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 University of Agriculture in Krakow, Department of Cattle Breeding, 30-059 Krako ´w, Al. Mickiewicza 24/28, Poland b Animal and Bioscience Research Department, Animal & Grassland Research and Innovation Centre, Teagasc, Grange, Dunsany, Co. Meath, Ireland article info Article history: Received 11 July 2012 Received in revised form 18 January 2013 Accepted 29 January 2013 Keywords: Cattle Genetics Behavioural traits Breeding programme abstract 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. Contents 1. Introduction ........................................................................................... 2 2. The main problems in the evaluation of cattle behaviour ....................................................... 2 2.1. Definition of behavioural traits ...................................................................... 2 2.2. A fear as a basic criterion in cattle temperament assessment .............................................. 3 2.3. Assessment of cattle temperament for breeding purposes ................................................. 3 2.4. Objectivity of methods for the assessment of cattle behaviour ............................................. 4 3. Population genetics and behavioural traits of cattle ........................................................... 4 3.1. Variation in behavioural traits....................................................................... 4 3.2. Heritability of behavioural traits in cattle and their genetic correlations with production traits................... 5 3.3. Breeding for behavioural traits in cattle ............................................................... 6 4. Molecular genetics and behavioural traits in cattle ............................................................ 7 4.1. Quantitative trait loci affecting behavioural traits in cattle ................................................ 7 4.2. Candidate genes for behavioural traits in cattle ......................................................... 7 Contents lists available at SciVerse ScienceDirect journal homepage: www.elsevier.com/locate/livsci Livestock Science 1871-1413/$ - see front matter & 2013 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.livsci.2013.01.016 n Corresponding author. Tel./fax: þ48 12 6624162. E-mail address: [email protected] (K. Adamczyk). Livestock Science 154 (2013) 1–12
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Contents lists available at SciVerse ScienceDirect
Livestock Science
Livestock Science 154 (2013) 1–12
1871-14
http://d
n Corr
E-m
journal homepage: www.elsevier.com/locate/livsci
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 University of Agriculture in Krakow, Department of Cattle Breeding, 30-059 Krakow, Al. Mickiewicza 24/28, Polandb Animal and Bioscience Research Department, Animal & Grassland Research and Innovation Centre, Teagasc, Grange, Dunsany,
primigenius. People kept cattle for easy access to food,including milk, blood, and meat, and for use as load-bearers and as work animals (e.g. ploughing). Bos taurus
cattle were domesticated approximately 8000 years ago(Hirst, 2009). Cattle use their senses to communicate, thustheir behaviour will largely depend on their perception.Most forms of communication are related to the impor-tant sensory perceptions, for example, vision, sound,smell and touch. The means of communication will havean important impact on the group structure and cohesion(Albright and Arave, 1997; Phillips, 2002). Cattle beha-viour is a means of communication between animals andtheir environment, enabling them to satisfy the needsnecessary for survival of the species under differentenvironmental conditions (Phillips, 2002; Fraser andBroom, 1997; Broom and Fraser, 2007). The way ananimal will react will most of the time directly dependson its senses, sensory-related behaviour or its sensoryenvironment. Cattle possess the same senses as othermammals: vision, olfaction, hearing, touch and taste. Themost important behavioural traits without which animaldomestication and breeding would be impossible include:the capacity for a gradual reduction of fearfulness towardshumans; the ability to become gradually subordinate tohumans as a dominant individual, the ability to learndesired responses and behaviours, the capacity to breedand to rear offspring under human-created conditions;and the capacity to accept feed provided by humans(Keeling and Gonyou, 2001; Jezierski, 2004). Since thebehavioural traits of cattle affect their longevity, breedersregard them as workability traits (Boettcher, 2005; Foghet al., 2009).
Thus the process of cattle domestication and theirgenetic improvement depend on the flexibility of beha-vioural traits of animals, which have to adapt to theconditions created by humans (Mignon-Grasteau et al.,2005). These traits play an important role in human–animal–environment relationships, which is particularlynoticeable in intensified milk and beef production, when
behavioural disorders (e.g. lameness, bar-biting, tongue-rolling, excessive licking and grooming or the buller steersyndrome) in cattle are especially frequent (Grandin and
Deesing, 1998; Phillips, 2002; Broucek et al., 2008).Selection towards single purpose breeds induced beha-
vioural 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 withtheir human-created environment and enables breeders,while respecting the behavioural needs of animals, toobtain higher quantity and/or better quality products fromthem (Price, 2003; Gruber et al., 2010; Sheahan et al., 2011).
