Multilocus phylogeography of a widespread savanna-woodland-adapted rodent reveals the influence of Pleistocene geomorphology and climate change in Africa's Zambezi region.

Understanding historical influences of climate and physiographic barriers in shaping patterns of biodiversity remains limited for many regions of the world. For mammals of continental Africa, phylogeographic studies, particularly for West African lineages, implicate both geographic barriers and climate oscillations in shaping small mammal diversity. In contrast, studies for southern African species have revealed conflicting phylogenetic patterns for how mammalian lineages respond to both climate change and geologic events such as river formation, especially during the Pleistocene. However, these studies were often biased by limited geographic sampling or exclusively focused on large-bodied taxa. We exploited the broad southern African distribution of a savanna-woodland-adapted African rodent, Gerbilliscus leucogaster (bushveld gerbil) and generated mitochondrial, autosomal and sex chromosome data to quantify regional signatures of climatic and vicariant biogeographic phenomena. Results indicate the most recent common ancestor for all G. leucogaster lineages occurred during the early Pleistocene. We documented six divergent mitochondrial lineages that diverged ~0.270-0.100 mya, each of which was geographically isolated during periods characterized by alterations to the course of the Zambezi River and its tributaries as well as regional 'megadroughts'. Results demonstrate the presence of a widespread lineage exhibiting demographic expansion ~0.065-0.035 mya, a time that coincides with savanna-woodland expansion across southern Africa. A multilocus autosomal perspective revealed the influence of the Kafue River as a current barrier to gene flow and regions of secondary contact among divergent mitochondrial lineages. Our results demonstrate the importance of both climatic fluctuations and physiographic vicariance in shaping the distribution of southern African biodiversity.

Tracking chromosome evolution in southern African gerbils using flow-sorted chromosome paints.

Desmodillus and Gerbilliscus (formerly Tatera) comprise a monophyletic group of gerbils (subfamily Gerbillinae) which last shared an ancestor approximately 8 million years ago; diploid chromosome number variation among the species ranges from 2n = 36 to 2n = 50. In an attempt to shed more light on chromosome evolution and speciation in these rodents, we compared the karyotypes of 7 species, representing 3 genera, based on homology data revealed by chromosome painting with probes derived from flow-sorted chromosomes of the hairy footed gerbil, Gerbillurus paeba (2n = 36). The fluorescent in situ hybridization data revealed remarkable genome conservation: these species share a high proportion of conserved chromosomes, and differences are due to 10 Robertsonian (Rb) rearrangements (3 autapomorphies, 3 synapomorphies and 4 hemiplasies/homoplasies). Our data suggest that chromosome evolution in Desmodillus occurred at a rate of ~1.25 rearrangements per million years (Myr), and that the rate among Gerbilliscus over a time period spanning 8 Myr is also ~1.25 rearrangements/Myr. The recently diverged Gerbillurus (G. tytonis and G. paeba) share an identical karyotype, while Gerbilliscus kempi, G. afra and G. leucogaster differ by 6 Rb rearrangements (a rate of ~1 rearrangement/Myr). Thus, our data suggests a very slow rate of chromosomal evolution in Southern African gerbils.

Desert gerbils affect bacterial composition of soil.

Rodents affect soil microbial communities by burrow architecture, diet composition, and foraging behavior. We examined the effect of desert rodents on nitrogen-fixing bacteria (NFB) communities by identifying bacteria colony-forming units (CFU) and measuring nitrogen fixation rates (ARA), denitrification (DA), and CO2 emission in soil from burrows of three gerbil species differing in diets. Psammomys obesus is folivorous, Meriones crassus is omnivorous, consuming green vegetation and seeds, and Dipodillus dasyurus is predominantly granivorous. We also identified NFB in the digestive tract of each rodent species and in Atriplex halimus and Anabasis articulata, dominant plants at the study site. ARA rates of soil from burrows of the rodent species were similar, and substantially lower than control soil, but rates of DA and CO2 emission differed significantly among burrows. Highest rates of DA and CO2 emission were measured in D. dasyurus burrows and lowest in P. obesus. CFU differed among bacteria isolates, which reflected dietary selection. Strains of cellulolytic representatives of the family Myxococcaceae and the genus Cytophaga dominated burrows of P. obesus, while enteric Bacteroides dominated burrows of D. dasyurus. Burrows of M. crassus contained both cellulolytic and enteric bacteria. Using discriminant function analysis, differences were revealed among burrow soils of all rodent species and control soil, and the two axes accounted for 91 % of the variance in bacterial occurrences. Differences in digestive tract bacterial occurrences were found among these rodent species. Bacterial colonies in P. obesus and M. crassus burrows were related to bacteria of A. articulata, the main plant consumed by both species. In contrast, bacteria colonies in the burrow soil of D. dasyurus were related to bacteria in its digestive tract. We concluded that gerbils play an important role as ecosystem engineers within their burrow environment and affect the microbial complex of the nitrogen-fixing organisms in soils.

