Mus Spicilegus Research Articles

The Effect of Reciprocal Cross-Fostering of Pups in Two Species of Mice Mus musculus and Mus spicilegus: 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.

The prey composition of the Barn Owl(Tyto alba)with respect to landscape structure of its hunting area (Zala County, Hungary)

AbstractThe prey composition of the Barn Owl(Tyto alba)can be monitored indirectly by pellet analysis and we used this method to investigate less known small mammal species of Zala County. The number and abundance of small mammal species depend on the structure of the landscape of Barn Owls’ hunting area, therefore we analysed landscape features in the surrounding circles with 2 km radius around the sampling sites. In 2016 we collected 1106 pellets from 13 sampling localities. From the pellets we identified 21 species of 3022 individuals of small mammals (more than 98% of prey). Among the 21 species there was the rare Parti-colured Bat(Vespertilio murinus)and a new species for the county the Steppe Mouse(Mus spicilegus). Positive correlation was found between the diversity of the small mammal fauna of each sampling site and the landscape complexity (number of the landscape patches) of the Barn Owl hunting area. Relative abundance of the Wood Mouse(Apodemus sylvaticus)showed positive correlation with the number of landscape patches, while the abundance of the Lesser White-toothed Shrew(Crocidura suaveolens), the Miller’s Water Shrew(Neomys anomalus), the Striped Field Mouse(Apodemus agrarius)and the Harvest Mouse(Micromys minutus)was higher in hunting areas with more homogenous landscapes. Significant correlations were found between the relative abundance of some small mammal species and the landscape structure of the potential hunting area of owls that confirmed the consistency in habitat preference of some species. Our results proved that the prey-composition of Barn Owls reflects the land use through the distribution and abundance of small mammal species, therefore this method is suitable for ecological analyses of landscape.

Species differences in egocentric navigation: the effect of burrowing ecology on a spatial cognitive trait in mice

Efficient navigation is a critical component of fitness for most animals. While most species use a combination of allocentric (external) and egocentric (internal) cues to navigate through their environment, subterranean environments present a unique challenge in that visually mediated allocentric cues are unavailable. The relationship between egocentric spatial cognition and species differences in ecology is surprisingly understudied. We used a maze-learning task to test for differences in egocentric navigation between two closely related species of mice, the eastern house mouse, Mus musculus musculus, and the mound-building mouse, Mus spicilegus. The two species are sympatric in Eastern Europe and overlap in summer habitat use but differ dramatically in winter space use: whereas house mice occupy anthropogenic structures, mound-building mice survive the winter underground in intricate burrow systems. Given species differences in burrowing ecology, we predicted that M. spicilegus would learn the maze significantly faster than M. m. musculus when tested in complete darkness, a condition that eliminated allocentric spatial information and served as a proxy for the subterranean environment. We found strong support for this prediction. In contrast, the two species performed equally well when different mice were tested in the same maze with lights on. This context-specific species difference in spatial cognition suggests that enhanced egocentric navigation in M. spicilegus is an adaptation to the burrow systems on which the overwinter survival of young mound-building mice depends. The results of this study highlight the importance of ecological adaptations to the evolution of cognitive traits.

Small Mammals in an Urban Area: Habitat Preferences and Urban-Rural Gradient in Nitra City, Slovakia

ABSTRACT The small mammal species were investigated in the urbanized environment of Nitra city (Slovakia) in a multiscale-approach: at habitat level and at landscape level (urban-rural gradient). Continuous comprehensive rodent samplings from 2012 to 2015 were conducted in ten study sites, classified into three urban zones (landscape level). The total effort comprised 1,250 specimens of 13 species (Microtus arvalis, Apodemus sylvaticus, A. flavicollis, A. uralensis, Clethrionomys (Myodes) glareolus, M. subterraneus, Micromys minutes, Mus spicilegus, M. musculus, Crocidura suaveolens, C. leucodon, Sorex araneus, S. minutus) gathered in 14950 trapxnights. Environmental variables (habitat level) at each site were processed in the Geographical Information System as a proportion of landscape units around the trapping line and by a phytosociological survey. At the habitat level, we found a relationship between the landscape habitat structure and each species of small mammals. Diversity, species richness and rel...

