Bat rabies in urban centers in Chile

One hundred and five rabies isolates obtained from domestic animals and insectivorous bats in Chile between 1977 and 1998 were molecularly characterized by limited sequence analysis of their nucleoprotein genes. These isolates were compared with viruses isolated from known domestic and wildlife rabies reservoirs in the Americas to identify potential reservoirs of rabies in Chile. The phylogenetic analyses showed that none of the Chilean isolates segregated with viruses from the terrestrial reservoirs. No non-rabies lyssaviruses were found in this study. The Chilean samples were not related to viruses of the sylvatic cycle maintained by the common vampire bat (Desmodus rotundus) in Latin America. Five genetic variants were identified from insectivorous bats in Chile. The Brazilian free-tailed bat (Tadarida brasiliensis) was identified as the reservoir for the rabies genetic variant most frequently isolated in the country between 1977 and 1998. The close association of a group of viruses obtained from a domestic dog (Canis familiaris), Brazilian free-tailed bats, and a red bat (Lasiurus borealis) with viruses maintained by Lasiurus spp. in North America implicated species of this genus as the possible reservoirs of this particular genetic variant in Chile. Reservoirs for the other three variants remain unknown.     

Molecular Inferences Suggest Multiple Host Shifts of Rabies Viruses from Bats to Mesocarnivores in Arizona during 2001–2009

In nature, rabies virus (RABV; genus Lyssavirus, family Rhabdoviridae) represents an assemblage of phylogenetic lineages, associated with specific mammalian host species. Although it is generally accepted that RABV evolved originally in bats and further shifted to carnivores, mechanisms of such host shifts are poorly understood, and examples are rarely present in surveillance data. Outbreaks in carnivores caused by a RABV variant, associated with big brown bats, occurred repeatedly during 2001–2009 in the Flagstaff area of Arizona. After each outbreak, extensive control campaigns were undertaken, with no reports of further rabies cases in carnivores for the next several years. However, questions remained whether all outbreaks were caused by a single introduction and further perpetuation of bat RABV in carnivore populations, or each outbreak was caused by an independent introduction of a bat virus. Another question of concern was related to adaptive changes in the RABV genome associated with host shifts. To address these questions, we sequenced and analyzed 66 complete and 20 nearly complete RABV genomes, including those from the Flagstaff area and other similar outbreaks in carnivores, caused by bat RABVs, and representatives of the major RABV lineages circulating in North America and worldwide. Phylogenetic analysis demonstrated that each Flagstaff outbreak was caused by an independent introduction of bat RABV into populations of carnivores. Positive selection analysis confirmed the absence of post-shift changes in RABV genes. In contrast, convergent evolution analysis demonstrated several amino acids in the N, P, G and L proteins, which might be significant for pre-adaptation of bat viruses to cause effective infection in carnivores. The substitution S/T₂₄₂ in the viral glycoprotein is of particular merit, as a similar substitution was suggested for pathogenicity of Nishigahara RABV strain. Roles of the amino acid changes, detected in our study, require additional investigations, using reverse genetics and other approaches.     

Environmental niche equivalency versus conservatism: quantitative approaches to niche evolution

Environmental niche models, which are generated by combining species occurrence data with environmental GIS data layers, are increasingly used to answer fundamental questions about niche evolution, speciation, and the accumulation of ecological diversity within clades. The question of whether environmental niches are conserved over evolutionary time scales has attracted considerable attention, but often produced conflicting conclusions. This conflict, however, may result from differences in how niche similarity is measured and the specific null hypothesis being tested. We develop new methods for quantifying niche overlap that rely on a traditional ecological measure and a metric from mathematical statistics. We reexamine a classic study of niche conservatism between sister species in several groups of Mexican animals, and, for the first time, address alternative definitions of "niche conservatism" within a single framework using consistent methods. As expected, we find that environmental niches of sister species are more similar than expected under three distinct null hypotheses, but that they are rarely identical. We demonstrate how our measures can be used in phylogenetic comparative analyses by reexamining niche divergence in an adaptive radiation of Cuban anoles. Our results show that environmental niche overlap is closely tied to geographic overlap, but not to phylogenetic distances, suggesting that niche conservatism has not constrained local communities in this group to consist of closely related species. We suggest various randomization tests that may prove useful in other areas of ecology and evolutionary biology.     

