A comparative study of parental care between two rodent species: implications for the mating system of the mound-building mouse Mus spicilegus

Paternal care is uncommon in mammals where males are more often involved in sexual competition than in providing care for their own offspring. However some species present some form of paternal care and, most of the time, this phenomenon is associated with a monogamous mating system. Mice of the genus Mus, such as the house mouse Mus musculus domesticus, are commonly considered to be polygamous-polygynous species. In Mus spicilegus, the mound-building mouse, previous results on female sexual preferences have suggested the existence of pair bonding more compatible with a monogamous mating system than with a polygamous one. We therefore tested the hypothesis that male M. spicilegus present a higher level of paternal care than males of the polygynous house mouse. Results showed that male M. spicilegus spent significantly more time covering the young during the first week after birth than male M. m. domesticus, particularly when the female was exploring, and retrieved stray pups significantly more frequently and more rapidly than male M. m. domesticus. There were practically no differences between the females of these two species. M. spicilegus parents also more significantly alternated their protection of the pups than M. m. domesticus parents. We discuss the evolution of paternal care in M. spicilegus in relation to monogamy.     

Male-female interactions and socio-sexual isolation of Mus spicilegus toward two other species of east-European mice, M. macedonicus and M. m. musculus.

Social and sexual interactions were analysed as potential behavioural processes assessing reproductive isolation between the mound-building mouse, Mus spicilegus, and two other wild species, M. macedonicus and M. musculus. Dyadic encounters among strange M. spicilegus individuals and between M. spicilegus and the two other species members were conducted with females in an oestrus state. In intraspecific M. spicilegus encounters, there was a high incidence of close contact behaviours initiated by the females. In interspecific encounters M. musculus males and females and M. macedonicus females showed social interest toward their M. spicilegus protagonists, whereas the later behaved in an unfriendly or aggressive manner. Thus socio-sexual interactions shown by the different species seem to be sufficient to prevent any attempt to mate interspecifically. Arguments in favour of recognition against reinforcement hypothesis are discussed.     

The Effect of Reciprocal Cross-Fostering of Pups in Two Species of Mice <Emphasis Type="Italic">Mus musculus</Emphasis> and <Emphasis Type="Italic">Mus spicilegus</Emphasis>: An Altered Response to Con- and Heterospecific Odors

The effect of pup cross-fostering by the house mouse Mus musculus and the mound-building mouse M. spicilegus on the odor preferences of sexually mature individuals has been studied for the first time. House and mound-building mice reared by females of a closely related species did not prefer any of the odors, in contrast to intact individuals of these species. Some individuals reared by females of a closely related species preferred the odor of foster species to conspecific odor. Early olfactory experience has been shown to alter the response of house mice and mound-building mice to odors of their own species and foster species.     

Concordance in mate choice in female mound-building mice

Females must evaluate male quality to perform mate choice. Since females generally base their selection on different male features, individual females may differ in their choice. In this study, we show that concordance between females in mate choice decisions may arise without any experimental maximization of a particular attractive trait. Choice tests were performed in mound-building mice, Mus spicilegus, a monogamous species. Body odours of two male donors were presented to 12 female subjects individually. To determine female choice, the same pair of males was presented three times to a female. Four different pairs of male body odours were used. Male donors, not related to females, were selected at random in our polymorphic breeding stock. Using this two-way choice design, female mice displayed a clear choice and had a similar preference for particular males.     

The ownership signature in mouse scent marks is involatile

Male house mice advertise their territory ownership through urinary scent marks and use individual-specific patterns of major urinary proteins (MUPs) to discriminate between their own scent and that of other males. It is not clear whether recognition occurs through discrimination of the non-volatile proteins or protein-ligand complexes (direct model), or by the detection of volatile ligands that are released from MUPs (indirect model). To examine the mechanism underlying individual scent mark signatures, we compared investigatory and countermarking responses of male laboratory mice presented with male scent marks from a strain with a different MUP pattern, when they could contact the scent or when contact was prevented by a porous nitrocellulose sheet to which proteins bind. Mice investigated scent marks from other males whether these were covered or not, and biochemical analysis confirmed that the porous cover did not prevent the release of volatiles from scent marks. Having gained information through investigation, mice increased their own scent marking only if they had direct contact with another male's urine, failing to do this when contact was prevented. Individual signatures in scent marks thus appear to be carried by non-volatile proteins or by non-volatile protein-ligand complexes, rather than by volatiles emanating from the scent.     