Behavioral and neuronal responses of two mouse species, Mus musculus and Mus spicilegus, to con- and heterospecific olfactory signals

The behavioral and neuronal responses of the males of two closely related species of mice (Mus musculus wagneri, M. spicilegus) to the urine odors of estrus con- and heterospecific females were studied. In two-choice odor tests males significantly longer investigated odor of conspecific females in comparison with heterospecific ones. To investigate neuronal activation in the main and accessory olfactory bulbs (MOB and AOB), one of the methods of functional tomography – manganese-enhanced MRI ( ME-MRI) – was used. There was a significant increase in Mn2+ accumulation in the dorsal section of the posterior part of the MOB in male M. m. wagneri and M. spicilegus exposed to odor of conspecific females compared with the control group males (odor not exposed). There was a local significant increase in manganese accumulation in the dorsal region of the anterior part of the MOB in the case of the exposure of odor of a heterospecific female. The exposure of heptanone-2 to mice resulted not only in an increase in Mn2+ accumulation in certain zones, but also in a significant decrease in the accumulation of Mn2+ in the rest of the olfactory bulbs. A significant increase in the accumulation of MRI contrast in AOB was observed in males only in the case of female urine-conspecific odor exposure. The results support the previously stated assumption of a significant difference in chemical communication systems in two species of mice. A comparison of these results and results obtained previously demonstrated the absence of any differences in behavioral and neuronal responses to con- and heterospecific odors of the house mouse subspecies allopatric (M. m. wagneri) and sympatric (M. m. musculus) to M. spicilegus. This fact does not allow us to assume the effect of the mechanism of “reinforcement” in the process of evolution in the formation of precopulatory reproductive isolation between the sympatric species M. spicilegus and M. musculus.

Personality modulates proportions of CD4+ regulatory and effector T cells in response to socially induced stress in a rodent of wild origin

The way how individuals respond to chronic challenges can vary tremendously, and such differences are closely linked to personality. The few available studies on individual differences in stress-related immunosuppression in non-human mammals have been mainly carried out with laboratory strains. We conducted a study in male mound-building mice (Mus spicilegus) of wild origin. We distinguished between high (HAN) and low anxious/neophobic (LAN) personality types, quantified by subjects' consistent and associated behavioral responses in repeated elevated plus maze and novel object tests. After reaching maturity, parts of the subjects were regularly confronted to different resident pairs over a period of 5days to provoke a condition of chronic social stress, while others were used as untreated controls. We measured fecal corticosteroid metabolite (FCM) concentrations and different cellular immune parameters from blood and spleen. Socially confronted HAN showed higher increases in FCM concentrations than LAN, indicating a more pronounced physiological stress response in the former personality type. HAN of the experimental group also showed lower percentages of effector T cells (Teff) and higher regulatory T cells (Treg) in the spleen; the latter are known for their immunosuppressive activity. Considering the ratio of Teff/Treg, animals with higher increases in FCM concentrations during the late period of the experiment showed a stronger shift towards Treg cells, supporting immunosuppressive effects of chronically elevated corticosteroid levels. Summarizing, our results strongly suggest that immunomodulatory effects of socially induced stress were altered by individual differences in anxiety/neophobia, emphasizing the significance of personality in shaping physiological responses to challenge.

Ultrasonic Vocalizations of Male Mice Differ among Species and Females Show Assortative Preferences for Male Calls.

Male house mice (Mus musculus) emit ultrasonic vocalizations (USVs) during courtship, which attract females, and we aimed to test whether females use these vocalizations for species or subspecies recognition of potential mates. We recorded courtship USVs of males from different Mus species, Mus musculus subspecies, and populations (F1 offspring of wild-caught Mus musculus musculus, Mus musculus domesticus (and F1 hybrid crosses), and Mus spicilegus), and we conducted playback experiments to measure female preferences for male USVs. Male vocalizations contained at least seven distinct syllable types, whose frequency of occurrence varied among species, subspecies, and populations. Detailed analyses of multiple common syllable types indicated that Mus musculus and Mus spicilegus could be discriminated based on spectral and temporal characteristics of their vocalizations, and populations of Mus musculus were also distinctive regardless of the classification model used. Females were able to discriminate USVs from different species, and showed assortative preferences for conspecific males. We found no evidence that females discriminate USVs of males from a different subspecies or separate populations of the same species, even though our spectral analyses identified acoustic features that differ between species, subspecies, and populations of the same species. Our results provide the first comparison of USVs between Mus species or between Mus musculus subspecies, and the first evidence that male USVs potentially facilitate species recognition.

