Hybridization and gene flow in house mice introduced into an existing population on an island

Seventy-seven house mice ( Mus domesticus ) from the Orkney island of Eday were released on the Isle of May, Firth of Forth in April 1982. The May had a long-established mouse population, which was effectively homozygous at 71 allozymic loci scored; the Eday population had a heterozygosity at allozymic loci of 5% (80 loci scored) and was homozygous for three pairs of Robertsonian fusions. Introduced alleles at six loci expressed in blood were scored in animals trapped on the May at the beginning and end of the breeding season each year from 1982 to 1988. Hybrids between native and introduced animals were found in all parts of the island six months after the original release. All the introduced alleles survived and increased in frequency, albeit to different extents. There was no clear evidence of natural selection from differential survival of individuals or seasonal fluctuation of allele frequencies, but the change and apparent stabilization of frequencies after about three years (at different levels to both the parental Eday population and in the animals released) implies that some controlling factors must have acted.
These results were wholly unexpected. House mouse populations are divided into small demes, apparently with very restricted gene flow between them. The introduced mice on the May may have been successful because the native population had a low variability, but the latter had persisted successfully for over a century and certainly had a normal social structure. The spread of the Eday alleles to stability in the May population destroys the myth that population division inevitably restricts gene flow in house mice, and draws attention to the importance of coadaptation (or 'genetic architecture') in maintaining variation and affecting allele frequencies.     

Aneuploidy in metaphases II of spermatocytes of wild house mice from a hybrid zone between a Robertsonian population (CD: 2n = 22) and a population with the standard karyotype (2n = 40)

Meiotic metaphases II from archival slides were studied of male house mice caught in a hybrid zone between a population monomorphic for nine centric fusions (2n = 22) and a population with the standard karyotype (2n = 40), near Rome. The frequency of aneuploidy increases, up to 50%, with increasing number of heterozygous centric fusions (1–4). This revised version was published online in July 2006 with corrections to the Cover Date.     

Gene flow and hybridization following introduction of Mus domesticus into an established population

Seventy-seven house mice ( Mus domesticus ) from Eday, Orkney were released into a long-established population on the Isle of May (56^o 12'N) in 1982. Introduced allozymes, mt and Y-chromosome DNA, and Robertsonian chromosomes spread rapidly, reaching approximate stability c . 3 years later at frequencies different to those in both parental populations. The hybrid population was morphometrically intermediate between the two parents. This is a preliminary summary only; full details will be published elsewhere.     

New Robertsonian populations of the house mouse (Mus musculus domesticus) from north of the Alps]

New Robertsonian (Rb) populations of the house mouse (Mus musculus domesticus) carrying different combinations of centric fusions are reported in France, Switzerland, and Germany. In Alsace (France), the diploid number varied from 2n = 38 to 34; four fusions were present, with Rb(4.12) homozygous in all populations whereas Rb(5.10), Rb(5.7), or Rb(10.14) were found to be segregating. In Switzerland, only all-acrocentric mice (2n = 40) were present in Bern while Rb(5.7) and Rb(9.16) occurred in Basel. In the Konstanz locality from southern Germany, all the mice were homozygous for nine Rb fusions: Rb(1.18), Rb(2.5), Rb(3.6), Rb(4.12), Rb(7.15), Rb(8.17), Rb(9.14), Rb(10.11), and Rb(13.16). The phylogenetic relationship of these new Rb populations with those already known is discussed.     

Competition and extinction: the mice of Foula, with notes on those of Fair Isle and St Kilda

House mice ( Mus rnusculus muralis ) on St Kilda became extinct within about 18 months of the human population leaving the island in 1930. Although it was argued at the time that they died out because they were unable to find enough food, house mice flourish on a number of uninhabited islands and it seems more probable that they could not successfully compete with the Long-tailed field mouse ( Apodemus sylvaticus ) in the absence of man.
A study of the distribution and diet of both house and field mice on the Shetland islands of Foula and Fair Isle shows that the house mouse populations tend to be centred on human dwellings, although both species were found apparently living together on Foula away from habitation. The natural history of the two species is reviewed, and it is concluded that the breeding of the house mouse is the most probable characteristic to be upset by disturbance, and that the disappearance of man on St Kilda allowed Apodemus to enter a habitat previously occupied almost exclusively by Mus .     

