Evolutionary Insights from a Genetically Divergent Hantavirus Harbored by the European Common Mole (Talpa europaea)

Background

The discovery of genetically distinct hantaviruses in shrews (Order Soricomorpha, Family Soricidae) from widely separated geographic regions challenges the hypothesis that rodents (Order Rodentia, Family Muridae and Cricetidae) are the primordial reservoir hosts of hantaviruses and also predicts that other soricomorphs harbor hantaviruses. Recently, novel hantavirus genomes have been detected in moles of the Family Talpidae, including the Japanese shrew mole (Urotrichus talpoides) and American shrew mole (Neurotrichus gibbsii). We present new insights into the evolutionary history of hantaviruses gained from a highly divergent hantavirus, designated Nova virus (NVAV), identified in the European common mole (Talpa europaea) captured in Hungary.

Methodology/Principal Findings

Pair-wise alignment and comparison of the full-length S- and L-genomic segments indicated moderately low sequence similarity of 54–65% and 46–63% at the nucleotide and amino acid levels, respectively, between NVAV and representative rodent- and soricid-borne hantaviruses. Despite the high degree of sequence divergence, the predicted secondary structure of the NVAV nucleocapsid protein exhibited the characteristic coiled-coil domains at the amino-terminal end, and the L-segment motifs, typically found in hantaviruses, were well conserved. Phylogenetic analyses, using maximum-likelihood and Bayesian methods, showed that NVAV formed a distinct clade that was evolutionarily distant from all other hantaviruses.

Conclusions

Newly identified hantaviruses harbored by shrews and moles support long-standing virus-host relationships and suggest that ancestral soricomorphs, rather than rodents, may have been the early or original mammalian hosts.     

Cryptic diversity in forest shrews of the genus Myosorex from southern Africa,with the description of a new species and comments on Myosorex tenuis

Forest or mouse shrews (Myosorex) represent a small but important radiation of African shrews generally adapted to montane and/or temperate conditions. The status of populations from Zimbabwe, Mozambique, and the north of South Africa has long been unclear because of the variability of traits that have traditionally been ‘diagnostic’ for the currently recognized South African taxa. We report molecular (mitochondrial DNA and nuclear DNA), craniometric, and morphological data from newly collected series of Myosorex from Zimbabwe (East Highlands), Mozambique (Mount Gorogonsa, Gorongosa National Park), and the Limpopo Province of South Africa (Soutpansberg Range) in the context of the available museum collections from southern and eastern Africa and published DNA sequences. Molecular data demonstrate close genetic similarity between populations from Mozambique and Zimbabwe, and this well‐supported clade (herein described as a new species, M yosorex meesteri sp. nov. ) is the sister group of all South African taxa, except for Myosorex longicaudatus Meester & Dippenaar, 1978. Populations of Myosorex in Limpopo Province (herein tentatively assigned to Myosorex cf. tenuis) are cladistically distinct from both Myosorex varius (Smuts, 1832) and Myosorex cafer (Sundevall, 1846), and diverged from M. varius at approximately the same time (2.7 Mya) as M. cafer and Myosorex sclateri Thomas & Schwann, 1905 diverged (2.4 Mya). Morphometric data are mostly discordant with the molecular data. For example, clearly distinct molecular clades overlap considerably in craniometric variables. On the other hand, extreme size differentiation occurs between genetically closely related populations in the Soutpansberg Range, which coincides with the bissection of the mountain range by the dry Sand River Valley, indicating the potential for strong intraspecific phenotypic divergence in these shrews. © 2013 The Linnean Society of London     

Biogeography and diversity among montane populations of mouse shrew (Soricidae: Myosorex) in Tanzania

We assess variation in morphological and molecular characters among three species of Myosorex (the mouse shrew) –Myosorex geata, Myosorex kihaulei, and Myosorex zinki– as a means to test previously proposed biogeographic hypotheses for Tanzanian ‘sky islands’ and systematic hypotheses for Tanzanian mouse shrews. We analyse 17 cranial and dental variables using multivariate statistics and perform phylogenetic and phylogeographic analyses on sequences of mitochondrial and nuclear DNA; samples are drawn from every known Tanzanian population of Myosorex. Morphometric and phylogenetic analyses reveal that M. zinki is distinct, but that currently isolated populations of M. geata and M. kihaulei are relatively similar to one another, and may not have been isolated over geological time scales. Analyses of molecular variance identify statistically significant, but limited, genetic variation within and between isolated populations of M. geata and M. kihaulei. Between two putative regional biogeographic boundaries, greater genetic variation is explained by grouping populations on either side of the Ruaha River than by grouping populations on either side of the Makambako Gap. Our results are in agreement with recent studies illustrating the close relationship between faunas of the Southern Highlands and southern Eastern Arc Mountains, diminishing the apparent importance of the Makambako Gap as a historical biogeographic barrier. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100 , 669–680.     