保加利亚北部地区匈牙利小家鼠的空间组织结构

本文研究了保加利亚北部地区的匈牙利小家鼠在繁殖期的空间关系和分布。这种动物最普遍的空间关系是一雄一雌,也观察到两个或三个雄鼠与一个雌鼠、一个雄鼠与两个或三个雌鼠的组织形式。很少观察到雌性的社群小组。雌鼠之间的巢区没有发现重叠。一般雄鼠的巢区大于雌鼠。有一半雄鼠的巢区与一个雌鼠的巢区相重叠,其他的雄鼠与两个成年雌鼠的巢区相重叠。这些结果表明,匈牙利小家鼠具有多变的社群繁殖婚配体制,即单配制和多配制共存。比较普遍的一雄一雌的配对形式和雌性的独居特性,以及雌性之间巢区的相对独立性,表明单配制是该物种的主要婚配体制。     

The scent of senescence: sexual signalling and female preference in house mice

Sexual signals are expected to be costly to produce and maintain, thus ensuring that only males in good condition can sustain their expression at high levels. When males reach senescence they lose physiological function and condition, which could constrain their ability to invest in costly sexual signals, decreasing their attractiveness to mates. Furthermore, females may have evolved mating preferences that cause avoidance of senesced males to enhance fertilization success and viability of offspring. Among mammals, the size of antlers and other weapons can decrease with senescence, but changes in olfactory sexual signals have been largely unexplored. We examined changes in olfactory signals with senescence in house mice (Mus musculus domesticus), where males excrete volatile and involatile molecules in scent marks that elicit behavioural and priming responses in females. Compared to middle-aged males, the urine of senesced males contained a lower concentration of involatile signalling proteins (major urinary proteins or MUPs), and associated volatiles that bind to these proteins. The reduced intensity of male scent will affect the longevity of scent signals deposited in the environment and, accordingly, females were less attracted to urine from senesced males deposited 12 h previously. Females also discriminated against senesced males encountered behind a mesh barrier. These results reveal that investment in olfactory signalling is reduced during senescence and suggest that senesced males and their scent may be less attractive to females.     

Evaluation of the social bond: a new method tested in Mus spicilegus

Innovative and fruitful studies of social bonds have been developed in recent years, although the methods used to establish the existence of a social bond between two individuals have not evolved significantly. Two types of paradigms have been currently used: the separation-reunion paradigm, which evaluates the distress caused by the disruption of the social bond, and choice paradigms, which test the specificity of the bond to a given individual. We have developed a new paradigm based on the idea that the cost an individual was ready to pay in order to gain access to a conspecific depended on the strength of the social bond between the two individuals. To test our paradigm we used mound-building mice, Mus spicilegus that present, in both males and females, a level of tolerance that differs greatly according to the degree of familiarity between the individuals. Our new method for testing social bond revealed unsuspected differences between males and females. Our results suggested that, at least in Mus spicilegus, strong social bonds were not necessary to the development of a high level of tolerance between individuals.     

Oestrous females investigate the unfamiliar male more than the familiar male in both commensal and non-commensal populations of house mice

We studied female preferences for familiar and unfamiliar males. The subjects were laboratory-born house mice: (1) non-commensal Mus musculus domesticus from the eastern part of Syria along the Euphrates River; and (2) commensal M. m. musculus from the Czech Republic. Pair-choice preference tests have revealed that oestrous females of both populations sniffed towards unfamiliar males more than familiar males. In the case of females exhibiting postpartum oestrus, this preference was less pronounced and statistically not significant. Thus, our mice clearly exhibited the behavioural pattern known from commensal populations of polygynous and/or promiscuous M. m. domesticus. We found no inverse tendency to seek proximity to the familiar male that has been previously reported from closely related and presumably monogamous aboriginal mouse Mus spicilegus. We conclude that neither commensal M. m. musculus, nor non-commensal M. m. domesticus, are likely to share a monogamous mating system with mound-building mice.     

Predators Are Attracted to the Olfactory Signals of Prey

Background

Predator attraction to prey social signals can force prey to trade-off the social imperatives to communicate against the profound effect of predation on their future fitness. These tradeoffs underlie theories on the design and evolution of conspecific signalling systems and have received much attention in visual and acoustic signalling modes. Yet while most territorial mammals communicate using olfactory signals and olfactory hunting is widespread in predators, evidence for the attraction of predators to prey olfactory signals under field conditions is lacking.

Methodology/Principal Findings

To redress this fundamental issue, we examined the attraction of free-roaming predators to discrete patches of scents collected from groups of two and six adult, male house mice, Mus domesticus, which primarily communicate through olfaction. Olfactorily-hunting predators were rapidly attracted to mouse scent signals, visiting mouse scented locations sooner, and in greater number, than control locations. There were no effects of signal concentration on predator attraction to their prey''s signals.

