The Evolution and Genetics of Virus Host Shifts

Emerging viral diseases are often the product of a host shift, where a pathogen jumps from its original host into a novel species. Phylogenetic studies show that host shifts are a frequent event in the evolution of most pathogens, but why pathogens successfully jump between some host species but not others is only just becoming clear. The susceptibility of potential new hosts can vary enormously, with close relatives of the natural host typically being the most susceptible. Often, pathogens must adapt to successfully infect a novel host, for example by evolving to use different cell surface receptors, to escape the immune response, or to ensure they are transmitted by the new host. In viruses there are often limited molecular solutions to achieve this, and the same sequence changes are often seen each time a virus infects a particular host. These changes may come at a cost to other aspects of the pathogen''s fitness, and this may sometimes prevent host shifts from occurring. Here we examine how these evolutionary factors affect patterns of host shifts and disease emergence.     

Vertically transmitted viral endosymbionts of insects: do sigma viruses walk alone?

Insects are host to a wide range of vertically transmitted bacterial endosymbionts, but we know relatively little about their viral counterparts. Here, we discuss the vertically transmitted viral endosymbionts of insects, firstly examining the diversity of this group, and then focusing on the well-studied sigma viruses that infect dipterans. Despite limited sampling, evidence suggests that vertically transmitted viruses may be common in insects. Unlike bacteria, viruses can be transmitted through sperm and eggs, a trait that allows them to rapidly spread through host populations even when infection is costly to the host. Work on Drosophila melanogaster has shown that sigma viruses and their hosts are engaged in a coevolutionary arms race, in which the spread of resistance genes in the host population is followed by the spread of viral genotypes that can overcome host resistance. In the long-term, associations between sigma viruses and their hosts are unstable, and the viruses persist by occasionally switching to new host species. It therefore seems likely that viral endosymbionts have major impacts on the evolution and ecology of insects.     

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.     

Phylogenetic determinants of potential host shifts in fungal pathogens

Understanding what determines the host range of pathogens and the potential for host shifts is of critical importance to controlling their introductions into new environments. The phylogeny of the hosts has been shown to be important: pathogens are more likely to be infectious on hosts closely related to their host‐of‐origin because of the similar host environments that is shared by descent. The importance of pathogen phylogenies for predicting host range has never been investigated, although a pathogen should also be able to exploit a new host that its close relative can infect. We performed cross‐inoculations using a plant–fungal association and showed that both host and pathogen phylogenies were significant predictors of host range, with at least partly independent effects. Furthermore, we showed that some pathogens were better at infecting novel hosts. Our results should have implications in the context of biological invasions and emergences of new diseases due to globalization.     

Clade-limited colonization in brood parasitic finches (Vidua spp.)

The African brood parasitic finches (Vidua spp.) are host specialists that mimic the songs and nestling mouth markings of their finch hosts (family Estrildidae). Although recent molecular analyses suggest rapid speciation associated with host switches in some members of this group, the association of different Vidua lineages with particular host genera suggests the possibility of cospeciation at higher levels in the host and parasite phylogenies. We compared a phylogeny of all Vidua species with a phylogeny of their estrildid finch hosts and compared divergence time estimates for the two groups. Basal divergences among extant members of the Vidulidae and among Vidua species are more recent than those among host genera and species, respectively, allowing a model of cospeciation to be rejected at most or all levels of the Vidua phylogeny. Nonetheless, some tests for cospeciation indicated significant congruence between host and parasite tree topologies. This result may be an artifact of clade-limited colonization. Host switches in parasitic finches have most often involved new hosts in the same or a closely related genus, an effect that increases the apparent congruence of host and parasites trees.     

Host-Specific Parvovirus Evolution in Nature Is Recapitulated by In Vitro Adaptation to Different Carnivore Species

