Late Pleistocene Expansion of Small Murid Rodents across the Palearctic in Relation to the Past Environmental Changes.

We investigated the evolutionary history of the striped field mouse to identify factors that initiated its past demographic changes and to shed light on the causes of its current genetic structure and trans-Eurasian distribution. We sequenced mitochondrial cyt b from 184 individuals, obtained from 35 sites in central Europe and eastern Mongolia. We compared genetic analyses with previously published historical distribution models and data on environmental and climatic changes. The past demographic changes displayed similar population trends in the case of recently expanded clades C1 and C3, with the glacial (MIS 3-4) expansion and postglacial bottleneck preceding the recent expansion initiated in the late Holocene and were related to environmental changes during the upper Pleistocene and Holocene. The past demographic trends of the eastern Asian clade C3 were correlated with changes in sea level and the formation of new land bridges formed by the exposed sea shelf during the glaciations. These data were supported by reconstructed historical distribution models. The results of our genetic analyses, supported by the reconstruction of the historical spatial distributions of the distinct clades, confirm that over time the local populations mixed as a consequence of environmental and climatic changes resulting from cyclical glaciation and the interglacial period during the Pleistocene.

Molecular systematics and biogeographic history of the African climbing-mouse complex (Dendromus).

Climbing mice in the genus Dendromus (sensu lato) are widely distributed in Africa, south of the Saharan Desert. The 17 currently recognized species in the genus range from widespread taxa to single-mountain endemics, and there is considerable variation across species with respect to habitats occupied. These habitats range from arid grasslands and savannahs to sub-alpine and alpine vegetation. Using the most comprehensive geographic and genetic survey to date and after reviewing many type specimens, we assess the systematics and biogeography of Dendromus. Given the structure of our molecular phylogenetic hypotheses, in which we recover six major clades, we propose the recognition of three genera within the Dendromus group (sensu lato): in addition to Dendromus (26 lineages), we suggest the retention of Megadendromus (monotypic) and the resurrection of the genus Poemys (six lineages). From our model-based molecular phylogenetic results and morphological comparisons, we suggest that six formerly synonymized taxa should be resurrected, and we highlight 14 previously undescribed lineages. We also constructed time-calibrations on our phylogeny, and performed ancestral area reconstructions using BioGeoBEARS. Based on fossil evidence, Dendromus appears to have had a widespread African distribution dating back to the Late Miocene (8-10 Ma), and our basal ancestral area reconstruction (Ethiopians Highlands + Eastern African Mountains + Zambezian region) supports this. Divergence of the six major clades we recover (Poemys, Megadendromus and four within Dendromus) occurred prior to or at the Miocene-Pliocene boundary 5.3 Ma. Biogeographically, Megadendromus is restricted to the Ethiopian Highlands. The ancestral area for Poemys is reconstructed as the Zambezian region, with species distributions ranging from South Africa to Western Africa. The ancestral area for Dendromus is reconstructed as the Ethiopian Highlands, with the ancestral areas of the four major clades being reconstructed as Ethiopian Highlands, Albertine Rift, South Africa or Western Africa. None of the four Dendromus clades are reciprocally monophyletic with respect to distributional area.

Australian Rodents Reveal Conserved Cranial Evolutionary Allometry across 10 Million Years of Murid Evolution.

AbstractAmong vertebrates, placental mammals are particularly variable in the covariance between cranial shape and body size (allometry), with rodents being a major exception. Australian murid rodents allow an assessment of the cause of this anomaly because they radiated on an ecologically diverse continent notably lacking other terrestrial placentals. Here, we use 3D geometric morphometrics to quantify species-level and evolutionary allometries in 38 species (317 crania) from all Australian murid genera. We ask whether ecological opportunity resulted in greater allometric diversity compared with other rodents or whether conserved allometry suggests intrinsic constraints and/or stabilizing selection. We also assess whether cranial shape variation follows the proposed rule of craniofacial evolutionary allometry (CREA), whereby larger species have relatively longer snouts and smaller braincases. To ensure we could differentiate parallel versus nonparallel species-level allometric slopes, we compared the slopes of rarefied samples across all clades. We found exceedingly conserved allometry and CREA-like patterns across the 10-million-year split between Mus and Australian murids. This could support both intrinsic-constraint and stabilizing-selection hypotheses for conserved allometry. Large-bodied frugivores evolved faster than other species along the allometric trajectory, which could suggest stabilizing selection on the shape of the masticatory apparatus as body size changes.

