Mus Spicilegus Research Articles

Agonistic and sociable behaviors in the mound‐building mice, Mus spicilegus: A comparative study with Mus musculus domesticus

AbstractPresent social organization and mating systems result from selective pressures and ecological conditions but also from proximate interactions between individuals. Many studies report on a polygynous mating system with a social group territoriality in commensal populations of Mus musculus domesticus. However, little is known about the social organization of other Mus species living in outdoor conditions, such as the mound‐building mouse Mus spicilegus. Comparative studies between M. m. domesticus and M. spicilegus have already shown behavioral differences in female sexual preferences and paternal care. To study agonistic and sociable interactions and gain insight into the social organization and the mating system of M. spicilegus, the present study compared intraspecific dyadic encounters between unfamiliar adults in these two species. Results demonstrated less tolerance between females and between the sexes in M. spicilegus than in M. m. domesticus unfamiliar mice. The consequences of those differences between M. spicilegus and M. m. domesticus on social organization and mating system are discussed. Aggr. Behav. 28:75–84, 2002. © 2002 Wiley‐Liss, Inc.

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.

LINE-1 (L1) lineages in the mouse.

Recently, a rapidly amplifying family of mouse LINE-1 (L1) has been identified and named T(F). The evolutionary context surrounding the derivation of the T(F) family was examined through phylogenetic analysis of sequences in the 3' portion of the repeat. The Mus musculus domesticus T(F) family was found to be the terminal subfamily of the previously identified L1Md4 lineage. The L1Md4 lineage joins the other prototypical mouse LINE-1 lineage (the L1MdA2 lineage) approximately 1 MYA at about the time of the common ancestor of M. m. domesticus, Mus spicilegus, and Mus spretus. However, the T(F) family from M. m. domesticus was found to join to the previously reported M. spretus Ms475 and Ms7024 LINE-1 families at just 0.5 MYA, indicating horizontal transfer. The T(F) family from M. m. domesticus was then found to be even more recently related to LINE-1's from another species, M. spicilegus. A separate spretus A2 lineage was found through a directed search of a PCR library. This lineage, in contrast to the spretus T(F) lineage, does join domesticus at about 1 MYA, as would be expected in the absence of horizontal transfer. A third major family was also found that splits off from the L1Md4 lineage shortly after its departure from the L1MdA2 lineage. The new family, named the Z family, was found to contain the de novo LINE-1 inserts causing the beige and med mutations. Whether the split with the Z family was before or after the recombination that introduced the F-type promoters and defined the inception of T(F) as a lineage is unclear. In enumerating copies of the various LINE-1 families, we found that T(F) 3' ends were not much more numerous than the reported number of 5' ends, suggesting that T(F) may not be subjected to the 90% truncation pattern typical of LINE-1 as a whole.

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.

Female sexual preferences differ inMus spicilegusandMus musculus domesticus: the role of familiarization and sexual experience

Mating systems correspond to particular ecological conditions and result from proximate interactions between individuals. We compared the mating preferences of female mice of two species: the house mouse,Mus musculus domesticus, and the mound-builder mouse,Mus spicilegus. Because of differences in their habitat, we expected to observe differences in their sexual preferences. We studied female preferences for a familiar or an unfamiliar male and the occurrence of copulation with the unfamiliar male, during two states of female sexual activity: (1) the postpartum oestrus of paired females, to evaluate the stability of their sexual partnership; and (2) the oestrus of females familiarized with a male, to study the mechanisms underlying their sexual preferences. In the polygamous house mouse, postpartum oestrous females did not show a clear preference between their familiar male and the unfamiliar one. Moreover, oestrous females, familiarized with a male (without sexual interactions), preferred an unfamiliar male and copulated with him. In contrast, postpartum oestrous females and oestrous females ofM.spicileguspreferred their familiar male and rarely copulated with the unfamiliar male. This study indicates a strong pair bond in established breeding pairs inM.spicilegusand shows that this bond can be established by familiarization, which is not the case inM.m. domesticus. Our study suggests the existence of monogamous traits inM.spicilegusin contrast to the polygamousM.m. domesticus.

