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The importance of kinship and familiarity in social interactions between mice
Anim. Behav., 1982, 30, 594-601
THE IMPORTANCE OF KINSHIP AND FAMILIARITY IN SOCIAL INTERACTIONS BETWEEN MICE BY A. M. K A R E E M & C. J. BARNARD
Animal Behaviour Research Group, Department of Zoology, University of Nottingham, University Park, Nottingham NG7 2RD Abstract. We investigated a range of social interactions between mice which differed in their degree of relatedness and familiarity. Unfamiliar half siblings (sharing paternity only) differed significantly from unfamiliar non-siblings (sharing neither mother nor father) in their tendency to perform aggressionrelated interactions and in the amount of passive body contact they showed. Differences between half and full siblings in patterns of interaction appeared to be due to differing degrees of familiarity with companions. Kinship effects disappeared completely when animals were allowed to become familiar. We discuss the functional significance of the familiarity and kinship effects we found, including differences between the sexes in the types of interaction showing kinship effects. Differences between adult and juvenile mice are also briefly discussed. Much interest has recently centred on the influence o f kin recognition on social interactions within various species (e.g. Gilder & Slater 1978; Porter et al. 1978; Greenberg 1979; Wu et al. 1980; Blaustein & O'Hara 1981; Porter et al. 1981a). Since Hamilton (1964) and Maynard Smith (1964) first emphasized the importance of kin selection in the evolution of social behaviour several studies have attempted to identify the cues used by animals in behaving differentially towards closely related individuals. In particular they have tested for the existence of an 'innate' or genetically-determined recognition mechanism which would enable animals to recognize close relatives without having had prior experience of them (Greenberg 1979; Wu et al. 1980; Blaustein & O'Hara 1981). In a recent review, Bekoff (1981) has also stressed the abundant literature showing the effect of familiarity on social responses in various mammal species, and points to the use of familiarity by animals in assessing kinship. That is, animals may use familiarity with conspecifics as a guide to their likely degree of relatedness. Depending on the 'viscosity' of the popuIation, animals responding differentially towards those with which they are familiar will incidentally do so towards close relatives. Many studies of kin recognition have not convincingly distinguished kin recognition per se from possible familiarity effects. This is particularly true where recognition between full siblings has been used (e.g. Gilder & Slater 1978; Porter et al. 1978; Porter & Wyrick 1979: Waldman & Adler 1979; Porter et al. 1981a). Even when sibs are separated at birth, in utero or pre-hatching 594
familiarity cannot be ruled out. While some recent studies have attempted to control for prenatal familiarity by using half siblings (sharing only paternity) (Wu et al. 1980) or siblings separated before hatching (Blaustein & O'Hara 1981), their indices of kin recognition (the tendency to approach unfamiliar sibs rather than unrelated conspecifics) have been very general. If kin recognition enhances an individual's inclusive fitness, however, we should look for its effects on the individual's total repertoire of social interactions. Only then are we likely to be able to hypothesize about its probable survival value. In this paper, we describe two experiments with laboratory mice (Mus musculus) in which we have attempted to separate familiarity effects in kin recognition from apparently unlearned or self-familiarity recognition abilities. In doing so, we examine the effects of relatedness and familiarity on a range of social interactions between individuals and draw some conclusions about the function of the implied recognition effects we find. In the first experiment we investigate kin recognition in both male and female mice and in adults and juveniles. In the second, we make a more detailed investigation of the role of familiarity in adult males.
Experiment 1 Methods The subjects tested were 60 male and 60 female mice of the non-inbred C. F. L. P. strain. All animals were reared by their own mother and maintained under a 14 h light/10 h dark light/dark-reversed cycle. During the dark
KAREEM & BARNARD: KINSHIP AND FAMILIARITY. IN MICE period and all experimental tests, animals were illuminated by a dim red light. Each litter from which subjects came was reduced at weaning (22 days) to eight pups (four of each sex). Pups were individually marked and the sexes kept together before they reached sexual maturity. On day 33 the sexes were separated and animals were maintained as unisexual groups of four littermates. From these unisexual groups, three sets of pairwise treatments could b e arranged. These comprised full sibling pairs (siblings from the same cage), half-sibling pairs (in which mice shared fathers but had been conceived and reared by different mothers in different cages) and non-sibling pairs (in which mice from different cages shared neither mother nor father). In all cases the coefficient of relatedness of non-sibling mice was less than 0.125 (the mother and father of any given litter used in 'non-sibling' tests were related by less than 0.5--that is, there were no sibling or parent-offspring relationships between individual parents of different litters). Experimental 'pair' of course, refers to unisexual dyads, not a mated pair. Mice were tested in a plastic observation cage (44 x 26 x 12 cm) with a glass cover and an opaque central .partition. Between each test, the cage was cleaned with alcohol, a n d fresh sawdust was put in. Individuals of a pair were placed one on either side of the partition and allowed to settle for 5 min before testing. The partition was then removed for 5 min and interactions between the animals (see below) were recorded on a cassette tape recorder. Tests with each type of pair (familiar full-sib, unfamiliar half-sib and unfamiliar non-sib) were repeated 10 times using different individuals in each case. The procedure was repeated twice for each sex (i.e. four times in all), once when mice were juveniles (30-32 days) and once when they were adult (68-73 days). Given pairs were therefore tested for two 5-rain periods separated by about 40 days. Food and water were available ad libitum except during tests. During tests, six types of interaction were recorded: (1) Sniff: olfactory exploration of the anogenital region. (2) Nose: contact between noses. (3) Investigate: olfactory exploration of body areas other than the face and anogenital region. (4) Aggression: a physical struggle between two animals which included wrestling, rolling and occasionally biting.
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(5)Allo-groom: one animal groomed the other by mandibulating or licking. (6) Touch: apparently undirected body contact which could not be classified as any of 1-5. Categories 1-5 are similar to those first defined by Grant & Mackintosh (1963). Results
Table I shows the mean frequency with which each type of interaction was performed per 5min test; Table Ia shows mean frequencies for male pairs as adults and juveniles: Table Ib the same for female pairs. Taking adult male pairs first, Table Ia shows several important trends. In particular, unfamiliar half-sib pairs showed significantly less Investigate and Allo-groom and significantly more Touch than unfamiliar non-sib pairs. In the case of Touch and Allo-groom, half-sib scores were comparable with those of familiar full sibs. The frequency of Investigate in half sibs, however, was significantly higher than in full sibs, as was also the frequency of Sniff: we shall return to this point later. Although not significant, another interesting result is the occurrence of Aggression only in adult non-sib pairs. Comparing the results for adult males with those for adult females (Table Ib), some important differences are apparent. Adult female halfsib pairs do not differ from non-sib pairs in their frequency of performing Investigate and Allogroom (cf. results for adult males in Table Ia). Moreover, no Aggression was observed in any test involving female pairs. Adult female half sibs differed significantly from non-sib pairs only in the frequency of Touch where, as in males, they were comparable with full sibs. As in males also, adult half sibs differed significantly from full sibs in the frequency of performing Sniff and Investigate. Some interesting differences within and between the two sexes can also be seen when scores for adult and juvenile pairs are compared. Adult males and females, of all pair types showed significantly less Investigation than juveniles. Only non-sib male pairs, however, showed a significant increase in the frequency of Allo-groom as adults. Also, no Aggression was observed in juvenile non-sib male pairs. Conversely, only half-sib and non-sib females showed increased levels of Touch as adults. Pairwise comparisons between juveniles showed, in general, the same trends as between adults. However, in females, juvenile half sibs showed significantly less Investigate than pairs (cf. adult females).