Niche similarities among white‐eared opossums (Mammalia,Didelphidae): Is ecological niche modelling relevant to setting species limits?

A complex of white‐eared opossums (Didelphis spp.) is distributed across three distinct areas of South America, but recent taxonomic treatments have disagreed regarding species limits in the group. We used ecological niche modelling to test whether ecological niches have been conserved or have diverged among the three forms in this group. Differences in combinations of niche and range were clear; however, when hypotheses of accessible areas for each species were considered, coarse‐grained niche dimensions (i.e. climatic dimensions) were seen not to differ across the complex. We discuss implications of these results for taxonomic recognition of species based on geographic and ecological characteristics and the implications of using ENM approaches to setting species limits. We suggest that ENM should be used to explore speciation mechanisms, rather than being applied to questions of setting species limits.     

Unravelling virus community ecology in bats through the integration of metagenomics and community ecology

The spillover of viruses from wildlife into agricultural animals or humans has profound socioeconomic and public health impact. Vampire bats, found throughout South America, feed directly on humans and other animals and are an important reservoir for zoonotic viruses, including rabies virus. This has resulted in considerable effort in understanding both the ecology of bat‐borne viruses and the composition and associated correlates of the structure of entire virus communities in wildlife, particularly in the context of disease control interventions. In a From the Cover article in this issue of Molecular Ecology, Bergner et al. (2019) set out to reveal virus community dynamics in vampire bats by interrogating factors that affect the structure, diversity and richness of these communities. Due to the linkage of metagenomic sequence data with community ecology, this study represents an important advance in the field of virus ecology.     

Rates of Viral Evolution Are Linked to Host Geography in Bat Rabies

Rates of evolution span orders of magnitude among RNA viruses with important implications for viral transmission and emergence. Although the tempo of viral evolution is often ascribed to viral features such as mutation rates and transmission mode, these factors alone cannot explain variation among closely related viruses, where host biology might operate more strongly on viral evolution. Here, we analyzed sequence data from hundreds of rabies viruses collected from bats throughout the Americas to describe dramatic variation in the speed of rabies virus evolution when circulating in ecologically distinct reservoir species. Integration of ecological and genetic data through a comparative Bayesian analysis revealed that viral evolutionary rates were labile following historical jumps between bat species and nearly four times faster in tropical and subtropical bats compared to temperate species. The association between geography and viral evolution could not be explained by host metabolism, phylogeny or variable selection pressures, and instead appeared to be a consequence of reduced seasonality in bat activity and virus transmission associated with climate. Our results demonstrate a key role for host ecology in shaping the tempo of evolution in multi-host viruses and highlight the power of comparative phylogenetic methods to identify the host and environmental features that influence transmission dynamics.     

Climatic Niche Conservatism and Biogeographical Non-Equilibrium in Eschscholzia californica (Papaveraceae), an Invasive Plant in the Chilean Mediterranean Region

Species climate requirements are useful for predicting their geographic distribution. It is often assumed that the niche requirements for invasive plants are conserved during invasion, especially when the invaded regions share similar climate conditions. California and central Chile have a remarkable degree of convergence in their vegetation structure, and a similar Mediterranean climate. Such similarities make these geographic areas an interesting natural experiment for testing climatic niche dynamics and the equilibrium of invasive species in a new environment. We tested to see if the climatic niche of Eschscholzia californica is conserved in the invaded range (central Chile), and we assessed whether the invasion process has reached a biogeographical equilibrium, i.e., occupy all the suitable geographic locations that have suitable conditions under native niche requirements. We compared the climatic niche in the native and invaded ranges as well as the projected potential geographic distribution in the invaded range. In order to compare climatic niches, we conducted a Principal Component Analysis (PCA) and Species Distribution Models (SDMs), to estimate E. californica''s potential geographic distribution. We also used SDMs to predict altitudinal distribution limits in central Chile. Our results indicated that the climatic niche occupied by E. californica in the invaded range is firmly conserved, occupying a subset of the native climatic niche but leaving a substantial fraction of it unfilled. Comparisons of projected SDMs for central Chile indicate a similarity, yet the projection from native range predicted a larger geographic distribution in central Chile compared to the prediction of the model constructed for central Chile. The projected niche occupancy profile from California predicted a higher mean elevation than that projected from central Chile. We concluded that the invasion process of E. californica in central Chile is consistent with climatic niche conservatism but there is potential for further expansion in Chile.     

