Use of the MHC for mate choice in wild house mice (Mus domesticus)

The mechanisms maintaining natural diversity at the major histocompatibility complex (MHC) are not well understood. To increase knowledge of one potential mechanism, I examined the use of MHC genes for mate choice by wild house mice in a controlled laboratory setting. Three rearing groups of wild test mice were produced: non‐fostered control mice, mice fostered into families of an inbred laboratory mouse strain, and mice fostered into families of a second, MHC‐congenic mouse strain. Mature test mice were given a choice of two opposite‐sex stimulus mice from the two MHC‐congenic strains used for fostering, and were scored for several measures of preference. The results were non‐significant in general, but females of two rearing groups spent significantly more time with mice of one MHC‐type, and in most rearing groups, mice tended to spend more time with this same MHC‐type. Other results showed that male test mice ejaculated indiscriminantly and that female wild mice mated to ejaculation more often in longer length trials, but showed no significant preferences. In this study, fostering seemed to have little or no effect on MHC‐based mate preferences of wild house mice, and wild mice did not appear to be using the MHC to avoid inbreeding. However, some wild female mice used the MHC to choose potential mates. This revised version was published online in July 2006 with corrections to the Cover Date.     

A molecular characterization of the charismatic Faroe house mouse

Faroe house mice are a ‘classic’ system of rapid and dramatic morphological divergence highlighted by J. S. Huxley during the development of the Modern Synthesis. In the present study, we characterize these charismatic mice using modern molecular techniques, examining specimens from all Faroe islands occupied by mice. The aims were to classify the mice within the modern house mouse taxonomy (i.e. as either Mus musculus domesticus or Mus musculus musculus) using four molecular markers and a morphological feature, and to examine the genetic diversity and possible routes of colonization using mitochondrial (mt) control region DNA sequences and microsatellite data (15 loci). Mice on the most remote islands were characterized as M. m. domesticus and exhibited exceptionally low genetic diversity, whereas those on better connected islands were more genetically diverse and had both M. m. musculus and M. m. domesticus genetic elements, including one population which was morphologically M. m. musculus‐like. The mtDNA data indicate that the majority of the mice had their origins in south‐western Norway (or possibly southern Denmark/northern Germany), and probably arrived with the Vikings, earlier than suggested by Huxley. The M. m. musculus genetic component appears to derive from recent mouse immigration from Denmark. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 102 , 471–482.     

Inferences of selection and migration in the Danish house mouse hybrid zone

We analysed the patterns of allele frequency change for ten diagnostic autosomal allozyme loci in the hybrid zone between the house mouse subspecies Mus musculus domesticus and M. m. musculus in central Jutland. After determining the general orientation of the clines of allele frequencies, we analysed the cline shapes along the direction of maximum gradient. Eight of the ten clines are best described by steep central steps with coincident positions and an average width of 8.9 km (support limits 7.6–12.4) flanked by tails of introgression, indicating the existence of a barrier to gene flow and only weak selection on the loci studied. We derived estimates of migration from linkage disequilibrium in the centre of the zone, and by applying isolation by distance methods to microsatellite data from some of these populations. These give concordant estimates of σ =  0.5–0.8 km generation     . The barrier to gene flow is of the order of 20 km (support limits 14–28), and could be explained by selection of a few per cent at 43–120 underdominant loci that reduces the mean fitness in the central populations to 0.45. Some of the clines appear symmetrical, whereas others are strongly asymmetrical, and two loci appear to have escaped the central barrier to gene flow, reflecting the differential action of selection on different parts of the genome. Asymmetry is always in the direction of more introgression into musculus , indicating either a general progression of domesticus into the musculus territory, possibly mediated by differential behaviour, or past movement of the hybrid zone in the opposite direction, impeded by potential geographical barriers to migration in domesticus territory.  © 2005 The Linnean Society of London, Biological Journal of the Linnean Society , 2005, 84 , 593–616.     

