Christophe Féron

Social regulation of reproduction in the female mound-builder mouse (Mus spicilegus)

Social environment influences the reproductive physiology and sexual behaviour of the female house mouse Mus musculus. An all-female environment tends to suppress the oestrous cycles, whereas the presence of a male induces and synchronises sexual receptivity. However, reproductive responses to social environment may differ among the various species of rodents. In mound-builder female mice, Mus spicilegus, periods of sexual receptivity are interrupted by periods where adult females display a vaginal closure. We investigated the influence of different social environments on the vaginal opening and oestrous state of adult female M. spicilegus. Result showed that when females were grouped their vaginas were generally closed but that vaginal opening occurred when they were isolated or housed with a sexual partner. Females became sexually receptive when housed with a male, but when isolated their cervical smears did not reach characteristics of the oestrus. In female M. spicilegus, male presence thus has a stimulating effect on oestrous induction. Furthermore, cohabitation with females has an inhibiting effect on vaginal opening.

Seasonal reproduction and delayed sexual maturity in mound-building mice Mus spicilegus

In the mound-building mouse, Mus spicilegus, which is found from Central to Eastern Europe, reproduction is seasonal and limited to spring and summer. In autumn, the mice build voluminous mounds composed of vegetable matter covered with earth, where juvenile animals (autumnal individuals) over-winter in groups without reproducing. Autumnal animals delay reproduction until the next spring when they are 6 months old. The influence and interactions of environmental (short light period and cold temperature (C conditions) compared with long light period and temperate temperature (T conditions)) and social factors (lack of odours from breeding adults (NB conditions) compared with presence of odours from breeding adults (B conditions)) on reproduction and sexual maturation were studied. Forty groups of three autumnal individuals (two males and a female or two females and a male) were placed in four experimental conditions (CB, CNB, TB and TNB), corresponding to interactions between environmental and social factors (n = 10 groups for each condition). Of the 40 groups only one initiated reproduction during the 18 weeks of cohabitation. Subsequently, animals were separated and isolated for 1 month and then paired with unfamiliar partners. Reproduction was monitored for an additional month, and 24 out of 39 females reproduced. In addition, of eight reproducing pairs placed in C conditions and 10 reproducing pairs maintained in T conditions, all but one pair continued reproduction. It was concluded that the delay in reproduction observed in autumnal individuals was the result of the social effects of living in groups as opposed to the environmental conditions of winter.

Paternal care in the mound-building mouse reduces inter-litter intervals

In many rodent species males display paternal behaviour. The primary reported effect of this paternal care is to increase pup survival. In mammal females, pregnancy and lactation are energetically demanding, especially when they are concurrent in post-partum reproduction. To face this energy requirement, females generally lengthen the duration of their post-partum pregnancy. In the present study we tested whether paternal care could affect this duration in the monogamous mound building mouse Mus spicilegus. In this species, females have a short reproductive life that does not exceed 4 months. Reduction of inter-delivery latencies would then be an efficient way to increase reproductive success. In a male removal experiment, we showed that inter-delivery latency was shortened by male presence. Moreover, behavioural estimations of paternal involvement were correlated with inter-delivery latency. The longer the male spent inside the nest the shorter the inter-delivery latency. In the mound-building mouse, the female might be able to monopolise the parental care of a single male, which could be important for the evolution of monogamy. The characteristics of first reproduction as compared to post-partum reproduction suggest that it may contribute to the formation of a strong and exclusive social bond between the reproductive partners.

Deficit in reproduction in polygynously mated females of the monogamous mound-building mouse Mus spicilegus

In monogamous mound-building mice Mus spicilegus, facultative polygyny was observed in April, at the beginning of the reproductive season. In order to evaluate the cost of polygyny, we compared, under laboratory conditions, the reproductive success of trios and pairs composed of sister females mated with unrelated brother males. Females in trios were able to tolerate each other during the reproductive period and to reproduce with the same male under spatial constraints. Nevertheless, polygyny had a strong negative effect on the reproductive success of the females. The average number of young per litter was smaller in trio females than in paired females, whereas the interval between two successive litters was higher. As a result, the number of litters and the number of young per time unit were smaller in each of the trio females compared with paired females. Agonistic behaviour being absent in trios, our results strongly suggest that living in trios led to pheromonal production that affected the female physiological state and reproduction. Males of trios did not obtain a better reproductive success than males in pairs.

