mol. Biol. Rep. 39, 4411–4421. Albright, J.L., Arave, C.W., 1997. The Behaviour of Cattle. CAB International, Walingford. AnimalQTLdb, 2013. Cattle QTL. Available from: /http://animalge nome.org/QTLdbS (accessed 14.01.13). Bagnato, A., Rossoni, A., Nicoletti, C., Jakobsen, J., Santus, E., 2007. Milkability and temperament MACE correlation and pilot study in dairy cattle populations. In. Proceedings of the Interbull Meeting Dublin, Bulletin 37, pp. 95–97. Ball, N., 2004. Temperament traits in cattle: Measurement and preliminary genetic analysis, PhD thesis. The University of Edinburgh, 80–86. ¨ Balzer, H.-U., Kultus, K., Kohler, S., 2009. A new generation of fertility monitoring in cattle herds. In: Proceedings of the Joint International Agricultural Conference in Wageningen, pp. 225–234. Barrozo, D., Buzanskas, M.E., Oliveira, J.A., Munari, D.P., Neves, H.H.R., Queiroz, S.A., 2011. Genetic parameters and environmental effects

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