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Female sexual preferences differ in mus spicilegus and mus musculus domesticus: the role of familiarization and sexual experience

ANIMAL BEHAVIOUR, 1998, 56, 1465–1470
Article No. ar980919
Female sexual preferences differ in Mus spicilegus and Mus musculus domesticus: the role of familiarization B. PATRIS & C. BAUDOIN
Laboratoire d’Ethologie Expe´rimentale et Compare´e, CNRS UPRES-A 7025, Universite´ Paris-Nord (Received 19 January 1998; initial acceptance 19 February 1998; final acceptance 19 June 1998; MS. number: 5754R) ABSTRACT
Mating systems correspond to particular ecological conditions and result from proximate interactionsbetween individuals. We compared the mating preferences of female mice of two species: the housemouse, Mus musculus domesticus, and the mound-builder mouse, Mus spicilegus. Because of differences intheir habitat, we expected to observe differences in their sexual preferences. We studied femalepreferences for a familiar or an unfamiliar male and the occurrence of copulation with the unfamiliarmale, during two states of female sexual activity: (1) the postpartum oestrus of paired females, to evaluatethe stability of their sexual partnership; and (2) the oestrus of females familiarized with a male, to studythe mechanisms underlying their sexual preferences. In the polygamous house mouse, postpartumoestrous females did not show a clear preference between their familiar male and the unfamiliarone. Moreover, oestrous females, familiarized with a male (without sexual interactions), preferred anunfamiliar male and copulated with him. In contrast, postpartum oestrous females and oestrous femalesof M. spicilegus preferred their familiar male and rarely copulated with the unfamiliar male. This studyindicates a strong pair bond in established breeding pairs in M. spicilegus and shows that this bond can beestablished by familiarization, which is not the case in M. m. domesticus. Our study suggests the existenceof monogamous traits in M. spicilegus in contrast to the polygamous M. m. domesticus.
1998 The Association for the Study of Animal Behaviour The characteristics of social organization and mating distributed (and studied) species of mice, Mus musculus systems result from particular ecological conditions domesticus, the female’s choice of a male depends in but also from the proximate interactions between indi- viduals. In many rodent species these interactions are partners of their species and subspecies In M. m. domesticus, the commensal species of the mating systems correspond to particular ecological con- another species of mouse living under very different Mate choice, especially in male mice, is also affected by ecological conditions, such as the mound-builder mouse, previous social and ontogenetic experience, mainly, but M. spicilegus, would have a different mating system. These not only, during the first weeks after birth mice from the steppes of eastern Europe are mainly characterized by their autumnal behaviour of buildingtumuli (with stocks of seeds) where they overwinter Correspondence: B. Patris, Laboratoire d’Ethologie Expe´rimentaleet Compare´e, UPRES-A 7025 CNRS, Universite´ Paris-Nord, 93430 Villetaneuse, France (email: The Association for the Study of Animal Behaviour 1466 ANIMAL BEHAVIOUR, 56, 6
Male–female bonding in particular should be consid- ered as an important factor that can affect a female’schoice of a mate, as it does in several monogamousspecies (Microtus ochrogaster: We compared the sexual preferences of female M. m. domesticus and M. spicilegus, allowed to choose betweentwo males (familiar versus unfamiliar). To evaluate thestability of their sexual partnership, we first studied paired females in postpartum oestrus. Second, to investi-gate the mechanisms of these sexual preferences, westudied oestrous females familiarized with a male. Wethen recorded whether the female would copulate with In the polygamous species, M. m. domesticus, we expected the female to show interest in, and to copulatewith, the unfamiliar male. Mound-builder mice show a high level of paternal care compared with house mice(unpublished data), which is considered to be a mono- Figure 1. Experimental apparatus used for testing female prefer-
ences. The female was placed into zone 1. Zones 2a and 3a were
areas with male odours; zones 2b and 3b, areas with active males.
Areas a and b were separated by a transparent plastic sheet with fore, we expected the female to prefer the familiar maleand to refrain from copulating with an unfamiliar male.
16 cm and 14 cm high) for 8 days before the choice test to make their social status similar and to stimulatetheir sexual behaviour Animals and Breeding Conditions
We used mice derived from stocks caught in the wild and reared in captivity for 15 generations: M. m. Choice Test Between Familiar and Unfamiliar
domesticus, strain DDO (Odis, Denmark) and M. spicilegus, strain ZYP (Pancevo, Yugoslavia). The mice were main-tained in our laboratory under a 14:10 h light:dark cycle with lights on at 2200 hours, and an ambient temperature The experimental apparatus consisted of a 2 C in the breeding and experimental rooms. The mice were housed in polycarbonate cages measuring was introduced (zone 1), connected to two other terraria 16 cm and 14 cm high, food (mice pellets, U.A.R.
