One hundred years of eruptions of house mice in Australia – a natural biological curio

The house mouse has adapted well to the cereal crops of south-eastern Australia where populations show aperiodic outbreaks over large areas. A 20-year population study has provided a wealth of information on breeding ecology, demographic changes, spatial behaviour and epidemiology. The breeding season can be as short as 4.5 months and as long as 10 months with litter size changing seasonally from high values in spring to low values in autumn. There are marked changes in litter size between years. Rates of increase of populations also vary between years. The rate of change of populations during the breeding season is independent of density effects, but if the population density is high at the commencement of breeding then the litter size is depressed throughout that breeding season. There are density-dependent effects on survival during the non-breeding season. Rates of increase of populations over spring and summer are highly correlated with accumulated rainfall from the previous winter–spring (April–October). Studies of helminths and viruses indicate that Australian mice carry only a subset of the helminths found in Europe. There have been no published studies on murine viruses in Europe. Perhaps a reduced diversity of diseases partially accounts for the ability of mice to increase rapidly to extreme population densities in cereal-growing areas of south-eastern Australia.  © 2005 CSIRO, Biological Journal of the Linnean Society , 2005, 84 , 617–627.     

Is reproduction of the Australian house mouse (<Emphasis Type="Italic">Mus domesticus</Emphasis>) constrained by food? A large-scale field experiment

Food quantity and especially food quality are thought to be key factors driving reproductive changes in the house mouse, Mus domesticus, leading to outbreaks of house mouse populations in the Australian grain-growing region. Characteristic changes during an incipient mouse plague are an early start of breeding, a high proportion of females breeding at a young age and a prolonged breeding season. We conducted a large-scale food manipulation during an incipient mouse plague, which started with early breeding and relatively high spring numbers of mice. We measured background food availability in four farms throughout the study and conducted a food manipulation experiment from November to March in two of them. After harvest in December 100-200 kg/ha spilled grain remained in the stubble. This was depleted by March. In two treatment farms we added high-protein food pellets on a weekly basis between November and March and two farms served as controls. We measured changes in mouse numbers by capture-mark-recapture trappings and changes in reproduction by scoring embryos and recent placental scars at necropsy. Mouse numbers did not differ between treatments and controls. There were no differences in the litter size or the proportion of females breeding between treatments and controls. We observed the normal pattern of high litter size in spring and decreasing litter size towards the end of summer in treatments and controls. In all farms reproduction stopped in March. Mouse numbers were high but not at plague densities. Contrary to our prediction we did not observe food constraint affecting the reproduction of female mice. Our field experiment seems to rule out food quality as the driving factor for improved reproduction and formation of an outbreak of mice. We suggest that physiological mechanisms in mice might not enable them to take advantage of food with a high protein content in arid summers in southeastern Australian grain fields because of the lack of free-standing water.     

Reproductive changes in fluctuating house mouse populations in southeastern Australia

House mice (Mus domesticus) in the Victorian mallee region of southeastern Australia show irregular outbreaks. Changes in reproductive output that could potentially drive changes in mouse numbers were assessed from 1982 to 2000. Litter size in females is positively correlated with body size. When standardized to an average size female, litter size changes seasonally from highest in spring to lowest in autumn and winter. Litter size is depressed throughout breeding seasons that begin when the abundance of mice is high, but is similar in breeding seasons over which the abundance of mice increases rapidly or remains low. Breeding begins early and is extended on average by about five weeks during seasons when mouse abundance increases rapidly. The size at which females begin to reproduce is larger during breeding seasons that begin when mouse abundance is high. An extended breeding season that begins early in spring is necessary for the generation of a house mouse plague, but it is not in itself sufficient. Reproductive changes in outbreaks of house mice in Australia are similar but not identical to reproductive changes that accompany rodent population increases in the Northern Hemisphere. We conclude that food quality, particularly protein, is a probable mechanism driving these reproductive changes, but experimental evidence for field populations is conflicting.     

