Biological Journal of the Linnean Society (1990) 41: 257-269
Variation in aggressiveness in house mouse
populations
PAUL F. BRAIN
Biological Sciences, University College of Swansea, SA2 8PP, Wales
AND
S T E F A N 0 PARMIGIANI
Istituto di Zoologia, Universitri degli Studi di Parma, 43100 Parma, Italy
Clearly the ability of ‘house mice’ to vary their social structures is an important feature contributing
to their success in a wide range of habitats. Social structure is strongly influenced by aggressiveness
and other behaviours in male and female mice. Material is presented illustrating how genotype,
intrauterine location and social experiences influence dyadic encounters in this ‘species’.
KEY WORDS:-House
structure.
mouse - aggressiveness - genes - intrauterine location - experience
CONTENTS
Introduction . . . . . . . . . . . . .
Genetic influences on ‘social aggression’ in male mice .
. .
Material and methods . . . . . . . . . . .
Husbandry . . . . . . . . . . . .
Behavioural tests . . . . . . . . . . .
Results
. . . . . . . . . . . . . .
Individually housed male ‘residents’ us. ‘TO’ strain intruders
Individually housed male ‘residents’ us. like-strain intruders.
Responses of intruders to residents . . . . . . .
. . . . . .
‘Female aggression’ and social structure
Intrauterine location phenomena . . . . . . . .
Effects of prior social experiences on individual aggressiveness .
Concluding comments . . . . . . . . . . .
Acknowledgements
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References.
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social
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INTRODUCTION
Competition for space, mates, social status and resources is a n almost
ubiquitous phenomenon in the Animal Kingdom. Intraspecific aggression
crucially shapes social structure and spatial distribution of conspecifics via
territorial and/or of migratory responses (Van Oortmerssen & Busser, 1989).
0024-4066/90/090257
+ 13 S03.00jO
257
01990 The Linnean
Society of London
258
P. F. BRAIN AND S. PARMIGIANI
Understanding relationships between aggressiveness and distribution may o n b
be currently possible in the house mouse. The ‘house mouse’ is clearly a very
divergent ‘species’, essentially consisting of a group of seven recognized species,
numerous subspecies and several chromosomal races. This highly opportunistic
animal flourishes in environments as diverse as fields, cold stores, warehouses,
hayricks, Pacific atolls and islands close to Antartica. Individuals may be largely
surface-dwelling or inhabitants of complex burrow systems. Different
populations of mice, at different locations and a t varied times within the same
location, exhibit different social organizations (e.g. male territoriality and
hierarchial groups). Such organizations (which often seem suited to prevailing
local conditions of food distribution, available cover and animal density)
generally reflect variations in female and male aggressiveness. Genetic
endowment, intrauterine location and experience give rise to individual
differences in murine aggressiveness which could underpin variations in the
probability of assuming particular social structures. Different behavioural
phenotypes may be suited to different phases of the population ‘cycle’ seen in
such animals.
GENETIC INFLUENCES ON ‘SOCIAL AGGRESSION’ IN MALE MICE
Attack and threat may serve different functions. Fighting and threat may be
employed in offence or defence (both personal or of a nest site or parental
investment) in such animals. These activities may also be used to assess fitness of
potential mates.
Over 200 strains of inbred laboratory mice offer unique opportunities to assess
whether laboratory tests of ‘aggression’ actually measure the same attribute.
This has been doubted (see Brain, 1989); indeed preliminary accounts suggest
that such tests assess mixtures of offensive, defensive and (in some cases)
predatory motivations (Mainardi et al., 1986; Jones & Brain, 1987). More
detailed measures of behaviour in murine ‘social aggression’ encounters in which
the genotype of the resident and of the intruder are varied are reported here.
Using an ‘ethoexperimental’ approach (Brain, 1989) one can distinguish
variations of aggressiveness from changes in attack mediated by differences in
sociability or fearfulness and/or altered in social communication.