Linkage-dependent gene flow in a house mouse chromosomal hybrid zone

In the alpine valley of Valtellina there are two Robertsonian chromosomal races of house mouse, the Poschiavo (POS: 2n = 24-26) characterized by metacentric 8.12 and acrocentrics 2 and 10 and the Upper Valtellina (UV: 2n = 22-24) characterized by metacentrics 2.8 and 10.12. The races inhabit separate villages in the valley except in Sommacologna and Sondalo, where they both occur together with hybrids. A total of 179 mice from 16 villages were typed at 13 microsatellite loci. Seven of these loci were localized close to the centromeres of chromosomes 10 and 12, with the prediction that these regions on the race-specific chromosomes would be the most likely to experience a barrier to gene flow. The remaining six loci were localized at the telomeres of chromosomes 10 and 12 and at the centromeres of chromosomes that do not differ between the races. Substantial differences in allelic frequencies were found between the villages with POS and UV races at five of the loci at the centromeres of chromosomes 10 and 12 but at none of the other loci. These differences were not found to distinguish the two races in Sommacologna and Sondalo. Therefore, the centromeric regions of race-specific chromosomes do appear to experience a barrier to gene flow, although this can break down under intense interbreeding between the races. These results are considered in the context of Harrison's (1990) concept of the semipermeability of hybrid zones to gene exchange and in relation to parapatric speciation.     

Influence of physical environmental characteristics and anthropogenic factors on the position and structure of a contact zone between two chromosomal races of the house mouse on the island of Madeira (North Atlantic, Portugal)

Aim This study aimed to investigate if and how environmental characteristics (physical factors of the natural environment and the human impact on the landscape) influence the position and structure of a contact zone between two chromosomal races of the house mouse (Mus musculus domesticus Rutty 1712) from the island of Madeira. Location The western part of Madeira, a volcanic island in the North Atlantic. Methods Mice were sampled along a south/north‐western transect following the main road, in human‐modified outdoor habitats. Karyotypes of mice were determined using the yeast‐stimulated bone marrow cell method. Trapping sites were characterized in terms of their physical (altitude, temperature, precipitation and soil type) and habitat (human landscape use and occupancy) features. Demographic parameters of mouse populations, based on trapping‐with‐removal techniques, were also analysed (relative abundance, sex‐ratio, juvenile ratio and female fertility ratio), as well as body size (weight and length). Results Four chromosomal zones were identified on the basis of the frequency of two diagnostic rearrangements (Rb(6.7) in race E. Calheta and Rb(7.15) in race A. Cruz). E. Calheta was present in the two southern‐most zones, followed by the contact zone characterized by the presence of two inter‐racial hybrids and the co‐occurrence of mice belonging to the two races. The northern‐most part of the transect was occupied by A. Cruz. Environmental features differed leading us to split the transect into two parts. The southern part is characterized by lower altitude and precipitation, milder temperature, better soil quality supporting vegetable crops and vineyards, and more abundant and evenly distributed human habitats. This southern part is occupied by E. Calheta mice. The north‐western part presents characteristics opposite to those described above with cereals as the main cultivated crop, and it includes the contact zone as well as the zone inhabited by A. Cruz mice. The demographic parameters evaluated in this study did not differ significantly between chromosomal zones. Main conclusions This ecological survey highlights differences in climatic and edaphic features that have moulded the agricultural activities of humans, contributing to a differentiation of their spatial development, and hence the structure of potential habitats for mice. Results are interpreted within the source–sink framework of population dynamics, following which E. Calheta may function as a source and the areas where A. Cruz and the contact zone are located may function as a sink. Our study suggests that the position and chromosomal composition of the contact zone is influenced by the human component underlying broader environmental features. Similar characteristics were most likely present during the historical settlement of Madeira. They may have favoured the independent divergence of the two races and influenced the dynamics of the contact zone.     