Using environmental niche models to test the ‘everything is everywhere' hypothesis for Badhamia

It is often discussed whether the biogeography of free-living protists is better explained by the ‘everything is everywhere''(EiE) hypothesis, which postulates that only ecology drives their distribution, or by the alternative hypothesis of ‘moderate endemicity'' in which geographic barriers can limit their dispersal. To formally test this, it would be necessary not only to find organisms restricted to a geographical area but also to check for their presence in any other place with a similar ecology. We propose the use of environmental niche models to generate and test null EiE distributions. Here we have analysed the distribution of 18S rDNA variants (ribotypes) of the myxomycete Badhamia melanospora (belonging to the protozoan phylum Amoebozoa) using 125 specimens from 91 localities. Two geographically structured groups of ribotypes congruent with slight morphological differences in the spores can be distinguished. One group comprises all populations from Argentina and Chile, and the other is formed by populations from North America together with human-introduced populations from other parts of the world. Environmental climatic niche models constructed separately for the two groups have significant differences, but show several overlapping areas. However, only specimens from one group were found in an intensively surveyed area in South America where both niche models overlap. It can be concluded that everything is not everywhere for B. melanospora. This taxon constitutes a complex formed by at least two cryptic species that probably diverged allopatrically in North and South America.     

A comparative analysis reveals little evidence for niche conservatism in aquatic macrophytes among four areas on two continents

One of the most intriguing questions in current ecology is the extent to which the ecological niches of species are conserved in space and time. Niche conservatism has mostly been studied using coarse‐scale data of species' distributions, although it is at the local habitat scales where species' responses to ecological variables primarily take place. We investigated the extent to which niches of aquatic macrophytes are conserved among four study regions (i.e. Finland, Sweden and the US states of Minnesota and Wisconsin) on two continents (i.e. Europe and North America) using data for 11 species common to all the four study areas. We studied how ecological variables (i.e. local, climate and spatial variables) explain variation in the distributions of these common species in the four areas using species distribution modelling. In addition, we examined whether species' niche parameters vary among the study regions. Our results revealed large variation in both species' responses to the studied ecological variables and in species' niche parameters among the areas. We found little evidence for niche conservatism in aquatic macrophytes, though local environmental conditions among the studied areas were largely similar. This suggests that niche shifts, rather than different environmental conditions, were responsible for variable responses of aquatic macrophytes to local ecological variables. Local habitat niches of aquatic macrophytes are mainly driven by variations in local environmental conditions, whereas their climate niches are more or less conserved among regions. This highlights the need to study niche conservatism using local‐scale data to better understand whether species' niches are conserved, because different niches (e.g. local versus climate) operating at various scales may show different degrees of conservatism. The extent to which species' niches are truly conserved has wide practical implications, including for instance, predicting changes in species' distributions in response to global change.     

Bats and zoonotic viruses: can we confidently link bats with emerging deadly viruses?

