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1.  Novel Papillomaviruses in Free-Ranging Iberian Bats: No Virus–Host Co-evolution, No Strict Host Specificity, and Hints for Recombination 
Genome Biology and Evolution  2014;6(1):94-104.
Papillomaviruses (PVs) are widespread pathogens. However, the extent of PV infections in bats remains largely unknown. This work represents the first comprehensive study of PVs in Iberian bats. We identified four novel PVs in the mucosa of free-ranging Eptesicus serotinus (EserPV1, EserPV2, and EserPV3) and Rhinolophus ferrumequinum (RferPV1) individuals and analyzed their phylogenetic relationships within the viral family. We further assessed their prevalence in different populations of E. serotinus and its close relative E. isabellinus. Although it is frequent to read that PVs co-evolve with their host, that PVs are highly species-specific, and that PVs do not usually recombine, our results suggest otherwise. First, strict virus–host co-evolution is rejected by the existence of five, distantly related bat PV lineages and by the lack of congruence between bats and bat PVs phylogenies. Second, the ability of EserPV2 and EserPV3 to infect two different bat species (E. serotinus and E. isabellinus) argues against strict host specificity. Finally, the description of a second noncoding region in the RferPV1 genome reinforces the view of an increased susceptibility to recombination in the E2-L2 genomic region. These findings prompt the question of whether the prevailing paradigms regarding PVs evolution should be reconsidered.
doi:10.1093/gbe/evt211
PMCID: PMC3914694  PMID: 24391150
bats; papillomavirus; evolution; phylogeny; biodiversity; wildlife
2.  Novel Lyssavirus in Bat, Spain 
Emerging Infectious Diseases  2013;19(5):793-795.
A new tentative lyssavirus, Lleida bat lyssavirus, was found in a bent-winged bat (Miniopterus schreibersii) in Spain. It does not belong to phylogroups I or II, and it seems to be more closely related to the West Causasian bat virus, and especially to the Ikoma lyssavirus.
doi:10.3201/eid1905.121071
PMCID: PMC3647500  PMID: 23648051
Lyssavirus; Lleida bat lyssavirus; bent-winged bat; rabies; viruses; Spain
3.  A Triple-Isotope Approach to Predict the Breeding Origins of European Bats 
PLoS ONE  2012;7(1):e30388.
Despite a commitment by the European Union to protect its migratory bat populations, conservation efforts are hindered by a poor understanding of bat migratory strategies and connectivity between breeding and wintering grounds. Traditional methods like mark-recapture are ineffective to study broad-scale bat migratory patterns. Stable hydrogen isotopes (δD) have been proven useful in establishing spatial migratory connectivity of animal populations. Before applying this tool, the method was calibrated using bat samples of known origin. Here we established the potential of δD as a robust geographical tracer of breeding origins of European bats by measuring δD in hair of five sedentary bat species from 45 locations throughout Europe. The δD of bat hair strongly correlated with well-established spatial isotopic patterns in mean annual precipitation in Europe, and therefore was highly correlated with latitude. We calculated a linear mixed-effects model, with species as random effect, linking δD of bat hair to precipitation δD of the areas of hair growth. This model can be used to predict breeding origins of European migrating bats. We used δ13C and δ15N to discriminate among potential origins of bats, and found that these isotopes can be used as variables to further refine origin predictions. A triple-isotope approach could thereby pinpoint populations or subpopulations that have distinct origins. Our results further corroborated stable isotope analysis as a powerful method to delineate animal migrations in Europe.
doi:10.1371/journal.pone.0030388
PMCID: PMC3264582  PMID: 22291947
4.  Discovery of an Ebolavirus-Like Filovirus in Europe 
PLoS Pathogens  2011;7(10):e1002304.