Behavioural traits are therefore helpful in assessing cattlewelfare and thus in determining the ethical limits to animalhandling by humans (Praks et al., 2007; D’Eath et al., 2009;Nicol, 2011).
The considerable role of cattle behaviour from theperspective of milk and beef production resulted inbehavioural traits being increasingly used in breedingprograms for individual breeds in many countries(Miglior, 2004), although these traits appear to be muchmore difficult to assess than production traits. This isstrictly dependent on the progress of knowledge on cattlebehaviour and its genetic and environmental determi-nants (Morm�ede, 2005).
Therefore, the aim of this paper was to review the keyproblems in efficient breeding for behavioural traits ofcattle, including their phenotypic evaluation, utilisation ofpopulation and of molecular genetics in the estimation ofgenetic parameters and breeding values. Additionally,examples of cattle selection for behavioural traits acrosscountries were reviewed and presented.
2. The main problems in the evaluation of cattlebehaviour
2.1. Definition of behavioural traits
Cattle behaviour is a function of the whole brain/bodyand the molecular pathways involved in genetic varia-bility (Herskin et al., 2004; Van Reenen et al., 2004;Morm�ede, 2005). The plasticity of cattle behaviour andthe learning capacities are well developed and are com-parable with that of other mammals such as rodents, catsand horses (Kilgour, 1981). Cattle learn by memorisinginformation received by their sensory organs. The infor-mation is analysed in the cerebral cortex and learning ismade by association, generalisation or discrimination ofthe stimuli (Albright and Arave, 1997).
Robust evaluation of behavioural traits is difficult dueto the problems with their definition and subjectivity ofmeasurement. This even applies to such a seemingly wellstudied trait as cattle temperament. For example, Hurniket al. (1995) hold that temperament is an animal’s generaltrait that includes behaviours such as level of physicalactivity, persistent habits, emotionality, alertness andcuriosity. According to the same authors, animal tempera-ment depends on the interaction between excitatory andinhibitory reactions. Meanwhile, Burrow (1997) regardedtemperament only as an animal’s behavioural response tohandling by humans. Likewise, Phillips (2002) definedthis term as an animal’s main personality or mood trait inrelation to humans. Sewalem et al. (2011) state thatmilking temperament is broadly defined as milking beha-viour, ease of handling or aggressiveness at feeding.
Depending on the definition of cattle temperamentdifferent methods of its assessment are used in researchand breeding work. Burrow (1997) classified several
K. Adamczyk et al. / Livestock Science 154 (2013) 1–12 3
dozen methods for assessment of cattle temperament intorestrained and non-restrained tests, dairy cow scoringsystem, dominance tests, free movement test and assess-ment of maternal temperament.
2.2. A fear as a basic criterion in cattle temperament
assessment
Temperament is the most important trait of an ani-mal’s personality since it determines their perception andresponse to different situations (Grandin et al., 1995). Thisresponse can be behavioural and/or psychological innature and can remain constant over time and in differentcontexts. The visible demonstration of cattle tempera-ment is reactivity (Grignard et al., 2001). Reactivity tohumans is mainly be influenced by the previous experi-ence of an animal towards humans and changes depend-ing on the context. In cattle it can be influenced by fearwhich is defined as a reaction to the perception of anactual danger that threatens the integrity of the indivi-dual. Fear is a powerful, emotional state that plays animportant role in avoiding potentially dangerous situa-tions (Boissy, 1995). An animal’s response to prepare andcope with danger may be assessed using physiologicaland behavioural measures (Forkman et al., 2007). Fearreactions are generally triggered by stimuli from theenvironment that may be associated with a previousnegative experience, for example novelty, noise or suddenmovements, aggressive handling (Jones, 1997). The maintypes of reactions that can be observed are: active reac-tions that can be active defence (threat, attack) and activeavoidance (flight, hiding, escape) and passive reactions(immobility, urination, defecation). During challengingsituations, it can happen that both active and passivereactions are observed. Other types of behavioural pat-terns such as postures, facial expressions, calls and emis-sion of pheromones can also be considered as indicatingfear (Forkman et al., 2007).