An increasingly asked question is ''can we confidently link bats with emerging viruses?''. No, or not yet, is the qualified answer based on the evidence available. Although more than 200 viruses - some of them deadly zoonotic viruses - have been isolated from or otherwise detected in bats, the supposed connections between bats, bat viruses and human diseases have been raised more on speculation than on evidence supporting their direct or indirect roles in the epidemiology of diseases (except for rabies). However, we are convinced that the evidence points in that direction and that at some point it will be proved that bats are competent hosts for at least a few zoonotic viruses. In this review, we cover aspects of bat biology, ecology and evolution that might be relevant in medical investigations and we provide a historical synthesis of some disease outbreaks causally linked to bats. We provide evolutionary-based hypotheses to tentatively explain the viral transmission route through mammalian intermediate hosts and to explain the geographic concentration of most outbreaks, but both are no more than speculations that still require formal assessment.     

Rabies prevalence in migratory tree-bats in Alberta and the influence of roosting ecology and sampling method on reported prevalence of rabies in bats

The migratory tree-roosting hoary bat (Lasiurus cinereus) and silver-haired bat (Lasionycteris noctivagans) are among the bat species with the highest reported prevalence of rabies in North America. However, bats submitted for rabies testing typically have been those that have come in contact with humans or pets. Given the roosting ecology of L. cinereus and L. noctivagans, contact with healthy individuals of these species is expected to be rare, with a bias in contact and submission of infected individuals and thus an overestimation of rabies prevalence. We tested 121 L. cinereus and 96 L. noctivagans specimens, collected during mortality surveys at wind energy facilities in Southern Alberta, Canada in 2007 and 2008, for rabies. None of the L. cinereus (0%) and one L. noctivagans (1%) tested positive for rabies. Prevalence of rabies was significantly lower than previously reported estimates, passive and active, for L. cinereus and L. noctivagans. In a review of the literature including multiple bat species, we found a significant difference in estimates of rabies prevalence based on passive versus active surveillance testing. Furthermore, roosting ecology influenced estimates of rabies prevalence, with significantly higher prevalence among passive surveillance submissions of nonsynanthropic species compared to synanthropic species, a trend not evident in active surveillance reports. We conclude that rabies prevalence in randomly collected L. cinereus and L. noctivagans is low and comparable to active surveillance estimates from other species (≤ 1%), and that roosting ecology influences estimates of rabies prevalence among bats submitted to public health laboratories in North America.     

Molecular and geographic analyses of vampire bat-transmitted cattle rabies in central Brazil

Background

Vampire bats are important rabies virus vectors, causing critical problems in both the livestock industry and public health sector in Latin America. In order to assess the epidemiological characteristics of vampire bat-transmitted rabies, the authors conducted phylogenetic and geographical analyses using sequence data of a large number of cattle rabies isolates collected from a wide geographical area in Brazil.

Methods

Partial nucleoprotein genes of rabies viruses isolated from 666 cattle and 18 vampire bats between 1987 and 2006 were sequenced and used for phylogenetic analysis. The genetic variants were plotted on topographical maps of Brazil.

Results

In this study, 593 samples consisting of 24 genetic variants were analyzed. Regional localization of variants was observed, with the distribution of several variants found to be delimited by mountain ranges which served as geographic boundaries. The geographical distributions of vampire-bat and cattle isolates that were classified as the identical phylogenetic group were found to overlap with high certainty. Most of the samples analyzed in this study were isolated from adjacent areas linked by rivers.

Conclusion

This study revealed the existence of several dozen regional variants associated with vampire bats in Brazil, with the distribution patterns of these variants found to be affected by mountain ranges and rivers. These results suggest that epidemiological characteristics of vampire bat-related rabies appear to be associated with the topographical and geographical characteristics of areas where cattle are maintained, and the factors affecting vampire bat ecology.

     

The influence of bat ecology on viral diversity and reservoir status

Repeated emergence of zoonotic viruses from bat reservoirs into human populations demands predictive approaches to preemptively identify virus‐carrying bat species. Here, we use machine learning to examine drivers of viral diversity in bats, determine whether those drivers depend on viral genome type, and predict undetected viral carriers. Our results indicate that bat species with longer life spans, broad geographic distributions in the eastern hemisphere, and large group sizes carry more viruses overall. Life span was a stronger predictor of deoxyribonucleic acid viral diversity, while group size and family were more important for predicting ribonucleic acid viruses, potentially reflecting broad differences in infection duration. Importantly, our models predict 54 bat species as likely carriers of zoonotic viruses, despite not currently being considered reservoirs. Mapping these predictions as a proportion of local bat diversity, we identify global regions where efforts to reduce disease spillover into humans by identifying viral carriers may be most productive.     

