Heterogeneous distributions are a fundamental principle of ecology, manifesting as natural variability within ecological levels of organization from individuals to ecosystems. In disease ecology, variability in biotic and abiotic factors can result in heterogeneous patterns of transmission and virulence—broadly defined here as the negative consequences of infection. Still, our classic theoretical understanding of disease dynamics comes from models that assume homogeneous transmission and virulence. Here, we test this assumption by assessing the contribution of various sources of individual and spatial heterogeneity to patterns of transmission and sublethal measurements of virulence in two lizard–malaria systems: a three‐parasite assemblage (
- Award ID(s):
- 1831952
- NSF-PAR ID:
- 10484393
- Publisher / Repository:
- Ecosphere
- Date Published:
- Journal Name:
- Ecosphere
- Volume:
- 13
- Issue:
- 12
- ISSN:
- 2150-8925
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract Understanding the consequences of environmental fluctuations for parasite dynamics requires a long-term view stretching over many transmission cycles. Here we studied the dynamics of three malaria parasites ( Plasmodium azurophilum , P. leucocytica and P. floridense ) infecting the lizard Anolis gundlachi , in the rainforest of Puerto Rico. In this malaria–anole system we evaluated temporal fluctuations in individual probability of infection, the environmental drivers of observed variation and consequences for host body condition and Plasmodium parasites assemblage. We conducted a total of 15 surveys including 10 from 1990 to 2002 and five from 2015 to 2017. During the early years, a lizard's probability of infection by all Plasmodium species appeared stable despite disturbances ranging from two hurricanes to short droughts. Over a longer timescale, probability of infection and overall prevalence varied significantly, following non-linear relationships with temperature and rainfall such that highest prevalence is expected at intermediate climate measures. A perplexing result was that host body condition was maximized at intermediate levels of rainfall and/or temperature (when risk of infection was highest), yet we found no significant decreases in body condition due to infection. Plasmodium parasite species composition varied through time with a reduction and near local extinction of P. floridense . Our results emphasize the need for long-term studies to reveal host–parasite dynamics, their drivers and consequences.more » « less
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Abstract Understanding parasite transmission in communities requires knowledge of each species' capacity to support transmission. This property, ‘competence’, is a critical currency for modelling transmission under community change and for testing diversity–disease theory. Despite the central role of competence in disease ecology, we lack a clear understanding of the factors that generate competence and drive its variation.
We developed novel conceptual and quantitative approaches to systematically quantify competence for a multi‐host, multi‐parasite community. We applied our framework to an extensive dataset: five amphibian host species exposed to four parasitic trematode species across five ecologically realistic exposure doses. Together, this experimental design captured 20 host–parasite interactions while integrating important information on variation in parasite exposure. Using experimental infection assays, we measured multiple components of the infection process and combined them to produce competence estimates for each interaction.
With directly estimated competence values, we asked which components of the infection process best explained variation in competence: barrier resistance (the initial fraction of administered parasites blocked from infecting a host), internal clearance (the fraction of established parasites lost over time) or pre‐transmission mortality (the probability of host death prior to transmission). We found that variation in competence among the 20 interactions was best explained by differences in barrier resistance and pre‐transmission mortality, underscoring the importance of host resistance and parasite pathogenicity in shaping competence.
We also produced dose‐integrated estimates of competence that incorporated natural variation in exposure to address questions on the basis and extent of variation in competence. We found strong signals that host species identity shaped competence variation (as opposed to parasite species identity). While variation in infection outcomes across hosts, parasites, individuals and doses was considerable, individual heterogeneity was limited compared to among‐species differences. This finding highlights the robustness of our competence estimates and suggests that species‐level values may be strong predictors for community‐level transmission in natural systems.
Competence emerges from distinct underlying processes and can have strong species‐level characteristics; thus, this property has great potential for linking mechanisms of infection to epidemiological patterns.
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Abstract Aim Macroecological analyses provide valuable insights into factors that influence how parasites are distributed across space and among hosts. Amid large uncertainties that arise when generalizing from local and regional findings, hierarchical approaches applied to global datasets are required to determine whether drivers of parasite infection patterns vary across scales. We assessed global patterns of haemosporidian infections across a broad diversity of avian host clades and zoogeographical realms to depict hotspots of prevalence and to identify possible underlying drivers.
Location Global.
Time period 1994–2019.
Major taxa studied Avian haemosporidian parasites (genera
Plasmodium ,Haemoproteus ,Leucocytozoon andParahaemoproteus ).Methods We amalgamated infection data from 53,669 individual birds representing 2,445 species world‐wide. Spatio‐phylogenetic hierarchical Bayesian models were built to disentangle potential landscape, climatic and biotic drivers of infection probability while accounting for spatial context and avian host phylogenetic relationships.
Results Idiosyncratic responses of the three most common haemosporidian genera to climate, habitat, host relatedness and host ecological traits indicated marked variation in host infection rates from local to global scales. Notably, host ecological drivers, such as migration distance for
Plasmodium andParahaemoproteus , exhibited predominantly varying or even opposite effects on infection rates across regions, whereas climatic effects on infection rates were more consistent across realms. Moreover, infections in some low‐prevalence realms were disproportionately concentrated in a few local hotspots, suggesting that regional‐scale variation in habitat and microclimate might influence transmission, in addition to global drivers.Main conclusions Our hierarchical global analysis supports regional‐scale findings showing the synergistic effects of landscape, climate and host ecological traits on parasite transmission for a cosmopolitan and diverse group of avian parasites. Our results underscore the need to account for such interactions, in addition to possible variation in drivers across regions, to produce the robust inference required to predict changes in infection risk under future scenarios.
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