Systematics and evolution of the subfamily Gerbillinae (Mammalia, Rodentia, Muridae)

Although they represent a quarter of the mammalian species, the evolutionary relationships among as well as within, the main murid lineages are still controversial. The subfamily Gerbillinae is no exception as previous studies based on morphological, karyotypical, and allozyme characters are highly incongruent. Here, we present the first molecular phylogeny for gerbils based on cytochrome b and 12S rRNA mitochondrial genes. Results are largely congruent between the two genes as well as with the concatenated data set with most of the nodes being well-supported. Based on the topologies retrieved here, we (1) propose the identification of three main clades, (2) support the split of Tatera genus into an Asian and an African group, the latter including Gerbillurus species, and (3) provide some evidence towards the inaccuracy of subgeneric divisions within both Gerbillus and Meriones. In addition, the sharp contrast between the genetic characters and morphological data sets suggest high levels of convergence, probably as a result of strong environmental constraints imposed on these rodents adapted to arid and semi-arid regions. Finally, molecular datings for the various cladogenetic events are in good agreement with the known gerbilline fossil record and support an African origin with subsequent migrations to Asia.     

Behavioural Divergence in Allopatric and Sympatric Gerbil Species (Rodentia: Gerbillinae)

Southern African gerbils comprise 3 genera, each genus represented by morphologically- and ecologically-similar species. All species are monomorphic, with social systems varying from asocial (Desmodillus auricularis) to colonial (Tatera species). This study compares the behaviour patterns of an allopatric species, T. afra, 2 sympatric species, T. leucogaster and T. brantsii, and a species of a different genus, D. auricularis which is sympatric with T. leucogaster and T. brantsii. Interactions between males and females of the same species were staged and quantified in terms of the frequencies of each of 23 behavioural acts. D. auricularis performed 2 acts, namely “sidle” and “fight” which have not been identified in Gerbillurus or Tatera interactions. Sequences of behaviour were similar in all species, and involved females moving away from males, which followed, sniffed the anogenital region and attempted to mount the females. Females responded by presenting, if receptive, or agonistic behaviour such as aggressive or upright postures. Exploration of the terrarium accounted for a large proportion of the behaviour during the 20 min encounter, and watching the opponent also occurred frequently. Discriminant function analysis successfully separated all 4 species on the basis of behaviour frequencies. Individuals were assigned to the correct species with an accuracy of 80%, indicating that each species exhibits species-specific patterns of behaviour. D. auricularis displayed more agonistic and sexual behaviour and less huddling behaviour than any of the Tatera species. The sympatric species-pair, T. leucogaster and T. brantsii, exhibited more significant difference in behaviour than either of the allopatric species-pairs, T. afra and T. brantsii, and T. afra and T. leucogaster. Divergence in behaviour patterns has occurred in allopatric species, but divergence is more marked in species which are sympatric. It is not known whether divergence between T. leucogaster and T. brantsii occurred during a period of allopatry, or whether divergence has occurred due to selection against hybrids in sympatry.     

The origin of multiple sex chromosomes in the gerbil Gerbillus gerbillus (Rodentia: Gerbillinae)

The sex chromosomes of the partly sympatric species of gerbils Gerbillus pyramidum and G. gerbillus (Mammalia: Gerbillinae) were investigated by a variety of light- and electron-microscope methods, including DNA replication banding and synaptonemal complex (SC) techniques. The sex-chromosome mechanism of G. pyramidum is of the maleXY:femaleXX type, whereas that of G. gerbillus is of the less common maleXY1Y2:femaleXX system. The results include the demonstration that the X chromosomes of both species are compound. One segment is added to the X chromosome of G. pyramidum, leading to an increase in length from the standard 5% to approximately 7.3%, whereas two different extra segments increase the length of the X chromosome of G. gerbillus to approximately 11% of the length of the haploid genome. In both cases the extra material is autosomal and is also represented in the respective Y chromosomes. Classifying heterochromatin by the variation in staining quality was helpful in elucidating the possible origin of the different chromosome segments, including the pericentromeric regions. Observations on meiotic chromosome pairing and chiasma formation have confirmed the homologies established by band comparisons. The occurrence of chiasmata between the sex chromosomes supports the autosomal origin of the pairing segments. These and other findings have been interpreted in the framework of a multistep evolutionary model. This sequence starts from a hypothetical pair of sex chromosomes, the X element of which amounts to 5% of the haploid genome, and leads through three translocations involving two pairs of autosomes and one pericentric inversion to the most complex situation of this series, manifested in G. gerbillus. The adaptive value, if any, of autosome incorporation into the sex chromosomes repeatedly occurring here is unknown. It is, however, a remarkable fact that in one species, G. gerbillus, the complex sex-chromosome constitution is conserved over vast geographic distances, and in the other, G. pyramidum, the compound X and Y chromosomes withstand change in the face of extreme autosome restructuring.     