Lutzomyia vectors for cutaneous leishmaniasis in Southern Brazil: ecological niche models,predicted geographic distributions,and climate change effects

Geographic and ecological distributions of three Lutzomyia sand flies that are cutaneous leishmaniasis vectors in South America were analysed using ecological niche modelling. This new tool provides a large-scale perspective on species' geographic distributions, ecological and historical factors determining them, and their potential for change with expected environmental changes. As a first step, the ability of this technique to predict geographic distributions of the three species was tested statistically using two subsampling techniques: a random-selection technique that simulates 50% data density, and a quadrant-based technique that challenges the method to predict into broad unsampled regions. Predictivity under both test schemes was highly statistically significant. Visualisation of ecological niches provided insights into the ecological basis for distributional differences among species. Projections of potential geographic distributions across scenarios of global climate change suggested that only Lutzomyia whitmani is likely to be experiencing dramatic improvements in conditions in south-eastern Brazil, where cutaneous leishmaniasis appears to be re-emerging; Lutzomyia intermedia and Lutzomyia migonei may be seeing more subtle improvements in climatic conditions, but the implications are not straightforward. More generally, this technique offers the possibility of new views into the distributional ecology of disease, vector, and reservoir species.     

Emerging infectious diseases associated with bat viruses

Bats play important roles as pollen disseminators and pest predators. However, recent interest has focused on their role as natural reservoirs of pathogens associated with emerging infectious diseases. Prior to the outbreak of severe acute respiratory syndrome (SARS), about 60 bat virus species had been reported. The number of identified bat viruses has dramatically increased since the initial SARS outbreak, and most are putative novel virus species or genotypes. Serious infectious diseases caused by previously identified bat viruses continue to emerge throughout in Asia, Australia, Africa and America. Intriguingly, bats infected by these different viruses seldom display clinical symptoms of illness. The pathogenesis and potential threat of bat-borne viruses to public health remains largely unknown. This review provides a brief overview of bat viruses associated with emerging human infectious diseases.     

Using host traits to predict reservoir host species of rabies virus

Wildlife are important reservoirs for many pathogens, yet the role that different species play in pathogen maintenance frequently remains unknown. This is the case for rabies, a viral disease of mammals. While Carnivora (carnivores) and Chiroptera (bats) are the canonical mammalian orders known to be responsible for the maintenance and onward transmission of rabies Lyssavirus (RABV), the role of most species within these orders remains unknown and is continually changing as a result of contemporary host shifting. We combined a trait-based analytical approach with gradient boosting machine learning models to identify physiological and ecological host features associated with being a reservoir for RABV. We then used a cooperative game theory approach to determine species-specific traits associated with known RABV reservoirs. Being a carnivore reservoir for RABV was associated with phylogenetic similarity to known RABV reservoirs, along with other traits such as having larger litters and earlier sexual maturity. For bats, location in the Americas and geographic range were the most important predictors of RABV reservoir status, along with having a large litter. Our models identified 44 carnivore and 34 bat species that are currently not recognized as RABV reservoirs, but that have trait profiles suggesting their capacity to be or become reservoirs. Further, our findings suggest that potential reservoir species among bats and carnivores occur both within and outside of areas with current RABV circulation. These results show the ability of a trait-based approach to detect potential reservoirs of infection and could inform rabies control programs and surveillance efforts by identifying the types of species and traits that facilitate RABV maintenance and transmission.     