ANIMAL
596
BEHAVIOUR,
Discussion and Conclusions T h e m o s t i m p o r t a n t c o n c l u s i o n s t h a t arise f r o m e x p e r i m e n t 1 i n v o l v e the differences bet w e e n a d u l t m a l e half-sib a n d n o n - s i b p a i r s i n levels o f Investigate, A l l o - g r o o m , T o u c h a n d
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p o s s i b l y A g g r e s s i o n . T h e l o w e r levels o f I n v e s t i gate a n d A l l o - g r o o m i n h a l f sibs are p a r t i c u l a r l y i n t e r e s t i n g b e c a u s e b o t h these types o f i n t e r a c t i o n h a v e b e e n f o u n d to correlate positively w i t h d o m i n a n c e r a n k i n g a n d to b e p r e l u d e s to
Table I. Frequency (Mean • sE) of Each Behaviour per 5-min Test in Experiment 1 (a) Males Full sibs (familiar)
Half sibs (unfamiliar)
Non-sibs (unfamiliar) 6.4 • 1.26 7.6 4- 2.26
Sniff
J A
0.2 4- 0.20tit 0.3 4- 0.15t~t
5.3 • 1.61"** 3.2 -4- 0.98**
Investigate
J A
2.8 q- 0.42ttt 1.1 • 0.38ttt
8.3 ~ 0.91ttt*** 5.0 4- 0.62tt***
Nose
J A
2.2 • 0.39 2.2 -4- 0.36
4.1 :~ 0.86 1.9 -4- 0.50
4.0 -4- 0.83 2.9 -4- 0.89
Touch
J A
20.8 -4- 2.73t 27.0 -4- 2.42tit
12.9 -4- 1.22 10.0 • 1.27
Aggression
J A
0 0
0 0
0 2.3 • 1.48
Allo-groom
J A
0tt 0.2 -4- 0.13tit
0.7 -4- 0.40 0.7 -4- 0.34t
1.5 -4- 0.50 4.2 -4- 1.35
24.0 -4- 2.73ttt 26.8 -4- 2.85ttt
15.3 -4- 1.35 8.7 • 1.10
(b) Females Full sibs (familiar)
Half sibs (unfamiliar)
Non-sibs (unfamiliar)
Sniff
J A
0.5 -4- 0.22tt 0.3 -4- 0.15tt
4.2 • 1.32"* 5.5 -4- 1.78"**
4.0 -4- 1.66 5.1 -4- 2.11
Investigate
J A
4.1 -4- 0.81ttt 2.2 -4- 0.33ttt
8.8 -4- 1.02t** 4.9 -4- 0.96*
14.2 -4- 1.45 6.8 -4- 0.84
Nose
J A
2.9 -4- 0.50 1.6 -4- 0.43
2.3 -4- 0.76 3.0 -4- 0.83
Touch
J A
Aggression
J A
0 0
0 0
0 0
Allo-groom
J A
0 0
0.6 • 0.27 0.2 -4- 0.13
0.1 -4- 0.10 0.2 -4- 0.13
22.4 • 2.08ttt 25.0 4- 1.90tit
19.1 -4- 2.00tt 25.1 -4- 1.45ttt
3.2 -4- 0.70 3.2 -4- 0.77 12.5 -4- 0.91 15.5 -4- 1.20
J = juvenile; A = adult. *, t : P < 0.05; **, t t : P < 0.01; ***, t t t : P < 0.002 (significance levels for Mann-Whitney U-test; *compares half sibs with full sibs,t compares half and full sibs with non-sibs). Underlining: - - : P < 0.05; ~_~ : P < 0.02; ~ : P < 0.01 (significance levels for Wilcoxon matched-pairs signed ranks test comparing juvenile with adult frequencies).
KAREEM & BARNARD: KINSHIP AND FAMILIARITYIN MICE fighting in mice (e.g. Banks 1962; Clark & Sehein 1966; van Oortmerssen 1971). Indeed, Grant & Mackintosh (1963) categorized one component (see later) of Allo-groom (there called 'aggressive groom') as an aggressive behaviour. In this respect, it is noteworthy that overt aggression occurred only in adult male non-sib pairs. The most pronounced differences between unfamiliar non-sibs and unfamiliar half and full sibs therefore occurred in those interactions having a high risk element. Although not the case in our experiment, aggression between mice can be very damaging (Southwick 1970). In contrast to adult males, adult female halfsib and non-sib pairs showed no significant differences in levels of Investigate and Allo-groom and neither pair type showed Aggression. Fullsib pairs, however, did show significantly lower levels of Investigate than did non-sib pairs. The fact that apparently aggressively motivated behaviours occur less often in female mice might be expected, since it is primarily males which aggressively defend family territories (Rowe & Redfern 1969; Harrington 1976; but see Mackintosh 1981) and the physiology of aggression is different between the sexes (Scott 1975), with females showing less tendency to fight than males. Both adult male and female full-sib and halfsib pairs showed significantly higher levels of Touch than non-sib pairs. Touch refers to apparently undirected, passive body contact between animals. Although it is not a category specifically distinguished by previous workers, its inclusion is important because it provides a qualitative index of spacing at times other than during specific interactions. In other interaction categories, there were differences between adults and juveniles. In particular, juvenile males and females of all pair types showed significantly more Investigate than adults. However, the relationship between age and frequency of performing aggressionrelated interactions is not clear-cut. In males, unrelated juveniles showed less AUo-groom and no Aggression, while in females there was no difference between juveniles and adults. In females, however, there was a significant increase in the amount of passive body contact (Touch) in adult half-sib and non-sib pairs. There was no similar increase in males. These results suggest different maturation effects between the sexes in patterns of social interaction which may
597
be influenced by the degree of relatedness between individuals. While the results of experiment 1 suggest an 'innate' kin recognition mechanism (in that, depending on age and sex, unfamiliar half sibs behave more like familiar full sibs than unfamiliar non-sibs in a variety of social interactions), there are complications. The most important is that, in both sexes and in both adults and juveniles, half-sib pairs differed significantly from full-sib pairs in their frequency of performing Sniff (classified by Dixon & Mackintosh as "social investigation') and Investigate. For Sniff, and in adult females, Investigate, half sibs did not differ significantly from non-sibs. These differences could be explained in three ways. They could be due to (a) individuals matching their responses to the detected degree of relatedness of their companion (see e.g. Greenberg 1979), hence responding to half sibs at levels intermediate between those for full sibs and non-sib partners; (b) a familiarity effect (full sibs are familiar whereas half sibs and non-sibs are unfamiliar); or (c) a combination of (a) and (b). There is an overwhelming literature showing the importance of familiarity in rodent social interactions (e.g. Poole & Morgan 1975; Huck & Banks 1979; Bekoff 1981; Geyer et al. 1981 ; Porter et al. 1981b). In order to control for confounding familiarity effects more closely, therefore, we carried out a second experiment.