Population dynamics of an outbreak of house mice (Mus domesticus) in the mallee wheatlands of Australia—hypothesis of plague formation

A plague of mice ( Mus domesticus ) in the Victorian mallee wheatlands of south-eastern Australia in autumn 1984 appeared to be generated by a sequence of rainfall events: high autumn (March), mid winter and late winter rainfall in 1983, and high summer rainfall in 1983/84. The March rainfall in 1983 ended a drought; mice began to breed and bred until the end of May. Relatively high survival of mice for 12 months after March 1983, together with early onset of breeding and high reproductive performance throughout the 1983/84 breeding season, including summer, were key demographic processes during the formation of the plague. Temporal differences in mouse abundance and breeding performance between habitats highlighted the relevance of specific habitats to the dynamics of mouse populations in the wheatlands. Fencelines were the most important habitat of mice because they were foci for breeding at the start of the breeding season, good nesting sites which were rarely disturbed, and widespread and in close proximity to crops. Cereal crops were colonized in spring 1983 and in autumn 1984; they became important habitats in 1983 when mice dispersed and bred there in early spring. Redhead's (1988) model was sufficient to explain the 1984 plague, but not the magnitude of the decline of mouse numbers in 1984, nor the absence of a further outbreak in 1985. A new model is proposed based on a sequence of rainfall events beginning at least 10 months prior to a plague.     

Pathogens of house mice on arid Boullanger Island and subantarctic Macquarie Island, Australia

Studies on island populations of house mice (Mus domesticus) and their viruses reveal insights into viral persistence in isolated communities. We surveyed the ectoparasites, endoparasites, and antiviral antibodies for 11 murine viruses and two bacteria of house mice inhabiting two islands off Australia. House mice on Boullanger Island were seropositive to two viruses, murine cytomegalovirus and epizootic diarrhea of infant mice. On subantarctic Macquarie Island, house mice were seropositive for five viruses: murine cytomegalovirus, lymphocytic choriomeningitis virus, mouse parvovirus, epizootic diarrhea of infant mice, and Theiler's murine encephalomyelitis virus. The diversity of antiviral antibodies was lower among populations of house mice on islands than those inhabiting mainland Australia. The decreased diversity of viruses in island populations of house mice may be a function of which agent the founder mice transfer to the island and related to the low densities which the host population may periodically reach over time.     

Preventing desert locust plagues: optimizing management interventions

Solitarious desert locusts, Schistocerca gregaria (Forskål) (Orthoptera: Acrididae), inhabit the central, arid, and semi‐arid parts of the species’ invasion area in Africa, the Middle East, and South‐West Asia. Their annual migration circuit takes them downwind to breed sequentially where winter, spring, and summer rains fall. In many years, sparse and erratic seasonal rains support phase change and local outbreaks at only a few sites. Less frequently, seasonal rains are widespread, frequent, heavy, and long lasting, and many contemporaneous outbreaks occur. When such seasonal rains fall sequentially, populations develop into an upsurge and eventually into a plague unless checked by drought, migration to hostile habitats, or effective control. Increases in the proportion of gregarious populations as the plague develops alter the effectiveness of control. As an upsurge starts, only a minority of locusts is aggregated into treatable targets and spraying them leaves sufficient unsprayed individuals to continue the upsurge. Spraying all individuals scattered within an entire infested zone is arguably both financially and environmentally unacceptable. More of the population gregarizes and forms sprayable targets after each successive season of good rains and successful breeding. Eventually, unless the rains fail, the entire upsurge population becomes aggregated at high densities so that the infested area diminishes and a plague begins. These populations must continue to increase numerically and spread geographically to achieve peak plague levels, a stage last reached in the 1950s. Effective control, aided by poor rains, accompanied each subsequent late upsurge and early plague stage and all declined rapidly. The control strategy aims to reduce populations to prevent plagues and damage to crops and grazing. Differing opinions on the optimum stage to interrupt pre‐plague breeding sequences are reviewed.     

