Mus Spicilegus Research Articles

Effects of mound building and caching by steppe mouse (Mus spicilegus Petényi) on the vegetation in agroecosystems

Several rodent species are considered ecosystem engineers. They exert profound changes in agroecosystems by disturbing the soil during their activities. The steppe mouse (Mus spicilegus) inhabits various agroecosystems and constructs conspicuous mounds for overwintering using piled up plant material and soil. These mounds are widespread in many agroecosystems and may significantly affect the vegetation. In our study, we evaluated the effect of mound building activity of the steppe mouse on the vegetation of agroecosystems in Hungary. We sampled the cache content of 90 mounds in total located in old fields, alfalfa fields, and annual crop fields, and surveyed the aboveground vegetation of the mounds and their surrounding undisturbed matrix in 39 paired plots. Mice cached large amounts of seeds belonging mostly to weeds. In total we found 50,413 germinable seeds of 30 species in the cache content samples. However, the mound vegetation and the cache shared only a few species, suggesting that seeds cached by the mice do not contribute to the regenerating vegetation on the mounds. Soil disturbance by mice created distinct vegetation patches with species composition and structure different from the neighbouring undisturbed matrix. Early secondary successional vegetation patches on mounds introduced small-scale heterogeneity into the homogenous agricultural landscape, increased plant diversity and provided distinct flower resources for pollinators. The detected differences in the aboveground vegetation between the mound and the matrix in the studied habitats suggest that the steppe mouse acts as a facultative engineer species in agroecosystems.

Full-length RNA transcript sequencing traces brain isoform diversity in house mouse natural populations.

The ability to generate multiple RNA transcript isoforms from the same gene is a general phenomenon in eukaryotes. However, the complexity and diversity of alternative isoforms in natural populations remain largely unexplored. Using a newly developed full-length transcript enrichment protocol with 5' CAP selection, we sequenced full-length RNA transcripts of 48 individuals from outbred populations and subspecies of Mus musculus, and from the closely related sister species Mus spretus and Mus spicilegus as outgroups. The data set represents the most extensive full-length high-quality isoform catalog at the population level to date. In total, we reliably identify 117,728 distinct isoforms, of which only 51% were previously annotated. We show that the population-specific distribution pattern of isoforms is phylogenetically informative and reflects the segregating single nucleotide polymorphism (SNP) diversity between the populations. We find that ancient housekeeping genes are a major source of the overall isoform diversity, and that the generation of alternative first exons plays a major role in generating new isoforms. Given that our data allow us to distinguish between population-specific isoforms and isoforms that are conserved across multiple populations, it is possible to refine the annotation of the reference mouse genome to a set of about 40,000 isoforms that should be most relevant for comparative functional analysis across species.

Comparison of the exploratory behaviour of wild and laboratory mouse species

In this study, we compared the exploratory behaviour of mound-building mice (Mus spicilegus) and house mice (Mus musculus) with domesticated laboratory mouse strains (BALB/c and C57BL/6). The animals spent 15 minutes in the furnished test box before the exit to the outside world became free. During the 5-minute test, it was noted whether the animal left the familiar environment; if it did, it was recorded in how many seconds. Based on our results, the wild mouse species were more likely to leave the familiar mouse box and explore the outside environment earlier than the laboratory mice. We also found a difference within the wild mouse species, the mound-building mouse being the one that explored the external environment to a greater extent and faster. The effect of domestication manifests in the fact that laboratory mouse strains are less likely to leave their familiar environment and are significantly less active than their wild ancestors.

Матеріали до фауни Бузького Гарду: огляд знахідок дрібних ссавців (Soricidae, Muridae, Cricetidae)

New data on micromammals of the Bug Gard National Nature Park obtained in 2022–2023 are presented. Eight species of this survey group were recorded. They include three species of shrews of the family Soricidae (Crocidura suaveolens, Sorex araneus, and Neomys fodiens); four species of rodents of the family Muridae (Sylvaemus uralensis, S. sylvaticus, Apodemus agrarius, and Mus spicilegus); and one species of rodents of the family Cricetidae (Microtus levis). Two species were found for the first time in the fauna of the Bug Gard NNP: Sylvaemus uralensis and Neomys fodiens. Information on the morphometry and habitats of the collected animals is presented.

