scholarly journals Dynamics of viral index infections in novel hosts

2020 ◽  
Author(s):  
Nardus Mollentze ◽  
Daniel G. Streicker ◽  
Pablo R. Murcia ◽  
Katie Hampson ◽  
Roman Biek
Keyword(s):  
Rabies Virus ◽  
Host Species ◽  
Host Shift ◽  
Single Infection ◽  
Limiting Factor ◽  
New Host ◽  
Host Shifts ◽  
Virus Excretion ◽  
Novel Host ◽  
Meta Analyses

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.

scholarly journals Virulence mismatches in index hosts shape the outcomes of cross-species transmission

2020 ◽  
Vol 117 (46) ◽  
pp. 28859-28866 ◽  
Author(s):  
Nardus Mollentze ◽  
Daniel G. Streicker ◽  
Pablo R. Murcia ◽  
Katie Hampson ◽  
Roman Biek
Keyword(s):  
Rabies Virus ◽  
Host Species ◽  
Single Infection ◽  
Limiting Factor ◽  
New Host ◽  
Host Shifts ◽  
Complex Interactions ◽  
Dead End ◽  
Novel Host ◽  
Meta Analyses

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.

scholarly journals Rapid divergence in independent aspects of the compatibility phenotype in the Spiroplasma/Drosophila interaction

2021 ◽  
Author(s):  
Joanne S. Griffin ◽  
Michael Gerth ◽  
Gregory D. D. Hurst
Keyword(s):  
Vertical Transmission ◽  
Host Species ◽  
High Efficiency ◽  
Host Shift ◽  
Direct Selection ◽  
New Host ◽  
Host Shifts ◽  
Species Pairs ◽  
Novel Host ◽  
Rapid Divergence

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.

scholarly journals Simultaneously reconstructing viral cross-species transmission history and identifying the underlying constraints

2013 ◽  
Vol 368 (1614) ◽  
pp. 20120196 ◽  
Author(s):  
Nuno Rodrigues Faria ◽  
Marc A. Suchard ◽  
Andrew Rambaut ◽  
Daniel G. Streicker ◽  
Philippe Lemey
Keyword(s):  
Rabies Virus ◽  
Host Species ◽  
Bayesian Model Averaging ◽  
Model Averaging ◽  
Viral Gene ◽  
Human Pathogens ◽  
New Host ◽  
Discrete State ◽  
Transition Processes ◽  
Host Shifts

The factors that determine the origin and fate of cross-species transmission events remain unclear for the majority of human pathogens, despite being central for the development of predictive models and assessing the efficacy of prevention strategies. Here, we describe a flexible Bayesian statistical framework to reconstruct virus transmission between different host species based on viral gene sequences, while simultaneously testing and estimating the contribution of several potential predictors of cross-species transmission. Specifically, we use a generalized linear model extension of phylogenetic diffusion to perform Bayesian model averaging over candidate predictors. By further extending this model with branch partitioning, we allow for distinct host transition processes on external and internal branches, thus discriminating between recent cross-species transmissions, many of which are likely to result in dead-end infections, and host shifts that reflect successful onwards transmission in the new host species. Our approach corroborates genetic distance between hosts as a key determinant of both host shifts and cross-species transmissions of rabies virus in North American bats. Furthermore, our results indicate that geographical range overlap is a modest predictor for cross-species transmission, but not for host shifts. Although our evolutionary framework focused on the multi-host reservoir dynamics of bat rabies virus, it is applicable to other pathogens and to other discrete state transition processes.

scholarly journals Host shifts result in parallel genetic changes when viruses evolve in closely related species

2017 ◽  
Author(s):  
Ben Longdon ◽  
Jonathan P Day ◽  
Joel M Alves ◽  
Sophia CL Smith ◽  
Thomas M Houslay ◽  
...  
Keyword(s):  
Host Species ◽  
Related Species ◽  
Rna Virus ◽  
Parallel Evolution ◽  
Emerging Infectious Diseases ◽  
New Host ◽  
Closely Related Species ◽  
Genetic Changes ◽  
Host Shifts ◽  
Novel Host

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.

scholarly journals Genetic analysis of a rabies virus host shift event reveals within-host viral dynamics in a new host

2017 ◽  
Vol 3 (2) ◽  
Author(s):  
Denise A Marston ◽  
Daniel L Horton ◽  
Javier Nunez ◽  
Richard J Ellis ◽  
Richard J Orton ◽  
...  
Keyword(s):  
Genetic Analysis ◽  
Rabies Virus ◽  
Host Shift ◽  
Viral Dynamics ◽  
New Host

scholarly journals Host phylogeny and ecological associations best explain Wolbachia host shifts in scale insects

