Evolution rampant: house mice on Madeira

House mice are extra-ordinary animals – extra -ordinary in the literal sense of that word. They are pests – but also a valued laboratory animal. They are generalized rodents – and successful in habitats from tundra to tropics and from sea-level to high altitudes. They have differentiated into a perplexity of taxa, yet differ little in their general morphology. They were long scorned by ecologists as recently arrived commensals, but are increasingly illuminating evolutionary processes as new techniques are applied to their study. Local forms, once valued only by taxonomists, are proving ever more interesting as their genetics are probed. In 1992, Mathias & Mira described the apparently unexciting characteristics of mice living on the two main islands of the Madeira group, 600 km west of continental Portugal. Then in 2000, Britton-Davidian et al. discovered that there were at least six chromosomal (Robertsonian) races on the main island. In the past decade, studies of molecular and mitochondrial genomes have shown an array of variables and posed questions about the origins and subsequent evolution of these island mice. In this issue of Molecular Ecology , Förster et al. report on the mtDNA haplotypes found on the island and in mainland Portugal, discuss the probable source of the island colonizers, and consider data which might give information about the timing of the colonizing event(s).     

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.     

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.     

On the origin of Robertsonian fusions in nature: evidence of telomere shortening in wild house mice

The role of telomere shortening to explain the occurrence of Robertsonian (Rb) fusions, as well as the importance of the average telomere length vs. the proportion of short telomeres, especially in nature populations, is largely unexplored. In this study, we have analysed telomere shortening in nine wild house mice from the Barcelona Rb system with diploid numbers ranging from 29 to 40 chromosomes. We also included two standard (2n = 40) laboratory mice for comparison. Our data showed that the average telomere length (considering all chromosomal arms) is influenced by both the diploid number and the origin of the mice (wild vs. laboratory). In detail, we detected that wild mice from the Rb Barcelona system (fused and standard) present shorter telomeres than standard laboratory mice. However, only wild mice with Rb fusions showed a high proportion of short telomeres (only in p‐arms), thus revealing the importance of telomere shortening in the origin of the Rb fusions in the Barcelona system. Overall, our study confirms that the number of critically short telomeres, and not a simple reduction in the average telomere length, is more likely to lead to the origin of Rb fusions in the Barcelona system and ultimately in nature.     

Adaptive energetics in house mice, Mus musculus domesticus, from the island of Porto Santo (Madeira archipelago, North Atlantic)

The bioenergetic strategies of house mice (Mus musculus domesticus) from the island of Porto Santo were investigated and compared with those of mice from mainland Portugal. Energy obtained from food ingestion was 18.2% lower in Porto Santo mice than in mainland mice (1.53 vs. 1.87 kJ/g/day). The same pattern was observed for metabolisable energy intake, which was 19.2% lower in island specimens (0.87 vs. 1.08 kJ/g/day for mainland specimens). Apparent digestibility was similar in both groups of mice. Basal metabolic rate (BMR) of Porto Santo individuals was low (1.16 ml O(2)/g/h), representing only 56% of the predicted value, based on body mass, while mainland individuals exhibited a BMR closer to the expected value, corresponding to 87% of the predicted value (1.80 ml O(2)/g/h). Thermoregulatory abilities within the range of 10-28 degrees C ambient temperature did not differ between island and mainland mice. Results suggest an adaptation of Porto Santo mice to the environmental aridity of the island of Porto Santo, leading to a conservative energetic strategy.     

Parapatric hybridization in the chromosomal speciation of the house mouse

Chromosomal races of the house mouse ( Mus domesticus ) occur extensively in Italy. The present paper reports results of studies on a hybrid zone in Central Italy on a chromosomal race with a 2 n = 22 karyotype and surrounding populations with a standard 2 n = 40 karyotype. Karyotypic and morphometric patterns of variation in this area are discussed in an attempt to contribute to an understanding of the chromosomal speciation in this species. Data are compared, where possible, with other findings on the same hybrid zone. Finally, it is suggested that changes in behavioural traits (inter-male aggression and female socio-sexual preferences) may help in promoting complete genetic isolation.     