Comparison of Urinary Scents of Two Related Mouse Species, Mus spicilegus and Mus domesticus

Whereas the house mouse (Mus domesticus) has been studied extensively in terms of physiology/behavior and pheromonal attributes, the evolutionarily related mound-building mouse (Mus spicilegus) has received attention only recently due to its divergent behavioral traits related to olfaction. To date, no chemical studies on urinary volatile compounds have been performed on M. spicilegus. The rationale for our investigations was to determine if there are differences in urinary volatiles of intact and castrated M. spicilegus males and to explore further whether this species could utilize the same or structurally similar pheromones as the male house mouse, M. domesticus. The use of capillary gas chromatography/mass spectrometry (GC-MS) together with sorptive stir bar extraction sampling enabled quantitative comparisons between the intact and castrated M. spicilegus urinary profiles. Additionally, through GC-MS and atomic emission (sulfur-selective) detection, we identified qualitative molecular differences between intact M. spicilegus and M. domesticus. A series of volatile and odoriferous lactones and the presence of coumarin were the unique features of M. spicilegus, as was the notable absence of 2-sec-butyl-4,5-dihydrothiazole (a prominent M. domesticus male pheromone) and other sulfur-containing compounds. Castration of M. spicilegus males eliminated several substances, including δ-hexalactone and γ-octalactone, and substantially decreased additional compounds, suggesting their possible role in chemical communication. Some other M. domesticus pheromone components were also found in M. spicilegus urine. These comparative chemical analyses support the notion of metabolic similarities as well as the uniqueness of some volatiles for M. spicilegus, which may have a distinct physiological function in reproduction and behavior.

Sexual experience and preferences for odors of estrous females in staggerer mutant male mice

Staggerer mutant male mice generally do not mate and olfactory disabilities may be involved. Choice tests were used to determine the preference of C57BL/6 male mice with the staggerer mutation for urine and vaginal secretions from receptive and unreceptive females. The staggerer mutation does not prevent the olfactory discrimination between vaginal secretions of estrous and anestrous females. Male preferences for odors of receptive females are related to the presence of sexual experience.

Reactions of staggerer and non-mutant male mice to female urine and vaginal secretion odors

Previous studies have shown that staggerer male mice do not copulate spontaneously. When meeting unfamiliar non-mutant females either in estrus or in anestrus condition, these neurological mutants behave similarly. One possible explanation is that staggerer males are unable to detect female odors. To test this hypothesis, male reactions to urine and vaginal secretions of females, either in estrous or in anestrous, were studied in a circular device allowing mutant and non-mutant males to move and to explore sources of odors during 20 minutes. Concerning vaginal secretions odors, the duration of time spent in different sectors by mutants was identical for both conditions of female sexual receptivity whereas non-mutant males spent more time on location with vaginal secretions of estrus females. For non-mutant and mutant males as well, duration of time spent in sectors with urine odors was similar for both conditions of female sexual receptivity. We hypothetised a possible deficiency for social odor detection and/or integration due to the staggerer mutation.

Behavioral differentiation during collective building in wild mice Mus spicilegus

Although well documented in social insects, the possibility of behavioral differentiation during collective building has been poorly studied in mammals. In this context, the mound-building mouse Mus spicilegus is an interesting model. Under natural conditions, juveniles from different litters gather vegetal material and build a sophisticated structure, the mound, under which the mice will spend winter. The first steps of this complex building process may be elicited under laboratory conditions by offering cotton balls as building material. Spatio-temporal distribution of both animals and cotton balls was automatically recorded by RFID (Radio-Frequency Identification Device) technique. Our results revealed a behavioral differentiation during a collective building task. In a group of six individuals, only two mice (called carriers) transported 80% of the building material whereas the contribution of the remaining mice was weak or even non-existent. The proportion of carriers was constant in all of the six groups studied. This behavioral differentiation was implemented immediately after the building material was made available and remained stable during the 4 days of experiment. The high contribution level of carriers did not result from resource monopolization, nor did it depend on the gender or parental origin of the mice.

Male—female interactions in staggerer and non-mutant mice: impairment to react to novelty as a possible explanation of staggerer male social behaviour

Associated with neurological anomalies, many behavioural deficits are induced by the staggerer mutation. In order to define the consequences of this mutation on the staggerer male social behaviour we realised experimental dyadic encounters with non-mutant and unfamiliar females, either in estrous or in anestrous condition. We compared mutant behaviour to non-mutant male behaviour. Staggerer male behaviour presents the same characteristics during encounters with both types of females. It differs from non-mutant male behaviour in a similar context. Non-mutant males present more interactions (social interest, sniffing and sexual behaviours) with females than staggerer males. Females modify their behaviour as a function of their state of receptivity and according to their partner. Behaviours of staggerer males towards females may be interpreted in terms of general exploratory behaviour.

Early behavioral development of mice is affected by staggerer mutation as soon as postnatal day three

Staggerer is a neurological mutation of mice that affects the development of the central nervous system and causes abnormal behaviors. The staggerer cerebellum is already abnormal at birth and as the animal grows up there is a progressive loss of granule cells which have all disappeared by day 28. The earliest behavioral disturbance observed is a motor deficiency which occurs between 10 and 15 days-i.e. several days later than the appearance of the cortical abnormalities. To show that staggerer mutant mice also differ from normal mice in behavioral aspects before the age of 10 days, 28 staggerer pups and 246 normal pups aged from 1 to 9 days underwent different motor tests. In addition, the number of ultrasounds emitted during 40 s was recorded, and the animals were weighted every day. Differences between staggerer and normal mice were found as early as 3 days: staggerers were less efficient in motor tasks and they weighed less than normal mice. Staggerers also differed from normal mice in ultrasound production.