Canine parvovirus (CPV) emerged as a new pandemic pathogen of dogs in the 1970s and is closely related to feline panleukopenia virus (FPV), a parvovirus of cats and related carnivores. Although both viruses have wide host ranges, analysis of viral sequences recovered from different wild carnivore species, as shown here, demonstrated that >95% were derived from CPV-like viruses, suggesting that CPV is dominant in sylvatic cycles. Many viral sequences showed host-specific mutations in their capsid proteins, which were often close to sites known to control binding to the transferrin receptor (TfR), the host receptor for these carnivore parvoviruses, and which exhibited frequent parallel evolution. To further examine the process of host adaptation, we passaged parvoviruses with alternative backgrounds in cells from different carnivore hosts. Specific mutations were selected in several viruses and these differed depending on both the background of the virus and the host cells in which they were passaged. Strikingly, these in vitro mutations recapitulated many specific changes seen in viruses from natural populations, strongly suggesting they are host adaptive, and which were shown to result in fitness advantages over their parental virus. Comparison of the sequences of the transferrin receptors of the different carnivore species demonstrated that many mutations occurred in and around the apical domain where the virus binds, indicating that viral variants were likely selected through their fit to receptor structures. Some of the viruses accumulated high levels of variation upon passage in alternative hosts, while others could infect multiple different hosts with no or only a few additional mutations. Overall, these studies demonstrate that the evolutionary history of a virus, including how long it has been circulating and in which hosts, as well as its phylogenetic background, has a profound effect on determining viral host range.     

You stay,but I Hop: Host shifting near and far co‐dominated the evolution of Enchenopa treehoppers

The importance and prevalence of phylogenetic tracking between hosts and dependent organisms caused by co‐evolution and shifting between closely related host species have been debated for decades. Most studies of phylogenetic tracking among phytophagous insects and their host plants have been limited to insects feeding on a narrow range of host species. However, narrow host ranges can confound phylogenetic tracking (phylogenetic tracking hypothesis) with host shifting between hosts of intermediate relationship (intermediate hypothesis). Here, we investigated the evolutionary history of the Enchenopa binotata complex of treehoppers. Each species in this complex has high host fidelity, but the entire complex uses hosts across eight plant orders. The phylogenies of E. binotata were reconstructed to evaluate whether (1) tracking host phylogeny; or (2) shifting between intermediately related host plants better explains the evolutionary history of E. binotata. Our results suggest that E. binotata primarily shifted between both distant and intermediate host plants regardless of host phylogeny and less frequently tracked the phylogeny of their hosts. These findings indicate that phytophagous insects with high host fidelity, such as E. binotata, are capable of adaptation not only to closely related host plants but also to novel hosts, likely with diverse phenology and defense mechanisms.     

Phylogeny and geography predict pathogen community similarity in wild primates and humans

In natural systems, host species are often co-infected by multiple pathogen species, and recent work has suggested that many pathogens can infect a wide range of host species. An important question therefore is what determines the host range of a pathogen and the community of pathogens found within a given host species. Using primates as a model, we show that infectious diseases are more often shared between species that are closely related and inhabit the same geographical region. We find that host relatedness is the best overall predictor of whether two host species share the same pathogens. A higher frequency of pathogen host shifts between close relatives or inheritance of pathogens from a common ancestor may explain this result. For viruses, geographical overlap among neighbouring primate hosts is more important in determining host range. We suggest this is because rapid evolution within viral lineages allows host jumps across larger evolutionary distances. We also show that the phylogenetic pattern of pathogen sharing with humans is the same as that between wild primates. For humans, this means we share a higher proportion of pathogens with the great apes, including chimpanzees and gorillas, because these species are our closest relatives.     

BUTTERFLIES AND PLANTS: A PHYLOGENETIC STUDY

A database on host plant records from 437 ingroup taxa has been used to test a number of hypotheses on the interaction between butterflies and their host plants using phylogenetic methods (simple character optimization, concentrated changes test, and independent contrasts test). The butterfly phylogeny was assembled from various sources and host plant clades were identified according to Chase et al.'s rbcL-based phylogeny. The ancestral host plant appears to be associated within a highly derived rosid clade, including the family Fabaceae. As fossil data suggest that this clade is older than the butterflies, they must have colonized already diversified plants. Previous studies also suggest that the patterns of association in most insect-plant interactions are more shaped by host shifts, through colonization and specialization, than by cospeciation. Consequently, we have focused explicitly on the mechanisms behind host shifts. Our results confirm, in the light of new phylogenetic evidence, the pattern reported by Ehrlich and Raven that related butterflies feed on related plants. We show that host shifts have generally been more common between closely related plants than between more distantly related plants. This finding, together with the possibility of a higher tendency of recolonizing ancestral hosts, helps to explain the apparent large-scale conservation in the patterns of association between insects and their host plants, patterns which at the same time are more flexible on a more detailed level. Plant growth form was an even more conservative aspect of the interaction between butterflies and their host plants than plant phylogeny. However, this is largely explained by a higher probability of colonizations and host shifts while feeding on trees than on other growth forms.     

