Predicting the effects of climate change on plant disease is critical for protecting ecosystems and food production. Here, we show how disease pressure responds to short-term weather, historical climate and weather anomalies by compiling a global database (4339 plant-disease populations) of disease prevalence in both agricultural and wild plant systems. We hypothesised that weather and climate would play a larger role in disease in wild versus agricultural plant populations, which the results supported. In wild systems, disease prevalence peaked when the temperature was 2.7°C warmer than the historical average for the same time of year. We also found evidence of a negative interactive effect between weather anomalies and climate in wild systems, consistent with the idea that climate maladaptation can be an important driver of disease outbreaks. Temperature and precipitation had relatively little explanatory power in agricultural systems, though we observed a significant positive effect of current temperature. These results indicate that disease pressure in wild plants is sensitive to nonlinear effects of weather, weather anomalies and their interaction with historical climate. In contrast, warmer temperatures drove risks for agricultural plant disease outbreaks within the temperature range examined regardless of historical climate, suggesting vulnerability to ongoing climate change.

Climate change can impact the rates at which parasites are transmitted between hosts, ultimately determining if and when an epidemic will emerge. As such, our ability to predict climate-mediated epidemic emergence will become increasingly important in our efforts to prepare for and mitigate the effects of disease outbreaks on ecological systems and global public health. Theory suggests that statistical signatures termed "early warning signals" (EWS), can function as predictors of epidemic emergence. While a number of works report post hoc detections of EWS of epidemic emergence, the theory has yet to be experimentally tested. Here, we analyse experimental and simulated time series of disease spread within populations of the model disease system Daphnia magna-Ordospora colligata for EWS of climate-mediated epidemic emergence. In this system, low temperatures prevent disease emergence, while sufficiently high temperatures force the system through a critical transition to an epidemic state. We found that EWS of epidemic emergence were nearly as likely to be detected in populations maintained at a sub-epidemic temperature as they were to be detected in populations subjected to a warming treatment that induced epidemic spread. Our findings suggest that the detection of false positives may limit the reliability and utility of EWS as predictors of climate-mediated epidemic emergence.

The geographical range of schistosomiasis is affected by the ecology of schistosome parasites and their obligate host snails, including their response to temperature. Previous models predicted schistosomiasis' thermal optimum at 21.7 °C, which is not compatible with the temperature in sub-Saharan Africa (SSA) regions where schistosomiasis is hyperendemic. We performed an extensive literature search for empirical data on the effect of temperature on physiological and epidemiological parameters regulating the free-living stages of S. mansoni and S. haematobium and their obligate host snails, i.e., Biomphalaria spp. and Bulinus spp., respectively. We derived nonlinear thermal responses fitted on these data to parameterize a mechanistic, process-based model of schistosomiasis. We then re-cast the basic reproduction number and the prevalence of schistosome infection as functions of temperature. We found that the thermal optima for transmission of S. mansoni and S. haematobium range between 23.1-27.3 °C and 23.6-27.9 °C (95 % CI) respectively. We also found that the thermal optimum shifts toward higher temperatures as the human water contact rate increases with temperature. Our findings align with an extensive dataset of schistosomiasis prevalence in SSA. The refined nonlinear thermal-response model developed here suggests a more suitable current climate and a greater risk of increased transmission with future warming for more than half of the schistosomiasis suitable regions with mean annual temperature below the thermal optimum.

Temperature can influence mosquito-borne diseases like dengue. These effects are expected to vary geographically and over time in both magnitude and direction and may interact with other environmental variables, making it difficult to anticipate changes in response to climate change. Here, we investigate global variation in temperature–dengue relationship by analyzing published correlations between temperature and dengue and matching them with remotely sensed climatic and socioeconomic data. We found that the correlation between temperature and dengue was most positive at intermediate (near 24°C) temperatures, as predicted from an independent mechanistic model. Positive temperature–dengue associations were strongest when temperature variation and population density were high and decreased with infection burden and rainfall mean and variation, suggesting alternative limiting factors on transmission. Our results show that while climate effects on diseases are context-dependent they are also predictable from the thermal biology of transmission and its environmental and social mediators.