Molecular insights into the colonization and chromosomal diversification of Madeiran house mice

The colonization history of Madeiran house mice was investigated by analysing the complete mitochondrial (mt) D-loop sequences of 156 mice from the island of Madeira and mainland Portugal, extending on previous studies. The numbers of mtDNA haplotypes from Madeira and mainland Portugal were substantially increased (17 and 14 new haplotypes respectively), and phylogenetic analysis confirmed the previously reported link between the Madeiran archipelago and northern Europe. Sequence analysis revealed the presence of four mtDNA lineages in mainland Portugal, of which one was particularly common and widespread (termed the 'Portugal Main Clade'). There was no support for population bottlenecks during the formation of the six Robertsonian chromosome races on the island of Madeira, and D-loop sequence variation was not found to be structured according to karyotype. The colonization time of the Madeiran archipelago by Mus musculus domesticus was approached using two molecular dating methods (mismatch distribution and Bayesian skyline plot). Time estimates based on D-loop sequence variation at mainland sites (including previously published data from France and Turkey) were evaluated in the context of the zooarchaeological record of M. m. domesticus. A range of values for mutation rate (μ) and number of mouse generations per year was considered in these analyses because of the uncertainty surrounding these two parameters. The colonization of Portugal and Madeira by house mice is discussed in the context of the best-supported parameter values. In keeping with recent studies, our results suggest that mutation rate estimates based on interspecific divergence lead to gross overestimates concerning the timing of recent within-species events.     

A potential multivariate index of condition for small mammals

Abstract

Post‐weaning growth rates were measured for juvenile house mice (Mus domesticus) reared under four experimental treatments representing dietary conditions in cereal‐growing areas of southeastern Australia. The mice were bred in captivity from adult wild mice captured in mature dry cereal crops during summer. Juvenile mice were caged in pairs at 23°C and offered a diet of either ripening wheat heads or mature dry wheat heads, with or without access to free water. All diets were adequate for survival, but juvenile mice on a diet of ripening wheat with water available grew at 0.25 g day–1, 260% faster than those on a diet of mature wheat and deprived access to free water. Mice on a diet of ripening wheat but deprived of free water and those on a diet of mature wheat with water available grew at intermediate rates. Post‐weaning growth rates of mice in all treatment groups were higher when the young were weaned at higher body mass. The results have implications for estimates of growth, timing of sexual maturity and reproduction of mice in field populations, and indicate that prolonged access to ripening grain and/or relief from moisture stress are likely to be critical to rapid population increase during population outbreaks.     

Chromosomal variation in the house mouse

Although the standard karyotype of the western house mouse, Mus musculus domesticus , consists entirely of acrocentric chromosomes, there are 97 distinct 'populations' that are characterized by various combinations of metacentric chromosomes that have arisen by Robertsonian (Rb) fusions and whole-arm reciprocal translocations (WARTs). In this review we discuss the processes behind the origin and fixation of these rearrangements and then present a unified list of all known metacentric populations and evaluate their phylogenetic relationships. Eleven independent phylogeographical 'systems', each consisting of 2–25 metacentric populations, were identified in Scotland, Denmark, Northern Europe–Northern Switzerland, Southern Switzerland, Northern Italy, Croatia, Spain, Central–Southern Italy, Peloponnesus, Mainland Greece and Madeira. There are six isolated metacentric populations that do not belong to any of these systems. To generate phylogenies of the metacentric populations within each system, we determined those outcomes with the fewest steps regarding accumulation of metacentrics by Rb fusions, WARTs and zonal raciation and taking into account geographical proximity. These phylogenies should be viewed as working hypotheses that will be refined with further chromosomal and molecular data and improvements in methods of phylogenetic reconstruction. The list of metacentric populations and our phylogenies are also published electronically and can be accessed at http://www.studenec.ivb.cz/Projects/RobertsonianMice/ .  © 2005 The Linnean Society of London, Biological Journal of the Linnean Society , 2005, 84 , 535–563.     

Assessment of mate preference in the house mouse with reference to investigations on assortative mating

This study analysed patterns of mate choice based on different types of laboratory test, and points out the advantages of combined methods to assess mate preference. We compared dyadic encounters and two-way choice tests involving a pair of mice or their urinary signature. Preference was assessed in males and females of the two European subspecies of the house mouse Mus musculus that share a secondary hybrid zone. A preference was deduced from directional choice or behavioural discrimination in favour of a mouse. Our results show discrepancies between the outcomes of the different types of test, which we discuss in terms of the quality of the stimuli involved, and of physical access to the information carried by those stimuli. Despite variation, our results indicate that M. m. domesticus did not show a preference, but could discriminate between stimuli of the two subspecies and tended to direct sexual behaviour assortatively. In contrast, both male and female M. m. musculus showed positive discrimination and preference for potential mates and signals carried by their own subspecies. Additionally, our results confirm that subspecies informative signals are present in mouse urine and suggest that they may be molecules of low volatility, necessitating contact for preference to be displayed.  © 2005 The Linnean Society of London, Biological Journal of the Linnean Society , 2005, 84 , 461–471.     

