Molecular systematics of gerbils and deomyines (Rodentia: Gerbillinae,Deomyinae) and a test of desert adaptation in the tympanic bulla

Recent molecular studies in gerbils found multiple instances of discordance between molecular and morphological phylogenies. In this study, we analyse the largest molecular data set to date of gerbils and their sister group the deomyines to estimate their phylogenetic relationships. Maximum‐likelihood and Bayesian analyses were largely concordant, and both generally had high levels of node support. For gerbils, the results were generally concordant with previous molecular phylogenies based on allozymes, chromosomes, DNA/DNA hybridization and DNA sequences, and discordant with morphological phylogenies. None of the traditional gerbil tribes and subtribes were monophyletic. In addition, paraphyly was found in the genera Gerbillus, Gerbilliscus and Meriones as well as in five subgenera within Dipodillus, Gerbillurus and Meriones. Short branches separating taxa in small clusters within Dipodillus and Meriones suggest synonymy. Within deomyines, all genera and subgenera were monophyletic; however, two species groups within Acomys appear to contain synonymous taxa. We also find support for the discordance between molecular and morphological phylogenies in gerbils being partly due to convergent adaptations to arid environments, primarily in the suite of traits associated with inflation of the tympanic bullae. Relative bullar size does appear to be a desert adaptation and is correlated with aridity independent of phylogeny. Further, it varies more strongly along bioclimatic clines than between binary habitat classifications (desert versus mesic).     

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.     

Geometric morphometrics, neural networks and diagnosis of sibling Taterillus species (Rodentia, Gerbillinae)

The lack of diagnostic traits in sibling species means that great quantities of biogeographical and ecological data held in museum collections cannot be utilized effectively, leading to underestimates of biodiversity. In this study we applied neural networks (NN) and canonical variates analyses (CVA) to landmark measurements on the skulls of the West African species Taterillus arenarius , T. petteri , T. gracilis and T. pygargus in an attempt to discriminate species previously identified unambiguously from their karyotypes. Among suggested differences, the relationship between inflation of the tympanic bullae and lower population density is discussed. Cross-validated classification rates did not exceed 73%. Two hypotheses are proposed to explain such high phenotypic similarity: morphological plasticity limited by environmental constraints and the possibility that speciation has been too recent to allow significant morphological divergence.  © 2002 The Linnean Society of London, Biological Journal of the Linnean Society , 2002, 77 , 319−327.     

Intraspecific Allometric comparison of Laboratory gerbils with Mongolian Gerbils Trapped in the Wild Indicates Domestication in Meriones unguiculatus (Milne-Edwards, 1867) (Rodentia: Gerbillinae)

A survey of adult male Mongolian gerbils, Meriones unguiculatus (Milne-Edwards, 1867), either trapped during an expedition in Mongolia near 47 °N and 105,5 °E in June 1995 (WILD) or obtained from a laboratory strain bred in captivity since 1935 (LAB), revealed significant morphological and behavioural differences, which are likely a result of domestication in the laboratory strain. Mean body length (125.4 mm), tail length (95.5 mm) and body weight (53.6 g) was lower in WILD, although no other external characteristics were obviously different. Related allometrically to net carcass weight, organ weights were significantly lower (p < 0.01) in LAB (brain – 17.6%, eyes – 26.0%, heart – 22.3%, lungs – 43.3%). Seizures frequently seen in LAB were absent in WILD trapped (n = 167) or subsequently housed in Germany (n = 81), and rare in their offspring. Mean litter size was greater in LAB (n = 5.5) than in WILD bred in the laboratory (n = 4.4). The WILD breeding strain was named Ugoe:MU95.A genetic bottleneck (n = 9) that occurred in 1954 and remarkably smaller brains in LAB indicate that the laboratory strain has become domesticated and should be designated as “Laboratory gerbils” (M. unguiculatus forma domestica) to signify this new case of domestication among rodents.     

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.     

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...     

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.     