Сучасна теріофауна лівобережжя Каньйонового Придністер’я

The article analyses the current state of the mammal fauna of part of Podolian Transnistria, which lies between the rivers Zbruch and Zolota Lypa (southern Ternopil Oblast, Ukraine). To designate the region, the publication uses a term from old Polish sources—Canyon Transnistria—which reflects the prevailing landform. The area of research in old faunal summaries is mentioned only as part of wider regions, such as Galicia, western Ukraine, or Ternopil Oblast. Over the past decades, the number of publications on the mammal fauna of this particular region has increased substantially, which makes it possible to make a summary overview. The modern mammal fauna of the region comprises 60 species belonging to 7 orders, 20 families, and 41 genera. Over the past 70 years, the mammal fauna of the studied region has undergone significant changes. Its dynamic component is almost 27%. It includes species of recent immigrants (Blyth’s pipistrelle Pipistrellus lepidus, mound-building mouse Mus spicilegus, muskrat Ondatra zibethicus), as well as two species that recovered their range (Eurasian beaver Castor fiber, wildcat Felis silvestris); the dynamic component also includes three extinct or probably extinct species—Geoffroy’s bat (Myotis emarginatus), Podolian ground squirrel (Spermophilus odessanus), and European rabbit (Oryctolagus cuniculus). A group of phantom species has been singled out, which are known only from single old finds, and modern studies of these species are far from sufficient to understand their status. It includes the lesser mouse-eared bat (Myotis oxygnathus), Nathusius’s pipistrelle (Pipistrellus nathusii), southern birch mouse (Sicista loriger), and Podolian mole rat (Spalax zemni). Such species as the long-eared bat (Plecotus austriacus) and the pygmy field mouse (Sylvaemus uralensis) appeared in the lists of the mammal fauna of the region due to changes in taxonomy. The rare component of the mammal fauna comprises 18 species (30%). The article provides a brief description of the current state of mammal populations in the region. Conservation recommendations are given for rare species.

The Expansion of House Mouse Major Urinary Protein Genes Likely Did Not Facilitate Commensalism with Humans.

Mouse wild-derived strains (WDSs) combine the advantages of classical laboratory stocks and wild animals, and thus appear to be promising tools for diverse biomedical and evolutionary studies. We employed 18 WDSs representing three non-synanthropic species (Mus spretus, Mus spicilegus, and M. macedonicus) and three house mouse subspecies (Mus musculus musculus, M. m. domesticus, M. m. castaneus), which are all important human commensals to explore whether the number of major urinary protein (MUP) genes and their final protein levels in urine are correlated with the level of commensalism. Contrary to expectations, the MUP copy number (CN) and protein excretion in the strains derived from M. m. castaneus, which is supposed to be the strongest commensal, were not significantly different from the non-commensal species. Regardless of an overall tendency for higher MUP amounts in taxa with a higher CN, there was no significant correlation at the strain level. Our study thus suggests that expansion of the Mup cluster, which appeared before the house mouse diversification, is unlikely to facilitate commensalism with humans in three house mouse subspecies. Finally, we found considerable variation among con(sub)specific WDSs, warning against generalisations of results based on a few strains.

Early Postnatal Experience Modifies Activation of the Pituitary Testicular Complex in Male House Mice (Mus Musculus) Exposed to the Odor of Receptive Con- and Heterospecific Females

For the first time, it was shown that activation of the pituitary–testicular complex in male house mice exposed to the odor of receptive females of their own and closely related species was modified under the influence of early postnatal experience and the maternal environment. We have confirmed associated formation of behavioral and physiological mechanisms of precopulatory isolation in early ontogenesis. The serum levels of free testosterone in males of closely related species M. spicilegus and M. m. wagneri differ, it is significantly lower in mound-building mice. In males fostered by a conspecific female, the level of free testosterone was significantly lower when exposed to a heterospecific female odor in comparison with a conspecific odor. The rearing of M. m. wagneri males by females of a closely related species led to a decrease in the testosterone response caused by exposure to female chemosignals (both con- and heterospecific) and to the absence of differences in the serum level of free testosterone when exposed to the odor of a female of their own or closely related species. These results indicate that the rearing conditions had a significant influence on the formation of hormonal mechanisms of reproductive isolation.

