scholarly journals Between virus correlations in the outcome of infection across host species: evidence of virus genotype by host species interactions

2021 ◽  
Author(s):  
Ryan M. Imrie ◽  
Katherine E. Roberts ◽  
Ben Longdon

AbstractVirus host shifts are a major source of outbreaks and emerging infectious diseases, and predicting the outcome of novel host and virus interactions remains a key challenge for virus research. The evolutionary relationships between host species can explain variation in transmission rates, virulence, and virus community composition between hosts, but the potential for different viruses to interact with host species effects has yet to be established. Here, we measure correlations in viral load of four Cripavirus isolates across experimental infections of 45 Drosophilidae host species. We find positive correlations between every pair of viruses tested, suggesting that broadly susceptible host clades could act as reservoirs and donors for certain types of viruses. Additionally, we find evidence of genotype-by-genotype interactions between viruses and host species, highlighting the importance of both host and virus traits in determining the outcome of virus host shifts. More closely related viruses tended to be more strongly correlated, providing tentative evidence that virus evolutionary relatedness may be a useful proxy for determining the likelihood of novel virus emergence, which warrants further research.Impact SummaryMany new infectious diseases are caused by viruses jumping into novel host species. Estimating the probability that jumps will occur, what the characteristics of new viruses will be, and how they are likely to evolve after jumping to new host species are major challenges. To solve these challenges, we require a detailed understanding of the interactions between different viruses and hosts, or metrics that can capture some of the variation in these interactions. Previous studies have shown that the evolutionary relationships between host species can be used to predict traits of infections in different hosts, including transmission rates and the damage caused by infection. However, the potential for different viruses to influence the patterns of these host species effects has yet to be determined. Here, we use four viruses of insects in experimental infections across 45 different fruit fly host species to begin to answer this question. We find similarities in the patterns of replication and persistence between all four viruses, suggesting susceptible groups of related hosts could act as reservoirs and donors for certain types of virus. However, we also find evidence that different virus genotypes interact in different ways with some host species. Viruses that were more closely related tended to behave in similar ways, and so we suggest that virus evolutionary relatedness may prove to be a useful metric for predicting the traits of novel infections and should be explored further in future studies.

2021 ◽  
Author(s):  
Joanne S. Griffin ◽  
Michael Gerth ◽  
Gregory D. D. Hurst

AbstractHeritable symbionts represent important components of host biology, both as antagonistic reproductive parasites and as beneficial protective partners. An important component of heritable microbes’ biology is their ability to establish in new host species, a process equivalent to a host shift for an infectiously transmitted parasite or pathogen. For a host shift to occur, the symbiont must be compatible with the host: it must not cause excess pathology, must have good vertical transmission, and possess a drive phenotype that enables spread. Classically, compatibility has been considered a declining function of genetic distance between novel and ancestral host species. Here we investigate the evolutionary lability of compatibility to heritable microbes by comparing the capacity for a symbiont to establish in two novel host species equally related to the ancestral host. Compatibility of the protective Spiroplasma from D. hydei with D. simulans and D. melanogaster was tested. The Spiroplasma had contrasting compatibility in these two host species. The transinfection showed pathology and low vertical transmission in D. melanogaster but was asymptomatic and transmitted with high efficiency in D. simulans. These results were not affected by the presence/absence of Wolbachia in either of the two species. The pattern of protection was not congruent with that for pathology/transmission, with protection being weaker in the D. simulans, the host in which Spiroplasma was asymptomatic and transmitted well. Further work indicated pathological interactions occurred in D. sechellia and D. yakuba, indicating that D. simulans was unusual in being able to carry the symbiont without damage. The differing compatibility of the symbiont with these closely related host species emphasises first the rapidity with which host-symbiont compatibility evolves despite compatibility itself not being subject to direct selection, and second the independence of the different components of compatibility (pathology, transmission, protection). This requirement to fit three different independently evolving aspects of compatibility, if commonly observed, is likely to be a major feature limiting the rate of host shifts. Moving forward, the variation between sibling species pairs observed above provides an opportunity to identify the mechanisms behind variable compatibility between closely related host species, which will drive hypotheses as to the evolutionary drivers of compatibility variation.


2017 ◽  
Author(s):  
Ben Longdon ◽  
Jonathan P Day ◽  
Joel M Alves ◽  
Sophia CL Smith ◽  
Thomas M Houslay ◽  
...  

