Genomic signatures of population decline in the malaria mosquito Anopheles gambiae.

Samantha M O’Loughlin,Austin Burt,Janet Midega,Stephen M Magesa,Franklin Mosha,Charles Mbogo

doi:10.1186/s12936-016-1214-9

Abstract

BackgroundPopulation genomic features such as nucleotide diversity and linkage disequilibrium are expected to be strongly shaped by changes in population size, and might therefore be useful for monitoring the success of a control campaign. In the Kilifi district of Kenya, there has been a marked decline in the abundance of the malaria vector Anopheles gambiae subsequent to the rollout of insecticide-treated bed nets.MethodsTo investigate whether this decline left a detectable population genomic signature, simulations were performed to compare the effect of population crashes on nucleotide diversity, Tajima’s D, and linkage disequilibrium (as measured by the population recombination parameter ρ). Linkage disequilibrium and ρ were estimated for An. gambiae from Kilifi, and compared them to values for Anopheles arabiensis and Anopheles merus at the same location, and for An. gambiae in a location 200 km from Kilifi.ResultsIn the first simulations ρ changed more rapidly after a population crash than the other statistics, and therefore is a more sensitive indicator of recent population decline. In the empirical data, linkage disequilibrium extends 100–1000 times further, and ρ is 100–1000 times smaller, for the Kilifi population of An. gambiae than for any of the other populations. There were also significant runs of homozygosity in many of the individual An. gambiae mosquitoes from Kilifi.ConclusionsThese results support the hypothesis that the recent decline in An. gambiae was driven by the rollout of bed nets. Measuring population genomic parameters in a small sample of individuals before, during and after vector or pest control may be a valuable method of tracking the effectiveness of interventions.Electronic supplementary materialThe online version of this article (doi:10.1186/s12936-016-1214-9) contains supplementary material, which is available to authorized users.

Highlights

Population genomic features such as nucleotide diversity and linkage disequilibrium are expected to be strongly shaped by changes in population size, and might be useful for monitoring the success of a control campaign
Strong population decline a long time in the past gave too few segregating sites for analyses, so some curves are truncated
Population declines lead to reductions in π, θW and ρ, and increases in Tajima’s D, with larger reductions in population size producing larger and more rapid effects on the population genomic statistics. (Simulating reductions even further in the past than 10,000 generations resulted in Tajimas’s D returning towards zero; this reflects the fact that the population has remained small but stable for a long enough time equilibrium to be restored.) Importantly, for all scenarios, ρ responded faster and/or by a larger relative amount than the other three statistics, suggesting it can be a more sensitive measure of population control

Summary

Introduction

Population genomic features such as nucleotide diversity and linkage disequilibrium are expected to be strongly shaped by changes in population size, and might be useful for monitoring the success of a control campaign. In many parts of Africa there have been concerted efforts to control malaria transmission by controlling the mosquito vector using insecticide treated bed nets (ITNs) and indoor residual spraying (IRS). In some places these efforts have been successful, resulting in substantial reductions in the numbers of Anopheles gambiae (the most important vector species in sub-Saharan Africa)

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