A behaviour test on German Shepherd dogs: heritability of seven different traits
←
→
Page content transcription
If your browser does not render page correctly, please read the page content below
Applied Animal Behaviour Science 79 (2002) 113±132
A behaviour test on German Shepherd dogs:
heritability of seven different traits
Silvia Ruefenachta,*, Sabine Gebhardt-Henrichb,
Takeshi Miyakea, Claude Gaillarda
a
Division of Genetic Epidemiology, Institute of Animal Genetics, Nutrition and Housing,
University of Berne, Bremgartenstrasse 109a, CH-3012 Berne, Switzerland
b
Division of Animal Housing and Welfare, Institute of Animal Genetics, Nutrition and Housing,
University of Berne, Bremgartenstrasse 109a, CH-3012 Berne, Switzerland
Accepted 11 July 2002
Abstract
In this study, genetic and non-genetic effects on behavioural traits were estimated, based on records
of the ®eld behaviour test of the Swiss German Shepherd Dog breeding club. This standardized test
has been applied since 1949 and comprised the following seven traits: self-con®dence, nerve stability,
temperament, hardness, sharpness, defence drive and ®ghting drive. The analyses were based on the
test results of 3497 German Shepherds between 1978 and 2000. Gender, age, judge and kennel had
signi®cant effects on all behaviour traits. The heritabilities were calculated using three different
methods and ranged between 0.09 and 0.24, with a standard error varying between 0.04 and 0.06.
Phenotypic correlations among the traits lay between 0.28 and 0.94, the genetic correlations between
0.34 and 1.0. No signi®cant correlations between hip dysplasia scores and the behavioural traits were
found ( 0.04 to 0.01). The modest genetic improvement over the last 25 years in the studbook
population of the German Shepherd dog (GSD) was due to the low heritabilities of the behaviour
traits, but mainly because of the low selection intensities after the test (only 8% failed). Some
recommendations were made to improve the test and selection response.
# 2002 Elsevier Science B.V. All rights reserved.
Keywords: Behaviour test; Breeding; Dog; Genetic; German Shepherd; Heritability; Selection response
*
Corresponding author. Present address: Interdisciplinary Dermatology Unit, Department of Clinical
Veterinary Medicine, Laenggassstrasse 128, CH-3012 Berne, Switzerland. Tel.: 41-31-631-26-18/22-71;
fax: 41-31-631-25-41.
E-mail address: silvia.ruefenacht@itz.unibe.ch (S. Ruefenacht).
0168-1591/02/$ ± see front matter # 2002 Elsevier Science B.V. All rights reserved.
PII: S 0 1 6 8 - 1 5 9 1 ( 0 2 ) 0 0 1 3 4 - X114 S. Ruefenacht et al. / Applied Animal Behaviour Science 79 (2002) 113±132 1. Introduction The behaviour of dogs is of growing public concern. In today's hectic, technical and loud world, dogs are nevertheless expected to behave without endangering or annoying people. Behaviour tests are used in breeding programs, as well as for the prediction of the potential danger of particular dogs, for the selection of service dogs, for the prediction of behaviour of dogs from shelters, as performance testing, etc. Standardized behaviour tests for the purpose of evaluating the character or temperament of dogs in regard to people and environment have been applied in Switzerland in various breeds for breeding purposes. Every breeding club uses its own test with a different request pro®le. Frightened dogs with a disposition to aggression and with a tendency to run away are generally excluded from breeding. Special behaviour tests have been designed and used to predict the potential danger of a particular dog (Planta and Netto, 1997, behaviour test used in Germany; Lower Saxony, 2002, http://www.ml.niedersachsen.de/wesenstest.htm). Other performance tests, such as dog racing, hunting tests, ``Schutzhund'' tests (guard dogs), etc. are applied for selection purposes too. Besides their use as selection criteria, they are also used as aptitude tests. The objectives of aptitude tests are to predict the suitability and future performance of the dogs, e.g. as police dogs (Slabbert and Odendaal, 1999), guide dogs for the blind (Wilsson and Sundgren, 1997a,b, 1998), family dogs (Venzl et al., 1989), and shelter dogs (van der Borg et al., 1991; Weiss and Greenberg, 1997; Ledger and Baxter, 1997). Behavioural traits can only be integrated in breeding programs, if they can be measured accurately, as objectively as possible, and if they demonstrate signi®cant genetic variation. In one of the ®rst comprehensive studies, Scott and Fuller (1965) looked for develop- mental, behavioural, and genetic differences in ®ve different dog breeds and their crosses and backcrosses in different age groups. They found signi®cant genetic variation and important maternal effects in different behavioural traits. Since Scott and Fuller (1965), heritabilities of a multitude of behavioural traits have been estimated in various dog breeds. In Table 1, heritability estimates of different studies are presented. The heritability values concerning the character of dogs were heterogeneous ranging from 0 to 0.58 with an average of 0.20. In the other two groups of traits (achievements in training/working and sensitivity) heritabilities were lower averaging 0.12 in both groups. Comparisons between these values have to be done with care because the de®nitions of the traits, the sampling procedures, the methods of evaluations, the breeds, etc. varied between the authors. The aim of this study was to estimate the importance of genetic and non-genetic effects on behavioural traits measured by the behaviour test of the Swiss German Shepherd Dog breeding club. Genetic parameters such as heritabilities and genetic correlations should point out which traits could be suitable to be included in a breeding program. 2. Materials and methods 2.1. Data Since 1949 the Swiss German Shepherd breeding club has applied a standardized behaviour test (Seiferle and Leonhardt, 1984). Results of these tests have been stored in a