Climate change has profound effects on infectious disease dynamics, yet the impacts of increased short-term temperature fluctuations on disease spread remain poorly understood. We empirically tested the theoretical prediction that short-term thermal fluctuations suppress endemic infection prevalence at the pathogen's thermal optimum. This prediction follows from a mechanistic disease transmission model analyzed using stochastic simulations of the model parameterized with thermal performance curves (TPCs) from metabolic scaling theory and using nonlinear averaging, which predicts ecological outcomes consistent with Jensen's inequality (i.e., reduced performance around concave-down portions of a thermal response curve). Experimental observations of replicated epidemics of the microparasite Ordospora colligata in Daphnia magna populations indicate that temperature variability had the opposite effect of our theoretical predictions and instead increase endemic infection prevalence. This positive effect of temperature variability is qualitatively consistent with a published hypothesis that parasites may acclimate more rapidly to fluctuating temperatures than their hosts; however, incorporating hypothetical effects of delayed host acclimation into the mechanistic transmission model did not fully account for the observed pattern. The experimental data indicate that shifts in the distribution of infection burden underlie the positive effect of temperature fluctuations on endemic prevalence. The increase in disease risk associated with climate fluctuations may therefore result from disease processes interacting across scales, particularly within-host dynamics, that are not captured by combining standard transmission models with metabolic scaling theory.

Background West Nile virus (WNV) is the leading cause of mosquito-borne illness in the continental USA. WNV occurrence has high spatiotemporal variation, and current approaches to targeted control of the virus are limited, making forecasting a public health priority. However, little research has been done to compare strengths and weaknesses of WNV disease forecasting approaches on the national scale. We used forecasts submitted to the 2020 WNV Forecasting Challenge, an open challenge organized by the Centers for Disease Control and Prevention, to assess the status of WNV neuroinvasive disease (WNND) prediction and identify avenues for improvement. Methods We performed a multi-model comparative assessment of probabilistic forecasts submitted by 15 teams for annual WNND cases in US counties for 2020 and assessed forecast accuracy, calibration, and discriminatory power. In the evaluation, we included forecasts produced by comparison models of varying complexity as benchmarks of forecast performance. We also used regression analysis to identify modeling approaches and contextual factors that were associated with forecast skill. Results Simple models based on historical WNND cases generally scored better than more complex models and combined higher discriminatory power with better calibration of uncertainty. Forecast skill improved across updated forecast submissions submitted during the 2020 season. Among models using additional data, inclusion of climate or human demographic data was associated with higher skill, while inclusion of mosquito or land use data was associated with lower skill. We also identified population size, extreme minimum winter temperature, and interannual variation in WNND cases as county-level characteristics associated with variation in forecast skill. Conclusions Historical WNND cases were strong predictors of future cases with minimal increase in skill achieved by models that included other factors. Although opportunities might exist to specifically improve predictions for areas with large populations and low or high winter temperatures, areas with high case-count variability are intrinsically more difficult to predict. Also, the prediction of outbreaks, which are outliers relative to typical case numbers, remains difficult. Further improvements to prediction could be obtained with improved calibration of forecast uncertainty and access to real-time data streams (e.g. current weather and preliminary human cases). Graphical Abstract

SUMMARY Predicting effects of climate change on plant disease is critical for protecting ecosystems and food production. Climate change could exacerbate plant disease because parasites may be quicker to acclimate and adapt to novel climatic conditions than their hosts due to their smaller body sizes and faster generation times. Here we show how disease pressure responds to the anomalous weather that will increasingly occur with climate change by compiling a global database (5380 plant populations; 437 unique plant–disease combinations; 2,858,795 individual plant–disease samples) of disease incidence in both agricultural and wild plant systems. Because wild plant populations are assumed to be adapted to local climates, we hypothesized that large deviations from historical conditions would increase disease incidence. By contrast, since agricultural plants have been transported globally, we did not expect the historical climate where they are currently grown to be as predictive of disease incidence. Supporting these hypotheses, we found that disease outbreaks tended to occur during periods of warm temperatures in agricultural and cool-climate wild plant systems, but also occurred in warm-adapted wild (but not agricultural) plant systems experiencing anomalously cool weather. Outbreaks were additionally associated with higher rainfall in wild systems, especially those with historically wet climates. Our results suggest that historical climate affects susceptibility to disease for wild plant–disease systems, while warming drives risks for agricultural plant disease outbreaks regardless of historical climate.

