Correction: Elevational Distribution and Ecology of Small Mammals on Tanzania's Second Highest Mountain.

[This corrects the article DOI: 10.1371/journal.pone.0162009.].

Tigray Orthohantavirus Infects Two Related Rodent Species Adapted to Different Elevations in Ethiopia.

Orthohantaviruses are RNA viruses that some members are known to cause severe zoonotic diseases in humans. Orthohantaviruses are hosted by rodents, soricomorphs (shrews and moles), and bats. Only two orthohantaviruses associated with murid rodents are known in Africa, Sangassou orthohantavirus (SANGV) in two species of African wood mice (Hylomyscus), and Tigray orthohantavirus (TIGV) in the Ethiopian white-footed rat (Stenocephalemys albipes). In this article, we report evidence that, like SANGV, two strains of TIGV occur in two genetically related rodent species, S. albipes and S. sp. A, occupying different elevational zones in the same mountain. Investigating the other members of the genus Stenocephalemys for TIGV could reveal the real diversity of TIGV in the genus.

The Complete Phylogeny of Pangolins: Scaling Up Resources for the Molecular Tracing of the Most Trafficked Mammals on Earth.

Pangolins, considered the most-trafficked mammals on Earth, are rapidly heading to extinction. Eight extant species of these African and Asian scale-bodied anteaters are commonly recognized, but their evolutionary relationships remain largely unexplored. Here, we present the most comprehensive phylogenetic assessment of pangolins, based on genetic variation of complete mitogenomes and 9 nuclear genes. We confirm deep divergence among Asian and African pangolins occurring not later than the Oligocene-Miocene boundary ca. 23 million years ago (Ma) (95% HPD = 18.7-27.2), limited fossil evidence suggesting dispersals from Europe. We recognize 3 genera including Manis (Asian pangolins), Smutsia (large African pangolins), and Phataginus (small African pangolins), which first diversified in the Middle-Upper Miocene (9.8-13.3 Ma) through a period of gradual cooling coinciding with a worldwide taxonomic diversification among mammals. Based on large mitogenomic distances among the 3 genera (18.3-22.8%) and numerous (18) morphological traits unique to Phataginus, we propose the subfamily Phatagininae subfam. nov. to designate small African pangolins. In contrast with the morphological-based literature, our results establish that the thick-tailed pangolin (Manis crassicaudata) is sister-species of the Sunda (Manis javanica) and Palawan (Manis culionensis) pangolins. Mitogenomic phylogenetic delineations supported additional pangolin species subdivisions (n = 13), including 6 African common pangolin (Phataginus tricuspis) lineages, but these patterns were not fully supported by our multi-locus approach. Finally, we identified more than 5000 informative mitogenomic sites and diagnostic variation from 5 nuclear genes among all species and lineages of pangolins, providing an important resource for further research and for effectively tracing the worldwide pangolin trade.

Assessing Monkeypox Virus Prevalence in Small Mammals at the Human-Animal Interface in the Democratic Republic of the Congo.

During 2012, 2013 and 2015, we collected small mammals within 25 km of the town of Boende in Tshuapa Province, the Democratic Republic of the Congo. The prevalence of monkeypox virus (MPXV) in this area is unknown; however, cases of human infection were previously confirmed near these collection sites. Samples were collected from 353 mammals (rodents, shrews, pangolins, elephant shrews, a potamogale, and a hyrax). Some rodents and shrews were captured from houses where human monkeypox cases have recently been identified, but most were trapped in forests and agricultural areas near villages. Real-time PCR and ELISA were used to assess evidence of MPXV infection and other Orthopoxvirus (OPXV) infections in these small mammals. Seven (2.0%) of these animal samples were found to be anti-orthopoxvirus immunoglobulin G (IgG) antibody positive (six rodents: two Funisciurus spp.; one Graphiurus lorraineus; one Cricetomys emini; one Heliosciurus sp.; one Oenomys hypoxanthus, and one elephant shrew Petrodromus tetradactylus); no individuals were found positive in PCR-based assays. These results suggest that a variety of animals can be infected with OPXVs, and that epidemiology studies and educational campaigns should focus on animals that people are regularly contacting, including larger rodents used as protein sources.

