Andrew G. Hope

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.

Satellite imagery characterizes local animal reservoir populations of Sin Nombre virus in the southwestern United States

The relationship between the risk of hantaviral pulmonary syndrome (HPS), as estimated from satellite imagery, and local rodent populations was examined. HPS risk, predicted before rodent sampling, was highly associated with the abundance of Peromyscus maniculatus, the reservoir of Sin Nombre virus (SNV). P. maniculatus were common in high-risk sites, and populations in high-risk areas were skewed toward adult males, the subclass most frequently infected with SNV. In the year after an El Niño Southern Oscillation (ENSO), captures of P. maniculatus increased only in high-risk areas. During 1998, few sites had infected mice, but by 1999, 18/20 of the high-risk sites contained infected mice and the crude prevalence was 30.8%. Only 1/18 of the low-risk sites contained infected rodents, and the prevalence of infection was lower (8.3%). Satellite imagery identified environmental features associated with SNV transmission within its reservoir population, but at least 2 years of high-risk conditions were needed for SNV to reach high prevalence. Areas with persistently high-risk environmental conditions may serve as refugia for the survival of SNV in local mouse populations.

Beringia: Intercontinental exchange and diversification of high latitude mammals and their parasites during the Pliocene and Quaternary

ABSTRACT Beringia is the region spanning eastern Asia and northwestern North America that remained ice-free during the full glacial events of the Pleistocene. Numerous questions persist regarding the importance of this region in the evolution of northern faunas. Beringia has been implicated as both a high latitude refugium and as the crossroads (Bering Land Bridge) of the northern continents for boreal mammals. The Beringian Coevolution Project (BCP) is an international collaboration that has provided material to assess the pattern and timing of faunal exchange across the crossroads of the northern continents and the potential impact of past climatic events on differentiation. Mammals and associated parasite specimens have been collected and preserved from more than 200 field sites in eastern Russia, Alaska and northwestern Canada since 1999. Previously, fossils and taxonomic comparisons between Asia and North America mammals have shed light on these events. Molecular phylogenetics based on BCP specimens is now being used to trace the history of faunal exchange and diversification. We have found substantial phylogeographic structure in the Arctic and in Beringia in mustelid carnivores, arvicoline rodents, arctic hares and soricine shrews, including spatially concordant clades and contact zones across taxa that correspond to the edges of Beringia. Among the tapeworms of these mammalian hosts, new perspectives on diversity have also been developed. Arostrilepis horrida (Hymenolepididae) was considered to represent a single widespread and morphologically variable species occurring in a diversity of voles and lemmings in eastern and western Beringia and more broadly across the Holarctic region. The BCP has demonstrated a complex of at least 10 species that are poorly differentiated morphologically. The diversity of Paranoplocephala spp. and Anolocephaloides spp. (Anoplocephalidae) in Beringia included relatively few widespread and morphologically variable species in arvicolines. BCP collections have changed this perspective, allowing the recognition of a series of highly endemic species of Paranoplocephala that demonstrate very narrow host specificity, and additional species complexes among arvicolines. Thus, extensive, previously unrecognized, diversity for tapeworms of 2 major families characterizes the Beringian fauna. By elucidating evolutionary relationships and phylogeographic variation among populations, species and assemblages, refined views of the sequence and timing of biotic expansion, geographic colonization and impact of episodic climate change have been developed for Beringia. Ultimately, Beringia was a determining factor in the structure and biogeography of terrestrial faunas across the Nearctic and Neotropical regions during the Pliocene and Quaternary.

Shared Ancestry between a Newfound Mole-Borne Hantavirus and Hantaviruses Harbored by Cricetid Rodents

ABSTRACT Discovery of genetically distinct hantaviruses in multiple species of shrews (order Soricomorpha, family Soricidae) and moles (family Talpidae) contests the conventional view that rodents (order Rodentia, families Muridae and Cricetidae) are the principal reservoir hosts and suggests that the evolutionary history of hantaviruses is far more complex than previously hypothesized. We now report on Rockport virus (RKPV), a hantavirus identified in archival tissues of the eastern mole (Scalopus aquaticus) collected in Rockport, TX, in 1986. Pairwise comparison of the full-length S, M, and L genomic segments indicated moderately low sequence similarity between RKPV and other soricomorph-borne hantaviruses. Phylogenetic analyses, using maximum-likelihood and Bayesian methods, showed that RKPV shared a most recent common ancestor with cricetid-rodent-borne hantaviruses. Distributed widely across the eastern United States, the fossorial eastern mole is sympatric and syntopic with cricetid rodents known to harbor hantaviruses, raising the possibility of host-switching events in the distant past. Our findings warrant more-detailed investigations on the dynamics of spillover and cross-species transmission of present-day hantaviruses within communities of rodents and moles.