MATERIAL AND METHODS
Husbandry
Outbred albino, Tuck Ordinary (‘TO’) and Swiss-Webster and inbred
NZW/Ola, BALB/c, C57BL/10, DBA/2, CBA/Ca and C3H/He stocks were used
in this study. All animals were bred and housed in the Animal Facility of the
University College of Swansea under standardized housing and rearing
conditions (see Jones, 1983).
Behavioural tests
Intermale fighting induced by individual housing (otherwise known as ‘social
aggression’) is the most investigated form of ‘aggression’ in laboratory rodents, is
AGGRESSIVENESS I N THE HOUSE MOUSE
259
reliably generated in many strains and is comparable to behaviour seen in
natural populations (Corti et al., 1989). One week after weaning, males of each
line were individually housed for 28 days. Each ‘resident’ had a single 10-minute
home cage encounter with an anosomic (largely lacking a sense of smell) grouphoused male ‘intruder’. Such opponents elicit attack but rarely initiate such
behaviour or retaliate when attacked (Brain & Al-Maliki, 1978). Male residents
encountered a ‘TO’ strain intruder or an intruder of their own strain (detailed
results are only given for the former). Tests took place during the ‘dark’ phase of
the light cycle under dim, red lighting (c. 9 lux) using transparent cage-lids to
facilitate videotaping. There were 8- 12 animals per observation category.
Tapes were transcribed as durations of some 45 behavioural components
(defined in Brain, McAllister & Warmsley, 1989). Elements were assigned (on
the basis of sequence analysis) to broad categories of activity (see Brain et al.,
1989) and times allocated by experimental subjects to categories summed.
Encounters between individually housed males and ‘TO’ or same-strain
opponents were examined because:(i) some attack behaviour was evident in most strains;
(ii) this was the only form of aggression examined in all strains using both
‘TO’ and same-strain opponents;
(iii) videotape recordings of encounters involving individually-housed males
could be analysed en masse increasing observer reliability.
RESULTS
Durations of broad categories of activity are tabulated as medians, with ranges
in parentheses. The data refer to all animals tested, irrespective of whether they
showed overt attack.
Individually housed male ‘residents’ vs. ‘TO’ strain intruders
Table 1 lists times allocated to behaviours in individually housed males of the
strains in response to TO standard opponents. Interestingly, durations of
‘aggression’ (comprising e.g. ‘chase’, ‘tail rattle’, ‘biting attack’ and threat
postures) do not show a consistent relationship to the more conservative measure
of accumulative attacking time (i.e. number of seconds allocated to biting attack
on the ‘standard opponent) across strains. Perhaps proportions of overt attack to
other components of aggressive behaviour (e.g. threat postures) vary from strain
to strain?
Overt attack was not associated with particular distributions of other broad
activities. For example, DBA/2 and C3H/He males showed very different levels
of attack but similar durations of social behaviour. Other strains showing levels
of attack greater than those of DBA/2 males (i.e. T O , Swiss and C57BL/10) have
lower incidences of social behaviour. The ‘non-aggressive’ CBA/Ca and C3H/He
strains, although showing comparable levels of social and non-social behaviour,
have very different durations of defence and immobility.