Genomes, expression profiles, and diversity of mitochondria of the White-footed Deermouse Peromyscus leucopus, reservoir of Lyme disease and other zoonoses.

The cricetine rodents Peromyscus leucopus and P. maniculatus are key reservoirs for several zoonotic diseases in North America. We determined the complete circular mitochondrial genome sequences of representatives of 3 different stock colonies of P. leucopus, one stock colony of P. maniculatus and two wild populations of P. leucopus. The genomes were syntenic with that of the murids Mus musculus and Rattus norvegicus. Phylogenetic analysis confirmed that these two Peromyscus species are sister taxa in a clade with P. polionotus and also uncovered a distinction between P. leucopus populations in the eastern and the central United States. In one P. leucopus lineage four extended regions of mitochondrial pseudogenes were identified in the nuclear genome. RNA-seq analysis revealed transcription of the entire genome and differences from controls in the expression profiles of mitochondrial genes in the blood, but not in liver or brain, of animals infected with the zoonotic pathogen Borrelia hermsii. PCR and sequencing of the D-loop of the mitochondrion identified 32 different haplotypes among 118 wild P. leucopus at a Connecticut field site. These findings help to further establish P. leucopus as a model organism for studies of emerging infectious diseases, ecology, and in other disciplines.

First levantine fossil murines shed new light on the earliest intercontinental dispersal of mice.

Recent extensive field prospecting conducted in the Upper Miocene of Lebanon resulted in the discovery of several new fossiliferous localities. One of these, situated in the Zahleh area (Bekaa Valley, central Lebanon) has yielded a particularly diverse vertebrate fauna. Micromammals constitute an important part of this assemblage because not only do they represent the first Neogene rodents and insectivores from Lebanon, but they are also the only ones from the early Late Miocene of the Arabian Peninsula and circumambient areas. Analyses of the murines from Zahleh reveal that they belong to a small-sized early Progonomys, which cannot be assigned to any of the species of the genus hitherto described. They are, thereby, shown to represent a new species: Progonomys manolo. Morphometric analyses of the outline of the first upper molars of this species suggest a generalist and omnivorous diet. This record sheds new light onto a major phenomenon in the evolutionary history of rodents, which is the earliest dispersal of mice. It suggests that the arrival of murines in Africa got under way through the Levant rather than via southern Europe and was monitored by the ecological requirements of Progonomys.

Fossils know it best: Using a new set of fossil calibrations to improve the temporal phylogenetic framework of murid rodents (Rodentia: Muridae).

Murid rodents (Rodentia: Muridae) represent the most diverse and abundant mammalian family. In this study, we provide a refined set of fossil calibrations which is used to reconstruct a dated phylogeny of the family using a multilocus dataset (six nuclear and nine mitochondrial gene fragments) encompassing 161 species representing 82 murid genera from four extant subfamilies (Deomyinae, Gerbillinae, Lophiomyinae and Murinae). In comparison with previous studies on murid or muroid rodents, our work stands out for the implementation of nine robust fossil constraints within the Muridae thanks to a thorough review of the fossil record. Before being assigned to specific nodes of the phylogeny, all potential fossil constraints were carefully assessed; they were also subjected to several cross-validation analyses. The resulting phylogeny is consistent with previous phylogenetic studies on murids, and recovers the monophyly of all sampled murid subfamilies and tribes. Based on nine controlled fossil calibrations, our inferred temporal timeframe indicates that the murid family likely originated in the course of the Early Miocene, 22.0-17.0 million years ago (Ma), and that most major lineages (i.e. tribes) started diversifying ca. 10 Ma. Historical biogeography analyses support the tropical origin for the family, with an initial internal split (vicariance event) between Afrotropical and Oriental (Indomalaya and Philippines) lineages. During the course of their diversification, the biogeographic pattern of murids is marked by several dispersal events toward the Australasian and the Palearctic regions. The Afrotropical region was also secondarily colonized at least three times from the Indomalaya, indicating that the latter region has acted as a major centre of diversification for the family.

