Temperature extremes constrain climate-sensitive life traits and reveal genetic correlates of thermal tolerance in the malaria mosquito Anopheles coluzzii

Background Temperature shifts associated with climate change are reshaping mosquito distributions, fitness-related life-history traits and pathogen transmission potential. While moderate warming may enhance survival, development and reproduction, thermal extremes may constrain fitness and vectorial capacity. Predicting temperature effects on Anopheles population dynamics is essential for evidence-based vector control and malaria risk management in the future warmer world. Methods We investigated discrete, acute temperature exposures on survival and development of immature stages of the field-derived malaria mosquito Anopheles coluzzii. Eggs, larvae and pupae were exposed for 1 h to temperatures ranging from 0 to 43°C. Stage-specific egg hatching, larval mortality, pupation and adult emergence were assessed, together with carry-over effects of larval temperature exposure. Results Eggs were more heat- than cold-sensitive, with 23.60°C predicted as the optimum for hatching, a narrow 25–28°C window supporting hatching over time, and 38–39°C as the threshold beyond which hatching ceases. Larval survival was optimal at 24.6°C, with lowest mortality within 25–28°C. Larvae were also more heat- than cold-sensitive; mortality was 55% at 0°C, whereas no larvae survived 43°C. Larval thermal exposure reduced pupation from 85% in controls to 55% at 38°C and 45% at 0°C, with no pupation at 43°C. Adult emergence from exposed larvae declined from 85% in controls to 38% at 42°C. Stage-specific pupal mortality increased from 3% in controls to 52% at 0°C and 100% at 43°C, with 24.41°C predicted as the optimum for survival, and 25–28°C defining the best survivorship window. Emergence from exposed pupae declined from 97% in controls to 48% at 0°C and 60% at 42°C, with optimum of 24.19°C. Genotyping of extreme larval and pupal phenotypes (alive at 41°C vs dead at 38°C) revealed associations between heat tolerance and the 2L ^a chromosomal inversion polymorphism and the 1014F vgsc kdr mutation. Conclusion Beyond 42°C larval and pupal survival ceased, with thermal hierarchy of survival established as pupae > larvae > eggs. These findings demonstrate broad thermal breadth in this species and implicate 2L ^a and 1014F kdr mutation in heat tolerance, providing insight into mechanisms that may shape future population dynamics and malaria transmission risk.