Higher levels of social behaviour were, however, generally associated with
reduced defence. Such associations indicate ‘tolerant’ residents, since defence is
often evoked by the intruder’s behaviour (e.g. reciprocated social investigation)
P. F. BRAIN AND S. PARMIGIANI
260
TABLE
1. Durations of activities shown by individually-housed male residents in encounters with
‘TO’ strain intruders
Strain of
resident
Category of activity
Social sexual
TO
SWISS
NZWjO 1a
BALB/c
C57BL/IO
DBA/2
CBA/Ca
C3H/He
179.7
(74.0-460.4)
188.5
(123.6-388.4)
291.1
(114.2-413.6)
149.2
(46.5-223.3)
177.6
( 1 17.4-33 1.O)
321.9
(231.5-422.0)
241.9
(168.3-47 1.4)
360.8
(227.6-462.4)
Active non-social
Immobile
Aggression
Defence/flight
239.9
45.1
(0.4-72.4)
35.4
(8.1-99.6)
19.5
(3.6-53.6)
101.5
(51.3-242.5)
24.6
(5.6-41.9)
30.2
(2.5-188.6)
53.3
(15.4-139.1)
37.3
( 7.3-88.4)
61.0
(2.1-105.0)
49.9
(5.6-158.0)
7.6
(4.8-14.0)
10.7
(3.6-36.5)
7.3
(1.8-14.5)
13.6
(5.1-33.2)
15.9
(1 .l-70.2)
1.1
(0.0-32.6)
35.8
(4.9-59.2)
4.8
(2.0-1 1.8)
11.4
(5.3-2 1.3)
( 108.3-424.3)
308.6
(162.6-335.0)
219.0
(150.2-360.6)
251.1
( 148.7-343.9)
306.1
(230.6-424.4)
218.8
(146.4-304.9)
280.0
(8 1.6-357.2)
210.9
( 1 18.0-333.0)
20.2
(5.9-160.2)
11.2
(3.0-15.3)
15.7
(6.1-38.1)
16.6
(1 1.9-34.4)
9.4
(6.0-29.1)
during periods of close physical contact (recorded as ‘social’ activity). Using this
line of reasoning, C3H/He and BALB/c residents are respectively the most and
least ‘tolerant’ to TO opponents. Significant strain differences were evident in
durations of social and defence but not non-social behaviour. Differences in
‘aggression’ durations largely reflected strain differences in the incidence and
intensity of attack fJones & Brain, 1987). The most obvious strain difference,
however, concerns the extremely high levels of immobility shown by BALB/c
males. Blanchard & Blanchard (1989a, b) interpret immobility as indicative of
‘fear’; others suggest it represents passive avoidance. If one applies the latter
interpretation, BALB/c males ‘passively avoid’ their opponent when not
engaged in attack. Van Oortmerssen (1971) suggested that extremes of
avoidance and defence (also of long duration in this line) might typify a strain
descended from surface-living (c.f. burrow-living) ancestors, which could not
easily hide from an aggressor and would be forced to flee. Since ‘crouching’ and
‘freezing’ (components of immobility) have been interpreted (Grant, 1963) as
responses of animals prevented from fleeing by the cage’s physical restrictions,
the immobility of BALB/c mice seems consistent with thwarted flight and hence
with a surface-living ancestry.
Individually housed male ‘residents’ vs. like-strain intruders
Most of the conclusions reached above concerning strain differences in
behavioural characteristics were confirmed when using like-strain opponents
(consequently, these data are not given in detail). Some differences in the
resident’s behaviour may be, at least in part, consequences of the opponent’s
behaviour. Responses of opponents to a given ‘behavioural stimulus’ of a resident
may be determined by many factors, e.g. including the genotype and previous
experience of that opponent. For example, C57BL mice (Van Oortmerssen,
1971) and juvenile TO males (Brain et al., 1981) tend to flee rather than assume
AGGRESSIVENESS IN THE HOUSE MOUSE
26 1
defensive postures in response to being bitten. Since attacking mice frequently
chase fleeing opponents (Childs, 1979), ‘strain differences’ in chasing by
residents might simply reflect variability in fleeing by opponents. To detect
behaviour which is ‘typical’ of a resident strain therefore, one should seek
features which are consistent across different types of opponent. As BALB/c mice
showed immobility in both situations, this may be ‘characteristic’ of this strain.
Similarly, high levels of social behaviour seem typical of isolated C3H/He males.
All resident strains (except C3H/He) showed more defence against TO than
like-strain opponents; significantly so in five out of eight strains. Perhaps TO
opponents have a strong tendency to reciprocate social investigation during
periods of physical contact with the resident and hence stimulate more defence?