A SIMPLE MODEL EXPLAINS THE DYNAMICS OF PREFERENTIAL HOST SWITCHING AMONG MAMMAL RNA VIRUSES

A growing number of studies support a tendency toward preferential host switching, by parasites and pathogens, over relatively short phylogenetic distances. This suggests that a host switch is more probable if a potential host is closely related to the original host than if it is a more distant relative. However, despite its importance for the health of humans, livestock, and wildlife, the detailed dynamics of preferential host switching have, so far, been little studied. We present an empirical test of two theoretical models of preferential host switching, using observed phylogenetic distributions of host species for RNA viruses of three mammal orders (primates, carnivores, and ungulates). The analysis focuses on multihost RNA virus species, because their presence on multiple hosts and their estimated ages of origin indicate recent host switching. Approximate Bayesian computation was used to compare observed phylogenetic distances between hosts with those simulated under the theoretical models. The results support a decreasing sigmoidal model of preferential host switching, with a strong effect from increasing phylogenetic distance, on all three studied host phylogenies. This suggests that the dynamics of host switching are fundamentally similar for RNA viruses of different mammal orders and, potentially, a wider range of coevolutionary systems.     

Evolutionary dynamics of host-plant use in a genus of leaf-mining moths

Abstract. We used nuclear 28S rDNA sequence data to estimate the phylogeny of 77 leaf-mining Phyllonorycter (Gracillariidae) moth species, including all 55 British species, feeding on 44 different plant genera. There was strong support for both the monophyly of Phyllonorycter and the placement of the genus Cameraria as its sister group. Host-plant use was mapped onto the moth phylogeny and investigated statistically in several ways. First, we show that the estimated level of cospeciation between leaf miners and their host plants is not greater than expected by chance, despite the physical intimacy of the association. Nevertheless, the pattern of host-plant use is far from random, with closely related Phyllonorycter species generally feeding on closely related plants. However, although Phyllonorycter species from a given host plant tend to form distinct clades, there is also statistical support for multiple independent colonizations of some host-plant taxa (e.g. the order Rosales and the genus Corylus ). Despite numerous host shifts, most Phyllonorycter species feed on trees and the few species that attack shrubs or herbs have mostly acquired these habits independently. There is also limited evidence that host shifts to herbs are more likely from shrubs than from trees. Similarly, most species mine the lower surface of leaves but the few upper-surface miners have each evolved the habit independently. Consequently, these shifts to new adaptive zones have not led to substantial radiations.     

Infection success in novel hosts: an experimental and phylogenetic study of Drosophila-parasitic nematodes

Surprisingly little is known about what determines a parasite's host range, which is essential in enabling us to predict the fate of novel infections. In this study, we evaluate the importance of both host and parasite phylogeny in determining the ability of parasites to infect novel host species. Using experimental lab assays, we infected 24 taxonomically diverse species of Drosophila flies (Diptera: Drosophilidae) with five different nematode species (Tylenchida: Allantonematidae: Howardula, Parasitylenchus), and measured parasite infection success, growth, and effects on female host fecundity (i.e., virulence). These nematodes are obligate parasites of mushroom-feeding Drosophila, particularly quinaria and testacca group species, often with severe fitness consequences on their hosts. We show that the potential host ranges of the nematodes are much larger than their actual ranges, even for parasites with only one known host species in nature. Novel hosts that are distantly related from the native host are much less likely to be infected, but among more closely related hosts, there is much variation in susceptibility. Potential host ranges differ greatly between the related parasite species. All nematode species that successfully infected novel hosts produced infective juveniles in these hosts. Most novel infections did not result in significant reductions in the fecundity of female hosts, with one exception: the host specialist Parasitylenchus nearcticus sterilized all quinaria group hosts, only one of which is a host in nature. The large potential host ranges of these parasites, in combination with the high potential for host colonization due to shared mushroom breeding sites, explain the widespread host switching observed in comparisons of nematode and Drosophila phylogenies.     

