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.     

Demographic and environmental drivers of metagenomic viral diversity in vampire bats

Viruses infect all forms of life and play critical roles as agents of disease, drivers of biochemical cycles and sources of genetic diversity for their hosts. Our understanding of viral diversity derives primarily from comparisons among host species, precluding insight into how intraspecific variation in host ecology affects viral communities or how predictable viral communities are across populations. Here we test spatial, demographic and environmental hypotheses explaining viral richness and community composition across populations of common vampire bats, which occur in diverse habitats of North, Central and South America. We demonstrate marked variation in viral communities that was not consistently predicted by a null model of declining community similarity with increasing spatial or genetic distances separating populations. We also find no evidence that larger bat colonies host greater viral diversity. Instead, viral diversity follows an elevational gradient, is enriched by juvenile‐biased age structure, and declines with local anthropogenic food resources as measured by livestock density. Our results establish the value of linking the modern influx of metagenomic sequence data with comparative ecology, reveal that snapshot views of viral diversity are unlikely to be representative at the species level, and affirm existing ecological theories that link host ecology not only to single pathogen dynamics but also to viral communities.     

Network analysis of host–virus communities in bats and rodents reveals determinants of cross‐species transmission

Bats are natural reservoirs of several important emerging viruses. Cross‐species transmission appears to be quite common among bats, which may contribute to their unique reservoir potential. Therefore, understanding the importance of bats as reservoirs requires examining them in a community context rather than concentrating on individual species. Here, we use a network approach to identify ecological and biological correlates of cross‐species virus transmission in bats and rodents, another important host group. We show that given our current knowledge the bat viral sharing network is more connected than the rodent network, suggesting viruses may pass more easily between bat species. We identify host traits associated with important reservoir species: gregarious bats are more likely to share more viruses and bats which migrate regionally are important for spreading viruses through the network. We identify multiple communities of viral sharing within bats and rodents and highlight potential species traits that can help guide studies of novel pathogen emergence.     

Viral Richness is Positively Related to Group Size,but Not Mating System,in Bats

Characterizing host traits that influence viral richness and diversification is important for understanding wildlife pathogens affecting conservation and/or human health. Behaviors that affect contact rates among hosts could be important for viral diversification because more frequent intra- and inter-specific contacts among hosts should increase the potential for viral diversification within host populations. We used published data on bats to test the contact-rate hypothesis. We predicted that species forming large conspecific groups, that share their range with more heterospecifics (i.e., sympatry), and with mating systems characterized by high contact rates (polygynandry: multi-male/multi-female), would host higher viral richness than species with small group sizes, lower sympatry, or low contact-rate mating systems (polygyny: single male/multi-female). Consistent with our hypothesis and previous research, viral richness was positively correlated with conspecific group size although the relationship plateaued at group sizes of approximately several hundred thousand bats. This pattern supports epidemiological theory that, up to a point, larger groups have higher contact rates, greater likelihood of acquiring and transmitting viruses, and ultimately greater potential for viral diversification. However, contrary to our hypothesis, there was no effect of sympatry on viral richness and no difference in viral richness between mating systems. We also found no residual effect of host phylogeny on viral richness, suggesting that closely related species do not necessarily host similar numbers of viruses. Our results support the contact-rate hypothesis that intra-specific viral transmission can enhance viral diversification within species and highlight the influence of host group size on the potential of viruses to propagate within host populations.     

A comparison of bats and rodents as reservoirs of zoonotic viruses: are bats special?

Bats are the natural reservoirs of a number of high-impact viral zoonoses. We present a quantitative analysis to address the hypothesis that bats are unique in their propensity to host zoonotic viruses based on a comparison with rodents, another important host order. We found that bats indeed host more zoonotic viruses per species than rodents, and we identified life-history and ecological factors that promote zoonotic viral richness. More zoonotic viruses are hosted by species whose distributions overlap with a greater number of other species in the same taxonomic order (sympatry). Specifically in bats, there was evidence for increased zoonotic viral richness in species with smaller litters (one young), greater longevity and more litters per year. Furthermore, our results point to a new hypothesis to explain in part why bats host more zoonotic viruses per species: the stronger effect of sympatry in bats and more viruses shared between bat species suggests that interspecific transmission is more prevalent among bats than among rodents. Although bats host more zoonotic viruses per species, the total number of zoonotic viruses identified in bats (61) was lower than in rodents (68), a result of there being approximately twice the number of rodent species as bat species. Therefore, rodents should still be a serious concern as reservoirs of emerging viruses. These findings shed light on disease emergence and perpetuation mechanisms and may help lead to a predictive framework for identifying future emerging infectious virus reservoirs.     