Adaptive Transcriptome Profiling of Subterranean Zokor, Myospalax baileyi, to High- Altitude Stresses in Tibet.

Animals living at high altitudes have evolved distinct phenotypic and genotypic adaptations against stressful environments. We studied the adaptive patterns of altitudinal stresses on transcriptome turnover in subterranean plateau zokors (Myospalax baileyi) in the high-altitude Qinghai-Tibetan Plateau. Transcriptomes of zokors from three populations with distinct altitudes and ecologies (Low: 2846 m, Middle: 3282 m, High: 3,714 m) were sequenced and compared. Phylogenetic and principal component analyses classified them into three divergent altitudinal population clusters. Genetic polymorphisms showed that the population at H, approaching the uppermost species boundary, harbors the highest genetic polymorphism. Moreover, 1056 highly up-regulated UniGenes were identified from M to H. Gene ontologies reveal genes like EPAS1 and COX1 were overexpressed under hypoxia conditions. EPAS1, EGLN1, and COX1 were convergent in high-altitude adaptation against stresses in other species. The fixation indices (F ST and G ST )-based outlier analysis identified 191 and 211 genes, highly differentiated among L, M, and H. We observed adaptive transcriptome changes in Myospalax baileyi, across a few hundred meters, near the uppermost species boundary, regardless of their relatively stable underground burrows' microclimate. The highly variant genes identified in Myospalax were involved in hypoxia tolerance, hypercapnia tolerance, ATP-pathway energetics, and temperature changes.

Consequences of Secondary Calibrations on Divergence Time Estimates.

Secondary calibrations (calibrations based on the results of previous molecular dating studies) are commonly applied in divergence time analyses in groups that lack fossil data; however, the consequences of applying secondary calibrations in a relaxed-clock approach are not fully understood. I tested whether applying the posterior estimate from a primary study as a prior distribution in a secondary study results in consistent age and uncertainty estimates. I compared age estimates from simulations with 100 randomly replicated secondary trees. On average, the 95% credible intervals of node ages for secondary estimates were significantly younger and narrower than primary estimates. The primary and secondary age estimates were significantly different in 97% of the replicates after Bonferroni corrections. Greater error in magnitude was associated with deeper than shallower nodes, but the opposite was found when standardized by median node age, and a significant positive relationship was determined between the number of tips/age of secondary trees and the total amount of error. When two secondary calibrated nodes were analyzed, estimates remained significantly different, and although the minimum and median estimates were associated with less error, maximum age estimates and credible interval widths had greater error. The shape of the prior also influenced error, in which applying a normal, rather than uniform, prior distribution resulted in greater error. Secondary calibrations, in summary, lead to a false impression of precision and the distribution of age estimates shift away from those that would be inferred by the primary analysis. These results suggest that secondary calibrations should not be applied as the only source of calibration in divergence time analyses that test time-dependent hypotheses until the additional error associated with secondary calibrations is more properly modeled to take into account increased uncertainty in age estimates.

Repeated evolution of carnivory among Indo-Australian rodents.