Filoviruses, amongst the most lethal of primate pathogens, have only been reported as natural infections in sub-Saharan Africa and the Philippines. Infections of bats with the ebolaviruses and marburgviruses do not appear to be associated with disease. Here we report identification in dead insectivorous bats of a genetically distinct filovirus, provisionally named Lloviu virus, after the site of detection, Cueva del Lloviu, in Spain.
Author Summary
A novel filovirus, provisionally named Lloviu virus (LLOV), was detected during the investigation of Miniopterus schreibersii die-offs in Cueva del Lloviu in southern Europe. LLOV is genetically distinct from other marburgviruses and ebolaviruses and is the first filovirus detected in Europe that was not imported from an endemic area in Africa. Filoviruses, amongst the most lethal of primate pathogens, have only been reported as natural infections in sub-Saharan Africa and the Philippines. Infections of bats with the ebolaviruses and marburgviruses do not appear to be associated with disease. Here we report identification of genetically distinct filovirus in dead insectivorous bats in caves in Spain.
doi:10.1371/journal.ppat.1002304
PMCID: PMC3197594  PMID: 22039362
5.  Detection of alpha and betacoronaviruses in multiple Iberian bat species 
Archives of Virology  2011;156(10):1883-1890.
Bat coronaviruses (CoV) are putative precursors of the severe acute respiratory syndrome (SARS) CoV and other CoV that crossed the species barrier from zoonotic reservoirs into the human population. To determine the presence and distribution of CoV in Iberian bats, 576 individuals of 26 different bat species were captured in 13 locations in Spain. We report for the first time the presence of 14 coronaviruses in 9 Iberian bat species. Phylogenetic analysis of a conserved CoV genome region (RdRp gene) shows a wide diversity and distribution of alpha and betacoronavirus in Spain. Interestingly, although some of these viruses are related to other European BatCoV, or to Asian CoV, some of the viruses found in Spain cluster in new groups of α and β CoV.
doi:10.1007/s00705-011-1057-1
PMCID: PMC3181409  PMID: 21766197
6.  Phylogeny of European Bat Lyssavirus 1 in Eptesicus isabellinus Bats, Spain 
Emerging Infectious Diseases  2011;17(3):520-523.
To better understand the epidemiology of European bat lyssavirus 1 (EBLV-1) in Europe, we phylogenetically characterized Lyssavirus from Eptesicus isabellinus bats in Spain. An independent cluster of EBLV-1 possibly resulted from geographic isolation and association with a different reservoir from other European strains. EBLV-1 phylogeny is complex and probably associated with host evolutionary history.
doi:10.3201/eid1703100894
PMCID: PMC3166003  PMID: 21392449
Lyssavirus; bats; phylogeny; rabies; EBLV-1; Eptesicus isabellinus; viruses; Spain; dispatch
7.  Novel intron markers to study the phylogeny of closely related mammalian species 
Background
Multilocus phylogenies can be used to infer the species tree of a group of closely related species. In species trees, the nodes represent the actual separation between species, thus providing essential information about their evolutionary history. In addition, multilocus phylogenies can help in analyses of species delimitation, gene flow and genetic differentiation within species. However, few adequate markers are available for such studies.
Results
In order to develop nuclear markers that can be useful in multilocus studies of mammals, we analyzed the mammalian genomes of human, chimpanzee, macaque, dog and cow. Rodents were excluded due to their unusual genomic features. Introns were extracted from the mammalian genomes because of their greater genetic variability and ease of amplification from the flanking exons. To an initial set of more than 10,000 one-to-one orthologous introns we applied several filters to select introns that belong to single-copy genes, show neutral evolutionary rates and have an adequate length for their amplification. This analysis led to a final list of 224 intron markers randomly distributed along the genome. To experimentally test their validity, we amplified twelve of these introns in a panel of six mammalian species. The result was that seven of these introns gave rise to a PCR band of the expected size in all species. In addition, we sequenced these bands and analyzed the accumulation of substitutions in these introns in five pairs of closely related species. The results showed that the estimated genetic distances in the five species pairs was quite variable among introns and that this divergence cannot be directly predicted from the overall intron divergence in mammals.
