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Indication of a genetic basis of stereotypies in
ž
laboratory-bred bank voles Clethrionomys
/
glareolus
B. Schoenecker
), K.E. Heller
Zoological Institute, UniÕersity of Copenhagen, TagensÕej 16, Copenhagen N DK-2200, Denmark
Accepted 9 February 2000
Abstract
The development of stereotypies was studied in two successive laboratory-bred generations of
Ž . Ž .
bank voles representing F1 ns248 and F2 ns270 of an originally wild caught stock. It was
shown that the propensity to develop stereotypies under barren housing conditions strongly relates to the same propensity of the parents. Stereotypies were approximately seven times more frequent in the offspring of stereotyping parents than in the offspring of permanent non-stereotypers. This held true even when only one of the parents was stereotyper. The paternal and maternal contributions to stereotypies in the offspring appeared to be equal. Males showing stereotypies but prevented from any physical contact with the offspring were as potent as stereotyping females in producing stereotyping offspring. Moreover, the specific type of stereotypy appearing in the offspring after isolation was very much related to the type of stereotypy developed in the mothers. We found no support for the possible importance of social facilitation from littermates, in that the development of stereotypies was independent of the length of time the voles were kept socially with littermates before isolation. We suggest that the possible genetic basis of individual differences in the propensity to develop stereotypies in captivity may result from differences in genetic predispositions and their interactions with discrete frustrating stimuli early in life andror to genetically different predispositions to cope with frustrating experiences later in life.q2000
Elsevier Science B.V. All rights reserved.
Keywords: Bank vole; Stereotypies; Genetics
)Corresponding author. Tel.:q45-3532-1302; fax:q45-3532-1299.
Ž .
E-mail address: [email protected] B. Schoenecker .
0168-1591r00r$ - see front matterq2000 Elsevier Science B.V. All rights reserved.
Ž .
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1. Introduction
Stereotypies, or stereotypic behaviour, represent a wide range of invariant and
¨
Ž
frequently repeated activities with no obvious goal or function Odberg, 1978; Mason, .
1991a . In humans, stereotypies are associated with schizophrenia, autism and mental Ž
retardation Hutt and Hutt, 1968; Frith and Done, 1990; Bergson et al., 1995; Bodfish et .
al., 1995 . In animals, stereotypic behaviour is commonly seen as the result of caging
Ž .
under barren housing conditions Sørensen, 1987; Mason, 1991a , scheduled or
re-Ž . Ž
stricted feeding Falk, 1969; Lawrence and Terlouw, 1993 , social deprivation Sahakian
¨
. Ž .
et al., 1975 , frustration Feldman, 1978; Odberg, 1978, 1987; Rushen, 1985 , or
Ž .
tethering Cronin et al., 1985 . Psychostimulant drugs which increase brain dopaminer-Ž
gic activity also elicit stereotypies Randrup and Munkvad, 1967; Munkvad et al., 1968; Fog, 1969; Post and Rose, 1976; Cheal et al., 1978; Porsolt et al., 1982; Dantzer, 1986;
.
Walter and Kuschinsky, 1989; Morimasa et al., 1995 . This effect is prevented by Ž
selective inhibition of dopamine receptors Robbins et al., 1990; Mittleman et al., 1991; .
Cabib 1993 , and it is therefore assumed that dopaminergic pathways play an important role in mediating stereotypic behaviour.
Since stereotypies are considered rare in nature, it is generally assumed that animal stereotypic behaviour results from poor coping with the environment and therefore may
Ž
be related to current or early experienced stress Mason, 1991b; Wurbel and Stauffacher,
¨
. Ž .