High diversity of centric fusions with monobrachial homology in an area of chromosomal polymorphism of Mus musculus domesticus

One of the simplest models of chromosomal speciation is speciation by monobrachial centric fusion. This model is based on the assumption that a sterility barrier can develop between populations, in which fixed centric fusions show monobrachial homology, i.e. share only one chromosome arm. However, studies aimed at delineating intermediate stages of transition to reproductive isolation are lacking. In this paper, we describe a new area of chromosomal polymorphism in the house mouse, Mus musculus domesticus Schwarz and Schwarx, 1943, in Sicily (Italy). We trapped 79 mice at eighteen localities in an area of approximately 500 Km² surrounding the largest active European volcano, Mount Etna. Combining G‐banding and chromosome painting we identified twelve different Robertsonian (Rb) metacentrics. Considering the high number of Rb fusions, some of them shared with other documented areas, the presently studied area of chromosomal polymorphism is very likely to represent a mixture of allochthonous and autochthonous Rb fusions. The Rb(9.16) is the most widespread metacentric (overall frequency 0.80). Two Rb metacentrics, Rb(4.10) and Rb(5.6), have similar overall frequency, 0.29 and 0.37, respectively, and are narrowly co‐distributed in ten populations. Nine fusions – Rb(2.13), Rb(1.3), Rb(12.17), Rb(8.17), Rb(2.14), Rb(10.14), Rb(11.17), Rb(3.15), and Rb(11.14) – show a low frequency (0.04–0.01) and mostly non‐overlapping localization, but each of them shares monobrachial homology with at least one other metacentric. The overall geographical distribution of different Rb fusions seems to match an early stage of race formation. The eventual role of the presently studied hybrid zone in the context of chromosomal speciation by monobrachial centric fusions is discussed. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 103 , 722–731.     

Genic differentiation and origin of Robertsonian populations of the house mouse (Mus musculus domesticus Rutty)

This paper examines the relation between chromosomal and nuclear-gene divergence in 28 wild populations of the house mouse semi-species, Mus musculus domesticus, in Western Europe and North Africa. Besides describing the karyotypes of 15 of these populations and comparing them to those of 13 populations for which such information was already known, it reports the results of an electrophoretic survey of proteins encoded by 34 nuclear loci in all 28 populations. Karyotypic variation in this taxon involves only centric (or Robertsonian) fusions which often differ in arm combination and number between chromosomal races. The electrophoretic analysis showed that the amount of genic variation within Robertsonian (Rb) populations was similar to that for all-acrocentric populations, i.e. bearing the standard karyotype. Moreover, divergence between the two types of populations was extremely low. These results imply that centric fusions in mice have not modified either the level or the nature of genic variability. The genetic similarity between Rb and all-acrocentric populations is not attributed to the persistence of gene flow, since multiple fusions cause marked reproductive isolation. Rather, we attribute this extreme similarity to the very recent origin of chromosomal races in Europe. Furthermore, genic diversity measures suggest that geographically separated Rb populations have in situ and independent origins. Thus, Rb translocations are probably not unique events, but originated repeatedly. Two models are presented to explain how the rapid fixation of a series of chromosomal rearrangements can occur in a population without lowering variability in the nuclear genes. The first model assumes that chromosomal mutation rates are between 10(-3) and 10(-4) and that populations underwent a series of transient bottlenecks in which the effective population size did not fall below 35. In the second model, genic variability is restored following severe bottlenecks, through gene flow and recombination.     