South African mouse shrews (<Emphasis Type="Italic">Myosorex</Emphasis>) feel the heat: using species distribution models (SDMs) and IUCN Red List criteria to flag extinction risks due to climate change

Five species of mouse or forest shrews (Myosorex) are endemic to South Africa, Lesotho and Swaziland, four of which (Myosorex varius, Myosorex cafer, Myosorex longicaudatus and Myosorex cf. tenuis) are associated with montane or temperate grassland, fynbos and/or forest habitats while a fifth (Myosorex sclateri) is associated with lowland subtropical forests. Due to their small size, specialised habitat, low dispersal capacity, high metabolism and sensitivity to temperature extremes, we predicted that, particularly for montane species, future climate change should have a negative impact on area of occupancy (AOO) and ultimately extinction risks. Species distribution models (SDMs) indicated general declines in AOO of three species by 2050 under the A1b and A2 climate change scenarios (M. cafer, M. varius, M. longicaudatus) while two species (M. sclateri and M. cf. tenuis) remained unchanged (assuming no dispersal) or increased their AOO (assuming dispersal). While temperate species such as M. varius appear to be limited by temperature maxima (preferring cooler temperatures), the subtropical species M. sclateri appears to be limited by temperature minima (preferring warmer temperatures). Evidence for declines in AOO informed the uplisting (to a higher category of threat) of the Red List status of four Myosorex species to either vulnerable or endangered as part of a separate regional International Union for Conservation of Nature (IUCN) Red List assessment.     

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.     

An analysis of two Myosorex species (Soricidae) from the Early Pliocene site of Langebaanweg (West coast, South Africa) using geometric morphometrics, linear measurements, and non-metric characters

This represents the first study of the soricid community from the Early Pliocene site of Langebaanweg (LBW) which is represented by four species, two of which belong to the soricid genus Myosorex (Forest shrew). Using geometric morphometrics the two Myosorex fossil species are compared with each other, and the extant western and eastern Cape species: Myosorex varius, M. cafer and M. longicaudatus. In addition, the results from an analysis of a number of non-metric characters and linear measurements on the fossil species are presented. The mandibles of the fossil species are characterized by extremely broad teeth, ascending rami which are relatively gracile and differ in shape and size from modern species, and the existence of a number of primitive features of the mandibles and teeth. This evidence is interpreted as indicating that the two LBW Myosorex species represent an archaic lineage now extinct in southern Africa.     

Muscle aging and oxidative stress in wild-caught shrews

Red-toothed shrews (Soricidae, subfamily Soricinae) are an intriguing model system to examine the free-radical theory of aging in wild mammals, given their short (< 18 months) lifespan and high mass-specific metabolic rates. As muscle performance underlies both foraging ability and predator avoidance, any age-related decline should be detrimental to fitness and survival. Muscle samples of water shrews (Sorex palustris) and sympatrically distributed short-tailed shrews (Blarina brevicauda) were therefore assessed for oxidative stress markers, protective antioxidant enzymes and apoptosis. Activity levels of catalase and glutathione peroxidase increased with age in both species. Similarly, Cu,Zn-superoxide dismutase isoform content was elevated significantly in older animals of both species (increases of 60% in the water shrew, 25% in the short-tailed shrew). Only one oxidative stress marker (lipid peroxidation) was age-elevated; the others were stable or declined (4-hydroxynonenal adducts and dihydroethidium oxidation). Glutathione peroxidase activity was significantly higher in the short-tailed shrew, while catalase activity was 2× higher in water shrews. Oxidative stress indicators were on average higher in short-tailed shrews. Apoptosis occurred in < 1% of myocytes examined, and did not increase with age. Within the constraints of the sample size we found evidence of protection against elevated oxidative stress in wild-caught shrews.     

Shedding of Infectious Borna Disease Virus-1 in Living Bicolored White-Toothed Shrews

Background

Many RNA viruses arise from animal reservoirs, namely bats, rodents and insectivores but mechanisms of virus maintenance and transmission still need to be addressed. The bicolored white-toothed shrew (Crocidura leucodon) has recently been identified as reservoir of the neurotropic Borna disease virus 1 (BoDV-1).

