Subgenus Nannomys Research Articles

Taxonomic position and biogeography of Mus callewaerti, the largest species of the subgenus Nannomys (Rodentia: Muridae)

The Callewaert’s mouse (Mus callewaerti) is shown as an ancient lineage of the African endemic subgenus Nannomys. Described in 1925 as a large-bodied species with proodont (forward pointing) incisors, it was long known only from a handful of localities in Angola and southern Democratic Republic of the Congo. Here, it is revealed identical with a genetically distinctive Nannomys, provisionally called Mus sp. “Nyika” in previous studies and reported from Nyika Plateau (Malawi) and the Angolan Escarpment. The skull shape analysis clearly associated the holotype of M. callewaerti with other specimens ascribed to the species (including the genotyped ones). It also pinpointed diagnostic features distinguishing M. callewaerti from other large bodied Nannomys, especially its sympatric Mus triton, for which the species was repeatedly mistaken. Mus callewaerti is presumably insectivorous and rare or not easy to capture. The divergence between its Malawian and Angolan populations is relatively shallow, dated to 0.32 million years ago, which suggests that at least in the past the species could be widespread. Mus callewaerti is known from grassy, locally moisty habitats. Together with a handful of other rodent taxa it provides evidence of persistence and historic connection of these habitats across the Zambezian region.

Evolution of the Grey-bellied pygmy mouse group: Highly structured molecular diversity with predictable geographic ranges but morphological crypsis

The grey-bellied pygmy mouse (Mus triton) from the endemic African subgenus Nannomys is a widespread rodent species inhabiting the highlands of eastern and central Africa. Although it has long been considered as a single species, recent data has suggested the existence of a species complex. In order to evaluate the geographical structure and current taxonomy of M. triton, we analysed one mitochondrial and six nuclear genes from individuals covering most of its distribution range. Our analysis revealed the existence of at least five distinct genetic lineages with only marginal overlaps among their distributional ranges. Morphological comparisons, however, showed large overlaps in external body measurements and only a weak differentiation in skull form. Therefore, we suggest maintaining M. triton as a single taxon with pronounced intraspecific genetic structure. Divergence dating analysis placed the most recent common ancestor of the extant lineages of M. triton to the early Pleistocene (about 2.0 Ma). The phylogeographic structure of the species was likely shaped by Pleistocene climatic oscillations and the highly diverse topography of eastern Africa.

Pan-African phylogeny of Mus (subgenus Nannomys) reveals one of the most successful mammal radiations in Africa.

BackgroundRodents of the genus Mus represent one of the most valuable biological models for biomedical and evolutionary research. Out of the four currently recognized subgenera, Nannomys (African pygmy mice, including the smallest rodents in the world) comprises the only original African lineage. Species of this subgenus became important models for the study of sex determination in mammals and they are also hosts of potentially dangerous pathogens. Nannomys ancestors colonized Africa from Asia at the end of Miocene and Eastern Africa should be considered as the place of their first radiation. In sharp contrast with this fact and despite the biological importance of Nannomys, the specimens from Eastern Africa were obviously under-represented in previous studies and the phylogenetic and distributional patterns were thus incomplete.ResultsWe performed comprehensive genetic analysis of 657 individuals of Nannomys collected at approximately 300 localities across the whole sub-Saharan Africa. Phylogenetic reconstructions based on mitochondrial (CYTB) and nuclear (IRBP) genes identified five species groups and three monotypic ancestral lineages. We provide evidence for important cryptic diversity and we defined and mapped the distribution of 27 molecular operational taxonomic units (MOTUs) that may correspond to presumable species. Biogeographical reconstructions based on data spanning all of Africa modified the previous evolutionary scenarios. First divergences occurred in Eastern African mountains soon after the colonization of the continent and the remnants of these old divergences still occur there, represented by long basal branches of M. (previously Muriculus) imberbis and two undescribed species from Ethiopia and Malawi. The radiation in drier lowland habitats associated with the decrease of body size is much younger, occurred mainly in a single lineage (called the minutoides group, and especially within the species M. minutoides), and was probably linked to aridification and climatic fluctuations in middle Pliocene/Pleistocene.ConclusionsWe discovered very high cryptic diversity in African pygmy mice making the genus Mus one of the richest genera of African mammals. Our taxon sampling allowed reliable phylogenetic and biogeographic reconstructions that (together with detailed distributional data of individual MOTUs) provide a solid basis for further evolutionary, ecological and epidemiological studies of this important group of rodents.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-014-0256-2) contains supplementary material, which is available to authorized users.