Genetic structure of insular Mediterranean populations of the house mouse

The genetic structure of six western Mediterranean island populations of Mus musculus domesticus were investigated by means of an electrophoretic analysis at 34 loci and compared to that of five neighbouring mainland populations. No reduction in variability (H = 0.09 for both island and mainland samples) was observed in the island populations except for a very small island (6 ha), in which one-third of the variability was lost. Patterns of colonization inferred from a Wagner cluster analysis and the distribution of rare variants suggest that, although these island populations are clearly related to European mainland mice, their genetic structure is the result of multiple founding events from sources dispersed throughout the Mediterranean Basin. Furthermore, the presence of the same rare alleles in Sardinia, Corsica and Piana, suggest that the three islands share a common history of colonization.
Estimates of genetic distance and gene flow indicate that the level of genie differentiation is greater between island and mainland populations that between the latter due to geographic isolation. Multiple founder events and post-colonization evolution are the factors that best explain the observed levels of genie variability and differentiation in these Mediterranean islands.     

An analysis of signatures of selective sweeps in natural populations of the house mouse

Population and locus-specific reduction of variability of polymorphic loci could be an indication of positive selection at a linked site (selective sweep) and therefore point toward genes that have been involved in recent adaptations. Analysis of microsatellite variability offers a way to identify such regions and to ask whether they occur more often than expected by chance. We studied four populations of the house mouse (Mus musculus) to assess the frequency of such signatures of selective sweeps under natural conditions. Three samples represent the subspecies Mus m. dometicus [corrected] and came from Germany, France, and Cameroon. One sample came from Kazakhstan and constitutes a population of the subspecies Mus m. [corrected] musculus. Mitochondrial D-loop sequences from all animals confirm their respective assignments. Approximately 200 microsatellite loci were typed for up to 60 unrelated individuals from each population and evaluated for signs of selective sweeps on the basis of Schl?tterer's ln RV and ln RH statistics. Our data suggest that there are slightly more signs of selective sweeps than would have been expected by chance alone in each of the populations and also highlights some of the statistical challenges faced in genome scans for detecting selection. Single-nucleotide polymorphism typing of one sweep signature in the M. m. domesticus populations around the beta-defensin 6 locus confirms a lowered nucleotide diversity in this region and limits the potential sweep region to about 20 kb. However, no amino acid exchange has occurred in the coding region when compared to M. m. musculus. If this sweep signature is due to a recent adaptation, it is expected that a regulatory change would have caused it. Our data provide a framework for conducting a systematic whole genome scan for signatures of selective sweeps in the mouse genome.     

Molecular studies on the colonization of the Madeiran archipelago by house mice

To study the colonization history of the house mouse (Mus musculus domesticus) on the Madeiran archipelago, complete mitochondrial D-loop sequences were obtained for 44 individuals from Madeira, Porto Santo and Ilhas Desertas. Altogether, 19 D-loop haplotypes were identified which formed part of a single clade in a phylogeny incorporating haplotypes from elsewhere in the range of M. m. domesticus, indicating that the Madeiras were colonized from a single source. Similarities between the sequences found in the Madeiras and those in Scandinavia and northern Germany suggest that northern Europe was the source area, and there is the intriguing possibility that the Vikings may have accidentally brought house mice to the archipelago. However, there is no record of Vikings visiting the Madeiras; on historical grounds, Portugal is the most likely source area for Madeiran mice and further molecular data from Portugal are needed to rule out that possibility.     