Experiment 2 Methods The subjects tested in experiment 2 were 154 male C. F. L. P. mice. All were tested as adults at 66-73 days of age. The mice were drawn from 32 litters of known relationship. Shortly before birth, the litters were arranged to produce different degrees of relatedness and familiarity among individuals. Eight litters of half sibs (again sharing only paternity) were born with two litters per cage. Eight litters of non-sibs were arranged similarly, and eight litters each of half sibs and non-sibs were born and reared as single litters in separate cages. All mice were individually marked so their litter of origin and parentage were known, and all were reared by their own mothers. All individuals born and reared in the same cage were considered to be 'familiar' at the time of testing. When litters reached 32 days of age, females were removed and the number of males in each cage was reduced to a maximum of eight. Other conditions
598
ANIMAL
BEHAVIOUR,
of maintenance were identical to those in experiment 1. Animals were assigned for testing into arbitrarily picked pairs of familiar half sibs (F-HS, 13 pairs), familiar non-sibs (F-NK, 11 pairs), unfamiliar half sibs (UF-HS, 17 pairs) and unfamiliar non-sibs (UF-NK, 20 pairs). Sixteen pairs of full sibs, each pair from a different litter, were also tested. Pairs were tested in exactly the same way as those in experiment 1: However, some interaction categories recorded in experiment 1 were subdivided into more precise identifiable categories, and some additional behaviours not recorded in experiment 1 were included. Some of the additional behaviours referred to the actions of just one individual rather than to interactions between both members of a pair. The modified or additional behaviour categories are defined similarly to those of Grant & Mackintosh (1963) and van Oortmerssen (1971). Modified categories. Allo-groom of experiment 1 was subdivided into two components: Social Groom: licking and mandibulating the fur of the companion, mostly on the head and back. This sometimes involved placing forepaws on the companion. Aggressive Groom; vigorous licking and mandibulation of the companion's fur, often localized at the shoulder region; fur sometimes pulled with the teeth. Additional categories: Follow: following a locomoting companion. Squire: following a locomoting partner while maintaining nasal contact with the companion's fur. Self-groom: wiping, licking and nibbling own fur with forepaws, tongue or teeth. Sniffing at sawdust: standing still, usually briefly, with nose in the sawdust. Sometimes the sawdust was pushed sideways with the nose or forepaws. Upright: standing or 'sitting' on hind legs, sniffing the air. Total Exploration: the total frequency of Sniffing at Sawdust and Upright. Total Interaction: the total frequency of all behaviours which involved mutual interaction. Results Mean frequencies of performance of each behavioural category for each pair type are shown in Table II. When scores for U F - N K and U F - H S pairs are compared, similar trends
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emerge to those in experiment 1. U F - H S mice showed significantly less Investigate and significantly more Touch t h a n U F - N K mice (Table III). Although there were no significant differences in scores for Social Groom and Aggressive Groom (combined as Allo-groom in experiment 1), U F - N K pairs were the only ones with a score greater than zero for Aggressive Groom. Similarly, the mean frequency of Aggression in U F - N K pairs was 4.5 times higher than the the next highest mean (F-HS pairs), although the difference was not significant. When F - N K and F-HS pairs (in which companions are familiar with one another) are compared, however, all significant differences disappear. The effects of familiarity were more pronounced in nonsibs than in half sibs. Column 3 of Table III, comparing U F - N K and F - N K pairs, shows that all significant differences had an associated probability of 2 % or less. Column 4, comparing UF-HS and F-HS pairs, shows only 50% of significant differences with probabilities of 2% or less. Familiar animals (both half-sib and non-sib) tended to Sniff and Investigate less often and hence show less Total Interaction, but performed more Upright and Total Exploration activity. In addition, F-HS pairs showed less Squire + Follow (lumped in analysis) compared with U F - H S pairs, and F - N K pairs showed more Sniff at Sawdust. When U F - H S pairs are compared with fullsib pairs (Table III, column 6), significant differences between the two pair types are mainly similar to those in experiment 1. U F - H S pairs showed more Sniff and Investigate, but this time also showed less Touch (cf. Table Ia, b). In addition, UF-HS pairs showed more Squire + Follow and less Sniff at Sawdust and Total Exploration. When full-sib and F-HS pairs are compared, however, no significant differences emerge (Table III, column 5). Discussion The results of the experiments described here suggest the existence of a kin recognition mechanism in mice which appears not to depend on prior experience with encountered animals. Unfamiliar non-siblings tended to show less passive body contact and more interactions related to aggression than did unfamiliar half siblings. Unfamiliar half sibs however, did not always interact in the same way as full sibs. They differed significantly from full sibs in the direction of non-sib scores in 33 % of recorded categories in experiment 1 and 43 % of recorded
K A R E E M & B A R N A R D : KINSHIP A N D F A M I L I A R I T Y IN MICE
599
r u l e o u t s e l f - f a m i l i a r i t y as a m e c h a n i s m f o r rec o g n i t i o n b e t w e e n u n f a m i l i a r h a l f s i b s , t h i s is n o t a n i m p o r t a n t difficulty. T h e i m p o r t a n t f i n d i n g o f t h i s s t u d y is t h e a p p a r e n t a b i l i t y o f m i c e t o r e c o g n i z e h a l f sibs w i t h o u t a n y p r i o r experience of them. Whether they achieve this by an innate recognition mechanism or by r e c o g n i z i n g c u e s t h e y t h e m s e l v e s p o s s e s s is l a r g e l y i m m a t e r i a l . W h a t m a t t e r s is t h a t m i c e h a v e e v i d e n t l y b e e n s e l e c t e d t o r e c o g n i z e close relatives and to respond differently towards t h e m a t a first m e e t i n g . A n o t h e r i m p o r t a n t f i n d i n g o f t h e s t u d y is t h a t k i n d i s c r i m i n a t i o n is n o t a p p a r e n t i n all t y p e s o f i n t e r a c t i o n s . I t it m o s t p r o n o u n c e d i n
c a t e g o r i e s i n e x p e r i m e n t 2. C o m p a r i s o n b e t w e e n a d u l t m a l e f u l l sibs a n d f a m i l i a r h a l f s i b s suggested these differences were due to unfamiliarity r a t h e r t h a n r e c o g n i t i o n o f a l o w e r d e g r e e o f relatedness. Similarly, differences between nons i b a n d b o t h h a l f - s i b a n d fuU-sib p a i r s d i s a p peared when companions had had prior experience of one another. The fact that familiarity h a d a m o r e p r o n o u n c e d effect o n b e h a v i o u r i n non-sib pairs bears out the tendency for half sibs' scores to be intermediate between those for non-sib and full-sib pairs in a wide range of c a t e g o r i e s ( T a b l e II). W h i l e , i n c o m m o n w i t h o t h e r s t u d i e s ( W u et al. 1980; B l a u s t e i n & O ' H a r a 1981), w e c a n n o t
Table II. Frequency (Mean • SE) of Each Behavioural Category Performed per 5 rain by Each Pair Type in Experiment 2
Unfamiliar non-sibs (N = 20 pairs) Sniff Investigate Nose Squire+Follow Aggression Aggressive G r o o m Social Groom Touch Total Interaction Self-groom Sniffing at Sawdust Upright Total Exploration Total Activity
6.25 12.80 5.40 3.45 6.25 0.10 0.60 9.90 44.75 1.35 18.65 79.50 98.15 144.25
Unfamiliar half sibs (N = 17 pairs)
• t.ll • 0.80 4- 0.81 4- 0.60 4- 3.22 4- 0.10 4- 0.22 4- 1.39 4- 2.60 • 0.23 :~ 2.00 4- 3.92 4- 5.16 4- 3.24
3.77 9.29 5.65 3.88 1.00 0 1.53 15.41 40.53 1.82 19.65 84.18 103.82 146.18
Familiar non-sibs (N = 11 pairs)
4- 0.77 =L 0.91 4- 1.02 4- 0.69 4- 0.94 44444444-
0.62 1.50 1.47 0.t5 1.00 4.15 4.46 4.25
1.46 7.18 3.18 1.64 0 0 0 20.64 34.09 1.46 26.36 94.27 120.64 156.18
4444-
0.49 1.29 0.64 0.45
444444•
1.16 1.64 0.25 1.56 3.14 3.51 3.60
Familiar half sibs (N = 13 pairs) 1.23 5.54 3.62 1.0 1.39 0 0.39 20.15 33.31 1.54 22.92 96.69 119.62 154.46
4• • i 4-
0.28 1.38 0.54 0.42 0.90
44• 444• 4-
0.19 1.70 1.98 0.24 1.72 3.92 4.48 4.88
Table HI. Comparisons between Pair Types of the Frequency of Each Behavioural Category per 5 rain in Experiment 2
Comparisons
Behaviour Sniff Investigate Nose Squire + follow Aggression Aggressive groom Social groom Touch Total interaction Self-groom Sniff at Sawdust Upright Total exploration Total activity
UF-NK vs UF-HS
F-NK vs F-HS
--
--
**
. -. . . * -. ---.
--
--. ---.
*
.
.
. . . *** *** . ** ** **** .
. . .
-. . .
.
*
****
.
. . .
UF-HS vs F-HS
***
--
.
UF-NK vs F-NK
.
FS vs UF-HS
--
*
--
****
--
***
---
*** --
----
** -*
. *** . . . -***
.
. -* **
.
FS vs F-HS
.
*P < 0.05; **P < 0.02; ***P < 0.01; ****P < 0.002 (Mann-Whitney U-test).
