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Chromosomal Dynamics of Nucleolar Organizer Regions (Nors) in the House Mouse: Micro-Evolutionary Insights

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Chromosomal Dynamics of Nucleolar Organizer Regions (Nors) in the House Mouse: Micro-Evolutionary Insights Heredity (2012) 108, 68–74 & 2012 Macmillan Publishers Limited All rights reserved 0018-067X/12 www.nature.com/hdy ORIGINAL ARTICLE Chromosomal dynamics of nucleolar organizer regions (NORs) in the house mouse: micro-evolutionary insights J Britton-Davidian, B Cazaux and J Catalan Variation in the number and chromosomal location of nucleolar organizer regions (NORs) was studied in the house mouse, Mus musculus (2n¼40). From an origin in Western Asia, this species colonized the Middle East, Europe and Asia. This expansion was accompanied by diversification into five subspecies. NOR diversity was revealed by fluorescence in situ hybridization using 18S and 28S probes on specimens spanning Asia to Western Europe. The results showed that the house mouse genome possessed a large number of NOR-bearing autosomes and a surprisingly high rate of polymorphism for the presence/absence of rRNA genes on all these chromosomes. All NOR sites were adjacent to the centromere except for two that were telomeric. Subspecific differentiation established from the NOR frequency data was concordant with the overall pattern of radiation proposed from molecular studies, but highlighted several discrepancies that need to be further addressed. NOR diversity in M. musculus consisted of a large number of polymorphic NORs that were common to at least two subspecies, and a smaller number of NORs that were unique to one subspecies. The most parsimonious scenario argues in favor of a subspecific differentiation by lineage sorting of ancestral NOR polymorphisms; only the unique NORs would have appeared by inter- chromosomal transposition, except for the two telomeric ones that may have originated by hybridization with another species. Such a scenario provides an alternative view from the one prevailing in most systematic and phylogenetic analyses that NORs have a high transposition rate due to concerted evolution of rRNA genes. Heredity (2012) 108, 68–74; doi:10.1038/hdy.2011.105; published online 16 November 2011 Keywords: NOR; house mouse; phylogeny; radiation; mus musculus;rDNA INTRODUCTION position events (Eickbush and Eickbush, 2007). When no chromosomal Nucleolar organizer regions (NORs) are chromosomal landmarks that repatterning is observed, several authors have ascribed the high consist of tandemly repeated sequences of ribosomal genes (rRNA). In transposition rates of NORs to the existence of transposons in the eukaryotes, each unit is composed of three genes coding for 18S, 5.8S rDNA clusters; such elements have been observed in plants, inverte- and 28S ribosomal RNA; these genes are separated by two intergenic brates and recently in intergenic spacer (IGS) repeats of the house spacers and an external transcribed spacer. Head-to-tail repeats of mouse (Grozdanov et al., 2003; Raskina et al., 2008; da Silva et al., these units form distinct clusters on one to several chromosome pairs. 2010). The vast majority of these investigations are based on the silver- The rRNA multigene family undergoes concerted evolution, whereby staining method which presents two drawbacks: it reveals only the the coding fraction of the rDNA sequences is homogenized so that active fraction of the rRNA genes, that is, those that were transcribed copies within a species are generally more similar than those between during the previous interphase, and in some cases, it may lead to non- species (Eickbush and Eickbush, 2007). Several molecular processes specific staining of heterochromatic regions (Dobigny et al., 2003; are involved in sequence homogenization: unequal crossover, gene Cabrero and Camacho, 2008; Carvalho et al., 2009). Access to the conversion and non-homologous recombination (Gonzalez and genes themselves by the fluorescence in situ hybridization (FISH) Sylvester, 2001; Parkin and Butlin, 2004). The concerted evolution technique has provided a cytogenetic tool to explore the extent of of these sequences is thought to be under purifying selection to ensure NOR diversity between species irrespective of their expression status the functionality of these essential translational genes. As the number (Matsubara et al., 2004; Datson and Murray, 2006; Nguyen et al., and position of the rDNA clusters are often species-specific, these 2008). However, many of these studies involve comparisons between chromosomal characters have been widely used in systematics and species, and thus provide little information on the evolutionary phylogenetic reconstructions. Studies on NOR variation in numerous processes acting on variation at the intraspecific level. To investigate plant, insect and vertebrate groups have invariably described changes