Population ecology of Mus musculus on Mana Island, New Zealand

Feral house mice ( Mus musculus ) living on 217 ha Mana Island, New Zealand, with no mammalian predators, were snap-trapped and autopsied. A 7-month breeding season took the population from a spring low to extremely high density in autumn. Litters were largest in the middle of the breeding season, and significantly larger on Mana than on the New Zealand mainland. Litter size in early pregnancy was similar for young and old mice but more embryos were resorbed by old females. The breeding season ended in April when adult females stopped ovulating and young failed to mature. When the population declined over winter no animals bred, they all lost weight, and even previously mature males lost their reproductive ability. Mice continue to grow throughout life and become larger than mice in most populations on the New Zealand mainland. The regular and pronounced seasonal pulse in Mana's mouse population contrasts with longer-term fluctuations generally seen in mainland populations at lower density in indigenous forest. These differences may be explained by absence of predators, habitat features or lack of any chance to disperse on the island.     

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.     

Assessment of genetic diversity and population structure in cultured Australian Pacific oysters

The recent development of Pacific oyster (Crassostrea gigas) SNP genotyping arrays has allowed detailed characterisation of genetic diversity and population structure within and between oyster populations. It also raises the potential of harnessing genomic selection for genetic improvement in oyster breeding programmes. The aim of this study was to characterise a breeding population of Australian oysters through genotyping and analysis of 18 027 SNPs, followed by comparison with genotypes of oyster sampled from Europe and Asia. This revealed that the Australian populations had similar population diversity (H_E) to oysters from New Zealand, the British Isles, France and Japan. Population divergence was assessed using PCA of genetic distance and revealed that Australian oysters were distinct from all other populations tested. Australian Pacific oysters originate from planned introductions sourced from three Japanese populations. Approximately 95% of these introductions were from geographically, and potentially genetically, distinct populations from the Nagasaki oysters assessed in this study. Finally, in preparation for the application of genomic selection in oyster breeding programmes, the strength of LD was evaluated and subsets of loci were tested for their ability to accurately infer relationships. Weak LD was observed on average; however, SNP subsets were shown to accurately reconstitute a genomic relationship matrix constructed using all loci. This suggests that low‐density SNP panels may have utility in the Australian population tested, and the findings represent an important first step towards the design and implementation of genomic approaches for applied breeding in Pacific oysters.     

A rapid population expansion retains genetic diversity within European rabbits in Australia

The well documented historical translocations of the European rabbit (Oryctolagus cuniculus) offer an excellent framework to test the genetic effects of reductions in effective population size. It has been proposed that rabbits went through an initial bottleneck at the time of their establishment in Australia, as well as multiple founder events during the rabbit's colonization process. To test these hypotheses, genetic variation at seven microsatellite loci was measured in 252 wild rabbits from five populations across Australia. These populations were compared to each other and to data from Europe. No evidence of a genetic bottleneck was observed with the movement of 13 rabbits from Europe to Australia when compared to French data. Within Australia the distribution of genetic diversity did not reflect the suggested pattern of sequential founder effects. In fact, the current pattern of genetic variation in Australia is most likely a result of multiple factors including mutation, genetic drift and geographical differentiation. The absence of reduced genetic diversity is almost certainly a result of the rabbit's rapid population expansion at the time of establishment in Australia. These results highlight the importance of population growth following a demographic bottleneck, which largely determines the severity of genetic loss.     

Are recession populations of the desert locust (Schistocerca gregaria) remnants of past swarms?