A new cytotype of the African pygmy mouse Mus minutoides in Eastern Africa. Implications for the evolution of sex-autosome translocations.

The African pygmy mice (genus Mus, subgenus Nannomys) are recognized for their highly conserved morphology but extensive chromosomal diversity, particularly involving sex-autosome translocations, one of the rarest chromosomal rearrangements among mammals. It has been shown that in the absence of unambiguous diagnostic morphological traits, sex-autosome translocations offer accurate taxonomic markers. For example, in Mus minutoides, irrespective of the diploid number (which ranges from 2n = 18 to 34), all specimens possess the sex-autosome translocations (X.1) and (Y.1) that are unique to this species. In this study, we describe a new cytotype that challenges this view. Males are characterized by the translocation (Y.1) only, while females carry no sex-autosome translocation, the X chromosome being acrocentric. Hence, although sex-autosome translocations (X.1) and (Y.1) are still diagnostic when one or both are present, their absence does not rule out M. minutoides. This cytotype has a large distribution, with specimens found in Tanzania and in the eastern part of South Africa. The nonpervasive distribution of Rb(X.1) provides an opportunity to investigate different evolutionary scenarios of sex-autosome translocations using a phylogenetic framework and the distribution of telomeric repeats. The results tend to support a scenario involving a reversal event, i.e., fusion then fission of Rb(X.1), and highlighted the existence of a new X1X1X2X2/X1X2Y sex chromosome system, confirming the remarkable diversity of neo-sex chromosomes and sex determination systems in the African pygmy mice.

A phylogeographic survey of the pygmy mouse Mus minutoides in South Africa: taxonomic and karyotypic inference from cytochrome b sequences of museum specimens.

The African pygmy mice (Mus, subgenus Nannomys) are a group of small-sized rodents that occur widely throughout sub-Saharan Africa. Chromosomal diversity within this group is extensive and numerous studies have shown the karyotype to be a useful taxonomic marker. This is pertinent to Mus minutoides populations in South Africa where two different cytotypes (2n = 34, 2n = 18) and a modification of the sex determination system (due to the presence of a Y chromosome in some females) have been recorded. This chromosomal diversity is mirrored by mitochondrial DNA sequences that unambiguously discriminate among the various pygmy mouse species and, importantly, the different M. minutoides cytotypes. However, the geographic delimitation and taxonomy of pygmy mice populations in South Africa is poorly understood. To address this, tissue samples of M. minutoides were taken and analysed from specimens housed in six South African museum collections. Partial cytochrome b sequences (400 pb) were successfully amplified from 44% of the 154 samples processed. Two species were identified: M. indutus and M. minutoides. The sequences of the M. indutus samples provided two unexpected features: i) nuclear copies of the cytochrome b gene were detected in many specimens, and ii) the range of this species was found to extend considerably further south than is presently understood. The phylogenetic analysis of the M. minutoides samples revealed two well-supported clades: a Southern clade which included the two chromosomal groups previously identified in South Africa, and an Eastern clade that extended from Eastern Africa into South Africa. Congruent molecular phylogenetic and chromosomal datasets permitted the tentative chromosomal assignments of museum specimens within the different clades as well as the correction of misidentified museum specimens.

Enigmatic Ethiopian endemic rodent Muriculus imberbis (Rüppell 1842) represents a separate lineage within genus Mus

The phylogenetic position of the Ethiopian striped mouse (Muriculus imberbis) has remained obscure since its description. Here, we report, for the first time, the phylogenetic analysis of this species using mitochondrial (cytochrome b) and nuclear (interphotoreceptor binding protein) gene sequences obtained from a specimen recently caught in the Galama Mountain in the south-central Ethiopian highland region. The recent finding of the species in ericaceous shrub in the Afroalpine habitat is remarkable, as decades of attempts to capture it in this habitat failed, probably because of inappropriate trapping methods. Our analyses strongly suggest that the Ethiopian striped mouse does not belong to a distinct monotypic genus, but to the genus Mus, as the ancient lineage of the African subgenus Nannomys

Increased geographic sampling reveals considerable new genetic diversity in the morphologically conservative African Pygmy Mice (Genus Mus; Subgenus Nannomys)

