Briefing Document: Heat Exposure and Mosquito-Virus Interaction

Source: Perdomo, H. D., Khorramnejad, A., Cham, N. M., Kropf, A., Sogliani, D., & Bonizzoni, M. (2025). Prolonged exposure to heat enhances mosquito tolerance to viral infection. Communications Biology, 8(1), 761. https://doi.org/10.1038/s42003-025-07617-8

Dates: Received - 27 September 2024 | Accepted - 28 January 2025 | Published - 04 February 2025

Prepared for: Saleh Lab

Executive Summary:

This study investigates the impact of increased environmental temperature on the interaction between the mosquito species Aedes albopictus and the cell fusing agent virus (CFAV), an insect-specific virus. The researchers examined how short-term (one generation) and long-term (ten generations) exposure to a higher temperature (32°C/26°C day/night cycle) influences mosquito tolerance and resistance to CFAV infection, as well as their overall fitness. The key findings reveal that prolonged heat exposure leads to increased viral tolerance in mosquitoes without significant fitness costs, while short-term heat exposure results in increased resistance but at the expense of mosquito fitness. These findings have significant implications for understanding the effects of climate change on arbovirus transmission dynamics and the evolution of both mosquito vectors and the viruses they carry.

Main Themes and Important Ideas/Facts:

• Climate Change and Arbovirus Transmission:
• The study highlights the complex interplay between climate change, mosquito biology, and virus interactions, emphasizing the relevance of this research to the prevalence and transmission dynamics of arboviruses like dengue, Zika, and chikungunya, which threaten billions globally.
• "Current anthropogenic climate change has profound and complex impli-cations for the prevalence and the transmission dynamics of arboviruses such as dengue, Zika and chikungunya, which are an impending risk for 3.9 billion people in tropical and subtropical areas of the world."
• Rising temperatures are expected to shift the distribution and phenology of key arboviral vectors, Aedes aegypti and Aedes albopictus, further expanding disease risk.
• While increased temperature is known to accelerate viral replication in mosquitoes, the impact of temperature on the mosquito's response to viruses has been largely unexplored.
• Resistance vs. Tolerance in Mosquito Immunity:
• The study distinguishes between two key immunological strategies in mosquitoes: resistance (limiting viral replication) and tolerance (controlling the cost of infection without reducing viral load).
• The researchers employed a framework developed in plant pathology using reaction norms (measuring host longevity across pathogen doses) to differentiate between resistance and tolerance.
• Resistance exerts strong selective pressure on viruses, while tolerance has neutral or even positive effects on them. Understanding the shift between these responses due to climate change is crucial for predicting viral transmission dynamics and long-term evolutionary impacts.
• Experimental Design: Thermal Acclimation vs. Evolution:
• The study mimicked both acute thermal fluctuations (heat waves) and gradual, prolonged warming by exposing Aedes albopictus mosquitoes to a hot thermal regime (32°C for 14 hours, 26°C for 10 hours) for one generation (warm-acclimated) or ten generations (warm-evolved).
• These groups were compared to a control group maintained under standard laboratory conditions (28°C). All infected mosquitoes were kept at their rearing temperature post-infection.
• Prolonged Heat Exposure Enhances Viral Tolerance:
• Warm-evolved mosquitoes demonstrated increased tolerance to CFAV infection, meaning they could withstand higher viral loads without significant reductions in longevity.
• "We show that the length of the thermal challenge influences the outcome of the infection with warm-evolvedmosquitoes beingmore tolerant to CFAV infection..."
• Tolerance curves showed that warm-evolved mosquitoes had comparable vigour (survival time of uninfected hosts) to the standard group and the lowest severity (longevity at the highest viral load).
• "Multi-generational exposure to heat imposes no cost on CFAV infected mosquitoes."
• Short-Term Heat Exposure Enhances Viral Resistance but with Fitness Costs:
• Warm-acclimated mosquitoes exhibited higher resistance to CFAV, showing lower viral prevalence and load at 3 days post-infection compared to both warm-evolved and standard mosquitoes.
• "...warm-acclimatedmosquitoes being more resistant..."
• However, this increased resistance came at a cost, as warm-acclimated mosquitoes displayed reduced longevity and fecundity, and increased sterility and infertility, even in the absence of viral infection, suggesting the thermal challenge itself is stressful.
• "One generational exposure to heat...results in fitness costs and increased resistance to viral infection."
• Implications for Arbovirus Transmission:
• The shift towards tolerance in warm-evolved mosquitoes has significant implications for arbovirus transmission. While they may control viral replication less effectively (lower resistance), their ability to survive infection with higher viral loads could increase the likelihood of transmission over a longer period.
• "Increased viral tolerance raises the likelihood of viral trans-mission in warm-evolved mosquitoes."
• The study suggests that the duration of heat exposure is a critical factor in determining mosquito immune response and, consequently, arbovirus transmission dynamics.
• Implications for Biological Control using Insect-Specific Viruses (ISVs):
• The findings that temperature modulates CFAV prevalence and load have implications for the potential use of CFAV as a biological control agent against arboviruses.
• Short-term heat fluctuations could negatively impact CFAV prevalence in mosquito populations, while prolonged warming might favor its persistence.
• "Considering the potential application of CFAV as a biological control agent, our results support the conclusion that global warming could favour CFAV persistence, but unexpected thermal fluctuations could negatively impact its prevalence in mosquito populations."
• Evolutionary Consequences of Resistance and Tolerance:
• The study discusses the contrasting evolutionary pressures exerted by resistance and tolerance mechanisms on both mosquitoes and viruses.
• Resistance can drive an "arms race" leading to rapid molecular evolution.
• Tolerance, by minimizing the cost of infection, may reduce selective pressure on viruses, leading to different evolutionary trajectories.
• The interplay and potential trade-offs between resistance and tolerance mechanisms are crucial for understanding the long-term co-evolution of vectors and viruses.

Quotes:

• "These results highlight the importance of considering fluctuations in vector immunity in relation to the length of a thermal challenge to understand natural variation in vector response to viruses and frame realistic transmission models."
• "Exposure to heat increases overall Ae. albopictus tolerance to CFAV infection, but the length of the thermal challenge alters mosquito fitness and influences the immunological response to CFAV."
• "Thermal adaptation includesprofoundand...