Correlates between ear postures and emotional reactivity in a wild type mouse species

Facial expressions have been extensively used to assess emotions in humans and thus could be extended to other species that also display facial movements. In mice both painful and fearful situations have been associated with particular shifts in facial expressions. Like other species, mice frequently show a great inter-individual variability when exposed to emotional situations, but so far no study has been conducted to investigate if facial expressions are related to these differences. The aim of this study is to explore if mice of wild origin (Mus spicilegus) express different facial expressions when confronted to novelty and to relate these mimics to their emotional reactivity profile. We used individual exploration scores in a novel odour test and in the elevated plus maze test as proxy measures of individual emotional reactivity. Our results showed that exploration scores in both tests were positively correlated, and both were related to the ear postures expressed by the individuals during their first exploration of the novel odour. This single component of facial expression was in fact a good indicator of inter-individual differences expressed in these two different tests suggesting a strong link between this marker and the individual emotional reactivity. These results highlight the great potential of facial expressions to assess emotional states in animals.

Communities of small mammals (Soricomorpha, Rodentia) in urbanized environment

AbstractThe study is focused on analyses of the impact of urbanized environment on the occurrence and structure of small mammals that are important with regard to transmission of diseases to man and domestic animals. The city of Nitra (Slovakia) was chosen as a model area, where an urban - rural gradient was determined. It was categorized into three zones, depending on the distance from the city centre. Small mammals were examined by a comprehensive annual research during the seasons. Overall, 12 species of small mammals were found, Microtus arvalis (29.6%), Apodemus sylvaticus (23.1%), Apodemus flavicollis (20.6%) were eudominant. The communities of small mammals showed an increase in species diversity and richness from the suburban to the peripheral zone, and a decrease of diversity and richness with increasing urban conditions from the peripheral to the pericentral zone. The identified species of small mammals were categorized according to their dependence on urban environment as exoanthropic species, avoiding the presence of man and his habitations (A. sylvaticus, A. flavicollis, and Clethrionomys glareolus); hemisynantropic species, which thrive on the edges of towns, with greater or lesser affinity to humans (M. arvalis, Apodemus uralensis, Sorex araneus, Sorex minutus, Mus spicilegus, and Microtus subterraneus); and synanthropic species, tied to human dwellings, very dependent on human resources (Crocidura suaveolens).

Similarity of personalities speeds up reproduction in pairs of a monogamous rodent

Animal personality, i.e. stable individual differences in behaviour, is considered to be subject to evolutionary processes, as it has been shown to be heritable and to entail fitness consequences. Different hypotheses have been developed to explain why personality variation is maintained within populations, most likely via processes of balancing selection. One mechanism discussed is that combinations of similar personalities within breeding pairs could increase fitness. We investigated this purported mechanism by studying the association between personality combinations within nulliparous pairs and their onset of reproduction in a monogamous rodent, the mound-building mouse, Mus spicilegus. In seasonal iteroparous breeders, reproductive timing is relevant to fitness, as a delayed onset of breeding potentially limits the number of breeding occasions and lowers the chance that offspring will start reproducing during the same season. Repeated standardized tests carried out prior to pairing revealed consistent individual differences in subjects' behavioural responses with respect to anxiety and exploratory activity, indicating the existence of personality types. Within-pair similarity in anxiety levels affected the chance of reproduction: pairs with similar anxiety scores had a higher probability of breeding, and were quicker to start, during the observation period, independently of the scores of both partners of the pair. We propose that this association between ‘personality matching’ and the onset of reproduction could have important life history consequences in this species and might be one of the mechanisms leading to the maintenance of personality variation within populations.

Stable individual differences in separation calls during early development in cats and mice.

BackgroundThe development of ethologically meaningful test paradigms in young animals is an essential step in the study of the ontogeny of animal personality. Here we explore the possibility to integrate offspring separation (distress) calls into the study of consistent individual differences in behaviour in two species of mammals, the domestic cat (Felis silvestris catus) and the mound-building mouse (Mus spicilegus). Such vocal responses in young mammals are a potentially useful test option as they represent an important element of mother-offspring communication with strong implications for offspring survival. In addition, the neural control of vocalisation is closely associated with emotional state.ResultsWe found marked similarities in the pattern of individual responses of the young of both species to separation from their mother and littermates. In the domestic cat as well as in the mound-building mouse, individual differences in the frequency of calls and to a lesser extent in locomotor activity were repeatable across age, indicating the existence of personality types. Such consistencies across age were also apparent when only considering relative individual differences among litter siblings. In both species, however, individual patterns of vocalisation and locomotor activity were unrelated. This suggests that these two forms of behavioural responses to isolation represent different domains of personality, presumably based on different underlying neurophysiological mechanisms.ConclusionsBrief separation experiments in young mammals, and particularly the measurement of separation calls, provide a promising approach to study the ontogeny of personality traits. Future long-term studies are needed to investigate the association of these traits with biologically meaningful and potentially repeatable elements of behaviour during later life.