S. Ruefenacht et al. / Applied Animal Behaviour Science 79 (2002) 113±132 115
Table 1
Heritabilities of behaviour traits in dogs
Traitsa Heritability Breed References
Character
Activity 0.53 German Shepherd Wilsson and Sundgren (1998)
Adaptiveness 0.00/0.04b German Shepherd Reuterwall and Ryman (1973)
Affability 0.37 German Shepherd Wilsson and Sundgren (1997b)
Affability 0.15 Labrador Wilsson and Sundgren (1997b)
Affability 0.17/0.09b German Shepherd Reuterwall and Ryman (1973)
Character 0.12 German Shepherd Pfleiderer-HoÈgner (1991)
Closeness 0.04 California guide dogs Scott and Bielfelt (1976) (cited in
Mackenzie et al., 1986)
Concentration 0.28 Labrador and others Goddard and Beilharz (1982)
Confidence 0.16 American guide dogs Bartlett (1976) (cited in Mackenzie
et al., 1986)
Courage 0.05/0.13b German Shepherd Reuterwall and Ryman (1973)
Courage 0.26 German Shepherd Wilsson and Sundgren (1997b)
Courage 0.28 Labrador Wilsson and Sundgren (1997b)
Contact 1 0.21 German Shepherd Wilsson and Sundgren (1998)
Contact 2 0.42 German Shepherd Wilsson and Sundgren (1998)
Excitability 0.09 Labrador and others Goddard and Beilharz (1982
Energy 0.05 American guide dogs Bartlett (1976) (cited in Mackenzie
et al., 1986)
Fear 0.46 Labrador and others Goddard and Beilharz (1982)
Forgetting unpleasant 0.1/0.17b German Shepherd Reuterwall and Ryman (1973)
incidents
Hardness 0.15 German Shepherd Wilsson and Sundgren (1997b)
Hardness 0.2 Labrador Wilsson and Sundgren (1997b)
Heel 0.10 California guide dogs Scott and Bielfelt (1976) (cited in
Mackenzie et al., 1986)
Intelligence 0.06 American guide dogs Bartlett (1976) (cited in Mackenzie
et al., 1986)
Large ball 0.27 German Shepherd Wilsson and Sundgren (1998)
Motivation 0.34 Div. purebred dogs Scott and Fuller (1965)
New-experience response 0.06 California guide dogs Scott and Bielfelt (1976) (cited in
Mackenzie et al., 1986)
Nervousness 0.58 Labrador and others Goddard and Beilharz (1982)
Nerve stability 0.25 German Shepherd Wilsson and Sundgren (1997b)
Nerve stability 0.17 Labrador Wilsson and Sundgren (1997b)
Self-right 0.22 American guide dogs Bartlett (1976) (cited in Mackenzie
et al., 1986)
Shriek 0.24 German Shepherd Wilsson and Sundgren (1998)
Success 0.44 Labrador and others Goddard and Beilharz (1982)
Suspicion 0.10 Labrador and others Goddard and Beilharz (1982)
Temperament 0.51 German Shepherd Mackenzie et al. (1985)
Temperament 0.15 German Shepherd Wilsson and Sundgren (1997b)
Temperament 0.10 Labrador Wilsson and Sundgren (1997b)
Tug of war 0.48 German Shepherd Wilsson and Sundgren (1998)
Willing in training 0.12 California guide dogs Scott and Bielfelt (1976) (cited in
Mackenzie et al., 1986)
Willingness 0.03 American guide dogs Bartlett (1976) (cited in Mackenzie
et al., 1986)116 S. Ruefenacht et al. / Applied Animal Behaviour Science 79 (2002) 113±132
Table 1 (Continued )
Traitsa Heritability Breed References
Willingness 0.22 Labrador and others Goddard and Beilharz (1982)
Willing new experience 0.24 California guide dogs Scott and Bielfelt (1976) (cited in
Mackenzie et al., 1986)
Yelp 0.22 German Shepherd Wilsson and Sundgren (1998)
Achievement in training and working characteristics
Ability to cooperate 0.28 German Shepherd Wilsson and Sundgren (1997b)
Ability to cooperate 0.35 Labrador Wilsson and Sundgren (1997b)
Come 0.14 California guide dogs Scott and Bielfelt (1976) (cited in
Mackenzie et al., 1986)
Defence drive 0.20 German Shepherd Wilsson and Sundgren (1997b)
Defence drive 0.22 Labrador Wilsson and Sundgren (1997b)
Fetch 0.24 California guide dogs Scott and Bielfelt (1976) (cited in
Mackenzie et al., 1986)
Fetch 0.21 German Shepherd Wilsson and Sundgren (1998)
Fighting instinct 0.04 American guide dogs Bartlett (1976) (cited in Mackenzie
et al., 1986)
Fighting the leash 0.44 Div. purebred dogs Scott and Fuller (1965)
Footing-crossing 0.06 California guide dogs Scott and Bielfelt (1976) (cited in
Mackenzie et al., 1986)
Hare tracking 0.03 German Hunting dogs Geiger (1973) (cited in
Pfleiderer-HoÈgner, 1979)
Hare tracking 0.02 German Wirehaired KraÈmer (1981) (cited in Hruby,
Pointer 1991)
Man-work 0.06 German Shepherd Pfleiderer-HoÈgner (1979)
Nose 0.01 German Hunting dogs Geiger (1973) (cited in
Pfleiderer-HoÈgner, 1979)
Nose 0.03 German Wirehaired KraÈmer (1981) (cited in Hruby,
Pointer 1991)
Obedience 0.16 Div. purebred dogs Scott and Fuller (1965)
Obedience 0.01 German Hunting dogs Geiger (1973) (cited in
Pfleiderer-HoÈgner, 1979)
Obedience 0.01 German Wirehaired KraÈmer (1981) (cited in Hruby,
Pointer 1991)
Obedience 0.09 German Shepherd Pfleiderer-HoÈgner (1991)
Playful fighting 0.16/0.21b German Shepherd Reuterwall and Ryman (1973)
Pointing 0.01 German Wirehaired KraÈmer (1981) (cited in Hruby,
Pointer 1991)
Prey drive 0.05 Labrador Wilsson and Sundgren (1997b)
Prey drive 0.31 German Shepherd Wilsson and Sundgren (1997b)
Protective instinct 0.12 American guide dogs Bartlett (1976) (cited in Mackenzie
et al., 1986)
Retrieve 0.20 German Shepherd Wilsson and Sundgren (1998)
Search 0.00 German Hunting dogs Geiger (1973) (cited in
Pfleiderer-HoÈgner, 1979)
Search 0.03 German Wirehaired KraÈmer (1981) (cited in Hruby,
Pointer 1991)
Self-defence 0.11/0.26b German Shepherd Reuterwall and Ryman (1973)
Self- and handler-defence 0.04/0.16b German Shepherd Reuterwall and Ryman (1973)
Sharpness 0.13 German Shepherd Wilsson and Sundgren (1997b)S. Ruefenacht et al. / Applied Animal Behaviour Science 79 (2002) 113±132 117
Table 1 (Continued )
Traitsa Heritability Breed References
Sharpness 0.11 Labrador Wilsson and Sundgren (1997b)
Sit 0.06 California guide dogs Scott and Bielfelt (1976) (cited in
Mackenzie et al., 1986)
Tracking 0.10 German Shepherd Pfleiderer-HoÈgner (1991)
Traffic 0.12 California guide dogs Scott and Bielfelt (1976) (cited in
Mackenzie et al., 1986)
Trained response 0.08 California guide dogs Scott and Bielfelt (1976) (cited in
Mackenzie et al., 1986)
Sensitivity
Body sensitivity 0.16 California guide dogs Scott and Bielfelt (1976) (cited in
