Host Range Shifts Research Articles

Utilizing citizen science data to rapidly assess changing associations between wild birds and avian influenza outbreaks in poultry.

High pathogenicity avian influenza virus (HPAIV) is a rapidly evolving virus causing significant economic and environmental harm. Wild birds are a key viral reservoir and an important source of viral incursions into animal populations, including poultry. However, we lack a thorough understanding of which species drive incursions and whether this changes over time. We explored associations between the abundances of 152 avian species and outbreaks of highly pathogenic avian influenza (HPAI) in poultry premises across Great Britain between October 2021 and January 2023. Spatial generalized additive models were used, with species abundance distributions sourced from eBird. Associations were investigated at the species-specific level and across species aggregations. During autumn/winter, associations were generally strongest with waterbirds such as ducks and geese; however, we also found significant associations in groups such as non-native gamebirds and rapid change in species-specific associations over time. Our results demonstrate the value of citizen science to rapidly explore wild species as potential facilitators of disease incursions into well-monitored populations, especially in regions where viral surveillance in wild species is limited. This can be a critical step towards prioritizing targeted surveillance that could inform species-specific biosecurity measures; particularly for HPAIV, which has undergone sudden shifts in host range and continues to rapidly evolve.

Evolution of SARS-CoV-2 Spikes shapes their binding affinities to animal ACE2 orthologs.

Spike-receptor interaction is a critical determinant for the host range of coronaviruses. In this study, we investigated the SARS-CoV-2 WHU01 strain and five WHO-designated SARS-CoV-2 variants of concern (VOCs), including Alpha, Beta, Gamma, Delta, and the early Omicron variant, for their Spike interactions with ACE2 proteins of 18 animal species. First, the receptor-binding domains (RBDs) of Alpha, Beta, Gamma, and Omicron were found to display progressive gain of affinity to mouse ACE2. More interestingly, these RBDs were also found with progressive loss of affinities to multiple ACE2 orthologs. The Omicron RBD showed decreased or complete loss of affinity to eight tested animal ACE2 orthologs, including that of some livestock animals (horse, donkey, and pig), pet animals (dog and cat), and wild animals (pangolin, American pika, and Rhinolophus sinicus bat). These findings shed light on potential host range shift of SARS-CoV-2 VOCs, especially that of the Omicron variant.

Climate, host and geography shape insect and fungal communities of trees

Non-native pests, climate change, and their interactions are likely to alter relationships between trees and tree-associated organisms with consequences for forest health. To understand and predict such changes, factors structuring tree-associated communities need to be determined. Here, we analysed the data consisting of records of insects and fungi collected from dormant twigs from 155 tree species at 51 botanical gardens or arboreta in 32 countries. Generalized dissimilarity models revealed similar relative importance of studied climatic, host-related and geographic factors on differences in tree-associated communities. Mean annual temperature, phylogenetic distance between hosts and geographic distance between locations were the major drivers of dissimilarities. The increasing importance of high temperatures on differences in studied communities indicate that climate change could affect tree-associated organisms directly and indirectly through host range shifts. Insect and fungal communities were more similar between closely related vs. distant hosts suggesting that host range shifts may facilitate the emergence of new pests. Moreover, dissimilarities among tree-associated communities increased with geographic distance indicating that human-mediated transport may serve as a pathway of the introductions of new pests. The results of this study highlight the need to limit the establishment of tree pests and increase the resilience of forest ecosystems to changes in climate.

Long-term and rapid evolution in powdery mildew fungi.