Conspecific and heterospecific behavioural discrimination of individual odours by mound-building mice

We have tested the ability of male mound-building mice, Mus spicilegus, to discriminate on the basis of their social odours a) two males of their own species; and b) two males of the house mouse, Mus musculus domesticus. An habituation-dishabituation procedure was used. An experimental animal was presented with the scent from the same stimulus animal for four trials; on the fifth trial, scent from a second stimulus animal was presented. Male Mus spicilegus were able to discriminate the olfactory signatures of two mound-building mouse males but did not discriminate between the olfactory signatures of two house mouse males. The lack of inter-specific individual recognition is discussed in terms of specificity and attractive value of odour cues.

Morphological differentiation in Mus spicilegus and the taxonomic status of mound‐building mice from the Adriatic coast of Yugoslavia

AbstractThe systematic status of a mound‐building mouse population from the Adriatic coast at Ulcinj, Montenegro (Yugoslavia), originally reported as M. hortulanus ssp., is assessed using morphological and morphometric analyses. This population was compared to other M. spicilegus samples from Ukraine & Moldavia, Voivodina (Yugoslavia) and Austria, and to M. macedonicus from Turkey, Greece, and Macedonia. Character states of selected non‐metric traits, along with the presence of a typical mound‐building behaviour, allowed classification of the study population with M. spicilegus. This was also supported by Canonical Variate Analysis on size‐adjusted dental traits. Uni‐ and multivariate morphometric studies revealed marked differentiation between the Ulcinj sample and the remaining M. spicilegus populations. The great deal of morphological divergence suggests a distinct systematic position of the Adriatic population, here described as Mus spicilegus adriaticus ssp. nova. Hypotheses about the possible origin and evolutionary history of the two eastern aboriginal mouse species are discussed.

Morphological differentiation in Mus spicilegus and the taxonomic status of mound-building mice from the Adriatic coast of Yugoslavia

Morphological differentiation in Mus spicilegus and the taxonomic status of mound-building mice from the Adriatic coast of Yugoslavia

6-month-old infants dishabituate to a change in an object's actual postion and not to a change in an object's egocentric position

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.

Social structure of the mound-building mouse Mus spicilegus revealed by genetic analysis with microsatellites.

The Mound-building mouse Mus spicilegus possesses a unique behaviour amongst mice. It constructs large earthen mounds and associated nesting chambers which serve to store food for immature individuals during the winter nesting period. We have used genetic analysis of four autosomal and four X-linked microsatellite loci to determine relationships between individuals inhabiting 40 mounds in Bulgaria. We show that, in almost all cases, individuals in a mound are the product of multiple parentage. We estimate the minimum number of males and female parents contributing offspring to each mound and demonstrate that at least two male and two female parents contribute offspring to a minimum of seven mounds. Analyses of relatedness coefficients and allele sharing values demonstrate that parents of different sibships within mounds are more related than if they had been chosen at random from the population and suggest that it is the female parents that contribute this excess relatedness. These results suggest that the mechanism by which individuals congregate to build mounds is kin-based and that the evolution of mound building and communal nesting in M. spicilegus is due in part to kin selection. This study represents a novel approach to the study of mammalian behavioural ecology. We have used a genetic dataset to construct an outline of social structure in the absence of behavioural data. These inferences can now be used to direct further work on this species.

Do insulin-like growth factors play a role in final follicular maturation: Superovulation as a test model

Mouse oocytes can be obtained via superovulation or using in vitro maturation although several factors, including genetic background, may affect response. Our previous studies have identified various mouse species as models to understand the role of sexual selection on the evolution of sperm traits and function. In order to do comparative studies of sperm–oocyte interaction, we sought reliable methods for oocyte superovulation and in vitro maturation in mature females of three mouse species (genus Mus). When 5 IU pregnant mare's serum gonadotrophin (PMSG) and 5 IU human chorionic gonadotrophin (hCG) were injected 48 h apart, and oocytes collected 14 h post-hCG, good responses were obtained in Mus musculus (18 ± 1.3 oocytes/female; mean ± S.E.M.) and Mus spretus (12 ± 0.8), but no ovulation was seen in Mus spicilegus. Changes in PMSG or hCG doses, or longer post-hCG intervals, did not improve results. Use of PMSG/luteinizing hormone (LH) resulted in good responses in M. musculus (19 ± 1.2) and M. spretus (12 ± 1.1) but not in M. spicilegus (5 ± 0.9) with ovulation not increasing with higher LH doses. Follicular puncture 48 h after PMSG followed by in vitro maturation led to a high oocyte yield in the three species (M. musculus, 23 ± 0.9; M. spretus, 17 ± 1.1; M. spicilegus, 10 ± 0.9) with a consistently high maturation rates. In vitro fertilization of both superovulated and in vitro matured oocytes resulted in a high proportion of fertilization (range: 83–87%) in the three species. Thus, in vitro maturation led to high yields in all three species. These results will allow future studies on gamete interaction in these closely related species and the role of sexual selection in gamete compatibility.