Ultrasonic Vocalizations of Six Taxa of Southern African Gerbils (Rodentia: Gerbillinae)

Ultrasonic calling during male-female encounters between individuals of the same species was investigated in six taxa of southern African gerbils, namely Tatera brantsii, Gerbillurus paeba paeba, G. p. cxilis, G. tytonis, G. setzeri, and G. vallinus. Vocalizations were detected by means of a bat detector utilizing a superheterodyne signal converter and a countdown circuit. Signals were recorded at audible frequencies and analysed with a sonograph. All taxa vocalized at ultrasonic frequencies by means of strongly modulated frequency “sweep” calls, which differed among taxa in duration, maximum and minimum frequency. “Clicks” were emitted by G. p. paeba and G. p. exilis, and G. tytonis emitted a “stutter” vocalization which consisted of a series of clicks. Long modulated “whistles” were identified from G. vallinus and T. brantsii at lower frequencies than “sweep” calls. Only one call type, a “sweep” call which differed in duration and frequency from all other taxa, was identified in G. setzeri. Cluster analysis was applied to the data using 7 acoustic characters. G. p. paeba and G. p. exilis displayed the highest similarity level between taxa and differed only in frequency of “sweep” vocalizations. G. paeba, G. tytonis and G. setzeri formed one cluster, while G. vallinus and T. brantsii formed a separate cluster. Numbers of calls in interspecific encounters were non-significantly less than in intraspecific encounters in all taxa except G. p. paeba, in which more vocalizations were recorded in inter- than intraspecific encounters. It is not clear whether species discrimination, measured by numbers of vocalizations in interspecific encounters, occurs.     

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.     

Recent radiation in West African Taterillus (Rodentia, Gerbillinae): the concerted role of chromosome and climatic changes

West African gerbils of the genus Taterillus constitute a complex of seven sibling species distributed from sudano-guinean to saharo-sahelian regions. They display radically rearranged karyotypes despite low genic divergence and a very recent differentiation, that is, within the last 0.4 Myr for the six most derived species. We here provide a comparison of the seven specific karyotypes and perform a cladistic analysis using chromosomal rearrangements character states. When a posteriori polarized mutations were mapped onto the phylogenetic tree, 38 rearrangements were identified as fixed during the evolution of these rodents. This makes Taterillus one of the most striking examples of accelerated chromosomal evolution within placental mammals. Taking into account the types of chromosomal changes involved, divergence times between lineages, genetic distances, as well as reassessed geographic distributions, we suggest that (1) speciation in West African Taterillus was driven by chromosomal changes, and (2) the paleoclimatic oscillations of the Sahara desert have played a major role in their evolution. In particular, elevated plasticity of the Taterillus genome, as suggested by the patterns observed for some repetitive elements, would have led to a higher probability of mutation. We hypothesize that the process underpinning cladogenesis most probably involved highly underdominant genomic rearrangements that were fixed following pronounced populational bottlenecks resulting from drastic climatic and subsequent environmental changes. Major African rivers formed significant barriers to dispersal, limiting expansion during the more moist and so favorable periods. This scenario would explain the current parapatric species distributions and their relationship to the West African hydrographic features.     

Evolutionary relationships between morphology, performance and habitat openness in the lizard genus Niveoscincus (Scincidae: Lygosominae)

Correlations between an animal's morphology and ecological parameters such as habitat characteristics emphasize the intimate link between phenotype and the environment, but are often difficult to interpret because the functional consequences of morphological variation are frequently unknown. We provide one of the few studies relating limb morphology, functional capabilities, and habitat in reptiles. We tested the hypothesis that species occupying open microhabitats would possess relatively longer limbs and faster sprint speeds than those occurring in more closed microhabitats. A number of morphological characteristics relevant to locomotion were quantified, including the length of the bones of the fore- and hindlimbs and body size. A phylogenetic analysis was then used to examine the evolutionary relationships between morphology, locomotor performance and microhabitat openness in seven species of Niveoscincus and one species of the closely related genus Pseudemoia. A significant evolutionary relationship was established between sprinting ability, morphology, and the openness of the microhabitat occupied by a species. The phylogenetic analysis demonstrated an evolutionary trend in Niveoscincus of species occupying open microhabitats (e.g. N. greeni, N ocellatus) being large with long limbs and high sprinting ability, while those occupying closed microhabitats (e.g. N coventryi, P. entrecasteauxii) art smaller with short limbs and much slower maximum sprint speeds.     

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.     

A new karyological variant of Oecomys (Rodentia: Sigmodontinae) and its phylogenetic relationship based on molecular data.

A new karyological variant of the Sigmodontinae genus Oecomys was detected in specimens from Brazilian Pantanal. Karyologic analyses showed 2n = 72 and FN = 90, which differs from all known chromosomal complements of the genus. This new karyomorph showed distinctive morphological attributes and could not be attributed to any described Oecomys species. Molecular analysis using cytochrome-b sequence data suggested the monophyly of Oecomys. Maximum-likelihood analyses placed the Oecomys sp. haplotype clade as the sister branch to Oecomys bicolor, whereas maximum-parsimony analyses did not resolve its relationship with the other Oecomys species. Kimura's two parameters distance estimates between this and other Oecomys species are high, and active gene flow has been found not to coexist with these divergence estimates.     