EARLY POSTNATAL EXPERIENCE MODIFIES ACTIVATION OF THE PITUITARY-TESTICULAR COMPLEX IN MALE HOUSE MICE (<i>MUS MUSCULUS)</i> EXPOSED TO THE ODOR OF RECEPTIVE CON- AND HETEROSPECIFIC FEMALES

For the first time, data were obtained proving the modification of the activation of the pituitary-testicular complex of male house mice under the influence of early postnatal experience and the maternal environment when exposed to the odor of receptive females of their own and closely related species. We have confirmed the conjugacy of the formation of behavioral and physiological mechanisms of precopulatory isolation in early ontogenesis. The serum level of free testosterone in males of closely related species M. spicilegus and M. m. wagneri differ, it is significantly lower in mound-building mice. The level of free testosterone of males fostered by a conspecific female was significantly lower when they exposed a heterospecific in comparison with a conspecific female odor. The rearing of M. m. wagneri males by females of a closely related species caused a decrease in the testosterone response of males to the exposure of chemosignals from a female (both con-and heterospecific) and led to the absence of differences in the serum level of free testosterone when they exposed to the odor of a female of their own or closely related species. The data obtained indicate a significant influence of the rearing conditions on the formation of hormonal mechanisms of reproductive isolation.

REARING RODENT PUPS IN FOSTER FAMILIES OF TNEIR OWN OR ANOTHER MAMMAL SPECIES: SURVIVAL AND THE CAUSES OF MORTALITY

Conditions of rearing pups at an early age render a significant impact on subsequent development, reproduction and certain features of the behavior of mammals including rodents. Parents, mostly lactating females, are the main component of the social environment of pups at the early period of postnatal ontogenesis in most mammal species. Therefore, rearing pups in foster families of their own (in-fostering) or another, even taxonomically distant species (cross-fostering) is one of the main methods of assessing the impact of early experience and maternal environment on the development of animal behavior. Cross-fostering or in-fostering is also used for the conservation of valuable animal species. Therefore, more effective fostering methods that provide the maximum survival of the young are necessary to be developed. According to this, we investigated the survival and possible causes of the mortality of rodent pups representing several species in foster families of their own or another mammal species. We conducted a series of experiments on the cross-fostering and in-fostering of house (Mus musculus) and mound-building (Mus spicilegus) mice, yellow steppe lemmings (Eolagurus luteus) and brown rats (Rattus norvegicus), and on rearing rat pups in foster families of the European polecat (Mustela putorius). The proportion of successfully cross-fostered pups (0–68.4) was lower compared to the in-fostered (93.3–100) ones. This result is presumably explained by more significant differences in the maternal environment when reared by a heterospecific female. According to the literature data, the age of foster and recipient female pups, species-specific differences of odor, the presence or absence of a male and the level of paternal care, the level of stress of the mother and offspring, the expression of maternal instinct, the previous female experience in rearing its own and foster pups, the duration of lactation and the nutritional value of maternal milk are the factors that seem to affect the survival and mortality of foster pups.

Study of climbing ability for two closely related mouse species

We tested the climbing ability of two native Hungarian rodent species under laboratory conditions. One mouse species is the mound-building mouse (Mus spicilegus), which is associated with flat, arable environments; the other is the house mouse (Mus musculus), which occurs in many natural and artificial environments following human settlements. We sought answers to the following questions, whether each of these species can use the vertical dimension and whether there is a difference in climbing ability between individuals of different ages of the two species. From our results, we concluded that the climbing ability of mound-building mice is much lower than that of house mice, but young mound-building mice show a much greater inclination towards climbing than adult mound-building mice.