1997 . Mason 1991b suggests that, instead of reflecting current stress, adult stereotypy performance may be like a ‘‘scar’’ representing a severe problem experienced at the onset of stereotypy development. This view is supported by studies of stereotypy
Ž .
development in bank voles Clethrionomys glareolus reared under barren housing conditions. Bank voles stereotypic behaviour appears related to early experienced maladaptation to environmental conditions in that increasing the size and complexity of
¨
Ž .
the environment reduces the incidence of stereotypies in the voles Odberg, 1987 . Old voles, however, show stronger perseverance of stereotypies than younger voles after
Ž .
environmental enrichment Cooper and Nicol, 1996 . With age, stereotypies may
Ž .
become emancipated from the eliciting stimuli Fentress, 1976, 1977 , and it has been suggested that this could imply that the underlying dopaminergic pathways become
Ž .
sensitised Dantzer, 1986, 1991 .
Although stereotypies appear strongly related to environmental conditions, it is commonly observed that only a proportion of individuals develops stereotypies under identical conditions. This variation may relate to individual differences in response to the eliciting environmental stimuli early in life and in subsequent neuronal sensitisation ŽWurbel and Stauffacher, 1997 .
¨
.The possible relevance of differences in genetic dispositions for the development of stereotypies is obvious, but this aspect has been subjected to only a minimum of
Ž .
scientific attention. Smith 1984 suggests that the occurrence of stereotypies in thor-oughbred racehorses may be of genetic origin, as indicated by stereotyping stallions producing stereotyping offspring. A similar positive correlation between the occurrence
Ž of stereotypies in parents and their offspring has been indicated in other species Kiley,
¨
.1977; Odberg, 1986; Hansen, 1993 . Drug-induced stereotypies have also been shown Ž
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Puglesi-Allegra et al., 1990; Skrinskaya et al., 1992; Tolliver et al., 1994; Golden et al., .
1995; Morimasa et al., 1995; Sluyter et al., 1995; Ballas et al., 1996 .
The literature provides numerable examples on successful selection for normal Ž
behaviour as well as non-stereotypic behavioural disorders e.g. Bruell, 1962; Murphree et al., 1967; Peters et al., 1967; Symons and Sprott, 1976; McCaffrey et al., 1980; . McDonough et al., 1981; Plomin, 1990; Benus et al., 1991; Rosengarten et al., 1994 .
The present study aimed at examining the possible genetic basis of stereotypies in the bank vole. Laboratory- bred, but not wild caught, bank voles housed isolated in barren cages develop high frequencies of locomotor stereotypies, including easily recognisable
¨
Žbackwards somersaulting, jumping, and windscreen wiper movements Odberg, 1986; . Sørensen, 1987; Sørensen and Randrup, 1986; Cooper and Nicol, 1991, 1994 . We
Ž .
repeated this finding in our recent study Schoenecker et al., 2000 on wild caught
Ž . Ž .
Danish voles P: ns92 and their laboratory-bred offspring F1: ns248 . While none of the wild caught voles showed stereotypies under isolation, 74 or 30% of the F1 offspring developed stereotypies at the average age of 96 days. In the present study, voles from the abovementioned F1 generation were chosen for selective matings between non-stereotypers and stereotypers. The subsequent development of stereotypic
Ž .
behaviour in the resulting offspring F2 was then compared with the stereotypy status of their parents when the fathers were removed at the day of delivery. Moreover, we attempted to evaluate a possible influence of social facilitation by keeping the litters together after weaning for variable lengths of time before isolation and relate this to subsequent development of stereotypies.
2. Materials and methods
2.1. Animals, housing and breeding
The animals in the present study consisted of two successive laboratory-bred
genera-Ž . Ž .
tions of bank voles representing F1 ns248 and F2 ns270 of an originally wild caught stock.
Ž .
F1 individuals 138 males and 110 females from 52 different litters were weaned at the age of 36 days and transferred to individual housing in small barren cages of
Ž 3. Ž .
transparent plastic 13.5=16.0=22.5 cm under a 12-h light regime 0800–2000 h . The cages were supplied with a woodcutting bed and the voles had access to food Žstandard rat chow and water ad libitum. Cage cleaning was performed every second. week or when necessary, and a portion of a grain mixture was given when the cages were cleaned.