Principal Findings

Six out of eleven wild living bicoloured white-toothed shrews were trapped and revealed to be naturally infected with BoDV-1. All shrews were monitored in captivity in a long-term study over a time period up to 600 days that differed between the individual shrews. Interestingly, all six animals showed an asymptomatic course of infection despite virus shedding via various routes indicating a highly adapted host-pathogen interaction. Infectious virus and viral RNA were demonstrated in saliva, urine, skin swabs, lacrimal fluid and faeces, both during the first 8 weeks of the investigation period and for long time shedding after more than 250 days in captivity.

Conclusions

The various ways of shedding ensure successful virus maintenance in the reservoir population but also transmission to accidental hosts such as horses and sheep. Naturally BoDV-1-infected living shrews serve as excellent tool to unravel host and pathogen factors responsible for persistent viral co-existence in reservoir species while maintaining their physiological integrity despite high viral load in many organ systems.     

Differences in abundance and species richness between shrews and rodents along an elevational gradient in the Udzungwa Mountains,Tanzania

Small mammals (shrews and rodents) were surveyed along an elevational transect in the Udzungwa Scarp Forest Reserve, in the Udzungwa Mountains, Tanzania. Trap lines and pitfall lines were installed at 600, 910, 1460, and 2000 m a.s.l. In a total of 10341 sample nights (7448 trap-nights and 2893 bucket-nights) 343 specimens (148 shrews, 205 rodents) were captured representing 9 shrew and 14 rodent species for a total of 23 species. While overall species diversity generally increased with elevation, this pattern was not constant for each group sampled. For rodents, both species richness and abundance were lowest at 600 m and greatest at 2000 m a.s.l., and were significantly correlated with elevation. While the highest species number and abundance for shrews was at 2000 m, there was no correlation of these two values with elevation. Rainfall appears to have affected the capture of shrews, but not rodents, and capture success of individual buckets and traps indicated a lack of capture independence. Eastern Arc endemics such asCrocidura desperata Hutterer, Jenkins and Verheyen, 1991 andMyosorex kihaulei Stanley and Hutterer, 2000 were more abundant at 2000 m a.s.l., than at lower elevations. Implications of results of this survey for analyses of future biotic surveys are discussed.     

Distribution and coexistence of shrews in patchy landscapes: A field test of multiple hypotheses

Despite the important role of shrews (Soricomorpha: Soricidae) in the functioning of ecosystems, as predators and prey, the effects of habitat loss and fragmentation on this guild of mammals are still unclear. We studied the distribution of 5 species (the greater white toothed shrew Crocidura leucodon; the lesser white toothed shrew Crocidura suaveolens; the pigmy shrew Sorex minutus; the Appennine shrew Sorex samniticus and the Etruscan shrew Suncus etruscus) in a fragmented landscape in central Italy.Shrews were trapped with pitfall traps made from plastic water bottles, the number of traps increased with patch size. A total of 170 individuals, of 5 species of shrews were captured. Shrews were widely distributed in our study area, however patch occupancy was determined mainly by vegetation and geometrical characteristics of the patches. Our data supports the hypotheses that patterns of habitat selection and the dynamics of seasonal abundance (habitat and temporal partitioning between similarly sized species) reduce competitive pressure, thus allowing coexistence of shrews in relatively species-rich assemblages, for such small amounts of habitat. The most important outcome of our results is the crucial role played by vegetation structure in determining distribution patterns. These results strongly suggest that measurements of the vegetation structure of habitat patches should always be included as explanatory variables when studying the distribution of shrews in fragmented landscapes.     

The occurrence of the Pigmy shrew Sorex minutus on moorland, and the implications for its presence in Ireland

Throughout most of its range in western Europe, the Pigmy shrew Sorex minutus is sympatricwith the Common shrew Sorex araneus but greatly outnumbered by it. This makes it difficult to explain the presence of the Pigmy shrew, in the absence of its congener, in Ireland. A limited pitfall trapping exercise in England has shown that in moorland on deep peat, the Pigmy shrew may in fact outnumber the Common shrew. Reference to the literature on the ecology of the two shrews shows that this result is readily explained by existing knowledge of their diet; earthworms are a major prey for Common shrews and are absent from waterlogged, acidic, peats. Further, evidence on the nature of the possible land bridge from Scotland to Ireland suggests that it was at best low-lying, and probably partly flooded. By analogy with moorland, such a land bridge might have been suitable for Pigmy shrews but not for Common shrews.     

