Extensive recombination rate variation in the house mouse species complex inferred from genetic linkage maps
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Abstract:
The rate of recombination is a key genomic parameter that displays considerable variation among taxa. Species comparisons have demonstrated that the rate of evolution in recombination rate is strongly dependent on the physical scale of measurement. Individual recombination hotspots are poorly conserved among closely related taxa, whereas genomic-scale recombination rate variation bears a strong signature of phylogenetic history. In contrast, the mode and tempo of evolution in recombination rates measured on intermediate physical scales is poorly understood. Here, we conduct a detailed statistical comparison between two whole-genome F₂ genetic linkage maps constructed from experimental intercrosses between closely related house mouse subspecies (Mus musculus). Our two maps profile a common wild-derived inbred strain of M. m. domesticus crossed to distinct wild-derived inbred strains representative of two other house mouse subspecies, M. m. castaneus and M. m. musculus. We identify numerous orthologous genomic regions with significant map length differences between these two crosses. Because the genomes of these recently diverged house mice are highly collinear, observed differences in map length (centimorgans) are suggestive of variation in broadscale recombination rate (centimorgans per megabase) within M. musculus. Collectively, these divergent intervals span 19% of the house mouse genome, disproportionately aggregating on the X chromosome. In addition, we uncover strong statistical evidence for a large effect, sex-linked, site-specific modifier of recombination rate segregating within M. musculus. Our findings reveal considerable variation in the megabase-scale recombination landscape among recently diverged taxa and underscore the continued importance of genetic linkage maps in the post-genome era.Keywords:
Centimorgan
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House mouse
House mice
Genetic linkage
Analysis at 20 genetic loci by starch gel electrophoresis of a population from Greece shows that contrary to most accepted views, the outdoor Eastern Mediterranean Short-tailed Mouse (i) does not belong to the same species as the House Mouse (Mus musculus), (ii) is not less distant from the Eastern European semi-species of House Mouse (biochemical group 2) than from the Western and Mediterranean European semi-species (group 1), and (iii) is not more closely related to the outdoor Western Mediterranean Short-tailed Mouse Mus spretus (group 3), than to M. musculus. It represents a new biochemical group (group 4) and deserves a species rank (Mus spicilegus).
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Abstract We investigated the distributions and routes of colonization of two commensal subspecies of house mouse in Norway: Mus musculus domesticus and M. m. musculus . Five nuclear markers ( Abpa , D11 cenB2 , Btk , SMCY and Zfy2 ) and a morphological feature (tail length) were used to differentiate the two subspecies and assess their distributions, and mitochondrial (mt) D‐loop sequences helped to elucidate their colonization history. M. m. domesticus is the more widespread of the two subspecies, occupying the western and southern coast of Norway, while M. m. musculus is found along Norway’s southeastern coast and east from there to Sweden. Two sections of the hybrid zone between the two subspecies were localized in Norway. However, hybrid forms also occur well away from that hybrid zone, the most prevalent of which are mice with a M. m. musculus ‐type Y chromosome and an otherwise M. m. domesticus genome. MtDNA D‐loop sequences of the mice revealed a complex phylogeography within M. m. domesticus , reflecting passive human transport to Norway, probably during the Viking period. M. m. musculus may have colonized earlier. If so, that leaves open the possibility that M. m. domesticus replaced M. m. musculus from much of Norway, with the widely distributed hybrids a relict of this process. Overall, the effects of hybridization are evident in house mice throughout Norway.
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Hybrid zone
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Abstract Patterns of H-2 and allozyme polymorphism in natural populations of house mice from Europe, North Africa and South America were analyzed. The purpose of the analysis was to determine whether H-2 and allozyme polymorphisms were similarly distributed both geographically and temporally in wild mice. Two subspecies of house mice, Mus musculus domesticus and M. m. musculus were sampled and the polymorphisms of two H-2 class I genes, H-2K and H-2D, and 34 allozyme-encoding genes were surveyed. The three kinds of analyses that were conducted included a hierarchical gene diversity analysis, an analysis of the effects of barriers to gene flow, and an analysis of similarity networks. Each of the comparisons demonstrated that H-2 polymorphisms were more uniformly distributed than allozyme polymorphisms and provided additional evidence that H-2 and allozyme polymorphisms are subject to different evolutionary pressures. The analysis of similarity networks also demonstrated that H-2 genes provide little information about the phylogeny of wild mice.
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Abstract For more than 100 years, house mice ( Mus musculus ) have been used as a key animal model in biomedical research. House mice are genetically diverse, yet their genetic background at the global level has not been fully understood. Previous studies suggested that they originated in South Asia and diverged into three major subspecies almost simultaneously, approximately 350,000–500,000 years ago; however, they have spread across the world with the migration of modern humans in prehistoric and historic times (∼10,000 years ago to present), and undergone secondary contact, which have complicated the genetic landscape of wild house mice. In this study, we sequenced the whole genomes of 98 wild house mice collected from Eurasia, particularly East Asia, Southeast Asia, and South Asia. We found that although wild house mice consist of three major genetic groups corresponding to the three major subspecies, individuals representing admixture between subspecies are much more ubiquitous than previously recognized. Furthermore, several samples showed an incongruent pattern of genealogies between mitochondrial and autosomal genomes. Using samples likely retaining the original genetic components of subspecies with least admixture, we estimated the pattern and timing of divergence among the subspecies. The results are important for understanding the genetic diversity of wild mice on a global level and the information will be particularly useful in future biomedical and evolutionary studies using laboratory mice established from these wild mice.
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Molecular markers and morphological characters can help infer the colonization history of organisms. A combination of mitochondrial (mt) d -loop DNA sequences, nuclear DNA data, external measurements and skull characteristics shows that house mice ( Mus musculus ) in New Zealand and its outlying islands are descended from very diverse sources. The predominant genome is Mus musculus domesticus (from western Europe), but Mus musculus musculus (from central Europe) and Mus musculus castaneus (from southern Asia) are also represented genetically. These subspecies have hybridized to produce combinations of musculus and domesticus nuclear DNA coupled with domesticus mtDNA, and castaneus or musculus mtDNA with domesticus nuclear DNA. The majority of the mice with domesticus mtDNA that we sampled had d -loop sequences identical to two haplotypes common in Britain. This is consistent with long-term British–New Zealand cultural linkages. The origins of the castaneus mtDNA sequences widespread in New Zealand are less easy to identify.
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On the Miura Peninsula of central Honshu, Japan, there are international ports that, it is concerned, provide opportunities for the introduction of house mice via overseas cargoes. To evaluate the occurrence of such an introduction of overseas mice, in this study, we analyzed mitochondrial cytochrome b (Cytb) gene and the morphological characteristics of house mouse (Mus musculus) samples (n = 47) from five localities on the Miura Peninsula. All of the Cytb sequences of the present mouse samples were recognized as the musculus type corresponding to the subspecies musculus in Eurasia, which have been seen frequently in the Japanese Islands in previous studies. In addition, consistent with typical Japanese house mice, external morphology of the present mouse samples showed a shorter tail length and head and body length as compared with those of M. domesticus domesticus in Europe, M. musculus musculus in northern Europe and M. castaneus castaneus in southeastern Asia in Marshal (1998). Accordingly, in the current research area on the Miura Peninsula, it seems that there has been no influence by overseas mice, and the present mice examined are recognized as the typical Japanese house mice, considering the above Cytb properties and morphological characteristics.
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