The powdery mildew fungi (Erysiphaceae) are globally distributed plant pathogens with a range of more than 10,000 plant hosts. In this review, we discuss the long- and short-term evolution of these obligate biotrophic fungi and outline their diversity with respect to morphology, lifestyle, and host range. We highlight their remarkable ability to rapidly overcome plant immunity, evolve fungicide resistance, and broaden their host range, for example, through adaptation and hybridization. Recent advances in genomics and proteomics, particularly in cereal powdery mildews (genus Blumeria), provided first insights into mechanisms of genomic adaptation in these fungi. Transposable elements play key roles in shaping their genomes, where even close relatives exhibit diversified patterns of recent and ongoing transposon activity. These transposons are ubiquitously distributed in the powdery mildew genomes, resulting in a highly adaptive genome architecture lacking obvious regions of conserved gene space. Transposons can also be neofunctionalized to encode novel virulence factors, particularly candidate secreted effector proteins, which may undermine the plant immune system. In cereals like barley and wheat, some of these effectors are recognized by plant immune receptors encoded by resistance genes with numerous allelic variants. These effectors determine incompatibility ("avirulence") and evolve rapidly through sequence diversification and copy number variation. Altogether, powdery mildew fungi possess plastic genomes that enable their fast evolutionary adaptation towards overcoming plant immunity, host barriers, and chemical stress such as fungicides, foreshadowing future outbreaks, host range shifts and expansions as well as potential pandemics by these pathogens.

Demographic Expansions and the Emergence of Host Specialization in Genetically Distinct Ecotypes of the Tick-Transmitted Bacterium Anaplasma phagocytophilum.

In Europe, genetically distinct ecotypes of the tick-vectored bacterium Anaplasma phagocytophilum circulate among mammals in three discrete enzootic cycles. To date, potential ecological factors that contributed to the emergence of these divergent ecotypes have been poorly studied. Here, we show that the ecotype that predominantly infects roe deer (Capreolus capreolus) is evolutionarily derived. Its divergence from a host generalist ancestor occurred after the last glacial maximum as mammal populations, including roe deer, recolonized the European mainland from southern refugia. We also provide evidence that this host specialist ecotype's effective population size (Ne) has tracked changes in the population of its roe deer host. Specifically, both host and bacterium have undergone substantial increases in Ne over the past 1,500 years. In contrast, we show that while it appears to have undergone a major population expansion starting ~3,500 years ago, in the past 500 years, the contemporary host generalist ecotype has experienced a substantial reduction in genetic diversity levels, possibly as a result of reduced opportunities for transmission between competent hosts. IMPORTANCE The findings of this study reveal specific events important for the evolution of host specialization in a naturally occurring, obligately intracellular bacterial pathogen. Specifically, they show that host range shifts and the emergence of host specialization may occur during periods of population growth in a generalist ancestor. Our results also demonstrate the close correlation between demographic patterns in host and pathogen for a specialist system. These findings have important relevance for understanding the evolution of host range diversity. They may inform future work on host range dynamics, and they provide insights for understanding the emergence of pathogens that have human and veterinary health implications.

Emergence and Evolution of Novel Canine-Avian Reassortant H3N2 Influenza A Viruses in Duck in Leizhou Peninsula, China.

Avian-to-mammal transmission and mammalian adaptation of avian influenza virus (AIV) are threats to public health and of great concern. The H3 subtype of influenza virus has low pathogenicity and is widely distributed in humans, canines, equines and avians. In 2018–2019, we isolated six H3N2 subtype influenza viruses from 329 samples acquired from ducks on the Leizhou Peninsula, China, as part of an ongoing virus surveillance program. All viruses were analyzed by whole-genome sequencing with subsequent genetic comparison and phylogenetic analysis. Phylogenetic analysis demonstrated that reassortment of these viruses has occurred among different hosts and subtypes. Some of the H3 AIV isolates have similar genes as subtypes H5 and H7 of highly pathogenic avian influenza viruses (HPAIVs). Most importantly, one strain of H3N2 virus is a novel reassortant influenza virus containing HA and PB2 segments from canine H3N2 virus. The time of most recent common ancestor (tMRCA) data indicated that this reassortant H3N2 virus might have emerged in 2011–2018. The findings suggest that the viruses studied here have undergone multiple reassortment events. Our results provide a framework for understanding the molecular basis of host-range shifts of influenza viruses and we should pay more attention to canine which lived with avian together.

