Is Côte D'Ivoire a new high hybridization zone for the two major malaria vectors, Anopheles coluzzii and An. gambiae (Diptera, Culicidae)?

Beniamino Caputo,Verena Pichler,Zanakoungo Ibrahim Coulibaly,Andre Offianan,Alessandra Della Torre,Paola Serini,Chiara Virgillito,Naminata Tondossoma,Mattia Manica,Ibrahima Dia,Maria Calzetta,Maurice Akré

doi:10.1016/j.meegid.2022.105215

Abstract

Anopheles gambiae and An. coluzzii are very closely related and recently differentiated species representing the main malaria vectors in the Afrotropical region and responsible of up to >3 infective bites/person/night in Côte D'Ivoire, where prevention and control has stagnated in recent years. The aim of the present study was to genetically and ecologically characterize An. gambiae and An. coluzzii populations from two villages of Côte D'Ivoire, lying in the coastal forest belt and 250 km inland in the Guinean savannah mosaic belt, respectively. Results reveal high frequencies of both species in both study sites and high frequencies of hybrids (4-33%) along the whole year of sampling. Consistently with observations for the well-known high hybridization zone at the far-west of the species range, hybrid frequencies were higher in the coastal village and highest when the two species occurred at more balanced frequencies, supporting the "frequency-dependent hybridization" ecological speciation theory. Pilot genotyping revealed signatures of genomic admixture in both chromosome-X and -3. Coupled with previous reports of hybrids in the region, the results point to the coastal region of Côte D'Ivoire as a possible regions of high hybridization. Preliminary characterization of parameters relevant for malaria transmission and control (e.g. possibly higher sporozoite rates and indoor biting preferences in hybrids than in the parental species) highlight the possible relevance of the breakdown of reproductive barriers between An. gambiae and An. coluzzii not only in the field of ecological evolution, but also in malaria epidemiology and control.

Highlights

Malaria is a leading cause of morbidity and mortality in Cote D’Ivoire (PMI 2018-2019, 2019)
The total number of An. gambiae s.l. females collected in the inland village was 505, with an m/p/n ranging from 1.3 in October to 0.15 in March (GLMM-1, Table S0)
No significant differences were observed between the two villages (GLMM-3; Table S1, Fig. S1)

Summary

Introduction

Malaria is a leading cause of morbidity and mortality in Cote D’Ivoire (PMI 2018-2019, 2019). Among factors responsible of the high malaria burden in the region is the very efficient vectorial system accountable for up to >3 infective bites/person/night (PMI 2018-2019, 2019; PMI, 2020). This system is largely constituted by the two most synanthropic species of the An. gambiae complex (Diptera, Culicidae), i.e. An. coluzzii Coetzee & Wilkerson, 2013 and An. gambiae Giles, 1900. The latter strongly predominates in northern forestsavannahs and Sudanese savannahs, while An. coluzzii predominates in the south-western forested region (Edi et al, 2014). Extensive insecticide resistance is observed throughout the country, with pop ulations showing resistance to all 4 classes of insecticides (Oumbouke et al, 2020)

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