How will mosquitoes adapt to climate warming?

  1. Lisa I Couper  Is a corresponding author
  2. Johannah E Farner
  3. Jamie M Caldwell
  4. Marissa L Childs
  5. Mallory J Harris
  6. Devin G Kirk
  7. Nicole Nova
  8. Marta Shocket
  9. Eloise B Skinner
  10. Lawrence H Uricchio
  11. Moises Exposito-Alonso
  12. Erin A Mordecai
  1. Department of Biology, Stanford University, United States
  2. Department of Biology, University of Hawaii at Manoa, United States
  3. Emmett Interdisciplinary Program in Environment and Resources, Stanford University, United States
  4. Department of Zoology, University of Toronto, Canada
  5. Department of Ecology and Evolutionary Biology, University of California Los Angeles, United States
  6. Environmental Futures Research Institute, Griffith University, Australia
  7. Department of Integrative Biology, University of California, Berkeley, United States
  8. Department of Plant Biology, Carnegie Institution for Science, United States
3 figures and 4 tables

Figures

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.

Case study on Ae. aegypti-transmitted dengue suitability.

Under current conditions, monthly dengue transmission suitability (i.e., R0(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
Population growth rate as a function of temperature for vector species listed in Appendix 2—table 1.

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 dataState of knowledge
Some data
Minimal or indirect data
No dataMosquitoesDrosophila
Generation timeMordecai et al., 2017Johnson et al., 2015; Shocket et al., 2020Crow and Chung, 1967; Lin et al., 2014; Fernández-Moreno et al., 2007; Ashburner, 1989; Emiljanowicz et al., 2014
Maximum population growth rateMordecai et al., 2017Johnson et al., 2015; Shocket et al., 2020; Amarasekare and Savage, 2012Siddiqui 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., 2010Hangartner and Hoffmann, 2016; ; Rashkovetsky et al., 2006; Lockwood et al., 2018
HeritabilityMitchell 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 selectionreviewed in Mordecai et al., 2019Rezende et al., 2020; Huey et al., 1991; Huey et al., 1992; Loeschcke and Hoffmann, 2007
Phenotypic plasticityAcclimationGray, 2013; Lyons et al., 2012; Benedict et al., 1991; Armbruster et al., 1999; Sivan et al., 2021MacLean et al., 2019; Hoffmann and Watson, 1993; Sgrò et al., 2010; Overgaard et al., 2011; Berrigan and Hoffmann, 1998
Behavioral thermo-regulationReisen and Aslamkhan, 1978; Voorham, 2002; Barrera et al., 2008; Haufe and Burgess, 1956; Verhulst et al., 2020; Blanford et al., 2013; Thomson, 1938Castañeda 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
DormancyDao et al., 2014; Lehmann et al., 2010; Adamou et al., 2011; Yaro et al., 2012Tatar 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.

SpeciesMax growth rate (r)Max growth rate temperatureUpper thermal limit for growth rateMinimum generation time (days)Reference
Ae. aegypti0.33530.3°C35.3°C14Mordecai et al., 2017
Anopheles spp.0.18726.2°C31.6°C17Johnson et al., 2015
Cx. pipiens0.37928.1°C34.6°C17Shocket 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.