type AO4) and water were supplied ad libitum, and plastic tubes (3 cm in diameter and 9 cm in length). The cotton was provided for nesting material. At 21 days of acrylic opaque walls of the terraria prevented the mice age mice of both sexes were housed in unisex sibling seeing each other. Terraria 2 and 3 were divided in half (zones a and b) by an acrylic transparent partition with When they were 4–6 months old, we randomly assigned unrelated males and females to breeding pairs ina terrarium measuring 50 each species two groups of pairs were studied: nine We determined the receptive period of the postpartum oestrous females behaviourally when, after delivery, we oestrous female groups) and 10 pairs without sexual observed the female adopt a lordotic posture after a experience but with 15 days of familiarization (oestrous female groups). Postpartum oestrous females were paired was similar for the oestrous females during the daily for several weeks with their male and these pairs had direct interactions. At the time of the first lordotic already had two litters. Oestrous females, during a 15-day posture of the female after a mount we separated the dyad period of familiarization with a male, were allowed to and introduced the female into zone 1 of the testing interact (except to copulate) with him daily for several apparatus for 15 min. The familiar male and the unfam- hours; for the rest of the day they were allowed to sniff iliar male were placed randomly during this period into each other by naso-nasal contact through holes in a zones 2a and 3a which were disconnected from zone 1.
After 15 min we transferred these males into zones 2b and Unfamiliar and unrelated males (19 M m. domesticus 3b, respectively. The tubes connecting zone 1 to zones 2a and 19 M. spicilegus) were isolated in standard cages and 3a were then opened and the female was allowed to PATRIS & BAUDOIN: FEMALE MOUSE SEXUAL PREFERENCES 1467
explore freely these areas and zone 1 for 10 min. During this period she could see the males and sniff them through the holes of the partition during naso-nasalcontacts. Using a Psion Organizer 2 we recorded the total duration of female presence in each zone (zone 1+tubes, zones 2a and 3a) and the duration of sniffing familiar andunfamiliar males during naso-nasal contacts through 100 M. m. domesticus M. spicilegus M. m. domesticus M. spicilegus Copulation with Unfamiliar Male
At the end of the 10-min choice test, we closed the door between zone 1 and zone 2a or 3a once the female had entered the compartment of the apparatus close to the unfamiliar male Then we removed the partition between the female and the unfamiliar male and recorded the presence (or absence) of copulation during 30 min. If copulation occurred, the interaction was stopped after the first intromission with lordosis. All the females were then reunited with their familiar males and we recorded M. m. domesticus M. spicilegus M. m. domesticus M. spicilegus the first copulation as the sign that they were receptive at the end of the experiment. We cleaned the experimentalapparatus between tests with 70% ethanol.
Figure 2. (a) Time (s) spent by females in zones with odours of the
familiar male () and an unfamiliar male () and (b) the time (s)
spent sniffing these males: postpartum oestrous females of M. m.
Data Analysis
domesticus (N=9), postpartum oestrous females of M. spicilegus(N=9), oestrous females of M. m. domesticus (N=10), oestrous females of M. spicilegus (N=10). *P<0.05; ** P<0.01; ***P<0.001.
used a paired t test (two-tailed) to compare how long thefemales stayed in the zones with odours of the familiar the partition. If amicable interaction occurred immedi- and unfamiliar males, and to compare how long they ately, we left the animals together and replaced them in sniffed familiar and unfamiliar males during naso-nasal their cage the day after. If agonistic interactions occurred, contacts (we verified the normality of distribution of data we separated the animals using the central partition and for all parameters using the Kolmogorov–Smirnov test).
used the same procedure during the next few days until Then we used an ANOVA to compare the allocation of interactions were amicable (maximum 2 days with these time between the two males in the two species for each parameter, when the females were in postpartum oestrus and in oestrus. We used only the ‘all effects’ analysis agonistic behaviour occurred at the beginning of the meeting (threat, pursuit, boxing); these fights lasted 1–5 s For each species and each type of oestrus, we used the would have separated the partners if fights were observed McNemar test to compare the presence/absence of copu- after 5 min but there was no persistent or injurious lation during successive encounters with familiar and aggression and as soon as the male perceived the female then unfamiliar males. Then we used Fisher’s exact test was receptive we observed only defensive behaviour by (one-tailed) to compare the frequency of copulation with the female refusing to copulate. This work was carried out under licence from the French Ministry of Agriculture.