Mackenzie et al., 1986)
Body sensitivity 0.10 American guide dogs Bartlett (1976) (cited in Mackenzie
et al., 1986)
Body sensitivity 0.33 Labrador and others Goddard and Beilharz (1982)
Ear sensitivity 0.00 California guide dogs Scott and Bielfelt (1976) (cited in
Mackenzie et al., 1986)
Ear sensitivity 0.25 American guide dogs Bartlett (1976) (cited in Mackenzie
et al., 1986)
Hearing sensitivity 0.00 Labrador and others Goddard and Beilharz (1982)
Sound shy 0.14 Labrador and others Goddard and Beilharz (1982)
Auditory disturbance 0.04/0.15b German Shepherd Reuterwall and Ryman (1973)
Nose distraction 0.00 Labrador and others Goddard and Beilharz (1982)
Nose distraction 0.12 American guide dogs Bartlett (1976) (cited in Mackenzie
et al., 1986)
Distraction 0.08 Labrador and others Goddard and Beilharz (1982)
Dog distraction 0.09 Labrador and others Goddard and Beilharz (1982)
Dog distraction 0.27 Labrador and others Goddard and Beilharz (1982)
a
Original terms used by the authors.
b
Heritabilities of males/heritabilities of females.
database starting in 1978. Data of the present study consisted of behaviour test results of
3497 dogs from 1978 until 2000. Fifty-two percent were females and 48% males. The
average age at test was 21.5 months (9.1) where 71% were between 12 and 23 months,
22% between 24 and 35 months and 7% were 3 years or older. The average number of
progeny per dam was 2.2 (ranging from 1 to 18) and per sire 3.3 (ranging from 1 to 52). All
the dogs were born in 729 kennels. Among the 3497 dogs, 122 were inbred. The average
inbreeding coef®cient of all dogs was very low (0.1%). The inbreeding coef®cient of the
inbred dogs ranged from 0.7 to 14% (83 dogs were between 0.7 and 5%, 27 dogs between 5
and 10% and 12 dogs between 10 and 14%).
2.2. The standardized behaviour test
The test is standardized and has remained unchanged for years (Seiferle and Leonhardt,
1984), except for the traits self-defence and ®ghting drive, which were not tested after 1989
(see later). In most cases, the owner handles the dog (handler). During the test the handler118 S. Ruefenacht et al. / Applied Animal Behaviour Science 79 (2002) 113±132 should not force the dog into submission. Only a few commands should be given to allow the dog to react independently in the different situations. Except at the beginning and during the last part (handler-defence) the dog is not leashed. The dog must be at least 12 months of age and should not be older than 2 years. It can be tested only once. The behaviour test is performed in different locations in Switzerland during the year. It takes place in an open area, which can be as large as half a football ®eld. The test lasts 30± 40 min per dog. Judges have to take a monthly 3-year training course including a ®nal examination before they are licensed as a judge for the behaviour test. They also have to attend a yearly brush up meeting. Between 1978 and 2000, 38 judges had rated on average 92 dogs (ranging from 6 to 419). In order to obtain a good estimate of the effect of the judges in the statistical analyses, we pooled the 16 judges with fewer than 30 evaluated dogs. The behaviour test is divided into eight different parts. 2.2.1. Part 1: Approaching the handler The judge approaches the handler, who keeps the dog on the leash. The judge veri®es the identity of the dog by controlling its ear tattoo. The dog is let off the leash and the judge asks the handler several questions about the dog: age, living space, contact with the environment, history of ownership, relationship of dog to handler, previous working dog training, etc. 2.2.2. Part 2: Behaviour in friendly situations Several different situations are tested: 10±20 people, the judge, handler and the dog move around freely. Then the people form a line and walk towards the dog and the handler, ®rst at a normal pace, then faster. While they are walking towards each other, the handler with the dog crosses the line formed by the people. Next, dog and handler walk through a narrow lane of standing people. Then the people form a wide circle, while dog and handler are in the middle of it. The people walk towards the dog and the handler, ®rst at a normal pace, and then at running speed while clapping their hands until they almost touch the dog. All these situations have to be done in a friendly and not threatening way for the dog. The sequences can be changed. 2.2.3. Part 3: Reactions to different environmental stimuli Several optical and acoustical objects are presented to the dog in a playful manner: bicycle bell, empty cans in a bag, large steel plate, plastic cans ®lled with stones and an umbrella. A blanket or large piece of plastic is held high while handler and dog pass underneath it, then it is placed on the ¯oor, and dog and handler tread on it. There should be no provocation or intimidation, it should be more like a game for the dog. The methods and objects can vary and are changed frequently. 2.2.4. Part 4: Reaction to gunfire The reaction to gun®re shot with a big bore blank pistol is tested at a distance of about 20 m. The ®rst shot is ®red when the dog and handler are moving away from the shooter, a second one when they are moving parallel to him. The movements of the shooter should not be visible for the dog.
S. Ruefenacht et al. / Applied Animal Behaviour Science 79 (2002) 113±132 119
2.2.5. Part 5: Play with a toy (dummy made of French linen)
First the handler plays with the dog while holding the toy in his hands, inciting the dog to
bite, gripping it and dragging it. Then the judge takes the toy and continues the animation
while increasing the distance to the handler.
2.2.6. Part 6: Handler-defence
The handler holds the dog on a 1 m leash. The judge ®rst approaches the handler in a
friendly way and shakes hands with him. Then the judge takes a few steps away from the
handler and the dog and suddenly attacks the handler in a way that looks physically and
verbally serious.