Full sibs (N = 16 pairs) 1.69 4.81 3.31 1.38 1.38 0 0.25 22.88 35.81 1.63 24.0 94.56 118.56 156.0
44• 44-
0.71 1.10 0.52 0.35 1.38
44444444-
0.19 2.00 2.30 0.18 1.28 3.81 4.24 5.21
600
ANIMAL
BEHAVIOUR,
those types which tend to be associated with aggression, and in the frequency o f undirected, passive body contact. In general, however, mice appear to use familiarity as a rule of thumb (see Dawkins 1979; Bekoff 1981) during interaction. Prior familiarity completely overrides differences in the degree of relatedness in deciding patterns of interaction. A 'regard familiar individuals as kin' rule is likely to operate well in the wild. House mice tend to live in small, closed breeding groups (for details, see Anderson 1970; Berry 1981), maintained mainly by males defending group territories (Harrington 1976; but see Mackintosh (1981) for the possible role of pregnant females in territorial defence). Individuals able to regulate their aggressive responses, and the initiation of interactions likely to lead to aggression, according to the detected degree of kinship in an unfamiliar companion, are likely to increase their inclusive fitness, We should therefore expect the familiarity rule of thumb to operate only for interactions like Sniff, Nose and following behaviour, where the cost of mistaken identity is likely to be low. We should expect a back-up recognition mechanism which distinguishes closely related from other unfamiliar individuals when potentially aggressive interactions are involved. Discrimination in aggression-related interactions m a y be less important in adult female mice. Since females are not usually involved in group defence, the familiarity rule as a guide to patterns of interaction may be evolutionarily more economical. Among adult females, the only apparent discrimination based on kinship occurred in Touch. Increased frequency of passive body contact between unfamiliar half sibs occurred in both males and females, and may have been associated with a reduced risk of close contact leading to aggression. Related and familiar animals are undoubtedly recognized on the basis of olfactory cues (see Brown 1979; Halpin 1980). Archer (1968) suggested that the odour of male mice had two functionally distinct components. One component was of a general nature and tended to elicit attack by another male: the other was an 'identifier' specific to an individual. Animals housed together habituated to each other's individual identifier and only animals with unfamiliar identifiers were subsequently attacked. In addition, group members tend to scent-mark each other so that all end up with a composite 'group scent' (Brown 1979). There is good experimental evidence for individual recogni-
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tion by odour in mice (Mackintosh & Grant 1966; Bowers & Alexander 1967; Kalkowski 1967: H a h n & Simmel 1968; Kimelman & Lubow 1974). It m a y be that such odours are similiar in closely related individuals and so form the basis for the recognition of nonfamiliar kin demonstrated here.
Acknowledgments We thank Hilary Stephens, Desmond Thompson and Chris Brown for reading an earlier draft of the manuscript and two anonymous referees for helpful criticism. The work was supported by a grant from the University of Sulaimaniyah to A. M. K. REFERENCES Anderson, P. K. 1970. Ecological structure and gene flow in small mammals. Symp. zool. Soc. Lond., 26, 299-325. Archer, J. 1968. The effect of strange male odor on aggressive behavior in male mice. J. Mammal., 49, 572-575. Banks, E. M. 1962. A time and motion study of prefighting behavior in mice. J. genet. PsychoL, 101, 165183. Bekoff, M. 1981. Mammalian sibling interactions: genes, facilitative environments and the coefficient of familiarity. In: Parental Care in Mammals (Ed. by D. J. Guberniek & P. H. Klopfer), pp. 307-346. New York: Plenum Press. Berry, R. J. 1981. Population dynamics of the house mouse. Symp. zooL Soc. Lond., 47, 395--425. Blaustein, A. R. & O'Hara, R. K. 1981. Genetic control for sibling recognition. Nature, Lond., 290, 246248. Bowers, J. M. & Alexander, B. K. 1967. Mice: individual recognition by olfactory cues. Science, N.Y., 158, 1208-1210. Brown, R. E. 1979. Mammalian social odours: a critical review. Adv. Study Behav., 10, 103-162. Clark, L. H. & Sehein, M. W. 1966. Activities associated with conflict behaviour in mice. Anim. Behav., 14, 44--49. Dawkins, R. 1979. Twelve misunderstandings of kin selection. Z. TierpsychoL, 51, 184-200. Dixon, A. K. & Mackintosh, J. H. 1976. Olfactory mechanisms affording protection from attack to juvenile mice (Mus musculus L.). Z. Tierpsychol., 41, 225-234. Geyer, L. A., Beauchamp, G. K., Seygal, G. & Rogers, J. G. Jr. 1981. Social behaviour of pine voles, Microtus pinetorum: effects of gender, familiarity and isolation. Behav. neut. BioL, 31, 331-341. Gilder, P. M. & Slater, P. J. B. 1978. Interest of mice in conspeeifie male odours is influenced by degree of kinship. Nature, Lond., 274, 364-365. Grant, E. C. & Mackintosh, J. H. 1963. A comparison of the social postures of some common laboratory rodents. Behaviour, 21, 246--259. Greenberg, L. 1979. Genetic component of bee odor in kin recognition. Science, N.Y., 206, 1095-1097. Hahn, M. E. & Simmel, E. C. 1968. Individual recognition by natural concentrations of olfactory cues in mice. Psychon. Sci., 12, 183-184.
K A R E E M & B A R N A R D : KINSHIP A N D FAMILIARITY "IN MICE Halpin, Z. T. 1980. Individual odors and individual recognition: review and conmaentary. Biol. Behav., 5, 233-248. Hamilton, W. D. 1964. The genetical evolution of social hehaviour. J. theoret. BioL, 7, 1-52. Harrington, J. E. 1976. Recognition of territorial boundaries by olfactory cues in mice (Mus muscuhts L.). Z. Tierpsychol., 41, 295-306. Huck, U. W. & Banks, E. M. 1979. Behavioral components of individual recognition in the collared lemming (Dicrostonyx groenlandicus). Behav. Ecol. SociobioL, 6, 85-90. Kalkowski, W. 1967. Olfactory bases of social orientation in the white mouse. Folia bioL, Krakow, 15, 69-87. Kimelman, B . R . & Lubow, R. E. 1974. The inhibitory effect of pre-exposed olfactory cues on intermale aggression in mice. PhysioL Behav., 12, 919-922. Mackintosh, J. H. 1981. Behaviour of the house mouse. Symp. zooL Soc. Lond., 47, 337-365. Mackintosh, J. H. & Grant, E. C. 1966. The effect of olfactory stimuli on the agonistic behaviour of laboratory mice. Z. Tierpsychol., 23, 584-587. Maynard Smith, J. 1964. Kin selection and group selection. Nature, Lond., 201, 1145-1147. Oortmerssen, G. A. van. 1971. Biological significance, genetic and evolutionary origin of variability in behaviour within and between inbred strains of mice (Mus masculus). Behaviour, 38, 1-92. Poole, T. B. & Morgan, H. D. R. 1975. Aggressive behaviour of male mice (Mus musculas) towards familiar and unfamiliar opponents. Anim. Behav., 23, 470-479.
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Porter, R. H. & Wyrick, M, 1979. Sibling recognition in spiny mice (Acomys cahirinus): influence of age and isolation. Anim. Behav., 27, 761-766. Porter, R. H., Wyrick, M. & Pankey, J. 1978. Sibling recognition in spiny mice (Acomys cahirinus). Behav. EcoL SociobioL, 3, 61-68. Porter, R. H., Moore, J. D. & White, D. M. 1981a. Food sharing by sibling versus nonsibling spiny mice
(Acomys cahirinus). Behav. EcoL Sociobiol., 8,
207-212. Porter, R. H., Tepper, V. J. & White, D. M. 1981b. Experiential influences on the development of huddling preferences and 'sibling' recognition in spiny mice. Dev. Psychobiol., 14, 375-382. Rowe, F. P. & Redfern, R. 1969. Aggressive behaviour in related and unrelated wild house mice (Mus musculus L.). Ann. appl. Biol., 64, 425--431. Scott, J. P. 1975. Aggression. Chicago, IL: University of Chicago Press. Southwick, C. H. 1970. Genetic and environmental variables influencing animal aggression. In: Animal Aggression (Ed. by C. H. Southwick), pp. 213-229. New York: Van Nostrand Reinhold. Waldman, B. & Adler, K. 1979. Toad tadpoles associate preferentially with siblings. Nature, Lond., 282, 611-613. Wu, H. M. H., Holmes, W. G., Medina, S. R. & Saekett, G. P. 1980. Kin preference in infant Macaca nemestrina. Nature, Lond., 285, 225-227.