Changes in body condition and body size affect breeding and recruitment in fluctuating house mouse populations in south‐eastern Australia

Changes in body condition and body size in field populations of house mice, Mus domesticus, were examined to investigate why mouse populations do not increase rapidly in some years when favourable environmental and demographic conditions indicate they might. Mice had repeated seasonal patterns each year in breeding, growth rates and body condition that reflected the seasonal availability of food, but mean levels for each parameter varied among years. In most years mice lost body condition during summer, breeding declined and population growth slowed. Rapid population growth occurred when body condition was generally high and was maintained throughout summer. Female mice with large body length were more likely to breed than smaller mice, at all times, but changes in body condition accounted for most of the variability in female breeding activity between years and between habitats, and for the seasonal changes in the importance of body length. During rapid population growth, the recruitment rate of juveniles relative to the number of breeding females was 150–300% higher than in other years but adult survival rates were not higher. The data indicate that the ability of mice to maintain body condition, particularly when subject to moisture stress in summer, affects the proportion of females breeding, the number of juveniles weaned and their body condition at weaning, and is promoted by foraging conditions that favour maintenance of juvenile body condition after weaning. These factors, in turn, greatly affect juvenile recruitment rates and eventual population density of mice. Low juvenile survival is suggested as a reason that numbers of house mice in southern Australian cereal‐growing areas do not increase rapidly in some years when other parameters are favourable. Similar processes are likely to play a role in regulating other rodent populations.     

Effect of Robertsonian translocations on sperm head form in the house mouse

Sperm morphology reflects a long process of adaptation to external conditions and the barriers encountered before ova fertilization can take place; however, not all morphological variation found in gametes can be explained by the effects of these selective forces, as the genetic component may also contribute to the establishment of different gametic features. In north‐eastern Spain, there is a wide Robertsonian system of Mus musculus domesticus, where individuals with 2n ranging from 27 to 40 chromosomes have been described. To elucidate the effect of the karyotype on sperm head form, a comparative analysis between different chromosomal groups of mice from this zone was carried out. Sperm heads from eight St (2n = 40) and 24 Rb (2n = 30–39) males were processed for scanning electron microscopy and analysed using geometric morphometric techniques. Canonical variate analyses showed substantial shape differences between St and Rb mice in the ventral spur region and between Rb groups in the post‐acrosomal region. Significant differences in sperm head size were also detected between chromosomal groups. Structural disorders related to spermatogenesis, genetic alterations, and epistatic interactions among loci are probably involved in the relationship between the phenotypic variation of the sperm head and Rb translocations. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 110 , 878–889.     

Morphology, growth and reproduction in the Australian house mouse: differential effects of moderate temperatures

The house mouse ( Mus musculus domesticus ) was introduced into Australia two centuries ago and is now succeeding in a wide range of habitats and climatic regions. To explore how mice exploit such extreme environments, we compared growth rate, morphology and reproductive success of animals reared under differing thermal regimes (13 °C 'cool', 22 °C 'moderate' and 30 °C 'warm') in laboratory mice derived from wild stock. 'Warm' group young were smaller and grew more slowly than those from other groups. At 6 weeks of age, body mass was less in 'warm' than in 'cool' treatment individuals; and liver mass/body mass also was less in 'warm' than in 'cool' treatment individuals. Paired kidney mass/body mass and paired adrenal mass/body mass were less in 'warm' than in 'cool' and 'moderate' treatment mice. Low heritability values indicate that these effects were from the temperature treatments rather than genetic influences. Irrespective of temperature treatment, females were more likely to produce a litter from post-partum matings if they were experienced, rather than young or reproductively naïve, and also bore more young from post-partum matings. These observations contribute to understanding of the sudden plague activities of mice in some parts of Australia and also their sparse distribution in the interior of the continent.  © 2008 The Linnean Society of London, Biological Journal of the Linnean Society , 2008, 94 , 21–30.     