Morphometric analysis of six Gerbillus species (Rodentia,Gerbillinae) from Tunisia

Size and shape changes in the skull of the genus Gerbillus were investigated using geometric morphometrics. Six species from Tunisia were studied (G. gerbillus, G. campestris, G. nanus, G. tarabuli, G. simoni and G. latastei). Statistical analyses of shape variability allowed us to discriminate three morphological groups which are congruent with the three groups suggested by previous morphological and molecular studies. However, our results contrast with previous molecular investigations. In fact, according to results obtained by the use of principal component analysis, canonical variate analysis and UPGMA, we found a higher degree of divergence between the subgenus Dipodillus and the other two subgenera Gerbillus and Hendecapleura. This fact suggests that the morphometric differences observed among species within the genus Gerbillus are not mainly related to phylogeny. To reconciliate the molecular and morphological approaches, we propose a hypothesis of differential rates of phenotypic evolution in the genus Gerbillus. In this view, the species belonging to the subgenus Dipodillus evolved apomorphic features of the skull likely related to a higher degree of habitat specialization. By contrast, the more generalist Gerbillus and Hendecapleura subgenera show less differentiated plesiomorphic morphology.     

Phylogeography of Mus (Nannomys) minutoides (Rodentia,Muridae) in West Central African savannahs: singular vicariance in neighbouring populations

We studied the phylogeography of the strict savannah pygmy mice Mus (Nannomys) minutoides in West Central Africa. A total of 846 base pairs of the cytochrome b sequence were obtained for 66 individuals collected in Gabon, Cameroon, Republic of Congo and Central African Republic. These sequences were compared to those of M. minutoides from other African countries and to eight other species of the genus Mus. We performed maximum likelihood, Bayesian and nested clade analyses, as well as neutrality tests and time estimates. We show that M. minutoides is a well‐differentiated monophyletic species that separated from other pygmy mice 1.17 Myr ago. A distinct West Central African M. minutoides clade diverged early from the other African populations of the species, with a more recent common ancestor dating 0.14 Myr. West Central African populations are globally homogeneous, despite the present fragmentation of savannahs by the rain forest. However, our analyses show an unexpected vicariance between geographically close savannahs, embedded in the rain forest in Central Gabon. One of these populations is genetically more similar to very distant peripheral populations than to three closely neighbouring populations situated on both sides of the Ogooué River. A non‐river geographical barrier probably persisted in this area, durably isolating these local populations. This hypothesis about the history of the savannah landscape should be testable through the biogeographical analysis of other strict savannah small mammal species.     

Systematics and phylogeny of West African gerbils of the genus Gerbilliscus (Muridae: Gerbillinae) inferred from comparative G- and C-banding chromosomal analyses

Comparative analysis of the G- and C-banding patterns in six morphologically similar species of the genus Gerbilliscus(G. gambianus, G. guineae, G. kempi, Gerbilliscus sp., G. robustus and G. leucogaster) and one belonging to the genus Gerbillurus (G. tytonis) from 27 West, East and South African localities was carried out. Our study revealed that 17 rearrangements comprising seven fissions, five translocations and five inversions occurred in the evolution of this group, with 1-13 rearrangements differentiating the various species. In addition the unusually large sex chromosomes appear to be species-specific as judged by size and morphology reflecting structural rearrangements as well as the variable presence of a large amount of C-heterochromatin found in each species at a particular chromosomal location. These karyotypic features allow us to recognize five distinct species in West Africa (compared to the two recognized in recent taxonomic lists) and to roughly delimit their geographical distributions. The pattern of phylogenetic relationships inferred from a cladistic analysis of the chromosomal data is in good agreement with recent molecular phylogenetic studies that recognize a West African species group within the genus Gerbilliscus, and the monophyly of both Gerbilliscus and Gerbillurus.     

