Adaptive introgression between Anopheles sibling species eliminates a major genomic island but not reproductive isolation

Chris S. Clarkson (), David Weetman, John Essandoh, Alexander E. Yawson, Gareth Maslen, Magnus Manske, Stuart G. Field, Mark Webster, Tiago Antão, Bronwyn MacInnis, Dominic Kwiatkowski and Martin J. Donnelly
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Chris S. Clarkson: Liverpool School of Tropical Medicine, Pembroke Place
David Weetman: Liverpool School of Tropical Medicine, Pembroke Place
John Essandoh: Liverpool School of Tropical Medicine, Pembroke Place
Alexander E. Yawson: School of Biological Science, University of Cape Coast
Gareth Maslen: Malaria Programme, Wellcome Trust Sanger Institute, Hinxton
Magnus Manske: Malaria Programme, Wellcome Trust Sanger Institute, Hinxton
Stuart G. Field: Immunology and Pathology, Colorado State University, Fort Collins
Mark Webster: 18a Church Lane, Hornsey
Tiago Antão: Liverpool School of Tropical Medicine, Pembroke Place
Bronwyn MacInnis: Malaria Programme, Wellcome Trust Sanger Institute, Hinxton
Dominic Kwiatkowski: Malaria Programme, Wellcome Trust Sanger Institute, Hinxton
Martin J. Donnelly: Liverpool School of Tropical Medicine, Pembroke Place

Nature Communications, 2014, vol. 5, issue 1, 1-10

Abstract: Abstract Adaptive introgression can provide novel genetic variation to fuel rapid evolutionary responses, though it may be counterbalanced by potential for detrimental disruption of the recipient genomic background. We examine the extent and impact of recent introgression of a strongly selected insecticide-resistance mutation (Vgsc-1014F) located within one of two exceptionally large genomic islands of divergence separating the Anopheles gambiae species pair. Here we show that transfer of the Vgsc mutation results in homogenization of the entire genomic island region (~1.5% of the genome) between species. Despite this massive disruption, introgression is clearly adaptive with a dramatic rise in frequency of Vgsc-1014F and no discernable impact on subsequent reproductive isolation between species. Our results show (1) how resilience of genomes to massive introgression can permit rapid adaptive response to anthropogenic selection and (2) that even extreme prominence of genomic islands of divergence can be an unreliable indicator of importance in speciation.

Date: 2014
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DOI: 10.1038/ncomms5248

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