The characterization of complete mitochondrial genome and phylogenetic relationship within Rattus genus (Rodentia: Muridae)

The genus Rattus is one of the main pest genus of rodent. Most species of the genus carry all kinds of pathogenic bacteria to human being. They are traditionally considered to be a least understood group. The complete mitochondrial genome of the White-Footed Indochinese Rat, Rattus nitidus was determined in this study. The characterization of mitochondrial genomes of Rattus genus was also analyzed based on comprehensive comparison. The result of evolutionary patterns of protein-coding genes (PCGs) suggested purifying selection was the predominant evolutionary forces in the mitochondrial genomes of Rattus genus. The NADH dehydrogenase 4 gene (ND4) showed a highly elevated Ka/Ks ratio compared to the other protein-coding genes, which indicated ND4 was most likely under relaxed selection pressure. Phylogenetic analysis provided a well-supported outline of Rattus genus, and revealed two groups in the genus. R. nitidus had a sister relationship with R. norvegicus.     

Morphological evolution and phylogenetic relationships of the European ground voles (Arvicolidae, Rodentia)

Brunet-Lecomte, P. & Chaline, J. 1991 01 15: Morphological evolution and phylogcnctic relationships of the European ground voles (Arvicolidae. Rodentia). Lethaia. Vol. 24. pp. 45–53. Oslo. ISSN 0024–1164. A new morphological study of the first lower molar M₁ of European Quaternary ground voles (Arvicolidac. Rodcntia. Microtus (Terricola)) by means of multivariate analysis renews the systematics. phylogenetic relationships and their evolutionary group history. An Allophaiomyan origin of ground voles has been confirmed and the evolution of Mediterranean and middle Europcan groups has now been clarified. Primitive species of middle European groups display plesiomorphics. except for M. (T.) arvalidens, which shows certain apomorphies of the present species. The occurrence of M. (T.) multiplex in France at the end of the middle Pleistocene before the appearance of M. (T.) suhterraneus completely reverses previous ideas which considered that M. (T.) multiplex was a sibling species derived from M. (T.) subterraneus during the Würmian glaciation. The Atlantic species M. (T.) pyrenaicus is probably derived from the middle Pleistocene species M. (T.) mariaclaudiue whose exact origin is unknown. M. (T.) sauii, M. (T.) tarentina. M. (T.) melirensis and M. (T.) henseli belong to the same geographic group. Perhaps M. (T.) savii derived from M. (T.) tarentina or shares the same ancestor with M. (T.) tarentina. M. (T.) duodecimcostarus probably indirectly derived from an Iberian specics of Allophuiomys such as A. chalinei, while M. (T.) lusitanicus was separated from M. (T.) duodecimcostutus about 60,000 years ago. A sketch of the stratigraphical records and geographical distribution of the Terricola species in Western Europe showing their phylogenetic relationships and migrations during the middle and upper Pleistocene is included. Morphometry, variance analysis, phylogeneric relationships. Mammalia. Rodentia. Arvicolidae. Microtus, Terricola.     

The phylogenetic position of "Acomyinae" (Rodentia, Mammalia) as sister group of a Murinae + Gerbillinae clade: evidence from the nuclear ribonuclease gene.

The phylogenetic relationships of Acomys and Uranomys within Muridae were investigated using nuclear pancreatic ribonuclease A gene sequences. The various kinds of substitutions in the data matrix (15 taxa x 375 nucleotides) were examined for saturation, in order to apply a weighted parsimony approach. Phylogenies were derived by maximum parsimony (weighted and unweighted) and maximum likelihood procedures, using a dormouse (Gliridae) as outgroup. Maximum likelihood gave the most robust results. All analyses cluster some traditional taxa with a strong robustness, such as three species of the genus Mus, two South-East Asian rats, and two genera in each of the gerbil and vole families. When analyzed with those of other murid rodents representing Murinae, Gerbillinae, Arvicolinae, Cricetinae, and Sigmodontinae, sequences of the ribonuclease gene suggest that Acomys and Uranomys constitute a monophyletic clade at the subfamily level, denoted "Acomyinae." The relationships between the six subfamilies of Muridae appear poorly resolved, except for a clade uniting Murinae, Acomyinae, and Gerbillinae. Within this clade, the sister group of Acomyinae could not be identified, as the branch length defining a Gerbillinae + Murinae cluster is extremely short. The poor resolution of our phylogenetic inferences is probably the result of two confounding factors, namely the limited size of the pancreatic ribonuclease sequence and the probable short time intervals during the radiation of the six murid subfamilies involved in this study.