The desert locust (Schistocerca gregaria) undergoes crowding-induced phase transformation from solitary to gregarious, which involves changes in behaviour, colour, development, morphometry, fecundity and endocrine physiology. During recession, solitary locusts persist in the central, drier part of the species' range in small pocket populations that are prone to extinction. During the intermittent upsurges and the subsequent plagues, gregarious swarms attain huge population size and invade a vast area causing major damage to agriculture. A highly variable nuclear DNA marker, a noncoding 3' end fragment of an antennapedia-class homeobox gene, was screened in locust samples from Eritrea. Despite the homogenizing potential of plague swarms, the last of which was in 1986-89 and originated in this region, the population genetic structure of solitary phase locusts along the Red Sea coast of Eritrea revealed significant divergence. The pattern of divergence indicated that the invasion of the western and northern plains in the summer of 1995 may not, as reported then, have originated in eastern Chad or western Sudan. A number of interrelated hypotheses have been presented to explain the observed genetic heterogeneity between the sampled populations. We conclude, with caution due to the limited sample sizes, that: (i) geographical isolation between breeding sites during plagues and recession; (ii) the marked differences in the flight behaviour of plague swarms and recession populations; (iii) possible failure of gregarious locusts to solitarize and re-establish in recession areas; and (iv) the effect of repeated extinction and recolonization in the meta-population contribute to the maintenance of the genetic structure of recession populations. Potentially productive future research has been identified.     

Invasion success and genetic diversity of introduced populations of guppies Poecilia reticulata in Australia

High genetic diversity is thought to characterize successful invasive species, as the potential to adapt to new environments is enhanced and inbreeding is reduced. In the last century, guppies, Poecilia reticulata, repeatedly invaded streams in Australia and elsewhere. Quantitative genetic studies of one Australian guppy population have demonstrated high additive genetic variation for autosomal and Y-linked morphological traits. The combination of colonization success, high heritability of morphological traits, and the possibility of multiple introductions to Australia raised the prediction that neutral genetic diversity is high in introduced populations of guppies. In this study we examine genetic diversity at nine microsatellite and one mitochondrial locus for seven Australian populations. We used mtDNA haplotypes from the natural range of guppies and from domesticated varieties to identify source populations. There were a minimum of two introductions, but there was no haplotype diversity within Australian populations, suggesting a founder effect. This was supported by microsatellite markers, as allelic diversity and heterozygosity were severely reduced compared to one wild source population, and evidence of recent bottlenecks was found. Between Australian populations little differentiation of microsatellite allele frequencies was detected, suggesting that population admixture has occurred historically, perhaps due to male-biased gene flow followed by bottlenecks. Thus success of invasion of Australia and high additive genetic variance in Australian guppies are not associated with high levels of diversity at molecular loci. This finding is consistent with the release of additive genetic variation by dominance and epistasis following inbreeding, and with disruptive and negative frequency-dependent selection on fitness traits.     

Demographic history of a recent invasion of house mice on the isolated Island of Gough

Island populations provide natural laboratories for studying key contributors to evolutionary change, including natural selection, population size and the colonization of new environments. The demographic histories of island populations can be reconstructed from patterns of genetic diversity. House mice (Mus musculus) inhabit islands throughout the globe, making them an attractive system for studying island colonization from a genetic perspective. Gough Island, in the central South Atlantic Ocean, is one of the remotest islands in the world. House mice were introduced to Gough Island by sealers during the 19th century and display unusual phenotypes, including exceptionally large body size and carnivorous feeding behaviour. We describe genetic variation in Gough Island mice using mitochondrial sequences, nuclear sequences and microsatellites. Phylogenetic analysis of mitochondrial sequences suggested that Gough Island mice belong to Mus musculus domesticus, with the maternal lineage possibly originating in England or France. Cluster analyses of microsatellites revealed genetic membership for Gough Island mice in multiple coastal populations in Western Europe, suggesting admixed ancestry. Gough Island mice showed substantial reductions in mitochondrial and nuclear sequence variation and weak reductions in microsatellite diversity compared with Western European populations, consistent with a population bottleneck. Approximate Bayesian computation (ABC) estimated that mice recently colonized Gough Island (~100 years ago) and experienced a 98% reduction in population size followed by a rapid expansion. Our results indicate that the unusual phenotypes of Gough Island mice evolved rapidly, positioning these mice as useful models for understanding rapid phenotypic evolution.     