Small mammals in natural and agricultural lands of Slobozhanshchyna (eastern Ukraine): results of a five-year-long survey

The study of the species composition, biological and ecological features of small mammals was carried out for five years (2018–2022) in the surroundings of the village of Rozsohuvata (Kharkiv Oblast, Ukraine). During the study period, nine species of mouse-like rodents and three species of insectivorans were detected. The re-search area is represented by a ravine-beam system, agrocoenoses, field-protecting forest strips, riparian vege-tation around artificial reservoirs and streams, dry meadows, and pastures. Trappings of small mammals were carried out on thirty lines of traps. During the entire period of trapping, the dominant species was Sylvaemus uralensis and in some seasons Sylvaemus sylvaticus dominated. Starting from 2018, the relative abundance increased in autumn, reached a peak in 2020 and declined in the following years. In general, 2019 was the year of maximum abundance and most species were recorded in the summer of this year. The greatest number of species was found in the ecotone between riparian vegetation and field (10 species), as well as in the area of the multi-grass steppe in the beam (8 species). The eurytopic species include Sylvaemus uralensis and Syl-vaemus sylvaticus, whereas the stenotopic species is Mus spicilegus. According to the obtained abundance scores, only one species—Myodes glareolus—occurs randomly, whereas the rare species here are Mus spicile-gus, Sorex minutus, and Crocidura suaveolens. Six species are non-abundant: Apodemus agrarius, Sylvaemus tauricus, Mus musculus, Microtus levis, Cricetulus migratorius, and Sorex araneus. Only Sylvaemus sylvaticus belongs to common species, and only Sylvaemus uralensis is abundant. It should be mentioned that Cri-cetulus migratorius, which usually belongs to the category of random or rare species, turned out to be non-abundant in the study region, and it was recorded regularly in almost half of the studied biotopes. Myodes glareolus, which usually prefers oak forest, was extremely rare. The abundance of Apodemus agrarius, which usually belongs to common species in river valleys, was also low. Sylvaemus showed greater ecological valence, dominated in abundance and inhabited most biotopes, except for Sylvaemus tauricus, which began to occur only in the last two years and mainly in forest strips.

Feed preference and feeding behavior of different mouse species in laboratory housing

The feed preference of two species of wild mice, the house mouse (Mus musculus), and the mound-building mouse (Mus spicilegus) was investigated (kept in our laboratory for 25 generations). Our interest focused on the feed preference (i.e. if the mice choose the type of feed closest to their natural food). The proximate composition of the two granulated feeds offered to mice differed minimally; the crude fat and crude fibre content of the natural feed mixture was higher, and only this feed contained insect protein. Based on the obtained results, both wild mice species approached the natural feed mixture more frequently than the two other granulated feeds. The same tendency was observed for feed consumption where the animals mostly consumed the natural feed mixture. During the 5-day long study, the consumption of the natural feed mixture increased continuously, while the consumption of the granulated laboratory feed decreased significantly. The average feed consumption was also influenced by room temperature. Our studies can help to develop the optimized indoor keeping and breeding of small domesticated mammals.

Bioenergetic changes in response to sperm capacitation and two-way metabolic compensation in a new murine model

The acquisition of fertilizing ability by mammalian spermatozoa, known as “capacitation,” includes processes that depend on particular metabolic pathways. This has led to the hypothesis that ATP demands might differ between capacitated and non-capacitated cells. Mouse sperm can produce ATP via OXPHOS and aerobic glycolysis, an advantageous characteristic considering that these cells have to function in the complex and variable environment of the female reproductive tract. Nonetheless, despite evidence showing that both metabolic pathways play a role in events associated with mouse sperm capacitation, there is contradictory evidence regarding changes promoted by capacitation in this species. In addition, the vast majority of studies regarding murine sperm metabolism use Mus musculus laboratory strains as model, thus neglecting the wide diversity of sperm traits of other species of Mus. Focus on closely related species with distinct evolutionary histories, which may be the result of different selective pressures, could shed light on diversity of metabolic processes. Here, we analyzed variations in sperm bioenergetics associated with capacitation in spermatozoa of the steppe mouse, Mus spicilegus, a species with high sperm performance. Furthermore, we compared sperm metabolic traits of this species with similar traits previously characterized in M. musculus. We found that the metabolism of M. spicilegus sperm responded to capacitation in a manner similar to that of M. musculus sperm. However, M. spicilegus sperm showed distinct metabolic features, including the ability to perform cross-pathway metabolic compensation in response to either respiratory or glycolytic inhibition, thus revealing a delicate fine-tuning of its metabolic capacities.