ABSTRACTParasitism is expected to change in a warmer future, but whether warming leads to substantial increases in parasitism remains unclear. Understanding how warming effects on parasitism in individual hosts (e.g., parasite load) translate to effects on population-level parasitism (e.g., prevalence, R0) remains a major knowledge gap. We analyzed the temperature dependence of parasitism at both host and population levels in thirteen empirical vector-borne host–parasite systems and found a strong, significant positive correlation between the thermal optima of individual- and population-level parasitism. We also found a significant, positive correlation in eleven environmentally-transmitted parasite systems, though several of these systems exhibited thermal optima >5ºC apart between individual and population levels. Similarly, parasitism thermal optima were close to host performance thermal optima in vector-borne systems but not in environmentally-transmitted systems. We then adapted and simulated simple models for both transmission modes and found a similar pattern to the empirical systems: thermal optima in vector-borne systems were more strongly correlated across scales compared to environmentally-transmitted systems. Generally, our results suggest that information on the temperature-dependence, and specifically the thermal optimum, at either the individual- or population-level should provide a useful—though not quantitatively exact—baseline for predicting temperature dependence at the other level, especially in vector-borne parasite systems. Environmentally-transmitted parasitism may operate by a different set of rules, in which temperature-dependence is decoupled in some systems, requiring the need for trait-based studies of temperature-dependence at individual and population levels.

The costs of mounting and maintaining an immune response lead to trade-offs with investment in (or maintenance of) other organ systems or functions such as reproduction, as has been observed in several taxa, including birds, insects, and mammals. Given these trade-offs, optimal strategies can be affected by biotic and abiotic conditions; however, how these trade-offs are affected by environmental variability remains unclear. Using a deterministic within-host model of disease dynamics, we analyzed the effect of environmental variability (here, the coefficient of variation in the host's background survival distribution) on the optimal resolution to a trade-off between investment in reproduction and the immune system. We found that higher variability led to increased investment in the immune system at the cost of decreased early-life reproduction when the immune investment strategy was assumed to be constant through life. Since we manipulated the distribution of lifespans while keeping the mean lifespan constant, our results suggest that even the small probability of living far past the mean lifespan for individuals in highly variable environments has a large effect on the optimal investment strategy. When immune investment was able to change over the age of the organism, the optimal investment strategies were again contingent on the level of environmental variability experienced by individuals. Our results support and extend previous work on optimal life-history theory in variable environments by showing that in the context of ecological immunology, the most fit individuals in constant environments are not the most fit individuals in variable environments. The effects of environmental variability on optimal immune investment are likely to have consequences for other aspects of infectious disease such as transmission dynamics, virulence evolution, and the likelihood of epidemics occurring.

The potential for adaptive evolution to enable species persistence under a changing climate is one of the most important questions for understanding impacts of future climate change. Climate adaptation may be particularly likely for short-lived ectotherms, including many pest, pathogen, and vector species. For these taxa, estimating climate adaptive potential is critical for accurate predictive modeling and public health preparedness. Here, we demonstrate how a simple theoretical framework used in conservation biology-evolutionary rescue models-can be used to investigate the potential for climate adaptation in these taxa, using mosquito thermal adaptation as a focal case. Synthesizing current evidence, we find that short mosquito generation times, high population growth rates, and strong temperature-imposed selection favor thermal adaptation. However, knowledge gaps about the extent of phenotypic and genotypic variation in thermal tolerance within mosquito populations, the environmental sensitivity of selection, and the role of phenotypic plasticity constrain our ability to make more precise estimates. We describe how common garden and selection experiments can be used to fill these data gaps. Lastly, we investigate the consequences of mosquito climate adaptation on disease transmission using Aedes aegypti-transmitted dengue virus in Northern Brazil as a case study. The approach outlined here can be applied to any disease vector or pest species and type of environmental change.

