Review Article

Ecology

How will mosquitoes adapt to climate warming?

Department of Biology, Stanford University, United States
Department of Biology, University of Hawaii at Manoa, United States
Emmett Interdisciplinary Program in Environment and Resources, Stanford University, United States
Department of Zoology, University of Toronto, Canada
Department of Ecology and Evolutionary Biology, University of California Los Angeles, United States
Environmental Futures Research Institute, Griffith University, Australia
Department of Integrative Biology, University of California, Berkeley, United States
Department of Plant Biology, Carnegie Institution for Science, United States

Aug 17, 2021

https://doi.org/10.7554/eLife.69630

Open access
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Figures
Tables

3 figures and 4 tables

Figures

Figure 1

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Framework for investigating climate adaptive potential.

Several mechanisms may enable in situ population persistence (evolutionary adaptations in physiology, phenotypic plasticity, phenological shifts, and life history adjustments; panels A and B). Investigating the potential for evolutionary climate adaptation requires first identifying the climate factors and traits limiting population persistence (panel C), then comparing the rate of projected climatic change to potential evolutionary rates (panel D). Evolutionary rates can be estimated based on evolutionary potential (strength of selection, and heritability and variation in the trait of interest), population demographic characteristics (maximum growth rate and generation time), and trait – environment relationships (phenotypic plasticity and environmental sensitivity of selection) (panel E). In the strength of selection image (top left, panel E), the dashed and solid lines indicate the population before and after natural selection, respectively. In the heritability panel (bottom left), P1 and F1 denote the parental and offspring generations, respectively.

Figure 2

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Case study on *Ae. aegypti*-transmitted dengue suitability.

Under current conditions, monthly dengue transmission suitability (i.e., $R_{0} (T)$ > 0) based on mean monthly temperatures is high throughout Northern Brazil (A, B). Transmission suitability is projected to decline by 2080 under the RCP 8.5 climate scenario (C), as temperatures exceed mosquito upper thermal limits. To maintain current monthly transmission suitability under temperatures projected for 2080, evolutionary change, in the form of an increased critical thermal maximum of *Ae. aegypti* fecundity (D) may be required, with greater evolutionary change required in areas with greater projected warming.

Appendix 2—figure 1

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Tables

Table 1

State of knowledge on evolutionary rescue model parameters for mosquito and Drosophila species.

Numbers correspond to references; colors correspond to data availability. Purple indicates that data for these parameters are readily available (but not for all species or contexts). Blue indicates that some data are available, but further collection is warranted. Green indicates that minimal or indirect data are available (e.g. dormancy mechanisms suspected based on rapid mosquito population increases following the dry season). Yellow indicates that no estimates are available on these parameters (to our knowledge). Measurements on variation in thermal tolerance are designated as ‘inter-population’ or ‘intra-population.’.

	Available data	State of knowledge
	Some data
	Minimal or indirect data
	No data	Mosquitoes	Drosophila
Generation time		Mordecai et al., 2017; Johnson et al., 2015; Shocket et al., 2020	Crow and Chung, 1967; Lin et al., 2014; Fernández-Moreno et al., 2007; Ashburner, 1989; Emiljanowicz et al., 2014
Maximum population growth rate		Mordecai et al., 2017; Johnson et al., 2015; Shocket et al., 2020; Amarasekare and Savage, 2012	Siddiqui and Barlow, 1972; Emiljanowicz et al., 2014; Chiang and Hodson, 1950; Mueller and Ayala, 1981
Variation in thermal tolerance		[Inter-population variation] Ruybal et al., 2016; Dodson et al., 2012; Reisen, 1995; Mogi, 1992; Chu et al., 2019; Vorhees et al., 2013; Rocca et al., 2009	[Intra-population variation] Rolandi et al., 2018; Fallis et al., 2011 [Between-population variation] Sørensen et al., 2001; Sgrò et al., 2010 Hangartner and Hoffmann, 2016; ; Rashkovetsky et al., 2006; Lockwood et al., 2018
Heritability			Mitchell and Hoffmann, 2010; Huey et al., 1992; Hangartner and Hoffmann, 2016; Jenkins and Hoffmann, 1994; McColl et al., 1996; Castañeda et al., 2019
Strength of selection		reviewed in Mordecai et al., 2019	Rezende et al., 2020; Huey et al., 1991; Huey et al., 1992; Loeschcke and Hoffmann, 2007
Phenotypic plasticity	Acclimation	Gray, 2013; Lyons et al., 2012; Benedict et al., 1991; Armbruster et al., 1999; Sivan et al., 2021	MacLean et al., 2019; Hoffmann and Watson, 1993; Sgrò et al., 2010; Overgaard et al., 2011; Berrigan and Hoffmann, 1998
	Behavioral thermo-regulation	Reisen and Aslamkhan, 1978; Voorham, 2002; Barrera et al., 2008; Haufe and Burgess, 1956; Verhulst et al., 2020; Blanford et al., 2013; Thomson, 1938	Castañeda et al., 2013; Dillon et al., 2009; MacLean et al., 2019; Huey and Pascual, 2009; Wang et al., 2008; ; Feder et al., 1997; Gibbs et al., 2003
	Dormancy	Dao et al., 2014; Lehmann et al., 2010; Adamou et al., 2011; Yaro et al., 2012	Tatar et al., 2001
Environmental sensitivity of selection

Appendix 2—table 1

Measurements of mosquito demographic rates for major mosquito vector species.