Host specialization is ancestral in Torymus (Hymenoptera, Chalcidoidea) cynipid gall parasitoids

AbstractThe host range of parasitoids varies greatly among species: Some only parasitize one to a few hosts (specialists), while others parasitize multiple species or a variety of host types (generalists). The direction of most host range shifts in parasitoid groups, that is from generalist to specialist or, alternatively, from specialist to generalist, is unknown. To explore the origin of host range shifts, we studied a clade within the genus Torymus (Hymenoptera, Chalcidoidea) that includes both generalist and specialist parasitoids of Cynipidae (Hymenoptera). We analysed the phylogenetic relationships of the species of Torymus on the basis of two gene fragments (cox1 and ITS2) of 246 specimens and performed an ancestral state reconstruction of the specialist/generalist trait. Our results revealed the following: (a) The ancestral state of this group of Torymus is specialist, with the generalist state evolving through a loss of specialization. (b) The species Torymus cyaneus and Torymus flavipes both have a strong genetic structure, suggesting the existence of different biological identities. (c) There has been a host plant shift in the lineage(s) leading to Torymus rubi and Torymus bedeguaris from galls on Quercus to those on Rosaceae. (d) The alien species Torymus sinensis and the native European species Torymus notatus are phylogenetically closely related. (e) Speciation within Torymus was likely associated with the diversification of their cynipid hosts, which itself was driven by the dramatic changes in climate and vegetation that occurred during the Miocene.

Cross-continental comparison of parasite communities in a wide-ranging carnivore suggests associations with prey diversity and host density.

Parasites are integral to ecosystem functioning yet often overlooked. Improved understanding of host–parasite associations is important, particularly for wide‐ranging species for which host range shifts and climate change could alter host–parasite interactions and their effects on ecosystem function.Among the most widely distributed mammals with diverse diets, gray wolves (Canis lupus) host parasites that are transmitted among canids and via prey species. Wolf–parasite associations may therefore influence the population dynamics and ecological functions of both wolves and their prey. Our goal was to identify large‐scale processes that shape host–parasite interactions across populations, with the wolf as a model organism.By compiling data from various studies, we examined the fecal prevalence of gastrointestinal parasites in six wolf populations from two continents in relation to wolf density, diet diversity, and other ecological conditions.As expected, we found that the fecal prevalence of parasites transmitted directly to wolves via contact with other canids or their excreta was positively associated with wolf density. Contrary to our expectations, the fecal prevalence of parasites transmitted via prey was negatively associated with prey diversity. We also found that parasite communities reflected landscape characteristics and specific prey items available to wolves.Several parasite taxa identified in this study, including hookworms and coccidian protozoans, can cause morbidity and mortality in canids, especially in pups, or in combination with other stressors. The density–prevalence relationship for parasites with simple life cycles may reflect a regulatory role of gastrointestinal parasites on wolf populations. Our result that fecal prevalence of parasites was lower in wolves with more diverse diets could provide insight into the mechanisms by which biodiversity may regulate disease. A diverse suite of predator–prey interactions could regulate the effects of parasitism on prey populations and mitigate the transmission of infectious agents, including zoonoses, spread via trophic interactions.

Climate Warming’s Alteration of Host-Parasite Dynamics

Parasites and pathogens have significant roles in host population control, and thus host-parasite interactions affect biodiversity. The important question reviewed in this paper is how changes in temperature due to climate change affect host-parasite interactions. There is mounting evidence that elevated temperatures have both beneficial and detrimental effects on parasites and independently on hosts. These independent changes result in altered host-parasite dynamics through various mechanisms. If elevated temperatures enhance parasite survival, risk of disease transmission among hosts is enhanced as well. This enhancement is dependent on temperature-induced shifts in the host lifecycle, as asynchrony in host and parasite development can result in decreased infection rate and disrupted disease transmission regardless of the increase in parasite survival and density. Host species differ in their responses to temperature elevation. Increased temperature can alter their susceptibility to parasites through changes in their immune functions. Climate shifts also result in host range shifts. As host ranges expand, they may encounter novel pathogens, increasing the risk of spillovers and resulting in a greater mortality rate. From the point of view of native species, newly arriving host species present the potential danger of introducing novel parasites and diseases, which can be detrimental to native species. For seasonally migratory species whose parasites typically decrease during their absence, any climate-induced increase in their parasites’ survival prior to their return may decrease the effectiveness of migration, shift their lifestyle to become more sedentary and thus reshape host-parasite dynamic. Altered balance of host-parasite interactions produces changes at higher ecological levels, and the efforts to conserve parasites should thus have the same priority as the need to conserve host species.

Bioinformatic Detection of Positive Selection Pressure in Plant Pathogens: The Neutral Theory of Molecular Sequence Evolution in Action.