Conclusions/Significance

This implies that communication will be costly if conspecific receivers and eavesdropping predators are simultaneously attracted to a signal. Significantly, our results also suggest that receivers may be at greater risk of predation when communicating than signallers, as receivers must visit risky patches of scent to perform their half of the communication equation, while signallers need not.     

Memorisation des marques olfactives chez la Genette (Genetta genetta L.): durée de reconnaissance par les femelles de marques olfactives de males

Memorization of Scent Marks in Genets (Genetta genetta L.): Duration of Female Memory of Male Scent Marks The aim of this work was to study the memorization of scent marks of known males by females in genets (Genetta genetta L.). An attempt was made to determine how long, after separation from a given male, females could discriminate between his scent marks and those of strange males. Significant differences in sniffing duration at the scent marks were observed nine weeks after separation. These results showed that olfactory cues could permit individual recognition in genets, and that memorizing the scent marks could also act in the regulation of aggressive behaviour in free-living animals.     

Olfactory Communication and Neighbor Recognition in Giant Kangaroo Rats

We hypothesized that olfactory communication facilitates neighbor recognition in the giant kangaroo rat, Dipodomys ingens , and is therefore influential in coordinating social interactions in this solitary, desert rodent. We tested whether (i) D. ingens can discriminate between odors of same- and opposite-sex conspecifics; and (ii) the kangaroo rats exhibit scent preferences based on familiarity. In habituation-discrimination tests, we found that both genders distinguish differences between the scent of individuals of the same- and opposite-sex. In olfactory preference tests, both males and females spent significantly more time investigating the scent of their familiar cagemate than the scent of an unfamiliar conspecific. Giant kangaroo rats may be able to recognize familiar neighbors from olfactory cues, thus supporting a hypothesis of neighbor recognition. Neighbor recognition may be an important mechanism of social interactions in this endangered species.     

Odour-genes eovariance and differential investigation of individual odours in the Mus species complex

Previous research using habituation techniques has demonstrated that greater genetic similarity between two individuals is associated with more similarity in the qualities of their individual odours ('odour-genes eovariance'). We assessed odour similarities across species in two pairs of genetically close species within the Mus species complex (M. musculus and M. domesticus; M. spicilegus and M. macedonicus). Subjects treated odours within each species pair as similar compared with an odour from the other species pair. Subjects also treated odours of M. spicilegus males from the same population as similar compared with the odour of M. spicilegus males from a different population. This confirms odour-genes eovariance across species and within populations and also supports previous findings that odour similarities are more salient than specific odour markers. When adult males were presented with odours of females from two different heterospecific species, subjects spent more time investigating the odour from his own species pair than the other species pair, indicating greater interest in the odour of the closer heterospecific and demonstrating that odour-genes eovariance is reflected in behavioural responses to odours. Implications of odour-genes eovariance as a basis for identifying degrees of genetic relatedness of unfamiliar individuals through similarities in individual odours are discussed.     

Sensory processes in the discrimination of pups by female mice (Mus musculus)

Maternal pup retrieval by house mice (Mus musculus) was studied in an investigation of sensory processes in the discrimination of ‘own’ from ‘alien’ pups. In a control condition, mothers were able to discriminate their own from alien young. This ability seemed to be based on olfactory cues, while visual and auditory cues did not seem to be involved. Furthermore, it is suggested that retrieval consists of: elicitation (probably mediated by auditory cues); location of the pup (auditory and olfactory cues); and recognition of the pup (initially olfactory cues, with subsequent gustatory and tactile cues).     

Reduced nucleotide variability at an androgen-binding protein locus (Abpa) in house mice: evidence for positive natural selection.

Previous work has shown that the gene for the alpha subunit of androgen-binding protein, Abpa, may be involved in premating isolation between different subspecies of the house mouse, Mus musculus. We investigated patterns of DNA sequence variation at Abpa within and between species of mice to test several predictions of a model of neutral molecular evolution. Intraspecific variation among 10 Mus musculus domesticus alleles was compared with divergence between M. m. domesticus and M. caroli for Abpa and two X-linked genes, Glra2 and Amg. No variation was observed at Abpa within M. m. domesticus. The ratio of polymorphism to divergence was significantly lower at Abpa than at Glra2 and Amg, despite the fact that all three genes experience similar rates of recombination. Interspecific comparisons among M. m. domesticus, Mus musculus musculus, Mus musculus castaneus, Mus spretus, Mus spicilegus, and Mus caroli revealed that the ratio of nonsynonymous substitutions to synonymous substitutions on a per-site basis (Ka/Ks) was generally greater than one. The combined observations of no variation at Abpa within M. m: domesticus and uniformly high Ka/Ks values between species suggest that positive directional selection has acted recently at this locus.     