Fear is regarded as one of the main psychologicaldeterminant factors of cattle temperament, however, itis an emotion thus fleeting, whereas fearfulness is areflection of the personality of an animal. Therefore, thedegree of fearfulness is taken as the major criterion for theassessment of temperament in cattle (Houpt, 2005).
Fear seems to be the most important factor influencingthe quality of the human–animal relationship (HAR). Inorder to measure the quality of HAR several tests to assessfear responses or reactivity of cattle, pigs, sheep, poultryand horses have been designed and used (e.g. open fieldarenas/novel arena tests, novel object tests, forced andvoluntary 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 thevalidity of the measures used to assess fear in cattle.Studies have been conducted on dairy cows but little dataare available for beef cattle (Munksgaard et al., 2001;Welp et al., 2004; Mazurek et al., 2011a, 2011b). The mainproblem encountered is that fear responses are verycomplex mechanisms and fear cannot be measuredper se but only evaluated using indicators related to fear
reactions (Boissy et al., 2005). The second problem is thatthe environment has a large influence on the reactions ofcattle. Most of the studies present procedures that candetect differences from one to another and it is a neces-sary to have more standardized procedures when tryingto assess fearfulness of animals (Forkman et al., 2007).Nowadays, there is still a debate among scientists tounderstand fear, thus the validity of the behavioural andendocrine reactions are under scrutiny. It is thereforeimportant to understand how cattle perceive their envir-onment and their care taker(s).
Most of the tests used for cattle (except the onesimplicating exposure to humans) were originallydesigned for laboratory animals and most commonly forrodents (Moberg and Mench, 2000). They were then usedfor applied ethology but generally without taking thebiological significance of farm animals into account(Forkman et al., 2007). Since laboratory species anddomestic species live in different environments and pla-cing a rat in an open-field test is very different from itsusual environment, whereas cows that are kept in pens orpaddocks are already living in an open-field type environ-ment. The motivations of the animals will also changedepending on the species (Moberg and Mench, 2000). It isthus important to study animals in their own environ-ment. Since fear responses are very complex it is notpossible to measure precisely fear and fear responses.Behavioural and endocrine responses can only be seen asindicators of fear but are not measuring it directly (Boissy,1998). The validation of the fear responses of cattleshould then be investigated by trying to find correlationsbetween the responses using different tests. Anotherconcern is that environmental conditions varies betweenstudies, thus using these tests under different conditionsmakes interpretation difficult. Kilgour et al. (2006) con-ducted a study involving several fear tests (11 tests) andobserved that the most discriminating responses were thegeneral agitation of the animals and the avoidance ofhumans. Consequently, the restraint tests, the open-fieldtests, the fear of humans tests and flight distance were themost appropriate to assess individual responses in cattle.Waiblinger et al. (2006) also showed that forced approachtests would be better to assess the HAR than voluntaryapproach tests. The forced approach induced more activeresponses than the voluntary approach and induced morepassive responses or no responses could be seen.
2.3. Assessment of cattle temperament for breeding
purposes
For breeding purposes the assessment of dairy cowtemperament generally includes milking behaviour (milk-ing temperament). Different scoring scales are used for thispurpose: for example, a scale of 1 to 3 in the CzechRepublic, Norway and Poland; a scale of 1 to 5 in Germany,France, Finland and Canada; a scale of 1 to 9 in TheNetherlands, Denmark and Sweden. As a rule, the tempera-ment of dairy cattle (first-calf heifers) is assessed directlyby the breeder. In countries such as Denmark, Sweden andFinland, the assessment is made every time by the advisor/classifiers when classification is done or by AI technicians
K. Adamczyk et al. / Livestock Science 154 (2013) 1–124
when the cow is inseminated for the first time after firstcalving. Extreme scores are assigned to very calm and slowanimals and those that are very nervous and excitable. Insome countries (e.g. Canada, Germany, The Netherlands)this assessment is combined with the assessment ofmilking speed while in other countries temperament isregarded as the general excitability of animals (PFCBDF,2008; Interbull, 2009; Fogh et al., 2011).
