Adaptive introgression in an African malaria mosquito coincident with the increased usage of insecticide-treated bed nets

Laura C. Norris; Bradley J. Main; Yoosook Lee; Travis C. Collier; Abdrahamane Fofana; Anthony J. Cornel; Gregory C. Lanzaro

doi:10.1073/pnas.1418892112

Edited by Tilahun D. Yilma, University of California, Davis, CA, and approved December 2, 2014 (received for review October 6, 2014)

Significance

We report that during a recent period of hybridization between two major African malaria mosquitoes, Anopheles gambiae and Anopheles coluzzii, an island of divergence on chromosome 2 introgressed from the A. gambiae into the A. coluzzii genome and its frequency subsequently increased. This introgression was coincident with the start of a major insecticide-treated bed net campaigns in Mali. These observations suggest that increased insecticide exposure acted as a selective force sufficient to drive introgression of an entire genomic island of divergence across the reproductive barrier separating these two species. This study provides a rare example of adaptive introgression in an animal species and elucidates the dynamics of how insecticide resistance evolved in A. coluzzii.

Abstract

Animal species adapt to changes in their environment, including man-made changes such as the introduction of insecticides, through selection for advantageous genes already present in populations or newly arisen through mutation. A possible alternative mechanism is the acquisition of adaptive genes from related species via a process known as adaptive introgression. Differing levels of insecticide resistance between two African malaria vectors, Anopheles coluzzii and Anopheles gambiae, have been attributed to assortative mating between the two species. In a previous study, we reported two bouts of hybridization observed in the town of Selinkenyi, Mali in 2002 and 2006. These hybridization events did not appear to be directly associated with insecticide-resistance genes. We demonstrate that during a brief breakdown in assortative mating in 2006, A. coluzzii inherited the entire A. gambiae-associated 2L divergence island, which includes a suite of insecticide-resistance alleles. In this case, introgression was coincident with the start of a major insecticide-treated bed net distribution campaign in Mali. This suggests that insecticide exposure altered the fitness landscape, favoring the survival of A. coluzzii/A. gambiae hybrids, and provided selection pressure that swept the 2L divergence island through A. coluzzii populations in Mali. We propose that the work described herein presents a unique description of the temporal dynamics of adaptive introgression in an animal species and represents a mechanism for the rapid evolution of insecticide resistance in this important vector of human malaria in Africa.

Footnotes

↵¹To whom correspondence should be addressed. Email: gclanzaro{at}ucdavis.edu.

Author contributions: L.C.N., Y.L., and G.C.L. designed research; L.C.N., B.J.M., Y.L., A.F., and A.J.C. performed research; Y.L. contributed new reagents/analytic tools; L.C.N., B.J.M., Y.L., and T.C.C. analyzed data; and L.C.N., B.J.M., Y.L., T.C.C., A.J.C., and G.C.L. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
Data deposition: All karyotype and SNP data have been deposited in the PopI OpenProject “AgKDR” database (popi.ucdavis.edu/).
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1418892112/-/DCSupplemental.