Some effects of strain differences in the maternal behavior of inbred mice

Some Effects of Strain Differences in the Maternal Behavior of Inbred Mice

ROGER WARD Debart em ent d e Psy chologie

Un iwsite’ d u Quebec h Tro is-R ivi2res Trois-RiviPres, Quibec, Canada

The frequencies of occurrence of a variety of activities were recorded for inbred female mice of 3 strains in the presence of their own offspring, in the presence of isogenic fostered offspring, and in the presence of nonisogenic fostered offspring. Differences in the frequency of nursing, of grooming and handling the offspring, and of the absence of t h e female from the nest were related t o differences in the rate of early postnatal development of 2 of these strains: in general, those pups receiving less maternal attention developed more rapidly. The effective stimulus for accelerated maturation may lie in the sequential organization of the manipulation of the offspring b y the foster mother, rather than in the overall quantity of manipulation received.

If newborn mammals are brought up by females of a different species, these fostered animals differ from their conventionally reared controls in a number of ways. Mice that are fostered onto rat mothers, for example, appear to be less aggressive, to be less active, to weigh more, to defecate less in an open field when compared to their controls, and to prefer rats to mice when placed in a test of social preference (Denenberg, Hudgens, & Zarrow, 1966; Denenberg, Paschke, & Zarrow, 1973, Hudgens, Denenberg, & Zarrow, 1967, 1968). Similar modifications of aggressiveness, open field activity, social preference and weight at weaning have been reported for cross-fostered laboratory mice and feral pygmy mice (Buiomys sp.; Quadagno & Banks, 1970).

When fostering takes place within a particular species rather than across a species barrier, its effects are less dramatic. Southwick (1968) reported that normally passive A/J mice became somewhat more aggressive if raised by CFW mothers, but that fostering by A/J mice had little if any effect upon the aggressive behavior of CFW mice. Lagerspetz and Wuorinen (1965) reported similar results of cross-fostering between stocks of mice selectively bred for high or low incidence of aggressive behavior. Broadhurst (1961) found that avoidance learning in rats selectively bred for performance at an avoidance task was not affected by cross-fostering between “high” and “10~’’ avoidance lines.

Reprint requests should be sent to Roger Ward, Ph.D., Dipartement de Psychologie, Ilnlvcrsit& d r ~ Q d b e c i Trois-Rivikres, C.P. 500, Trois-Rivikres, QuCbec G9A 5H7, Canada.

Received for publication 31 August 1978 Revised for publication 20 December 1978 Developmental PsychobioZogy, 13(2): 18 1-1 90 (1 980) @ 1980 by John Wiley & Sons, Inc. 001 2-1630/80/0013-0181501 .00

182 WARD

A number of explanations may be offered for these effects. For example, little or no variability of maternal behavior may exist within a single species, so that the postulated treatment is essentially t h e same for both groups when cross-fostering is carried out between inbred strains or selected stocks of the same species. Or, the particular behavioral phenotype chosen for study may be so deeply canalized (Waddington, 1957) that it fails to interact with cross-fostering and n o differences between groups can be detected.

An alternative theoretical approach may be offered which has been previously raised in a slightly different context by Ressler and Andersen (Andersen & Ressler, 1973; Ressler & Andersen, 1973). Those interactions between a mother and her progeny which subsequently influence the behavior of the progeny may be thought of as a process of transmission from generation t o generation by evidently non-Mendelian means, which has been described as “cultural” transmission (e.g., Medawar, 1959). Our knowledge of the mechanisms underlying this process is limited: beyond pointing out that some non- genetic process is responsible, for example, for the fact that some Canadians speak French while others speak English, or providing instances of the cultural transmission by unknown means of a definite trait (Collins, 1970, 1975), we are hampered by a lack of theoretical systems analogous t o those used in Mendelian contexts (e.g., Li, 1955; Mayr, 1963). By analogy with the analysis of Mendelian transmission, our appreciation of cultural transmission depends upon the existence of variability with respect t o the trait of interest. Although a certain amount is known about differences of maternal behavior between inbred strains of mice-for example, Ressler (1962) found that BALB/cJ mice handle their offspring more than d o C57BL/6J mice-the mechanisms underlying the effects of cross-fostering remain obscure (Quadagno & Banks, 1970).