Substitution rate variation in closely related rodent species.

The existence of evolutionary rate variation has previously been demonstrated between different orders, different species and even between different regions of the same gene. To examine rate variation between closely related species of rodents we have sequenced the adenine phosphorybosyltransferase (APRT) gene from Mus spicilegus, Mus pahari, Mastomys hildebrandtii, Stochomys longicaudatus and Gerbillus campestris and compared these sequences with the previously published Mus musculus, Rattus norvegicus and Mesocricetus auratus APRT sequences. The alignment of these eight rodent APRT sequences reveals two large insertions within the introns: an insertion with sequence similar to a B1 repetitive element is found within Mastomys and an insertion with sequence similar to a B2 repetitive element is found within M. pahari. A phylogeny for the rodent APRTs agrees with the previously published rodent phylogeny based on other molecular and morphological data. The relative rate test which is often used to test for variation in rates of evolution in different lineages is shown here to be sensitive to the choice of outgroup and therefore should be used with great caution. This sensitivity is detectable only with closely related species and results from the prevalence of homoplastic substitutions. Rate variation is demonstrated within the APRT exons and introns and between the rodent species (with the most significant difference being a rate difference in M. spicilegus). In addition, some third codon positions are shown to be more prone to substitution than others. This clearly demonstrates that even between very closely related species there is ample evidence of major differences in rates of evolution among species, among regions of the gene and among different positions within the gene. We also demonstrate that standard methods of analysis might not detect this variation.

Evolutionary rate variation within Mus APRT.

Rodents are thought to have relatively high rates of evolution, twice as fast as the rates for mammals in other orders. However, the uniformly high rates of evolution inferred for the order Rodentia from Mus musculus and Rattus norvegicus are not consistently found for other rodent species. Using a maximum likelihood phylogenetic algorithm (DNAML), we show here that Mus spicilegus has a fivefold different rate of evolution in 1100 bp around the adenine phosphoribosyltransferase gene (APRT) since its divergence from a common ancestor with Mus musculus. A greater than threefold difference in rates is also found in a comparison of the number of evolutionary events directly detected from the APRT sequences of these two closely related Mus species. The evolutionary events can be directly detected, since M. spicilegus, M. musculus, and the four rodent outgroup species used to determine the ancestral sequence are so closely related. One of the major differences between M. spicilegus and M. musculus that might affect evolutionary rate is the degree of commensalism with man. The Mus species therefore provide a useful model for testing various hypotheses for the causes of rate variations between genes, and possibly, between lineages.

Different patterns of retinal cone topography in two genera of rodents, Mus and Apodemus

Recently, we have reported the peculiar topographic separation of shortwave- and middlewave-sensitive (S and M) cones in the retina of the common house mouse (Mus musculus) and in a number of inbred laboratory mouse strains derived from the same species. In an attempt to follow the phylogeny of the complementary cone fields, we have investigated the retina of other mouse-like rodents. Two monoclonal anti-visual pigment antibodies, OS-2 and COS-1, specific to the S and M cones, respectively, have been used to identify the two cone types. Immunocytochemistry on retinal sections and on whole-mount preparations have shown that, as in the house mouse, the two cone types in the mound builder mouse (Mus spicilegus) occupy opposite halves of the retina. In contrast, in the wood mouse (Apodemus sylvaticus), both cone types are scattered uniformly across the whole retinal surface. Another distinguishing feature between the two genera is the frequency of the S cones. Whereas their density in the Mus species is above 7,000/mm2 in the S-field, the maximum density of the S cones in A. sylvaticus is one order of magnitude smaller. In another species of this genus (the herb field mouse, A. microps), the S cones are completely missing.