The assessment of temperament in beef cattle is mostoften subjective (based on behavioural observations ofanimals in their new environment), although more objec-tive 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 theirhusbandry and breeding, it is necessary to assess indivi-dual behavioural characteristics using objective measures.Studies reported in the literature show some possibilitiesin this area. For example, Lanier and Grandin (2002)reported that cannon bone thickness and width in steersdiffered significantly depending on their temperament.An objective measure of temperament is facial hair whorlposition in relation to the eye level of bulls (Randle,1998; Lanier et al., 2001) or eye white percentage(Core et al., 2009). Relationship between temperamentand bulls facial hair whorl position could possibly beattributed to the fact that during embryonic development,skin, its products and the nervous system arise from thesame germ layer, or ectoderm (Fletcher and Weber, 2010).Therefore the mentioned traits could serve as preciseindicators of cattle temperament and/or perhaps evenother behavioural traits.
Also, it is expected that in the future, objective meth-ods of temperament assessment will be applied in prac-tice 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 cowsinto an automatic milking system could be used toestimate breeding value for animal temperament.Whereas, Pastell et al. (2006) concluded that measuringthe load on each leg of a cow can be used to assess itsmilking behaviour, including milking temperament. Per-haps this method could be adapted to assess the beha-viour of young heifers and bulls.
In case of beef cattle, two types of methods forelectronic measurement of animal behaviour appear tobe practically useful—the assessment of animal reactivityin the mobile cage/chute and the assessment of speedflight (measurement of exit time). These applicationsindicate that traditional subjective scoring techniques canbe replaced with more repeatable objective measures forexample, when temperaments are assessed for performancestudies (Maffei et al., 2006; Maffei, 2009; Sebastian et al.,2011; Schwartzkopf-Genswein et al., 2012).
Technological advances of the last decade have providedtools to develop systems for real-time assessment of cattle
behaviour. For this purpose, use is made of knowledgeconcerning applied ethology, animal psychology or chron-obiology, which examines periodic biological phenomena inanimals under different environmental conditions (Balzeret al., 2009). At the same time, current knowledge andtechnological solutions ‘‘work’’ together. Today, cattle beha-viour can be studied using the Global Positioning System(GPS) and the Geographic Information System (GIS) in openspaces (e.g. pastures), or using tracking and monitoringsystems (x-, y-, z-positioning in 3D and 2D space) in barns.In many cases, these systems are still being improved andadapted for use in research and breeding practice. One ofthe major limitations to the use of these systems on a widescale has been the cost of purchase and installation (Turneret 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 reportedabove could serve to assess temperament and otherbehavioural traits in cattle of different ages maintainedunder different conditions, while minimising the effect ofanthropomorphic interpretations of animal behaviour andtaking into account the importance of positive/negativestates 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 consid-erably high individual variation, despite the fact that forexample, cows, being gregarious by nature, perform manyactivities during the same time, using similar patterns ofbehaviour. This variation increases as animals are allowedto freely demonstrate their behaviours (e.g. in pasture andloose-housing systems) and concerns especially thosebehavioural traits that did not play a key role in cattledomestication and breeding. When studying the beha-vioural responses of dairy cows to weaning of calves,Hopster et al. (1995) found no clear similarities in thebehaviour of multiparous cows. The authors analysedphysiological and behavioural parameters such as plasmacortisol 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, andorder of entry into the milking parlour. Adamczyk et al.(2011) reported high individual variation (V) in dailyphysical activity (V¼37–78%) of Holstein–Friesian cowswithin particular technological/treatment groups raisedunder welfare conditions in a free-stall barn. During thestudy period, no animal diseases and no occurrence ofoestrus were observed, and no additional procedures (e.g.artificial insemination, pregnancy checks) were per-formed. Barrozo et al. (2011) also found high variationin temperament of Nellore cattle (V¼41.15%) using four-point scale. Similarly Cafe et al. (2011) assessed thetemperament of young Brahman and Angus cattle basedon measurements of flight speed (FS) and crush score (CS),found that despite using tests with different degrees ofscoring objectivity, animals of both breeds were charac-terised by equally high individual variation, as evidenced
K. Adamczyk et al. / Livestock Science 154 (2013) 1–12 5
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 traitsare inherited as quantitative traits influenced by additivegene effects. They are much less frequently associatedwith single gene effect as exemplified by the relationshipbetween excitability and the muscle hypertrophy gene inbeef cattle (Holmes et al., 1972; Holmes et al., 1973;Newman, 1994; Phillips, 2002).