Responses of house mice to the removal of mammalian predators and competitors

Efforts to eradicate multiple mammal pests from offshore islands and fenced mainland ‘habitat islands’ often fail to remove mice, and such failures can result in a dramatic change in the food‐web whereby the removal of larger mammal pests facilitates a population explosion of mice through predator and competitor release. We investigated the ecological responses of house mice to the removal of mammalian predators from a 500‐ha fenced sanctuary at Tawharanui, northern New Zealand. Data on population structure and body condition of mice trapped in 2007, in four habitat types within the sanctuary, were compared with baseline data collected in 2001, before mammal control operations commenced. We hypothesized that: (i) in the absence of mammalian predators mouse densities would increase in all habitat types that provide vegetation cover, and (ii) in the absence of mammalian competitors mice would become heavier due to greater access to food resources. Mouse densities were significantly higher in 2007 than in 2001 in three habitat types. The high density of mice in forest – where none were trapped prior to control – suggests a competitive release, in which mice profited from the removal of ship rats. No mice were caught in the presence of ship rats on a forest trap‐line at a control site outside the sanctuary. Mice trapped in 2007 were significantly heavier than those trapped in 2001, and significantly heavier than mice trapped at the control site. Greater access to food in the absence of competing and predatory mammals probably explains the heavier body weight of Tawharanui mice. There has been a significant change in the mammalian food‐web at Tawharanui, such that the house mouse is now the primary pest. A rapid and dramatic increase in mouse numbers is likely to adversely impact invertebrates and seedling recruitment, which in turn could affect ecosystem functions.     

Mitochondrial DNA phylogeny of Brimstone butterflies (genus Gonepteryx) from the Canary Islands and Madeira

Part of the mitochondrial Cytochrome Oxidase I gene was sequenced for seven species of Gonepteryx (Pieridac) butterflies. Four of the species are island endemics inhabiting the Canary Island archipelago and Madeira. The remaining three are European and African conspecifics. Sequence data were analysed phylogenetically by maximum parsimony and maximum likelihood methods. The resulting trees were used to deduce Canarian species' ancestry, sequential inter-island colonization and systematics. They suggest African ancestry for the Canary Island taxa and a colonization pattern, within the archipelago, compatible with the geological ages of the islands and other Canarian fauna: a colonization sequence from Africa to Tenerife and Gomera, followed by Tenerife to La Palma. The molecular phylogeny indicated that there are three Canarian endemics, G. cleobule, G. palmae and G. eversi from Tenerife, La Palma and Gomera, respectively.     

Genetic differentiation of U.S.S.R. house mice: electrophoretic study of proteins

Protein electrophoresis at 24 loci was used to characterize house mice from 56 localities in the U.S.S.R., concentrating on samples from Moldavia to Primorye (extreme south-east of the U.S.S.R.). Mus -2A is the most widespread form, extending over the European part of the U.S.S.R., Middle Asia and Siberia as far east as the Pacific Ocean. In Moldavia the group is sympatric with Mus-iB . It is found with Mus -4A in Transcaucasus, where it may hybridize with Mus -1. In Primorye Mus -2A and M. raddei have a wide zone of hybridization with Mus -2C.     

The structure of a chromosomal hybrid zone of house mice (Mus domesticus) in central Italy: cytogenetic analysis

Parapatric hybridization between the chromosomal race “CD” (2n = 22) and standard karyotype populations (2n = 40) of Mus domesticus occurs extensively in central Italy. The present paper reports the results of a ctogenetic surve on a transect crossin the hybrid zone north of Rome. No clinal variation in eitier diloid nuders and chromosome frequencies was found to occur in this area, and drift seems to be responsible for the observed atchy pattern of variation. The previous assumption of a strong fertility reduction in structuray heterozyous hybrids contrasts sharply with the width (32 km) of the zone and the average structural aeterozygosity of the hybrid poulations. It is suggested that fitness of structural heterozygotes in nature is not strongly aPfected as has been inferred from laboratory experiments. The results of this study are discussed in context together with the role of hybrid zones in chromosomal speciation in Mus domesticus.     