Reconstructing the molecular phylogeny of giant sengis (Macroscelidea; Macroscelididae; Rhynchocyon).

Giant sengis (Macroscelidea; Macroscelididae; Rhynchocyon), also known as giant elephant-shrews, are small-bodied mammals that range from central through eastern Africa. Previous research on giant sengi systematics has relied primarily on pelage color and geographic distribution. Because some species have complex phenotypic variation and large geographic ranges, we used molecular markers to evaluate the phylogeny and taxonomy of the genus, which currently includes four species: R. chrysopygus, R. cirnei (six subspecies), R. petersi (two subspecies), and R. udzungwensis. We extracted DNA from fresh and historical museum samples from all taxa except one R. cirnei subspecies, and we generated and analyzed approximately 4700 aligned nucleotides (2685 bases of mitochondrial DNA and 2019 bases of nuclear DNA) to reconstruct a molecular phylogeny. We genetically evaluate Rhynchocyon spp. sequences previously published on GenBank, propose that the captive R. petersi population in North American zoos is likely R. p. adersi, and suggest that hybridization among taxa is not widespread in Rhynchocyon. The DNA sample we have from the distinctive but undescribed giant sengi from the Boni forest of northern coastal Kenya is unexpectedly nearly identical to R. chrysopygus, which will require further study. Our analyses support the current morphology-based taxonomy, with each recognized species forming a monophyletic clade, but we propose elevating R. c. stuhlmanni to a full species.

Elevational Distribution and Ecology of Small Mammals on Tanzania's Second Highest Mountain.

Mt. Meru is Tanzania's second highest mountain and the ninth highest in Africa. The distribution and abundance of small mammals on this massif are poorly known. Here we document the distribution of shrews and rodents along an elevational gradient on the southeastern versant of Mt. Meru. Five sites were sampled with elevational center points of 1950, 2300, 2650, 3000, and 3600 m, using a systematic methodology of standard traps and pitfall lines, to inventory the shrews and rodents of the slope. Ten species of mammal were recorded, comprising 2 shrew and 8 rodent species with the greatest diversity for each group at 2300 m. No species previously unrecorded on Mt. Meru was observed. Two rodent genera that occur in nearby Eastern Arc Mountains (Hylomyscus and Beamys) were not recorded. The rodent Lophuromys verhageni and a recently described species of shrew, Crocidura newmarki, are the only endemic mammals on Mt. Meru, and were widespread across the elevational gradient. As in similar small mammal surveys on other mountains of Tanzania, rainfall positively influenced trap success rates for shrews, but not for rodents. This study provides new information on the local small mammal fauna of the massif, but numerous other questions remain to be explored. Comparisons are made to similar surveys of other mountains in Tanzania.

Diverse sampling of East African haemosporidians reveals chiropteran origin of malaria parasites in primates and rodents.

Phylogenies of parasites provide hypotheses on the history of their movements between hosts, leading to important insights regarding the processes of host switching that underlie modern-day epidemics. Haemosporidian (malaria) parasites lack a well resolved phylogeny, which has impeded the study of evolutionary processes associated with host-switching in this group. Here we present a novel phylogenetic hypothesis that suggests bats served as the ancestral hosts of malaria parasites in primates and rodents. Expanding upon current taxon sampling of Afrotropical bat and bird parasites, we find strong support for all major nodes in the haemosporidian tree using both Bayesian and maximum likelihood approaches. Our analyses support a single transition of haemosporidian parasites from saurian to chiropteran hosts, and do not support a monophyletic relationship between Plasmodium parasites of birds and mammals. We find, for the first time, that Hepatocystis and Plasmodium parasites of mammals represent reciprocally monophyletic evolutionary lineages. These results highlight the importance of broad taxonomic sampling when analyzing phylogenetic relationships, and have important implications for our understanding of key host switching events in the history of malaria parasite evolution.