The genomes of plant pathogenic fungi and oomycetes are often exposed to strong positive selection pressure. During speciation, shifts in host range and preference can lead to major adaptive changes. Furthermore, evolution of total host resistance to most isolates can force rapid evolutionary changes in host-specific pathogens. Crop pathogens are subjected to particularly intense selective pressures from monocultures and fungicides. Detection of the footprints of positive selection in plant pathogen genomes is a worthwhile endeavor as it aids understanding of the fundamental biology of these important organisms. There are two main classes of test for detection of positively selected alleles. Tests based on the ratio of non-synonymous to synonymous substitutions per site detect the footprints of multiple fixation events between divergent lineages. Thus, they are well-suited to the study of ancient adaptation events spanning speciations. On the other hand, tests that scan genomes for local fluctuations in allelic diversity within populations are suitable for detection of recent positive selection in populations. In this review, I briefly describe some of the more widely used tests of positive selection and the theory underlying them. I then discuss various examples of their application to plant pathogen genomes, emphasizing the types of genes that are associated with signatures of positive selection. I conclude with a discussion of the practicality of such tests for identification of pathogen genes of interest and the important features of pathogen ecology that must be taken into account for accurate interpretation.

Host-Range Shift Between Emerging P[8]-4 Rotavirus and Common P[8] and P[4] Strains

In Tunisia, we observed that rotavirus P[8]-3 and P[4] strains in young children with gastroenteritis associate with secretor histo-blood group phenotype. In contrast, the emerging P[8]-4 strain, representing 10% of cases, was exclusively found in nonsecretor patients. Unlike VP8* from P[8]-3 and P[4] strains, the P[8]-4 VP8* protein attached to glycans from saliva samples regardless of the donor's secretor status. Interestingly, a high frequency of FUT2 enzyme deficiency (nonsecretor phenotype) was observed in the population. This may allow cocirculation of P[8]-3 and P[8]-4 strains in secretor and nonsecretor children, respectively.

Host-range shift of H3N8 canine influenza virus: a phylodynamic analysis of its origin and adaptation from equine to canine host

Prior to the emergence of H3N8 canine influenza virus (CIV) and the latest avian-origin H3N2 CIV, there was no evidence of a circulating canine-specific influenza virus. Molecular and epidemiological evidence suggest that H3N8 CIV emerged from H3N8 equine influenza virus (EIV). This host-range shift of EIV from equine to canine hosts and its subsequent establishment as an enzootic CIV is unique because this host-range shift was from one mammalian host to another. To further understand this host-range shift, we conducted a comprehensive phylodynamic analysis using all the available whole-genome sequences of H3N8 CIV. We found that (1) the emergence of H3N8 CIV from H3N8 EIV occurred in approximately 2002; (2) this interspecies transmission was by a reassortant virus of the circulating Florida-1 clade H3N8 EIV; (3) once in the canine species, H3N8 CIV spread efficiently and remained an enzootic virus; (4) H3N8 CIV evolved and diverged into multiple clades or sublineages, with intra and inter-lineage reassortment. Our results provide a framework to understand the molecular basis of host-range shifts of influenza viruses and that dogs are potential “mixing vessels” for the establishment of novel influenza viruses.

Expecting the unexpected: factors influencing the emergence of fungal and oomycete plant pathogens.

SummaryIn recent years, the number of emergent plant pathogens (EPPs) has grown substantially, threatening agroecosystem stability and native biodiversity. Contributing factors include, among others, shifts in biogeography, with EPP spread facilitated by the global unification of monocultures in modern agriculture, high volumes of trade in plants and plant products and an increase in sexual recombination within pathogen populations. The unpredictable nature of EPPs as they move into new territories is a situation that has led to sudden and widespread epidemics. Understanding the underlying causes of pathogen emergence is key to managing the impact of EPPs. Here, we review some factors specifically influencing the emergence of oomycete and fungal EPPs, including new introductions through anthropogenic movement, natural dispersal and weather events, as well as genetic factors linked to shifts in host range.