On the trail of Neolithic mice and men towards Transcaucasia: zooarchaeological clues from Nakhchivan (Azerbaijan)

Transcaucasia comprises a key region for understanding the history of both the hybrid zone between house mouse lineages and the dispersal of the Neolithic way of life outside its Near Eastern cradle. The opportunity to document the colonization history of both men and mice in Transcaucasia was made possible by the discovery of mouse remains accumulated in pits from a 6000‐year‐old farming village in the Nakhchivan (Autonomous Republic of Nakhchivan, Azerbaijan). The present study investigated their taxonomy and most likely dispersal path through the identification of the Mus lineage to which they might belong using a geometric morphometric approach of dental traits distances between archaeological and modern populations of the different Mus lineages of South‐West Asia. We demonstrate that the mouse remains trapped in the deep storage pits of the dwelling belong to the Mus musculus domesticus from the Near East, with dental shapes similar to current populations in Northern Syria. These results strongly suggest that the domesticus lineage was dispersed into Transcaucasia from the upper Euphrates valley by Neolithic migration, some time between the 7th and 5th millennium BC, providing substantial evidence to back up the scenario featuring near‐eastern stimuli in the emergence of agriculture in the South Caucasus. The domesticus mitochondrial DNA signature of the current house mouse in the same location 5000 years later, as well as their turnover towards a subspecies musculus/castaneus phenotype, suggests that early domesticus colonizers hybridized with a later musculus (and maybe castaneus) dispersal originating from south of the Caspian Sea and/or Northern Caucasia. © 2013 The Linnean Society of London     

Variation in aggressiveness in house mouse populations

Clearly the ability of 'house mice' to vary their social structures is an important feature contributing to their success in a wide range of habitats. Social structure is strongly influenced by aggressiveness and other behaviours in male and female mice. Material is presented illustrating how genotype, intrauterine location and social experiences influence dyadic encounters in this 'species'.     

Can the variability of mitochondrial DNA distinguish between commensal and feral populations of the house mouse?

The dynamics and variability of mitochondrial DNA (mtDNA) were compared in one commensal and one feral population of the house mouse ( Mus domesticus ) in Israel. The rate of turnover was high in both populations (the average proportion of new or discontinuing mice per trapping session was about 50%), as was the level of heterogeneity of mtDNA: using six restriction enzymes, 18 mice from the commensal population had eight different haplotypes (the degree of heterogeneity, h , was 0.802), and 412 mice from the feral population had 16 ( h = 0.894). These results suggest that neither population was composed of rigid breeding units made up of relatives, but that in the commensal population the few neighbouring resident mice that had the same mtDNA haplotype may have been siblings.     

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.     

On the problem of the origin of Pogonophora

A number of embryological features of the Pogonophora suggest that they could not derive from the Polychaeta and are closely related to Deuterostomia. These are: (1) traces of spiral cleavage that sharply differ the from cleavage of polychaetes in the prospective value of blastomeres; (2) enterocoelic formation of mesoderm; (3) the larva most closely resembles Balanoglossus that has just completed metamorphosis; proto-, meso-, and metasoma of pogonophoran larva correspond (or are homologous) to the proboscis, collar, and trunk of Balanoglossus respectively; while the telosoma can be regarded as an organ appearing late in phylogenesis that serves to burrow into the bottom; (4) larvae of Siboglinum have a transitory mouth located, as it is the case in Enteropneusta, between proto-and mesosoma, very far from the posterior end, where there is closed blastopore; therefore, the former can be considered as a secondary mouth; (5) the asymmetrical development of the anterior pair of coeloms in Pogonophora, Echinodermata, and Amphioxus allows finding homologies between organs developing from these coeloms.     