African endemic pygmy mice (Genus Mus; sub-genus Nannomys) have considerable economic and public health significance, and some species exhibit novel sex determination systems, making accurate knowledge of their phylogenetics and distribution limits important. This phylogenetic study was based on the mitochondrial control region and cytochrome b gene, for which a substantial body of published data was available. Study specimens were sourced from eight previously unsampled or poorly sampled countries, and include samples morphologically identified as Mus bufo, M. indutus, M. callewaerti, M. triton and M. neavei. These analyses increase the known genetic diversity of Nannomys from 65 to 102 haplotypes; at least 5 unassigned haplotypes are distinguished by potentially species-level cytochrome b genetic distances. The monophyly of Nannomys is supported. Mus musculoides, M. callewaerti, M. indutus, M. bufo, M. haussa, M. mattheyi, M. baoulei and M. sorella are supported as discrete species. The range of M. indutus is extended to include Botswana. M. setulosus and M. minutoides appear to be species complexes. A south and east African M. minutoides clade was defined and includes 8 new haplotypes out of 15. M. setulosus sensu lato includes M. setulosus sensu stricto and a strongly-supported M. bufo clade. Two samples, morphologically identified as M. triton and M. neavei, fall within the M. minutoides clade.

Systematics and evolution of the African pygmy mice, subgenus Nannomys: A review

African pygmy mice (subgenus Nannomys) are a group of small murine rodents that are widespread throughout Sub-Saharan Africa. Although this group has long been recognized for its extensive chromosomal diversity, the highly conserved morphology of its members has made taxonomic assignments problematic. Renewed interest resulting from a series of cytogenetic and molecular investigations has led to the identification of novel patterns of diversification in these rodents that are reviewed herein. These approaches have considerably improved species delimitation and provide tentative diagnostic criteria as well as preliminary phylogenetic relationships that will be refined as more taxa are investigated. Although sparse, ecological data suggest that pygmy mice may exhibit original reproductive traits that deserve further investigation. Chromosomal diversity undoubtedly remains one of the most interesting features of African pygmy mouse biology. They display several karyotypic traits that are rare in mammals: (i) their genomes tolerate the recurrent formation of tandem fusions and sex-autosome translocations, both of which are rare in other mammals due to their highly deleterious effects on fertility; (ii) they exhibit the first case of a whole arm exchange involving an X chromosome, and (iii) two species show novel means of sex chromosome determination – one exhibits XY females, whereas the other harbors populations in which males have no Y chromosome. The diversity of African pygmy mice offers a unique opportunity to study the processes involved in their radiation, and in a broader context, the evolution of sex chromosome determination in mammals.

Taxonomy and biogeography of the African Pygmy mice, Subgenus Nannomys (Rodentia, Murinae, Mus) in Ivory Coast and Guinea (West Africa)

Recent investigations in Guinea and Ivory Coast showed that Mus (Nannomys) are hosts of new arenaviruses. However, the taxonomy and biogeography of the western pygmy mice are poorly known, as this genus contains many cryptic species. To improve our taxonomic knowledge on this subgenus and its distribution range in West Africa, we performed a molecular, cytogenetical and morphological study of all Mus (Nannomys) species in this part of Africa. This approach allowed us to detect five species in Guinea (Mus mattheyi, M. minutoides, M. setulosus, M. baoulei, M. musculoides) and four (M. minutoides, M. setulosus, M. baoulei, M. musculoides) in Ivory Coast. Our molecular results confirm the validity of M. baoulei and the extended distribution range of M. mattheyi. We also observed a high degree of genetic differentiation between and within these species, especially within the M. setulosus clade which may be a species complex. The canonical analyses on the craniometrical and external morphological features of the sequenced specimens are insufficient to perfectly separate the studied species. Nevertheless, our results confirm that M. setulosus and M. baoulei are the largest Mus species that occur in Guinea and Ivory Coast. M. baoulei can be distinguished by its short tail and M. setulosus by an enlarged and bilobated lower molar (M3). Among the smaller species, M. musculoides is difficult to identify using morphological data alone, but differences in tail length proportions, size of tympanic bullae, the length and shape of the upper dental row allow identification of this species with some confidence. Our results allow us to provide some conclusions about the distribution ranges of the studied Mus (Nannomys) spp. in both countries and to discuss their presence in relation to vegetation, habitat and human settlements.