The animals were kept under these conditions for at least 180 days, except for short breeding sessions. Mating pairs were selected according to the possible four combina-tions of stereotypic or non-stereotypic males and females and transferred to larger
Ž 3.
enriched cages 14.5=21.5=37.5 cm supplied with woodcutting bed, toilet paper and card board rolls. Breeding males were returned to isolation at the day of delivery.
Ž .
The resultant offspring F2 consisted of 138 males and 132 females in 58 different litters. Equal numbers of litters from each of the four possible mating pair combinations
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were either weaned at the age of 20 days and allowed company with their littermates for 12 days before transference to isolation, or they were weaned at the age of 32 days and immediately transferred to isolation. The isolation period for F2 pups lasted until they reached the age of 180 days after which the study was terminated.
2.2. ObserÕations and classification
The occurrence of stereotypic behaviour was examined before and after isolation by one-zero sampling every 15 min for 3–4 h every day during the whole study period. When stereotypies were recognisable, the age and sex of the voles were noted along
Ž . with the type of stereotypy performed. Voles were classified as stereotypers S if individual stereotypic behaviour were noted in bouts of at least five repetitions during the daily observation periods. These bouts, separated by small intervals, could continue Ž . for hours. The classification S covered voles showing backward somersaulting BS ,
Ž . Ž .
high speed jumping JUMP , pacing following a fixed route PF and windscreen wiper
¨
Ž . Ž . Ž .
movements WIN as previously defined by Odberg 1986 , Sørensen 1987 , Sørensen
Ž . Ž .
and Randrup 1986 , and Cooper and Nicol 1991, 1996 . Voles neither showing Ž .
stereotypies nor polydipsia were classified as non-stereotypers N .
At the end of the study, the proportion of voles classified as S and N in F2 was calculated and related to the development of stereotypies in their parents. This allowed investigation of stereotypy development among the offspring of the following four possible F1 mating groups: N male mating N female, S male mating N female, N male mating S female, and S male mating S female. Some voles in F1 developed severe
Ž
polydipsia after delivery and the age of 180 days water intake)21 mlrday vs. .
normally 10 mlrday . The offspring of these voles were omitted from the present study,
Ž .
leaving 187 F2 voles 93 males and 94 females in 42 litters for further data treatment.
2.3. Statistical analyses
Differences in proportions of voles classified as S or N in F1 and F2 were tested by chi square tests using Yates continuity correction factor when n-20. Spearman rank
Ž .
correlation tests corrected for ties were used to estimate effects of isolation age on stereotypies. The chosen significance level was 0.05 and all tests were two-tailed.
3. Results
Table 1 shows the development of stereotypies in F2 voles according to the four F1 mating groups. There was no significant sex effect on stereotypy development in the offspring descending from non-stereotypers or from parents with only one stereotyper. When both parents were stereotypers, however, stereotypies were more frequent in the
Ž .
female than in the male offspring P-0.05 .
The propensity of F2 voles to develop stereotypies was markedly related to the occurrence of stereotypies in their parents. When one or both parents developed stereotypies, 53% of the offspring also developed stereotypies, whereas the same
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Table 1
Ž . Ž . Ž
The number of individuals n F2 , the number of stereotypers n S F2 and the percentage of stereotypers %
.
S F2 in the offspring of the four different mating types in F1
Mating type F1 n F2 n S F2 % S F2 P
Ž .
N male=N female F2 malesqfemales 86 7 8
) ) )
Ž .
S male=N female F2 malesqfemales 11 6 55
) )
Ž .
N male=S female F2 malesqfemales 14 5 36
) ) )
Ž .
S male=S female F2 males 48 23 48
) ) )
Ž .