the short-term evolutionary dynamics of rDNA clusters, we analyzed in the number and chromosomal location of NORs even in closely NOR diversity by the FISH approach in an emblematic species, the related species, suggesting that rDNA clusters are highly mobile house mouse. components of the genome (Gallagher et al., 1999; Datson and The house mouse, Mus musculus, is one of the 14 species compris- Murray, 2006; Cabrero and Camacho, 2008; Nguyen et al., 2010; da ing the subgenus Mus, which is remarkable for its highly conserved Silva et al., 2010; Cazaux et al., 2011). This important inter-species karyotype (2n¼40). A previous phylogenetic analysis of NOR lability is generated either by chromosomal rearrangements or trans- variation within the subgenus indicated that the number and location Institut des Sciences de l’Evolution, Universite´ Montpellier 2, Montpellier cedex, France Correspondence: Dr J Britton-Davidian, Institut des Sciences de l’Evolution, Universite´ Montpellier 2, Place E Bataillon, cc065, 34095 Montpellier cedex 05, France. E-mail: [email protected] Received 29 June 2011; revised 13 September 2011; accepted 30 September 2011; published online 16 November 2011 NOR dynamics in the house mouse J Britton-Davidian et al 69 of clusters between species differed, each taxon showing its own and the Robertsonian mice (2no40) was not significantly different chromosomal distribution (Cazaux et al., 2011). This extensive (FST¼0.0015; P¼0.41). Subsequently, DOM specimens were pooled irrespective NOR diversity indicated that high rates of inter-chromosomal trans- of their karyotype. The subspecific assignation of the studied specimens was position existed within the Mus genome in the absence of cytogen- determined from published molecular analyses of these individuals (mitochon- etically visible rearrangements. The house mouse is an Eurasian drial and nuclear sequences; Duplantier et al., 2002; Auffray et al., 2003; Bonhomme et al., 2007). These studies revealed that the mouse from Mada- polytypic species with five currently recognized subspecies: M. m. gascar had a mosaic genome: while it clearly harbored a distinct mitochondrial domesticus, the Western European house mouse, occupies western genome attributed to GEN (Prager et al., 1998; Duplantier et al., 2002), nuclear Europe and the Mediterranean Basin to southwestern Iran; M. m. markers indicated an affinity with CAS (Bonhomme et al., 2007). Where musculus, the eastern European house mouse, extends in fact from possible, the samples were pooled by geographic origin; given the extensive data northern Europe to China; M. m. castaneus, the Asian house mouse, is for DOM, the specimens were grouped into three regional clusters: the present from central to southeast Asia (Bonhomme et al., 2007; Mediterranean Basin, including southern Europe (S), northern Europe (N) Geraldes et al., 2008; Rajabi-Maham et al., 2008); M. m. molossinus, and the Atlantic Coast (A). the Japanese house mouse, is restricted to Japan and neighboring countries and originated by hybridization between M. m. musculus Methods and M. m. castaneus (Yonekawa et al., 2012); finally M. m. gentilulus, Mitotic metaphases were obtained by the air-drying method from bone the Arabian house mouse, is the most recently rehabilitated subspecies marrow cells after yeast stimulation. The number and location of the rRNA genes were detected by FISH using 18S (SalC-pSP64; 2 kb) and 28S (BE-2- occupying the southern Arabian peninsula (Prager et al., 1998; pSP64; 1.5 kb) probes, following the procedure detailed in Cazaux et al., 2011. Duplantier et al., 2002). Two extant hybrid zones exist involving Identification of chromosomes was performed by DAPI (4,6-diamidino-2- M. m. musculus, one with M. m. domesticus in Europe and the other phenylindole)-Banding following the standard nomenclature. A minimum of with M. m. castaneus in China (Bonhomme et al., 2007). From its 10 metaphases was observed per individual. All observations were made with a native Eurasian distribution, the house mouse subsequently expanded Zeiss Axiophot fluorescence microscope (Oberkochen, Germany) equipped its range worldwide through passive transport with humans. The with an image analyzer (Cytovision 3.93.2, Genetix, New Milton, UK). evolutionary history of the subspecific radiation of M. musculus has been extensively documented and most of the molecular analyses Analyses concur with the paleontological data in identifying the Indian rDNA genotypes. The rDNA genotypes were scored directly from the meta- subcontinent as the cradle from which the species expanded phase FISH signals, considering each chromosomal location as a locus with two (Bonhomme et al., 2007; Geraldes et al., 2008; Duvaux et al., in allelic states (presence and absence) and three possible genotypes (homozygous with or without an rDNA cluster, heterozygous). Thus, rRNA genes were press). This region
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