The experiments and observations presented below seek to answer the following questions: To what extent does maternal behavior vary within a given population or species? To what extent may the effects of this variability express themselves in the offspring‘? What factors may be responsible for this variability? The 1 st experiment presents evidence concerning the differences that exist between 3 inbred strains of mice with respect to maternal behavior.

Experiment I

Method

Mice (Mns musculus) of the inbred strains A/J, C57BL/6J, and DBA/2J were used (hereafter referred to as A , B6, and D2, respectively). These 3 strains were chosen because each is free of retinal degeneration, a recessive form of blindness that affects a large number of commercially available inbred strains (Sidman & Green, 1965), and the coat colors differ markedly. All mice used, both in this experiment and in those described below, were the immediately progeny of mice obtained from the Production Department, The Jackson Laboratory, Bar Harbor. Maine, and were housed in clear plastic cages 28 X 13 X 18 cm on sawdust bedding with food and water continuously available. The animal quarters were illuminated between midnight and noon b y two 40-W fluorescent lamps controlled by a timer and were dimly lit between noon and midnight by a single 25-W in- candescent lamp.

MATERNAL BEHAVIOR AND DEVELOPMENT 183

TABLE 1. Relative Frequencies # and Durations ( t ) of’specified Activities.

A/J C5 7 8 L/6 J DBA/2J

Activity 0“ 0 ) mb (t) mc (0

(1) Out of nest (2) Start nurse (3) Nurse (4) Stop nurse (5) Groom/Handle (6) Retrieve (7) Nest maintenance (8) Groom self (9) Eat/Drink

(10) Miscellaneous

Comparison

.31 .26

.02 .oo

.02 .28

.02 .oo

.18 .06

.o 1 .oo

.06 .03

.15 .12

.14 .21

.09 .03

.20 . I9

.03 .o I

.05 .38

.03 .oo

.22 .oo

.02 .oo

.07 .05

.13 .I0

.13 .15

.13 .06

.36 .36

.o 1 .oo

.o 1 .15

.o 1 .oo

.o 1 .oo

.o 1 .oo

.06 .03

. I 1 .08

.14 .24

.2 1 .10

1 .o 1 .o I .o 1 .o 1 .o 1 .o Analysis of Frequency Data

G = DBA/2J vs (A/J C57BL/6J) + A/J vs C57BL/6J ( d j = 2)

( 1 ) vs (2-10) (2) vs (3-10) (3) vs (4-10) (4) vs (5-10) (5) vs (6-10) (6) vs (7-10) (7) vs (8-10) (8) vs (9-10) (9) vs (10)

75.21 4.69

23.26 9.52

68.78 5.20 2.90

21.41 27.01

38.77*** 4.59*

14.63*** 6.67**

67.61*** .26

2.39 19.23 *** 21.53***

36.44*** .10

8.63** 2.85 1.18 4.94*

.5 1 2.18 5.48*

237.98 178.68 62.30

***p < .001. **p < .01.

* p < .05. ‘n = 1130, 10 litters. bn = 1046, 15 litters.

= 935, 8 litters.

Matings were set up between pairs of mice, and as soon as the female was clearly pregnant the male was removed and housed separately. On the day following the birth of a litter and on each subsequent day until weaning, the female with her offspring was observed for 30 min and the onsets and durations of each of the 10 activities listed in Table 1 were recorded. (The category “out of nest” was used to cover all activities of the female during each absence.)

Given the correlation ( r = .55;F= 10.58,df= 1/28,p < .01) between frequency and duration data, the analysis presented below (and in Table 1 ) is concerned with frequencies of occurrence.

All observations were made between 1400 and 1700 hours, during the early part of the dark phase of the light cycle, initially by the author and a student assistant together and subsequently by one or the other of the pair.