S male=S female F2 females 28 20 71
) )
Indicates P-0.01 in comparisons of n S F2 with N male=N female. ) ) )
Indicates P-0.001 in comparisons of n S F2 with N male=N female.
proportion was only 8% in the offspring from parents that did not develop stereotypies ŽP-0.01–0.001 . There were no significant differences in the proportions of stereotyp-. ing F2 voles descending from the two different mating groups involving only one stereotyping parent, although stereotyping fathers tended to produce more stereotyping
Ž .
offspring than stereotyping mothers 55% vs. 36% . Two stereotyping parents produced Ž
more stereotypers than mating pairs involving only a single stereotyper P-0.05 for .
female offspring, NS for male offspring .
There was a close relationship between the maternal type of stereotypy developed in F1 and the type of stereotypy developed in the offspring. The two most commonly observed stereotypies were BS and JUMP. In the stereotyping offspring from BS mothers, 94% developed BS and 6% developed JUMP, whereas mothers developing
Ž
JUMP had 83% offspring showing JUMP and 17% showing BS P-0.001 in compari-.
son with preferred stereotypy in the offspring .
There was a non-significant negative correlation between age at isolation and the
Ž .
number of voles developing stereotypies in F2 Ps0.067 , but there was no correlation between the time spent with littermates and subsequent tendencies to develop stereotyp-ies.
4. Discussion
The present study shows that the propensity of laboratory-bred bank voles to develop stereotypies under barren housing conditions is strongly related to the same propensity of their parents. Stereotypies were six to seven times more frequent in the offspring of stereotyping parents than in the offspring of permanent non-stereotypers. This held true even when only one of the parents was a stereotyper. The paternal and maternal contributions to stereotypies in the offspring appeared to be equal. Males showing stereotypies but prevented from any physical contact with the offspring were as potent
Ž as stereotyping females in producing stereotyping offspring, or perhaps more 55% vs.
.
36%, but NS . Moreover, the type of stereotypy appearing in the offspring after weaning and isolation was very much related to the mothers’ type of stereotypy.
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These findings suggest the existence of a genetic basis of stereotypies in laboratory-bred bank voles, although the relevance of social facilitation or other social influences on stereotypy development cannot be ignored. The young voles spent much of their early life with their mothers and littermates. The possible influence of the mothers’ stereotypic behaviour on subsequent stereotypy development in the offspring may, of course, play an important role. If stereotypic behaviour at least partially is influenced by
Ž
frustrating or stressful experiences early in life Mason, 1991b; Wurbel and Stauffacher,
¨
.1997; Schoenecker et al., 2000 , the nursing behaviour and parental care of stereotyping females could be deviant and perhaps frustrating or stressful to the young voles. Permanent non-stereotyping females, however, also produced stereotypic offspring when mated with a stereotyping male and that to at least the same extent as stereotyping females mated with non-stereotyping males. A possible explanation is that stereotyping males may affect the female during mating and pregnancy so that she will show deviant and stereotypy-inducing behaviour towards her offspring. The finding that the voles tend to perform the same type of stereotypy as their mothers adds to the possible relevance of social influence on the more accurate shaping of stereotypies. The possible importance of social influences from the parents on stereotypy development, however, needs to be examined by careful comparisons of the females’ behavioural responses to stereotyping and non-stereotyping males and by comparing other possible behavioural differences among stereotyping and permanent non-stereotyping females independently of stereo-typy status of the males.
Social facilitation effects from littermates on stereotypy development could also play a role. But since no correlation was found between the length of time spent socially with littermates after weaning but before isolation and the tendency to develop stereotypies, we find no support of the importance of such a social facilitation effect. There were no differences in litter size produced by the different mating groups in the present study, and this seems to rule out the possibility of a stereotypy-inducing effect of pre-weaning
Ž . social stress as suggested by Hansen 1993 .
Matings between stereotyping males and stereotyping females resulted in approxi-mately 50% stereotyping offspring. This relatively low penetrance of a behavioural trait, if genetically determined, is not unusual since genetic variance rarely accounts for more
Ž .
than the half of behavioural variance Plomin, 1990 . A more detailed genetic analysis, however, requires the establishment of pure-bred stereotypers and non-stereotypers, a recombinant F1 strain, a segregated F2 strain, reciprocal backcrosses with pure-bred strains, and studies of the behavioural development in voles reared by different combinations of foster mothers.