2.2.7. Part 7: Self-defence (not tested since 1990)
The dog is tied to a stable object and left alone for 3 min. He cannot see the handler during
this test. The judge approaches the dog in a friendly way, seeks contact with him, speaks
some words and pets him. Then, as in part 6 of the test, the judge takes a few steps away from
the dog and then suddenly attacks the dog in a way that looks physically and verbally serious
by waving at the dog and threatening it with a stick without actually beating it.
2.2.8. Part 8: Fighting drive (not tested since 1990)
The handler holds the dog. The judge threatens the dog (in the same way as described
before in part 7). The dog can be gently struck with a ¯exible, padded stick. Two blows can
be given on the ¯anks, thighs, or withers. The handler encourages the dog to attack the
``enemy''. Now the judge runs 20±30 m away. The handler lets the dog go, still encoura-
ging it vocally to attack the escaping judge. The judge turns around before the dog reaches
him. Although using aggressive and threatening motions, words, and gestures with the
stick, the judge does not beat the dog anymore. The handler stays in the same place and is
allowed to encourage the dog to ``®ght''.
2.3. Evaluation of the behaviour test
The judge watches the dog attentively during the whole test and then assesses the
behaviour in eight different traits (Seiferle and Leonhardt, 1984). The subjective grading is
recorded verbally:
Self-confidence (ability to react to new situations): A calm, interested, self-confident,
fearless, uninhibited, dauntless, attentive, and friendly behaviour is desired without any
signs of aggression, distrust or tendency to run away in the presence of optical or
acoustical stimuli or sudden approach of strangers.
Nerve stability (the way the dog reacts to the different test parts): The dog should react
neither nervously nor hypersensitively nor jumpy.
Reaction to gunfire: The behaviour should be dauntless, maybe interested but not
fearful.
Temperament (physical flexibility and intensity of reaction to different environmental
stimuli): The dog should be temperamental and interested in the environment with a big
radius of action.120 S. Ruefenacht et al. / Applied Animal Behaviour Science 79 (2002) 113±132
Hardness (severity or ability to accept unpleasant perceptions without being deeply
impressed afterwards): A forceful play with the toy is desired as is untiring interest in
the different visual and acoustic objects.
Sharpness (ability to react in an aggressive way towards a serious or serious looking
attack): The sharpness is desired only when the dog is threatened. After the end of the
threatening period, the dog has to calm down immediately and has to be friendly
towards the participating people and the judge. This kind of sharpness is defined as
desired sharpness.
Defence drive (the ability and desire to guard and protect the threatened handler): The
dog should show a very well-developed defence drive.
Fighting drive (ability and desire of unimpressed and self-confident dogs to attack an
``enemy''): The dog should tolerate the gentle stick beats, persecute and seriously
attack the threatening judge.
One single person of the breeding club transformed the verbal grades into numerical
scores. The lowest scores re¯ect the desired behaviour pattern. The higher the scores are,
the increasingly undesired the behaviour is (Tables 2 and 3).
In order to obtain a measure of the overall behaviour, the grades of the seven particular
characteristics are added to an overall score. Because only some dogs were tested for
®ghting drive, this score was not included in the overall score. Dogs with the best grades
in every trait reached the overall score of 7. When dogs passed the behaviour test
successfully, then the trait outcome was coded with a 1 and those that failed got a 2. One
of the following features was suf®cient for failing: nervousness, insecurity, anxiety,
distrust, gun shyness, missing defence drive combined with anxiety, fear-related sharp-
ness, over-sharpness. If dogs showed none of these features, they passed the test,
regardless of the grades in the other behaviour traits. In case of failure, they are excluded
from breeding.
Table 2
Transformation of the verbal gradings into scores for self-confidence and nerve stability
Behaviour pattern Scorea for
Self-confidence Nerve stability
Self-confident, stable nerves 1 1
Self-confident, still fearless, good-natured, attentive 1 2
Still self-confident, still fearless, good-natured, attentive 2 1
Fearless, good-natured, attentive 2 2
Fearless, indifferent, reserved 2 3
Reserved, distrustful, combative 3 2
Reserved, distrustful, frightened 3 3
Fearful, frightened 4 3
Fearful, frightened, aggressive 4 4
Self-confident, fearless, combative, aggressive 1 4
Aggressive, over-sharpness, termination of the test 5 5
a
Score 1: most desirable; score 5: most undesirable.S. Ruefenacht et al. / Applied Animal Behaviour Science 79 (2002) 113±132 121
Table 3
Transformation of the verbal grades into scores for reaction to gunfire, temperament, hardness, fighting drive,
defence drive, and sharpness
Score Reaction to Temperament Hardness Fighting Defence Sharpness
gunfire drive drive
1 No fear Temperamental Middle to good Pronounced Pronounced Desired
2 Slightly impressed Slightly reduced Slightly reduced Good Good Slightly reduced
3 Impressed Reduced Reduced Latent Latent Missing
4 Fearful No temperament Dauntfull Absent Absent Slightly increased
a a a a a
5 Over-sharpness
a a a a a
6 Fear-related
a
In reaction to gunfire, temperament, hardness and fighting drive the grades range from 1 to 4.
2.4. Statistical methods
Descriptive statistics were implemented by use of the SAS1 software (Release 8.0, SAS
Institute Inc., NC, USA, 1999). Linear models were applied to analyse the in¯uence of
®xed non-genetic effects on the different behavioural traits. These results were used to
determine the ®xed effects for the genetic analysis. The applied model could explain 32±
40% of the total variation in the analysed traits (Table 4). Signi®cant differences were often
found between the gender, ages, judges, evaluation system before and after 1990, and the
kennels but rarely for the locations of the test (Table 4).
The different behaviour patterns were rated in four to six categories; therefore, the
phenotypic distribution of these traits may not follow a normal distribution. Evaluations of
categorical traits are tricky because many statistical methods assume normality. In order to
feel more con®dent about the estimated heritabilities variance components were calculated
by a restricted maximum likelihood (REML) and a Bayesian analysis.
