Clock genes and environmental cues coordinate Anopheles pheromone synthesis, swarming, and mating

G. Wang, J. Vega-Rodríguez, A. Diabate, J. Liu, C. Cui, C. Nignan, L. Dong, F. Li, C. O. Ouedrago, A. M. Bandaogo, P. S. Sawadogo, H. Maiga, T. L. Alves e Silva, T. V. Pascini, S. Wang and M. Jacobs-Lorena,  Science,  371:411. 2021.

Several species of anopheline mosquitoes are important malaria vectors in Africa. Male mosquitoes show species-specific swarming behaviors at certain times of the day to attract females for mating. Wang et al. found that transcriptional patterns of metabolic and immune function genes apparently showed a diurnal rhythm that correlated with the physiological demands of mating flight swarming (see the Perspective by Manoukis). By altering temperature and light regimes and by knocking out the master genes period and timeless for circadian clock regulation, the authors disrupted mating flight behavior in a combination of cage experiments and enclosed field conditions. Knocking out the rhythmically expressed desaturase enzyme reduced cuticular hydrocarbon pheromone production and limited mating success. These key interacting components of the diurnal regulation of mosquito mating behavior are potential targets for alternative malaria control strategies.Science, this issue p. 411; see also p. 340Anopheles mating is initiated by the swarming of males at dusk followed by females flying into the swarm. Here, we show that mosquito swarming and mating are coordinately guided by clock genes, light, and temperature. Transcriptome analysis shows up-regulation of the clock genes period (per) and timeless (tim) in the head of field-caught swarming Anopheles coluzzii males. Knockdown of per and tim expression affects Anopheles gambiae s.s. and Anopheles stephensi male mating in the laboratory, and it reduces male An. coluzzii swarming and mating under semifield conditions. Light and temperature affect mosquito mating, possibly by modulating per and/or tim expression. Moreover, the desaturase gene desat1 is up-regulated and rhythmically expressed in the heads of swarming males and regulates the production of cuticular hydrocarbons, including heptacosane, which stimulates mating activity.

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