Experimental Hybridization and Breeding Intensity of House (Mus musculus wagneri) and Mound-Building (Mus spicilegus) Mice: Effect of Early Experiences and the Maternal Environment

Experimental Hybridization and Breeding Intensity of House (Mus musculus wagneri) and Mound-Building (Mus spicilegus) Mice: Effect of Early Experiences and the Maternal Environment

The maturation of exploratory behavior in adolescent Mus spicilegus on two photoperiods.

Dispersal from the natal site or familial group is a core milestone of adolescent development in many species. A wild species of mouse, Mus spicilegus, presents an exciting model in which to study adolescent development and dispersal because it shows different life history trajectory depending on season of birth. M. spicilegus born in spring and summer on long days (LD) disperse in the first 3 months of life, while M. spicilegus born on shorter autumnal days (SD) delay dispersal through the wintertime. We were interested in using these mice in a laboratory context to compare age-matched mice with differential motivation to disperse. To first test if we could find a proxy for dispersal related behavior in the laboratory environment, we measured open field and novel object investigation across development in M. spicilegus raised on a LD 12 h:12 h light:dark cycle. We found that between the first and second month of life, distance traveled and time in center of the open field increased significantly with age in M. spicilegus. Robust novel object investigation was observed in all age groups and decreased between the 2nd and 3rd month of life in LD males. Compared to male C57BL/6 mice, male M. spicilegus traveled significantly longer distances in the open field but spent less time in the center of the field. However, when a novel object was placed in the center of the open field, Male M. spicilegus, were significantly more willing to contact and mount it. To test if autumnal photoperiod affects exploratory behavior in M. spicilegus in a laboratory environment, we reared a cohort of M. spicilegus on a SD 10 h:14 h photoperiod and tested their exploratory behavior at P60-70. At this timepoint, we found SD rearing had no effect on open field metrics, but led to reduced novel object investigation. We also observed that in P60-70 males, SD reared M. spicilegus weighed less than LD reared M. spicilegus. These observations establish that SD photoperiod can delay weight gain and blunt some, but not all forms of exploratory behavior in adolescent M. spicilegus.

Early life parameters and personality affect oxidative status during adulthood in an altricial rodent

It is increasingly recognized that alterations of the cellular oxidative status might be an important cost underlying challenging early life conditions. For example, an increased litter size can impose challenges as the offspring will face increased competition for maternal resources. Within a litter, individuals with relatively higher starting mass typically show higher growth rates, which can lead to increased oxidative damage. We investigated the long‐term consequences of these early life parameters on the oxidative status in mature mound‐building mice (Mus spicilegus). Individual differences in the animals' exploration tendency were assessed by repeated open field and novel object tests. We predicted less exploratory phenotypes, which typically show a higher stress responsiveness, to be particularly susceptible to possible effects of these early life parameters on oxidative status. We quantified oxidative damage of DNA (8‐hydroxy‐2'‐deoxyguanosine levels, 8‐OHdG) and proteins (protein carbonyl content, PCC), and activities of the antioxidants catalase (CAT), glutathione peroxidase (GPx), and superoxide dismutase (SOD) in liver and skeletal muscle tissue. 8‐OHdG levels were positively associated with CAT and SOD in both tissues, indicating that increased oxidative DNA damage was associated with an upregulation of antioxidant production. Hepatic DNA damage after maturity was increased in animals from larger litters. In less exploratory animals, DNA damage and the activity of CAT and SOD in the muscle were increased, but only in individuals with higher relative starting mass (measured on postnatal day 9). This interaction may be explained by the typically higher adrenocortical activity in less exploratory phenotypes and by the higher growth in relatively heavier pups, two factors known to increase oxidative stress. These findings contribute to enlightening the complex interplay between early life conditions, personality, and oxidative status.