Sex chromosome aneuploidy in wild small mammals

We describe four examples of the XO condition in wild mammals. One XO house mouse (Mus musculus domesticus) was caught in nature and subsequently gave birth to three litters in captivity, confirming for wild mice the fertility observed for XO laboratory mice. Two other XO house mice were produced from laboratory crosses of wild-caught mice. An immature XO common shrew (Sorex araneus) was caught in nature; this appears to be the first XO recorded in the order Insectivora. We collected data from researchers studying chromosome variation in house mice and common shrews and found an overall incidence of 0.22% sex chromosome aneuploidy in 4608 mice and 0.05% in 6625 shrews. The discrepancy related to a much higher frequency of XO's in mice than shrews. Single XXY and XYY shrews and an XXX mouse have been recorded in nature.     

Episodic chromosomal evolution in Planipapillus (Onychophora: Peripatopsidae): a phylogenetic approach to evolutionary dynamics and speciation

Planipapillus, a clade of onychophorans from southeastern Australia, exhibits substantial chromosomal variation. In the context of a robust phylogeny based on nuclear and mitochondrial sequence data, we evaluate models of chromosomal evolution and speciation that differ in the roles assigned to selection, mutation, and drift. Permutation tests suggest that all chromosome rearrangements in the clade have been centric fusions and, on the basis of parsimony and maximum-likelihood methods with independent estimates of branch lengths, we conclude that at least 31 centric fusions have been fixed in Planipapillus. A likelihood-ratio test approach, which is independent of our point estimates of ancestral states, rejects an evolutionary model in which the mutation rate is constant and centric fusions are effectively neutral. In contrast to the nucleotide sequence data, which are consistent with neutrality and rate constancy, centric fusions in Planipapillus are underdominant, spontaneous fusion rates vary among lineages, or both. We predict an inverse relationship between rates of chromosomal evolution and historical population size. Chromosomal evolution may play a role in speciation in Planipapillus, both by interactions between centric fusions with monobrachial homology and by the accumulation of multiple weakly underdominant fusions.     

Telomeres and mechanisms of Robertsonian fusion

The Robertsonian (Rb) fusion, a chromosome rearrangement involving centric fusion of two acro-(telo)centric chromosomes to form a single metacentric, is one of the most frequent events in mammalian karyotype evolution. Since one of the functions of telomeres is to preserve chromosome integrity, a prerequisite for the formation of Rb fusions should be either telomere loss or telomere inactivation. Possible mechanisms underlying the formation of various types of Rb fusion are discussed here. For example, Rb fusion in wild mice involves complete loss of p-arm telomeres by chromosome breakage within minor satellite sequences. By contrast, interstitial telomeric sites are found in the pericentromeric regions of chromosomes originating from a number of vertebrate species, suggesting the occurrence of Rb-like fusion without loss of telomeres, a possibility consistent with some form of telomere inactivation. Finally, a recent study suggests that telomere shortening induced by the deletion of the telomerase RNA gene in the mouse germ-line leads to telomere loss and high frequencies of Rb fusion in mouse somatic cells. Thus, at least three mechanisms in mammalian cells lead to the formation of Rb fusions. Received: 11 November 1997 / Accepted: 21 December 1997     

Prevalence of mouse mammary tumor virus (MMTV) in wild house mice (Mus musculis) in southeastern Australia