Alternatively, residents may be more generally ‘tolerant’ of opponents of their
own strain. Comparing social behaviour of TO and same-strain intruders does
not resolve this issue, since the recorded durations are similar. Perhaps the social
behaviour of TO intruders differs in composition from that of like-strain intruders
e.g. involving more physical contact, such as grooming? Same-strain intruders,
conversely, might engage in activities such as ‘attend’, which involve no direct
contact with residents and are unlikely to stimulate defence. General
assumptions that similar durations of activity reflect similar responses to
particular experimental situations are unjustified where the composition of
individual components is unknown. This is a common omission in investigations
employing this type of measure, however such studies are still more informative
than those which simply utilize measures of attack.
Responses of intruders to residents
Table 2 provides data for responses of TO intruders to different residents.
Comparisons of opponent behaviour in encounters with particular strains of
resident may suggest which behaviours are ‘typical’ of the resident strain. For
example, immobility is particularly evident in the opponents of NZW/Ol a
residents. Grant (1963) noted that ‘crouch’ (the major contributor to
immobility) is a frequent response to being groomed. One might, therefore,
reasonably predict high levels of grooming of their opponents by NZW/Ol a
residents (as is the case). ‘Crouch’ is shown by animals when their movement is
restricted by highly ‘aggressive’ residents. Opponents exposed to other residents
as aggressive as NZW/Ola males (e.g. Swiss) do not, however, show this degree
of immobility. The durations of defence shown by opponents are roughly
proportional to the amount of overt attack received. Durations of defence are,
however, disproportionately high in both the TO and same-strain intruders
encountering Swiss and NZW/Ol a residents. I n particular, the ratio of passive
(rigidly-held defence postures) to active (e.g. flight and kicking) defence is high
in these opponents. Perhaps more damage is inflicted by bites delivered by these
residents stimulating more extreme defence? The ratio of passive : active defence
is low in the remaining strains of opponents and especially in the case of
C57BL/10 intruders, where it indicates a greater tendency for flight (see Van
Oortmerssen, 1971). Irrespective of their strain or the strain of the resident
encountered, opponents showed elevated non-social behaviour (largely cageexploration) and reduced social behaviour and aggression (certainly involving
no overt attack).
P. F. BRAIN AND S. PARMIGIANI
262
TABLE
2. Durations of activities shown by ‘TO’ strain intruders in encounters with individuallyhoused male residents
Strain of
resident
Category of activity
Social sexual
14.1
(7.4-27.3)
23.1
SWISS
(9.8-28.1)
12.7
NZW/OlOa
(8.8-42.1)
23.8
BALB/C
(13.6-116.1)
16.0
C57BL/10
( 12.9-25.0)
12.5
DBA/P
(9.9-16.5)
13.2
CBA/Ca
(9.6-17.0)
14.0
C3H/He
(6.0-79.7)
TO
Active
non-social
Immobile
Aggression
Active
defencelflight
Passive
defence
458.4
(161.7-587.0)
383.1
(156.6-562.7)
332.9
(79.9-542.2)
514.9
(283.1-583.2)
37.7
(2.6-167.0)
79.0
(0.4-1 11.1)
126.5
(39.2-223.9)
12.2
(0.0-165.0)
0
(0.0-1.0)
0
(0.0-111.1)
16.6
(0.2-245.0)
66.3
(13.5-192.2)
477.2
(183.9-585.1)
486.5
(323.2-586.3)
581.5
(395.7-589.3)
533.4
(430.5-585.5)
13.8
( 1.2-63.7)
0
(0.0-1 16.5)
33.5
(0.0-181.4)
60.2
(0.0-217.9)
0
(0.0-96.7)
0
(0.0-124.8)
6.4
(0.0-37.9)
0
59.6
(2.0-163.5)
2.9
(0.9-192.4)
23.9
( 1.3-155.1)
0
(0.0-0.6)
0
(0.0-7.6)
0
(0.0-0.3)
0.1
(0.0-2.8)
0
(0.0-0.7)
0
(0.0-0.4)
52.2
(7.1-209.9)
57.1
(0.0-13 1.4)
58.8
(0.0-2 13.9)
31.7
(0.3-51.0)
1.1
(0.3-7.3)
2.1
(0.0-3.4)
(0)
0
(0)
‘FEMALE AGGRESSION’ AND SOCIAL STRUCTURE
Female mice were thought to attack conspecifics only when performing
parental care (i.e. maternal aggression), a behaviour protecting the young
(Ostermeyer, 1983). T h e mother’s attack is uninhibited, with bites to the most
vulnerable regions (i.e. head, ventral and inguinal areas, see Fig. 1) of the
intruders (Brain, 1981). As a consequence, aggression in lactating mice is termed
‘defensive’ to distinguish it from the ‘offensive’ behaviour of males in which the
topography of biting attack rarely involves vulnerable body regions.