Convergent evolution, often observed in island archipelagos, provides compelling evidence for the importance of natural selection as a generator of species and ecological diversity. The Indo-Australian Archipelago (IAA) is the world's largest island system and encompasses distinct biogeographic units, including the Asian (Sunda) and Australian (Sahul) continental shelves, which together bracket the oceanic archipelagos of the Philippines and Wallacea. Each of these biogeographic units houses numerous endemic rodents in the family Muridae. Carnivorous murids, that is those that feed on animals, have evolved independently in Sunda, Sulawesi (part of Wallacea), the Philippines, and Sahul, but the number of origins of carnivory among IAA murids is unknown. We conducted a comprehensive phylogenetic analysis of carnivorous murids of the IAA, combined with estimates of ancestral states for broad diet categories (herbivore, omnivore, and carnivore) and geographic ranges. These analyses demonstrate that carnivory evolved independently four times after overwater colonization, including in situ origins on the Philippines, Sulawesi, and Sahul. In each biogeographic unit the origin of carnivory was followed by evolution of more specialized carnivorous ecomorphs such as vermivores, insectivores, and amphibious rats.

Genetic diversity and genetic structure of the striped field mouse Apodemus agrarius coreae (Muridae, Rodentia) in Korea.

The aim of this study was to investigate the genetic diversity and genetic structure of the striped field mouse Apodemus agrarius coreae in Korea. The Korean A. a. coreae is characterized by high levels of haplotype diversity (Hd=0.967) and low levels of nucleotide diversity (π=0.00683). Haplogroup 1 is well separated from the haplotypes of the neighboring regions of the Korean Peninsula, while the other haplogroups are closely related to those from the Russian Far East. Thus, further investigations are required to confirm the validity of the subspecies status of A. a. coreae by implementing additional morphological characters as well as genetic data from the populations present in the Korean Peninsula and its neighboring countries. Haplogroup 1 includes most Korean haplotypes and forms a star-like haplotype network structure, which reveals relatively low levels of sequence divergence and high frequency of unique mutations (only few mutations are shared in most of the haplotype nodes). The results indicate that the haplotypes of Haplogroup 1 might have experienced population expansion since their migration into Korea, which was further corroborated with negative results of neutrality tests for Korean population of A. a. coreae.

Convergent evolution of aquatic foraging in a new genus and species (Rodentia: Muridae) from Sulawesi Island, Indonesia.

The island of Sulawesi, in Indonesia, lies at the crossroads of the Indo-Australian Archipelago and has remained isolated from the Asian (Sunda) and Australian (Sahul) continental shelves for at least the last 10 million years. Of the 50 native species of rodents on Sulawesi, all are endemic and represent the evolution of a variety of ecological and morphological forms within the Muridae and Sciuridae. Carnivorous rodents have evolved, perhaps independently, in Muridae from the Philippines, Sulawesi, and Sahul, but semi-aquatic murids are only known from Sahul. Here we describe a new genus and species of insectivorous water rat from Sulawesi. Phylogenetic analyses demonstrate that it is related to the shrew rats of Sulawesi and represents an origin of aquatic carnivory that is independent from the evolution of water rats on Sahul. Many areas of Sulawesi have not been surveyed systematically and current lists of mammal species are likely to dramatically underestimate actual diversity.

Molecular genetic evidence for the place of origin of the Pacific rat, Rattus exulans.

Commensal plants and animals have long been used to track human migrations, with Rattus exulans (the Pacific rat) a common organism for reconstructing Polynesian dispersal in the Pacific. However, with no knowledge of the homeland of R. exulans, the place of origin of this human-commensal relationship is unknown. We conducted a mitochondrial DNA phylogeographic survey of R. exulans diversity across the potential natural range in mainland and Island Southeast Asia in order to establish the origin of this human-commensal dyad. We also conducted allozyme electrophoresis on samples from ISEA to obtain a perspective on patterns of genetic diversity in this critical region. Finally, we compared molecular genetic evidence with knowledge of prehistoric rodent faunas in mainland and ISEA. We find that ISEA populations of R. exulans contain the highest mtDNA lineage diversity including significant haplotype diversity not represented elsewhere in the species range. Within ISEA, the island of Flores in the Lesser Sunda group contains the highest diversity in ISEA (across all loci) and also has a deep fossil record of small mammals that appears to include R. exulans. Therefore, in addition to Flores harboring unusual diversity in the form of Homo floresiensis, dwarfed stegodons and giant rats, this island appears to be the homeland of R. exulans.