被子植物起源研究中几种观点的思考

对被子植物起源研究中的几种观点进行了讨论。(1)由于被子植物存在着一组共同的性状,它们不可能是从不同祖先起源的,而是有着共同的祖先。被子植物是一个单源起源的类群。现存被子植物分类系统是依据包括形态学(广义)、分子系统学、古植物学和植物地理学等的综合性状建立的,只能表示出现存类群的亲缘关系并且追溯到它们最近的祖先。人们现在还不可能建立一个包括全部已绝灭的类群和现代生存类群的谱系发生系统。因此,现存被子植物分类系统只能看作是“亲缘”系统。(2)分析了用于推测被子植物起源时间的分子、化石和地理分布证据。我们认为,要确定被子植物起源时间,植物化石是一类重要证据,但化石只能说是植物本身可保存部分和当时当地所提供的化石条件的综合反映,它们不可能就是植物类群或种的起源时间。人们还必须考虑到化石本身的演化历史。应用分子钟也是一种手段,但误差比较大。如果我们除了利用上述两种资料之外,根据植物类群的现代分布格局及其形成,把植物的演化同地球的历史和板块运动联系起来,以推断它们起源的时间,这无疑会增加其可信度。通过对56个种子植物不同演化水平的重要科属地理分布的研究结果,我们曾提出被子植物的起源时间可能要追溯到早侏罗世,甚至晚三叠世。(3)分析了基于分子证据所提出的被子植物基部类群——ANITA成员(包括无油樟科Amborellaceae、睡莲科Nymphaeaceae、八角目Illiciales、早落瓣科Trimeniaceae、木兰藤科Austrobaileyaceae)的性质,讨论了ANITA成员在现代几个被子植物分类系统中的系统位置的不同观点,评价了它们的形态学(广义)性状。指出ANITA的成员由于包含大量的祖征,是属于原始的类群。但由于它们的共有衍征很少,如花粉球形,说明它们在被子植物演化早期就分道扬镳了,沿着不同的传代线分化。因此ANITA是一个源于不同传代线的复合群。     

Tracing the colonization of Madeira and the Canary Islands by Drosophila subobscura through the study of the rp49 gene region

Nucleotide variation at the nuclear ribosomal protein 49 (rp49) gene region has been analysed by fine restriction mapping in a sample of 47 lines from a population from Madeira. Five restriction-site (out of 37 sites scored) and 3 length polymorphisms have been detected, resulting in 14 different haplotypes. This population shows less variation than both continental and Canary Island populations. The population from Madeira shows some differentiation from mainland populations, which does not favor the idea of extensive migration between the continent and Madeira. Chromosomal and restriction-map variation of the rp49 region in D. subobscura populations, together with data on sequence comparison of this nuclear region in D. guanche and D. madeirensis clearly indicate that the Canary Islands underwent at least two colonization events from the nearby continent. Although the data for Madeira are compatible with a single colonization event by a continental sample polymorphic for gene arrangements O₃ and O_{3 + 4}, an alternative scenario with at least two colonization events seems more likely.     

Patterns of colonization, evolution and gene flow in species of the genus Patella in the Macaronesian Islands

The study of phylogeographical patterns may contribute to a better understanding of factors affecting the dispersal of organisms in ecological and historical times. For intertidal organisms, islands are particularly suitable models allowing the test of predictions related to the efficacy of pelagic larvae dispersal. Here, we study the phylogeographical patterns and gene flow within three groups of species of the genus Patella present in the Macaronesian Islands that have been previously shown to be monophyletic. The genetic variability of around 600 bp of the mitochondrial gene cytochrome c oxidase subunit I was studied by single strand conformation polymorphism and/or sequencing for seven species of limpets. A total of 420 samples were analysed from the Macaronesian archipelagos, North Africa, and Atlantic and Mediterranean shores of the Iberian Peninsula. No clear geographical pattern or temporal congruence was found between the three groups of species, pointing to independent histories and colonization events. However, for the three groups, the split between the Macaronesian and the mainland forms most probably occurred before 3.9 million years ago, predating the establishment of the current circulation patterns. The presence of pelagic larvae in these species is shown to be insufficient to ensure gene flow between continental and Macaronesian populations and between the Macaronesian archipelagos. In the endangered Azorean populations of Patella candei, there is restricted gene flow to Flores and Graciosa.     

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.