Genetic differentiation between Australian and North American populations of the monarch butterfly Danaus plexippus (L.) (Lepidoptera: Nymphalidae): an exploration using allozyme electrophoresis

Allozyme analysis was used to address the question of the source of the Australian populations of the monarch butterfly Danaus plexippus (L.). The study had three major aims: (1) To compare the levels of diversity of Australian and Hawaiian populations with potential source populations. (2) To determine whether eastern and western North American populations were sufficiently divergent for the Australian populations to be aligned to a source population. (3) To compare the differentiation among regions in Australia and North America to test the prediction of greater genetic structure in Australia, as a consequence of reduced migratory behaviour. The reverse was found, with F _ST values an order of magnitude lower in Australia than in North America. Predictably, Australian and Hawaiian populations had lower allelic diversity, but unexpected higher heterozygosity values than North American populations. It was not possible to assign the Australian populations to a definitive source, although the high levels of similarity of Australian populations to each other suggest a single colonization event. The possibility that the Australian populations have not been here long enough to reach equilibrium is discussed. © 2002 The Linnean Society of London, Biological Journal of the Linnean Society , 2002, 75 , 437–452.     

Breeding program for the lesser kudu (Tragelaphus imberbis) in North America

The lesser kudu (Tragelaphus imberbis) has been kept in North American zoological parks since 1930 but has never been a common species in collections. In 1987 this population totaled 28 animals: 15 males and 13 females. A pedigree evaluation in 1987 of the existing population indicated that eight effective founders and one potential founder were represented in the North American herd. Three new potential founders from European captive populations were added to the population in 1987 to increase the number of existing founder lines to 12 animals. As this species is not endangered or threatened in its native habitat, it is not a high priority to qualify for designation as an SSP species. Because of this, the institutions holding lesser kudu in North America decided to join informally and draft a breeding program to better manage this small captive population. This program was designed to minimize inbreeding and equalize genetic representation of founder animals to maximize genetic diversity. It requires a shift in management philosophy to establish stable groups of breeding females at participating institutions while rotating appropriate breeder males through these herds in a controlled manner to ensure minimization of inbreeding and maximization of genetic diversity. It is hoped that this program can serve as a model for the management of other small captive populations of non-SSP species.     

Microsatellite loci confirm a lack of population connectivity among globally distributed populations of the tope shark Galeorhinus galeus (Triakidae)

This study used 11 polymorphic nuclear microsatellite loci to determine the population connectivity of five geographically isolated populations of tope shark Galeorhinus galeus (Africa, Australia, North America, South America and western Europe). Genetic analyses revealed significant structure among all populations indicating a lack of population connectivity. These findings indicate that globally distributed populations of G. galeus are isolated and should be managed as distinct, independent stocks.     

High regional differentiation in a North American crab species throughout its native range and invaded European waters: a phylogeographic analysis

Rhithropanopeus harrisii (Gould 1841) has a native distribution from New Brunswick (Canada) to Veracruz (Mexico) and is considered an invasive species in northwestern North American (Oregon and California), South American (Brazil) and European estuaries and rivers. In Europe, it was observed for the first time in 1874, in The Netherlands. We sequenced and analyzed part of the cytochrome oxidase subunit I gene (mitochondrial DNA) of eight populations, three from the east coast of the United States of America (USA) and five from Europe, in order to assess their genetic diversity and to determine a potential founder population. European populations are characterized by a lower number of haplotypes than the whole native region of the eastern USA, suggesting that genetic bottlenecks occurred during the European colonisation. Along the North American East Coast, there is evidence of clearcut genetic heterogeneity, New Jersey being the most similar population in its genetic structure to the postulated Europe-founding population. Also the different European populations are heterogeneous and there is a tendency of higher genetic diversity in the populations founded earlier. R. harrisii is still in the process of expansion in Europe and may have been introduced once or repeatedly by different invasion mechanisms. The pronounced lack of gene flow among populations is of great ecological significance, since it may facilitate rapid adaptation and specialization to local conditions within single estuarine systems.     