Restriction fragment length polymorphism and evolution of the mouse immunoglobulin constant region gamma loci.

Genomic DNA from twelve laboratory mouse strains, in addition to 21 wild-derived strains belonging to different taxa (Mus musculus domesticus, Mus musculus musculus, Mus spretus, Mus macedonicus, and Mus spicilegus) and four mouse strains that are evolutionarily more distant, were analyzed by Southern blot for polymorphism of the Ig heavy chain constant region gamma isotype (Igh-C gamma) and for the distribution of the duplicated Igh-1 (C gamma 2 alpha) haplotype. Distinct allelic forms of each Igh-C locus could be defined by restriction fragment length polymorphism (RFLP). In laboratory mouse strains RFLP proved to be more sensitive in the detection of Igh-4 (C gamma 1) alleles than serological methods. Taq I digestion allowed the definition of two alleles in the Igh-8 (C gamma 3) locus, which is absolutely conserved at the protein levels. More extensive RFLP could be found in wild strains belonging to the subgenus Mus and in the evolutionarily more distant Mus species belonging to other subgenera. In previous studies we have shown that the Igh-1 locus is duplicated in M. m. musculus subspecies. We now extend this observations to the wild mouse strains belonging to M. spicilegus and M. macedonicus species and to the evolutionarily more distant wild mouse strain Mus pahari (subgenus coelomys), which is thought to have diverged from domestic mice about 5 million years ago. In addition, we found a similar RFLP pattern in ten of 18 wild mice trapped in India, suggesting that the haplotype containing the two Igh-1-like genes, organized in tandem as distinct isotypes, is widely spread in natural populations. The evolution of murine Igh-C gamma-encoded isotypes is also discussed.

Dominant expression of a distinctive V14+ T-cell antigen receptor alpha chain in mice.

A distinctive variable region 14-positive (V14+) alpha chain (V alpha 14+) of the T-cell antigen receptor is predominantly expressed in multiple mouse subspecies. The V alpha 14 family has two members, V alpha 14.1 and V alpha 14.2, which differ by only three amino acids at positions 50-52. Based on the EcoRI restriction fragment length polymorphism of the gene encoding V alpha 14, mice can be divided into three groups: type I with an 11.2-kilobase (kb) fragment, type II with a 2.0-kb fragment, and type III with the 2.0-kb and 11.2-kb fragments. Usage of V alpha 14-J alpha 281, where J alpha 281 is an alpha-chain joining segment, with a one-base N region dominates at the level of 0.02-1.5% of alpha chains in all laboratory strains, Mus musculus castaneus, and Mus musculus domesticus but not in Mus musculus molossinus, Mus musculus musculus, and Mus spicilegus samples. The preferential V alpha 14-J alpha 281 expression seems to be due to positive selection because the V-J junctional region is always glycine, despite the ability of the V alpha 14 gene to associate with J alpha other than J alpha 281. As V alpha 14-J alpha 281 expression is independent of known major histocompatibility complex antigens, including H-2, TLA, Qa, and HMT, the selecting ligand must be a monomorphic molecule of the mouse, expressed in a subspecies-specific manner. Additional observations, such as the expression of homogeneous V alpha 14-J alpha 281 in athymic mice, suggest that the positive selection of V alpha 14+ T cells occurs extrathymically.

Recent evolutionary origin of the expression of the glial fibrillary acidic protein (GFAP) in lens epithelial cells. A molecular and genetic analysis of various mouse species

We have investigated the phylogenetic distribution of the glial fibrillary acidic protein (GFAP) in lens epithelial cells (LEC) of various mouse species within the genus Mus. We have shown that lens GFAP is expressed in mice of the Mus musculus complex and in Mus spicilegus and Mus macedonicus species (L.GFAP(+) phenotype) while it is absent in Mus spretus, Mus caroli and Mus cooki species (L.GFAP(−) phenotype). Our results argue in favour of one of the phenograms illustrating the probable phylogenetic relationships between these species in the genus Mus. In animals where lens GFAP was immunodetected, Northern blots of lens RNA extracts hybridized with a mouse GFAP cDNA probe, revealed a single 2.7 kb band. Comparative Northern blot analysis of lens tissue from L.GFAP(+) mice or of brain tissue from L.GFAP(+) or L.GFAP(−) mice did not show any size heterogeneity of the GFAP mRNA. The pattern of the GFAP immunostaining of astroglial cells in brain was identical in both L.GFAP phenotypes. Analysis of interspecific crosses showed that the L.GFAP(+) character is transmitted in a dominant fashion and seems to be linked to the Mus musculus Gfap gene. In this study we have also confirmed the localization of the mouse Gfap gene on chromosome 11.