184 WARD

The analysis of frequency data rely traditionally on the x2 statistic and its subsequent partitioning (Castellian, 1965; Maxwell, 1961). A disadvantage of this procedure is that under certain circumstances the components of the overall xz do not behave in a perfectly additive fashion (Sokal & Rohlf, 1969). In accordance with these later authors, the analysis below is based on the log likelihood ratio statistic, which they represent by G . After the calculation of an overall value of G for the 3 X 10 contingency table of frequencies upon which Table 1 is based, a series of 3 X 2 tables was constructed in which each activity was compared with all activities not hitherto examined. Each 3 X 2 table servied to provide a pair of 2 X 2 tables, each representing an individual comparison. Be- cause the initial value of the test statistic possesses 18 degrees of freedom, 18 such individual comparisons were made.

Results

Overall, G = 237.98 which, with 18 degrees of freedom, is highly significant. The individual comparisons show that the D2 mice differed from both A and B6 mice with respect to all activities save retrieval and nest maintenance, whereas A mice differed from B6 mice only with respect to absences from the nest, nursing, retrieval, and miscellaneous activities such as climbing on the bars of the cage or digging in the litter. If we make the assumption that experimental error is uniformly distributed throughout the original contingency table, we may express these differences in another way by saying that more than 70% (1 75.68/237.98) of the interaction between strain and activity comes from differences between the D2 mice on the one hand and both the A and B6 mice on the other, and roughly 30% from differences between the A mice and the B6 mice. In general, D2 mice appeared to have occupied themselves much less with nursing and grooming or handling their offspring than did mice of the other 2 strains.

An additional analysis was carried out in order to answer the question, whether differences in the serial ordering, or sequential organization, of behavior exist between the 3 strains. A series of transition matrices was constructed in which a given cell entry represented the relative frequency of transition between 2 behaviors, irrespective of direc- tion, for a single inbred strain. A 4th table was constructed by summation of cell entries across strains, from which a series of expected frequencies were derived. Differences between the frequencies of each transition for each of the inbred strains were evaluated by means of the log likelihood ratio statistic (Sokal & Rohlf, 1969) partitioned as before into a term for the difference between the D2 mice on the one hand and both the A and B6 mice on the other, and a term for the difference between the A mice and B6 mice. (Copies of the transition matrices, together with details of the computational procedures, are available from the author.) This analysis yielded the following: overall, significant differences existed between the 3 strains (G = 393.14, df= 9 0 , p < .001) which, in con- trast to the results of the initial analysis, arc more or less equally distributed among the 3 strains. The comparison between the D2 mice and both the A and B6 mice yielded G = 105.14 (df = 45, p < ,001) and the comparison between the A and B6 mice yielded G = 188.00 (dJ = 45. p < ,001).

Experiment I1

Both differences in the relative frequency and in the serial ordering of the 10 activities listed in Table 1 existed between the 3 inbred strains. The 2nd experiment serves to


illustrate some effects of these strain differences in maternal behavior upon the development of the offspring. It represents an extension of some observations originally made by M. Hottum, a student working under my supervision in the context of a National Science Foundation Summer Program.

Method

Matings between pairs of B6 mice and of D2 mice were set up as in the 1st experiment; these 2 strains, rather than all 3, were chosen on the grounds of convenience and in the light of the results of the 1st experiment. As before, when the female was clearly pregnant, the male was removed and housed separately. When 2 litters were born within 24 hr of each other, each litter was culled to 3 pups and exchanged between females. Four mother-offspring combinations were thus produced which will be referred to in the following notation: D2fD2, D2 pups raised by D2 females other than their natural mothers; B6fD2, B6 pups reared by D2 females: D2fB6, D2 pups reared by B6 females: and B6fB6, B6 pups reared by B6 females other than their natural mothers.

All pups were weighed daily during the period between birth and weaning, and were subjected to the battery of tests described by Fox (1965). Testing was carried out by the author and a student assistant, each observer noting separately the presence or absence of a particular response. In those cases where the observers disagreed the data were discarded for the purposes of this study. Data derived from 7 litters of D2fD2 pups, 16 litters of B6fB6, 10 litters of D2fB6, and 14 litters of B6fD2 in which all pups survived until weaning were analyzed.

Results

Of 22 tests, 11 failed to reveal any differences. Each of the 11 remaining tests indicated that D2fD2 mice developed more rapidly than B6fB6 mice, and 5 of these latter tests also indicated systematic differences between pups raised by isogenic females and by nonisogenic females (see Fig. 1). The B6fD2 mice develop slightly faster than B6fB6 mice, and D2fB6 slightly more slowly than D2fD2 mice.