We determined the prevalence of mouse mammary tumor virus (MMTV) in introduced, free-roaming, wild house mice (Mus musculus domesticus) [corrected] and compared envelope (env) and long terminal repeat (LTR) nucleotide sequences of viruses from wild mice and other sources. Mice were trapped on two occasions, in October (spring) and the following May (autumn) of 2003-2004 in the Mallee region of northwestern Victoria, Australia. Animals were assigned to three cohorts (subadult, young, and old adults) based on their body length. The DNA from salivary glands (62 of 62 mice) and mammary glands (19 of 32 female mice) was screened for the MMTV envelope (env) gene, and the long terminal repeat (LTR) region including the superantigen (SAg) sequence was amplified from a subset. Positive polymerase chain reaction (PCR) results for the MMTV env PCR were detected from salivary gland tissues from 60 of 62 (97%) mice and from mammary gland tissues from 19 of 19 (100%) female mice. All but two mice were positive for MMTV env across both sexes and the three cohorts. Similarity of the SAg carboxy-terminal nucleotide sequence between free-roaming wild house mice varied from 64% to 99%, although most of this variation was due to DNA sequences from two mice (M4 and M5). Phylogenetic analysis of the LTR region did not result in distinct grouping of sequences derived from mice when comparisons were made among sequences from mice in the US, Europe, and Australia, and MMTV-like virus (MMTV-LV) env sequences derived from human hosts. We report a high prevalence of the MMTV env sequence during a sampling period when peak mouse density was low. This indicates that MMTV is an enzootic virus in a population of wild, free-ranging mice in northwestern Victoria, in Australia. Phylogenetic analysis, based upon env and LTR sequence data, indicated minor variation among all isolates. This represents the first report on the prevalence of MMTV in mouse populations in Australia.     

Evidence for eight tandem and five centric fusions in the evolution of the karyotype ofAethomys namaquensis A. Smith (Rodentia: Muridae)

G- and C-banded chromosomes ofAethomys namaquensis (2n=24),A. chrysophilus (2n=44), andPraomys coucha (2n=36) are compared and contrasted with publised material on Australian Muridae and North American Sigmodontidae. Direction and types of chromosomal rearrangements are established using cladistic methodology. An acrocentric morphology for chromosomes 5, 14, 15 and 20 (numbering system fromPeromyscus) are proposed as primitive for the common ancestor of the Muridae and Sigmodontidae rodent lineages. Reduced diploid number ofAethomys namaquensis is derived by eight tandem and five centric fusions since divergence from the common ancestor withA. chrysophilus. The two species ofAethomys share one derived metacentric chromosome that distinguishes them fromPraomys. Praomys has unique chromosomes which can be derived from the proposed primitive condition by five centric fusions and five pericentric inversions. It is concluded that karyotypic orthoselection for tandem and centric fusions is best explained by cellular or biochemical mechanisms rather than variation in population characteristics.     

Evolution of the chromosomal races of Mus musculus domesticus in the Rhaetian Alps: the roles of whole-arm reciprocal translocation and zonal raciation

The evolution of ten Robertsonian (Rb) races of the house mouse (Mus musculus domesticus) in the Rhaetian Alps of northern Italy and southern Switzerland is reconsidered. The mechanisms of centric fusion, zonal raciation and, for the first time, whole-arm reciprocal translocation (WART), are used in this non-mathematical approach to produce a phylogenetic tree (using chromosome fusions as characters) with the smallest number of steps. The shortest tree that we found (16 steps) is at least two to nine mutations shorter than previously published models. Three other trees (17 or 18 steps) are also considered, since they are geographically more sensible. In general, these four scenarios correspond more closely to the present distributions of the ten Rb races than previous trees. Our results suggest that zonal raciation and WARTs play an important role in the evolution of Rb races of the house mouse.     

Cytogenetics and reproduction of sheep with multiple centric fusions (Robertsonian translocations)

