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

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

Frederic Veyrunes et al. Proc Biol Sci. 2006.

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.

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Figures

Figure 1

Figure 1

Flow karyotype of a male Nannomys minutoides (2_n_=18) resolving 10 peaks, each containing an Rb fusion chromosome pair.

Figure 2

Figure 2

Examples of hybridization using mouse chromosome paints (MMU) to (a,b) Nannomys mattheyi and (c,d) Coelomys pahari metaphase spreads counterstained with DAPI.

Figure 3

Figure 3

G-banded karyotypes of (a) Nannomys mattheyi and (b) Coelomys pahari with the assignments of Mus musculus homologous segments (chromosome pair numbers on the right) revealed by the mouse probes. ‘dist’, ‘med’ and ‘prox’ refer to the distal, median and proximal segment of the chromosome, respectively, and a and b refer to unidentified subchromosomal segments.

Figure 4

Figure 4

Most parsimonious phylogeny using PAUP, based on the 67 chromosomal characters (electronic supplementary material). Bootstrap values supporting each clade are indicated in bold on nodes. The chromosomal rearrangements, which have occurred within the genus Mus are mapped onto the tree and are numbered in grey. Each rearrangement is coded as follows: transl, translocation; inv, inversion; fiss, fission; fus, fusion followed by the character numbers of the table in the electronic supplementary material. Asterisk indicates the emergence of a new centromere. Rearrangements 1–3: transl* + inv 52–53; fiss* 3—rearrangements 4–11: inv 14; fus 16; fus 8; fus 58; transl 11; transl* 60; transl* 10; transl* 2—rearrangements 12–14: transl* 57; transl* 56; fus 59—rearrangements 15–19: transl* 1; transl* 18; transl 5; transl* 4; fus 13—rearrangements 20–22: fiss* 25; fiss* 26; fiss* 58—rearrangements 23–29: transl* 66; transl* 65; transl* 67; fus 64; fus 62; fus 61; fus 63. The divergence times mentioned follow Chevret et al. (2005) and Veyrunes et al. (2005).

Figure 5

Figure 5

Inferred haploid set of the ancestral karyotype of the genus Mus (2_n_=46) reconstructed with Coelomys, Nannomys and Mus G-banded chromosomes. Homology to Mus chromosomes is indicated to the right of each putative ancestral chromosome. ‘dist’, ‘med’ and ‘prox’ refer to the distal, median and proximal segment of the chromosome, respectively, and a and b refer to unidentified subchromosomal segments.

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