2.4.1. REML approach
Estimates of genetic variance and covariance components were obtained by the
derivative-free REML approach (Boldman et al., 1995). In this analysis, the behavioural
traits were treated as quantitative traits. Heritabilities and genetic correlations were
estimated based on these (co)variance components. The following linear animal model
was ®tted to the data:
yijklm gi sj pk kl b1 ageijklm b2 age2ijklm am eijklm
where yijklm is the behaviour trait of dog m, gi the fixed effect of gender (i 1, 2), sj the
fixed effect of evaluation system (j 1 (up to 1989), 2 (from 1990)), pk the fixed effect of
the judge (k 1±23), kl the fixed effect of the kennel (l 1±729), age of the dog at
examination as a covariant (linear and quadratic), am is the additive genetic effect of the
dog m, and eijklm is the random residual. The random effects were distributed independently
as multivariate normal with mean zero and covariance matrix:
2
a Asa 0
Var
e 0 Is2e122
S. Ruefenacht et al. / Applied Animal Behaviour Science 79 (2002) 113±132
Table 4
Significance levels of fixed effects and coefficient of determination (R2) for eight behavioural traits, the outcome and the overall score
Effect Self- Nerve Reaction Temperament Hardness Defence Fighting Sharpness Outcome Overall
confidence stability to gunfire drive drive score
GenderS. Ruefenacht et al. / Applied Animal Behaviour Science 79 (2002) 113±132 123 where A is the numerator relationship matrix, I is the identity matrix of relevant size and scalars are variance components to be estimated. The REML method based on the animal model includes the effect of selection by means of the relationship matrix (Mrode, 1996), which results in robust and unbiased estimates of heritabilities. 2.4.2. Bayesian analysis with Gibbs sampling Theory of polygenic model and genetic analysis of quantitative traits by Bayesian analysis with Gibbs sampling is based on the ®ndings of Wang et al. (1994). Conditional posterior density functions needed to construct the polygenic model were obtained with the program package MAGGIC (Janss, 1998). The same model was used as in the REML approach. In this analysis, the burn-in period and the spacing were 20,000 and 100, respectively. A total of 270,000 Gibbs samplings were performed to obtain 2500 samples for each parameter. The basic theory of genetic analysis of categorical traits was based on Wright's liability concept (Wright, 1934) in which the underlying continuous variable, named liability, with thresholds imposes a discontinuity on the visible categorical traits. In order to construct conditional posterior density functions needed for the liability concept, the method of threshold model by Bayesian analysis with Gibbs sampling introduced by Sorensen et al. (1995) was adapted for the animal model. As suggested by these authors s2e 1:0 was used as a standardization of the scale. In addition, the maximum and minimum liability values were ®xed at 10.0 and 10.0 on the standardized liability scale. In this analysis, the dependent variable yijklm was replaced by the liability lijklm. The ®xed effects pk and kl of the above model were treated in this analysis as random effects, as suggested by Hoeschelle and Tier (1995) and discussed by Moreno et al. (1997). To treat them as random effects is useful because their mean is zero and therefore does not change the normal shape of liability distribution. The ®xed effects gi and sj that have only two classes were treated as covariates. In categorical trait analysis, it is generally rather dif®cult to obtain convergence compared to the quantitative trait analysis because the number of unknown parameters was increased (e.g. number of liability values for each individual and threshold value). That was the reason why a larger number of samplings was applied for the categorical trait analysis. A total of 540,000 Gibbs samplings were performed to obtain 5000 samples for each parameter. The burn-in period and spacing were 40,000 and 100, respectively. Mode and mean of the 2500 or 5000 samples were taken to estimate the heritability. Together with the means, standard deviations were also calculated, which correspond to the standard error of the estimates. The heritability (h2) is de®ned as the ratio of additive genetic variance to the total phenotypic variance. The phenotypic correlation between two characters is de®ned as phenotypic covariance over the product of the two standard deviations. The dogs' breeding values (BVs) for the different behaviour traits were estimated according to the best linear unbiased prediction (BLUP) method (Henderson, 1973) using the MTDFREML software. The value of an individual (related to a trait), judged by the mean value of its progeny, is called the breeding value of an individual and is twice the mean deviation of the progeny from the population mean (Falconer, 1983). To calculate the genetic trend between 1975 and 1999, averages of breeding values of each
124 S. Ruefenacht et al. / Applied Animal Behaviour Science 79 (2002) 113±132
year of birth were estimated. The trend was then characterized by ®tting a regression
curve to these averages.
3. Results
The distributions of the grading scores of all behavioural traits were skewed (Fig. 1).
The most frequent score was 1 (48±87%). The overall score showed a skewed distribu-
tion too, since 37% of the dogs reached the top score of 7, 12% a score of 8 and 6% a score
of 9. The dog with the poorest grading obtained an overall score of 29 (distribution not
shown).
The ®xed effects based on the REML analysis with the animal model are presented in
Table 5. In all analysed traits, the males reached a better score on average than the females.
The differences expressed in percent of the phenotypic standard deviation between gender
varied between 39% (overall score) and 18% (outcome). In all traits but reaction to gun®re,
temperament and hardness the average scores before 1990 were signi®cantly higher than
afterwards, the range of the differences lay between 37% (outcome) and 15% (overall
score). Highly signi®cant differences could be observed between judges. The largest
difference between two judges was observed for sharpness which amounted to 125% of the
phenotypic standard deviation; the largest difference for reaction to gun®re was only 45%.
All other largest differences lay between 68 and 95%. The effect of kennel was highly
signi®cant too (Table 4). As dogs got older the grading scores increased, i.e. they did worse
on average than younger dogs. This relationship followed a quadratic regression curve; for
an example, see Fig. 2. The average increase of the scores from 18 to 30 months of age
ranged between 15% (reaction to gun®re) and 38% (sharpness) of the phenotypic standard
deviation.
The heritability estimates calculated by REML and with Gibbs sampling, by treating
the traits as quantitative ones, were the same or very similar (Table 6). They varied
Table 5
Fixed effects (%) of the phenotypic standard deviation of the corresponding trait
Traits Difference between
Genders Evaluation The two 18 and 30
systema extreme judges months of age
Self-confidence 34 28 93 24
Nerve stability 37 29 92 28
Reaction to gunfire 20 ns 45 15
Temperament 28 ns 68 36
Hardness 28 ns 71 21
Defence drive 31 20 89 21
Fighting drive 35 ns 77 26
Sharpness desirability 26 34 125 38
Outcome 18 37 82 14
Overall score 39 15 95 31
a
ns: not significant.S. Ruefenacht et al. / Applied Animal Behaviour Science 79 (2002) 113±132
Fig. 1. Distribution of the grading scores in the different behavioural traits: SC, self-confidence; NS, nerve stability; RG, reaction to gunfire; T, temperament; H,
hardness; DD, defence drive; FD, fighting drive; Sh, sharpness.