Of all behavioural traits in cattle, temperament hasreceived the most attention. Burrow (1997) showed thatthe coefficients of heritability for temperament, estimatedwithin similar production systems and using the sameassessment method, varied considerably (h2
¼0.00–0.67)according to the age of animals and their genotype.
Table 1Heritability of cattle temperament (data for the last 30 years).
Items h27s.e. No. animals No. sires Type of catt
T5a 0.2270.03 14,596 334 Holstein cow
0.2570.06 4695 125 Jersey cows
TSb 0.00–0.1970.05–0.12 259 –n German Ang
calves
TRc 0.00–0.6170.05–0.24 259 – German Ang
calves
TSb 0.00–0.3870.05–0.26 206 – Simmental
TRc 0.00–0.5970.05–0.21 206 – Simmental
Tmultid 0.08–0.357� 5313 230 Bullfighting
MTe 0.1870.04 30,190 – Danish Hols
cows
TFf 0.1770.07 1032 54 Brahman he
0.3170.09 1142 51 Tropical
composite h
TNMWg 0.1470.08 1113 73 Limousin ca
TRMWh 0.1170.07 1113 73 Limousin ca
TNMHi 0.2270.08 1113 73 Limousin ca
TRMHj 0.2070.08 1113 73 Limousin ca
TNMWg 0.3170.10 1271 65 Limousin ca
TRMWh 0.2870.09 1271 65 Limousin ca
TNMHi 0.1770.07 1271 65 Limousin ca
TRMHj 0.1970.07 1271 65 Limousin ca
a Temperament scoring: five-point scale (1—good temperament, 5—bad teb Temperament scoring during separation tests based on the following tr
vocalisation.c Temperament scoring related to restraint tests on the following traits: Befo
in the restraint yard and time spent running in the restraint yard; During handli
the animal tried to escape during the test, signs of aggression, time spent in th
defecation and/or urination, vocalisation; Five-point scale (1– calm, 5– very exd Temperament scored based concurrently on the following traits: aggres
falling, homing instinct, development, distance, hiding of the face, straightforwe Milking temperament scoring: nine-point scale (36% herds in tie stalls, 6f 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.
Relatively the smallest differences (h2¼0.32–0.70)
were noted when temperament was assessed by measur-ing flight speed. Likewise, Schutz and Pajor (2001)demonstrated high variation in the coefficients of herit-ability 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 inHolstein–Friesian cattle and 0.25 in the Jersey breed.Meanwhile, the coefficients of heritability for beef cattletemperament 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 highcoefficients of heritability for feeding behaviour in feedlotfinished B. taurus and Bos indicus crossbreds (h2
¼0.36 fortime spent eating, h2
¼0.44 for number of eating sessions,h2¼0.51 for eating rate). The other behavioural traits in
cattle such as social behaviour or reproductive behaviourgenerally have medium or low heritability (Schutz andPajor, 2001; Boissy et al., 2005; Løvendahl and Chagunda,2009; Berry and McCarthy, 2012).
le Age Model used References
s 24.5mo Multivariate REML
with sire model
Visscher and
Goddard (1995)24.4mo
us 238d Multivariate REML Gauly et al. (2001)
us (average for
both
calves breeds)
calves
cattle 2-year-old
females, 3-4-
year-old
males
Multivariate REML Silva et al. (2002)
tein 579-1,379d (AI)–REML Lassen and Mark
(2008)
ifers 300d REML Prayaga et al. (2009)
eifers
300d
lves 80-179d (AI)-REML Benhajali et al.
(2010)lves 80-179d
lves 80-179d
lves 80-179d
lves 180-280d
lves 180-280d
lves 180-280d
lves 180-280d
mperament).
aits: total separation times, signs of aggression, separation success and
re handling period (60 s): time spent running before and during handling
ng period (180 s): time until animal reached the corner, number of times
e corner, stroking the animal for a maximum period of 30 s at the back,
cited).
siveness, ferocity, fixedness, involvement, mobility, enters in a gallop,
ardness, rhythm, nobility
4% herds in free stall).