Nevertheless, recent studies using Swiss albinos suggest that maternal aggression
is a heterogeneous phenomenon ranging from offensive to defensive attack.
These different patterns of attack are generated when lactating females
encounter females in the same condition, sexually naive males or virgin female
intruders (Parmigiani et al., 1988a). Sexually naive males are particularly
subjected to intense defensive attack whereas virgin and lactating female
intruders are attacked offensively. ‘Fear’ is also more characteristic of lactating
females responding to strange males (Parmigiani et al., 1988a). Studies with the
opiate antagonist naloxone (Parmigiani et al., 198813) and the antiaggressive
drug Fluprazine (Parmigiani et al., 1989) also suggest that maternal attack on
female and male intruders tap different neural substrates. Indeed, the female’s
attack on males may serve a sexual selection function (Parmigiani, 1989).
Comparing maternal aggression among the different lines and strains shows
that this form of attack usually covaries with the level of intrasexual aggression
and infanticide by males (Parmigiani, 1989), suggesting that aggressive
behaviour in the two sexes is controlled by the same autosomal genes (St. John &
Corning, 1973). Female aggression is not, however, restricted to the lactation
period and pup defence. I n fact, females become aggressive towards conspecifics
AGGRESSIVENESS IN THE HOUSE MOUSE
263
Figure 1 . Lateral view of a mouse in a defence posture showing the location of the bite targets. The
unshaded areas (basically the head and the ventral surface) are the regions animals are inhibited from
biting in offensive attack. In defensive attack, animals show a rather random distribution of bites.
(especially adult females) when associated with a territorial male. Virgin Swiss
albino females individually housed for 24 hours in cages previously inhabited by
a male, exhibit increased levels of attack and mounting-like behaviour towards
same sex intruders cf. counterparts isolated in cages containing clean sawdust.
Consequently, male urinary odour may stimulate female intrasexual aggression.
This observation suggests that inter-female attack may be a form of territorial
aggression and may also be important in population dynamics.
INTRAUTERINE LOCATION PHENOMENA
The intrauterine location phenomenon is a further source of variance in
aggressiveness. It is a naturally occurring consequence of foetuses being
positioned randomly next to others of the same or opposite sex, in mammals that
produce multiple offspring, e.g. mice, rats and hamsters. Fifty percent of the
offspring of such animals are I M (being located between male and female
foetuses), 25% 2M (being located between two males) and 25% O M (being
located between two females) (Vom Saal, 1981). Mice at the ends of a row are
simply classified with respect to their nearest partner so can only be OM or l M ,
but it is recognized that such animals occupy an unusual position. Male and
female mouse foetuses secrete differing titres of steroid hormones during the
prenatal period. Steroids secreted by one foetus seem to be transmitted to
contiguous foetuses by unknown mechanisms where they modify development in
a predictable manner.
Numerous comparisons of male and female mice from different intrauterine
positions have revealed radical differences in morphology, physiology and
behaviour (reviewed in Vom Saal, 1989). Many comparisons have used only OM
and 2M individuals, since, in all studies in which OM individuals have been
investigated, they are intermediate between OM and 2M individuals (Vom Saal,
1981).
