Ecological plasticity to ions concentration determines genetic response and dominance of Anopheles coluzzii larvae in urban coastal habitats of Central Africa

Neil M Longo-Pendy,Nicolas Berthet,Carlo Costantini,Robert E Tawedi,Jean-Jacques Braun,Ousman Akone-Ella,Nil Rahola,Celine Toty,Diego Ayala,Pierre Kengne,Billy Tene-Fossog

doi:10.1038/s41598-021-94258-6

Abstract

In Central Africa, the malaria vector Anopheles coluzzii is predominant in urban and coastal habitats. However, little is known about the environmental factors that may be involved in this process. Here, we performed an analysis of 28 physicochemical characteristics of 59 breeding sites across 5 urban and rural sites in coastal areas of Central Africa. We then modelled the relative frequency of An. coluzzii larvae to these physicochemical parameters in order to investigate environmental patterns. Then, we assessed the expression variation of 10 candidate genes in An. coluzzii, previously incriminated with insecticide resistance and osmoregulation in urban settings. Our results confirmed the ecological plasticity of An. coluzzii larvae to breed in a large range of aquatic conditions and its predominance in breeding sites rich in ions. Gene expression patterns were comparable between urban and rural habitats, suggesting a broad response to ions concentrations of whatever origin. Altogether, An. coluzzii exhibits a plastic response to occupy both coastal and urban habitats. This entails important consequences for malaria control in the context of the rapid urban expansion in Africa in the coming years.

Highlights

In Africa, where the urbanization rate is among the fastest in the world[14], malaria mosquitoes have been historically confined to rural areas because Anopheles larval development is strongly hindered in polluted w ater[11,15]
Anopheles coluzzii is the predominant mosquito in cities of Central Africa[20,22,33,34,35], whereas Anopheles arabiensis has been recorded in the cities of the West Africa[36,37,38]
Antonio-Nkondjio and co-workers reported the association between An. coluzzii larvae presence in polluted sites and resistance to insecticides of adults in the cities of Yaoundé and D ouala[46], leading to the hypothesis that anthropogenic pressures have conditioned the evolution of this main malaria v ector[51]

Summary

Introduction

In Africa, where the urbanization rate is among the fastest in the world[14], malaria mosquitoes have been historically confined to rural areas because Anopheles larval development is strongly hindered in polluted w ater[11,15]. Cassone et al, investigated the genetic basis of the presence of An. coluzzii in urban settings by transcriptomic analysis of larvae breeding in polluted sites of the city of Yaoundé (Cameroon)[50]. They found that genes related to oxidative stress and detoxification were upregulated in those larvae. Transcriptomic analysis of ten candidate’s genes involved in detoxification and osmoregulation revealed comparable levels across breeding sites analyzed, suggesting a common genetic response against different ions presence These results show the ability of An. coluzzii to colonize a broad number of aquatic conditions, with direct consequences for malaria control in urban settings

Methods

Results

Discussion

Conclusion