K. Adamczyk et al. / Livestock Science 154 (2013) 1–126
Research shows that cow temperament is a beha-vioural trait most correlated to dairy performance, inparticular milk yield and milking speed (rg¼�0.11–�0.40 and 0.36–0.57, respectively) (Foster et al., 1988;Lawstuen et al., 1988; Erf et al., 1992; Visscher andGoddard, 1995). In a population of Canadian dairy cattle(Holstein–Friesian, Jersey and Ayrshire), Sewalem et al.(2010) reported that longevity decreases with increasingnervousness. This is mainly due to the systematic selec-tion of bulls (since 2001) for milking temperament usingthe Lifetime Profit Index and giving preference to calmanimals during mating.
Feeding behaviour and temperament are mostly cor-related with meat performance traits. Robinson and Oddy(2004) found high genetic correlations between the fol-lowing traits assessed in beef cattle crosses: time spenteating and feed conversion ratio (rg¼0.78), eating rateand feed conversion ratio (rg¼�0.83), eating rate andweight gains (rg¼0.53), number of eating sessions andfeed conversion ratio (rg¼0.49). Nkrumah et al. (2007)noted slightly lower correlations between the tempera-ment of beef cattle sired by Angus, Charolais, or Hybridbulls and traits such as carcass weight (rg¼�0.54),carcass meat percentage (rg¼0.33) or average daily gain(rg¼�0.25). Phocas et al. (2006) demonstrated relativelyhigh genetic correlations between docility and fertility inLimousin heifers (rg¼0.55).
3.3. Breeding for behavioural traits in cattle
Among cattle behavioural traits, most attention isgiven by breeders to temperament. Long-term culling ofaggressive animals caused a marked increase in the
Table 2Coefficients of correlation between breeding values for temperament of dairy br
Countrya AUS CAN CHE DEA
AUS 1.00 �0.05b –n –
0.72c
CAN 0.64d 1.00 – –
�0.09e
CHE 0.15d 0.03d 1.00 –
– –
DEU 0.60d 0.97d 0.20d 1.00
– – –
DFS 0.72d 0.87d 0.15d 0.89d
0.73e 0.62e – –
GBR 0.65d 0.65d 0.46d 0.73d
– – – –
JPN 0.68d 0.79d 0.34d 0.81d
– – – –
NLD 0.72d 0.88d 0.21d 0.88d
0.97e�0.34e – –
NZL 0.76d 0.57d 0.22d 0.58d
0.83e�0.24e – –
a Abbreviation for country name: AUS–Australia, CAN–Canada; CHE–Switz
GBR–United Kingdom and Ireland; ITA–Italy; JPN–Japan; NLD–The Netherlandb Guernsey.c Red Dairy Cattle.d Holstein–Friesian.e Jersey.f Brown Swiss.n no data available.
proportion of cattle with a calm temperament. Thisconcerns both dairy and beef cattle populations. Forexample, the results of the evaluation of dairy cattlepopulation in Canada indicated that temperament ofmore than 90% milk-recorded cows can be described asan average, calm and very calm (Interbull, 2010). Also, inCanadian Limousine cattle a noticeable genetic improve-ment of docility was observed—from about 1.00 EPD in1985 to above 14.00 EPD in 2006 (CLA, 2007). Similarlygood results are achieved when selecting cattle with moreaggressive traits. An example of empirical selection foraggressiveness in bullfighting cattle was given by Silvaet al. (2002), who found a distinct increase of meanbreeding value for this trait in 1980–99.
Breeding value for temperament of dairy breed bulls,based on daughters, has been estimated internationallysince 2009. This was pioneered by Canada, Germany, TheNetherlands, Switzerland and Scandinavia for theHolstein–Friesian; by Canada, The Netherlands and Scan-dinavia for Red cattle; and by Canada, The Netherlandsand Scandinavia for the Jersey. The first data for 2009showed a high consistency of results across some coun-tries. For example, in Scandinavian countries it was 79–96% (Red breeds) and 83–91% (Holstein–Friesian). Thehighest breeding value (BV) for temperament of Holstein–Friesian bulls was estimated in Canada (BV¼104.2) andFinland (BV¼103.2), and the lowest in the Netherlands(BV¼98.6). In the case of Red cattle the highest and thelowest scores were given to Danish (BV¼107.5) andCanadian (BV¼95.1) bulls, respectively (Fogh et al., 2009).