In vivo classification of two closely related species of mice, mound-building mouse (Mus spicilegus) and house mouse (Mus musculus)

Correct identification of similar, closely related species with overlapping distribution is a crucial point in field biology. In small mammal studies, species identification is particularly problematic in population studies using trapping where live animals need to be identified. The aim of our research was to develop a method making the classification of the two Hungarian mouse species, mound-building mouse (Mus spicilegus) and house mouse (Mus musculus) possible based on morphometric characters. The basis to obtain reference data was the captive populations of caged animals housed in our laboratory where the true species classification was known for every animal. Body weight, body length, tail length, and tail diameter were measured for 56-56 individuals from both species. From these measurements the ratio of the body length/tail length was also calculated. Besides, the sex and age of these animals were also recorded. Data analysis consisted of stepwise discriminant procedure and discriminant analysis, respectively. The stepwise discriminant procedure restricted the morphometric characters to the ratio of the body length/tail length and tail diameter. Performing the discriminant analysis to these body measures a perfect classification was obtained even using cross-validation. Thus, applying the obtained discriminant function to the classification of any live trapped mice is feasible.

Does Living in Human-Altered Environments Affect Life-History and Personality of Wild Mice?

In urban habitats, animals are faced with different and often challenging environmental conditions compared to their native habitats. Behavior is the fastest response to environmental change and therefore a very important component to adjust to human-altered environments. Behaviors such as novelty responses and innovativeness which allow animals to cope with novel stimuli are often altered in urban populations. The mechanisms producing such adaptations are currently not well understood. In this study, we investigate whether urban living has an impact on the microevolution of mouse behavioral and life-history traits including boldness, stress-coping, growth, longevity, and emphasis on reproduction. We hypothesized that animals living together with humans for longer show increased novelty-seeking and boldness characteristics at the species and subspecies level. We, therefore, compared behavior and life history characteristics among Mus musculus, a commensal rodent, Mus spicilegus as a synanthropic but not commensal, and Apodemus uralensis as a strictly rural species. In addition, we compared three subspecies of M. musculus (in total six populations) that differ in the time living together with humans. Behavioral and life history differences are stronger between populations even of the same subspecies rather than showing a structural trend with the time animals have spent with humans. In addition, species differ in behavior and life history, albeit not in a pattern that suggests an evolutionary adaptation to living in human-altered habitats. We, therefore, suggest that behavioral adaptations of wild mice are geared toward environmental differences such as geographic origin or habitat specifics but not necessarily directly evolve by living together with humans.

Nest Material Preference of Wild Mouse Species in Laboratory Housing

Our research examined the nest-building characteristics of two mouse species native to Hungary, the mound-building mouse (Mus spicilegus) and the house mouse (Mus musculus), under laboratory housing conditions. In indoor housing, the nest-building material plays a very important role in the welfare of the animals. The present study examined how wild mouse species choose from natural nest material. In a three-way test, mice were able to choose whether to make their nest from long blades of hay, nonfibrous cotton, or paper strips. In addition, the effect of nest composition on its quality was also investigated. The test was run at the standard laboratory (21 °C) and lower (10 °C) temperatures, assuming that temperature influences the choice. Based on the results of the three-way selection tests, both species of wild mice chose hay nest material in the highest proportion, and it was also found that the increasing the hay proportion coincided with better nest quality. Mice kept in colder places used more hay nest material for their nests and built better quality nests. Our results show that wild mouse species prefer natural nest-building materials that meet their ecological needs even under laboratory conditions, resulting in a good quality nest. This finding is worth considering in designing appropriate enclosures for wild rodent species.

First knowledge of baculum size in males of the mound-building mouse (Mus spicilegus Petényi 1882) from Slovakia

Abstract In this study was quantified bacular size, variation, and allometry in mound-building mice (Mus spicilegus) from the western Carpathians (Slovakia). The study presents the first knowledge of morphological variation in three baculum traits based on the analysis of 11 adult and 60 subadult males. According to descriptive statistics, bacula are variable in size. Despite the small number of adult individuals, the Mann-Whitney test indicated significant differences (p < 0.05) in proportions between age groups. However, to confirm these results, larger numbers of adults and subadults will need to be tested in the future.