Metagenome-Assembled Viral Genomes Analysis Reveals Diversity and Infectivity of the RNA Virome of Gerbillinae Species.

Rodents are a known reservoir for extensive zoonotic viruses, and also possess a propensity to roost in human habitation. Therefore, it is necessary to identify and catalogue the potentially emerging zoonotic viruses that are carried by rodents. Here, viral metagenomic sequencing was used for zoonotic virus detection and virome characterization on 32 Great gerbils of Rhombomys opimus, Meriones meridianus, and Meiiones Unguiculataus species in Xinjiang, Northwest China. In total, 1848 viral genomes that are potentially pathogenic to rodents and humans, as well as to other wildlife, were identified namely Retro-, Flavi-, Pneumo-, Picobirna-, Nairo-, Arena-, Hepe-, Phenui-, Rhabdo-, Calici-, Reo-, Corona-, Orthomyxo-, Peribunya-, and Picornaviridae families. In addition, a new genotype of rodent Hepacivirus was identified in heart and lung homogenates of seven viscera pools and phylogenetic analysis revealed the closest relationship to rodent Hepacivirus isolate RtMm-HCV/IM2014 that was previously reported to infect rodents from Inner Mongolia, China. Moreover, nine new genotype viral sequences that corresponded to Picobirnaviruses (PBVs), which have a bi-segmented genome and belong to the family Picobirnaviridae, comprising of three segment I and six segment II sequences, were identified in intestines and liver of seven viscera pools. In the two phylogenetic trees that were constructed using ORF1 and ORF2 of segment I, the three segment I sequences were clustered into distinct clades. Additionally, phylogenetic analysis showed that PBV sequences were distributed in the whole tree that was constructed using the RNA-dependent RNA polymerase (RdRp) gene of segment II with high diversity, sharing 68.42-82.67% nucleotide identities with other genogroup I and genogroup II PBV strains based on the partial RdRp gene. By RNA sequencing, we found a high degree of biodiversity of Retro-, Flavi-, Pneumo-, and Picobirnaridae families and other zoonotic viruses in gerbils, indicating that zoonotic viruses are a common presence in gerbils from Xinjiang, China. Therefore, further research is needed to determine the zoonotic potential of these viruses that are carried by other rodent species from different ecosystems and wildlife in general.

Molecular phylogenetics of the genus Gerbillus (Rodentia, Gerbillinae): Implications for systematics, taxonomy and chromosomal evolution.

Although gerbils forms an important component of the mammalian fauna of arid and semi-arid area, the taxonomic and phylogenetic relationship within the species of the genus Gerbillus are still ambiguous. The present paper introduces findings based on the whole cytochrome b (1140 bp) mitochondrial genes of seven species (Gerbillus campestris, G. latastei, G. nanus, G. tarabuli, G. gerbillus, G. simoni and G. nigeriae) six of which are present in Tunisia. Our results show that all the Gerbillus species are monophyletic. Moreover, molecular phylogeny rejects the genus rank for the taxon Dipodillus. Gebillus nanus, a species belonging to the subgenus Hendecapleura, early diverged from the other species which are divided into two clades: the subgenus Dipodillus, including G. campestris and G. simoni and the subgenus Gerbillus including G. gerbillus, G. nigeriae, G. tarabuli and G. latastei. These results are congruent with morphological and karyological evidences. According to molecular clock, the appearance of the genus Gerbillus coincides with the Miocene-Pliocene expansion of African arid biomes. Extensive intraspecific chromosomal changes evolved in a relatively narrow lapse of time, like in the case of G. latastei, allowing the fixations of different chromosomal variants due to pericentric inversion.

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 370km 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.

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.

Repeated evolution of camouflage in speciose desert rodents.

There are two main factors explaining variation among species and the evolution of characters along phylogeny: adaptive change, including phenotypic and genetic responses to selective pressures, and phylogenetic inertia, or the resemblance between species due to shared phylogenetic history. Phenotype-habitat colour match, a classic Darwinian example of the evolution of camouflage (crypsis), offers the opportunity to test the importance of historical versus ecological mechanisms in shaping phenotypes among phylogenetically closely related taxa. To assess it, we investigated fur (phenotypic data) and habitat (remote sensing data) colourations, along with phylogenetic information, in the species-rich Gerbillus genus. Overall, we found a strong phenotype-habitat match, once the phylogenetic signal is taken into account. We found that camouflage has been acquired and lost repeatedly in the course of the evolutionary history of Gerbillus. Our results suggest that fur colouration and its covariation with habitat is a relatively labile character in mammals, potentially responding quickly to selection. Relatively unconstrained and substantial genetic basis, as well as structural and functional independence from other fitness traits of mammalian colouration might be responsible for that observation.