Diversity and Distribution of Hantaviruses in South America

Hantaviruses are important contributors to disease burden in the New World, yet many aspects of their distribution and dynamics remain uncharacterized. To examine the patterns and processes that influence the diversity and geographic distribution of hantaviruses in South America, we performed genetic and phylogeographic analyses of all available South American hantavirus sequences. We sequenced multiple novel and previously described viruses (Anajatuba, Laguna Negra-like, two genotypes of Castelo dos Sonhos, and two genotypes of Rio Mamore) from Brazilian Oligoryzomys rodents and hantavirus pulmonary syndrome cases and identified a previously uncharacterized species of Oligoryzomys associated with a new genotype of Rio Mamore virus. Our analysis indicates that the majority of South American hantaviruses fall into three phylogenetic clades, corresponding to Andes and Andes-like viruses, Laguna Negra and Laguna Negra-like viruses, and Rio Mamore and Rio Mamore-like viruses. In addition, the dynamics and distribution of these viruses appear to be shaped by both the geographic proximity and phylogenetic relatedness of their rodent hosts. The current system of nomenclature used in the hantavirus community is a significant impediment to understanding the ecology and evolutionary history of hantaviruses; here, we suggest strict adherence to a modified taxonomic system, with species and strain designations resembling the numerical system of the enterovirus genus.     

Spatio-temporal dynamics of rabies and habitat suitability of the common marmoset Callithrix jacchus in Brazil

Rabies transmitted by wildlife is now the main source of human rabies in the Americas. The common marmoset, Callithrix jacchus, is considered a reservoir of rabies causing sporadic and unpredictable human deaths in Brazil, but the extent of the spillover risk to humans remains unknown. In this study, we described the spatiotemporal dynamics of rabies affecting C. jacchus reported to Brazil’s Ministry of Health passive surveillance system between 2008 and 2020, and combined ecological niche modelling with C. jacchus occurrence data to predict its suitable habitat. Our results show that 67 outbreaks (91 cases) of rabies affecting C. jacchus were reported by 41 municipalities between January 2008 and October 2020, with a mean of 5 outbreaks/year [range: 1–14]. The maximum number of outbreaks and municipalities reporting cases occurred in 2018, coinciding with higher surveillance of primate deaths due to Yellow Fever. A mean of 3 [1–9] new municipalities reported outbreaks yearly, suggesting potential spatial expansions of the C. jacchus variant in northeastern Brazil and emerging rabies spillover from vampire bat Desmodus rotundus to C. jacchus in the north and south. Outbreaks were concentrated in the states of Ceará (72%) and Pernambuco (16%) up to 2012, but are now reported in Piauí since 2013, in Bahia since 2017 (D. rotundus’ antigenic variant, AgV3) and in Rio de Janeiro since 2019 (AgV3). Besides confirming suitable habitat for this primate in the northeast and the east coast of Brazil, our Maximum Entropy model also predicted suitable habitat on the north and the west states of the country but predicted low habitat suitability among inland municipalities of the Caatinga biome reporting rabies. Our findings revealed new areas reporting rabies infecting C. jacchus, highlighting the need to implement strategies limiting spillover to humans and to better understand the drivers of C. jacchus rabies dynamics.     

Spatial and temporal dynamics of rabies virus variants in big brown bat populations across Canada: footprints of an emerging zoonosis

Phylogenetic analysis of a collection of rabies viruses that currently circulate in Canadian big brown bats (Eptesicus fuscus) identified five distinct lineages which have emerged from a common ancestor that existed over 400 years ago. Four of these lineages are regionally restricted in their range while the fifth lineage, comprising two‐thirds of all specimens, has emerged in recent times and exhibits a recent demographic expansion with rapid spread across the Canadian range of its host. Four of these viral lineages are shown to circulate in the US. To explore the role of the big brown bat host in dissemination of these viral variants, the population structure of this species was explored using both mitochondrial DNA and nuclear microsatellite markers. These data suggest the existence of three subpopulations distributed in British Columbia, mid‐western Canada (Alberta and Saskatchewan) and eastern Canada (Quebec and Ontario), respectively. We suggest that these three bat subpopulations may differ by their level of female phylopatry, which in turn affects the spread of rabies viruses. We discuss how this bat population structure has affected the historical spread of rabies virus variants across the country and the potential impact of these events on public health concerns regarding rabies.