Temperature drives ectothermic host - parasite interactions, making them particularly sensitive to climatic variation and change. To isolate the role of temperature, lab-based studies are increasingly used to assess and forecast disease risk under current and future climate conditions. However, in the field, the effects of temperature on parasitism may be mediated by other sources of variation, including local adaptation of hosts and parasites to one another and to the environment. To address the key knowledge gaps of how temperature influences host - parasite interactions and whether thermal responses measured in controlled experiments capture infection across temperature gradients in nature, we paired an extensive field survey of parasitism-by the ciliate Lambornella clarki on its tree hole mosquito host, Aedes sierrensis -with laboratory experiments describing parasitism thermal performance curves (TPCs) for six host populations from varying climates. We also investigated the mechanisms underlying the thermal biology of the host - parasite interaction by separately measuring TPCs for infection, host immunity, and parasite growth rates. Along the west coast of North America, across an 1100 km climate gradient spanning 12°C mean rainy season temperature variation, we found that parasitism peaked at intermediately cold temperatures of 9.2 - 10°C, and was consistent both between field seasons and with the lab experiment results. In the laboratory experiments, infection thermal responses were consistently nonlinear and peaked at 8.4 - 10°C, showing no evidence of host intraspecific variation in temperature sensitivity to parasitism. Importantly, parasitism peaked at temperatures below the thermal optimum for free-living L. clarki due to the balance of temperature effects on parasite growth and reproduction against the strength of the host melanization immune response. The results suggest that nonlinear responses to temperature drive parasitism in nature, and that simple lab and field studies can accurately capture the thermal biology of multilayered host - parasite interactions.

Land use change and deforestation drive both biodiversity loss and zoonotic disease transmission in tropical countrysides. For mosquito communities that can include disease vectors, forest loss has been linked to reduced biodiversity and increased vector presence. The spatial scales at which land use and tree cover shape mosquito communities present a knowledge gap relevant to both biodiversity and public health. We investigated the responses of mosquito species richness and Aedes albopictus disease vector presence to land use and to tree cover surrounding survey sites at different spatial scales. We also investigated species compositional turnover across land uses and along environmental gradients. We paired a field survey of mosquito communities in agricultural, residential, and forested lands in rural southern Costa Rica with remotely sensed tree cover data. We compared mosquito richness and vector presence responses to tree cover measured across scales from 30 to 1000 m, and across land uses. We analyzed mosquito community compositional turnover between land uses and along environmental gradients of tree cover, temperature, elevation, and geographic distance. Tree cover was both positively correlated with mosquito species richness and negatively correlated with the presence of the common invasive dengue vector Ae. albopictus at small spatial scales of 90–250 m. Land use predicted community composition and Ae. albopictus presence. The results suggest that local tree cover preservation and expansion can support mosquito species richness and reduce disease vector presence. The identified spatial range at which tree cover shapes mosquito communities can inform the development of land management practices to protect both ecosystem and public health.

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.

The concurrent pressures of rising global temperatures, rates and incidence of species decline, and emergence of infectious diseases represent an unprecedented planetary crisis. Intergovernmental reports have drawn focus to the escalating climate and biodiversity crises and the connections between them, but interactions among all three pressures have been largely overlooked. Non-linearities and dampening and reinforcing interactions among pressures make considering interconnections essential to anticipating planetary challenges. In this Review, we define and exemplify the causal pathways that link the three global pressures of climate change, biodiversity loss, and infectious disease. A literature assessment and case studies show that the mechanisms between certain pairs of pressures are better understood than others and that the full triad of interactions is rarely considered. Although challenges to evaluating these interactions—including a mismatch in scales, data availability, and methods—are substantial, current approaches would benefit from expanding scientific cultures to embrace interdisciplinarity and from integrating animal, human, and environmental perspectives. Considering the full suite of connections would be transformative for planetary health by identifying potential for co-benefits and mutually beneficial scenarios, and highlighting where a narrow focus on solutions to one pressure might aggravate another.