Olfactory environment of commensal house mice as a factor that affects the formation of the species composition of the population of rodents in buildings

It was demonstrated that in Y-maze individuals of the outdoor species Myodes glareolus and the semi-synanthropic species Microtus levis avoided the urine odor of commensal Mus musculus. On the contrary mice stayed longer in the maze compartment with the odor of voles. The level of avoidance of commensal mice odor was higher than the other strange odors (urine of rabbit or outdoor mouse Mus spicilegus). It is assumed that the sharp smell of commensal mice is an adaptation designed to hold and protect a particular ecological niche against other species of rodents, i.e., human buildings.

Variability of skull and dental characteristics in Mus spicilegus from the northern border of its distributional range

Results of morphometric analysis of the mound-building mouse (Mus spicilegus) evaluated in this study originate from field trapping in the eastern part of Slovakia during the years 2003–2008. Twenty-four cranial and dental variables and the zygomatic index (A/B) of 80 skulls (43 males, 37 females) were measured and evaluated with respect to the sex of the mice. Despite the fact that the overlap of skull measurements in adult males and females was high, sexual dimorphism was confirmed for several skull and dental traits. On average, the values for adult females of M. spicilegus were higher than males, with the exception of dental traits and the zygomatic index. Significant differences between adult males and females were found for the mean values of ten skull and dental parameters (LB, LCb, FL, LD, LMd, LaZ, LM1, LM1, LaM1 and LaM1). The values for the zygomatic index (A/B) overlapped between both sexes, but the higher average values in adult males were statistically significant. The results showed that the variability of the species confirmed in this paper was probably caused only at the regional level and did not differ from the findings reported by several authors for species from neighboring countries.

U-shaped relationship between ageing and risk-taking behaviour in a wild-type rodent

Coping efficiently with novelty is essential for survival. Although ageing is a universal process, its impact on exploration, gathering information and assessing potential risks in novel and stressful situations is still not well understood. In the mound-building mouse, Mus spicilegus, the dispersal process involves two age classes (2-month-old and overwintered 6-month-old individuals). We compared exploration and risk-taking behaviour of four age groups of these mice in both sexes: young and overwintered dispersers and two older groups (12-month-old and 24-month-old animals) to investigate long-term age-related effects. Responses of these animals to novelty and anxiogenic situations were tested by three different tests: open field, elevated plus-maze and novel object exploration test. As expected, 2-month-old individuals displayed a low level of freezing and a high exploration of aversive places and of a novel object. This risk-taking profile may enable young individuals to disperse efficiently. At 6 months old, although no change was found in males, females already showed signs of anxiety, indicating a sex difference in anxiety development in this species. When 12 months old, both sexes were risk-averse and displayed strong emotional responses. We thus conclude that ageing processes lead to an increase in anxiety in the mound-building mouse. Against all expectations, 24-month-old females and males showed a similar profile to 2-month-old individuals revealing that ageing and anxiety may present a U-shaped relationship. Because the relationship between ageing and anxiety may be nonlinear, a multiple-point approach might be systematically applied in ageing research.

Geometric morphometric analysis of the molars in three species of the genus <i>Mus (Mus)</i> (Rodentia, Muridae) based on the outline method

The relatively new technique of outline-based geometric morphometrics was applied in a study of the variation in the shape of the upper and lower molars among 122 mice, belonging to one species from Iran (Mus musculus) and two species from Europe (Mus macedonicus, Mus spicilegus). Differentiation of specimens based on molar shape was highly dependent on the details of the shape information. Among molars, the second upper and first lower molars are better at separating the species. This method provides a useful way to distinguish species based on the outline of their molars.Keywords: shape variation; upper and lower molars; mice; Iran; Europe.

Correction: Anogenital Distance and Condition as Predictors of Litter Sex Ratio in Two Mouse Species: A Study of the House Mouse (Mus musculus) and Mound-Building Mouse (Mus spicilegus)

Correction: Anogenital Distance and Condition as Predictors of Litter Sex Ratio in Two Mouse Species: A Study of the House Mouse (Mus musculus) and Mound-Building Mouse (Mus spicilegus)

Efficiency of delayed reproduction in Mus spicilegus.

To cope with seasonally varying ecological constraints, some mammals temporally suppress breeding or delay their first reproduction. In field conditions, mound-building mice (Mus spicilegus) born in spring begin to reproduce when 2-3 months old, whereas individuals born at the end of summer delay their first reproduction for 6-8 months until the following spring. In order to test age effects on reproductive performance in M. spicilegus, sexually naïve mice were paired when 2-3 months old or at 6-8 months of age, and surveyed for reproduction. We show here that under laboratory conditions the aging of these mice does not impair their reproductive efficiency. Thus, the hypothesis of a lower reproductive potential in these relatively aged females seems to be contradicted. More surprisingly, the latency from pairing to the first reproduction was greater in the 2-3-month-old adults than in the delayed reproducers (6-8-month-old mice). Mound-building mice that are old enough to have overwintered do not suffer significant reproductive declines, but appear to reproduce as well and more quickly than younger first-time breeders.