125126 S. Ruefenacht et al. / Applied Animal Behaviour Science 79 (2002) 113±132 Fig. 2. Effect of age on the score of self-confidence. The score increased from the age of 18 months ( 0.06) to the age of 30 months (0.11) by 0.17, which corresponded to 24% of the phenotypic standard deviation. between 0.09 (sharpness) and 0.24 (reaction to gun®re). The values for the outcome and the overall score were 0.19/0.20 and 0.18/0.18, respectively. The heritability for ®ghting drive was estimated with records up to 1990 (N 1671) and reached values of 0.11/0.13. The standard error of the estimates ranged from 0.04 to 0.06. When traits were treated as categorical ones, the heritabilities were generally the same or somewhat larger but only in one case (reaction to gun®re) it was much larger than in the other two methods. All correlations between the behavioural traits were positive and moderate to high (0.31±1.0; Table 6). Genetic correlations were always larger than the corresponding phenotypic correlations. The highest genetic correlation of 1.0 was observed between self-con®dence and nerve stability. The others ranged between 0.66 and 0.90 except the genetic correlations between sharpness and reaction to gun®re, temperament, as well as defence drive (0.34±0.47). Since the grading of the behavioural traits was part of the outcome and overall score, these correlations were not estimated (autocorrelation). Scores for hip dysplasia (FCI standard) were available from a part of the dogs (N 1166). The phenotypic correlations between hip dysplasia and behavioural traits were quite small ranging from 0.04 (temperament) to 0.01 (outcome). The effectiveness of the practised selection on behaviour during the last 25 years (1975± 1999) is presented in Fig. 3. All trends were signi®cantly negative, i.e. during this time, behaviour patterns have been improved, although only moderately. The curvilinear regressions were mainly caused by the fact that since the late 1980s the averages of the breeding values remained stable or increased slightly. The regressions of self-con- ®dence, nerve stability and overall score ®tted the data best (R2: 0.74±0.81), followed by reaction to gun®re and defence drive (R2: 0.54 and 0.47) and were low for temperament, hardness and sharpness (R2: 0.33±0.28). 4. Discussion In this retrospective study of the last 25 years results of ®eld tests of the standardized behaviour test were evaluated. The available German Shepherd dog (GSD) population consisted of dogs which were intended to be registered as breeding animals. This material is therefore not a representative sample of the whole GSD Swiss population since only
Table 6
Heritabilities of various behavioural traits (on the diagonal), phenotypic (above the diagonal) and genetic (below the diagonal) correlations among these traits in
German Shepherd dogs
Self-confidence Nerve stability Reaction to gunfire Temperament Hardness Defence drive Sharpness
S. Ruefenacht et al. / Applied Animal Behaviour Science 79 (2002) 113±132
a
Self-confidence 0.18 0.94 0.47 0.54 0.61 0.50 0.56
0.18 0.05b
0.21 0.05c
Nerve stability 1.00 0.18 0.47 0.52 0.59 0.48 0.57
0.18 0.05
0.22 0.05
Reaction to gunfire 0.69 0.72 0.23 0.32 0.41 0.34 0.28
0.24 0.06
0.42 0.09
Temperament 0.77 0.68 0.80 0.17 0.53 0.53 0.31
0.18 0.05
0.17 0.05
Hardness 0.87 0.79 0.75 0.67 0.14 0.72 0.44
0.15 0.05
0.17 0.05
Defence drive 0.68 0.66 0.87 0.81 0.90 0.10 0.38
0.11 0.05
0.11 0.04
Sharpness 0.83 0.83 0.44 0.34 0.77 0.47 0.09
0.10 0.04
0.13 0.04
a
Heritability estimation with the REML method.
b
Heritability estimation with Bayesian analysis, Gibbs sampling as a quantitative trait.
c
Heritability estimation with Bayesian analysis, Gibbs sampling as a categorical trait.
127128 S. Ruefenacht et al. / Applied Animal Behaviour Science 79 (2002) 113±132 Fig. 3. Genetic trend of behavioural traits from 1975 until 1999: BVs, breeding values; R2, coefficient of determination; P, significance of the fitted regression. about 10% of an annual birth cohort attends the behaviour test. The selection of these 10% is not random as the future dog owners choose the puppy according to the pedigree, the kennel, the conformation, colour, behaviour and gender. The education of these young dogs commonly includes puppies' school and various behaviour training courses. In addition, most of the dogs attending the behaviour test were especially trained by experienced dogs handlers. The preselection and the special training were not ideal conditions to estimate
S. Ruefenacht et al. / Applied Animal Behaviour Science 79 (2002) 113±132 129 genetic parameters. These handicaps, however, could be at least partially compensated by many generations of records and the application of the animal model approach. Besides random sampling, it is most important that the recorded traits were accurately and objectively measured. Even if behavioural traits are well de®ned, the grading of the performance of a dog will always be subjective. In studies with several judges, an additional non-genetic source of variation will affect the grading and in¯ate the total variance. As suggested by Wilsson and Sundgren (1997b) it is important to keep the number of people evaluating the dog's behaviour down to a minimum and to have routines that regularly coordinate the standard of these experts. Under ®eld test conditions, as in the present study, it was not possible to keep the number of judges small considering the time interval (25 years) and the wide dispersion of the dog owners in Switzerland. In contrast to P¯eiderer-HoÈgner (1979) who found no signi®cant differences between judges, the effect of judges was highly signi®cant for all traits in our population even in spite of annual training and continuing education of the judges. In all traits, scores increased signi®cantly when dogs got older. This is in contrast to Wilsson and Sundgren (1997a) who found no age effect in dogs between 15 and 20 months of age. P¯eiderer-HoÈgner (1979) was not able to show effects of age on behaviour scores in 11-month- to 4-year-old dogs. One possible explanation why older dogs did more badly in all the behaviour traits is that judges were more rigorous when rating these dogs. Another explanation could be that some dogs did not meet the standards to pass the test at a younger age and their owners decided to lengthen the preparation period in order to reach the required level. This practice is understandable because, according to the rules of the breeding organisation, the behaviour test can be performed only once. If the dif®culty to reach the level of education is an effect of the dog itself, then the model for the genetic analyses had to be modi®ed by removing the age effect from the model. In that case, the heritabilities should increase if the mentioned hypothesis is true. In fact, the heritabilities calculated with the reduced model were equal (sharpness) or 0.01±0.04 larger than the ones with the full model. Although the differences between the two values were not signi®cant, it cannot be excluded that at least some dogs needed more time to be ready for the test because they were (genetically) less quali®ed. One reason for the differences between genders may be the sex-related difference in social behaviour of female and male dogs (Wells and Hepper, 1999; Pal et al., 1999). Another reason could be that males, which are more often kept for working purposes than females (P¯eiderer-HoÈgner, 1979), received different training and had other experiences than dogs kept for breeding or as companion or guide dog. Differences between genders may also be affected by the choice of the behavioural traits. In the applied behaviour test, only general and guard dog traits were rated but no traits for companion, hunting or guide dogs. In their study with Labradors, Goddard and Beilharz (1982) found that males were less often rejected for fearfulness and excitability in the training program than females but more for distraction. Wilsson and Sundgren (1997a) showed that GSD and Labrador males were better in courage, prey drive and defence drive. However, they found breed dependent sex differences, e.g. males scored better in nerve stability in GSD but there was no signi®cant difference in Labradors. In ability to cooperate GSD males were better than GSD females, but it was opposite in Labradors, where females scored better.