Susceptibility of muridae cell lines to ecotropic murine leukemia virus and the cationic amino acid transporter 1 viral receptor sequences: implications for evolution of the viral receptor.

Ecotropic murine leukemia viruses (Eco-MLVs) infect mouse and rat, but not other mammalian cells, and gain access for infection through binding the cationic amino acid transporter 1 (CAT1). Glycosylation of the rat and hamster CAT1s inhibits Eco-MLV infection, and treatment of rat and hamster cells with a glycosylation inhibitor, tunicamycin, enhances Eco-MLV infection. Although the mouse CAT1 is also glycosylated, it does not inhibit Eco-MLV infection. Comparison of amino acid sequences between the rat and mouse CAT1s shows amino acid insertions in the rat protein near the Eco-MLV-binding motif. In addition to the insertion present in the rat CAT1, the hamster CAT1 has additional amino acid insertions. In contrast, tunicamycin treatment of mink and human cells does not elevate the infection, because their CAT1s do not have the Eco-MLV-binding motif. To define the evolutionary pathway of the Eco-MLV receptor, we analyzed CAT1 sequences and susceptibility to Eco-MLV infection of other several murinae animals, including the southern vole (Microtus rossiaemeridionalis), large Japanese field mouse (Apodemus speciosus), and Eurasian harvest mouse (Micromys minutus). Eco-MLV infection was enhanced by tunicamycin in these cells, and their CAT1 sequences have the insertions like the hamster CAT1. Phylogenetic analysis of mammalian CAT1s suggested that the ancestral CAT1 does not have the Eco-MLV-binding motif, like the human CAT1, and the mouse CAT1 is thought to be generated by the amino acid deletions in the third extracellular loop of CAT1.

Mitochondrial genome of bamboo rat Rhizomys pruinosus.

Abstract Bamboo rats are a group of subterranean rodents some of which feed on the roots and shoots of bamboo and other plants. In this study, we sequence the mitochondrial genome of a hoary bamboo rat Rhizomys pruinosus from the south of China. The genome is 16,575 bp in length, and had a gene content of 13 protein coding, 22 tRNAs and 2 rRNAs. The overall base composition is 30.94% T, 24.83% C, 32.21% A and 12.02% G, with an A+T bias of 63.15%. The cytochrome genes were the most conservative genes compared with plateau zokor (Eospalax baileyi) and blind mole rats (Spalax carmeli) in the family Spalacidae. These mitochondrial data are potentially important for the study of molecular evolution, conservation genetics, agricultural technology and epidemiology.

Is Leopoldamys neilli (Rodentia, Muridae) a synonym of Leopoldamys herberti? A reply to Balakirev et al. (2013).

Recently, Balakirev et al. (2013) presented a taxonomic revision of the genus Leopoldamys based on phylogenetic analyses. They identified five main Leopoldamys genetic lineages and suggested to rename several of them. According to these authors, the genetic lineage previously thought to belong to L. edwardsi (lineage L1) should be assigned to L. revertens while L. neilli (lineage L2) should be considered as a junior synonym of L. herberti. Using molecular and morphological data from a large sampling of Leopoldamys specimens, the aim of the present study was to investigate the taxonomic status of L. herberti and L. neilli. This study reveals that, contrary to Balakirev et al.'s statement, both genetic lineages L1 and L2 occur in Nakhon Ratchasima Province, close to the type locality of L. herberti. We also show that the external measurements and color pattern of L. herberti are highly similar to those of L1 specimens but are not consistent with the morphology of L2 specimens. Therefore these results strongly suggest that L. herberti should be assigned to the genetic lineage L1. Consequently L. neilli should not be considered as a junior synonym of L. herberti and this study confirms that the appropriate name of the genetic lineage L2 is L. neilli. Moreover, as our results show that L. herberti should be assigned to the lineage L1, this name has nomenclatural priority over L. revertens, the species name suggested by Balakirev et al. (2013) for this lineage.

The taxonomic position of Tonkinomys daovantieni (Rodentia: Muridae) based on karyological and molecular data.