Novel hantavirus in the flat-skulled shrew (Sorex roboratus).

Genetically distinct hantaviruses have been identified recently in multiple species of shrews (Order Soricomorpha, Family Soricidae) in Eurasia and North America. To corroborate decades-old reports of hantaviral antigens in shrews from Russia, archival liver and lung tissues from 4 Siberian large-toothed shrews (Sorex daphaenodon), 5 Eurasian least shrews (Sorex minutissimus), 12 flat-skulled shrews (Sorex roboratus), and 18 tundra shrews (Sorex tundrensis), captured in the Sakha Republic in northeastern Siberia during July and August 2006, were analyzed for hantavirus RNA by reverse transcription-polymerase chain reaction. A novel hantavirus, named Kenkeme virus, was detected in a flat-skulled shrew. Sequence analysis of the full-length S and partial M and L segments indicated that Kenkeme virus was genetically and phylogenetically distinct from Seewis virus harbored by the Eurasian common shrew (Sorex araneus), as well as all other rodent-, soricid-, and talpid-borne hantaviruses.

Genetic diversity and phylogeography of Seewis virus in the Eurasian common shrew in Finland and Hungary

Recent identification of a newfound hantavirus, designated Seewis virus (SWSV), in the Eurasian common shrew (Sorex araneus), captured in Switzerland, corroborates decades-old reports of hantaviral antigens in this shrew species from Russia. To ascertain the spatial or geographic variation of SWSV, archival liver tissues from 88 Eurasian common shrews, trapped in Finland in 1982 and in Hungary during 1997, 1999 and 2000, were analyzed for hantavirus RNAs by reverse transcription-polymerase chain reaction. SWSV RNAs were detected in 12 of 22 (54.5%) and 13 of 66 (19.7%) Eurasian common shrews from Finland and Hungary, respectively. Phylogenetic analyses of S- and L-segment sequences of SWSV strains, using maximum likelihood and Bayesian methods, revealed geographic-specific genetic variation, similar to the phylogeography of rodent-borne hantaviruses, suggesting long-standing hantavirus-host co-evolutionary adaptation.

Implications of the Circumpolar Genetic Structure of Polar Bears for Their Conservation in a Rapidly Warming Arctic

We provide an expansive analysis of polar bear (Ursus maritimus) circumpolar genetic variation during the last two decades of decline in their sea-ice habitat. We sought to evaluate whether their genetic diversity and structure have changed over this period of habitat decline, how their current genetic patterns compare with past patterns, and how genetic demography changed with ancient fluctuations in climate. Characterizing their circumpolar genetic structure using microsatellite data, we defined four clusters that largely correspond to current ecological and oceanographic factors: Eastern Polar Basin, Western Polar Basin, Canadian Archipelago and Southern Canada. We document evidence for recent (ca. last 1–3 generations) directional gene flow from Southern Canada and the Eastern Polar Basin towards the Canadian Archipelago, an area hypothesized to be a future refugium for polar bears as climate-induced habitat decline continues. Our data provide empirical evidence in support of this hypothesis. The direction of current gene flow differs from earlier patterns of gene flow in the Holocene. From analyses of mitochondrial DNA, the Canadian Archipelago cluster and the Barents Sea subpopulation within the Eastern Polar Basin cluster did not show signals of population expansion, suggesting these areas may have served also as past interglacial refugia. Mismatch analyses of mitochondrial DNA data from polar and the paraphyletic brown bear (U. arctos) uncovered offset signals in timing of population expansion between the two species, that are attributed to differential demographic responses to past climate cycling. Mitogenomic structure of polar bears was shallow and developed recently, in contrast to the multiple clades of brown bears. We found no genetic signatures of recent hybridization between the species in our large, circumpolar sample, suggesting that recently observed hybrids represent localized events. Documenting changes in subpopulation connectivity will allow polar nations to proactively adjust conservation actions to continuing decline in sea-ice habitat.