The present status, distribution, demography, and diet of the Dahl's Jird / Status atual, distribuição, demografia e dieta do Jird de Dahl

Meriones dahli (Shidlovsky, 1962) was previously accepted to be a subspecies of M. meridianus (Pallas, 1773). However, it was later suggested that they are geographically isolated from each other. Although hybridological studies and differences in certain external characteristics support the idea that M. dahli is a separate species, there are still doubts on its species status, and the exact range of its distribution is not known. In this paper, we provide some taxonomic information about the species, and compare these with the information given in previous studies. We argue that some differences exist among Armenian population regarding external measurements. Recent studies indicate that M. dahli is currently only distributed in Turkey, as an endemic mammal species. We provide predictions about the distribution of M. dahli, and report the estimated population size to its maximum value. Food preference studies for this species, conducted under laboratory conditions, are also introduced for the first time. We discuss the ecological data obtained from field studies, and emphasize that the habitat of M. dahli is about to disappear. Consequently, the protection status of this species should urgently be changed to the CR category and conservation studies must be carried out immediately.

Meriones dahli (Shidlovsky, 1962) foi previamente aceito como uma subespécie de M. meridianus (Pallas, 1773). No entanto, mais tarde, foi sugerido que eles estão geograficamente isolados um do outro. Embora estudos hibridológicos e diferenças em certas características externas apoiem a ideia de que M. dahli é uma espécie separada, ainda há dúvidas sobre o status de sua espécie, e a extensão exata de sua distribuição não é conhecida. Neste artigo, fornecemos algumas informações taxonômicas sobre as espécies e as comparamos com as informações fornecidas em estudos anteriores. Argumentamos que existem algumas diferenças entre a espécie armênia em relação às medidas externas. Estudos recentes indicam que M. dahli está atualmente distribuído apenas na Turquia como uma espécie endêmica de mamífero. Fornecemos previsões sobre a distribuição de M. dahli e relatamos o tamanho estimado da população em seu valor máximo. Estudos de preferência alimentar para essa espécie, conduzidos em condições de laboratório, também são introduzidos pela primeira vez. Discutimos sobre os dados ecológicos obtidos em estudos de campo e enfatizamos que o habitat de M. dahli está prestes a desaparecer. Consequentemente, o status de proteção dessa espécie deve ser alterado com urgência para a categoria CR, e estudos de conservação devem ser realizados imediatamente.

Unusually extensive karyotype reorganization in four congeneric Gerbillus species (Muridae: Gerbillinae).

Comparative analysis of the G- and C-banding patterns in four morphologically poorly differentiated Gerbillus species (G. pyramidum, G. perpallidus, G. tarabuli and G. occiduus) was carried out. These gerbils have similar karyotype morphology with 2n and NF equal to 38/76, 40/76, 40/78 and 40/80, respectively. Our study revealed that possibly 70 Robertsonian (Rb) fusions, two pericentric inversions, one tandem translocation and at least 13 non-identified rearrangements have occurred during the karyotypic evolution of these species. The number of chromosomal changes by which any of these species differ from each other ranges from 33 to 49. One Rb fusion was common to two of the species, with only a single autosome-gonosome translocation shared by all four, suggesting a monophyletic origin of these karyotypically highly divergent species. Based on the chromosomal data obtained here, the systematic and geographic implications for these North African species are also discussed.

Evidence for the existence of two distinct species: Psammomys obesus and Psammomys vexillaris within the sand rats (Rodentia, Gerbillinae), reservoirs of cutaneous leishmaniasis in Tunisia.