It is relevant to discuss why none of the originally wild caught P individuals developed stereotypies in captivity. Three explanations have previously been suggested: Ž .1 wild caught voles do not develop a locomotor response to captivity Cooper andŽ
. Ž . Ž
Nicol, 1996 ; 2 they are less prone to develop novel responses to external cues Cooper . Ž .
and Nicol, 1996 ; and 3 the stereotypic response to captivity takes several generations
Ž .
to develop Sørensen and Randrup, 1986 . We suggest that the lack of stereotypy development in wild caught voles may relate to the lack of frustrating or stressful experiences among young voles in the wild. This interpretation is partially supported by the finding that environmental enrichment of the cage milieu reduces the perseverance
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Ž of stereotypies in young, but not to the same extent in old laboratory-bred voles Cooper
.
and Nicol, 1996 . When cleaning the cages in the present study, it was necessary to transfer the animals from their home cages with old woodcut bedding to cages with new bedding material. During this process, young voles responded almost immediately by showing non-stereotyped jumping movements in the cage corners or against the cage walls in both old and new cages. Non-stereotyping older voles responded with digging in the new bedding material while stereotyping voles exhibited their preferred stereo-typy. The jumping responses of the young voles occurred in the breeding cages as well as after isolation. Non-stereotyped jumping in young voles may be interpreted as unsuccessful attempts to escape during disturbance, and the lack of a successful outcome of an otherwise adequate escape response could be the source of subsequent stereotypic
¨
Ž .
behaviour as also suggested by Odberg, 1986 . If so, stereotypic behaviour already developed may be elicited at least partially by the same circumstances that originally caused their development, but in addition that stereotypies also may occur in other contexts. It could be that these other contexts share the common frustrating feature of unsuccessful results of otherwise adequate behavioural responses, such as frustrating effects of social deprivation.
The possible genetic basis of individual differences in the propensity to develop stereotypies in captivity may thus relate to differences in genetic predispositions and their interactions with discrete frustrating stimuli early in life andror to genetically different predispositions to cope with frustrating experiences later in life.
Acknowledgements
The Danish Natural Science Research Council supported this study.
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Ž .
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were either weaned at the age of 20 days and allowed company with their littermates for 12 days before transference to isolation, or they were weaned at the age of 32 days and immediately transferred to isolation. The isolation period for F2 pups lasted until they reached the age of 180 days after which the study was terminated.
2.2. ObserÕations and classification
The occurrence of stereotypic behaviour was examined before and after isolation by one-zero sampling every 15 min for 3–4 h every day during the whole study period. When stereotypies were recognisable, the age and sex of the voles were noted along
Ž .
with the type of stereotypy performed. Voles were classified as stereotypers S if individual stereotypic behaviour were noted in bouts of at least five repetitions during the daily observation periods. These bouts, separated by small intervals, could continue
Ž .
for hours. The classification S covered voles showing backward somersaulting BS ,
Ž . Ž .
high speed jumping JUMP , pacing following a fixed route PF and windscreen wiper
¨
Ž . Ž . Ž .
movements WIN as previously defined by Odberg 1986 , Sørensen 1987 , Sørensen
Ž . Ž .
and Randrup 1986 , and Cooper and Nicol 1991, 1996 . Voles neither showing
Ž .
stereotypies nor polydipsia were classified as non-stereotypers N .
At the end of the study, the proportion of voles classified as S and N in F2 was calculated and related to the development of stereotypies in their parents. This allowed investigation of stereotypy development among the offspring of the following four possible F1 mating groups: N male mating N female, S male mating N female, N male mating S female, and S male mating S female. Some voles in F1 developed severe
Ž
polydipsia after delivery and the age of 180 days water intake)21 mlrday vs.