Mitochondrial phylogeny reveals differential modes of chromosomal evolution in the genus Tatera (Rodentia: Gerbillinae) in Africa

The African gerbils of the genus Tatera are widespread and abundant throughout sub-Saharan Africa. There is still today a certain controversy concerning the taxonomy of these rodents and very few attempts have been made to assess their systematic relationships. The present paper introduces findings based on the partial sequences of cytochrome b (495 bp) and the 16S rRNA (469 bp) mitochondrial genes of six (T. robusta, T. nigricauda, T. vicina, T. leucogaster, T. valida, and T. kempi) species together with two additional taxa. We also report the karyotypes of T. vicina and T. leucogaster. We propose that T. vicina should be considered as a valid species and show the monophyly of the robusta species group, with the exclusion of T. leucogaster. Our results show there is a different chromosomal evolutionary pattern within the two major lineages, which is recognizable through molecular phylogenetics. One is characterized by karyotype stability and the other by a considerable number of chromosomal rearrangements. The lineage divergence coincides with the formation of the East African Rift. The processes that led to the origin of the East African species seem to be related to the subsequent climatic changes, which caused cyclic contraction and expansion of the savannah biomes. Furthermore, geological activities that characterized East Africa during Plio-Pleistocene may also have contributed to lineage divergence.     

A Geometric Morphometric Analysis of Geographic Mandibular Variation in the Dwarf Gerbil Gerbillus nanus (Gerbillinae,Rodentia)

Journal of Mammalian Evolution - Previous studies have demonstrated the pliability and adaptability of mammalian mandibles in response to different ecological demands such as food availability. The...     

Notes on the distribution and phylogeography of two rare small Gerbillinae (Rodentia,Muridae) in Morocco: Gerbillus simoni and Gerbillus henleyi

Even though Gerbillinae rodents represent an important part of the mammalian fauna in North Africa, many gaps remain in our understanding of the distribution, ecology, evolution, and systematics of some lesser known species in this family. We present in this study the most recent findings on two of these species. The first species, Gerbillus simoni Lataste, 1881, is a short-tailed, small gerbil, endemic to North Africa. In Morocco, it is present only in a small area in the northeast, where it has not been caught since 1970. In 2014, we captured a small gerbil in this region that was identified as G. simoni based on morphology and molecular data (cytochrome b gene sequencing). This study represents the first genetic characterization of G. simoni in Morocco and the first one outside Tunisia. Populations from Morocco and Tunisia (mainland and Kerkennah Islands) show very little genetic differentiation. The second species, Gerbillus henleyi de Winton, 1903, is a long-tailed small gerbil that lives in the Sahel and North Africa with an extension to the Middle East. In Morocco, this species was only known in the southwest. Between 2014 and 2015, we have captured four gerbils in the northeast of the country, which were confirmed genetically and morphologically as belonging to this species. This represents an extension of its known distribution of about 370 km to the northeast of the country. These new Moroccan specimens form a distinct lineage. High genetic diversity is observed throughout the geographic range of G. henleyi, suggesting the existence of several cryptic species.     

Evolution of rRNA gene clusters and telomeric repeats during explosive genome repatterning in TATERILLUS X (Rodentia, Gerbillinae)

A survey of 28S and 5S rRNA gene clusters, and telomeric repeats was performed using single and double FISH in the Taterillus genus (Rodentia, Muridae, Gerbillinae). Taterillus was previously demonstrated to have undergone a very recent and extensive chromosomal evolution. Our FISH results demonstrate that rRNA genes can vary in location and number irrespective of the phylogenetic relationships. Telomeric repeats were detected in pericentromeric and interstitial regions of several chromosomes, thus providing nonambiguous evolutionary footprints of Robertsonian and tandem translocation events. These footprints are discussed in reference to the molecular process of these karyotypical changes. Also, examples of colocation of rDNA clusters and telomeric repeats lend support to their possible involvement in nucleolus formation. Finally, the presence of rRNA genes, and the extensive amplification of telomeric repeats at specific loci within a double X-autosome translocated element which were not observed on the homologous Y1 and Y2, served as basis for an epigenomic hypothesis on X-autosome translocation viability in mammals.     

