Rethinking vector immunology: the role of environmental temperature in shaping resistance

Murdock, Courtney C.; Paaijmans, Krijn P.; Cox-Foster, Diana; Read, Andrew F.; Thomas, Matthew B.

doi:10.1038/nrmicro2900

Cited by 120 publications

(104 citation statements)

References 102 publications

(139 reference statements)

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“…Furthermore, temperature may play a critical role, not just in the behavioral and physiological processes of the organism per se , but also in the host–pathogen interactions (Murdock et al. 2012b). For instance, thermoregulation and expression of behavioral fever in Schistocerca gregaria dramatically reduce its chance of succumbing to fungal disease (Elliot et al.…”

Section: Introductionmentioning

confidence: 99%

Temperature and population density: interactional effects of environmental factors on phenotypic plasticity, immune defenses, and disease resistance in an insect pest

Silva

Elliot

2016

Ecology and Evolution

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Temperature and crowding are key environmental factors mediating the transmission and epizooty of infectious disease in ectotherm animals. The host physiology may be altered in a temperature‐dependent manner and thus affects the pathogen development and course of diseases within an individual and host population, or the transmission rates (or infectivity) of pathogens shift linearly with the host population density. To our understanding, the knowledge of interactive and synergistic effects of temperature and population density on the host–pathogen system is limited. Here, we tested the interactional effects of these environmental factors on phenotypic plasticity, immune defenses, and disease resistance in the velvetbean caterpillar Anticarsia gemmatalis. Upon egg hatching, caterpillars were reared in thermostat‐controlled chambers in a 2 × 4 factorial design: density (1 or 8 caterpillars/pot) and temperature (20, 24, 28, or 32°C). Of the immune defenses assessed, encapsulation response was directly affected by none of the environmental factors; capsule melanization increased with temperature in both lone‐ and group‐reared caterpillars, although the lone‐reared ones presented the most evident response, and hemocyte numbers decreased with temperature regardless of the population density. Temperature, but not population density, affected considerably the time from inoculation to death of velvetbean caterpillar. Thus, velvetbean caterpillars succumbed to Anticarsia gemmatalis multiple nucleopolyhedrovirus (AgMNPV) more quickly at higher temperatures than at lower temperatures. As hypothesized, temperature likely affected caterpillars' movement rates, and thus the contact between conspecifics, which in turn affected the phenotypic expression of group‐reared caterpillars. Our results suggest that environmental factors, mainly temperature, strongly affect both the course of disease in velvetbean caterpillar population and its defenses against pathogens. As a soybean pest, velvetbean caterpillar may increase its damage on soybean fields under a scenario of global warming as caterpillars may reach the developmental resistance faster, and thus decrease their susceptibility to biological control by AgMNPV.

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Section: Introductionmentioning

confidence: 99%

Temperature and population density: interactional effects of environmental factors on phenotypic plasticity, immune defenses, and disease resistance in an insect pest

Silva

Elliot

2016

Ecology and Evolution

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“…The existence of such G Â G interactions implies that the effect of vector genes controlling competence depends on the pathogen genotype [6][7][8]. Several recent ecological studies have also emphasized the role of environmental factors, such as ambient temperature, in shaping mosquito vector competence for pathogens [9,10]. For example, the immune response and resistance of Anopheles mosquitoes to bacterial challenge strongly depended on environmental drivers such as mean temperature, diurnal temperature variation and time of infection [11].…”

Section: Introductionmentioning

confidence: 99%

Three-way interactions between mosquito population, viral strain and temperature underlying chikungunya virus transmission potential

et al. 2014

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Interactions between pathogens and their insect vectors in nature are under the control of both genetic and non-genetic factors, yet most studies on mosquito vector competence for human pathogens are conducted in laboratory systems that do not consider genetic and/or environmental variability. Evaluating the risk of emergence of arthropod-borne viruses (arboviruses) of public health importance such as chikungunya virus (CHIKV) requires a more realistic appraisal of genetic and environmental contributions to vector competence. In particular, sources of variation do not necessarily act independently and may combine in the form of interactions. Here, we measured CHIKV transmission potential by the mosquito Aedes albopictus in all combinations of six worldwide vector populations, two virus strains and two ambient temperatures (208C and 288C). Overall, CHIKV transmission potential by Ae. albopictus strongly depended on the three-way combination of mosquito population, virus strain and temperature. Such genotype-by-genotype-by-environment (G Â G Â E) interactions question the relevance of vector competence studies conducted with a simpler set of conditions. Our results highlight the need to account for the complex interplay between vectors, pathogens and environmental factors to accurately assess the potential of vector-borne diseases to emerge.

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“…55 Though the fundamental mechanism involved in viral blocking, demonstrated in both Drosophila and Aedes, does not seem to be dependent on the upregulation of the immune effectors, it is likely that Wolbachia-associated immune priming in mosquitoes can enhance the virus blocking phenotype. 56,57 Furthermore, microbial gut flora of mosquito interacts with host immune system to determine the outcome of host-pathogen interactions, 28,58 and evidence is emerging on how temperature can affect the presence and quantity of symbionts in insect's gut to influence host fitness.…”

Section: Discussionmentioning

confidence: 99%

The Effect of Temperature on Wolbachia-Mediated Dengue Virus Blocking in Aedes aegypti

Ye¹,

Carrasco²,

Dong³

et al. 2016

The American Journal of Tropical Medicine and Hygiene

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Abstract. Dengue fever, caused by dengue virus (DENV), is endemic in more than 100 countries. The lack of effective treatment of patients and the suboptimal efficacies of the tetravalent vaccine in trials highlight the urgent need to develop alternative strategies to lessen the burden of dengue fever. Wolbachia pipientis, an obligate intracellular bacterium, is being developed as a biocontrol strategy against dengue because it limits the replication of the DENV in the mosquito vector, Aedes aegypti. However, several recent studies have demonstrated the sensitivity of pathogens, vectors, and their symbionts to temperature. To understand how the tripartite interactions between the mosquito, DENV, and Wolbachia may change under different temperature regimes, we assessed the vector competence and transmission potential of DENV-infected mosquitoes reared at a common laboratory setting of a constant 25°C and at two diurnal temperature settings with mean of 25°C and 28°C and a fluctuating range of 8°C (±4°C). Temperature significantly affected DENV infection rate in the mosquitoes. Furthermore, temperature significantly influenced the proportion of mosquitoes that achieved transmission potential as measured by the presence of virus in the saliva. Regardless of the temperature regimes, Wolbachia significantly and efficiently reduced the proportion of mosquitoes achieving infection and transmission potential across all the temperature regimes studied. This work reinforces the robustness of the Wolbachia biocontrol strategy to field conditions in Cairns, Australia, and suggests that similar studies are required for local mosquito genotypes and field relevant temperatures for emerging field release sites globally.

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Rethinking vector immunology: the role of environmental temperature in shaping resistance

Cited by 120 publications

References 102 publications

Temperature and population density: interactional effects of environmental factors on phenotypic plasticity, immune defenses, and disease resistance in an insect pest

Temperature and population density: interactional effects of environmental factors on phenotypic plasticity, immune defenses, and disease resistance in an insect pest

Three-way interactions between mosquito population, viral strain and temperature underlying chikungunya virus transmission potential

The Effect of Temperature on Wolbachia-Mediated Dengue Virus Blocking in Aedes aegypti

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