Conclusions
We have designed a new set of 224 nuclear introns with optimal features for the phylogeny of closely related mammalian species. A large proportion of the introns tested experimentally showed a perfect amplification and enough variability in most species, indicating that this marker set can be very helpful in multilocus phylogenetics of mammals. Due to the lower variability and stronger stochasticity of nuclear markers with respect to mitochondrial genes, studies should be designed to make use of several markers like the ones designed here.
doi:10.1186/1471-2148-10-369
PMCID: PMC3087552  PMID: 21118501
8.  Endemic Circulation of European Bat Lyssavirus Type 1 in Serotine Bats, Spain 
Emerging Infectious Diseases  2008;14(8):1263-1266.
To determine the presence of European bat lyssavirus type 1 in southern Spain, we studied 19 colonies of serotine bats (Eptesicus isabellinus), its main reservoir, during 1998–2003. Viral genome and antibodies were detected in healthy bats, which suggests subclinical infection. The different temporal patterns of circulation found in each colony indicate independent endemic circulation.
doi:10.3201/1408.080068
PMCID: PMC2600403  PMID: 18680651
lyssavirus; bats; surveillance; rabies; dispatch
9.  Screening of Active Lyssavirus Infection in Wild Bat Populations by Viral RNA Detection on Oropharyngeal Swabs 
Journal of Clinical Microbiology  2001;39(10):3678-3683.
Brain analysis cannot be used for the investigation of active lyssavirus infection in healthy bats because most bat species are protected by conservation directives. Consequently, serology remains the only tool for performing virological studies on natural bat populations; however, the presence of antibodies merely reflects past exposure to the virus and is not a valid marker of active infection. This work describes a new nested reverse transcription (RT)-PCR technique specifically designed for the detection of the European bat virus 1 on oropharyngeal swabs obtained from bats but also able to amplify RNA from the remaining rabies-related lyssaviruses in brain samples. The technique was successfully used for surveillance of a serotine bat (Eptesicus serotinus) colony involved in a case of human exposure, in which 15 out of 71 oropharyngeal swabs were positive. Lyssavirus infection was detected on 13 oropharyngeal swabs but in only 5 brains out of the 34 animals from which simultaneous brain and oropharyngeal samples had been taken. The lyssavirus involved could be rapidly identified by automatic sequencing of the RT-PCR products obtained from 14 brains and three bat oropharyngeal swabs. In conclusion, RT-PCR using oropharyngeal swabs will permit screening of wild bat populations for active lyssavirus infection, for research or epidemiological purposes, in line not only with conservation policies but also in a more efficient manner than classical detection techniques used on the brain.
doi:10.1128/JCM.39.10.3678-3683.2001
PMCID: PMC88406  PMID: 11574590
10.  The shaping of genetic variation in edge-of-range populations under past and future climate change 
Ecology Letters  2013;16(10):1258-1266.
With rates of climate change exceeding the rate at which many species are able to shift their range or adapt, it is important to understand how future changes are likely to affect biodiversity at all levels of organisation. Understanding past responses and extent of niche conservatism in climatic tolerance can help predict future consequences. We use an integrated approach to determine the genetic consequences of past and future climate changes on a bat species, Plecotus austriacus. Glacial refugia predicted by palaeo-modelling match those identified from analyses of extant genetic diversity and model-based inference of demographic history. Former refugial populations currently contain disproportionately high genetic diversity, but niche conservatism, shifts in suitable areas and barriers to migration mean that these hotspots of genetic diversity are under threat from future climate change. Evidence of population decline despite recent northward migration highlights the need to conserve leading-edge populations for spearheading future range shifts.
doi:10.1111/ele.12158
PMCID: PMC4015367  PMID: 23890483
Approximate Bayesian computation; Chiroptera; ecological niche modelling; niche conservatism; phylogeography

Results 1-10 (10)