Climate change will alter interactions between parasites and their hosts. Warming may affect patterns of local adaptation, shifting the environment to favor the parasite or host and thus changing the prevalence of disease. We assessed local adaptation in the facultative ciliate parasite Lambornella clarki, which infects the western tree hole mosquito Aedes sierrensis. We conducted laboratory infection experiments with mosquito larvae and parasites collected from across a climate gradient, pairing sympatric or allopatric populations across three temperatures that were either matched or mismatched to the source environment. L. clarki parasites were locally adapted to their hosts, with 2.6x higher infection rates on sympatric compared to allopatric populations, but were not locally adapted to temperature. Infection peaked at the intermediate temperature of 13°C. Our results highlight the importance of host selective pressure on parasites, despite the impact of temperature on infection success.

Climate warming is expected to substantially impact the global landscape of mosquito-borne disease, but these impacts will vary across disease systems and regions. Understanding which diseases, and where within their distributions, these impacts are most likely to occur is critical for preparing public health interventions. While research has centered on potential warming-driven expansions in vector transmission, less is known about the potential for vectors to experience warming-driven stress or even local extirpations. In conservation biology, species risk from climate warming is often quantified through vulnerability indices such as thermal safety margins-the difference between an organism's upper thermal limit and its habitat temperature. Here, we estimated thermal safety margins for 8 mosquito species that are the vectors of malaria, dengue, chikungunya, Zika, West Nile and other major arboviruses, across their known ranges to investigate which mosquitoes and regions are most and least vulnerable to climate warming. We find that several of the most medically important mosquito vector species, including Ae. aegypti and An. gambiae, have positive thermal safety margins across the majority of their ranges when realistic assumptions of mosquito behavioral thermoregulation are incorporated. On average, the lowest climate vulnerability, in terms of both the magnitude and duration of thermal safety, was just south of the equator and at northern temperate range edges, and the highest climate vulnerability was in the subtropics. Mosquitoes living in regions including the Middle East, the western Sahara, and southeastern Australia, which are largely comprised of desert and xeric shrubland biomes, have the highest climate vulnerability across vector species.

Variation in heat tolerance among populations can determine whether a species is able to cope with ongoing climate change. Such variation may be especially important for ectotherms whose body temperatures, and consequently, physiological processes, are regulated by external conditions. Additionally, differences in body size are often associated with latitudinal clines, thought to be driven by climate gradients. While studies have begun to explore variation in body size and heat tolerance within species, our understanding of these patterns across large spatial scales, particularly regarding the roles of plasticity and genetic differences, remains incomplete. Here, we examine body size, as measured by wing length, and thermal tolerance, as measured by the time to immobilisation at high temperatures (“thermal knockdown”), in populations of the mosquito Aedes sierrensis collected from across a large latitudinal climate gradient spanning 1300 km (34–44° N). We find that mosquitoes collected from lower latitudes and warmer climates were more tolerant of high temperatures than those collected from higher latitudes and colder climates. Moreover, body size increased with latitude and decreased with temperature, a pattern consistent with James' rule, which appears to be a result of plasticity rather than genetic variation. Our results suggest that warmer environments produce smaller and more thermally tolerant populations.

How mosquitoes may respond to rapid climate warming remains unknown for most species, but will have major consequences for their future distributions, with cascading impacts on human well-being, biodiversity and ecosystem function. We investigated the adaptive potential of a wide-ranging mosquito species, Aedes sierrensis, across a large climatic gradient by conducting a common garden experiment measuring the thermal limits of mosquito life-history traits. Although field-collected populations originated from vastly different thermal environments that spanned over 1200 km, we found limited variation in upper thermal tolerance between populations. In particular, the upper thermal limits of all life-history traits varied by less than 3°C across the species range and, for most traits, did not differ significantly between populations. For one life-history trait-pupal development rate-we did detect significant variation in upper thermal limits between populations, and this variation was strongly correlated with source temperatures, providing evidence of local thermal adaptation for pupal development. However, we found that maximum environmental temperatures across most of the species' range already regularly exceed the highest upper thermal limits estimated under constant temperatures. This result suggests that strategies for coping with and/or avoiding thermal extremes are likely key components of current and future mosquito thermal tolerance.