Bat fly species richness in Neotropical bats: correlations with host ecology and host brain

Patterns of ectoparasite species richness in mammals have been investigated in various terrestrial mammalian taxa such as primates, ungulates and carnivores. Several ecological or life traits of hosts are expected to explain much of the variability in species richness of parasites. In the present comparative analysis we investigate some determinants of parasite richness in bats, a large and understudied group of flying mammals, and their obligate blood-sucking ectoparasite, streblid bat flies (Diptera). We investigate the effects of host body size, geographical range, group size and roosting ecology on the species richness of bat flies in tropical areas of Venezuela and Peru, where both host and parasite diversities are high. We use the data from a major sampling effort on 138 bat species from nine families. We also investigate potential correlation between bat fly species richness and brain size (corrected for body size) in these tropical bats. We expect a relationship if there is a potential energetic trade-off between costly large brains and parasite-mediated impacts. We show that body size and roosting in cavities are positively correlated with bat fly species richness. No effects of bat range size and group size were observed. Our results also suggest an association between body mass-independent brain size and bat fly species richness. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Mammal virus diversity estimates are unstable due to accelerating discovery effort

Host-virus association data underpin research into the distribution and eco-evolutionary correlates of viral diversity and zoonotic risk across host species. However, current knowledge of the wildlife virome is inherently constrained by historical discovery effort, and there are concerns that the reliability of ecological inference from host-virus data may be undermined by taxonomic and geographical sampling biases. Here, we evaluate whether current estimates of host-level viral diversity in wild mammals are stable enough to be considered biologically meaningful, by analysing a comprehensive dataset of discovery dates of 6571 unique mammal host-virus associations between 1930 and 2018. We show that virus discovery rates in mammal hosts are either constant or accelerating, with little evidence of declines towards viral richness asymptotes, even in highly sampled hosts. Consequently, inference of relative viral richness across host species has been unstable over time, particularly in bats, where intensified surveillance since the early 2000s caused a rapid rearrangement of species'' ranked viral richness. Our results illustrate that comparative inference of host-level virus diversity across mammals is highly sensitive to even short-term changes in sampling effort. We advise caution to avoid overinterpreting patterns in current data, since it is feasible that an analysis conducted today could draw quite different conclusions than one conducted only a decade ago.     

Do threatened hosts have fewer parasites? A comparative study in primates

1. Parasites and infectious diseases have become a major concern in conservation biology, in part because they can trigger or accelerate species or population declines. Focusing on primates as a well-studied host clade, we tested whether the species richness and prevalence of parasites differed between threatened and non-threatened host species. 2. We collated data on 386 species of parasites (including viruses, bacteria, protozoa, helminths and arthropods) reported to infect wild populations of 36 threatened and 81 non-threatened primate species. Analyses controlled for uneven sampling effort and host phylogeny. 3. Results showed that total parasite species richness was lower among threatened primates, supporting the prediction that small, isolated host populations harbour fewer parasite species. This trend was consistent across three major parasite groups found in primates (helminths, protozoa and viruses). Counter to our predictions, patterns of parasite species richness were independent of parasite transmission mode and the degree of host specificity. 4. We also examined the prevalence of selected parasite genera among primate sister-taxa that differed in their ranked threat categories, but found no significant differences in prevalence between threatened and non-threatened hosts. 5. This study is the first to demonstrate differences in parasite richness relative to host threat status. Results indicate that human activities and host characteristics that increase the extinction risk of wild animal species may lead simultaneously to the loss of parasites. Lower average parasite richness in threatened host taxa also points to the need for a better understanding of the cascading effects of host biodiversity loss for affiliated parasite species.     

Host population density as the major determinant of endoparasite species richness in floodplain fishes of the upper Paraná River, Brazil

A comparative analysis of parasite species richness was performed across 53 species of fish from the floodplain of the upper Paraná River, Brazil. Values of catch per unit effort, CPUE (number of individuals of a given fish species captured per 1000 m(2) of net during 24 h) were used as a rough measure of population density for each fish species in order to test its influence on endoparasite species richness. The effects of several other host traits (body size, social behaviour, reproductive behaviour, spawning type, trophic category, feeding habits, relative position in the food web, preference for certain habitats and whether the fish species are native or exotic) on metazoan endoparasite species richness were also evaluated. The CPUE was the sole significant predictor of parasite species richness, whether controlling for the confounding influences of host phylogeny and sampling effort or not. The results suggest that in the floodplain of the upper Paraná River (with homogeneous physical characteristics and occurrence of many flood pulses), population density of different host species might be the major determinant of their parasite species richness.     