A new species of the rodent genus Hylomyscus from Angola, with a distributional summary of the H. anselli species group (Muridae: Murinae: Praomyini).

A new species of Hylomyscus, H. heinrichorum, is described from mountains in western Angola. Based on morphological traits and cranial morphometry, the new species is assigned to the H. anselli species group and is hypothesized to be most closely related to H. anselli Bishop proper, a species named from Zambia. Members of both the H. anselli and H. denniae species groups occupy the Afromontane Biotic Zone, found in various mountain systems to the south and east of the Congo Basin. Evidence is reviewed that supports the independent radiation of these two species groups within montane forest from different Guineo-Congolian ancestral stocks.

Phylogeography and evolutionary history of the Crocidura olivieri complex (Mammalia, Soricomorpha): from a forest origin to broad ecological expansion across Africa.

BACKGROUND: This study aims to reconstruct the evolutionary history of African shrews referred to the Crocidura olivieri complex. We tested the respective role of forest retraction/expansion during the Pleistocene, rivers (allopatric models), ecological gradients (parapatric model) and anthropogenic factors in explaining the distribution and diversification within this species complex. We sequenced three mitochondrial and four nuclear markers from 565 specimens encompassing the known distribution of the complex, i.e. from Morocco to Egypt and south to Mozambique. We used Bayesian phylogenetic inference, genetic structure analyses and divergence time estimates to assess the phylogenetic relationships and evolutionary history of these animals. RESULTS: The C. olivieri complex (currently composed of C. olivieri, C. fulvastra, C. viaria and C. goliath) can be segregated into eight principal geographical clades, most exhibiting parapatric distributions. A decrease in genetic diversity was observed between central and western African clades and a marked signal of population expansion was detected for a broadly distributed clade occurring across central and eastern Africa and portions of Egypt (clade IV). The main cladogenesis events occurred within the complex between 1.37 and 0.48 Ma. Crocidura olivieri sensu stricto appears polyphyletic and C. viaria and C. fulvastra were not found to be monophyletic. CONCLUSIONS: Climatic oscillations over the Pleistocene probably played a major role in shaping the genetic diversity within this species complex. Different factors can explain their diversification, including Pleistocene forest refuges, riverine barriers and differentiation along environmental gradients. The earliest postulated members of the complex originated in central/eastern Africa and the first radiations took place in rain forests of the Congo Basin. A dramatic shift in the ecological requirements in early members of the complex, in association with changing environments, took place sometime after 1.13 Ma. Some lineages then colonized a substantial portion of the African continent, including a variety of savannah and forest habitats. The low genetic divergence of certain populations, some in isolated localities, can be explained by their synanthropic habits. This study underlines the need to revise the taxonomy of the C. olivieri complex.

Elevational distribution and ecology of small mammals on Africa's highest mountain.

Mt Kilimanjaro is Africa's highest mountain, and an icon for a country famous for its mammalian fauna. The distribution and abundance of small mammals on the mountain are poorly known. Here we document the distribution of shrews and rodents along an elevational gradient on the southeastern versant of Kilimanjaro. Five sites were sampled with elevational center points of 2000, 2500, 3000, 3500 and 4000 m, using a systematic methodology of standard traps and pitfall lines, to inventory the shrews and rodents of the slope. Sixteen species of mammal were recorded, including 6 shrew and 10 rodent species, and the greatest diversity of both was found at 3000 m, the elevational midpoint of the transect. No species previously unrecorded on Kilimanjaro were observed. Two genera of rodents that occur in nearby mountains (Hylomyscus and Beamys) were not recorded. Myosorex zinki, the only mammal endemic to Mt. Kilimanjaro, which previously was known by only a few specimens collected in the ericaceous or moorland habitat, was found in all but one (the lowest) of the sites sampled, and was one of the most widespread species of small mammal along the gradient. Two shrews (Crocidura allex and Sylvisorex granti) and one rodent (Dendromus insignis) were found throughout the entire transect, with Dendromus being observed at our highest trap point (4240 m). As in similar faunal surveys on other mountains of Tanzania, rainfall influenced the sample success of shrews, but not rodents. Trap success for rodents at 3500 m was notably low. This study contributes further justification for the conservation of the forest habitat of Mt. Kilimanjaro.