(Received 8 July 1981 ; revised 22 September 1981 ; MS. number: 2146)
THE IMPORTANCE OF KINSHIP AND FAMILIARITY IN SOCIAL INTERACTIONS BETWEEN MICE BY A. M. K A R E E M & C. J. BARNARD
Animal Behaviour Research Group, Department of Zoology, University of Nottingham, University Park, Nottingham NG7 2RD Abstract. We investigated a range of social interactions between mice which differed in their degree of relatedness and familiarity. Unfamiliar half siblings (sharing paternity only) differed significantly from unfamiliar non-siblings (sharing neither mother nor father) in their tendency to perform aggressionrelated interactions and in the amount of passive body contact they showed. Differences between half and full siblings in patterns of interaction appeared to be due to differing degrees of familiarity with companions. Kinship effects disappeared completely when animals were allowed to become familiar. We discuss the functional significance of the familiarity and kinship effects we found, including differences between the sexes in the types of interaction showing kinship effects. Differences between adult and juvenile mice are also briefly discussed. Much interest has recently centred on the influence o f kin recognition on social interactions within various species (e.g. Gilder & Slater 1978; Porter et al. 1978; Greenberg 1979; Wu et al. 1980; Blaustein & O'Hara 1981; Porter et al. 1981a). Since Hamilton (1964) and Maynard Smith (1964) first emphasized the importance of kin selection in the evolution of social behaviour several studies have attempted to identify the cues used by animals in behaving differentially towards closely related individuals. In particular they have tested for the existence of an 'innate' or genetically-determined recognition mechanism which would enable animals to recognize close relatives without having had prior experience of them (Greenberg 1979; Wu et al. 1980; Blaustein & O'Hara 1981). In a recent review, Bekoff (1981) has also stressed the abundant literature showing the effect of familiarity on social responses in various mammal species, and points to the use of familiarity by animals in assessing kinship. That is, animals may use familiarity with conspecifics as a guide to their likely degree of relatedness. Depending on the 'viscosity' of the popuIation, animals responding differentially towards those with which they are familiar will incidentally do so towards close relatives. Many studies of kin recognition have not convincingly distinguished kin recognition per se from possible familiarity effects. This is particularly true where recognition between full siblings has been used (e.g. Gilder & Slater 1978; Porter et al. 1978; Porter & Wyrick 1979: Waldman & Adler 1979; Porter et al. 1981a). Even when sibs are separated at birth, in utero or pre-hatching 594
familiarity cannot be ruled out. While some recent studies have attempted to control for prenatal familiarity by using half siblings (sharing only paternity) (Wu et al. 1980) or siblings separated before hatching (Blaustein & O'Hara 1981), their indices of kin recognition (the tendency to approach unfamiliar sibs rather than unrelated conspecifics) have been very general. If kin recognition enhances an individual's inclusive fitness, however, we should look for its effects on the individual's total repertoire of social interactions. Only then are we likely to be able to hypothesize about its probable survival value. In this paper, we describe two experiments with laboratory mice (Mus musculus) in which we have attempted to separate familiarity effects in kin recognition from apparently unlearned or self-familiarity recognition abilities. In doing so, we examine the effects of relatedness and familiarity on a range of social interactions between individuals and draw some conclusions about the function of the implied recognition effects we find. In the first experiment we investigate kin recognition in both male and female mice and in adults and juveniles. In the second, we make a more detailed investigation of the role of familiarity in adult males.
Experiment 1 Methods The subjects tested were 60 male and 60 female mice of the non-inbred C. F. L. P. strain. All animals were reared by their own mother and maintained under a 14 h light/10 h dark light/dark-reversed cycle. During the dark
KAREEM & BARNARD: KINSHIP AND FAMILIARITY. IN MICE period and all experimental tests, animals were illuminated by a dim red light. Each litter from which subjects came was reduced at weaning (22 days) to eight pups (four of each sex). Pups were individually marked and the sexes kept together before they reached sexual maturity. On day 33 the sexes were separated and animals were maintained as unisexual groups of four littermates. From these unisexual groups, three sets of pairwise treatments could b e arranged. These comprised full sibling pairs (siblings from the same cage), half-sibling pairs (in which mice shared fathers but had been conceived and reared by different mothers in different cages) and non-sibling pairs (in which mice from different cages shared neither mother nor father). In all cases the coefficient of relatedness of non-sibling mice was less than 0.125 (the mother and father of any given litter used in 'non-sibling' tests were related by less than 0.5--that is, there were no sibling or parent-offspring relationships between individual parents of different litters). Experimental 'pair' of course, refers to unisexual dyads, not a mated pair. Mice were tested in a plastic observation cage (44 x 26 x 12 cm) with a glass cover and an opaque central .partition. Between each test, the cage was cleaned with alcohol, a n d fresh sawdust was put in. Individuals of a pair were placed one on either side of the partition and allowed to settle for 5 min before testing. The partition was then removed for 5 min and interactions between the animals (see below) were recorded on a cassette tape recorder. Tests with each type of pair (familiar full-sib, unfamiliar half-sib and unfamiliar non-sib) were repeated 10 times using different individuals in each case. The procedure was repeated twice for each sex (i.e. four times in all), once when mice were juveniles (30-32 days) and once when they were adult (68-73 days). Given pairs were therefore tested for two 5-rain periods separated by about 40 days. Food and water were available ad libitum except during tests. During tests, six types of interaction were recorded: (1) Sniff: olfactory exploration of the anogenital region. (2) Nose: contact between noses. (3) Investigate: olfactory exploration of body areas other than the face and anogenital region. (4) Aggression: a physical struggle between two animals which included wrestling, rolling and occasionally biting.
595
(5)Allo-groom: one animal groomed the other by mandibulating or licking. (6) Touch: apparently undirected body contact which could not be classified as any of 1-5. Categories 1-5 are similar to those first defined by Grant & Mackintosh (1963). Results
Table I shows the mean frequency with which each type of interaction was performed per 5min test; Table Ia shows mean frequencies for male pairs as adults and juveniles: Table Ib the same for female pairs. Taking adult male pairs first, Table Ia shows several important trends. In particular, unfamiliar half-sib pairs showed significantly less Investigate and Allo-groom and significantly more Touch than unfamiliar non-sib pairs. In the case of Touch and Allo-groom, half-sib scores were comparable with those of familiar full sibs. The frequency of Investigate in half sibs, however, was significantly higher than in full sibs, as was also the frequency of Sniff: we shall return to this point later. Although not significant, another interesting result is the occurrence of Aggression only in adult non-sib pairs. Comparing the results for adult males with those for adult females (Table Ib), some important differences are apparent. Adult female halfsib pairs do not differ from non-sib pairs in their frequency of performing Investigate and Allogroom (cf. results for adult males in Table Ia). Moreover, no Aggression was observed in any test involving female pairs. Adult female half sibs differed significantly from non-sib pairs only in the frequency of Touch where, as in males, they were comparable with full sibs. As in males also, adult half sibs differed significantly from full sibs in the frequency of performing Sniff and Investigate. Some interesting differences within and between the two sexes can also be seen when scores for adult and juvenile pairs are compared. Adult males and females, of all pair types showed significantly less Investigation than juveniles. Only non-sib male pairs, however, showed a significant increase in the frequency of Allo-groom as adults. Also, no Aggression was observed in juvenile non-sib male pairs. Conversely, only half-sib and non-sib females showed increased levels of Touch as adults. Pairwise comparisons between juveniles showed, in general, the same trends as between adults. However, in females, juvenile half sibs showed significantly less Investigate than pairs (cf. adult females).