Variants of the Y‐chromosome in sympatric taxa ofMusin southern USSR

Abstract Karyotypes of males of house mice were studied in European and Asiatic areas of USSR. They are differentiated according to Y‐chromosome morphology, two variants of which are discussed with respect to species‐diagnostic differences. A ≪large≫ variant regards the 19th pair of autosomes, most common in indoor as well as outdoor samples, including biochemically tested Mus musculus and M. m. domesticus. A substantially ≪small≫ variant was found , in wild short‐tailed mice only. The miniature Y‐chromosome was also detected during analysis of karyograms of M. spretus from the western Mediterranean. The three taxa with unique miniature Y‐chromosome seem to correspond to three subspecies, which were considered to be united in a separate species, Mus spicilegus. The possibility of using the new simple cytogenetic marker for diagnosis of. sympatric mice populations of two presumably distinct species, M. musculus and M. spialegus, and for historic reconstructions of their man‐related distribution is discussed.

Serological survey of complement factor H in common laboratory and wild mice: a new third allotype

Antigenic specificities of complement factor H from mice were studied serologically. In addition to previously reported allotypes, referred to as H.1 and H.2, a new allotype of complement factor H, H.3, was identified in the BFM/2Ms strain derived from European wild mice. Using three different alloantisera raised against the various mouse factor H allotype, a serological survey of the common laboratory strains and wild-derived strains of Mus musculus and its relatives, Mus spretus, Mus spretoides, and Mus spicilegus was carried out. All of the common laboratory strains examined in this survey had the H.1 allotype except for STR/N which had H.2. The geographical distributions of factor H allotypes in M. musculus were specific to the subspecies. Mice derived from Mus musculus domesticus and Mus musculus castaneus had the H.1 allotype. Mice derived from M. m. musculus, Mus musculus bactrianus, and Mus musculus molossinus had the H.2 allotype. Only BFM/2Ms and BFM/1Mpl strains derived from M. m. domesticus had the novel H.3 allotype. Sera of mice from strains derived from M. spretoides and M. spicilegus cross-reacted with H.2-specific antiserum, and those from M. spretus cross-reacted with H.3-specific antiserum.

Evolutionary relationships between laboratory mice and subspecies of Mus musculus based on the genetic study of pancreatic proteinase loci, Prt-1, Prt-2, Prt-3, and Prt-6.

Various patterns of mouse pancreatic proteinase activity bands were observed on agarose gel electrophoresis. Prt-1a and Prt-1b genes control the positive (PRT-1A) and negative (PRT-1B) expression of tryptic band V, respectively; Prt-2a and Prt-2b correspond to chymotryptic bands II (PRT-2A) and III (PRT-2B); Prt-3a and Prt-3b control the low (PRT-3A) and high (PRT-3B) tryptic activities of band IV; the Prt-1 and Prt-3 loci are closely linked on the same chromosome; Prt-6a and Prt-6b correspond to tryptic bands I (PRT-6A) and I' (PRT-6B). Twenty-four laboratory strains from the United States showed the phenotype PRT-1A, PRT-3A, and PRT-2A. Of laboratory strains established in Europe, 6 showed PRT-1A, PRT-3A, and PRT-2A, and 10 had PRT-1B, PRT-3A, and PRT-2A bands. Most wild mice around the world and their descendants showed the phenotype PRT-1B, PRT-3B, and PRT-2A. Only the phenotype of M. m. brevirostris was PRT-1A, PRT-3A, and PRT-2A, which was the same as most laboratory inbred strains. PRT-2B was observed mainly in Japanese (M.m. molossinus) and Korean (M.m. yamashinai) wild mice. PRT-6B was detected only in Mus spicilegus and Mus caroli, but all other mice including wild populations and laboratory strains showed PRT-6A. New biochemical phenotypes such as PRT-2C and PRT-3C were also found in this study.