The roles of ecological fitting, phylogeny and physiological equivalence in understanding realized and fundamental host ranges in endoparasitoid wasps

Co-evolutionary theory underpins our understanding of interactions in nature involving plant-herbivore and host-parasite interactions. However, many studies that are published in the empirical literature that have explored life history and development strategies between endoparasitoid wasps and their hosts are based on species that have no evolutionary history with one another. Here, we investigated novel associations involving two closely related solitary endoparasitoids that originate from Europe and North America and several of their natural and factitious hosts from both continents. The natural hosts of both species are also closely related, all being members of the same family. We compared development and survival of both parasitoids on the four host species and predicted that parasitoid performance is better on their own natural hosts. In contrast with this expectation, survival, adult size and development time of both parasitoids were similar on all (with one exception) hosts, irrespective as to their geographic origin. Our results show that phylogenetic affinity among the natural and factitious hosts plays an important role in their nutritional suitability for related parasitoids. Evolved traits in parasitoids, such as immune suppression and development, thus enable them to successfully develop in novel host species with which they have no evolutionary history. Our results show that host suitability for specialized organisms like endoparasitoids is closely linked with phylogenetic history and macro-evolution as well as local adaptation and micro-evolution. We argue that the importance of novel interactions and 'ecological fitting' based on phylogeny is a greatly underappreciated concept in many resource-consumer studies.     

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.     

New hepatitis B virus of cranes that has an unexpected broad host range

All hepadnaviruses known so far have a very limited host range, restricted to their natural hosts and a few closely related species. This is thought to be due mainly to sequence divergence in the large envelope protein and species-specific differences in host components essential for virus propagation. Here we report an infection of cranes with a novel hepadnavirus, designated CHBV, that has an unexpectedly broad host range and is only distantly evolutionarily related to avihepadnaviruses of related hosts. Direct DNA sequencing of amplified CHBV DNA as well a sequencing of cloned viral genomes revealed that CHBV is most closely related to, although distinct from, Ross' goose hepatitis B virus (RGHBV) and slightly less closely related to duck hepatitis B virus (DHBV). Phylogenetically, cranes are very distant from geese and ducks and are most closely related to herons and storks. Naturally occurring hepadnaviruses in the last two species are highly divergent in sequence from RGHBV and DHBV and do not infect ducks or do so only marginally. In contrast, CHBV from crane sera and recombinant CHBV produced from LMH cells infected primary duck hepatocytes almost as efficiently as DHBV did. This is the first report of a rather broad host range of an avihepadnavirus. Our data imply either usage of similar or identical entry pathways and receptors by DHBV and CHBV, unusual host and virus adaptation mechanisms, or divergent evolution of the host genomes and cellular components required for virus propagation.     

Cross-Species Virus Transmission and the Emergence of New Epidemic Diseases

Summary: Host range is a viral property reflecting natural hosts that are infected either as part of a principal transmission cycle or, less commonly, as “spillover” infections into alternative hosts. Rarely, viruses gain the ability to spread efficiently within a new host that was not previously exposed or susceptible. These transfers involve either increased exposure or the acquisition of variations that allow them to overcome barriers to infection of the new hosts. In these cases, devastating outbreaks can result. Steps involved in transfers of viruses to new hosts include contact between the virus and the host, infection of an initial individual leading to amplification and an outbreak, and the generation within the original or new host of viral variants that have the ability to spread efficiently between individuals in populations of the new host. Here we review what is known about host switching leading to viral emergence from known examples, considering the evolutionary mechanisms, virus-host interactions, host range barriers to infection, and processes that allow efficient host-to-host transmission in the new host population.     

Molecular mechanisms of pathogenicity: how do pathogenic microorganisms develop cross-kingdom host jumps?

It is common knowledge that pathogenic viruses can change hosts, with avian influenza, the HIV, and the causal agent of variant Creutzfeldt-Jacob encephalitis as well-known examples. Less well known, however, is that host jumps also occur with more complex pathogenic microorganisms such as bacteria and fungi. In extreme cases, these host jumps even cross kingdom of life barriers. A number of requirements need to be met to enable a microorganism to cross such kingdom barriers. Potential cross-kingdom pathogenic microorganisms must be able to come into close and frequent contact with potential hosts, and must be able to overcome or evade host defences. Reproduction on, in, or near the new host will ensure the transmission or release of successful genotypes. An unexpectedly high number of cross-kingdom host shifts of bacterial and fungal pathogens are described in the literature. Interestingly, the molecular mechanisms underlying these shifts show commonalities. The evolution of pathogenicity towards novel hosts may be based on traits that were originally developed to ensure survival in the microorganism's original habitat, including former hosts.     