Expanded host diversity and geographic distribution of hantaviruses in sub-Saharan Africa.

The recent discovery of hantaviruses in shrews and bats in West Africa suggests that other genetically distinct hantaviruses exist in East Africa. Genetic and phylogenetic analyses of newfound hantaviruses, detected in archival tissues from the Geata mouse shrew (Myosorex geata) and Kilimanjaro mouse shrew ( Myosorex zinki) captured in Tanzania, expands the host diversity and geographic distribution of hantaviruses and suggests that ancestral shrews and/or bats may have served as the original mammalian hosts of primordial hantaviruses.

A new hero emerges: another exceptional mammalian spine and its potential adaptive significance.

The hero shrew's (Scutisorex somereni) massive interlocking lumbar vertebrae represent the most extreme modification of the vertebral column known in mammals. No intermediate form of this remarkable morphology is known, nor is there any convincing theory to explain its functional significance. We document a new species in the heretofore monotypic genus Scutisorex; the new species possesses cranial and vertebral features representing intermediate character states between S. somereni and other shrews. Phylogenetic analyses of DNA sequences support a sister relationship between the new species and S. somereni. While the function of the unusual spine in Scutisorex is unknown, it gives these small animals incredible vertebral strength. Based on field observations, we hypothesize that the unique vertebral column is an adaptation allowing these shrews to lever heavy or compressive objects to access concentrated food resources inaccessible to other animals.

A cryptic new species of Miniopterus from south-eastern Africa based on molecular and morphological characters.

Resolving species limits within the genus Miniopterus has traditionally been complicated by the presence of cryptic species with overlapping morphological features. We use molecular techniques, cranio-dental characters and tragus shape to describe a new species of Miniopterus from Mozambique, M. mossambicus. Miniopterus mossambicus shows > 12% divergence in cytochrome-b sequence from its nearest congeners (the Malagasy M. gleni and M. griveaudi) and > 15% divergence from the morphologically similar M. natalensis, M. fraterculus and M. minor (all of which occur in southern and eastern Africa). There is considerable overlap in cranio-dental characters of the southern African species, particularly M. natalensis and M. mossambicus. However, tragus shape and multivariate comparisons of skull measurements can be used to separate these species. Based on morphological comparisons of museum specimens, this species may also be present in neighbouring Malawi and Zimbabwe, suggesting that it is probably distributed widely in south-central Africa. 

Morphological systematics of the kipunji (Rungwecebus kipunji) and the ontogenetic development of phylogenetically informative characters in the Papionini.

