Corresponding author:
Lisa Couper
lcouper@stanford.edu
327 Campus Drive, Stanford CA, 94305
Type of article: Ideas and Perspectives
Short running title: Mosquito climate adaptation
Key words: climate change, adaptation, mosquito, vector, evolutionary rescue, thermal tolerance
Abstract word count: 202
Main text word count: 6,403
Text Box 1 word count: 232
Number of figures, tables, and textboxes : 3 total (2 figures, 0 tables, 1 textbox)
Statement of authorship: LIC, JEF, and EAM conceived of the project. All authors contributed to the conceptual design, literature review, and writing. MSS performed analysis for Table S2. LIC and JEF wrote the first draft of the manuscript, and all authors contributed substantially to revisions.
Data accessibility statement: All data supporting the results will be archived in Dryad and the data DOI will be included at the end of the article.
Abstract
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.
Introduction
The potential for adaptive evolution to enable species persistence under a changing climate is one of the most important questions for understanding future climate change impacts (Lavergne et al. 2010). Evolutionary change on ecological time scales (tens of generations) has been documented across a wide range of taxa, suggesting that some species could adapt as quickly as the climate is changing (reviewed in Thompson 1998, Hairston et al. 2005, Carroll et al. 2007, Reznick et al. 2019). Evidence of evolutionary adaptation to contemporary climate change is more limited, but has emerged for diverse taxa including mammals (Réale et al. 2003), fish (Kovach et al. 2012), plants (Franks et al. 2007, Exposito-Alonso et al. 2018), birds (Nussey et al. 2005, Karell et al. 2011), and insects (Umina et al. 2005). However, while climate adaptation has typically been studied in the context of conservation biology, population genetics theory suggests that evolutionary climate adaptation is more likely for short-lived species with large population sizes—properties of many pest species, including disease vector species (Lynch and Lande 1993, Bürger and Lynch 1995). For these pest and vector species, the unknown potential for climate adaptation threatens human health and well-being.
Mosquito-borne diseases are a major public health burden, causing an estimated 500 million cases and millions of deaths globally each year (World Health Organization 2014, 2018). Studies of how environmental conditions influence mosquito-borne disease risk highlight temperature—and by extension, climate warming—as an important driver of transmission dynamics (Shragai et al. 2017, Mordecai et al. 2019, Franklinos et al. 2019). Temperature influences mosquito-borne disease dynamics because it directly affects mosquito physiology, life cycles, behavior, and competence for disease transmission (Cator et al. 2020). For mosquitoes, as with other ectotherms, temperature has strong, nonlinear effects on traits such as survival and fecundity that lead to unimodal effects on fitness, where temperatures above and below intermediate thermal optima suppress mosquito population growth (Huey and Stevenson 1979, Huey and Berrigan 2001, Angilletta 2009, Amarasekare and Savage 2012). Recent forecasts based on this relationship predict that in some areas where disease risk is currently high, future risk will decrease as temperatures exceed mosquito thermal optima and limits (Gething et al. 2010, Ryan et al. 2015, 2019, Mordecai et al. 2019, 2020). However, if mosquitoes adapt to climate warming by increasing their thermal tolerance, then these predictions are likely to underestimate future disease risk.
Recent research demonstrates the potential for mosquito climate adaptation within a few decades. For example, multiple lines of evidence indicate that the invasive Asian tiger mosquito (Aedes albopictus ) responds to novel temperature conditions within 10 – 30 years of population expansions into new locations. Putative adaptive responses observed on this timescale include altered allele frequencies, thermal niche shifts reflecting greater cold tolerance, and photoperiod responses that influence overwintering survival (Medley 2010, Urbanski et al. 2012, Egizi et al. 2015, Medley et al. 2019). Similarly, genetically based shifts in photoperiod towards shorter, more southern daylengths in association with recent warming occurred in as little as five years in the pitcher-plant mosquito (Wyeomyia smithii ) (Bradshaw and Holzapfel 2001). While these examples cover just two species, and do not provide precise evidence for the pace of thermal adaptation in response to climate warming, they indicate that there is potential for rapid climate adaptation in mosquitoes.
Here, we take advantage of substantial recent research progress on mosquito thermal biology (reviewed in Mordecai et al. 2019) and the impact of temperature change on mosquito-borne disease (reviewed in Andriamifidy et al. 2019, Franklinos et al. 2019) to address a key open question: How will mosquitoes adapt to climate change? We provide a theoretical framework for addressing this question and synthesize direct and indirect evidence of mosquito climate adaptation. In the following sections, we 1) outline how to investigate mosquito adaptive potential, positing evolutionary rescue models as a guiding framework, 2) synthesize evidence and identify key data gaps for predictive modeling, and 3) highlight priorities and approaches for filling these gaps. We discuss the adaptive potential of mosquitoes broadly, but our principal interest is in major disease vector species (e.g., Aedes aegypti, Ae. albopictus, Anopheles gambiae, Culex pipiens, Cx. quinquefasciatus , which transmit dengue, chikungunya, Zika, and West Nile viruses, malaria, and other pathogens) and we discuss species-specific responses where possible. We focus here on adaptation to warming temperatures that exceed current mosquito thermal optima, but the approach we describe can be applied to study the adaptive potential of any species in response to any specific environmental change.
Framework for investigating climate adaptation
Mosquitoes may respond to warming temperatures through three primary mechanisms: tracking suitable temperatures through range shifts, avoiding or temporarily coping with stressful temperatures through phenotypic plasticity, and tolerating warming through evolutionary adaptation. Here we focus on evolutionary adaptation as it would enablein situ mosquito population persistence under sustained environmental change and is currently the least well-understood climate response (Merilä and Hendry 2014, Urban et al. 2016). Investigating the potential for evolutionary climate adaptation requires identifying: 1) the climate factors currently limiting population persistence, 2) the most climate-sensitive and fitness-relevant traits, and 3) the potential evolutionary rates of these traits (Figure 1).