2021 ◽  
Author(s):  
Ehsan Sanaei ◽  
Gregory F Albery ◽  
Yun Kit Yeoh ◽  
Yen-Po Lin ◽  
Lyn G Cook ◽  
...  
Keyword(s):  
Mixed Model ◽  
Amplicon Sequencing ◽  
Host Shift ◽  
Scale Insect ◽  
Scale Insects ◽  
Phylogenetic Distance ◽  
New Host ◽  
Host Shifts ◽  
Arthropod Species ◽  
Host Phylogeny

AbstractWolbachia are among the most prevalent and widespread endosymbiotic bacteria on earth. Wolbachia’ s success in infecting an enormous number of arthropod species is attributed to two features: the range of phenotypes they induce in their hosts, and their ability to switch to new host species. Whilst much progress has been made in elucidating the phenotypes induced by Wolbachia, our understanding of Wolbachia host shifting is still very limited: we lack answers to even fundamental questions concerning Wolbachia’s routes of transfer and the importance of factors influencing host shifts. Here, we investigate the diversity and host-shift patterns of Wolbachia in scale insects, a group of arthropods with intimate associations with other insects that make them well-suited to studying host shifts. Using Illumina pooled amplicon sequencing of Wolbachia-infected scale insects and their direct associates we determined the identity of all Wolbachia strains, revealing that 32% of samples were multiply infected (with up to five distinct strains per species). We then fitted a Generalised Additive Mixed Model (GAMM) to our data to estimate the influence of factors such as the host phylogeny and the geographic distribution of each species on Wolbachia strain sharing among scale insect species. The model predicts no significant contribution of host geography but strong effects of host phylogeny, with high rates of Wolbachia sharing among closely related species and a sudden drop-off in sharing with increasing phylogenetic distance. We also detected the same Wolbachia strain in scale insects and several intimately associated species (ants, wasps, beetles, and flies). This indicates putative host shifts and potential routes of transfers via these associates and highlights the importance of ecological connectivity in Wolbachia host-shifting.

scholarly journals Susceptibility across host species is independent of dietary protein to carbohydrate ratios

2020 ◽  
Author(s):  
Katherine E Roberts ◽  
Ben Longdon
Keyword(s):  
Viral Load ◽  
Dietary Protein ◽  
Host Species ◽  
Rna Virus ◽  
Ecological Factors ◽  
Host Shift ◽  
Host Susceptibility ◽  
Novel Host ◽  
Host Diet ◽  
Host Parasite

AbstractThe likelihood of a successful host shift of a parasite to a novel host species can be influenced by environmental factors that can act on both the host and parasite. Changes in nutritional resource availability have been shown to alter pathogen susceptibility and the outcome of infection in a range of systems. Here we examined how dietary protein to carbohydrate altered susceptibility in a large cross infection experiment. We infected 27 species of Drosophilidae with an RNA virus on three food types of differing protein to carbohydrate ratios. We then measured how viral load and mortality across species was affected by changes in diet. We found that changes in the protein:carbohydrate in the diet did not alter the outcomes of infection, with strong positive inter-species correlations in both viral load and mortality across diets, suggesting no species by diet interaction. Mortality and viral load were strongly positively correlated, and this association was consistent across diets. This suggests changes in diet may give consistent outcomes across host species, and may not be universally important in determining host susceptibility to pathogens.Impact StatementA successful host shift of a parasite from one susceptible species to a novel host can be influenced by many ecological factors. Changes in host diet can alter the immune response and outcomes of host–parasite interactions and could potentially alter the outcome of a virus host shift. To investigate, we infected 27 species of Drosophilidae with an RNA virus (DCV) across three food types with differing protein to carbohydrate ratios. We then looked at pathogen loads and survival of infected hosts compared to uninfected controls. Changes in the ratio of protein to carbohydrate did not alter susceptibility to DCV across host species.

scholarly journals A Novel Terrestrial Rabies Virus Lineage Occurring in South America: Origin, Diversification, and Evidence of Contact between Wild and Domestic Cycles

Viruses ◽  
2021 ◽  
Vol 13 (12) ◽  
pp. 2484
Author(s):  
Diego A. Caraballo ◽  
Cristina Lema ◽  
Laura Novaro ◽  
Federico Gury-Dohmen ◽  
Susana Russo ◽  
...  
Keyword(s):  
South America ◽  
Rabies Virus ◽  
Purifying Selection ◽  
Host Shift ◽  
Domestic Species ◽  
Nucleoprotein Gene ◽  
Consensus Sequences ◽  
Host Shifts ◽  
Single Host ◽  
Related Variant

