Elevated developmental temperatures below the lethal limit reduce Aedes aegypti fertility

Abstract

Aedes aegypti mosquitoes are the principal vectors of dengue and continue to pose a threat to human health, with ongoing urbanization, climate change and trade all impacting the distribution and abundance of this species. Hot periods are becoming increasingly common and their impacts on insect mortality have been well established, but they may have even greater impacts on insect fertility. In this study, we investigated the impacts of high temperatures on Ae. aegypti fertility both within and across generations. Mosquitoes developing under elevated temperatures exhibited higher critical thermal maxima (CTmax), reflecting developmental acclimation, but their fertility declined with increasing developmental temperature. In females, elevated developmental temperatures decreased fecundity while in males it tended to decrease the proportion of eggs that hatched and the proportion of individuals producing viable offspring. Rearing both sexes at 35°C increased fecundity in the subsequent generation but effects of elevated temperatures persisted across gonotrophic cycles within the same generation. Moreover, exposure of adults to 35°C further decreased fertility beyond the effects of developmental temperature alone. These findings highlight sub-lethal impacts of elevated temperatures on Ae. aegypti fertility and plastic responses to thermal stress within and across generations. This has significant implications for predicting the distribution and abundance of mosquito populations thriving in increasingly warmer environments.

Keywords: Acclimation; Fecundity; Heat stress; Mosquito; Thermal limit.

Fig. 1.

Experimental design. (A) In experiment 1, Aedes aegypti were reared under a range of temperatures to determine upper developmental lethal thermal limits for each life stage. (B) In experiments 2 and 3, Ae. aegypti were reared at a range of sub-lethal developmental temperatures and measured for their critical thermal maximum (CT_max; experiment 2) and fertility and reproductive success (experiment 3). (C) In experiment 4, each sex was reared at 26 or 35°C then crossed at 26°C to measure sex-specific effects on fertility and reproductive success. (D) In experiment 5, Ae. aegypti were reared at 26 or 35°C, then adults were maintained at both temperatures to measure combined effects of developmental and adult temperature on fertility and reproductive success. (E) In experiment 6, Ae. aegypti were reared at 26 or 35°C in the first generation then reared at both temperatures in the second generation to measure cross-generational effects of temperature on fertility and reproductive success across two gonotrophic cycles (GC1 and GC2).

Fig. 2.

Developmental lethal thermal limits of A. aegypti at constant temperatures. We measured the proportion of eggs (blue), larvae (green) and pupae (yellow) reaching the next life stage at a range of constant temperatures. Circles and error bars represent means and 95% confidence intervals based on 5–6 replicate batches of eggs for the proportion of eggs that hatched and 5 replicate trays of 50 larvae for larva to pupa and pupa to adult viability. Egg to adult viability (black) was estimated by multiplying the mean proportion of eggs that hatched by the proportion of larvae reaching adulthood at each temperature.

Fig. 3.

CT_max of A. aegypti females and males reared at sub-lethal elevated temperatures. Circles and error bars represent means and 95% confidence intervals for females (yellow) and males (blue). The n values represent the number of replicates measured per sex and temperature.

Fig. 4.

Fertility of A. aegypti reared at sub-lethal elevated temperatures. We measured (A) fecundity (number of eggs laid), (B) proportion of eggs that hatched and (C) total number of offspring when both sexes developed at elevated temperatures. Circles and error bars represent medians and 95% confidence intervals. The n values represent the number of replicates measured per treatment and trait. Different letters above plots indicate significant differences (P<0.05) between treatments according to Tukey's post hoc tests with a correction for multiple comparisons.

Fig. 5.

Fertility and reproductive success of A. aegypti females in crosses between males and females reared at 26 or 35°C. We measured (A) fecundity (number of eggs laid), (B) proportion of eggs that hatched and (C) total number of offspring. Solid vertical lines and error bars represent medians and 95% confidence intervals. Circles represent data for individual females. Different letters next to plots indicate significant differences (P<0.05) between treatments according to Tukey's post hoc tests with a correction for multiple comparisons, with capital letters for the binomial analysis of reproductive success and lowercase letters for the analysis of counts excluding zero values. The n values represent the number of replicates measured per treatment and trait.

Fig. 6.

Effects of elevated developmental and adult temperatures on A. aegypti fertility. We measured (A) fecundity (number of eggs laid), (B) proportion of eggs that hatched and (C) total number of offspring of mosquitoes reared at constant temperatures of 26 and 35°C until adult emergence then maintained at 26 or 35°C until laying eggs. Both sexes within a treatment were reared and maintained under the same conditions. Vertical lines and error bars represent medians and 95% confidence intervals. Circles represent data for individual females. Different letters next to plots indicate significant differences (P<0.05) between treatments according to Tukey's post hoc tests with a correction for multiple comparisons, with capital letters for the binomial analysis of reproductive success and lowercase letters for the analysis of counts excluding zero values. The n values represent the number of replicates measured per treatment and trait.

Fig. 7.

Cross-generational effects of elevated developmental temperatures on A. aegypti fertility persist across two gonotrophic cycles. We measured fertility in offspring reared at 26 or 35°C following rearing at 26 or 35°C in the parental generation. Both sexes within a treatment were reared at the same temperature. We measured (A,D) fecundity (number of eggs laid), (B,E) proportion of eggs that hatched and (C,F) total number of offspring across the (A–C) first and (D–F) second gonotrophic cycles. Vertical lines and error bars represent medians and 95% confidence intervals. Circles represent data for individual females. Different letters next to plots indicate significant differences (P<0.05) between treatments according to Tukey's post hoc tests with a correction for multiple comparisons, with capital letters for the binomial analysis of reproductive success and lowercase letters for the analysis of counts excluding zero values. The n values represent the number of replicates measured per treatment and trait.