Encoding choosiness: female attraction requires prior physical contact with individual male scents in mice

Scents, detected through both the main and vomeronasal olfactory systems, play a crucial role in regulating reproductive behaviour in many mammals. In laboratory mice, female preference for airborne urinary scents from males (detected through the main olfactory system) is learnt through association with scents detected through the vomeronasal system during contact with the scent source. This may reflect a more complex assessment of individual males than that implied by laboratory mouse studies in which individual variation has largely been eliminated. To test this, we assessed female preference between male and female urine using wild house mice with natural individual genetic variation in urinary identity signals. We confirm that females exhibit a general preference for male over female urine when able to contact urine scents. However, they are only attracted to airborne urinary volatiles from individual males whose urine they have previously contacted. Even females with a natural exposure to many individuals of both sexes fail to develop generalized attraction to airborne male scents. This implies that information gained through contact with a specific male's scent is essential to stimulate attraction, providing a new perspective on the cues and olfactory pathways involved in sex recognition and mate assessment in rodents.     

Female prairie voles do not choose males based on their frequency of scent marking

We conducted an experiment to test three alternative hypotheses for the function of frequency of scent marking in male prairie voles, MICROTUS OCHROGASTER: (1) sexual attraction (to advertise male quality for mating); (2) reproductive competition; and (3) self-advertisement or individual identity. In laboratory experiments, males deposited scent on all areas of a bare substrate, and more in an area next to a stimulus animal than other areas, regardless of the stimulus animal's sex. Females did not choose mates based on their frequency of scent marking and scent marking did not antagonize or stimulate aggression between males. The frequency of scent marking by males supports the individual identity hypothesis, and is less consistent with the sexual attraction or reproductive competition hypotheses. Mate choice is likely based on a complex suite of characters, but at least in prairie voles, the frequency of scent marking by males does not appear to be one of them.     

Molecular evolution of a Y-chromosomal repetitive sequence family in the genus Mus

A 522-base-long Y-chromosomal sequence was isolated from a BALB/c genomic library and was designated "BF046." It is repeated about 200 times in the male genome, and a difference was detected between the Mus musculus musculus and the M. m. domesticus type Y chromosomes. BF046- related sequences were present over the entire length of the Y chromosome as visualized by in situ hybridization. Southern blot analysis against DNAs isolated from eight species in the genus Mus showed that BF046-related sequences were amplified in the Y chromosomes of three closely related species: M. musculus, M. spicilegus, and M. spretus. To gain insight into the stability of the BF046 sequence family, we isolated 18 additional clones from these three mouse species and compared their sequences. The M. musculus sequences differed from the M. spicilegus and M. spretus sequences by two indels. The remaining parts of the sequences were very similar, but both parsimony and distance-based analytical methods divided the sequences into the same four subgroups, with each species having its own subgroup(s). Thus, the Y chromosomes of M. musculus, M. spicilegus, and M. spretus can be distinguished from one another.      

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.     

Testing for Odor Discrimination and Habituation in Mice

This video demonstrates a technique to establish the presence of a normally functioning olfactory system in a mouse. The test helps determine whether the mouse can discriminate between non-social odors and social odors, whether the mouse habituates to a repeatedly presented odor, and whether the mouse demonstrates dishabituation when presented with a novel odor. Since many social behavior tests measure the experimental animal’s response to a familiar or novel mouse, false positives can be avoided by establishing that the animals can detect and discriminate between social odors. There are similar considerations in learning tests such as fear conditioning that use odor to create a novel environment or olfactory cues as an associative stimulus. Deficits in the olfactory system would impair the ability to distinguish between contexts and to form an association with an olfactory cue during fear conditioning. In the odor habitation/dishabituation test, the mouse is repeatedly presented with several odors. Each odor is presented three times for two minutes. The investigator records the sniffing time directed towards the odor as the measurement of olfactory responsiveness. A typical mouse shows a decrease in response to the odor over repeated presentations (habituation). The experimenter then presents a novel odor that elicits increased sniffing towards the new odor (dishabituation). After repeated presentation of the novel odor the animal again shows habituation. This protocol involves the presentation of water, two or more non-social odors, and two social odors. In addition to reducing experimental confounds, this test can provide information on the function of the olfactory systems of new knockout, knock-in, and conditional knockout mouse lines.