AbstractHost shifts, where a pathogen invades and establishes in a new host species, are a major source of emerging infectious diseases. They frequently occur between related host species and often rely on the pathogen evolving adaptations that increase their fitness in the novel host species. To investigate genetic changes in novel hosts, we experimentally evolved replicate lineages of an RNA virus (Drosophila C Virus) in 19 different species of Drosophilidae and deep sequenced the viral genomes. We found a strong pattern of parallel evolution, where viral lineages from the same host were genetically more similar to each other than to lineages from other host species. When we compared viruses that had evolved in different host species, we found that parallel genetic changes were more likely to occur if the two host species were closely related. This suggests that when a virus adapts to one host it might also become better adapted to closely related host species. This may explain in part why host shifts tend to occur between related species, and may mean that when a new pathogen appears in a given species, closely related species may become vulnerable to the new disease.


2019 ◽  
Vol 116 (16) ◽  
pp. 7911-7915 ◽  
Author(s):  
Maxwell J. Farrell ◽  
T. Jonathan Davies

Infectious diseases of domesticated animals impact human well-being via food insecurity, loss of livelihoods, and human infections. While much research has focused on parasites that infect single host species, most parasites of domesticated mammals infect multiple species. The impact of multihost parasites varies across hosts; some rarely result in death, whereas others are nearly always fatal. Despite their high ecological and societal costs, we currently lack theory for predicting the lethality of multihost parasites. Here, using a global dataset of >4,000 case-fatality rates for 65 infectious diseases (caused by microparasites and macroparasites) and 12 domesticated host species, we show that the average evolutionary distance from an infected host to other mammal host species is a strong predictor of disease-induced mortality. We find that as parasites infect species outside of their documented phylogenetic host range, they are more likely to result in lethal infections, with the odds of death doubling for each additional 10 million years of evolutionary distance. Our results for domesticated animal diseases reveal patterns in the evolution of highly lethal parasites that are difficult to observe in the wild and further suggest that the severity of infectious diseases may be predicted from evolutionary relationships among hosts.


2020 ◽  
Vol 117 (46) ◽  
pp. 28859-28866 ◽  
Author(s):  
Nardus Mollentze ◽  
Daniel G. Streicker ◽  
Pablo R. Murcia ◽  
Katie Hampson ◽  
Roman Biek

Whether a pathogen entering a new host species results in a single infection or in onward transmission, and potentially an outbreak, depends upon the progression of infection in the index case. Although index infections are rarely observable in nature, experimental inoculations of pathogens into novel host species provide a rich and largely unexploited data source for meta-analyses to identify the host and pathogen determinants of variability in infection outcomes. We analyzed the progressions of 514 experimental cross-species inoculations of rabies virus, a widespread zoonosis which in nature exhibits both dead-end infections and varying levels of sustained transmission in novel hosts. Inoculations originating from bats rather than carnivores, and from warmer- to cooler-bodied species caused infections with shorter incubation periods that were associated with diminished virus excretion. Inoculations between distantly related hosts tended to result in shorter clinical disease periods, which are also expected to impede onward transmission. All effects were modulated by infection dose. Taken together, these results suggest that as host species become more dissimilar, increased virulence might act as a limiting factor preventing onward transmission. These results can explain observed constraints on rabies virus host shifts, describe a previously unrecognized role of host body temperature, and provide a potential explanation for host shifts being less likely between genetically distant species. More generally, our study highlights meta-analyses of experimental infections as a tractable approach to quantify the complex interactions between virus, reservoir, and novel host that shape the outcome of cross-species transmission.


2020 ◽  
Author(s):  
Nardus Mollentze ◽  
Daniel G. Streicker ◽  
Pablo R. Murcia ◽  
Katie Hampson ◽  
Roman Biek