Tonkinomys daovantieni was recently described from Northern Vietnam, but very sparse information exists for the taxon. We report for the first time the karyotype of this species and investigate its phylogenetic position in the Dacnomys division using both mitochondrial and nuclear genetic data. The diploid chromosome number of the species is 2n=44. This chromosomal set consists of one submetacentric pair, one metacentric pair, and nineteen pairs of subtelocentric/acrocentric autosomes progressively decreasing in size. The X chromosome is submetacentric and approximately equal in size to the largest subtelocentric autosome. The Y chromosome is metacentric and equal in size to the smallest pair of autosomes. The phylogenetic reconstruction based on the Cyt b COI and GHR genes reveals that Saxotilomys paulinae, a species distributed in the karst formations of the Lao PDR, is the closest relative to T. daovantieni. These two taxa are similar not only in a number of morphological characters, but also in their major ecological preferences (both are petrophylic species associated with limestone karst formations). Based on our data, we can conclude that the similarities among the ecological adaptations, natural conditions and habitat preferences of these species are a reflection of their phylogenetic relationship.

Revision of the genus Leopoldamys (Rodentia, Muridae) as inferred from morphological and molecular data, with a special emphasis on the species composition in continental Indochina.

A revision of the genus Leopoldamys is presented, and both the species composition and distribution in Indochina and Sundaic regions is reinvestigated. The phylogeny of the genus is recovered based on Cyt b, COI, and IRBP gene analyses. Five basal and 16 secondary monophyletic phylogenetic lineages were identified. A taxonomic reassessment of the continental and Sundaic populations is performed based on morphological verification of the genetically defined clades. Six clades were recovered in the phylogenetic analyses and correspond to morphologically defined species: L. revertens (distributed in lowlands of eastern and central Indochina), L. herberti (western and central Indochina, northward to northern Vietnam), L. edwardsi (China and northern Vietnam, northward of 21 degrees N), L. milleti (endemic of Dalat Plateau, southern Vietnam), L. sabanus (Borneo), and L. vociferans (lowlands of the Malacca Peninsula, northward to southwestern Thailand). The absence of proper L. sabanus in continental Indochina is revealed. The substitute name for the species known from the majority of Indochina under the name of L. sabanus should be L. revertens. The name L. neilli, which has been ascribed to populations from Thailand and Vietnam, is a junior synonym of L. herberti. Two related but rather divergent clades are found in Sumatra and the Malacca Peninsula. Based on their considerable genetic distances, these forms should be regarded as separate species from the L. sabanus type-bearing populations of Borneo, or as the members of L. sabanus polytypic superspecies. The substitute name for the lineage-bearing taxon from Malacca should be L. vociferans. The continental populations of Leopoldamys can be distinguished from each other by external and cranial characters and may be subdivided into four species. Two of these species (L. revertens and L. milleti) are well distinguished by external and cranial morphology, whereas the other two species (L. herberti and L. edwardsi) may be treated as sibling species that are difficult to distinguish based on morphological characters.

The complete mitochondrial genome of the large white-bellied rat, Niviventer excelsior (Rodentia: Muridae).

The first complete mitochondrial genome of the large white-bellied rat (Niviventer excelsior) was sequenced and annotated in order to provide a source of phylogenetic characters including an assessment of gene order arrangement. The mitochondrial genome sequence (16,298 bp) of N. excelsior contains 13 protein-coding, 2 rRNA and 22 tRNA genes as well as 1 typical control region (D-Loop), which are shared by other mammalian mitochondrial genomes. The codon usage also followed the typical vertebrate pattern except for an unusual CCA stop codon, which was termination codon of Cyt b. The 16 nucleotide insertion was detected in the central conserved domain of d-Loop. The 12 heavy-strand encoded protein-coding genes were used to reconstruct the phylogenetic relationships by the Bayesian inference and maximum likelihood methods. Topologies revealed that N. excelsior clustered together with the species in genus Rattus, indicating their closer phylogenetic relationship.