Diversity of Prdm9 zinc finger array in wild mice unravels new facets of the evolutionary turnover of this coding minisatellite.

In humans and mice, meiotic recombination events cluster into narrow hotspots whose genomic positions are defined by the PRDM9 protein via its DNA binding domain constituted of an array of zinc fingers (ZnFs). High polymorphism and rapid divergence of the Prdm9 gene ZnF domain appear to involve positive selection at DNA-recognition amino-acid positions, but the nature of the underlying evolutionary pressures remains a puzzle. Here we explore the variability of the Prdm9 ZnF array in wild mice, and uncovered a high allelic diversity of both ZnF copy number and identity with the caracterization of 113 alleles. We analyze features of the diversity of ZnF identity which is mostly due to non-synonymous changes at codons −1, 3 and 6 of each ZnF, corresponding to amino-acids involved in DNA binding. Using methods adapted to the minisatellite structure of the ZnF array, we infer a phylogenetic tree of these alleles. We find the sister species Mus spicilegus and M. macedonicus as well as the three house mouse (Mus musculus) subspecies to be polyphyletic. However some sublineages have expanded independently in Mus musculus musculus and M. m. domesticus, the latter further showing phylogeographic substructure. Compared to random genomic regions and non-coding minisatellites, none of these patterns appears exceptional. In silico prediction of DNA binding sites for each allele, overlap of their alignments to the genome and relative coverage of the different families of interspersed repeated elements suggest a large diversity between PRDM9 variants with a potential for highly divergent distributions of recombination events in the genome with little correlation to evolutionary distance. By compiling PRDM9 ZnF protein sequences in Primates, Muridae and Equids, we find different diversity patterns among the three amino-acids most critical for the DNA-recognition function, suggesting different diversification timescales.

Maternal energetic investment in a monogamous mouse

Concurrent gestation and lactation is costly and rodent females may manage their reproductive effort by adjusting the length of the inter-litter latency. In this study, we attempted to build a model of this phenomenon as a function of maternal condition and energetic investment (measured as the litter size and weight) in the mound-building mouse, Mus spicilegus. We analysed the distributions of two successive inter-litter latencies using linear models. These distributions revealed a high inter-individual variability in latencies (22–38d). Our results showed that none of the parameters reflecting female investment could explain this variability. The only link revealed by our analyses was a significant positive correlation between two successive inter-litter latencies. These results suggested that other parameters were involved in the regulation of inter-litter latencies. We propose that paternal care, which has a direct effect on inter-litter latency, may play a major role by allowing females to save energy or through differential allocation. In addition, genetic characteristics of the females and the prenatal environment of the female should also be considered.

Genetic Architecture of Skewed X Inactivation in the Laboratory Mouse

X chromosome inactivation (XCI) is the mammalian mechanism of dosage compensation that balances X-linked gene expression between the sexes. Early during female development, each cell of the embryo proper independently inactivates one of its two parental X-chromosomes. In mice, the choice of which X chromosome is inactivated is affected by the genotype of a cis-acting locus, the X-chromosome controlling element (Xce). Xce has been localized to a 1.9 Mb interval within the X-inactivation center (Xic), yet its molecular identity and mechanism of action remain unknown. We combined genotype and sequence data for mouse stocks with detailed phenotyping of ten inbred strains and with the development of a statistical model that incorporates phenotyping data from multiple sources to disentangle sources of XCI phenotypic variance in natural female populations on X inactivation. We have reduced the Xce candidate 10-fold to a 176 kb region located approximately 500 kb proximal to Xist. We propose that structural variation in this interval explains the presence of multiple functional Xce alleles in the genus Mus. We have identified a new allele, Xcee present in Mus musculus and a possible sixth functional allele in Mus spicilegus. We have also confirmed a parent-of-origin effect on X inactivation choice and provide evidence that maternal inheritance magnifies the skewing associated with strong Xce alleles. Based on the phylogenetic analysis of 155 laboratory strains and wild mice we conclude that Xcea is either a derived allele that arose concurrently with the domestication of fancy mice but prior the derivation of most classical inbred strains or a rare allele in the wild. Furthermore, we have found that despite the presence of multiple haplotypes in the wild Mus musculus domesticus has only one functional Xce allele, Xceb. Lastly, we conclude that each mouse taxa examined has a different functional Xce allele.