Status of research, breeding and protection of cucurbits in relation to cucurbit downy mildew: their limits and perspectives

Knowledge of the recent distribution, host range, virulence, DNA profiles, and resistance to fungicides of Pseudoperonospora cubensis (Berk. & M.A. Curtis) Rostovzev, and sources of host resistance to this pathogen are reviewed. P. cubensis is widely distributed in nearly all continents, with a high capacity to adapt to changing environmental conditions and new regions. Its host-plant range includes more than 60 species and 20 genera of Cucurbitaceae. It exhibits clear host specialization, with shifts in host range and an increasing spectrum of new host species. Temporal shifts to higher virulence levels and more complex virulence patterning within pathogen populations have been recorded in the Czech Republic, Israel (in 2002), and the USA (in 2004). Pathotypes have been described, and a triple-tetrad code proposed for their denomination. A differential host set for racial determination and denomination is under development. Forty-five different reaction patterns were recorded from the interaction of 115 Cucumis melo accessions to 8 isolates of P. cubensis with different levels of virulence; most C. melo accessions were highly susceptible to all isolates; but PI 315410 (VIR 5682) was resistant to 5 isolates. Because of race-specificity in host-pathogen interactions, resistance breeding is rather difficult and resistance typically not stable. In vitro tests of fungicide efficacy in 2001-2014 documented high levels of efficacy in fosetyl-Al (Aliette 80 WP) and propamocarb (Previcur 607 SL) to Czech strains of P. cubensis, with increased resistance of some strains, inefficacy of metalaxyl, metalaxyl-M and cymoxanil (Ridomil Plus 48 WP, Ridomil Gold MZ 68 WP, Curzate K), and inefficacy of dimethomorph (Acrobat MZ) with a temporal shift from resistant to tolerant and sensitive isolates. Changes in the genetic structure of populations of 67 P. cubensis isolates collected in the Czech Republic and other European countries during 1995-2012 were detected by Multilocus Sequence Analysis (MLSA) of four mitochondrial and two nuclear DNA regions. These changes may be associated with recently reported shifts in virulence. Data on host-range changes and spatio-temporal variability in virulence and fungicide resistance confirm the high micro-evolutionary potential of P. cubensis populations and more detailed research is required for a better understanding of these host-pathogen interactions as well as for more efficient disease management.

Is regulation preventing the development of therapeutics that may prevent future coronavirus pandemics?

Is regulation preventing the development of therapeutics that may prevent future coronavirus pandemics?

Who acquires infection from whom and how? Disentangling multi-host and multi-mode transmission dynamics in the 'elimination' era.

Multi-host infectious agents challenge our abilities to understand, predict and manage disease dynamics. Within this, many infectious agents are also able to use, simultaneously or sequentially, multiple modes of transmission. Furthermore, the relative importance of different host species and modes can itself be dynamic, with potential for switches and shifts in host range and/or transmission mode in response to changing selective pressures, such as those imposed by disease control interventions. The epidemiology of such multi-host, multi-mode infectious agents thereby can involve a multi-faceted community of definitive and intermediate/secondary hosts or vectors, often together with infectious stages in the environment, all of which may represent potential targets, as well as specific challenges, particularly where disease elimination is proposed. Here, we explore, focusing on examples from both human and animal pathogen systems, why and how we should aim to disentangle and quantify the relative importance of multi-host multi-mode infectious agent transmission dynamics under contrasting conditions, and ultimately, how this can be used to help achieve efficient and effective disease control.This article is part of the themed issue ‘Opening the black box: re-examining the ecology and evolution of parasite transmission’.

Identification of two lineages of host-associated eriophyoid mites predisposed to different levels of host diversification

Herbivorous arthropods can diversify as a consequence of evolutionary changes in response to their plant hosts. Current patterns of host association of herbivores are likely to reflect a long evolutionary history of herbivore-plant co-evolution. Here, we used molecular phylogenetics to track the evolutionary history of host shifts and diversification of 66 eriophyoid mites (Acari, Eriophyoidea), and linked past patterns of evolutionary diversification to more recent patterns of divergence by tracking population genetic variation in 13 of the eriophyoid mite species feeding on different gymnosperm hosts. This allowed us to explore the relationship between a past history of diversification and the current potential of mites to undergo host range shifts. We found that population-level diversity across gymnosperm hosts as measured by 28S rRNA markers was greater in species from the mite clade that had radiated across evolutionary time to utilize a variety of hosts including angiosperms, compared to species from the clade that has remained restricted to ancestral gymnosperm hosts. Species from the radiated clade exhibited higher variation in host use. Lineages of mites that have in the past been able to radiate and adapt to diverse plants may therefore be predisposed to continue their expansion on new hosts, although additional clades need to be tested.