The significance of centric fusions (Robertsonian translocations) in domestic animals, with special reference to sheep, is reviewed. The mating is described of a further 856 ewes with either a normal chromosome number 2n = 54 or carrying one or more of the three different translocations (centric fusions) t1, t2 and t3 in various heterozygous and homozygous arrangements. Rams which were used in the matings were homozygous for one of the translocation chromosomes (2n = 52), double heterozygotes (2n = 52), triple heterozygotes (2n = 51) or were carriers of 4 translocation chromosomes (2n = 50) and 5 translocation chromosomes (2n = 49). A remarkably even distribution of segregation products was recorded in the progeny of all combinations of translocation ewes x translocation rams in those groups in which sufficient animals were available for statistical analysis. Forty-eight chromosomally different groups of animals were mated. Further, the overall fertility of the translocation sheep, measured by conception rate to first service, lambing percentage and number of ewes which did not breed a lamb, was not significantly different from New Zealand national sheep breeding data. In some groups the poorer reproductive performance could be explained by the age structure of the flock and inbreeding depression, which probably affected the performance of some animals. Sheep with progressively decreasing chromosome numbers, due to centric fusion, 2n = 50, 2n = 49 and 2n = 48, are reported. The 2n = 48 category represents a triple homozygous ewe and a triple homozygous ram and is the first report of the viable evolution of such domestic animals. Less than 1% of phenotypically abnormal lambs were recorded in a total of 1995 progeny born over 10 years. It is now considered that there is little or no evidence to suggest that centric fusions in a variety of combinations affect the total productive fitness of domestic sheep. It is suggested that future research should be more actively directed to understanding their genetic significance.     

Increase in frequency of the bridled morph of the Common Guillemot Uria aalge on the Isle of May, 1946–2000: a return to former levels?

Bridling in the Common Guillemot Uria aalge is a classic example of a stable ratio-cline polymorphism. Between 1946 and 2000 the frequency of the bridled morph of the Common Guillemot colony on the Isle of May, south-east Scotland, increased significantly from 3.5% to 5.9%. Demographic data collected between 1982 and 2000 indicated that the average breeding success of a pair including at least one bridled bird was 83.8%, significantly greater than 79.5% in unbridled pairs. Over the same period the average overwinter survival was 96.3% for bridled birds and 94.7% for unbridled birds, but the difference was not statistically significant. A population model showed that the increase in frequency of bridling could be accounted for as a return to an equilibrium level close to the 5.04% observed in 1936. Differences in breeding success contributed relatively little to the increase, which could be explained without recourse to differential selection pressure. The latitudinal variation in bridling suggests that bridled morphs are more cold tolerant than unbridled ones. However, the increase in the frequency of bridled birds on the Isle of May was not associated with any decrease in sea or air temperatures over the period.     

Survival and non-breeding of adult Common Guillemots Una aalge

Annual survival of colour-ringed Common Guillemots Uria aalge with at least 1 year of breeding experience was measured in five study areas on the Isle of May, southeast Scotland from 1982 to 1993. Annual survival averaged 94.9%. There were no significant sex, year or area differences. Between 5% and 10% of the birds known to be alive in any year did not breed, and on average such birds appeared to survive less well (87%) than breeders (95%). Non-breeding did not occur randomly within the population, and 6% of birds accounted for 47% of the cases of non-breeding. It appeared that non-breeding in Common Guillemots on the Isle of May was socially induced with most cases occurring after an individual had lost its site.     

Survival of adult Common Guillemots Uria aalge at three Scottish colonies

We present the results of a mark–recapture analysis of survival rates of Common Guillemots with at least one year's breeding experience for birds from three Scottish colonies. Estimates of overall survival of adults from the Isle of May (North Sea), Canna and Colonsay (both off northwest Scotland) from an analysis combining data from the three colonies were 94.8% (se = ±0.6), 92.4% (se = ±0.9) and 96.7% (se = ±0.6) respectively. The rates from Canna (but not Colonsay) differed significantly from those of guillemots on the Isle of May. The Canna and Colonsay figures are the first survival estimates for guillemots in northwest Scotland, an area of high conservation concern for this species. Low input, long-term studies of seabirds can produce important data on adult survival.     