ANIMAL
596
BEHAVIOUR,
Discussion and Conclusions T h e m o s t i m p o r t a n t c o n c l u s i o n s t h a t arise f r o m e x p e r i m e n t 1 i n v o l v e the differences bet w e e n a d u l t m a l e half-sib a n d n o n - s i b p a i r s i n levels o f Investigate, A l l o - g r o o m , T o u c h a n d
30,
2
p o s s i b l y A g g r e s s i o n . T h e l o w e r levels o f I n v e s t i gate a n d A l l o - g r o o m i n h a l f sibs are p a r t i c u l a r l y i n t e r e s t i n g b e c a u s e b o t h these types o f i n t e r a c t i o n h a v e b e e n f o u n d to correlate positively w i t h d o m i n a n c e r a n k i n g a n d to b e p r e l u d e s to
Table I. Frequency (Mean • sE) of Each Behaviour per 5-min Test in Experiment 1 (a) Males Full sibs (familiar)
Half sibs (unfamiliar)
Non-sibs (unfamiliar) 6.4 • 1.26 7.6 4- 2.26
Sniff
J A
0.2 4- 0.20tit 0.3 4- 0.15t~t
5.3 • 1.61"** 3.2 -4- 0.98**
Investigate
J A
2.8 q- 0.42ttt 1.1 • 0.38ttt
8.3 ~ 0.91ttt*** 5.0 4- 0.62tt***
Nose
J A
2.2 • 0.39 2.2 -4- 0.36
4.1 :~ 0.86 1.9 -4- 0.50
4.0 -4- 0.83 2.9 -4- 0.89
Touch
J A
20.8 -4- 2.73t 27.0 -4- 2.42tit
12.9 -4- 1.22 10.0 • 1.27
Aggression
J A
0 0
0 0
0 2.3 • 1.48
Allo-groom
J A
0tt 0.2 -4- 0.13tit
0.7 -4- 0.40 0.7 -4- 0.34t
1.5 -4- 0.50 4.2 -4- 1.35
24.0 -4- 2.73ttt 26.8 -4- 2.85ttt
15.3 -4- 1.35 8.7 • 1.10
(b) Females Full sibs (familiar)
Half sibs (unfamiliar)
Non-sibs (unfamiliar)
Sniff
J A
0.5 -4- 0.22tt 0.3 -4- 0.15tt
4.2 • 1.32"* 5.5 -4- 1.78"**
4.0 -4- 1.66 5.1 -4- 2.11
Investigate
J A
4.1 -4- 0.81ttt 2.2 -4- 0.33ttt
8.8 -4- 1.02t** 4.9 -4- 0.96*
14.2 -4- 1.45 6.8 -4- 0.84
Nose
J A
2.9 -4- 0.50 1.6 -4- 0.43
2.3 -4- 0.76 3.0 -4- 0.83
Touch
J A
Aggression
J A
0 0
0 0
0 0
Allo-groom
J A
0 0
0.6 • 0.27 0.2 -4- 0.13
0.1 -4- 0.10 0.2 -4- 0.13
22.4 • 2.08ttt 25.0 4- 1.90tit
19.1 -4- 2.00tt 25.1 -4- 1.45ttt
3.2 -4- 0.70 3.2 -4- 0.77 12.5 -4- 0.91 15.5 -4- 1.20
J = juvenile; A = adult. *, t : P < 0.05; **, t t : P < 0.01; ***, t t t : P < 0.002 (significance levels for Mann-Whitney U-test; *compares half sibs with full sibs,t compares half and full sibs with non-sibs). Underlining: - - : P < 0.05; ~_~ : P < 0.02; ~ : P < 0.01 (significance levels for Wilcoxon matched-pairs signed ranks test comparing juvenile with adult frequencies).
KAREEM & BARNARD: KINSHIP AND FAMILIARITYIN MICE fighting in mice (e.g. Banks 1962; Clark & Sehein 1966; van Oortmerssen 1971). Indeed, Grant & Mackintosh (1963) categorized one component (see later) of Allo-groom (there called 'aggressive groom') as an aggressive behaviour. In this respect, it is noteworthy that overt aggression occurred only in adult male non-sib pairs. The most pronounced differences between unfamiliar non-sibs and unfamiliar half and full sibs therefore occurred in those interactions having a high risk element. Although not the case in our experiment, aggression between mice can be very damaging (Southwick 1970). In contrast to adult males, adult female halfsib and non-sib pairs showed no significant differences in levels of Investigate and Allo-groom and neither pair type showed Aggression. Fullsib pairs, however, did show significantly lower levels of Investigate than did non-sib pairs. The fact that apparently aggressively motivated behaviours occur less often in female mice might be expected, since it is primarily males which aggressively defend family territories (Rowe & Redfern 1969; Harrington 1976; but see Mackintosh 1981) and the physiology of aggression is different between the sexes (Scott 1975), with females showing less tendency to fight than males. Both adult male and female full-sib and halfsib pairs showed significantly higher levels of Touch than non-sib pairs. Touch refers to apparently undirected, passive body contact between animals. Although it is not a category specifically distinguished by previous workers, its inclusion is important because it provides a qualitative index of spacing at times other than during specific interactions. In other interaction categories, there were differences between adults and juveniles. In particular, juvenile males and females of all pair types showed significantly more Investigate than adults. However, the relationship between age and frequency of performing aggressionrelated interactions is not clear-cut. In males, unrelated juveniles showed less AUo-groom and no Aggression, while in females there was no difference between juveniles and adults. In females, however, there was a significant increase in the amount of passive body contact (Touch) in adult half-sib and non-sib pairs. There was no similar increase in males. These results suggest different maturation effects between the sexes in patterns of social interaction which may
597
be influenced by the degree of relatedness between individuals. While the results of experiment 1 suggest an 'innate' kin recognition mechanism (in that, depending on age and sex, unfamiliar half sibs behave more like familiar full sibs than unfamiliar non-sibs in a variety of social interactions), there are complications. The most important is that, in both sexes and in both adults and juveniles, half-sib pairs differed significantly from full-sib pairs in their frequency of performing Sniff (classified by Dixon & Mackintosh as "social investigation') and Investigate. For Sniff, and in adult females, Investigate, half sibs did not differ significantly from non-sibs. These differences could be explained in three ways. They could be due to (a) individuals matching their responses to the detected degree of relatedness of their companion (see e.g. Greenberg 1979), hence responding to half sibs at levels intermediate between those for full sibs and non-sib partners; (b) a familiarity effect (full sibs are familiar whereas half sibs and non-sibs are unfamiliar); or (c) a combination of (a) and (b). There is an overwhelming literature showing the importance of familiarity in rodent social interactions (e.g. Poole & Morgan 1975; Huck & Banks 1979; Bekoff 1981; Geyer et al. 1981 ; Porter et al. 1981b). In order to control for confounding familiarity effects more closely, therefore, we carried out a second experiment.
