skip to main content
US FlagAn official website of the United States government
dot gov icon
Official websites use .gov
A .gov website belongs to an official government organization in the United States.
https lock icon
Secure .gov websites use HTTPS
A lock ( lock ) or https:// means you've safely connected to the .gov website. Share sensitive information only on official, secure websites.


Title: Assessing Variation in the Individual-Level Impacts of a Multihost Pathogen
Most pathogens infect more than one host species, and given infection, the individual-level impact they have varies among host species. Nevertheless, variation in individual-level impacts of infection remains poorly characterised. Using the impactful and host-generalist ectoparasitic mite Sarcoptes scabiei (causing sarcoptic mange), we assessed individual-level variation in pathogen impacts by (1) compiling all documented individual-level impacts of S. scabiei across free-living host species, (2) quantifying and ranking S. scabiei impacts among host species, and (3) evaluating factors associated with S. scabiei impacts. We compiled individual-level impacts of S. scabiei infection from 77 host species, spanning 31 different impacts, and totalling 683 individual-level impact descriptions. The most common impacts were those affecting the skin, alopecia (130 descriptions), and hyperkeratosis coverage (106). From these impacts, a standardised metric was generated for each species (average impact score (AIS) with a 0-1 range), as a proxy of pathogen virulence allowing quantitative comparison of S. scabiei impacts among host species while accounting for the variation in the number and types of impacts assessed. The Japanese raccoon dog (Nyctereutes viverrinus) was found to be the most impacted host (AIS 0.899). We applied species inclusion criteria for ranking and found more well-studied species tended to be those impacted more by S. scabiei (26/27 species AIS < 0.5). AIS had relatively weak relationships with predictor variables (methodological, phylogenetic, and geographic). There was a tendency for Diprotodontia, Artiodactyla, and Carnivora to be the most impacted taxa and for research to be focussed in developed regions of the world. This study is the first quantitative assessment of individual-level pathogen impacts of a multihost parasite. The proposed methodology can be applied to other multihost pathogens of public health, animal welfare, and conservation concern and enables further research to address likely causes of variation in pathogen virulence among host species.  more » « less
Award ID(s):
2116748
PAR ID:
10469783
Author(s) / Creator(s):
; ; ;
Editor(s):
Ren, Lin-Zhu
Publisher / Repository:
Wiley
Date Published:
Journal Name:
Transboundary and Emerging Diseases
Volume:
2023
ISSN:
1865-1674
Page Range / eLocation ID:
1 to 16
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract Studying fungal virulence is often challenging and frequently depends on many contexts, including host immune status and pathogen genetic background. However, the role of ploidy has often been overlooked when studying virulence in eukaryotic pathogens. Since fungal pathogens, including the human opportunistic pathogenCandida albicans, can display extensive ploidy variation, assessing how ploidy impacts virulence has important clinical relevance. As an opportunistic pathogen,C. albicanscauses nonlethal, superficial infections in healthy individuals, but life‐threatening bloodstream infections in individuals with compromised immune function. Here, we determined how both ploidy and genetic background ofC. albicansimpacts virulence phenotypes in healthy and immunocompromised nematode hosts by characterizing virulence phenotypes in four near‐isogenic diploid and tetraploid pairs of strains, which included both laboratory and clinical genetic backgrounds. We found thatC. albicansinfections decreased host survival and negatively impacted host reproduction, and we leveraged these two measures to survey both lethal and nonlethal virulence phenotypes across the multipleC. albicansstrains. In this study, we found that regardless of pathogen ploidy or genetic background, immunocompromised hosts were susceptible to fungal infection compared to healthy hosts. Furthermore, for each host context, we found a significant interaction betweenC. albicansgenetic background and ploidy on virulence phenotypes, but no global differences between diploid and tetraploid pathogens were observed. 