oestrous females and then for oestrous females. We used aone-tailed test since we expected a lower frequency ofcopulation with the unfamiliar male in M. spicilegus Choice Test Between Familiar and Unfamiliar
Ethical Note
After their 8-day period of isolation, the unfamiliar males behaved normally when we used them for consti- In M. spicilegus, postpartum oestrous females spent tuting new pairs in our breeding stock or put them back more time near the familiar male (paired t test: t =2.59, with their sibling brothers after a period of familiariz- P<0.05, but did not sniff him for longer ation. Familiarization took place in a terrarium measuring No differences were observed for the postpartum oestrous 30 cm, divided in half with a partition between females in M. m. domesticus. An ANOVA revealed that the this male and his brothers, allowing olfactory communi- time allocation between the two males differed in the two cation and preventing aggression. After 24 h we removed 1468 ANIMAL BEHAVIOUR, 56, 6
species and becausefemales avoid contact with unknown males during In M. spicilegus, oestrous females spent more time in the area close to the familiar male (paired t test: t =2.36, Because of their differing ecology, we predicted behav- P<0.05; and sniffed him for longer (paired t test: ioural differences between the two species. Both oestrous t =4.30, P<0.01; In M. m. domesticus, oestrous and postpartum oestrous females of M. spicilegus were females, in contrast, spent more time near the unfamiliar more attracted to their familiar male than the unfamiliar one (except the duration of sniffing in the postpartum him for longer (paired t test: t = group). Moreover, the females generally refused to copu- An ANOVA revealed that the time allocation between the late with an unfamiliar male. These results indicate a two males differed in the two species (F strong pair bond in this species between the male and P<0.01; as well as the sniffing time allocation postpartum female and a sexual preference induced by familiarization in the oestrous state. Central vasopressincould act in the establishment of this sexual preference Copulation with Unfamiliar Male
after familiarization as in the monogamous prairie voles,Microtus ochrogaster All the females copulated with their familiar male both at the beginning and at the end of the experiment. All the We do not know exactly how populations of unfamiliar males attempted to copulate with the females.
M. spicilegus are organized under natural conditions.
In the postpartum oestrous state (paired females) They build mounds structured with alternate layers of M. spicilegus females rarely copulated with the unfamiliar earth and seeds in the autumn after breeding male (2/9) and preferred to copulate with their usual partner (McNemar test: df=1, P<0.01). Four out of nine analyses have shown that young found in the mounds M. m. domesticus females copulated with the unfamiliar originate from several related females and several males male showing a preference for copulating with their familiar male as well (McNemar test: df=1, P<0.05). Twice ible with polygynous or polyandrous mating systems.
as may paired females copulated with the unfamiliar male Our results concerning the existence of a pair bond in M. m. domesticus than in M. spicilegus but the difference between the partners could be interpreted as an indi- was not statistically significant (one-tailed Fisher’s exact cation of monogamy as described in several species of In the oestrous state (familiarized females) only a few M. spicilegus females copulated with the unfamiliar male (unpublished) results reveal a higher paternal invest- (3/10), and the majority preferred to copulate with their ment by M. spicilegus males than by M. m. domesticus.
familiar male (McNemar test: df=1, P<0.01). In contrast These results argue in favour of monogamous traits in the majority of M. m. domesticus oestrous females copu- lated with the unfamiliar male (8/10). Oestrous M. domes- ticus females copulated more often with an unfamiliar male than did oestrous M. spicilegus females (one-tailed Before concluding that M. spicilegus is monogamous, Fisher’s exact test: P=0.037).
however, we need to demonstrate the presence of someother common characteristics in monogamous species,such as stability of this bond (long-term association), DISCUSSION
a common territory and a symmetrical pattern ofdispersal in young males and females Since the commensal mouse M. m. domesticus is poly- gamous, we expected females to show sexual interest in need to conduct field studies to determine the validity an unfamiliar male and to copulate with him. Our results of experimental results from the laboratory and the partially confirm these predictions. Oestrous females characteristics of the mating processes under natural familiarized with a male during a 15-day period spent more time close to the unfamiliar male than to thefamiliar one, sniffed the unfamiliar male more often, andcopulated with him. A period of familiarization was not Acknowledgments
sufficient to induce a female sexual preference in thisspecies. Paired females in postpartum oestrus, which had We thank Franc¸ois Bonhomme and Annie Orth for already reproduced twice with the same male, had no providing the two species of mice. We are grateful to clear preference: they were not attracted to the unfamiliar Simone Demouron for her help in taking care of the male and did not sniff him more often. All the males animals. We thank Jean-Luc Durand for statistical attempted to copulate with the females and we conclude advices, Christophe Fe´ron, Gilles Gheusi, Patrick Gouat that their attractiveness was high. Nevertheless, about and the anonymous referees for their comments, Andrea half (5/9) of the females in this condition refused to Dejean and Lesya Vynogradska for help with the English copulate with the unfamiliar male. This could be because in the manuscript and Lesya Vynogradska for translation sexually inexperienced males commit infanticide in this PATRIS & BAUDOIN: FEMALE MOUSE SEXUAL PREFERENCES 1469
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