Strain differences in development have been described previously (e.g., van Abeelen & Schooner, 1977; Fuller & Geils, 1973; Wahlsten, 1975) and the more rapid development of D2 mice when compared to B6 mice has also been noted (Wahlsten, 1975; J. M. Stewart, unpublished observations). That those mice which develop more rapidly are those which receive less parental handling and general nursing care (e.g., those reared by D2 females) is surprising given the results presented above and in the light of Levine’s (1962) demonstration of the effects of early infantile manipulation, and by analogy with the stimulus-induced maturation of neuronal structures (Hughes, 1960, 1965). However, certain evidence enables us to question the generality of Levine’s (1 962) findings (Bar- nett & Burn, 1967; Cross & Labarba, 1978). In addition, the derivation of a single inbred strain necessarily involves not only the forcing of homozygosity by brother-sister mating (Green, 1970; Staats, 1966) but must also involve directional selection for reproductive performance. A potential inbred strain in which recessive characters diminishing reproductive performance emerge with successive increases in the inbreeding coefficient will die out before the requisite 20 generations of inbreeding have been realized. Moreover,

186 WARD

1.0-

0.5

C

%

0

e

walk forward farepow grosprng

Fig. 1. Age of appearance of forepaw and hindpaw grasping, walking forward, visual placing, and age of opening of eyes of mice fostered onto isogenic or nonisogenic females. Numbers in parentheses refer to the number of litters, each of 3 pups, that were examined.

one of the major components of overall reproductive performance is the postnatal development of the offspring. Thus the genetic history of the DBA/2 strain may involve the fixation of a genotypic combination expressing itself both as a reduction in the frequency of maternal behavior directed at the offspring and as an acceleration of postnatal development. However, this argument does not enable us to explain the effect upon the development of B6 mice of fostering onto D2 females nor the retardation of development seen in D2fEi6 mice (see Fig. 1). On the basis of the data presented so far we cannot assert that the behavior of a female towards her offspring is independent of the behavior of the offspring towards the female, that is, the behavior of females towards isogenic offspring may be the same as the behavior of females of the same strain towards nonisogenic offspring. The 3rd experiment to be described seeks to resolve this lack of evidence.

Experiment I11

Method

Matings were set up as before between pairs of A mice, pairs of B6 mice, and pairs of D2 mice. Following the procedure described in Experiment 11, litters born within 24 hr of each other were exchanged between females, so that all possible combinations of maternal and filial genotypes were created, with no pups being brought up by their natural mothers. As in the 1st experiment, the behavior of each female towards her


foster-offspring was recorded for 30 min daily between birth and weaning; observations were made during the early part of the dark phase of the light cycle.

Results

The analysis of the relative frequencies of the 10 activities follows that used in the 1st experiment: an overall value of the log likelihood ratio statistic was calculated for each maternal genotype, and subsequently partitioned into terms which examine each individual comparison. (The complete analysis is available from the author. The relative frequencies are presented in Table 2.) If, as before, we assume a uniform distribution of experimental error, the individual comparisons may be combined in a variety of ways each of which reveals a different aspect of the situation. Overall, G = 387.80 (df= 54, p < .OO 1) ; the comparison between isogenic and nonisogenic mother-offspring combinations gives G = 229.01 (df= 27) amounting to 60% of the total, comparisons within nonisogenic combinations giving G = 158.79 (df= 27) amounting to 40% of the total. Those differences involving absences from the nest yield C = 55.76 (df= 6, 15% of the total interaction); differences involving nursing and handling yield G = 96.28 (df= 30,25% of the total), and differences involving other activities yield G = 235.76 (df= 18,60% of the total). Finally, those differences involving D2 foster mothers give G = 203.66 (df= 18, 53% of the total), those involving A foster mothers give G = 126.68 (df= 18,32% of the total), and those involving A foster mothers give G = 126.68 (df= 18,32% of the total), and those involving B6 fostermothers give G = 57.46 (df= 18, 15% of the total). We thus note that differences between isogenic and nonisogenic combinations are only slightly greater than difference within nonisogenic combinations, that the major component of these differences involves activities other than presence in the nest and nursing or handling, and that of the 3 strains examined D2 mice appear to be the most affected by the presence of nonisogenic offspring, B6 mice the least, with A mice intermediate.

