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Phylogenomics of the genus Mus (Rodentia; Muridae): extensive genome repatterning is not restricted to the house mouse.

ABSTRACT: The house mouse (Mus musculus) is universally adopted as the mammalian laboratory model, and it is involved in most studies of large-scale comparative genomics. Paradoxically, this taxon is rarely the index species for evolutionary analyses of genome architecture owing to its highly rearranged karyotype. To unravel the origin and nature of this extensive repatterning genome, we performed a multidirectional chromosome painting study of representative species within the genus Mus. However, the latter includes four extant subgenera (Mus, Coelomys, Nannomys and Pyromys) between which the phylogenetic relationships remain elusive despite the numerous molecular studies. Comparative genomic maps were established using chromosome-specific painting probes of the laboratory mouse and Nannomys minutoides. Hence, by integrating closely related species within Mus, this study allowed us to: (i) unambiguously resolve for the first time the long-standing controversial phylogeny, (ii) trace the evolution of genome organization in the house mouse, (iii) track rearrangements that necessitated new centromere locations, i.e. formation of neocentromere or reactivation of latent centromeres, (iv) reveal an extremely high rate of karyotypic evolution, with a 10- to 30-fold acceleration which was coincidental with subgeneric cladogenesis and (v) highlight genomic areas of interest for high-resolution studies on neocentromere formation and synteny breakpoints.

SUBMITTER: Veyrunes F

PROVIDER: S-EPMC1639516 | biostudies-literature | 2006 Dec

REPOSITORIES: biostudies-literature

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Phylogenomics of the genus Mus (Rodentia; Muridae): extensive genome repatterning is not restricted to the house mouse.

Veyrunes Frederic F Dobigny Gauthier G Yang Fengtang F O'Brien Patricia C M PC Catalan Josette J Robinson Terence J TJ Britton-Davidian Janice J

Proceedings. Biological sciences 20061201 1604

The house mouse (Mus musculus) is universally adopted as the mammalian laboratory model, and it is involved in most studies of large-scale comparative genomics. Paradoxically, this taxon is rarely the index species for evolutionary analyses of genome architecture owing to its highly rearranged karyotype. To unravel the origin and nature of this extensive repatterning genome, we performed a multidirectional chromosome painting study of representative species within the genus Mus. However, the lat ...[more]

PMID: 17015352

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Project description:BackgroundRecent advances in comparative genomics have considerably improved our knowledge of the evolution of mammalian karyotype architecture. One of the breakthroughs was the preferential localization of evolutionary breakpoints in regions enriched in repetitive sequences (segmental duplications, telomeres and centromeres). In this context, we investigated the contribution of ribosomal genes to genome reshuffling since they are generally located in pericentromeric or subtelomeric regions, and form repeat clusters on different chromosomes. The target model was the genus Mus which exhibits a high rate of karyotypic change, a large fraction of which involves centromeres.ResultsThe chromosomal distribution of rDNA clusters was determined by in situ hybridization of mouse probes in 19 species. Using a molecular-based reference tree, the phylogenetic distribution of clusters within the genus was reconstructed, and the temporal association between rDNA clusters, breakpoints and centromeres was tested by maximum likelihood analyses. Our results highlighted the following features of rDNA cluster dynamics in the genus Mus: i) rDNA clusters showed extensive diversity in number between species and an almost exclusive pericentromeric location, ii) a strong association between rDNA sites and centromeres was retrieved which may be related to their shared constraint of concerted evolution, iii) 24% of the observed breakpoints mapped near an rDNA cluster, and iv) a substantial rate of rDNA cluster change (insertion, deletion) also occurred in the absence of chromosomal rearrangements.ConclusionsThis study on the dynamics of rDNA clusters within the genus Mus has revealed a strong evolutionary relationship between rDNA clusters and centromeres. Both of these genomic structures coincide with breakpoints in the genus Mus, suggesting that the accumulation of a large number of repeats in the centromeric region may contribute to the high level of chromosome repatterning observed in this group. However, the elevated rate of rDNA change observed in the chromosomally invariant clade indicates that the presence of these sequences is insufficient to lead to genome instability. In agreement with recent studies, these results suggest that additional factors such as modifications of the epigenetic state of DNA may be required to trigger evolutionary plasticity.