Taxonomic hypotheses regarding the genus Gerbillus (Rodentia,Muridae, Gerbillinae) based on molecular analyses of museum specimens

Methodological improvements now allow routine analyses of highly degraded DNA samples as found in museum specimens. Using these methods could be useful in studying such groups as rodents of the genus Gerbillus for which i) the taxonomy is still highly debated, ii) collection of fresh specimens may prove difficult. Here we address precise taxonomic questions using a small portion of the cytochrome b gene obtained from 45 dry skin/skull museum samples (from 1913 to 1974) originating from two African and three Asian countries. The specimens were labelled Gerbillus gerbillus, Gerbillus andersoni, Gerbillus nanus, Gerbillus amoenus, Gerbillus perpallidus and Gerbillus pyramidum, and molecular results mostly confirmed these assignations. The close relationship between Gerbillus nanus (Asian origin) and Gerbillus amoenus (African origin) confirmed that they represent vicariant sibling species which differentiated in allopatry on either side of the Red Sea. In the closely related Gerbillus perpallidus and Gerbillus pyramidum, specimens considered as belonging to one Gerbillus pyramidum subspecies (Gerbillus pyramidum floweri) appeared closer to Gerbillus perpallidus suggesting that they (Gerbillus pyramidum floweri and Gerbillus perpallidus) may represent a unique species, distributed on both sides of the Nile River, for which the correct name should be Gerbillus floweri. Furthermore, the three other Gerbillus pyramidum subspecies grouped together with no apparent genetic structure suggesting that they may not yet represent genetically differentiated lineages. This study confirms the importance of using these methods on museum samples, which can open new perspectives in this particular group as well as in other groups of interest.     

Geographic pattern of cranial differentiation in the Asian Midday Jird Meriones meridianus (Rodentia: Muridae: Gerbillinae) and its taxonomic implications

The existence of cryptic species in the midday jird (Meriones meridianus) has been suggested in literature, although based on little empirical data to support this hypothesis. In this study, a two‐dimensional landmark‐based geometric morphometric approach was used to investigate whether patterns in intraspecific variation in skull shape and size exist, using 110 skull specimens from more than 20 different localities along the distribution range of M. meridianus. This is the first study of morphological differences on such a big sample size and geographical range, and it tries to find whether skull shape variation in this species is best described as being clinal or rather reflecting cryptic diversity. The latter seems to be the case, as a dimorphic skull phenotype was found, reflecting a geographic disparity between the Middle East and the Far East specimens both in shape and in size. Distinct cranial differences were found in the overall cranial size and, also at the level of the inflation of the bulla, the elongation of the nasal, the length of the teeth row and the incisive foramen, as well as the distance in between the latter two. It thus seems that M. meridianus from Middle East is morphologically distinct from that of the Far East. Furthermore, our results also demonstrate that clinal variation could explain variation within Middle East populations, whereas a more heterogenous pattern is found for those of the Far East. The hypothesis that the observed phenotypic variation may reflect cryptic species is discussed, with the recommendation for a thorough taxonomical revision of the genus in the region.     

The role of chromosome rearrangements in the evolution of mole voles of the genus Ellobius (Rodentia,Mammalia)

Modern mole voles of the genus Ellobius are characterized by species-specific features of autosomes and sex chromosomes. Owing to the use of the Zoo-FISH method, the nomenclature of chromosomes was refined and nonhomologous Robertsonian translocations indistinguishable by G-staining were identified for Ellobius tancrei, which is a species with a wide chromosome variation of the Robertsonian type. The electron-microscopic analysis of synaptonemal complexes in F₁ hybrids of forms with 2n = 50 and 2n = 48 revealed the formation of a closed SC-pentavalent composed of three metacentrics with monobrachial homology and two acrocentrics. Segregation of chromosomes of such complex systems is impeded by disturbances in the nucleus architecture leading to the formation of unbalanced gametes and to a dramatic reduction in fertility of hybrids. Our data support the hypothesis that the formation of monobrachial homologous metacentric chromosomes can be considered as a way of chromosomal speciation.     

Comparative chromosome analysis (R- and C-bands) of two South African murid species, Lemniscomys rosalia and Rhabdomys pumilio (Rodentia, murinae)

We carried out a comparative chromosome analysis (R- and C-bands) on two South African murid rodent species, Lemniscomys rosalia and Rhabdomys pumilio, whose banded karyotypes are reported here for the first time. The study revealed that, in spite of minor differences in diploid number and the number of autosomal arms (48 vs. 46 and 58 vs. 60, respectively), these species differ by at least 10 structural rearrangements, comprising seven Robertsonian translocations (two of which share monobrachial homology), two tandem translocations, and one pericentric inversion. Despite the high level of chromosomal differentiation observed, almost complete homologous banding patterns were detected between the two species. The present study therefore strengthens the hypothesis about the close phylogenetic affinities between L. rosalia and R. pumilio and their belonging to a set of genera referred to as "arvicanthine" rodents.