Microsatellite DNA analysis of northern pike (Esox lucius L.) populations: insights into the genetic structure and demographic history of a genetically depauperate species

The northern pike Esox lucius L. is a freshwater fish exhibiting pronounced population subdivision and low genetic variability. However, there is limited knowledge on phylogeographical patterns within the species, and it is not known whether the low genetic variability reflects primarily current low effective population sizes or historical bottlenecks. We analysed six microsatellite loci in ten populations from Europe and North America. Genetic variation was low, with the average number of alleles within populations ranging from 2.3 to 4.0 per locus. Genetic differentiation among populations was high (overall θ_ST = 0.51; overall ρ_ST = 0.50). Multidimensional scaling analysis of genetic distances between populations and spatial analysis of molecular variance suggested a single phylogeographical race within the sampled populations from northern Europe, whereas North American and southern European populations were highly distinct. A population from Ireland was monomorphic at all loci, presumably reflecting founder events associated with introduction of the species to the island in the sixteenth century. Bayesian analysis of demographic parameters showed differences in θ (a product of effective population size and mutation rate) among populations from large and small water bodies, but the relative differences in θ were smaller than expected, which could reflect population subdivision within the larger water bodies. Finally, the analyses showed drastic population declines on a time scale of several thousand years within European populations, which we ascribe to either glacial bottlenecks or postglacial founder events.  © 2005 The Linnean Society of London, Biological Journal of the Linnean Society , 2005, 84 , 91–101.     

Genetic variation and differentiation in captive and wild zebra finches (Taeniopygia guttata)

The zebra finch (Taeniopygia guttata) is a small Australian grassland songbird that has been domesticated over the past two centuries. Because it is easy to breed in captivity, it has become a widely used study organism, especially in behavioural research. Most work has been conducted on domesticated populations maintained at numerous laboratories in Europe and North America. However, little is known about the extent to which, during the process of domestication, captive populations have gone through bottlenecks in population size, leading to inbred and potentially genetically differentiated study populations. This is an important issue, because (i) behavioural studies on captive populations might suffer from artefacts arising from high levels of inbreeding or lack of genetic variation in such populations, and (ii) it may hamper the comparability of research findings. To address this issue, we genotyped 1000 zebra finches from 18 captive and two wild populations at 10 highly variable microsatellite loci. We found that all captive populations have lost some of the genetic variability present in the wild, but there is no evidence that they have gone through a severe bottleneck, as the average captive population still showed a mean of 11.7 alleles per locus, compared to a mean of 19.3 alleles/locus for wild zebra finches. We found significant differentiation between the captive populations (F(ST) = 0.062). Patterns of genetic similarity closely match geographical relationships, so the most pronounced differences occur between the three continents: Australia, North America, and Europe. By providing a tree of the genetic similarity of the different captive populations, we hope to contribute to a better understanding of variation in research findings obtained by different laboratories.     

Genie differentiation in M. m. domesticus populations from Europe, the Middle East and North Africa: geographic patterns and colonization events

Geographic patterns of genie differentiation were investigated in the commensal house mouse subspecies, M. m. domesticus . The analysis by protein electrophoresis of 40 populations throughout Europe, the Middle East and North Africa indicated that genie differentiation was not highly structured on a macrogeographic scale. Mean genie distances between regions showed, however, that populations fell into three levels of differentiation: a low level in southern Europe within which interregional distances were no larger than intraregional ones, an intermediate level between southern European populations and North European and African ones, and finally, a higher level between all the latter and the Middle Eastern populations.
Gene flow estimates indicated that the homogeneity of southern European populations does not result from present high levels of gene flow, but more likely from a very recent ancestry. These data when argumented with the fossil records of mice from the Mediterranean Basin suggest a two-step colonization process, the most recent of which occurred very rapidly and resulted in the multiple founding of populations in southern Europe. The relationship of M. m. domesticus to other subspecies of mice is discussed in relation to introgression and taxonomy.
Microdifferentiation patterns with low levels of within population substructuring and of gene flow suggest that genie differentiation in the western European house mouse is largely determined by genetic drift and/or founder effects. Although historical factors are determinant in the large scale patterns of genie variation in commensal house mice, dispersal by man no longer seems to be a prominent feature moulding the genetic structure of M. m. domesticus .