Intercolony movement and behaviour of immature Guillemots Uria aalge

A minimum of 61 Guillemots Uria aalge ringed as chicks at other colonies was recorded at the Isle of May between 1987 and 1991 (four prior to 1990, six in 1990, 51 in 1991). Two were adults and 59 were immatures. Most of the British and Irish colonies where many chicks had been ringed were represented. Higher proportions of birds ringed at colonies relatively close to the Isle of May were observed compared to birds ringed at more distant sites. Visitors ranged in age from 2 to 5 years, with single 10- and 14-year-olds. Relatively fewer 2- and 5- than 3- and 4-year-old birds were seen. Visiting birds were usually recorded once only, significantly less often than native immatures of the same age, except for 2-year-olds. The proportion of birds occupying sites on intertidal rocks as against sites in the colony appeared to be higher compared with native birds of the same age. Visiting birds formed a substantial proportion of the immature population. Ten immature birds from the Isle of May were recorded elsewhere. Four of these had been seen on the Isle of May previously, and four were seen there subsequently. A 6-year-old hatched at Sumburgh ( c. 420 km by sea) bred at the Isle of May in 1992.     

Tandem and centric fusions in the chromosomal evolution of the South American phyllotines of the genus Auliscomys (Rodentia, cricetidae).

The karyotypes of three of the four extant species of the genus Auliscomys (A. micropus, living in central [2n = 32, NF = 34] and southern [2n = 34, NF = 36, 37] Chile; A. sublimis [2n = 28, NF = 32] and A. boliviensis [2n = 22, NF = 32], which inhabit the Andean Altiplano) were analyzed. Comparisons of G-, C-, and AgNOR-banded karyotypes showed that extensive conservation of entire chromosomes and chromosomal regions had occurred during the evolution of this genus, with centromeretelomere tandem fusions and centric fusions probably being the most frequent chromosome changes. A chromosomal phylogeny, based on the chromosome homoeologies detected and parsimonious analysis of the nature and distribution of the inferred chromosomal changes, is proposed. This hypothetical phylogeny assumes that the ancestral telocentric karyotype would have undergone three consecutive tandem fusions, first originating the 2n = 32 (NF = 34) karyomorph exhibited by present-day specimens of A. micropus captured in central Chile and then the 2n = 28 (NF = 32) karyotype of A. sublimis. Subsequent centric fusions involving the tandem-fusion products would presumably have generated the 2n = 22 (NF = 32) A. boliviensis karyotype. Assuming some conditions related to early geographic distribution, this chromosomal phylogeny is in agreement with a paleogeographic model, which explains the present distribution of living Auliscomys species mainly on the basis of geologic and climatic events.(ABSTRACT TRUNCATED AT 250 WORDS)     

Introduced house mice as a conservation concern on Gough Island

House mice have previously been identified as a significant threat to both species and ecosystems on Southern Ocean islands. To date, these impacts have been quantified on several sub-Antarctic islands, but the role of house mice on more temperate islands is poorly known. On South Atlantic Gough Island, non-commensal house mice (Mus musculus L.) were probably introduced in the early 19th century and are now extremely abundant. To assess the likely impacts of mice on the fauna and flora at Gough Island we examined the diet of this population from September 1999 to July 2000 using conventional snap trapping techniques. The population has a single breeding season from September to March and mean body mass is notable in being amongst the largest reported for non-laboratory M. musculus. At low elevations (<250 m above sea level [a.s.l.]), avian carrion was the most prevalent dietary item during September and October. From November to February, plant material constituted the bulk of stomach contents and from March to July lumbricid worms were the most common food item. Indigenous invertebrate matter contributed little to mouse diet, independent of season. At altitudes greater than 500 m a.s.l., larvae of endemic brachypterous moths made up a significant proportion of stomach contents. In light of studies elsewhere, these data suggest that mouse predation may pose a significant threat to these species. However, it is not clear whether conservation action, such as an eradication attempt, is warranted. Further assessments of the impacts of mice are required, and in the interim every effort should be made to prevent introductions of other potentially harmful invasive species.