Effect of additional food and water on house mice in a semi‐arid agricultural environment in Australia

Abstract We tested the hypothesis that providing high‐quality food and water would increase reproduction, survival and population size in house mice living in a semi‐arid cropping environment in the mallee region of western Victoria, Australia, where outbreaks of house mice (Mus domesticus) occur irregularly. We employed a factorial design and applied treatments along internal fencelines (16 sites), adjacent to cropping areas, from November 2003 to July 2004. Population abundance was low during the experiment (0–26 mice per site), and the summer rainfall was below average. We confirmed that mice used the supplementary food and water through a reduction in weight of food containers over time and for water through the presence of Rhodamine B in blood samples and positive bands in whiskers. Abundant food was also available through grain spilt on the ground after harvest of the wheat and barley crops. There was some evidence of increased breeding on sites where water was added, but no effect of food or food and water in combination. Sites where free water was available had marginally higher populations over summer (～2 more mice on average; P = 0.07). This difference was well below any biologically meaningful effect. Mice were 0.9 g heavier on sites where water was added (P = 0.04), and were in better condition (P = 0.03). The addition of high‐quality food did not affect mouse population dynamics, and the addition of water resulted in only marginal responses for some demographic characteristics. We conclude that other factors appear to be important for limiting mouse population growth in summer and autumn.     

Genetic structure of house mouse (Mus musculus Linnaeus 1758) populations in the Atlantic archipelago of the Azores: colonization and dispersal

We analyzed the genetic structure and relationships of house mouse (Mus musculus) populations in the remote Atlantic archipelago of the Azores using nuclear sequences and microsatellites. We typed Btk and Zfy2 to confirm that the subspecies Mus musculus domesticus was the predominant genome in the archipelago. Nineteen microsatellite loci (one per autosome) were typed in a total of 380 individuals from all nine Azorean islands, the neighbouring Madeiran archipelago (Madeira and Porto Santo islands), and mainland Portugal. Levels of heterozygosity were high on the islands, arguing against population bottlenecking. The Azorean house mouse populations were differentiated from the Portuguese and Madeiran populations and no evidence of recent migration between the three was obtained. Within the Azores, the Eastern, Western, and Central island groups tended to act as separate genetic units for house mice, with some exceptions. In particular, there was evidence of recent migration events among islands of the Central island group, whose populations were relatively undifferentiated. Santa Maria had genetically distinctive mice, which may relate to its colonization history. © 2013 The Linnean Society of London     

The frequency of multiple paternity suggests that sperm competition is common in house mice (Mus domesticus)

Sexual selection is an important force driving the evolution of morphological and genetic traits. To determine the importance of male-male, postcopulatory sexual selection in natural populations of house mice, we estimated the frequency of multiple paternity, defined as the frequency with which a pregnant female carried a litter fertilized by more than one male. By genotyping eight microsatellite markers from 1095 mice, we found evidence of multiple paternity from 33 of 143. Evidence for multiple paternity was especially strong for 29 of these litters. Multiple paternity was significantly more common in higher-density vs. lower-density populations. Any estimate of multiple paternity will be an underestimate of the frequency of multiple mating, defined as the frequency with which a female mates with more than a single male during a single oestrus cycle. We used computer simulations to estimate the frequency of multiple mating, incorporating observed reductions in heterozygosity and levels of allele sharing among mother and father. These simulations indicated that multiple mating is common, occurring in at least 20% of all oestrus cycles. The exact estimate depends on the competitive skew among males, a parameter for which we currently have no data from natural populations. This study suggests that sperm competition is an important aspect of postcopulatory sexual selection in house mice.     

The frequency of multiple paternity predicts variation in testes size among island populations of house mice

Polyandry generates selection on males through sperm competition, which has broad implications for the evolution of ejaculates and male reproductive anatomy. Comparative analyses across species and competitive mating trials within species have suggested that sperm competition can influence the evolution of testes size, sperm production and sperm form and function. Surprisingly, the intraspecific approach of comparing among population variation for investigating the selective potential of sperm competition has rarely been explored. We sampled seven island populations of house mice and determined the frequency of multiple paternity within each population. Applying the frequency of multiple paternity as an index of the risk of sperm competition, we looked for selective responses in male reproductive traits. We found that the risk of sperm competition predicted testes size across the seven island populations of house mice. However, variation in sperm traits was not explained by sperm competition risk. We discuss these findings in relation to sperm competition theory, and other intrinsic and extrinsic factors that might influence ejaculate quality.