For example, comparison of female mice differing in their in utero proximities
to males, reveals varied degrees of masculinization (Meisel & Ward, 1981; Vom
Saal & Bronson, 1978). Most studies have concerned the ontogeny of copulatory
behaviour. Fewer studies have addressed the role of sex steroid exposure during
perinatal life on other activities, such as infanticide, intersexual aggression,
postpartum aggression and social interaction (Vom Saal, 1989).
264
P. F. BRAIN AND S. PARMIGIANI
2M female mice are more aggressive towards female intruders than OM
counterparts regardless of the hormonal state a t the time of testing. Activation
by a specific hormone appears unnecessary to observe such aggression (Vom
Saal, 1983a). OM females, in contrast, display more active avoidance in
adulthood than 2M counterparts (Hauser & Gandelman, 1983).
Following castration at birth, 2M CF1 male mice, exhibited inter-male
aggression after 16 days of testosterone treatment, while OM males showed no
aggression after this duration of treatment (Vom Saal et al., 1983), indicating
that adult 2M males are the more sensitive to the ‘activational effects’ of
testosterone on the neural substrate. Studies of gonadally-intact male mice with
newborn young showed that most 2M males exhibited parental behaviour,
whereas most OM males exhibited infanticide (Vom Saal, 1983b). Obviously, the
intrauterine position phenomenon is capable of producing phenotypic variation
in the behaviour of male and female rats and mice, as are changes in gene
frequency. These changes would not require microevolution. There has been
considerable speculation about the impact of different behavioural phenotypes
especially in mice with their
in naturally-occurring mammal populations
cycles of ‘plagues’ and ‘crashes’.
~
EFFECTS OF PRIOR SOCIAL EXPERIENCES ON INDIVIDUAL AGGRESSIVENESS
Prior social experiences can also affect the natural propensity for individuals
to show aggressive responses. In spite of this, the impact of winning or losing
encounters on subsequent performance in laboratory mice has not been
systematically studied.
Andrade, Kamal & Brain (1989) showed that Swiss mice that had repeatedly
defeated conspecifics in daily tests, attack and threaten intruders in subsequent
encounters to a greater extent than counterparts without positive fighting
experience. The most marked changes in aggressive behaviour occurred between
the first and second daily test, there being little further change between the
second the fifth test. Latency to first attack significantly declined, whereas
numbers of attacks, as well as times allocated to attacking and threatening
significantly increased over consecutive tests. The detailed ethological analysis
confirmed that other behavioural consequences of repeated experience were
evident. Social investigatory behaviour and timid/defensive behaviour decreased
as mice spent more time attacking. Although aggression was the focus of the
study, these additional alterations may be important for interpreting the effects
of experience. Brazin & Al-Maliki (1978) also showed that repeated exposure to
male conspecifics is sufficient to elevate offensive behaviour in mice. Such
experience is superior to individual housing in producing sustained attack,
although isolates attack as readily as males which have had prior experience
with intruders in fights.
Strange or unfamiliar objects (Barnett, 1975) elicit fear in rats. Avoidance of
unfamiliar objects is most pronounced when the object is encountered in a
familiar place, such as the home-cage (Cowan & Barnett, 1975). Eventually,
however, rodents attend to such items for extended periods, a response obtained
even if the object has generated pain on previous occasions. Subjects also
frequently sniff and contact such items (Lore, Nikoletseas & Takahashi, 1984).
