mtDNA phylogeny and evolution of laboratory mouse strains.
Journal: 2007/April - Genome Research
ISSN: 1088-9051
Abstract:
Inbred mouse strains have been maintained for more than 100 years, and they are thought to be a mixture of four different mouse subspecies. Although genealogies have been established, female inbred mouse phylogenies remain unexplored. By a phylogenetic analysis of newly generated complete mitochondrial DNA sequence data in 16 strains, we show here that all common inbred strains descend from the same Mus musculus domesticus female wild ancestor, and suggest that they present a different mitochondrial evolutionary process than their wild relatives with a faster accumulation of replacement substitutions. Our data complement forthcoming results on resequencing of a group of priority strains, and they follow recent efforts of the Mouse Phenome Project to collect and make publicly available information on various strains.
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Genome Res 17(3): 293-298

mtDNA phylogeny and evolution of laboratory mouse strains

Instituto de Patologia e Imunologia Molecular da Universidade do Porto (IPATIMUP), 4200-465 Porto, Portugal;
Faculdade de Ciências da Universidade do Porto, 4099-002 Porto, Portugal;
Medical Faculty, University of Porto, 4200-319 Porto, Portugal;
The Jackson Laboratory, Bar Harbor, Maine 04609, USA;
Department of Statistics, University of Glasgow, G12 8QQ Glasgow, United Kingdom
Corresponding author.E-mail tp.pumitapi@adiemlaa; fax +351-22-5570799.
Received 2006 Sep 12; Accepted 2006 Dec 8.

Abstract

Inbred mouse strains have been maintained for more than 100 years, and they are thought to be a mixture of four different mouse subspecies. Although genealogies have been established, female inbred mouse phylogenies remain unexplored. By a phylogenetic analysis of newly generated complete mitochondrial DNA sequence data in 16 strains, we show here that all common inbred strains descend from the same Mus musculus domesticus female wild ancestor, and suggest that they present a different mitochondrial evolutionary process than their wild relatives with a faster accumulation of replacement substitutions. Our data complement forthcoming results on resequencing of a group of priority strains, and they follow recent efforts of the Mouse Phenome Project to collect and make publicly available information on various strains.

Abstract

Long before the beginning of mouse genetics, humans in Eastern Asia were already breeding mice in order to obtain animals with different coat colors. Modern mouse genetics, however, did not start until the early 20th century with William Castle’s studies on inheritance. Most of his mice derived from collections of mice fanciers, and they were the ancestors of many inbred strains that are still used today (Rader 2004).

Mouse strains are known to have mixtures of various ancestral genomes from different Mus musculus (house mouse) subspecies (for review, see Yoshiki and Moriwaki 2006). Different molecular markers suggest that the main contributors are M. musculus musculus (Bishop et al. 1985), M. musculus domesticus (Yonekawa et al. 1982; Sakai et al. 2005), and, to a lesser extent, M. musculus castaneus (Sakai et al. 2005). One other subspecies that is usually considered to have contributed is M. musculus molossinus (Sakai et al. 2005), although this itself is supposed to be a hybrid between M. m. musculus and M. m. castaneus (Lundrigan et al. 2002; Wade et al. 2002).

More than 450 mouse inbred strains have been established since the first—DBA/2 (dilute, brown, non-agouti)—was developed by Castle’s student Clarence Cook Little in what would become The Jackson Laboratory (Beck et al. 2000; Rader 2004). Furthermore, in different laboratories worldwide, many substrains of each strain have also been maintained.

A mouse strain is defined as inbred if the animals have been crossed brother × sister for ≥20 consecutive generations and individuals of the strain can be traced back to a single ancestor pair at the 20th or subsequent generation (Eppig et al. 2005). Theoretical studies indicate that, at this time, ≥98.6% of loci should be homozygous, but many strains have been bred for >150 generations, which makes them homozygous at virtually every locus (Beck et al. 2000).

Beck et al. (2000) extensively documented inbred mice genealogies, suggesting that independent inbreeding processes occurred in at least three regions of the globe: (1) Castle’s mice (Group B) and C57-related strains (Group E) originated from Abbie Lathrop’s stocks in the United States; (2) Swiss mice (Group A) derived from mice from Switzerland; and (3) strains derived from colonies from China and Japan (Group C). Little is known, however, of mitochondrial DNA (maternal) phylogenies of these strains. So far, there has been only one study on complete mtDNA sequences from different inbred strains, with the purpose of revising the complete mouse mtDNA reference sequence (Bayona-Bafaluy et al. 2003). The study of mtDNA phylogenies has the potential to elucidate the matrilineal lineage of common inbred strains and its relationship to the main subspecific lineages.

Mammalian mitochondrial DNA (mtDNA) is a circular double-stranded molecule that encodes 13 genes of the respiratory chain. Defects in these molecules have been associated with a variety of disorders that may affect different tissues in different ways (for review, see Wallace 1999). A number of mouse models have recently been developed that have clarified how mutations in mtDNA are transmitted. Examples include transmitochondrial mice carrying heteroplasmic point mutations (Sligh et al. 2000), heteroplasmic mice with mtDNAs from variants characteristic of two different strains (Battersby and Shoubridge 2001), and mice with homoplasmic replacement of endogenous mtDNA (McKenzie et al. 2004). With this recent increasing interest in mtDNA from mice models, it becomes important to know the mtDNA sequence in each of the different inbred strains.

The analysis of complete mtDNA sequences of inbred mice is also useful for the establishment of mutation/substitution rates. Given that, in principle, these restricted animal populations have a reasonably well documented history, with no inclusion of foreign DNA, variation that occurs can be generated only by mutation. Moreover, study of mice mitochondrial phylogenies may become helpful in clarifying differences that have been reported between mutation rates estimated from pedigrees and substitution rates calculated from phylogenies (Howell et al. 2003; Ho et al. 2005; Ho and Larson 2006).

Two main issues were addressed while performing this work: (1) validation of published genealogies and clarification of the matrilineal origin of common inbred strains and (2) evolutionary analysis of inbred strains. It was developed by focusing on 16 selected strains that are part of the Mouse Phenome Project (Bogue 2003), which aims to enhance the resources available for laboratory mice by collecting phenotypic and genotypic characteristics of these animals and making them publicly available through a Web-accessible database. These data may ultimately help researchers track down the genes involved in particular phenotypes, by allowing association of phenotypes with genotypes for each strain. A set of 40 priority strains has been established, and for 15 of them the complete genome is now being resequenced (Pearson 2004). By performing the mtDNA characterization of these 15 strains (plus C57BL/6), we are also contributing to this project.

Acknowledgments

This work was partially supported by Fundação para a Ciência e a Tecnologia through a research grant to A.G. (SFRH/BD/16518/2004) and by “Programa Operacional Ciência, e Inovação 2010” (POCI 2010), VI Programa-Quadro (2002–2006).

Acknowledgments

Footnotes

[Supplemental material is available online at www.genome.org. The sequence data from this study have been submitted to GenBank under accession nos. {"type":"entrez-nucleotide-range","attrs":{"text":"EF108330-EF108345","start_term":"EF108330","end_term":"EF108345","start_term_id":"118200613","end_term_id":"118200823"}}EF108330-EF108345.]

Article published online before print. Article and publication date are online at http://www.genome.org/cgi/doi/10.1101/gr.5941007

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