Parasites play key roles in regulating aquatic ecosystems, yet the impact of climate warming on their ecology and disease transmission remains poorly understood. Isolating the effect of warming is challenging as transmission involves multiple interacting species and potential intraspecific variation in temperature responses of one or more of these species. Here, we leverage a wide-ranging mosquito species and its facultative parasite as a model system to investigate the impact of temperature on host–parasite interactions and disease transmission. We conducted a common garden experiment measuring parasite growth and infection rates at seven temperatures using 12 field-collected parasite populations and a single mosquito population. We find that both free-living growth rates and infection rates varied with temperature, which were highest at 18–24.5 °C and 13 °C, respectively. Further, we find intraspecific variation in peak performance temperature reflecting patterns of local thermal adaptation—parasite populations from warmer source environments typically had higher thermal optima for free-living growth rates. For infection rates, we found a significant interaction between parasite population and nonlinear effects of temperature. These findings underscore the need to consider both host and parasite thermal responses, as well as intraspecific variation in thermal responses, when predicting the impacts of climate change on disease in aquatic ecosystems.

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.

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.

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.

The role of infectious disease in regulating host populations is increasingly recognized, but how environmental conditions affect pathogen communities and infection levels remains poorly understood. Over 3 y, we compared foliar disease burden, fungal pathogen community composition, and foliar chemistry in the perennial bunchgrass Stipa pulchra occurring in adjacent serpentine and nonserpentine grassland habitats with distinct soil types and plant communities. We found that serpentine and nonserpentine S. pulchra experienced consistent, low disease pressure associated with distinct fungal pathogen communities with high interannual species turnover. Additionally, plant chemistry differed with habitat type. The results indicate that this species experiences minimal foliar disease associated with diverse fungal communities that are structured across landscapes by spatially and temporally variable conditions. Distinct fungal communities associated with different growing conditions may shield S. pulchra from large disease outbreaks, contributing to the low disease burden observed on this and other Mediterranean grassland species.

The role of infectious disease in regulating host populations is increasingly recognized, but the environmental conditions that facilitate versus hinder pathogen-mediated population regulation remain poorly understood. We compared the relative contributions of soil type and pathogen community composition to foliar disease burden in a perennial bunchgrass species found on two distinct soil types that support distinct plant communities in a California grassland. We hypothesized that populations on different soil types would have significantly different disease burdens caused by unique pathogen communities. To test this hypothesis, we compared foliar disease burden and foliar fungal pathogen communities in nearby populations of Stipa pulchra found in nonserpentine greenstone soil that is dominated by invasive Mediterranean grasses, and in serpentine soil, a harsh soil high in heavy metals and low in essential nutrients that supports a diverse community of native plant species. We analyzed the chemical makeup of serpentine and nonserpentine plant tissue to understand potential impacts of soil chemistry on plant health and pathogen community composition. We found that serpentine and nonserpentine S. pulchra experienced consistent, low disease pressure caused by distinct communities of foliar pathogens, and that serpentine plants, like the soil in which they grew, had elevated Ni and Mg content and decreased C, N, Ca, and P content compared to nonserpentine plants. The results imply that pathogens are unlikely to regulate the population dynamics of this native plant, and that pathogen communities are structured either by plant community composition or tissue chemistry. Local variation in soil type and annually variable conditions associated with high species turnover in pathogen communities may create a refuge from disease outbreaks for S. pulchra, contributing to the low disease burden observed on this and other Mediterranean grassland species.