SpeciesVariation in source thermal environmentThermal tolerance measurementEvidence of local thermal adaptation?Main findingReference
Cx. pipiens~3°C in mean summer temperaturelarval survivalnoPopulation from the coolest environment had the lowest survival at all temperaturesRuybal et al., 2016
adult survivalnoPopulation from the coolest environment had the lowest survival at cool temperatures, but highest survival at the warmest temperature
development ratenoPopulation from the warmest environment had the highest development rate at all temperatures
biting ratenoPopulation rank order varied with temperature
An. darlingi~7, 6, 13°C in annual mean, min, and max temperature, respectivelyadult lifespannoPopulation rank order varied with temperatureChu et al., 2019
larval developmentnoPopulation from the highest minimum temperature environment developed faster at all temperatures
wing lengthnoPopulation 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 activityyesCritical 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. tarsalisUnspecified. Populations reared from two sites in CA, USAlarval development ratenoMinimal variation between populationsDodson et al., 2012
% larval survivalnoVariation in survival that was strongest at the high temperature extreme
pupal development ratenoMinimal variation between populations
% pupal survivalnoVariation in survival that was strongest at the high temperature extreme
wing lengthnoNo variation between populations
Cx. tarsalis~3°C difference in annual mean temperatureimmature development ratenoPopulation from warmer environment developed more quickly at all temperaturesReisen, 1995
development ratenoPopulation from warmer environment developed more quickly at all temperatures
adult lifespannoPopulation from warmer environment had higher survival at intermediate, but not extreme temperatures
Cx. quinque-fasciastusUnspecified. Populations reared from sites in New Zealand, Fiji, and Japanlarval developmentnoNo variation between populationsMogi, 1992
adult emergence ratenoNo variation between populations
biting ratenoPopulation rank order varied with temperature
ovariole numbersnoPopulation from the intermediate environment had the greatest number of ovarioles at all temperatures
egg maturationnoMinimal 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’).
FormSpeciesMain findingReference
Thermal acclimationCx. pipiensCritical thermal maxima increased 1°C when developed at 26°C versus 18°CGray, 2013
Thermal acclimationAn. arabiensis and An. funestusLittle variation in critical thermal maxima (typically increased by <2°C) after thermal acclimationLyons et al., 2012
Thermal acclimationAn. albimanusHeat tolerance increased with warming developmental temperatures and with a prior heat shock exposure, but mosquitoes from all treatments died at 40–43°CBenedict et al., 1991
Thermal acclimationW. smithiiLarval and adult survival after heat shock increased ~0–30% in populations subjected to fluctuating hot/cold temperatures during developmentArmbruster et al., 1999
Thermal acclimationAe. aegyptiLarvae pre-acclimated to warmer temperatures (37–39°C) survived longer at higher temperature extremes (43–45°C)Sivan et al., 2021
Behavioral thermoregulationAnopheles sp.Observed seasonal shifts in feeding time, with biting occurring at dusk in cooler times of the year and late at night during warmer timesReisen and Aslamkhan, 1978
Behavioral thermoregulationAn. darlingiObserved correlation between time of year and crepuscular biting rates, and high within-population variation in biting timeVoorham, 2002
Behavioral thermoregulationAe. communisObserved larvae resting in deeper, cooler waters when surface water temperatures became exceptionally highHaufe and Burgess, 1956
Behavioral thermoregulationAe. aegypti, Ae. japonicusObserved preference for 30°C when exposed to thermal gradient of 30–45°C in laboratory trialsVerhulst et al., 2020
Behavioral thermoregulationAn. stephensiObserved preference for resting at ~26°C when exposed to thermal gradient of 14–38°C in laboratory trialsBlanford et al., 2009
Behavioral thermoregulationCx. fatigansObserved avoidance of high temperatures when exposed to thermal gradient of 25–30°C in laboratory trialsThomson, 1938
AestivationAn. gambiae, An. coluzziiLower reproductive rates during the 3–6 month dry period were followed by rapidly rebounding population sizes after the first rain, suggesting persistence through aestivationYaro et al., 2012, Dao et al., 2014

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  1. Lisa I Couper
  2. Johannah E Farner
  3. Jamie M Caldwell
  4. Marissa L Childs
  5. Mallory J Harris
  6. Devin G Kirk
  7. Nicole Nova
  8. Marta Shocket
  9. Eloise B Skinner
  10. Lawrence H Uricchio
  11. Moises Exposito-Alonso
  12. Erin A Mordecai
(2021)
How will mosquitoes adapt to climate warming?
eLife 10:e69630.
https://doi.org/10.7554/eLife.69630