A thorough taxonomic knowledge about putative animal reservoirs of transmissible diseases is an absolute prerequisite to any ecological investigation and epidemiological survey of zoonoses. Indeed, accurate identification of these reservoirs is essential for predicting species-specific population outbreaks and therefore to develop accurate ecological control strategies. The systematic status of sand rats (genus Psammomys) remains unclear despite the pivotal role of these rodents in the epidemiology of Zoonotic Cutaneous Leishmaniasis (ZCL) disease as sand rats are the main known reservoir hosts of the protozoan parasite Leishmania major. In the present work, we expose morphological, biochemical, genetic and cytogenetic evidence supporting the identification of at least two cryptic species within the genus Psammomys in Tunisia. First, significant morphometric differences were observed and were correlated associated with external features and biogeographic origins. Second, differences in patterns of two isoenzymic systems (Glutamate Oxaloacetate Transaminase (GOT) and 6-PhosphoGluconate Dehydrogenase (6PGD)) were found, which makes it possible to amount these isoenzyme characters to two diagnostic loci. Third, based on the mitochondrial cytochrome b (cyt b) gene, a high magnitude of genetic distance (13.89%) was also observed. Fourth, cytogenetic analysis showed that these two populations groups differ in their diploid chromosome numbers, i.e. 2N=46 versus 2N=48. We consider that all these variations are enough important to be considered as demonstrative and we propose that these two lineages should be considered as two distinct species that we refer to the fat sand rat Psammomys obesus Cretzschmar, 1828 and the thin sand rat Psammomys vexillaris Thomas, 1925. Implications of such results on the eco-epidemiology of ZCL in Tunisia are discussed.

The complete mitochondrial genome of Meriones libycus (Rodentia: Cricetidae) and its phylogenetic analysis.

Meriones libycus belongs to the genus Meriones in Gerbillinae, its complete mitochondrial genome is 16,341 bp in length. The heavy strand contains 32.8% A, 13.1% G, 25.3% C, 28.8% T, protein-coding genes approximately accounting for 69.54%. Results of phylogenetic analysis showed that M. libycus and Meriones unguiculatus were clustered together, and it was consistent with that of primary morphological taxonomy. This study verifies the evolutionary status of M. libycus in Meriones at the molecular level. The mitochondrial genome would be a significant supplement for the gene pool of Rodentia and the conclusion of phylogenetic analysis could be an important molecular evidence for the classification of Gerbillinae.

The complete mitochondrial genome of Meriones meridianus (Rodentia: Cricetidae) and its phylogenetic analysis.

Meriones meridianus belongs to the genus Meriones in Gerbillinae. Total length of complete mitochondrial genome of M. meridianus is 16,376 bp and the heavy strand contains 32.8% A, 13.1% G, 25.3% C and 28.8% T. Sequences of protein-coding genes are 11,341 bp in length, accounting for 69.25%, approximately. Results of phylogenetic analysis shown that M. meridianus and Meriones unguiculatus were clustered in a single branch. This conclusion would be an important data for relevant studies about the genus Meriones, and mitochondrial genome would be an important supplement for the gene pool of Rodentia. It would play a pivotal role in researches about phylogeography and proteomics involving M. meridianus as well.

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.

Mitochondrial DNA diversity in the populations of great gerbils, Rhombomys opimus, the main reservoir of cutaneous leishmaniasis.

Accurate identification of animal reservoirs of transmissible diseases is an absolute requirement to any epidemiological survey of zoonoses and is essential for predicting species-specific population outbreaks and therefore to develop accurate ecological control strategies. The systematic status of the great gerbil (Rhombomys opimus) remains unclear, despite the fundamental role of these rodents as the main known reservoir hosts of the protozoan parasite Leishmania major in the epidemiology of zoonotic cutaneous leishmaniasis (ZCL) in central and south Asia. In the present work, we represent molecular evidence supporting the identification of at least two major lineages (subspecies) within the species of R. opimus in Iran. Analysis of the mitochondrial cytochrome b (cyt b) gene, revealed a range of 1-10% genetic variation among populations, which were well associated with biogeographic origins and subspecies. Results of laboratory cross hybridization between the subspecies and finding sympatric haplotypes of the two subspecies suggested that no pre- or post-zygotic barriers exist between the subspecies indicating that they still belong to a single taxon. However, the amount of genetic variations between populations/subspecies is high enough to lead them to speciation in future. Implications of such findings on the eco-epidemiology of ZCL in Iran are discussed.

Patterns of reproduction in two sympatric gerbil species in arid Egypt.

Despite a significant number of studies on the reproductive characteristics of small mammals, very little of this work has been conducted on species in Egpyt. Here, the Egyptian greater gerbil (Gerbillus pyramidum Saint-Hilaire, 1825) and Anderson's lesser Egyptian gerbil (Gerbillus andersoni De Winton, 1902) in northeastern Egypt were surveyed. Breeding behavior in these species was synchronized with rainfall in the winter and spring months. Surprisingly however, the removal of individual gerbils throughout the course of study resulted in an extension of reproductive activity into the dry summer and autumn months in the latter part of the sampling. These results are discussed in the context of density-dependent reproductive behavior in small mammals.

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.