Phylogenetic analyses of DNA and allozyme data suggest that Gonioctena leaf beetles (Coleoptera; Chrysomelidae) experienced convergent evolution in their history of host-plant family shifts

A phylogenetic analysis of the genus Gonioctena (Coleoptera, Chrysomelidae) based on allozyme data (17 loci) and mitochondrial DNA sequence data (three gene fragments, 1,391 sites) was performed to study the evolutionary history of host-plant shifts among these leaf beetles. This chrysomelid genus is characteristically associated with a high number of different plant families. The diverse molecular data gathered in this study are to a large extent congruent, and the analyses provide a well-supported phylogenetic hypothesis to address questions about the evolution of host-plant shifts in the genus Gonioctena. The most-parsimonious reconstruction of the ancestral host-plant associations, based on the estimated phylogeny, suggests that the Fabaceae was the ancestral host-plant family of the genus. Although most of the host-plant shifts (between different host species) in Gonioctena have occurred within the same plant family or within the same plant genus, at least eight shifts have occurred between hosts belonging to distantly related and chemically dissimilar plant families. In these cases, host shifts may have been simply directed toward plant species available in the environment. Yet, given that two Gonioctena lineages have independently colonized the same three new plant families (Salicaceae, Betulaceae, Rosaceae), including four of the same new genera (Salix, Alnus, Prunus, Sorbus), some constraints are likely to have limited the different possibilities of interfamilial host-plant shifts.     

Comparison of Viromes in Ticks from Different Domestic Animals in China

Ticks are involved in the transmission of various arboviruses and some tick-borne viruses pose significant threats to the health of humans or livestock. This study aimed to investigate the geographical distribution of tick species and tickassociated viruses in central and eastern China. Total 573 ticks from domestic animals including dogs, sheep and cattle were collected in 2017. Two genera of ticks were identified including Rhipicephalus and Haemaphysalis. Sequencing was performed on Miseq Illumina platform to characterize the tick viromes from the four different sampling locations.Following trimming, 13,640 reads were obtained and annotated to 19 virus families. From these sequences, above 37.74% of the viral reads were related to the RNA viruses. Virome comparison study revealed that the tick viral diversity was considerably different in the two identified tick genera. The viral diversity of R. microplus was significantly different from that of other Rhipicephalus species. On the other hand, substantial overlap in viral species was observed between the same genera. In addition, we found no evidence that the natural host played a major role in shaping virus diversity based on the comparison of their viromes. Rather, the geographic location seems to significantly influence the viral families. Phylogenetic study indicated that the novel negative-sense RNA viruses identified in this study was closely related to Bole tick virus 1 and 3 viruses. In conclusion, the present study provides a baseline for comparing viruses detected in ticks, according to species, natural hosts, and geographic locations.     

Evolutionary genomics of host-use in bifurcating demes of RNA virus phi-6

ABSTRACT: BACKGROUND: Viruses are exceedingly diverse in their evolved strategies to manipulate hosts for viral replication. However, despite these differences, most virus populations will occasionally experience two commonly-encountered challenges: growth in variable host environments, and growth under fluctuating population sizes. We used the segmented RNA bacteriophage [GREEK PHI SYMBOL]6 as a model for studying the evolutionary genomics of virus adaptation in the face of host switches and parametrically varying population sizes. To do so, we created a bifurcating deme structure that reflected lineage splitting in natural populations, allowing us to test whether phylogenetic algorithms could accurately resolve this 'known phylogeny'. The resulting tree yielded 32 clones at the tips and internal nodes; these strains were fully sequenced and measured for phenotypic changes in selected traits (fitness on original and novel hosts). RESULTS: We observed that RNA segment size was negatively correlated with the extent of molecular change in the imposed treatments; molecular substitutions tended to cluster on the Small and Medium RNA chromosomes of the virus, and not on the Large segment. Our study yielded a very large molecular and phenotypic dataset, fostering possible inferences on genotype-phenotype associations. Using further experimental evolution, we confirmed an inference on the unanticipated role of an allelic switch in a viral assembly protein, which governed viral performance across host environments. CONCLUSIONS: Our study demonstrated that varying complexities can be simultaneously incorporated into experimental evolution, to examine the combined effects of population size, and adaptation in novel environments. The imposed bifurcating structure revealed that some methods for phylogenetic reconstruction failed to resolve the true phylogeny, owing to a paucity of molecular substitutions separating the RNA viruses that evolved in our study.