Influence of host ecology and morphology on the diversity of Neotropical bird lice

Host‐parasite systems can be powerful arenas in which to explore factors influencing community structure. We used a comparative approach to examine the influence of host ecology and morphology on the diversity of chewing lice (Insecta: Phthiraptera) among 52 species of Peruvian birds. For each host species we calculated two components of parasite diversity: 1) cumulative species richness, and 2) mean abundance. We tested for correlations between these parasite indices and 13 host ecological and morphological variables. Host ecological variables included geographic range size, local population density, and microhabitat use. Host morphological variables included body mass, plumage depth, and standard dimensions of bill, foot and toenail morphology, all of which could influence the efficiency of anti‐parasite grooming. Data were analysed using statistical and comparative methods that control for sampling effort and host phylogeny. None of the independent host variables correlated with louse species richness when treated as a dependent variable. When richness was treated as an independent variable, however, it was positively correlated with mean louse abundance. Host body mass was also positively correlated with mean louse abundance. When louse richness and host body mass were held constant, mean louse abundance correlated negatively with the degree to which the upper mandible of the host's bill overhangs the lower mandible. This correlation suggests that birds with longer overhangs are better at controlling lice during preening. We propose a specific functional hypothesis in which preening damages lice by exerting a shearing force between the overhang and the tip of the lower mandible. This study is the first to suggest a parasite‐control function of such a detailed component of bill morphology across species. Avian biologists have traditionally focused almost exclusively on bills as tools for feeding. We suggest that the adaptive radiation of bill morphology should be reinterpreted with both preening and feeding in mind.     

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.     

Metazoan parasite species richness and genetic variation among freshwater fish species: cause or consequence?

The factors responsible for the maintenance of genetic variation among natural populations remain a mystery. Recent models of host-parasite co-evolution assume that parasites exert frequency-dependent selection on their hosts by favouring rare alleles that may confer resistance against infection. We tested this prediction in a comparative analysis that sought relationships between levels of genetic variation and the number of metazoan parasite species exploiting each host species. We used data on 40 species of North American freshwater fishes. After controlling for sampling effort and phylogenetic influences, we found no relationship between genetic polymorphism and parasite species richness among fish species. However, we found a marginal negative correlation between parasite species richness and heterozygosity. This result goes against the prediction that increased selective pressure by parasites should be associated with higher levels of genetic variation. Instead, it suggests that parasites may be colonising host species showing low levels of genetic variation with greater success than genetically more variable host species.     

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.     

The positive correlation between avian species richness and human population density in Britain is not attributable to sampling bias

Aim  To assess whether spatial variation in sampling effort drives positive correlations between human population density and species richness.
Location  British 10 × 10 km squares.
Methods  We calculated three measures of species richness from atlas data of breeding birds in Britain: total species richness, species richness standardised for sampling effort, and the number of species only recorded in supplementary casual records in a manner not standardised for survey effort. We then assessed the form of the relationship between these richness estimates and human population density, both with and without taking spatial autocorrelation into account.
Results  Both total and standardised species richness exhibit similar species richness–human population density relationships; species richness generally increases with human population density, but decreases at the very highest densities. Supplementary species richness is very weakly correlated with human population density.
Main conclusions  In this example, sampling effort only slightly influences the form of species richness–human population density relationships. The positive correlation between species richness and human population density and any resultant conservation conflicts are thus not artefactual patterns generated by confounding human density and sampling effort.     

Comparative tests of parasite species richness in primates

Some hosts harbor diverse parasite communities, whereas others are relatively parasite free. Many factors have been proposed to account for patterns of parasite species richness, but few studies have investigated competing hypotheses among multiple parasite communities in the same host clade. We used a comparative data set of 941 host-parasite combinations, representing 101 anthropoid primate species and 231 parasite taxa, to test the relative importance of four sets of variables that have been proposed as determinants of parasite community diversity in primates: host body mass and life history, social contact and population density, diet, and habitat diversity. We defined parasites broadly to include not only parasitic helminths and arthropods but also viruses, bacteria, fungi, and protozoa, and we controlled for effects of uneven sampling effort on per-host measures of parasite diversity. In nonphylogenetic tests, body mass was correlated with total parasite diversity and the diversity of helminths and viruses. When phylogeny was taken into account, however, body mass became nonsignificant. Host population density, a key determinant of parasite spread in many epidemiological models, was associated consistently with total parasite species richness and the diversity of helminths, protozoa, and viruses tested separately. Geographic range size and day range length explained significant variation in the diversity of viruses.     