Discussion

These 3 experiments taken together indicate that strain differences in maternal behavior exist in mice (notably with respect to absences from the nest and nursing or handling the offspring), that mice reared by isogenic foster mothers develop slightly differently from mice reared by nonisogenic foster mothers, and that the modification of maternal behavior by nonisogenic offspring appears to affect behaviors other than nursing or handling.

The modification of maternal behavior by nonisogenic offspring presumably arises through variations in responsiveness of the female to cues emitted by the offspring and, thus, represents a classical genotypeenvironment interaction. The D2 mice in general occupied themselves little with their offspring. Given that ultrasonic vocalizations of rodent pups influence maternal behavior (Colvin, 1973; Noirot, 1972), that D2 mice suffer from auditory anomalies associated with their proneness to audiogenic seizure (Henry & Saleh, 1975; Ward, 1972), and that D2 mice, of the 3 strains examined, are the most influenced by the presence of nonisogenic offspring, then either D2 mice are more reactive than mice of the other 2 strains to differences in auditory stimulation or, alter-

188 WARD

TABLE 2. Relative Frequencies ofActivities of Female Mice Rearing Isogenic or Nonisogenic 0 ffspring.

Activitya Offspring-Foster Mother Combination

AfA

.21** *c

.o 2

.03

.02

. lo*

.oo**

.O 8

.I6

.11

.25

B6fA (8)

.39

.04 .03 .02 .03 .oo .Ol .19

.20

.on

D2fA (7)

.30*d

.02*

.01

.01

.06

.02**

.12***

.14

.15**

.17

1 .o

B6fB6 (10)

.29

.05

.04

.03

.07

.03

.05**

. lo*

.17 16%:'

1 .0

D2fD2 (10)

.39

.oo**

.00*

.OO*

.05

.03

.17***

.14*

.11

. I 1

1 .o

AfB6 (8)

.19

.06

.06

.05

.07

.o 1

. I 3

.13

.10

.19 ___ 1 .0

Afl12 (8)

.29

.02

.o 1

.00

.0 3

.02

.03

.14

.18

.27

1 .o

D2fB6 (12)

.28*

.03

.03

.03

.05

.05**

.08*

.13

.10

.20

1 .0

r m ~ 2 (10)

.39**

.02

.02

.o I ** .06** .02 .02 .16** .19*** . I 0

1 .o 1 .o 1 .o

"Activities numbered as in Table 1 . bNumber of litters examined. 'Results of comparison of isogenic versus nonisogenic. dWithin nonisogenic. ***p < .001. * *p < .01.

*p < .05.


natively, differential auditory stimulation is less important than, say, differential olfactory stimulation in bringing about modifications of behavior of D2 mice in the presence of nonisogenic offspring.

Not all activities of the female were equally affected by nonisogenic offspring; those activities such as nursing or handling which are directed at the offspring are less affected than activities which do not directly involve the offspring. This state of affairs may have arisen from the canalization (Waddington, 1957) or buffering (Mayr, 1963) of the underlying genotypic mechanisms in response to stabilizing selection. Hence, the effects of cross-fostering seen in Experiment I1 were not, in all likelihood, brought about by simple differences in the overall frequency of manipulation of the offspring. This conclusion is supported by Cross and Labarba (1968) who inferred, from an examination of between- litter difference in the handling of BALB/cJ mice by their mothers, that simple amounts of manipulation could not explain differences in the rate of development of the pups. The most probable agent for the effect is the difference in serial ordering of maternal behavior; the alternative, that it is produced by those activities of the female which are not directed towards the offspring, is unlikely enough to be set aside.

Notes

This work was supported in part by the National Research Council of Canada and in part by the Fonds Institutionnel de Recherche de l’Universit6 du Que%ec. I thank H. Larivibre for assistance.

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Some effects of strain differences in the maternal behavior of inbred mice

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