130 S. Ruefenacht et al. / Applied Animal Behaviour Science 79 (2002) 113±132 Since the number of progeny per dam was low (a mean of 2.2 progeny), maternal effects were not investigated. Furthermore, these effects would probably be completely con- founded with the kennel effects. Wilsson and Sundgren (1998) mentioned that maternal effects are most likely to be found in behaviour characteristics tested at juvenile age and are small or negligible in dogs more than 1 year old. The heritabilities estimated by the different evaluation methods were very similar, which indicate that this genetic parameter was reliably estimated. One exception was observed for reaction to gun®re where the heritability calculated with Gibbs sampling by treating the trait as a categorical one, was much higher (0.42) than with the two other methods (0.23 and 0.24). This discrepancy may be due to the nearly binary character of the trait with 88% of the dogs with the best score of 1 and 10% with a score of 2. The estimated heritabilities were moderate to low, i.e. one cannot expect spectacular genetic improve- ment. Although comparisons between heritability values have to be carried out with care because of differences between de®nitions of the traits, sampling procedures, methods of evaluations, breeds, etc. most of our estimates were similar to those published in the literature (Table 1). Our heritability of self-con®dence (0.18) was very close to the one of Bartlett (1976) (cited in Mackenzie et al., 1986) in American guide dogs (0.16); the same was valid for nerve stability (0.18) where Wilsson and Sundgren (1997a,b) found values of 0.25 and 0.17 for GSD and Labrador, respectively. The latter authors estimated herit- abilities for temperament of 0.15 and 0.10 for GSD and Labradors whereas our estimate was 0.17; Mackenzie et al. (1985), however, found a much higher value of 0.51 in GSD. Wilsson and Sundgren (1997a,b) obtained similar values for hardness (0.15 and 0.20) and sharpness (0.13 and 0.11) in GSD and Labradors as in our study (0.15 and 0.09, respectively) but their heritability estimate for defence drive (0.20 and 0.22) is larger than our value (0.10). All correlations among traits were positive and showed a moderate to high relationship, i.e. all these traits could have, at least to some extent, a common genetic background. This situation facilitates the breeding work because no antagonistic correlations were found. The genetic correlation of 1 between self-con®dence and nerve stability means that the same trait is recorded twice. By looking at the de®nition and the scoring system of self- con®dence and nerve stability, it becomes clear why both traits are so closely related. One of them could easily be removed from the behaviour test without affecting the ef®ciency of the breeding program. Goddard and Beilharz (1982) found genetic correlations of 0.89 between nervousness and sound shy compared with 0.72 between nerve stability and reaction to gun®re in our study. Wilsson and Sundgren (1997a) obtained 0.07±0.31 smaller phenotypic correlations among comparable traits, except the relationship between defence drive and sharpness, which was larger (0.46 and 0.38, respectively). The largest observed difference was between nerve stability and temperament where they found a correlation of 0.03 against 0.52 in our study. These substantial differences between both studies can arise from the different de®nitions of the traits, from the different sampling procedures and from the different methods of evaluation. In contrast to Mackenzie et al. (1985), who estimated a phenotypic correlation of 0.31 between hip dysplasia and temperament, no relationship was found between hip dysplasia and any of the tested traits in our study ( 0.04 to 0.01).