Structure and Seasonal Dynamics of the Ectoparasite Community of the Pygmy Shrew <Emphasis Type="Italic">Sorex minutus</Emphasis> in the Ilmen-Volkhov Lowland

The species composition and seasonal dynamics of ectoparasites of the pygmy shrew Sorex minutus L., 1756 were studied in coniferous and mixed forests of the Ilmen-Volkhov Lowland (Novgorod Province of Russia) in 1999–2003. Examination of 265 specimens of the pygmy shrew revealed 670 specimens of ectoparasites that belonged to 13 species: 8 species of fleas, 2 species of ixodid ticks, 1 species of gamasid mites, and 2 species of myobiid mites. In total, 55.8% of shrew specimens were infested with ectoparasites. No more than 4 species of ectoparasites were found simultaneously on one host, and most of the examined shrews (64.8%) were infested with only 1 ectoparasite species. The pygmy shrew had lower infestation intensity and species diversity of acarines and fleas as compared with those of the common shrew Sorex araneus L., 1758 and the bank vole Myodes glareolus (Schreber, 1780) (13 vs. 23 and 29 species, respectively). Unlike these two other hosts, the prevalent ectoparasite of the pygmy shrew was the tick Ixodes trianguliceps Birula, 1895.     

Maximum Likelihood Analysis of the Complete Mitochondrial Genomes of Eutherians and a Reevaluation of the Phylogeny of Bats and Insectivores

The complete mitochondrial genomes of two microbats, the horseshoe bat Rhinolophus pumilus, and the Japanese pipistrelle Pipistrellus abramus, and that of an insectivore, the long-clawed shrew Sorex unguiculatus, were sequenced and analyzed phylogenetically by a maximum likelihood method in an effort to enhance our understanding of mammalian evolution. Our analysis suggested that (1) a sister relationship exists between moles and shrews, which form an eulipotyphlan clade; (2) chiropterans have a sister-relationship with eulipotyphlans; and (3) the Eulipotyphla/Chiroptera clade is closely related to fereuungulates (Cetartiodactyla, Perissodactyla and Carnivora). Divergence times on the mammalian tree were estimated from consideration of a relaxed molecular clock, the amino acid sequences of 12 concatenated mitochondrial proteins and multiple reference criteria. Moles and shrews were estimated to have diverged approximately 48 MyrBP, and bats and eulipotyphlans to have diverged 68 MyrBP. Recent phylogenetic controversy over the polyphyly of microbats, the monophyly of rodents, and the position of hedgehogs is also examined. Received: 21 December 2000 / Accepted: 16 February 2001     

The social organization and territoriality of short-tailed shrew (Blarina brevicauda) populations in old-field habitats

The social organization of short-tailed shrew (Blarina brevicauda) populations was studied using field and laboratory experiments and observation of a shrew population inside a large enclosure. Short-tailed shrew populations contain resident and nomadic components. Residents occupy small stationary areas at high prey densities and larger areas that are shifted frequently at low prey densities. Areas occupied by residents overlap minimally in winter, non-breeding populations. In summer breeding populations areas occupied by residents of the same sex do not overlap while those of residents of opposite sexes may overlap. Residents defend the area occupied against conspecifics. Scent markings along boundaries appear to maintain the spatial distribution of residents and deter intrusions by nomadic shrews. During encounters vocalizations function as offensive threats, and attacks and chases follow if the intruding shrew does not retreat. Visual communication appears to be less important than chemical and vocal communication in the defence of the area occupied. These data suggest that Blarina is a solitary territorial species.     

The Bicolored White-Toothed Shrew Crocidura leucodon (HERMANN 1780) Is an Indigenous Host of Mammalian Borna Disease Virus