    more » « less
  2. Plasmodium parasites infect thousands of species and provide an exceptional system for studying host- pathogen dynamics, especially for multi-host pathogens. However, understanding these interactions requires an accurate assay of infection. Assessing Plasmodium infections using microscopy on blood smears often misses infections with low parasitemias (the fractions of cells infected), and biases in malaria prevalence estimates will differ among hosts that differ in mean parasitemias. We examined Plasmodium relictum infection and parasitemia using both microscopy of blood smears and quantitative polymerase chain reaction (qPCR) on 299 samples from multiple bird species in Hawai’i and fit models to predict parasitemias from qPCR cycle threshold (Ct) values. We used these models to quantify the extent to which microscopy underestimated infection prevalence and to more accurately estimate infection pat- terns for each species for a large historical study done by microscopy. We found that most qPCR-positive wild-caught birds in Hawaii had low parasitemias (Ct scores 35), which were rarely detected by microscopy. The fraction of infections missed by microscopy differed substantially among eight species due to differences in species’ parasitemia levels. Infection prevalence was likely 4–5-fold higher than previous microscopy estimates for three introduced species, including Zosterops japonicus, Hawaii’s most abundant forest bird, which had low average parasitemias. In contrast, prevalence was likely only 1.5–2.3-fold higher than previous estimates for Himatione sanguinea and Chlorodrepanis virens, two native species with high average parasitemias. Our results indicate that relative patterns of infection among species differ substantially from those observed in previous microscopy studies, and that differences depend on variation in parasitemias among species. Although microscopy of blood smears is useful for estimating the frequency of different Plasmodium stages and host attributes, more sensitive quantitative methods, including qPCR, are needed to accurately estimate and compare infection prevalence among host species. 
    more » « less
  3. Abstract Changes to migration routes and phenology create novel contact patterns among hosts and pathogens. These novel contact patterns can lead to pathogens spilling over between resident and migrant populations. Predicting the consequences of such pathogen spillover events requires understanding how pathogen evolution depends on host movement behaviour. Following spillover, pathogens may evolve changes in their transmission rate and virulence phenotypes because different strategies are favoured by resident and migrant host populations. There is conflict in current theoretical predictions about what those differences might be. Some theory predicts lower pathogen virulence and transmission rates in migrant populations because migrants have lower tolerance to infection. Other theoretical work predicts higher pathogen virulence and transmission rates in migrants because migrants have more contacts with susceptible hosts.We aim to understand how differences in tolerance to infection and host pace of life act together to determine the direction of pathogen evolution following pathogen spillover from a resident to a migrant population.We constructed a spatially implicit model in which we investigate how pathogen strategy changes following the addition of a migrant population. We investigate how differences in tolerance to infection and pace of life between residents and migrants determine the effect of spillover on pathogen evolution and host population size.When the paces of life of the migrant and resident hosts are equal, larger costs of infection in the migrants lead to lower pathogen transmission rate and virulence following spillover. When the tolerance to infection in migrant and resident populations is equal, faster migrant paces of life lead to increased transmission rate and virulence following spillover. However, the opposite can also occur: when the migrant population has lower tolerance to infection, faster migrant paces of life can lead to decreases in transmission rate and virulence.Predicting the outcomes of pathogen spillover requires accounting for both differences in tolerance to infection and pace of life between populations. It is also important to consider how movement patterns of populations affect host contact opportunities for pathogens. These results have implications for wildlife conservation, agriculture and human health. 
    more » « less
  4. Understanding the ecological and evolutionary processes that drive host–pathogen interactions is critical for combating epidemics and conserving species. TheVarroa destructormite and deformed wing virus (DWV) are two synergistic threats to Western honeybee (Apis mellifera) populations across the globe. Distinct honeybee populations have been found to self-sustain despiteVarroainfestations, including colonies within the Arnot Forest outside Ithaca, NY, USA. We hypothesized that in these bee populations, DWV has been selected to produce an avirulent infection phenotype, allowing for the persistence of both host and disease-causing agents. To investigate this, we assessed the titre of viruses in bees from the Arnot Forest and managed apiaries, and assessed genomic variation and virulence differences between DWV isolates. Across groups, we found viral abundance was similar, but DWV genotypes were distinct. We also found that infections with isolates from the Arnot Forest resulted in higher survival and lower rates of symptomatic deformed wings, compared to analogous isolates from managed colonies, providing preliminary evidence to support the hypothesis of adaptive decreased viral virulence. Overall, this multi-level investigation of virus genotype and phenotype indicates that host ecological context can be a significant driver of viral evolution and host–pathogen interactions in honeybees. 
    more » « less
  5. Plant bacterial pathogens rely on host-derived signals to coordinate the deployment of virulence factors required for infection. In this review, I describe how diverse plant-pathogenic bacteria detect and respond to plant-derived metabolic signals for the purpose of virulence gene regulation. I highlight examples of how pathogens perceive host metabolites through membrane-localized receptors as well as intracellular response mechanisms. Furthermore, I describe how individual strains may coordinate their virulence using multiple distinct host metabolic signals, and how plant signals may positively or negatively regulate virulence responses. I also describe how plant defenses may interfere with the perception of host metabolites as a means to dampen pathogen virulence. The emerging picture is that recognition of host metabolic signals for the purpose of virulence gene regulation represents an important primary layer of interaction between pathogenic bacteria and host plants that shapes infection outcomes. 
    more » « less