Experiment 2 Methods The subjects tested in experiment 2 were 154 male C. F. L. P. mice. All were tested as adults at 66-73 days of age. The mice were drawn from 32 litters of known relationship. Shortly before birth, the litters were arranged to produce different degrees of relatedness and familiarity among individuals. Eight litters of half sibs (again sharing only paternity) were born with two litters per cage. Eight litters of non-sibs were arranged similarly, and eight litters each of half sibs and non-sibs were born and reared as single litters in separate cages. All mice were individually marked so their litter of origin and parentage were known, and all were reared by their own mothers. All individuals born and reared in the same cage were considered to be 'familiar' at the time of testing. When litters reached 32 days of age, females were removed and the number of males in each cage was reduced to a maximum of eight. Other conditions
598
ANIMAL
BEHAVIOUR,
of maintenance were identical to those in experiment 1. Animals were assigned for testing into arbitrarily picked pairs of familiar half sibs (F-HS, 13 pairs), familiar non-sibs (F-NK, 11 pairs), unfamiliar half sibs (UF-HS, 17 pairs) and unfamiliar non-sibs (UF-NK, 20 pairs). Sixteen pairs of full sibs, each pair from a different litter, were also tested. Pairs were tested in exactly the same way as those in experiment 1: However, some interaction categories recorded in experiment 1 were subdivided into more precise identifiable categories, and some additional behaviours not recorded in experiment 1 were included. Some of the additional behaviours referred to the actions of just one individual rather than to interactions between both members of a pair. The modified or additional behaviour categories are defined similarly to those of Grant & Mackintosh (1963) and van Oortmerssen (1971). Modified categories. Allo-groom of experiment 1 was subdivided into two components: Social Groom: licking and mandibulating the fur of the companion, mostly on the head and back. This sometimes involved placing forepaws on the companion. Aggressive Groom; vigorous licking and mandibulation of the companion's fur, often localized at the shoulder region; fur sometimes pulled with the teeth. Additional categories: Follow: following a locomoting companion. Squire: following a locomoting partner while maintaining nasal contact with the companion's fur. Self-groom: wiping, licking and nibbling own fur with forepaws, tongue or teeth. Sniffing at sawdust: standing still, usually briefly, with nose in the sawdust. Sometimes the sawdust was pushed sideways with the nose or forepaws. Upright: standing or 'sitting' on hind legs, sniffing the air. Total Exploration: the total frequency of Sniffing at Sawdust and Upright. Total Interaction: the total frequency of all behaviours which involved mutual interaction. Results Mean frequencies of performance of each behavioural category for each pair type are shown in Table II. When scores for U F - N K and U F - H S pairs are compared, similar trends
30,
2
emerge to those in experiment 1. U F - H S mice showed significantly less Investigate and significantly more Touch t h a n U F - N K mice (Table III). Although there were no significant differences in scores for Social Groom and Aggressive Groom (combined as Allo-groom in experiment 1), U F - N K pairs were the only ones with a score greater than zero for Aggressive Groom. Similarly, the mean frequency of Aggression in U F - N K pairs was 4.5 times higher than the the next highest mean (F-HS pairs), although the difference was not significant. When F - N K and F-HS pairs (in which companions are familiar with one another) are compared, however, all significant differences disappear. The effects of familiarity were more pronounced in nonsibs than in half sibs. Column 3 of Table III, comparing U F - N K and F - N K pairs, shows that all significant differences had an associated probability of 2 % or less. Column 4, comparing UF-HS and F-HS pairs, shows only 50% of significant differences with probabilities of 2% or less. Familiar animals (both half-sib and non-sib) tended to Sniff and Investigate less often and hence show less Total Interaction, but performed more Upright and Total Exploration activity. In addition, F-HS pairs showed less Squire + Follow (lumped in analysis) compared with U F - H S pairs, and F - N K pairs showed more Sniff at Sawdust. When U F - H S pairs are compared with fullsib pairs (Table III, column 6), significant differences between the two pair types are mainly similar to those in experiment 1. U F - H S pairs showed more Sniff and Investigate, but this time also showed less Touch (cf. Table Ia, b). In addition, UF-HS pairs showed more Squire + Follow and less Sniff at Sawdust and Total Exploration. When full-sib and F-HS pairs are compared, however, no significant differences emerge (Table III, column 5). Discussion The results of the experiments described here suggest the existence of a kin recognition mechanism in mice which appears not to depend on prior experience with encountered animals. Unfamiliar non-siblings tended to show less passive body contact and more interactions related to aggression than did unfamiliar half siblings. Unfamiliar half sibs however, did not always interact in the same way as full sibs. They differed significantly from full sibs in the direction of non-sib scores in 33 % of recorded categories in experiment 1 and 43 % of recorded
K A R E E M & B A R N A R D : KINSHIP A N D F A M I L I A R I T Y IN MICE
599
r u l e o u t s e l f - f a m i l i a r i t y as a m e c h a n i s m f o r rec o g n i t i o n b e t w e e n u n f a m i l i a r h a l f s i b s , t h i s is n o t a n i m p o r t a n t difficulty. T h e i m p o r t a n t f i n d i n g o f t h i s s t u d y is t h e a p p a r e n t a b i l i t y o f m i c e t o r e c o g n i z e h a l f sibs w i t h o u t a n y p r i o r experience of them. Whether they achieve this by an innate recognition mechanism or by r e c o g n i z i n g c u e s t h e y t h e m s e l v e s p o s s e s s is l a r g e l y i m m a t e r i a l . W h a t m a t t e r s is t h a t m i c e h a v e e v i d e n t l y b e e n s e l e c t e d t o r e c o g n i z e close relatives and to respond differently towards t h e m a t a first m e e t i n g . A n o t h e r i m p o r t a n t f i n d i n g o f t h e s t u d y is t h a t k i n d i s c r i m i n a t i o n is n o t a p p a r e n t i n all t y p e s o f i n t e r a c t i o n s . I t it m o s t p r o n o u n c e d i n
c a t e g o r i e s i n e x p e r i m e n t 2. C o m p a r i s o n b e t w e e n a d u l t m a l e f u l l sibs a n d f a m i l i a r h a l f s i b s suggested these differences were due to unfamiliarity r a t h e r t h a n r e c o g n i t i o n o f a l o w e r d e g r e e o f relatedness. Similarly, differences between nons i b a n d b o t h h a l f - s i b a n d fuU-sib p a i r s d i s a p peared when companions had had prior experience of one another. The fact that familiarity h a d a m o r e p r o n o u n c e d effect o n b e h a v i o u r i n non-sib pairs bears out the tendency for half sibs' scores to be intermediate between those for non-sib and full-sib pairs in a wide range of c a t e g o r i e s ( T a b l e II). W h i l e , i n c o m m o n w i t h o t h e r s t u d i e s ( W u et al. 1980; B l a u s t e i n & O ' H a r a 1981), w e c a n n o t
Table II. Frequency (Mean • SE) of Each Behavioural Category Performed per 5 rain by Each Pair Type in Experiment 2
Unfamiliar non-sibs (N = 20 pairs) Sniff Investigate Nose Squire+Follow Aggression Aggressive G r o o m Social Groom Touch Total Interaction Self-groom Sniffing at Sawdust Upright Total Exploration Total Activity
6.25 12.80 5.40 3.45 6.25 0.10 0.60 9.90 44.75 1.35 18.65 79.50 98.15 144.25
Unfamiliar half sibs (N = 17 pairs)
• t.ll • 0.80 4- 0.81 4- 0.60 4- 3.22 4- 0.10 4- 0.22 4- 1.39 4- 2.60 • 0.23 :~ 2.00 4- 3.92 4- 5.16 4- 3.24
3.77 9.29 5.65 3.88 1.00 0 1.53 15.41 40.53 1.82 19.65 84.18 103.82 146.18
Familiar non-sibs (N = 11 pairs)
4- 0.77 =L 0.91 4- 1.02 4- 0.69 4- 0.94 44444444-
0.62 1.50 1.47 0.t5 1.00 4.15 4.46 4.25
1.46 7.18 3.18 1.64 0 0 0 20.64 34.09 1.46 26.36 94.27 120.64 156.18
4444-
0.49 1.29 0.64 0.45
444444•
1.16 1.64 0.25 1.56 3.14 3.51 3.60
Familiar half sibs (N = 13 pairs) 1.23 5.54 3.62 1.0 1.39 0 0.39 20.15 33.31 1.54 22.92 96.69 119.62 154.46
4• • i 4-
0.28 1.38 0.54 0.42 0.90
44• 444• 4-
0.19 1.70 1.98 0.24 1.72 3.92 4.48 4.88
Table HI. Comparisons between Pair Types of the Frequency of Each Behavioural Category per 5 rain in Experiment 2
Comparisons
Behaviour Sniff Investigate Nose Squire + follow Aggression Aggressive groom Social groom Touch Total interaction Self-groom Sniff at Sawdust Upright Total exploration Total activity
UF-NK vs UF-HS
F-NK vs F-HS
--
--
**
. -. . . * -. ---.
--
--. ---.
*
.
.
. . . *** *** . ** ** **** .
. . .
-. . .
.
*
****
.
. . .
UF-HS vs F-HS
***
--
.
UF-NK vs F-NK
.
FS vs UF-HS
--
*
--
****
--
***
---
*** --
----
** -*
. *** . . . -***
.
. -* **
.
FS vs F-HS
.
*P < 0.05; **P < 0.02; ***P < 0.01; ****P < 0.002 (Mann-Whitney U-test).