Among the countries reported above, special mentionshould be given to breeding work on dairy cattle tem-perament in Denmark. This trait is evaluated in
eed bulls used in different countries (adapted from Bagnato et al., 2007).
DFS GBR JPN NLD NZL
– – – – 0.33b
0.67c 0.77c
– – – 0.99f 0.92b
0.94c 0.58c
– – – – –
– – – – –
1.00 – – – –
0.51c
0.82d 1.00 – – –
–
0.85d 0.75d 1.00 – –
– –
0.89d 0.73d 0.79d 1.00 –
0.53e – –
0.65d 0.52d 0.59d 0.74d 1.00
0.47e – – 0.87e
erland; DEA–Germany and Austria; DFS–Denmark, Finland and Sweden;
s and Flanders; NZL–New Zealand. Abbreviations for breed types.
K. Adamczyk et al. / Livestock Science 154 (2013) 1–12 7
primiparous cows of all milk-recorded dairy breeds (Hol-stein-Friesian, Jersey, Danish Red). According to Interbulldata, heritability of temperament in Danish dairy cattle is0.05 for Danish Jersey, 0.13 for Red Holstein and DanishHolstein, and 0.20 for Danish Red. By analogy with thecoefficients of heritability, the weights for cow tempera-ment 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 thatthe NTM index is also used in Sweden and Finland, whichfacilitates comparison of animal breeding value amongthese countries (Interbull, 2003; Fogh et al., 2011).
The diversity of methods for assessment of dairy cattletemperament makes it difficult to compare the breedingvalue of bulls from different countries. This was pointedout by Bagnato et al. (2007), who calculated correlationsbetween breeding values for dairy breed bulls, estimatedusing the Multiple Across Country Evaluation method.These authors reported the following values of correlationcoefficients 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 Cattleand 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 havebeen mapped (Hu et al., 2007; AnimalQTLdb, 2013). Incomparison, the search for QTLs affecting behaviouraltraits has been much less successful. So far most studiesin this area were conducted with other species of animals,mainly mice (Willis-Owen and Flint, 2006), in farmedanimals, including poultry (Buitenhuis et al., 2005) andpigs (Reiner et al., 2009).
Among the research results published on the identifi-cation of QTLs for behavioural traits in cattle, specialconsideration should be given to the studies by Fisheret al. (2001), Schmutz et al. (2001), Hiendleder et al.(2003), Wegenhoft (2005), Boldt (2008) and Gutierrez-Gilet al. (2008). This topic was also addressed by authorsinvestigating the genetic determinants of productiontraits in dairy cattle and their milking temperament(Spelman et al., 1999; Schrooten et al., 2000; Hiendlederet al., 2003).
Of the behavioural traits in cattle, researchers gener-ally focused on temperament and capacity for habitua-tion. To date, approximately 44 QTLs located on mostchromosomes except numbers 2, 13, 17, 22, 23, 24 and 27were identified for these traits (Table 3). Most QTLs forthe traits mentioned above were mapped on chromo-somes 1, 4, 9, 16, 19 and 29.
This significant dispersion of bovine genome regionsthat determine the behaviour of animals may be largelydue to using different research methods within a giventrait. Preliminary genome scanning results also indicatethe need for increasing the density of genetic markers toimprove the applicability of studies aimed at findingcandidate genes for cattle behaviour traits in the future.
4.2. Candidate genes for behavioural traits in cattle
The construction of genetic maps for different speciesof farm animals and efforts to improve their welfare indifferent production systems has increased the number ofstudies on the genetic background of animal behaviour.Identification of the molecular mechanisms of behaviourmay contribute to a better understanding of behaviouralproblems widespread in many fields of livestock produc-tion, such as animal handling, susceptibility to stress, oradaptability to different production conditions (Morm�ede,2005; Jensen et al., 2008).