.
normally 10 mlrday . The offspring of these voles were omitted from the present study,
Ž .
leaving 187 F2 voles 93 males and 94 females in 42 litters for further data treatment. 2.3. Statistical analyses
Differences in proportions of voles classified as S or N in F1 and F2 were tested by chi square tests using Yates continuity correction factor when n-20. Spearman rank
Ž .
correlation tests corrected for ties were used to estimate effects of isolation age on stereotypies. The chosen significance level was 0.05 and all tests were two-tailed.
3. Results
Table 1 shows the development of stereotypies in F2 voles according to the four F1 mating groups. There was no significant sex effect on stereotypy development in the offspring descending from non-stereotypers or from parents with only one stereotyper. When both parents were stereotypers, however, stereotypies were more frequent in the
Ž .
female than in the male offspring P-0.05 .
The propensity of F2 voles to develop stereotypies was markedly related to the occurrence of stereotypies in their parents. When one or both parents developed stereotypies, 53% of the offspring also developed stereotypies, whereas the same
(2)
Table 1
Ž . Ž . Ž
The number of individuals n F2 , the number of stereotypers n S F2 and the percentage of stereotypers % .
S F2 in the offspring of the four different mating types in F1
Mating type F1 n F2 n S F2 % S F2 P
Ž .
N male=N female F2 malesqfemales 86 7 8
) ) )
Ž .
S male=N female F2 malesqfemales 11 6 55
) )
Ž .
N male=S female F2 malesqfemales 14 5 36
) ) ) Ž .
S male=S female F2 males 48 23 48
) ) ) Ž .
S male=S female F2 females 28 20 71
) )
Indicates P-0.01 in comparisons of n S F2 with N male=N female. ) ) )
Indicates P-0.001 in comparisons of n S F2 with N male=N female.
proportion was only 8% in the offspring from parents that did not develop stereotypies
ŽP-0.01–0.001 . There were no significant differences in the proportions of stereotyp-.
ing F2 voles descending from the two different mating groups involving only one stereotyping parent, although stereotyping fathers tended to produce more stereotyping
Ž .
offspring than stereotyping mothers 55% vs. 36% . Two stereotyping parents produced
Ž
more stereotypers than mating pairs involving only a single stereotyper P-0.05 for
.
female offspring, NS for male offspring .
There was a close relationship between the maternal type of stereotypy developed in F1 and the type of stereotypy developed in the offspring. The two most commonly observed stereotypies were BS and JUMP. In the stereotyping offspring from BS mothers, 94% developed BS and 6% developed JUMP, whereas mothers developing
Ž
JUMP had 83% offspring showing JUMP and 17% showing BS P-0.001 in
compari-.
son with preferred stereotypy in the offspring .
There was a non-significant negative correlation between age at isolation and the
Ž .
number of voles developing stereotypies in F2 Ps0.067 , but there was no correlation between the time spent with littermates and subsequent tendencies to develop stereotyp-ies.
4. Discussion
The present study shows that the propensity of laboratory-bred bank voles to develop stereotypies under barren housing conditions is strongly related to the same propensity of their parents. Stereotypies were six to seven times more frequent in the offspring of stereotyping parents than in the offspring of permanent non-stereotypers. This held true even when only one of the parents was a stereotyper. The paternal and maternal contributions to stereotypies in the offspring appeared to be equal. Males showing stereotypies but prevented from any physical contact with the offspring were as potent
Ž
as stereotyping females in producing stereotyping offspring, or perhaps more 55% vs.
.
36%, but NS . Moreover, the type of stereotypy appearing in the offspring after weaning and isolation was very much related to the mothers’ type of stereotypy.
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These findings suggest the existence of a genetic basis of stereotypies in laboratory-bred bank voles, although the relevance of social facilitation or other social influences on stereotypy development cannot be ignored. The young voles spent much of their early life with their mothers and littermates. The possible influence of the mothers’ stereotypic behaviour on subsequent stereotypy development in the offspring may, of course, play an important role. If stereotypic behaviour at least partially is influenced by
Ž
frustrating or stressful experiences early in life Mason, 1991b; Wurbel and Stauffacher,
¨
.