Vector-borne diseases (VBDs) are embedded within complex socio-ecological systems. While research has traditionally focused on the direct effects of VBDs on human morbidity and mortality, it is increasingly clear that their impacts are much more pervasive. VBDs are dynamically linked to feedbacks between environmental conditions, vector ecology, disease burden, and societal responses that drive transmission. As a result, VBDs have had profound influence on human history. Mechanisms include: (1) killing or debilitating large numbers of people, with demographic and population-level impacts; (2) differentially affecting populations based on prior history of disease exposure, immunity, and resistance; (3) being weaponised to promote or justify hierarchies of power, colonialism, racism, classism and sexism; (4) catalysing changes in ideas, institutions, infrastructure, technologies and social practices in efforts to control disease outbreaks; and (5) changing human relationships with the land and environment. We use historical and archaeological evidence interpreted through an ecological lens to illustrate how VBDs have shaped society and culture, focusing on case studies from four pertinent VBDs: plague, malaria, yellow fever and trypanosomiasis. By comparing across diseases, time periods and geographies, we highlight the enormous scope and variety of mechanisms by which VBDs have influenced human history.

Mathematical models of epidemics are important tools for predicting epidemic dynamics and evaluating interventions. Yet, because early models are built on limited information, it is unclear how long they will accurately capture epidemic dynamics. Using a stochastic SEIR model of COVID-19 fitted to reported deaths, we estimated transmission parameters at different time points during the first wave of the epidemic (March–June, 2020) in Santa Clara County, California. Although our estimated basic reproduction number ( R 0 ) remained stable from early April to late June (with an overall median of 3.76), our estimated effective reproduction number ( R E ) varied from 0.18 to 1.02 in April before stabilizing at 0.64 on 27 May. Between 22 April and 27 May, our model accurately predicted dynamics through June; however, the model did not predict rising summer cases after shelter-in-place orders were relaxed in June, which, in early July, was reflected in cases but not yet in deaths. While models are critical for informing intervention policy early in an epidemic, their performance will be limited as epidemic dynamics evolve. This paper is one of the first to evaluate the accuracy of an early epidemiological compartment model over time to understand the value and limitations of models during unfolding epidemics.

The extent to which vector-borne diseases (VBDs) have shaped human history remains under-recognized, even in the disease ecology community, despite several well-known examples. Although they represent a significant threat to global human health, accounting for more than one billion cases and one million deaths annually, VBDs have coexisted with humans since the advent of civilization and have migrated with humans around the world. Here, we synthesize historical, anthropological, and archaeological evidence and examine it through an ecological lens to illustrate how four major VBDs—plague, malaria, yellow fever, and trypanosomiasis—have shaped the course of human history through three main pathways: (1) outcomes of colonialism, imperialism, war, and conflict; (2) human interactions with the environment; and (3) intrasocietal human interactions. For example, malaria tipped the American Revolution toward the Continental Army; plague promoted reforestation in Europe; yellow fever entrenched African slavery in colonies in the Americas; trypanosomiasis impeded large settlements and central governments in pre-colonial sub-Saharan Africa. By drawing comparisons across diseases, time periods, and geographic locations, we show how VBDs have historically affected human populations, from the age of early Homo sapiens to the modern context, and how they continue to impact the world.

Accurately predicting and mitigating the effects of climate change on species ranges and interactions is a critical challenge. In particular, mosquito-borne diseases like malaria and dengue are poised to shift with climate change. Understanding this impact hinges on a key open question: How will mosquitoes adapt to climate change? Here we adapt a simple framework widely used in conservation biology—evolutionary rescue models—to investigate the potential for mosquito climate adaptation, and we synthesize current evidence, focusing on adaptation to rising temperatures. Short mosquito generation times, high population growth rates, and strong temperature-imposed selection favor mosquito thermal adaptation. However, knowledge gaps about the extent of phenotypic and genotypic variation in thermal tolerance within mosquito populations, the environmental sensitivity of selection, and the role of phenotypic plasticity constrain our ability to make more precise estimates. Future research efforts should prioritize filling these data gaps. Specifically, we outline how common garden and selection experiments can be used to this end. Collecting and incorporating these data into an evolutionary rescue framework will improve estimates of mosquito adaptive potential and of changes in mosquito-borne disease transmission under climate change, and this approach can be applied more broadly to pests as well as species of conservation concern.