Full sibs (N = 16 pairs) 1.69 4.81 3.31 1.38 1.38 0 0.25 22.88 35.81 1.63 24.0 94.56 118.56 156.0
44• 44-
0.71 1.10 0.52 0.35 1.38
44444444-
0.19 2.00 2.30 0.18 1.28 3.81 4.24 5.21
600
ANIMAL
BEHAVIOUR,
those types which tend to be associated with aggression, and in the frequency o f undirected, passive body contact. In general, however, mice appear to use familiarity as a rule of thumb (see Dawkins 1979; Bekoff 1981) during interaction. Prior familiarity completely overrides differences in the degree of relatedness in deciding patterns of interaction. A 'regard familiar individuals as kin' rule is likely to operate well in the wild. House mice tend to live in small, closed breeding groups (for details, see Anderson 1970; Berry 1981), maintained mainly by males defending group territories (Harrington 1976; but see Mackintosh (1981) for the possible role of pregnant females in territorial defence). Individuals able to regulate their aggressive responses, and the initiation of interactions likely to lead to aggression, according to the detected degree of kinship in an unfamiliar companion, are likely to increase their inclusive fitness, We should therefore expect the familiarity rule of thumb to operate only for interactions like Sniff, Nose and following behaviour, where the cost of mistaken identity is likely to be low. We should expect a back-up recognition mechanism which distinguishes closely related from other unfamiliar individuals when potentially aggressive interactions are involved. Discrimination in aggression-related interactions m a y be less important in adult female mice. Since females are not usually involved in group defence, the familiarity rule as a guide to patterns of interaction may be evolutionarily more economical. Among adult females, the only apparent discrimination based on kinship occurred in Touch. Increased frequency of passive body contact between unfamiliar half sibs occurred in both males and females, and may have been associated with a reduced risk of close contact leading to aggression. Related and familiar animals are undoubtedly recognized on the basis of olfactory cues (see Brown 1979; Halpin 1980). Archer (1968) suggested that the odour of male mice had two functionally distinct components. One component was of a general nature and tended to elicit attack by another male: the other was an 'identifier' specific to an individual. Animals housed together habituated to each other's individual identifier and only animals with unfamiliar identifiers were subsequently attacked. In addition, group members tend to scent-mark each other so that all end up with a composite 'group scent' (Brown 1979). There is good experimental evidence for individual recogni-
30,
2
tion by odour in mice (Mackintosh & Grant 1966; Bowers & Alexander 1967; Kalkowski 1967: H a h n & Simmel 1968; Kimelman & Lubow 1974). It m a y be that such odours are similiar in closely related individuals and so form the basis for the recognition of nonfamiliar kin demonstrated here.
Acknowledgments We thank Hilary Stephens, Desmond Thompson and Chris Brown for reading an earlier draft of the manuscript and two anonymous referees for helpful criticism. The work was supported by a grant from the University of Sulaimaniyah to A. M. K. REFERENCES Anderson, P. K. 1970. Ecological structure and gene flow in small mammals. Symp. zool. Soc. Lond., 26, 299-325. Archer, J. 1968. The effect of strange male odor on aggressive behavior in male mice. J. Mammal., 49, 572-575. Banks, E. M. 1962. A time and motion study of prefighting behavior in mice. J. genet. PsychoL, 101, 165183. Bekoff, M. 1981. Mammalian sibling interactions: genes, facilitative environments and the coefficient of familiarity. In: Parental Care in Mammals (Ed. by D. J. Guberniek & P. H. Klopfer), pp. 307-346. New York: Plenum Press. Berry, R. J. 1981. Population dynamics of the house mouse. Symp. zooL Soc. Lond., 47, 395--425. Blaustein, A. R. & O'Hara, R. K. 1981. Genetic control for sibling recognition. Nature, Lond., 290, 246248. Bowers, J. M. & Alexander, B. K. 1967. Mice: individual recognition by olfactory cues. Science, N.Y., 158, 1208-1210. Brown, R. E. 1979. Mammalian social odours: a critical review. Adv. Study Behav., 10, 103-162. Clark, L. H. & Sehein, M. W. 1966. Activities associated with conflict behaviour in mice. Anim. Behav., 14, 44--49. Dawkins, R. 1979. Twelve misunderstandings of kin selection. Z. TierpsychoL, 51, 184-200. Dixon, A. K. & Mackintosh, J. H. 1976. Olfactory mechanisms affording protection from attack to juvenile mice (Mus musculus L.). Z. Tierpsychol., 41, 225-234. Geyer, L. A., Beauchamp, G. K., Seygal, G. & Rogers, J. G. Jr. 1981. Social behaviour of pine voles, Microtus pinetorum: effects of gender, familiarity and isolation. Behav. neut. BioL, 31, 331-341. Gilder, P. M. & Slater, P. J. B. 1978. Interest of mice in conspeeifie male odours is influenced by degree of kinship. Nature, Lond., 274, 364-365. Grant, E. C. & Mackintosh, J. H. 1963. A comparison of the social postures of some common laboratory rodents. Behaviour, 21, 246--259. Greenberg, L. 1979. Genetic component of bee odor in kin recognition. Science, N.Y., 206, 1095-1097. Hahn, M. E. & Simmel, E. C. 1968. Individual recognition by natural concentrations of olfactory cues in mice. Psychon. Sci., 12, 183-184.
K A R E E M & B A R N A R D : KINSHIP A N D FAMILIARITY "IN MICE Halpin, Z. T. 1980. Individual odors and individual recognition: review and conmaentary. Biol. Behav., 5, 233-248. Hamilton, W. D. 1964. The genetical evolution of social hehaviour. J. theoret. BioL, 7, 1-52. Harrington, J. E. 1976. Recognition of territorial boundaries by olfactory cues in mice (Mus muscuhts L.). Z. Tierpsychol., 41, 295-306. Huck, U. W. & Banks, E. M. 1979. Behavioral components of individual recognition in the collared lemming (Dicrostonyx groenlandicus). Behav. Ecol. SociobioL, 6, 85-90. Kalkowski, W. 1967. Olfactory bases of social orientation in the white mouse. Folia bioL, Krakow, 15, 69-87. Kimelman, B . R . & Lubow, R. E. 1974. The inhibitory effect of pre-exposed olfactory cues on intermale aggression in mice. PhysioL Behav., 12, 919-922. Mackintosh, J. H. 1981. Behaviour of the house mouse. Symp. zooL Soc. Lond., 47, 337-365. Mackintosh, J. H. & Grant, E. C. 1966. The effect of olfactory stimuli on the agonistic behaviour of laboratory mice. Z. Tierpsychol., 23, 584-587. Maynard Smith, J. 1964. Kin selection and group selection. Nature, Lond., 201, 1145-1147. Oortmerssen, G. A. van. 1971. Biological significance, genetic and evolutionary origin of variability in behaviour within and between inbred strains of mice (Mus masculus). Behaviour, 38, 1-92. Poole, T. B. & Morgan, H. D. R. 1975. Aggressive behaviour of male mice (Mus musculas) towards familiar and unfamiliar opponents. Anim. Behav., 23, 470-479.
601
Porter, R. H. & Wyrick, M, 1979. Sibling recognition in spiny mice (Acomys cahirinus): influence of age and isolation. Anim. Behav., 27, 761-766. Porter, R. H., Wyrick, M. & Pankey, J. 1978. Sibling recognition in spiny mice (Acomys cahirinus). Behav. EcoL SociobioL, 3, 61-68. Porter, R. H., Moore, J. D. & White, D. M. 1981a. Food sharing by sibling versus nonsibling spiny mice
(Acomys cahirinus). Behav. EcoL Sociobiol., 8,
207-212. Porter, R. H., Tepper, V. J. & White, D. M. 1981b. Experiential influences on the development of huddling preferences and 'sibling' recognition in spiny mice. Dev. Psychobiol., 14, 375-382. Rowe, F. P. & Redfern, R. 1969. Aggressive behaviour in related and unrelated wild house mice (Mus musculus L.). Ann. appl. Biol., 64, 425--431. Scott, J. P. 1975. Aggression. Chicago, IL: University of Chicago Press. Southwick, C. H. 1970. Genetic and environmental variables influencing animal aggression. In: Animal Aggression (Ed. by C. H. Southwick), pp. 213-229. New York: Van Nostrand Reinhold. Waldman, B. & Adler, K. 1979. Toad tadpoles associate preferentially with siblings. Nature, Lond., 282, 611-613. Wu, H. M. H., Holmes, W. G., Medina, S. R. & Saekett, G. P. 1980. Kin preference in infant Macaca nemestrina. Nature, Lond., 285, 225-227.
(Received 8 July 1981 ; revised 22 September 1981 ; MS. number: 2146)