As an intruder is, in a sense, a strange object, one might expect its presence to
AGGRESSIVENESS IN THE HOUSE MOUSE
265
elicit ‘fear’ in the resident. Blanchard & Blanchard (1981) suggested that
experience with intruders enhances aggressive behaviour by decreasing the
resident’s fear of strangers. Blanchard, Shelton & Blanchard ( 1970) confirmed
that even brief periods of familiarization with intruders substantially alter future
reactions. First experiences of naive residents with intruders are especially
important. These initial experiences are characterized by extensive investigation,
reminiscent of the interest shown towards inanimate objects. This behaviour
increases resident familiarity with ‘strangers’ and presumably decreases
associated ‘fear’. Even if the encounter is too brief to lead to attack in this first
meeting, residents may, over repeated encounters, become familiar with
intruders as a class of object. This use of ‘familiarity’, does not imply recognition
of the intruder as an individual but as a Qpe of object. This is a n important
distinction because individual recognition has the opposite effect on attack. Familiar
conspecifics (animals known to one another) are generally less likely to fight than
are strangers (see Kamal & Brain, 1985).
Kamal (1986) also observed that, after the initial increase, aggressive
behaviour declines over an extended series of consecutive daily tests. The most
marked decrement evident was in the tenth test. Winslow & Miczek (1984) also
reported that the frequency of biting and lateral threat by male mice toward
conspecific intruders declined over a series of ten confrontations. Decrements in
murine aggression in repeated confrontations may be a consequence of
habituation but fatigue is also important. Declines may also be discussed in terms
of the waning of aggressive motivation with repeated experience. Similar
phenomena occur in stable groups. Krsiak & Janku (1969) noted that groups of
male mice initially housed together show a period of intense fighting, followed by
a gradual decline in such behaviour. Three possible causes for such declines in
aggression have been advanced.
1. Increasing familiarity of subordinates makes them less efectiue stimuli for eliciting
aggression. Unfamiliar opponents are generally attacked more vigorously than
familiar counterparts. Kamal (1986) confronted Swiss males with the same
intruder each day but there was no decline in the level of aggression from the
initial confrontations with these intruders. If intruders became familiar, the
aggressive behaviour should have declined and Kamal (1986) suggested that
familiarity with an opponent lasts less than 24 hours in this strain of mouse.
2. Behauioural changes in subordinates may result f r o m their learning to avoid or paclfr
dominants. Grant & Mackintosh (1963) reported that subordinates responded to
attacks by fleeing or assuming defensive upright postures. Burg & Slotnik (1963)
suggested that declines in colony aggression occurring soon after groups are
established, are a consequence of the improved ability of subordinates to avoid
dominant mice. Indeed, Connor & Lynds (1977) reported that subordinate
animals quickly learn to avoid and run when approached by dominants. Grimm
(1980) also claims that defeated mice learn to assume submissive postures more
quickly on successive encounters with fighters, thus reducing the attacks they
receive. Strasser & Dixon (1988) suggest that decreased movement is an
additional factor reducing probability of attack in rats and mice.
Previous agonistic experience of intruders is critical. Lore et al. (1976) placed
the same male intruder rat, at weekly intervals, into the cages of two different
resident males. O n the first encounter, the resident fought and defeated the
intruder but when the now-experienced intruder was placed into the second
266
P. F. BRAIN AND S. PARMIGIANI
resident’s cage no serious fighting occurred. They suggested that since the same
intruders (but not the same residents) were used in both tests, the experienced
intruders modified their subsequent behaviour when confronting a resident
animal in a way that reduced attack. Brain et al. (1981) have also reported
differences between previously defeated and naive house mice in the defensive
strategies they show in response to conspecific attack. Male laboratory mice that
have been subjected to defeat, show greater use of the forepaws to push away the
partner and receive fewer bites overall. They are also subject to fewer bites on
their back (the preferred target site of attackers) as they keep that target away
from their attacker. I n Kamal’s (1986) studies, intruders used in consecutive
daily trials increased their timidity and defensive behaviour over days. These
animals were still vigorously attacked by residents which had experienced
winning, but less experienced residents showed lessened attack in response to the
pronounced defensive behaviour of these defeated intruders. When animals
became highly aggressive, intense attacks may be directed even against intruders
which are reintroduced each day. Lagerspetz (1964) reported that induction of
an ‘anger’ state in mice, results in attacks being directed even towards motionless
opponents or inanimate objects.