Non-pharmaceutical interventions to combat COVID-19 transmission have worked to slow the spread of the epidemic but can have high socio-economic costs. It is critical we understand the efficacy of non-pharmaceutical interventions to choose a safe exit strategy. Many current models are not suitable for assessing exit strategies because they do not account for epidemic resurgence when social distancing ends prematurely (e.g., statistical curve fits) nor permit scenario exploration in specific locations. We developed an SEIR-type mechanistic epidemiological model of COVID-19 dynamics to explore temporally variable non-pharmaceutical interventions. We provide an interactive tool and code to estimate the transmission parameter, β, and the effective reproduction number, R eff . We fit the model to Santa Clara County, California, where an early epidemic start date and early shelter-in-place orders could provide a model for other regions. As of April 22, 2020, we estimate an R eff of 0.982 (95% CI: 0.849 - 1.107) in Santa Clara County. After June 1 (the end-date for Santa Clara County shelter-in-place as of April 27), we estimate a shift to partial social distancing, combined with rigorous testing and isolation of symptomatic individuals, is a viable alternative to indefinitely maintaining shelter-in-place. We also estimate that if Santa Clara County had waited one week longer before issuing shelter-in-place orders, 95 additional people would have died by April 22 (95% CI: 7 - 283). Given early life-saving shelter-in-place orders in Santa Clara County, longer-term moderate social distancing and testing and isolation of symptomatic individuals have the potential to contain the size and toll of the COVID-19 pandemic in Santa Clara County, and may be effective in other locations.

Predicting the effects of seasonality and climate change on the emergence and spread of infectious disease remains difficult, in part because of poorly understood connections between warming and the mechanisms driving disease. Trait-based mechanistic models combined with thermal performance curves arising from the metabolic theory of ecology (MTE) have been highlighted as a promising approach going forward; however, this framework has not been tested under controlled experimental conditions that isolate the role of gradual temporal warming on disease dynamics and emergence. Here, we provide experimental evidence that a slowly warming host–parasite system can be pushed through a critical transition into an epidemic state. We then show that a trait-based mechanistic model with MTE functional forms can predict the critical temperature for disease emergence, subsequent disease dynamics through time and final infection prevalence in an experimentally warmed system of Daphnia and a microsporidian parasite. Our results serve as a proof of principle that trait-based mechanistic models using MTE subfunctions can predict warming-induced disease emergence in data-rich systems—a critical step towards generalizing the approach to other systems.

AbstractEcological communities are partly structured by indirect interactions, where one species can indirectly affect another by altering its interactions with a third species. In the absence of direct predation, nonconsumptive effects of predators on prey have important implications for subsequent community interactions. To better understand these interactions, we used a Daphnia‐parasite‐predator cue system to evaluate if predation risk affects Daphnia responses to a parasite. We investigated the effects of predator cues on two aspects of host–parasite interactions (susceptibility to infection and infection intensity), and whether or not these effects differed between sexes. Our results show that changes in response to predator cues caused an increase in the prevalence and intensity of parasite infections in female predator‐exposed Daphnia. Importantly, the magnitude of infection risk depended on how long Daphnia were exposed to the cues. Additionally, heavily infected Daphnia that were constantly exposed to cues produced relatively more offspring. While males were ~5× less likely to become infected compared to females, we were unable to detect effects of predator cues on male Daphnia–parasite interactions. In sum, predators, prey, and their parasites can form complex subnetworks in food webs, necessitating a nuanced understanding of how nonconsumptive effects may mediate these interactions.

Despite its pivotal role in evolutionary and ecological processes the genetic architecture underlying host-parasite interactions remains understudied. Here we use a quantitative trait loci approach to identify regions in the Daphnia magna genome that provide resistance against its microsporidium parasite Ordospora colligata . The probability that Daphnia became infected was affected by a single locus and an interaction between two additional loci. A fourth locus influenced the number of spores that grew within the host. Comparing our findings to previously published genetic work on Daphnia magna revealed that two of these loci may be the same as detected for another microsporidium parasite, suggesting a general immune response to this group of pathogens. More importantly, this comparison revealed that two regions previously identified to be under selection coincided with parasite resistance loci, highlighting the pivotal role parasites may play in shaping the host genome.