1997; Schoenecker et al., 2000 , the nursing behaviour and parental care of stereotyping females could be deviant and perhaps frustrating or stressful to the young voles. Permanent non-stereotyping females, however, also produced stereotypic offspring when mated with a stereotyping male and that to at least the same extent as stereotyping females mated with non-stereotyping males. A possible explanation is that stereotyping males may affect the female during mating and pregnancy so that she will show deviant and stereotypy-inducing behaviour towards her offspring. The finding that the voles tend to perform the same type of stereotypy as their mothers adds to the possible relevance of social influence on the more accurate shaping of stereotypies. The possible importance of social influences from the parents on stereotypy development, however, needs to be examined by careful comparisons of the females’ behavioural responses to stereotyping and non-stereotyping males and by comparing other possible behavioural differences among stereotyping and permanent non-stereotyping females independently of stereo-typy status of the males.
Social facilitation effects from littermates on stereotypy development could also play a role. But since no correlation was found between the length of time spent socially with littermates after weaning but before isolation and the tendency to develop stereotypies, we find no support of the importance of such a social facilitation effect. There were no differences in litter size produced by the different mating groups in the present study, and this seems to rule out the possibility of a stereotypy-inducing effect of pre-weaning
Ž .
social stress as suggested by Hansen 1993 .
Matings between stereotyping males and stereotyping females resulted in approxi-mately 50% stereotyping offspring. This relatively low penetrance of a behavioural trait, if genetically determined, is not unusual since genetic variance rarely accounts for more
Ž .
than the half of behavioural variance Plomin, 1990 . A more detailed genetic analysis, however, requires the establishment of pure-bred stereotypers and non-stereotypers, a recombinant F1 strain, a segregated F2 strain, reciprocal backcrosses with pure-bred strains, and studies of the behavioural development in voles reared by different combinations of foster mothers.
It is relevant to discuss why none of the originally wild caught P individuals developed stereotypies in captivity. Three explanations have previously been suggested:
Ž .1 wild caught voles do not develop a locomotor response to captivity Cooper andŽ
. Ž . Ž
Nicol, 1996 ; 2 they are less prone to develop novel responses to external cues Cooper
. Ž .
and Nicol, 1996 ; and 3 the stereotypic response to captivity takes several generations
Ž .
to develop Sørensen and Randrup, 1986 . We suggest that the lack of stereotypy development in wild caught voles may relate to the lack of frustrating or stressful experiences among young voles in the wild. This interpretation is partially supported by the finding that environmental enrichment of the cage milieu reduces the perseverance
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Ž
of stereotypies in young, but not to the same extent in old laboratory-bred voles Cooper
.
and Nicol, 1996 . When cleaning the cages in the present study, it was necessary to transfer the animals from their home cages with old woodcut bedding to cages with new bedding material. During this process, young voles responded almost immediately by showing non-stereotyped jumping movements in the cage corners or against the cage walls in both old and new cages. Non-stereotyping older voles responded with digging in the new bedding material while stereotyping voles exhibited their preferred stereo-typy. The jumping responses of the young voles occurred in the breeding cages as well as after isolation. Non-stereotyped jumping in young voles may be interpreted as unsuccessful attempts to escape during disturbance, and the lack of a successful outcome of an otherwise adequate escape response could be the source of subsequent stereotypic
¨
Ž .
behaviour as also suggested by Odberg, 1986 . If so, stereotypic behaviour already developed may be elicited at least partially by the same circumstances that originally caused their development, but in addition that stereotypies also may occur in other contexts. It could be that these other contexts share the common frustrating feature of unsuccessful results of otherwise adequate behavioural responses, such as frustrating effects of social deprivation.
The possible genetic basis of individual differences in the propensity to develop stereotypies in captivity may thus relate to differences in genetic predispositions and their interactions with discrete frustrating stimuli early in life andror to genetically different predispositions to cope with frustrating experiences later in life.
Acknowledgements
The Danish Natural Science Research Council supported this study.
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