3. Temporal decline in aggressiveness may result from motivational changes in the
dominant. Kamal’s ( 1986) repeated tests with docile ‘standard opponents’,
produced declines in fighting and threat on the tenth day, favouring the
explanation that the progressive decline in aggressiveness resulted from
motivational changes in these mice with positive fighting experience. Fatigue
may also be important for this reduction in aggressiveness but testing at 24-hour
intervals seems likely to minimize its relevance. I n cases where animals
confronted the same intruder in every trial, residents persisted in attack. The
decline in the attack on intruders could not be attributed to increasing
familiarity with the opponents or to a change in intruder behaviour with time.
Thus, the resident’s changed motivation seems the most likely explanation of
Kamal’s results and the phenomenon of ‘social inertia’ in stable groups of mice
(one should note, however, that the odour characteristics of subordinates are
changed due to suppressed androgen secretion; see Brain, 1983).
Andrade et al. (1989) have shown that the effects of exposure to defeat are
reversible. Mice repeatedly defeated over several days showed little sign of
aggression during the first two days of confrontation with docile anosmic
intruders displaying, instead, high levels of defence/timid behaviour. O n the
third daily confrontation, however, defeated mice started to threaten and attack
their anosmic apponents. Consequently, favourable daily encounters enable
defeated mice to recover from their submissive condition within three days of the
last defeat. A subsequent experiment used defeated mice with previous
experience of victory (unlike defeated mice in the above experiment). After the
last of an actually more intense series of defeats, these subjects confronted
anosmic intruders. Although they showed no fighting or threat immediately after
or up to 6 hours after the last defeat, the majority attacked their anosmic
opponents 12 hours after this experience. The recovery from substantial defeat in
experienced ‘winners’ thus occurs between 6 and 12 hours from the last negative
fighting experience. Positive experience before the defeat thus profoundly
changes the dynamics of the recovery from defeat. This characteristic may be of
great importance to animals such as the house mouse which may assume a
AGGRESSIVENESS IN THE HOUSE MOUSE
267
territorial organization. Subjects must be able to assume the characteristics of a
territory holder relatively quickly if an area becomes available. Also, territory
holders may be subject to defeat if they stray outside their defended areas.
Obviously such animals must be able to tolerate such occasional negative
experiences (these are actually likely to be much milder and shorter than the
exposures used here) without impairing their ability to hold their territory. The
point to emphasize is that it is not solely the outcome of immediately preceding
social experiences that determine ‘aggressiveness’ even in the ‘lowly’ mouse.
Accumulated positive and negative fighting experiences essentially determined
the behavioural characteristics of the individual animal.
CONCLUDING COMMENTS
There are obviously many potential sources of variation in aggressiveness
which underpin the wide range of ‘social’ organizations assumed by the highly
opportunistic ‘house mouse’, facilitating its successful exploitation of a wide
range of environments. The behavioural characteristics of male and female
individuals are influenced by the genotype of the individuals. Rather than this
being a simple variation in ‘aggressiveness’, genotypes differ on a range of
attributes. I t is probable that any elicited responses are consequences of the
resident and the intruder’s behaviours. One should also note that social structure
of mouse populations is much influenced by female individuals - that their
contribution is not essentially passive. Another source of phenotypic variance is
the intrauterine location phenomenon. This can throw up three different ‘types’
of male and females with varied physiological, morphological and behavioural
attributes. Finally, one should also record that prior social experiences have
considerable impact on the organism’s subsequent aggressive (and other)
behaviours which could also affect the range of social structures available to the
‘house mouse’. These data suggest that any relationship between ‘aggressiveness’
and success in feral mouse populations will be a complex one but they may
explain why such animals are able to readily vary their social organizations.
ACKNOWLEDGEMENTS
Data generated by Sandra Jones, Khalid B. H. Kamal and Yousif Y. Yousif is
cited in this account. Support by the SERC and the Governments of Italy, Iraq
and Saudi Arabia is acknowledged.
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