It is supposed that the identification of QTLs forbehavioural traits in cattle makes it possible to determinecandidate genes located near genetic markers that havethe largest influence on a given trait. However, thisprocedure is not sufficiently effective due to the highcomplexity of the expression of individual animal beha-viours and their interaction with the environment(Schmutz et al., 2001; Gutierrez-Gil et al., 2008).
To date, only several published studies determinedgenes that may affect cattle temperament, feeding beha-viour and reproductive behaviour. These studies concernthe location and polymorphism of genes related to reg-ulation of the stress hormone, neuropeptide and neuro-transmitter levels. For example, Boldt (2008) found norelationship between cattle temperament and four genes,bone morphogenetic protein 1 (BMP1), bridging integra-tor 3 (BIN3), farnesyl-diphosphate-farnesyltransferase 1(FDFT1) and cathepsin B (CTSB), localised on bovinechromosome 8 close to QTL associated with temperamentunderstood as disposition, this QTL being previouslyidentified by Wegenhoft (2005).
Studies in humans, mice and monkeys revealed arelationship between genetic variants of the neurotrans-mitter monoamine oxidase (MAOA) and the level ofindividual aggression (Brunner et al., 1993; Popovaet al., 2001; Karere et al., 2009), whereas Luhken et al.(2010) found no significant relationships between MAOAgene polymorphism and behavioural traits in beef breedsof cattle. Moreover, Glenske et al. (2011) reported a lowrelationship between the dopamine receptor D4 (DRD4)gene located near QTL for behavioural traits on chromo-some 29, and temperament of German Angus cattle. Astudy using the expression of the leucocyte heat shockprotein (Hsp) gene for early detection of the subclinicalsigns of bovine respiratory disease complex (BRD) con-firmed that this gene is associated with stress response ofanimals (Eitam et al., 2010).
Preliminary results of a study (Alam et al., 2012) on thepolymorphism of bovine neuropeptide Y5 receptor gene(NPY5R) suggest that it potentially modifies the action ofneuropeptide Y by modulating its effect, and thus may playan important role in the regulation of appetite and feedingbehaviour in beef cattle. Similar results of research on usingthe polymorphism of the melanocortin 4 receptor gene(MC4R) as a genetic marker of economic traits in KoreanHanwoo cattle suggest its possible effect on feed intakecapacity and feeding behaviour in cattle (Seong et al., 2011).
A study aimed at determining genes that affect repro-ductive behaviour in cows showed a significant
Table 3Quantitative trait loci for temperamenta and habituation abilityb of cattle.
K. Adamczyk et al. / Livestock Science 154 (2013) 1–12 9
relationship between the expression genes in the ventraltegmental area and the intensity of oestrus expression byhigh-yielding Holstein–Friesian cows (Wyszynska-Kokoet al., 2011). Furthermore, Kommadath et al. (2011)demonstrated a significant effect of the expression ofseveral brain neurotransmitter and neurotransmitterreceptor genes (OXT, AVP, POMC, MCHR1) on oestrousbehaviour of dairy cows such as socio-sexual anxiety,stress and feeding motivation.
It follows from the studies cited above that no candi-date genes with a substantial effect on cattle behaviouraltraits have been identified to date, regardless of the breedand the environment that modulates them. One of thereasons for this could be the complexity of cattle beha-viour and lack of phenotypic data used to characterise thebehavioural traits.
5. Conclusions
Identification of cattle behaviour is necessary forefficient production of milk and beef under welfare-friendly conditions. Unfortunately, our understanding ofthe neurohormonal and genetic determinants of cattlebehaviour warrants further investigation. Because thesetraits are essential for cattle breeding, they have beenincreasingly incorporated in breeding programs in recentyears. It appears that because behavioural traits still showconsiderable variation and correlate favourably to pro-duction traits, the prospects for their improvement arepromising with regard to both population genetics andmolecular genetics. However, for behavioural geneticstudies to achieve applied use, it is necessary to provideunambiguous phenotypic definitions of individual beha-vioural traits of cattle and to use objective methods fortheir assessments in order to compare breeding values inproduction systems within and between countries.
Conflict of interest
There is no conflict of interest in this manuscript.
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