The rabies virus (RABV) is characterized by a history dominated by host shifts within and among bats and carnivores. One of the main outcomes of long-term RABV maintenance in dogs was the establishment of variants in a wide variety of mesocarnivores. In this study, we present the most comprehensive phylogenetic and phylogeographic analysis, contributing to a better understanding of the origins, diversification, and the role of different host species in the evolution and diffusion of a dog-related variant endemic of South America. A total of 237 complete Nucleoprotein gene sequences were studied, corresponding to wild and domestic species, performing selection analyses, ancestral states reconstructions, and recombination analyses. This variant originated in Brazil and disseminated through Argentina and Paraguay, where a previously unknown lineage was found. A single host shift was identified in the phylogeny, from dog to the crab-eating fox (Cerdocyon thous) in the Northeast of Brazil. Although this process occurred in a background of purifying selection, there is evidence of adaptive evolution -or selection of sub-consensus sequences- in internal branches after the host shift. The interaction of domestic and wild cycles persisted after host switching, as revealed by spillover and putative recombination events.

scholarly journals Bacterial Pathogen Emergence Requires More than Direct Contact with a Novel Passerine Host

2018 ◽  
Vol 86 (3) ◽  
Author(s):  
Molly Staley ◽  
Geoffrey E. Hill ◽  
Chloe C. Josefson ◽  
Jonathan W. Armbruster ◽  
Camille Bonneaud
Keyword(s):  
Direct Contact ◽  
Clinical Symptoms ◽  
Bacterial Pathogen ◽  
Host Shift ◽  
The Novel ◽  
New Host ◽  
Content Type ◽  
House Finches ◽  
Adaptive Mutations ◽  
Novel Host

ABSTRACTWhile direct contact may sometimes be sufficient to allow a pathogen to jump into a new host species, in other cases, fortuitously adaptive mutations that arise in the original donor host are also necessary. Viruses have been the focus of most host shift studies, so less is known about the importance of ecological versus evolutionary processes to successful bacterial host shifts. Here we tested whether direct contact with the novel host was sufficient to enable the mid-1990s jump of the bacteriumMycoplasma gallisepticumfrom domestic poultry to house finches (Haemorhous mexicanus). We experimentally inoculated house finches with two genetically distinctM. gallisepticumstrains obtained either from poultry (Rlow) or from house finches (HF1995) during an epizootic outbreak. All 15 house finches inoculated with HF1995 became infected, whereas Rlow successfully infected 12 of 15 (80%) inoculated house finches. Comparisons among infected birds showed that, relative to HF1995, Rlow achieved substantially lower bacterial loads in the host respiratory mucosa and was cleared faster. Furthermore, Rlow-infected finches were less likely to develop clinical symptoms than HF1995-infected birds and, when they did, displayed milder conjunctivitis. The lower infection success of Rlow relative to HF1995 was not, however, due to a heightened host antibody response to Rlow. Taken together, our results indicate that contact between infected poultry and house finches was not, by itself, sufficient to explain the jump ofM. gallisepticumto house finches. Instead, mutations arising in the original poultry host would have been necessary for successful pathogen emergence in the novel finch host.

scholarly journals The genetic architecture of a host shift: An adaptive walk protected an aphid and its endosymbiont from plant chemical defenses

2020 ◽  
Vol 6 (19) ◽  
pp. eaba1070
Author(s):  
Kumar Saurabh Singh ◽  
Bartlomiej J. Troczka ◽  
Ana Duarte ◽  
Vasileia Balabanidou ◽  
Nasser Trissi ◽  
...  
Keyword(s):  
Host Shift ◽  
Chemical Defenses ◽  
Buchnera Aphidicola ◽  
Mutualistic Symbiosis ◽  
Host Shifts ◽  
Plant Chemical ◽  
Novel Host ◽  
Plant Chemical Defenses ◽  
Genetic Novelty ◽  
Adaptive Walk

Host shifts can lead to ecological speciation and the emergence of new pests and pathogens. However, the mutational events that facilitate the exploitation of novel hosts are poorly understood. Here, we characterize an adaptive walk underpinning the host shift of the aphid Myzus persicae to tobacco, including evolution of mechanisms that overcame tobacco chemical defenses. A series of mutational events added as many as 1.5 million nucleotides to the genome of the tobacco-adapted subspecies, M. p. nicotianae, and yielded profound increases in expression of an enzyme that efficiently detoxifies nicotine, both in aphid gut tissue and in the bacteriocytes housing the obligate aphid symbiont Buchnera aphidicola. This dual evolutionary solution overcame the challenge of preserving fitness of a mutualistic symbiosis during adaptation to a toxic novel host. Our results reveal the intricate processes by which genetic novelty can arise and drive the evolution of key innovations required for ecological adaptation.

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