S. Ruefenacht et al. / Applied Animal Behaviour Science 79 (2002) 113±132 131 The modest genetic improvement over the last 25 years in the studbook population of the GSD was partly due to the low heritabilities of the traits, but mainly because of the low selection intensities after the behaviour test (only 8% failed). To be more rigorous at selection is not an evident task, if we keep in mind that other traits had to be considered in the breeding program such as hip dysplasia, body conformation and working tests. Selection could be more rigorous by increasing the number of dogs that attend the behaviour test. A further improvement would be to select the dogs not only on their personal achieved results, but on their breeding values where their own performances and those of all relatives are combined. Modi®cations of the grading system could contribute to better results too. The actual grading is at the same time a rating by giving a score of 1 for the most desirable behaviour. This leads to a quite skewed distribution of the traits, which make genetic evaluation more dif®cult. Instead of classifying the dog's performance on a desirability scale, it could be done on a descriptive scale, e.g. for sharpness: reduced, slightly reduced, optimal, slightly too much, too much. The distribution would become more symmetrical and easier to evaluate. An other open question is, if it would not be more ef®cient to split the actual behaviour test in two distinct parts: one for the general behaviour where dogs' performances are focused on their ability to behave in today's world without endangering or annoying people or other dogs, and another one for working purposes as defence drive and sharpness. References Boldman, K.G., Kriese, L.A., van Vleck, L.D., Kachman, S.D., 1995. A Manual for Use of MTDFREMLÐA Set of Programs to Obtain Estimates of Variances and Covariances. US Department of Agriculture, Agricultural Research Service, University of Nebraska, Lincoln. Falconer, D.S., 1983. Introduction to Quantitative Genetics, 2nd ed. Essex, England. Goddard, M.E., Beilharz, R.G., 1982. Genetics of traits which determine the suitability of dogs as guide-dogs for the blind. Appl. Anim. Ethol. 9, 299±315. Henderson, C.R., 1973. Sire evaluation and genetic trend. In: Proceedings of the Anim. Breed. Genet. in honour of J.L. Lush. ASAS and ADSA, Champaign, IL, pp. 10±41. Hoeschelle, I., Tier, B., 1995. Estimation of variance components of threshold characters by marginal posterior modes and means via Gibbs sampling. Genet. Sel. Evol. 27, 519±540. Hruby, A., 1991. Populationsgenetische Untersuchungen von Leistungs- und Wesensmerkmalen bei Gebrauchshunden. Vet. Med. Diss., University of Veterinary Medicine, Vienna. Janss, L.L.G., 1998. MAGGIC: a package of subroutines for genetic analysis with Gibbs sampling. In: Proceedings of the Sixth World Congress on Genet. Appl. Livest. Prod., vol. 27. UNE, Armidale, NSW, Australia, pp. 459±460. Ledger, R.A., Baxter, M.R., 1997. The development of a validated test to assess the temperament of dogs in a rescue shelter. In: Proceedings of the First International Conference on Veterinary Behavourial Medicine, Birmingham, UK, pp. 87±92. Lower Saxony, 2002. Federal State of Germany, Law/Regulation About Dangerous Animals (Gefahrtier- VerordnungÐGefTVO), http://www.ml.niedersachsen.de/wesenstest.htm (accessed25 February 2002). Mackenzie, S.A., Oltenacu, E.A.B., Leighton, E., 1985. Heritability estimate for temperament scores in German Shepherd dogs and its genetic correlation with hip dysplasia. Behav. Genet. 15, 475±482. Mackenzie, S.A., Oltenacu, E.A.B., Houpt, K.A., 1986. Canine behavioural geneticsÐa review. Appl. Anim. Behav. Sci. 15, 365±395. Moreno, C., Sorensen, D., GarcõÂa-CorteÂs, L.A., Varona, L., Altarriba, J., 1997. On biased inferences about variance components in the binary threshold model. Genet. Sel. Evol. 29, 145±160.
132 S. Ruefenacht et al. / Applied Animal Behaviour Science 79 (2002) 113±132
Mrode, R.A., 1996. Linear Models for the Prediction of Animal Breeding Values. CAB International, Oxon, UK,
pp. 38±40.
Pal, S.K., Ghosh, B., Roy, S., 1999. Inter- and intra-sexual behaviour of free-ranging dogs (Canis familiaris).
Appl. Anim. Behav. Sci. 62, 267±278.
Pfleiderer-HoÈgner, M., 1979. MoÈglichkeiten der ZuchtwertschaÈtzung beim Deutschen SchaÈferhund anhand der
SchutzhundepruÈfung I. Vet. Med. Diss., Ludwig-Maximilian University of Munich.
Planta, D.J.U., Netto, W.J., 1997. Behavioural testing for aggression in the domestic dog. Appl. Anim. Behav.
Sci. 52, 243±263.
Reuterwall, C., Ryman, N., 1973. An estimate of the magnitude of additive genetic variation of some mental
characters in Alsatian dogs. Hereditas 73, 277±284.
Scott, J.P., Fuller, J.L., 1965. Genetics and the Social Behavior of Dog. The University of Chicago Press,
Chicago.
Seiferle, E., Leonhardt, E., 1984. In: Erni, S., Druck, A.G. (Eds.), Wesensgrundlagen und WesenspruÈfung des
Hundes, 2nd ed. Utznacherstr. 3, CH-8722 Kaltbrunn, Switzerland.
Slabbert, J.M., Odendaal, J.S.J., 1999. Early prediction of adult police dog efficiencyÐa longitudinal study.
Appl. Anim. Behav. Sci. 64, 269±288.
Sorensen, D.A., Andersen, S., Gianola, D., Korsgaard, I., 1995. Bayesian inference in threshold models using
Gibbs sampling. Genet. Sel. Evol. 27, 229±249.
van der Borg, J.A.M., Netto, W.J., Planta, D.J.U., 1991. Behavioural testing of dogs in animal shelters to predict
problem behaviour. Appl. Anim. Behav. Sci. 32, 237±251.
Venzl, E., Unshelm, J., Oldigs, B., 1989. Der Campell-test: eine WesenspruÈfung beim Hund, durchgefuÈhrt an der
Rasse Beagle. Kuratorium fuÈr Technik und Bauwesen in der Landwirtschaft, Deutsche VeterinaÈrmedizi-
nische Gesellschaft (Eds.), Aktuelle Arbeiten zur artgemaÈssen Tierhaltung 1989. Darmstadt Giessen,
pp. 134±152.
Wang, C.S., Rutledge, J.J., Gianola, D., 1994. Bayesian analysis of mixed linear models via Gibbs sampling with
an application to litter size in Iberian pigs. Genet. Sel. Evol. 26, 91±115.
Weiss, E., Greenberg, G., 1997. Service dog selection tests: effectiveness for dogs from animal shelters. Appl.
Anim. Behav. Sci. 53, 297±308.
Wells, D.L., Hepper, P.G., 1999. Male and female dogs respond differently to men and women. Appl. Anim.
Behav. Sci. 61, 341±349.
Wilsson, E., Sundgren, P.-E., 1997a. The use of a behaviour test for the selection of dogs for service and
breeding. I. Method of testing and evaluating test results in the adult dog, demands on different kinds of
service dogs, sex and breed differences. Appl. Anim. Behav. Sci. 53, 279±295.
Wilsson, E., Sundgren, P.-E., 1997b. The use of a behaviour test for the selection of dogs for service and
breeding. II. Heritability for tested parameters and effect of selection based on service dog characteristics.
Appl. Anim. Behav. Sci. 54, 233±239.
Wilsson, E., Sundgren, P.-E., 1998. Behaviour test for eight-week-old puppiesÐheritabilities of tested behaviour
traits and its correspondence to later behaviour. Appl. Anim. Behav. Sci. 58, 151±162.
Wright, S., 1934. An analysis of variability in number of digits in an inbred strain of guinea pigs. Genetics 19,
506±536.You can also read
