Cuticular hydrocarbons are associated with mating success and insecticide resistance in malaria vectors

Kelsey L Adams,Adam South,Simon P Sawadogo,Kristine Werling,Flaminia Catteruccia,W Robert Shaw,Roch K Dabiré,Abdoulaye Niang,Maurice A Itoe,Abdoulaye Diabaté,Charles Nignan,Douglas G Paton,Jennifer Wang

doi:10.1038/s42003-021-02434-1

Abstract

Anopheles coluzzii females, important malaria vectors in Africa, mate only once in their lifetime. Mating occurs in aerial swarms with a high male-to-female ratio, where traits underlying male mating success are largely unknown. Here, we investigated whether cuticular hydrocarbons (CHCs) influence mating success in natural mating swarms in Burkina Faso. As insecticides are widely used in this area for malaria control, we also determined whether CHCs affect insecticide resistance levels. We find that mated males have higher CHC abundance than unmated controls, suggesting CHCs could be determinants of mating success. Additionally, mated males have higher insecticide resistance under pyrethroid challenge, and we show a link between resistance intensity and CHC abundance. Taken together, our results suggest that CHC abundance may be subject to sexual selection in addition to selection by insecticide pressure. This has implications for insecticide resistance management, as these traits may be sustained in the population due to their benefits in mating even in the absence of insecticides.

Highlights

Anopheles coluzzii females, important malaria vectors in Africa, mate only once in their lifetime
Understanding whether cuticular hydrocarbons (CHCs) affect both mating biology and insecticide resistance (IR) is relevant in areas of Africa where widespread IR is threatening the efficacy of our best malaria control tools, which are predominantly based on the use of insecticides against vector species
We show that males that are successful in mating swarms have a higher abundance of CHCs, which could act as contact pheromones during interactions with females

Summary

Introduction

Important malaria vectors in Africa, mate only once in their lifetime. 1234567890():,; Two of the major malaria vectors in sub-Saharan Africa, Anopheles gambiae and Anopheles coluzzii of the A. gambiae complex, are largely monandrous, which means the lifetime reproductive fitness of females depends on a single mating event[1] In these anopheline species, mating occurs in aerial swarms where males heavily outnumber females. Biosynthesis occurs in specific cells called oenocytes, from where they are transported to the surface of the cuticle by lipophorin proteins, where they can regulate permeability in addition to playing pheromonal roles[21] These compounds are chemically diverse, and are thought to be highly tuned to environmental pressures such as aridity as well as subject to sexual selection, resulting in plasticity in their composition and levels[22]. Understanding whether CHCs affect both mating biology and IR is relevant in areas of Africa where widespread IR is threatening the efficacy of our best malaria control tools, which are predominantly based on the use of insecticides against vector species

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