Maximum population growth rates (r) were calculated using trait thermal responses from the references cited below and Equation S1 (Amarasekare and Savage, 2012). The temperature at which the maximum growth rate occurs, and the upper thermal limit for population growth (i.e., r = 0) are provided. The generation time is calculated as the sum of the immature development time, the gonotrophic period, and a minimum estimate of the host-blood meal and egg-laying time (4 days). We report the minimum generation time based on temperature.

Species	Max growth rate (r)	Max growth rate temperature	Upper thermal limit for growth rate	Minimum generation time (days)	Reference
Ae. aegypti	0.335	30.3°C	35.3°C	14	Mordecai et al., 2017
Anopheles spp.	0.187	26.2°C	31.6°C	17	Johnson et al., 2015
Cx. pipiens	0.379	28.1°C	34.6°C	17	Shocket et al., 2020

Appendix 3—table 1

Measurements of between-population variation in mosquito thermal tolerance.

‘Evidence of local thermal adaptation’ refers to measurements where populations from warmer source environments had higher thermal tolerance than those from cooler environments.

Species	Variation in source thermal environment	Thermal tolerance measurement	Evidence of local thermal adaptation?	Main finding	Reference
Cx. pipiens	~3°C in mean summer temperature	larval survival	no	Population from the coolest environment had the lowest survival at all temperatures	Ruybal et al., 2016
		adult survival	no	Population from the coolest environment had the lowest survival at cool temperatures, but highest survival at the warmest temperature
		development rate	no	Population from the warmest environment had the highest development rate at all temperatures
		biting rate	no	Population rank order varied with temperature
An. darlingi	~7, 6, 13°C in annual mean, min, and max temperature, respectively	adult lifespan	no	Population rank order varied with temperature	Chu et al., 2019
		larval development	no	Population from the highest minimum temperature environment developed faster at all temperatures
		wing length	no	Population from the coolest environment had the longest wing length at all temperatures
Cx. tarsalis	~5, 6, 15°C in mean daily, mean daily max, and max recorded temperature (in summer)	metabolic activity	yes	Critical thermal limits correlated positively with mean daily max temperature of source environment (but not with mean daily or max recorded temperature)	Vorhees et al., 2013
Cx. tarsalis	Unspecified. Populations reared from two sites in CA, USA	larval development rate	no	Minimal variation between populations	Dodson et al., 2012
		% larval survival	no	Variation in survival that was strongest at the high temperature extreme
		pupal development rate	no	Minimal variation between populations
		% pupal survival	no	Variation in survival that was strongest at the high temperature extreme
		wing length	no	No variation between populations
Cx. tarsalis	~3°C difference in annual mean temperature	immature development rate	no	Population from warmer environment developed more quickly at all temperatures	Reisen, 1995
		development rate	no	Population from warmer environment developed more quickly at all temperatures
		adult lifespan	no	Population from warmer environment had higher survival at intermediate, but not extreme temperatures
Cx. quinque-fasciastus	Unspecified. Populations reared from sites in New Zealand, Fiji, and Japan	larval development	no	No variation between populations	Mogi, 1992
		adult emergence rate	no	No variation between populations
		biting rate	no	Population rank order varied with temperature
		ovariole numbers	no	Population from the intermediate environment had the greatest number of ovarioles at all temperatures
		egg maturation	no	Minimal variation between populations

Appendix 3—table 2

Measurements of phenotypic plasticity in mosquito thermal tolerance, categorized as thermal acclimation, behavioral thermoregulation, and aestivation (see main text, ‘Phenotypic plasticity’).

Form	Species	Main finding	Reference
Thermal acclimation	Cx. pipiens	Critical thermal maxima increased 1°C when developed at 26°C versus 18°C	Gray, 2013
Thermal acclimation	An. arabiensis and An. funestus	Little variation in critical thermal maxima (typically increased by <2°C) after thermal acclimation	Lyons et al., 2012
Thermal acclimation	An. albimanus	Heat tolerance increased with warming developmental temperatures and with a prior heat shock exposure, but mosquitoes from all treatments died at 40–43°C	Benedict et al., 1991
Thermal acclimation	W. smithii	Larval and adult survival after heat shock increased ~0–30% in populations subjected to fluctuating hot/cold temperatures during development	Armbruster et al., 1999
Thermal acclimation	Ae. aegypti	Larvae pre-acclimated to warmer temperatures (37–39°C) survived longer at higher temperature extremes (43–45°C)	Sivan et al., 2021
Behavioral thermoregulation	Anopheles sp.	Observed seasonal shifts in feeding time, with biting occurring at dusk in cooler times of the year and late at night during warmer times	Reisen and Aslamkhan, 1978
Behavioral thermoregulation	An. darlingi	Observed correlation between time of year and crepuscular biting rates, and high within-population variation in biting time	Voorham, 2002
Behavioral thermoregulation	Ae. communis	Observed larvae resting in deeper, cooler waters when surface water temperatures became exceptionally high	Haufe and Burgess, 1956
Behavioral thermoregulation	Ae. aegypti, Ae. japonicus	Observed preference for 30°C when exposed to thermal gradient of 30–45°C in laboratory trials	Verhulst et al., 2020
Behavioral thermoregulation	An. stephensi	Observed preference for resting at ~26°C when exposed to thermal gradient of 14–38°C in laboratory trials	Blanford et al., 2009
Behavioral thermoregulation	Cx. fatigans	Observed avoidance of high temperatures when exposed to thermal gradient of 25–30°C in laboratory trials	Thomson, 1938
Aestivation	An. gambiae, An. coluzzii	Lower reproductive rates during the 3–6 month dry period were followed by rapidly rebounding population sizes after the first rain, suggesting persistence through aestivation	Yaro et al., 2012, Dao et al., 2014

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