High-latitude diversification within Eurasian least shrews and Alaska tiny shrews (Soricidae)

Abstract A novel shrew was discovered recently in Alaska and described based on morphological characters as Sorex yukonicus. This species is closely allied to Sorex minutissimus, a widespread shrew ranging through Eurasia. Together their distribution spans Beringia, a large Pleistocene nonglaciated area that connected Asia and North America. Beringia was repeatedly divided due to raised sea levels during Pleistocene interglacials and subsequently reconnected during glacials. We tested predictions related to the influence of large-scale geologic events on genetic variability through a phylogeographic analysis of both species of shrew using evidence from 3 independent genetic loci. We found low genetic divergence between S. minutissimus and S. yukonicus across continents. However, major phylogeographic breaks were found for Eurasian and Maritime Northeast Asia populations. Neither species is reciprocally monophyletic for any of the loci examined. Coalescence times for all pairwise population comparisons within both species fall within the Wisconsinan–Weichselian glacial (<130 thousand years ago), and significant population expansion estimates date to the Holocene suggesting that divergence between these taxa is minimal and may not warrant recognition of 2 distinct species. Phylogeographic relationships and sequence divergence estimates place populations of North American S. yukonicus and Siberian S. minutissimus as most closely related, and together they are sister to European S. minutissimus. We conclude that populations east and west of the Bering Strait represent a single Holarctic species, S. minutissimus. Temporal changes in range based on ecological niche predictions and a comparative assessment of other codistributed taxa provide a preliminary view of potential Last Glacial Maximum refugia in northern Asia.

Persistence and diversification of the Holarctic shrew, Sorex tundrensis (Family Soricidae), in response to climate change

Environmental processes govern demography, species movements, community turnover and diversification and yet in many respects these dynamics are still poorly understood at high latitudes. We investigate the combined effects of climate change and geography through time for a widespread Holarctic shrew, Sorex tundrensis. We include a comprehensive suite of closely related outgroup taxa and three independent loci to explore phylogeographic structure and historical demography. We then explore the implications of these findings for other members of boreal communities. The tundra shrew and its sister species, the Tien Shan shrew (Sorex asper), exhibit strong geographic population structure across Siberia and into Beringia illustrating local centres of endemism that correspond to Late Pleistocene refugia. Ecological niche predictions for both current and historical distributions indicate a model of persistence through time despite dramatic climate change. Species tree estimation under a coalescent process suggests that isolation between populations has been maintained across timeframes deeper than the periodicity of Pleistocene glacial cycling. That some species such as the tundra shrew have a history of persistence largely independent of changing climate, whereas other boreal species shifted their ranges in response to climate change, highlights the dynamic processes of community assembly at high latitudes.

A climate for speciation: rapid spatial diversification within the Sorex cinereus complex of shrews

The cyclic climate regime of the late Quaternary caused dramatic environmental change at high latitudes. Although these events may have been brief in periodicity from an evolutionary standpoint, multiple episodes of allopatry and divergence have been implicated in rapid radiations of a number of organisms. Shrews of the Sorex cinereus complex have long challenged taxonomists due to similar morphology and parapatric geographic ranges. Here, multi-locus phylogenetic and demographic assessments using a coalescent framework were combined to investigate spatiotemporal evolution of 13 nominal species with a widespread distribution throughout North America and across Beringia into Siberia. For these species, we first test a hypothesis of recent differentiation in response to Pleistocene climate versus more ancient divergence that would coincide with pre-Pleistocene perturbations. We then investigate the processes driving diversification over multiple continents. Our genetic analyses highlight novel diversity within these morphologically conserved mammals and clarify relationships between geographic distribution and evolutionary history. Demography within and among species indicates both regional stability and rapid expansion. Ancestral ecological differentiation coincident with early cladogenesis within the complex enabled alternating and repeated episodes of allopatry and expansion where successive glacial and interglacial phases each promoted divergence. The Sorex cinereus complex constitutes a valuable model for future comparative assessments of evolution in response to cyclic environmental change.