Project description:Murine cytomegalovirus (MCMV) is a betaherpesvirus of the house mouse, Mus musculus domesticus. It is a common infectious agent of wild mice and a highly studied pathogen of the laboratory mouse. Betaherpesviruses are specific to their hosts, and it is not known if other Mus taxa carry MCMV or if it is restricted to M. m. domesticus. We sampled mice over a 145-km transect of Bavaria-Bohemia crossing a hybrid zone between M. m. domesticus and Mus musculus musculus in order to investigate the occurrence of MCMV in two Mus subspecies and to test the limits of the specificity of the virus for its host. We hypothesized that if the two subspecies carry MCMV and if the virus is highly specific to its host, divergent MCMV lineages would have codiverged with their hosts and would have a geographical distribution constrained by the host genetic background. A total of 520 mice were tested by enzyme-linked immunosorbent assay (ELISA) and/or nested PCR targeting the M94 gene. Seropositive and PCR-positive individuals were found in both Mus subspecies. Seroprevalence was high, at 79.4%, but viral DNA was detected in only 41.7% of mice. Sequencing revealed 20 haplotypes clustering in 3 clades that match the host genetic structure in the hybrid zone, showing 1 and 2 MCMV lineages in M. m. domesticus and M. m. musculus, respectively. The estimated time to the most recent common ancestor (1.1 million years ago [Mya]) of the MCMVs matches that of their hosts. In conclusion, MCMV has coevolved with these hosts, suggesting that its diversity in nature may be underappreciated, since other members of the subgenus Mus likely carry different MCMVs.Murine cytomegalovirus (MCMV) is a betaherpesvirus of the house mouse, Mus musculus domesticus, an important lab model for human cytomegalovirus (HCMV) infection. The majority of lab studies are based on only two strains of MCMVs isolated from M. m. domesticus, Smith and K181, the latter derived from repeated passage of Smith in mouse submaxillary glands. The presence of MCMV in other members of the Mus subgenus had not even been investigated. By screening mouse samples collected in the European house mouse hybrid zone between M. m. domesticus and M. m. musculus, we show that MCMV is not restricted to the M. m. domesticus subspecies and that MCMVs likely codiverged with their Mus hosts. Thus, the diversity of MCMV in nature may be seriously underappreciated, since other members of the subgenus Mus likely carry their own MCMV lineages.

Project description:BACKGROUND:Intraspecific variation within the diverse southern African murine rodents has not been extensively investigated, yet cryptic diversity is evident in several taxa studied to date. The Namaqua rock mouse, Micaelamys namaquensis Smith, 1834 is a widespread endemic murine rodent from the subregion. Currently, a single species with four subspecies is recognised, but in the past up to 16 subspecies were described. Thus, this species is a good candidate for the investigation of patterns and processes of diversification in a diverse but under-studied mammalian subfamily and geographic region. Here, we report genetic differentiation based on mitochondrial DNA (mtDNA) cytochrome b (cyt b) sequences among samples collected over an extensive coverage of the species' range. RESULTS:Cytochrome b sequences of 360 widely sampled individuals identified 137 unique maternal alleles. Gene tree and phylogeographic analyses of these alleles suggest the presence of at least eight lineages or haplogroups (A-H), with varying degrees of intra-lineage diversity. This differentiation is in contrast with the most recent taxonomic treatment based on cranial morphometrics which only recognised four subspecies. The mtDNA diversity strongly supports earlier views that this taxon may represent a species complex. We further show statistical support for the association of several of these lineages with particular vegetation biomes of southern Africa. The time to the most recent common ancestor (TMRCA) dates to the Pliocene (~5 Mya) whereas coalescent-based divergence time estimates between lineages vary between 813 Kya [0.22-1.36] and 4.06 Mya [1.21-4.47]. The major diversification within lineages occurred during the Pleistocene. The identification of several regions of sympatry of distinct lineages offers future opportunities for the elucidation of the underlying speciation processes in the suggested species complex. CONCLUSIONS:Similar to other African murine rodents, M. namaquensis radiated during the Pliocene and Pleistocene coinciding with major periods of aridification and the expansion of savanna habitats. The suggested species complex is represented by at least eight lineages of which the majority are confined to only one or a few neighbouring biomes/bioregions. Contrasting intra-lineage phylogeographic patterns suggest differences in adaptation and responses to Plio-Pleistocene climatic and vegetation changes. The role of ecological factors in driving speciation in the group needs further investigation.

Dataset Information

Phylogenomics of the genus Mus (Rodentia; Muridae): extensive genome repatterning is not restricted to the house mouse.

Publications

Phylogenomics of the genus Mus (Rodentia; Muridae): extensive genome repatterning is not restricted to the house mouse.

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