Contact heterogeneity, rather than transmission efficiency, limits the emergence and spread of canine influenza virus.

Host-range shifts in influenza virus are a major risk factor for pandemics. A key question in the study of emerging zoonoses is how the evolution of transmission efficiency interacts with heterogeneity in contact patterns in the new host species, as this interplay influences disease dynamics and prospects for control. Here we use a synergistic mixture of models and data to tease apart the evolutionary and demographic processes controlling a host-range shift in equine H3N8-derived canine influenza virus (CIV). CIV has experienced 15 years of continuous transfer among dogs in the United States, but maintains a patchy distribution, characterized by sporadic short-lived outbreaks coupled with endemic hotspots in large animal shelters. We show that CIV has a high reproductive potential in these facilities (mean R0 = 3.9) and that these hotspots act as refugia from the sparsely connected majority of the dog population. Intriguingly, CIV has evolved a transmission efficiency that closely matches the minimum required to persist in these refugia, leaving it poised on the extinction/invasion threshold of the host contact network. Corresponding phylogenetic analyses show strong geographic clustering in three US regions, and that the effective reproductive number of the virus (Re) in the general dog population is close to 1.0. Our results highlight the critical role of host contact structure in CIV dynamics, and show how host contact networks could shape the evolution of pathogen transmission efficiency. Importantly, efficient control measures could eradicate the virus, in turn minimizing the risk of future sustained transmission among companion dogs that could represent a potential new axis to the human-animal interface for influenza.

Consequences of in vitro host shift for St. Louis encephalitis virus

Understanding the potential for host range shifts and expansions of RNA viruses is critical to predicting the evolutionary and epidemiological paths of these pathogens. As arthropod-borne viruses (arboviruses) experience frequent spillover from their amplification cycles and are generalists by nature, they are likely to experience a relatively high frequency of success in a range of host environments. Despite this, the potential for host expansion, the genetic correlates of adaptation to novel environments and the costs of such adaptations in originally competent hosts are still not characterized fully for arboviruses. In the studies presented here, we utilized experimental evolution of St. Louis encephalitis virus (SLEV; family Flaviviridae, genus Flavivirus) in vitro in the Dermacentor andersoni line of tick cells to model adaptation to a novel invertebrate host. Our results demonstrated that levels of adaptation and costs in alternate hosts are highly variable among lineages, but also that significant fitness increases in tick cells are achievable with only modest change in consensus genetic sequence. In addition, although accumulation of diversity may at times buffer against phenotypic costs within the SLEV swarm, an increased proportion of variants with an impaired capacity to infect and spread on vertebrate cell culture accumulated with tick cell passage. Isolation and characterization of a subset of these variants implicates the NS3 gene as an important host range determinant for SLEV.

Pathogen accumulation and long‐term dynamics of plant invasions

Summary The diversity of pathogens on highly abundant introduced hosts has been positively correlated with time since introduction, geographical range of the introduced species and diversity of invaded habitats. However, little is known about the ecological effects of pathogen accumulation on non‐native invasive plants. Pathogen accumulation on invasive plant species may result from ecological processes such as high plant densities, expanding geographical ranges and pathogen dispersal from the native range, or evolutionary mechanisms such as host range shifts and adaptation of native pathogens to invasive species. Over time pathogen accumulation may cause decline in the density and distribution of invasive plants and facilitate recovery of native species. Alternatively, pathogens might build up on invasive species and then spill back onto co‐occurring native species, further exacerbating the effects of invasions. Synthesis. Research efforts should focus on determining the long‐term outcomes of pathogen accumulation on invasive species. Such research will require multifaceted approaches including comparative studies of diverse invasive species and habitats, experimental manipulations of hosts and pathogens in nature and controlled environments, and predictive models of host‐pathogen interactions within an invasion framework. Results of this research will improve our understanding and ability to predict the outcomes of biological invasions.