Since its discovery and description, the systematic position of the kipunji (Rungwecebus kipunji) has been a matter of debate. Although it was first placed in the mangabey genus Lophocebus, subsequent molecular studies indicated that the kipunji is most closely related to baboons (Papio). However, the kipunji does not appear to possess cranial features typical of Papio, thus necessitating the erection of a new genus, Rungwecebus. The recovery of an M2-stage subadult male kipunji voucher specimen, in addition to the original M1-stage subadult male voucher specimen, has since allowed further study. Here, we describe the craniodental morphology of the newly acquired kipunji specimen and present a phylogenetic analysis of Rungwecebus craniodental morphology using quantitative and qualitative characters. We examined the skulls of 76 M1- and M2-stage subadult males representing all extant papionin genera, taking note of character states that are static throughout ontogeny. To control for ontogenetic changes, only those characters expressing unchanged character states between subadult and adult specimens were coded for Rungwecebus and entered into a larger, recently published 151-character matrix of adult male morphology. To account for allometry, the narrow allometric coding method and the general allometric coding method were applied. The resulting most parsimonious trees suggest that Rungwecebus is phylogenetically closest to Lophocebus, a result consistent with initial morphological descriptions. However, due to the large amount of missing data for Rungwecebus, there are low bootstrap support values associated with any relationships within the larger Theropithecus/Papio/Lophocebus/Rungwecebus grouping. Taken in combination with previous molecular, phenetic, and ecological studies, the results of this study suggest that Rungwecebus is best regarded as a distinct genus closely related to Papio, Lophocebus, and Theropithecus. Adult morphological specimens are necessary to fully understand the adult kipunji morphotype, and its phylogenetic position will only be more precisely resolved with additional morphological and molecular data.

The biogeography of introgression in the critically endangered African monkey Rungwecebus kipunji.

In the four years since its original description, the taxonomy of the kipunji (Rungwecebus kipunji), a geographically restricted and critically endangered African monkey, has been the subject of much debate, and recent research suggesting that the first voucher specimen of Rungwecebus has baboon mitochondrial DNA has intensified the controversy. We show that Rungwecebus from a second region of Tanzania has a distinct mitochondrial haplotype that is basal to a clade containing all Papio species and the original Rungwecebus voucher, supporting the placement of Rungwecebus as the sister taxon of Papio and its status as a separate genus. We suggest that the Rungwecebus population in the Southern Highlands has experienced geographically localized mitochondrial DNA introgression from Papio, while the Ndundulu population retains the true Rungwecebus mitochondrial genome.

The biogeography of Miniopterus bats (Chiroptera: Miniopteridae) from the Comoro Archipelago inferred from mitochondrial DNA.

The endemic fauna of the Comoro Archipelago is composed of a mixture of taxa originating from Africa and Madagascar. Bats are the only native land dwelling mammals on this archipelago, but the biogeographical origins for the vast majority of species within this group are ambiguous. We report here genetic analyses based on two mitochondrial DNA markers to infer the origin of Comorian bats belonging to a reputed species complex of Miniopterus that is further distributed across Africa and Madagascar. Phylogenetic reconstructions show that east African M. minor are not closely related to the insular Miniopterus of Madagascar and the Comoros (Grande Comore and Anjouan). The latter cluster into two distinct, monophyletic clades (Clade 1 and Clade 2). Representatives of these clades occur sympatrically both on the Comoros and on Madagascar, and are distinguished by a large genetic distance (K2P: 9.9% for cytochrome b). No haplotypes are shared between any islands, suggesting the absence of contemporary gene flow. Populations of the widespread Clade 1 are furthermore characterized by a significant inter-island structure (Phi(CT) = 0.249), and by high haplotype and nucleotide diversities (h = 0.90-0.98, pi = 0.04-0.06). Demographic analyses of Clade 1 suggest secondary contact between two distinct phylogroups (Subclade 1 A and 1B) that reached Grande Comore and Anjouan, and a large, stable population with a long evolutionary history on Madagascar. These results and the current distribution of related lineages suggest that the Comoros were colonized independently at least two or three times by ancestors from Madagascar.

A new genus of African monkey, Rungwecebus: morphology, ecology, and molecular phylogenetics.

A new species of African monkey, Lophocebus kipunji, was described in 2005 based on observations from two sites in Tanzania. We have since obtained a specimen killed by a farmer on Mount Rungwe, the type locality. Detailed molecular phylogenetic analyses of this specimen demonstrate that the genus Lophocebus is diphyletic. We provide a description of a new genus of African monkey and of the only preserved specimen of this primate. We also present information on the animal's ecology and conservation.