AbstractWhether a pathogen entering a new host species results in a single infection or in onward transmission, and potentially an outbreak, depends upon the progression of infection in the index case. Although index infections are rarely observable in nature, experimental inoculations of pathogens into novel host species have a long history in biomedical research. This provides a rich and largely unexploited data source for meta-analyses to identify the host and pathogen determinants of variability in infection outcomes. Here, we analysed the progressions of 514 experimental cross-species inoculations of rabies virus, a widespread zoonotic pathogen which in nature exhibits both dead end infections and varying levels of sustained transmission in novel hosts. Inoculations originating from bats rather than carnivores, and from warmer to cooler-bodied species caused infections with shorter incubation periods that were associated with diminished virus excretion. Inoculations between distantly related hosts tended to result in shorter clinical disease periods, which will also impede transmission. All effects were modulated by infection dose and together suggest that increased virulence as host species become more dissimilar is the limiting factor preventing onward transmission. These results explain observed constraints on rabies virus host shifts, allow us to evaluate the risk of novel reservoirs establishing, and give mechanistic insights into why host shifts are less likely between genetically distant species. More generally, our study highlights meta-analyses of experimental infections as a tractable approach to quantify the complex interactions between virus, reservoir, and novel host that shape the outcome of cross-species transmission.Significance statementEmerging disease epidemics often result from a pathogen establishing transmission in a novel host species. However, most cross-species transmissions fail to establish in the newly infected species for reasons that remain poorly understood. Examining cross-species inoculations involving rabies, a widespread viral zoonosis, we show that mismatches in virulence, which are predictable from host and viral factors, make sustained transmission in the novel host less likely. In particular, disease progression was accelerated and virus excretion decreased when the reservoir and novel host were physiologically or genetically more dissimilar. These mechanistic insights help to explain and predict host shift events and highlight meta-analyses of existing experimental inoculation data as a powerful and generalisable approach for understanding the dynamics of index infections in novel species.


2018 ◽  
Author(s):  
Maxwell J. Farrell ◽  
T. J. Davies

AbstractInfectious diseases of domesticated animals impact human well-being via food insecurity, loss of livelihoods, and human infections. While much research has focused on parasites that infect single host species, most parasites of domesticated mammals infect multiple species. The impact of multi-host parasites varies across hosts; some rarely result in death, whereas others are nearly always fatal. Despite their high ecological and societal costs, we currently lack theory for predicting the lethality of multi-host parasites. Here, using a global dataset of over 4000 case-fatality rates for 65 infectious diseases (caused by micro and macro-parasites) and 12 domesticated host species, we show that the average evolutionary distance from an infected host to other mammal host species is a strong predictor of disease-induced mortality. We find that as parasites infect species outside of their documented phy-1 logenetic host range, they are more likely to result in lethal infections, with the odds of death doubling for each additional 10 million years of evolutionary distance. Our results for domesticated animal diseases reveal patterns in the evolution of highly lethal parasites that are difficult to observe in the wild, and further suggest that the severity of infectious diseases may be predicted from evolutionary relationships among hosts.


2009 ◽  
Vol 84 (6) ◽  
pp. 2636-2647 ◽  
Author(s):  
James K. Jancovich ◽  
Michel Bremont ◽  
Jeffrey W. Touchman ◽  
Bertram L. Jacobs

ABSTRACT Members of the genus Ranavirus (family Iridoviridae) have been recognized as major viral pathogens of cold-blooded vertebrates. Ranaviruses have been associated with amphibians, fish, and reptiles. At this time, the relationships between ranavirus species are still unclear. Previous studies suggested that ranaviruses from salamanders are more closely related to ranaviruses from fish than they are to ranaviruses from other amphibians, such as frogs. Therefore, to gain a better understanding of the relationships among ranavirus isolates, the genome of epizootic hematopoietic necrosis virus (EHNV), an Australian fish pathogen, was sequenced. Our findings suggest that the ancestral ranavirus was a fish virus and that several recent host shifts have taken place, with subsequent speciation of viruses in their new hosts. The data suggesting several recent host shifts among ranavirus species increase concern that these pathogens of cold-blooded vertebrates may have the capacity to cross numerous poikilothermic species barriers and the potential to cause devastating disease in their new hosts.