Cytogenetics of a new cytotype of African Mus (subgenus Nannomys) minutoides (Rodentia, Muridae) from Kenya: C- and G- banding and distribution of (TTAGGG)n telomeric sequences

We present the results of a cytogenetic study on Mus (Nannomys) minutoides from Kenya by means of C- and G- banding and in-situ fluorescence hybridization (FISH) to localize the telomeric sequences. The karyotype is characterized by the occurrence of several Rb chromosomes Rb(1.X), Rb(1.Y). Rb(2.17), Rb(3.13), Rb(4.10), Rb(5.11), Rb(6.7), Rb(8.12), not previously described for this species. This finding suggests a high level of chromosomal diversification, which means it is possible to consider this cytotype as a new, well-differentiated, chromosomal lineage within the subgenus. The C-banding of the metaphases illustrated conspicuous blocks of centromeric heterochromatin at the paracentromeric regions of all telocentric chromosomes. Centromeric heterochromatin is not visible on all biarmed chromosomes. Following hybridization with telomeric probes, bright interstitial telomeric sequence (ITS) fluorescence signals are evident at the pericentromeric area of all Rb chromosomes, with the exception of Rb(2.17). Considering the localization of the C-positive heterochromatin and of the telomeric sequences, the events leading to the Kenyan cytotype from an all-telocentric condition probably included two steps: first, fusion without loss of heterochromatin and pericentromeric telomeric sequences; second, the reduction of the C-positive satellite DNA followed by the amplification of telomeric sequences in the C-negative paracentromeric region of Rb chromosomes. The presence of a single Rb(2.17) without ITS indicates possible variations of this mechanism.

Molecular phylogeny of the African pygmy mice, subgenus Nannomys (Rodentia, Murinae, Mus): Implications for chromosomal evolution

Molecular phylogenies based on sequences of mitochondrial cytochrome b and nuclear IRBP genes are assessed on a comprehensive taxonomic sampling of African pygmy mice (subgenus Nannomys of the genus Mus). They represent a taxonomically diversified group of morphologically similar species, and exhibit an important chromosomal diversity, particularly involving sex-autosome translocations, one of the rarest and most deleterious chromosomal changes among mammals. The results show that the species sampled are genetically well differentiated, and that chromosomal rearrangements offer accurate diagnostic characters for discriminating most species. Furthermore, the species carrying different sex-autosome translocations appear monophyletic, suggesting that a genome modification allowing a higher rate of occurrence and/or fixation of such translocations took place, leading to the emergence of this lineage. In addition to taxonomic and biogeographical clarifications, we provide a temporal framework within which patterns of genic and chromosomal evolution are discussed.

Molecular phylogeny of the genus Mus (Rodentia: Murinae) based on mitochondrial and nuclear data

The genus Mus encompasses at least 38 species divided into four subgenera: Mus, Pyromys, Nannomys and Co-elomys. The subgenus Mus, which comprises the house mouse and related species, is by far the most extensively studied, although the subgenus Nannomys is the most speciose. Although the relationships within the subgenus Mus are rather well characterized, those between subgenera are still unclear. In the present study, phylogenetic analyses of the whole genus were performed using a larger species sample of Nannomys than in previous studies, and a nuclear gene (IRBP) in addition to mitochondrial data (cytochrome b and 12S rRNA). Members of the Acomyinae and Murinae were used as outgroups. Separate and combined analyses were performed with maximum parsimony, maximum likelihood and Bayesian methods, and divergence times were estimated. The results showed that the monophyly of the genus Mus and of each subgenus was strongly supported by the three genes and the combined analysis. The phylogenies derived from the three genes were on the whole congruent; however, several conflicting topologies were observed such as the relationships between the three Asian species of the subgenus Mus (caroli, cervicolor and cookii). Increasing the taxonomic sampling of Nannomys did not satisfactorily improve the resolution of relationships between the four subgenera. In addition, molecular calibrations indicate that the Mus and Nannomys radiation coincided with major environmental changes.

Serologic variations in kappa light chains of various Mus species correlate with differences in gene structure

Kappa light chains were investigated in sera of several groups of wild derived mouse strains by radioimmunological analysis using xenogeneic anti-mouse κ light chain antibodies. Although the majority of strains tested expressed serologically indistinguishable κ chains, several significant exceptions were observed. Anti-κ chain reactivity was not detectable in normal sera of Mus caroli and Mus cervicolor species using specific antiserum. These strains express a variant of the κ light chain. Some serologic variation was also observed in κ chains from members of the subgenus Nannomys. Southern blot analyses using C κ and J κ probes indicated different patterns of hybridization in strains that were serologically distinguishable. Mus caroli and Mus cervicolor DNAs digested with the enzymes EcoRI or BamHI show variation from BALB/c and most other mouse strains tested in the size of the hybridizing fragments. This correlation between serologic and blotting analyses is no longer found in SJL and SPE strains, which show variation in BamHI cleavage but not at the serological level. The majority of laboratory and wild derived mice analyzed have the same pattern of hybridization. Taken together our results may also have implications for the phylogenetic classification of wild type mouse strains.