Parasite richness/sampling effort/host range: the fancy three-piece jigsaw puzzle

In this article, Jean-Fran?ois Guégan and Clive Kennedy propose an alternative explanation for the confounding effects of host geographical range and sampling effort on parasite species richness using pathway analysis procedure. They suggest that much of the species richness revealed by sampling effort is also a reflection of host range. Thus, the total contribution of host range logically incorporates a contribution from sampling effort. The implications of indirect effects of host range on richness estimates have not previously been discussed, and the authors here attempt to redress the balance. The contribution of host range to richness, as derived from control of sampling effort on richness estimates, therefore, is a mathematical expression that does not take into account the cause-and-effect nature of things.     

Niche theory‐based modeling of assembly processes of viral communities in bats

Understanding the assembly processes of symbiont communities, including viromes and microbiomes, is important for improving predictions on symbionts’ biogeography and disease ecology. Here, we use phylogenetic, functional, and geographic filters to predict the similarity between symbiont communities, using as a test case the assembly process in viral communities of Mexican bats. We construct generalized linear models to predict viral community similarity, as measured by the Jaccard index, as a function of differences in host phylogeny, host functionality, and spatial co‐occurrence, evaluating the models using the Akaike information criterion. Two model classes are constructed: a “known” model, where virus–host relationships are based only on data reported in Mexico, and a “potential” model, where viral reports of all the Americas are used, but then applied only to bat species that are distributed in Mexico. Although the “known” model shows only weak dependence on any of the filters, the “potential” model highlights the importance of all three filter types—phylogeny, functional traits, and co‐occurrence—in the assemblage of viral communities. The differences between the “known” and “potential” models highlight the utility of modeling at different “scales” so as to compare and contrast known information at one scale to another one, where, for example, virus information associated with bats is much scarcer.     

Metabarcoding of eukaryotic parasite communities describes diverse parasite assemblages spanning the primate phylogeny

Despite their ubiquity, in most cases little is known about the impact of eukaryotic parasites on their mammalian hosts. Comparative approaches provide a powerful method to investigate the impact of parasites on host ecology and evolution, though two issues are critical for such efforts: controlling for variation in methods of identifying parasites and incorporating heterogeneity in sampling effort across host species. To address these issues, there is a need for standardized methods to catalogue eukaryotic parasite diversity across broad phylogenetic host ranges. We demonstrate the feasibility of a metabarcoding approach for describing parasite communities by analysing faecal samples from 11 nonhuman primate species representing divergent lineages of the primate phylogeny and the full range of sampling effort (i.e. from no parasites reported in the literature to the best‐studied primates). We detected a number of parasite families and regardless of prior sampling effort, metabarcoding of only ten faecal samples identified parasite families previously undescribed in each host (x? = 8.5 new families per species). We found more overlap between parasite families detected with metabarcoding and published literature when more research effort—measured as the number of publications—had been conducted on the host species' parasites. More closely related primates and those from the same continent had more similar parasite communities, highlighting the biological relevance of sampling even a small number of hosts. Collectively, results demonstrate that metabarcoding methods are sensitive and powerful enough to standardize studies of eukaryotic parasite communities across host species, providing essential new tools for macroecological studies of parasitism.     

Diversity and composition of phytophagous insect guilds on Brassicaceae

We investigated the guild structure of phytophagous insects on Brassicaceae in Poland and the influence of host-plant parameters (e.g. sampling effort, geographical distribution, taxonomic isolation, nitrogen indicator values) on the species richness of these guilds. The data were extracted from a study published by Lipa et al. The overall number of recorded ectophagous species is about twice the number of endophagous species. Irrespective of the feeding niche, species are predominantly oligophagous, feeding on more than two Brassicaceae genera. The relative importance of endophagous species within the fauna decreases with increasing host range. The sampling effort predicts a high proportion of the variance of alpha-diversity in oligo- and polyphagous insects, but only a low proportion in specialized species. After correction for sampling effort, most of the plant parameters do not explain an additional proportion of the variance in species richness. We hypothesize that the uniform chemical defence system across genera in Brassicaceae is an important factor triggering host range and diversity patterns in phytophagous insects on crucifers. Received: 3 April 1997 / Accepted: 22 September 1997     

The evolutionary genetics of emerging plant RNA viruses

Over the years, agriculture across the world has been compromised by a succession of devastating epidemics caused by new viruses that spilled over from reservoir species or by new variants of classic viruses that acquired new virulence factors or changed their epidemiological patterns. Viral emergence is usually associated with ecological change or with agronomical practices bringing together reservoirs and crop species. The complete picture is, however, much more complex, and results from an evolutionary process in which the main players are ecological factors, viruses' genetic plasticity, and host factors required for virus replication, all mixed with a good measure of stochasticity. The present review puts emergence of plant RNA viruses into the framework of evolutionary genetics, stressing that viral emergence begins with a stochastic process that involves the transmission of a preexisting viral strain into a new host species, followed by adaptation to the new host.