Parasitology ◽  
2000 ◽  
Vol 120 (3) ◽  
pp. 319-327 ◽  
Author(s):  
D. W. KELLY ◽  
C. E. THOMPSON

Existing models of the basic case reproduction number (R0) for vector-borne diseases assume (i) that the distribution of vectors over the susceptible host species is homogenous and (ii) that the biting preference for the susceptible host species rather than other potential hosts is a constant. Empirical evidence contradicts both assumptions, with important consequences for disease transmission. In this paper we develop an Ideal Free Distribution (IFD) model of host choice by blood-sucking insects, predicated on the argument that vectors must have evolved to choose the least defensive hosts in order to maximize their feeding success. From a re-analysis of existing data, we demonstrate that the interference constant, m, of the IFD can vary between host species. As a result, the predicted distribution of insects over hosts has 2 desirable and intuitively plausible behaviours: that it is heterogeneous both within and between host species; and that the intensity of heterogeneity varies with host and vector density. When the IFD model is incorporated into R0, the relationship with the vector: host ratio becomes non-linear. If correct, the IFD could add considerable realism to models which seek to predict the effect of these ecological parameters on disease transmission as they vary naturally (e.g. through seasonality in vector density or host population movement) or as a consequence of artificial manipulation (e.g. zooprophylaxis, vector control). It raises the possibility of targeting transmission hot spots with greater accuracy and concomitant reduction in control effort. The robustness of the model to simplifying assumptions is discussed.


2020 ◽  
Vol 11 ◽  
Author(s):  
Alexander Stephen Byrne ◽  
Alex Goudreau ◽  
Nathalie Bissonnette ◽  
Isdore Chola Shamputa ◽  
Kapil Tahlan

Mixed strain infection (MSI) refers to the concurrent infection of a susceptible host with multiple strains of a single pathogenic species. Known to occur in humans and animals, MSIs deserve special consideration when studying transmission dynamics, evolution, and treatment of mycobacterial diseases, notably tuberculosis in humans and paratuberculosis (or Johne's disease) in ruminants. Therefore, a systematic review was conducted to examine how MSIs are defined in the literature, how widespread the phenomenon is across the host species spectrum, and to document common methods used to detect such infections. Our search strategy identified 121 articles reporting MSIs in both humans and animals, the majority (78.5%) of which involved members of the Mycobacterium tuberculosis complex, while only a few (21.5%) examined non-tuberculous mycobacteria (NTM). In addition, MSIs exist across various host species, but most reports focused on humans due to the extensive amount of work done on tuberculosis. We reviewed the strain typing methods that allowed for MSI detection and found a few that were commonly employed but were associated with specific challenges. Our review notes the need for standardization, as some highly discriminatory methods are not adapted to distinguish between microevolution of one strain and concurrent infection with multiple strains. Further research is also warranted to examine the prevalence of NTM MSIs in both humans and animals. In addition, it is envisioned that the accurate identification and a better understanding of the distribution of MSIs in the future will lead to important information on the epidemiology and pathophysiology of mycobacterial diseases.


Parasitology ◽  
1972 ◽  
Vol 65 (3) ◽  
pp. 403-425 ◽  
Author(s):  
Donald F. J. Hilton ◽  
Jerome L. Mahrt

(1)Spermophilus columbianus, S. franklinii, S. lateralis tescorum, S. richardsonii, S. tridecemlineatusands. undulatus plesius(ground squirrels) were collected from Alberta and Yukon Territory (S. u. plesiusonly), Canada. Trypanosome infections were detected in all butS. l. tescorum. (2) All six species of squirrels were experimentally inoculated with trypanosomes from naturally infectedS. columbianus, S. franklinii, S. richardsoniiandS. tridecemlineatus. The strains fromS. columbianus, S. richardsoniiandS. tridecemlineatusproduced infections in some or all of the other host species, whereas the strain fromS. frankliniidid not. (3) Natural transmission of trypanosomes has not been demonstrated, but it seems likely that fleas act as vectors. (4) Intensities and durations of experimental infections were variable and depended upon the trypanosome strain, host species and individual. Infections were non-pathogenic. (5) Previously infected ground squirrels could not be reinfected with the same or a different trypanosome strain and immunity appeared to be lifelong. (6) Size comparisons among and within trypanosome strains from naturally and experimentally infected ground squirrels revealed that the strains fromS. frankliniiandS. tridecemlineatuswere similar to one another, but different from the other three trypanosome strains (those fromS. columbianus, S. richardsoniiandS. undulatus). (7) It is suggested that there is only one species of trypanosome,Trypanosoma otospermophili, in the genusSpermophilusin North America and that differences in size and types of infection are due to host-induced variations (i.e. they are plastoxenodemes).T. spermophili(present in EurasianSpermophilusspp.) might be synonymous withT. otospermophili.


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