Borna disease (BD) is a sporadic neurologic disease of horses and sheep caused by mammalian Borna disease virus (BDV). Its unique epidemiological features include: limited occurrence in certain endemic regions of central Europe, yearly varying disease peaks, and a seasonal pattern with higher disease frequencies in spring and a disease nadir in autumn. It is most probably not directly transmitted between horses and sheep. All these features led to the assumption that an indigenous virus reservoir of BDV other than horses and sheep may exist. The search for such a reservoir had been unsuccessful until a few years ago five BDV-infected shrews were found in a BD-endemic area in Switzerland. So far, these data lacked further confirmation. We therefore initiated a study in shrews in endemic areas of Germany. Within five years 107 shrews of five different species were collected. BDV infections were identified in 14 individuals of the species bicolored white-toothed shrew (Crocidura leucodon, HERMANN 1780), all originating from BD-endemic territories. Immunohistological analysis showed widespread distribution of BDV antigen both in the nervous system and in epithelial and mesenchymal tissues without pathological alterations. Large amounts of virus, demonstrated by presence of viral antigen in epithelial cells of the oral cavity and in keratinocytes of the skin, may be a source of infection for natural and spill-over hosts. Genetic analyses reflected a close relationship of the BDV sequences obtained from the shrews with the regional BDV cluster. At one location a high percentage of BDV-positive shrews was identified in four consecutive years, which points towards a self-sustaining infection cycle in bicolored white-toothed shrews. Analyses of behavioral and population features of this shrew species revealed that the bicolored white-toothed shrew may indeed play an important role as an indigenous host of BDV.     

Prey size, prey nutrition, and food handling by shrews of different body sizes

We tested some predictions relating metabolic constraints offoraging behavior and prey selection by comparing food handlingand utilization in four sympatric shrew species: Sorex minutus(mean body mass = 3.0 g), S. araneus (8.0 g), Neomys anomalus(10.0 g), and N. fodiens (14.4 g). Live fly larvae, mealwormlarvae, and aquatic arthropods were offered to shrews as smallprey (body mass <0.1 g). Live earthworms, snails, and smallfish were offered as large prey (>0.3 g). The larvae werethe high-nutrition food (>8 kJ/g), and the other prey werethe low-nutrition food (<4 kJ/g). The smallest shrew, S.minutus, utilized (ate + hoarded) <30% of offered food,and the other species utilized >48% of food. The largerthe shrew, the more prey it ate per capita. However, highlyenergetic insect larvae composed 75% of food utilized by S.minutus and only >40% of the food utilized by the other species. Thus, inverse relationships appeared between shrewbody mass and mass-specific food mass utilization and betweenshrew body mass and mass-specific food energy utilization:the largest shrew, N. fodiens, utilized the least food massand the least energy quantity per 1 g of its body mass. Also,the proportion of food hoarded by shrews decreased with increase in size of shrew. With the exception of S. araneus, the sizeof prey hoarded by the shrews was significantly larger thanthe size of prey eaten. Tiny S. minutus hoarded and ate smallerprey items than the other shrews, and large N. fodiens hoardedlarger prey than the other shrews.     

Diversity of rodent and shrew assemblages in different vegetation types of the savannah biome in South Africa: no evidence for nested subsets or competition

Identifying nonrandom species composition patterns predicted by assembly rules has been a central theme in community ecology. Few studies have investigated the prevalence of multiple drivers on species composition patterns in small mammal assemblages in the Old World. This study investigated seasonal changes in rodent and shrew diversity in eleven savannah vegetation types in South Africa. We tested whether species composition patterns are nonrandom with respect to predictions from Diamond's assembly rules, niche limitation hypothesis and nestedness hypothesis. Species richness estimators indicated that inventories for the rodents (80%) and shrews (100%) were relatively complete. Rodent (n = 11 species) diversity and shrew (n = 5 species) diversity were highest in summer and lowest in autumn. Rodent richness was highest in the Terminalia sericea bushveld and woodlands and lowest in the Drypetes arguta sand forest, whilst shrew richness was highest in the T. sericea bushveld and woodlands and lowest in the Acacia nilotica/Dichrostachys cinerea open shrub savannah. We found no support for the predictions of competition and nestedness hypotheses and suggest that this was probably due to the high seasonal and annual variability in rodent and shrew diversity.     

Quantitative estimation of population numbers of shrews (mammalia,insectivora) after wintering

Autumn-winter mortality in shrews (Sorex araneus, S. caecutiens, S. minutus) was estimated on the basis of long-term (12 years) live-trapping on the permanent transect lines in Tver oblast. Relative as well as absolute population numbers were estimated. Lesser shrew (S. minutus) has permanently low population numbers. Fall in this species made 40.1%, and it was scattered through this term. Common shrew (Sorex araneus) lose 89.3% of population and in masked shrew (S. caecutiens) those lost was 73.6%. The most lost was found in autumn and winter fall was as least as 38,2% and 30.4% in the latter two species. The mortality is positively dependent on population density in preceding summer and with severity of winter.