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

Author

Listed:
  • 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
    School of Biological Science, University of Cape Coast)

  • Alexander E. Yawson

    (School of Biological Science, University of Cape Coast
    Biotechnology and Nuclear Agriculture Research Institute, Ghana Atomic Energy Commission, PO Box LG 80)

  • 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
    Wellcome Trust Centre for Human Genetics, University of Oxford)

  • Martin J. Donnelly

    (Liverpool School of Tropical Medicine, Pembroke Place
    Malaria Programme, Wellcome Trust Sanger Institute, Hinxton)

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.

Suggested Citation

  • 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 & Martin, 2014. "Adaptive introgression between Anopheles sibling species eliminates a major genomic island but not reproductive isolation," Nature Communications, Nature, vol. 5(1), pages 1-10, September.
    • Handle: RePEc:nat:natcom:v:5:y:2014:i:1:d:10.1038_ncomms5248
    DOI: 10.1038/ncomms5248
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    Cited by:

    1. Eric R. Lucas & Sanjay C. Nagi & Alexander Egyir-Yawson & John Essandoh & Samuel Dadzie & Joseph Chabi & Luc S. Djogbénou & Adandé A. Medjigbodo & Constant V. Edi & Guillaume K. Kétoh & Benjamin G. Ko, 2023. "Genome-wide association studies reveal novel loci associated with pyrethroid and organophosphate resistance in Anopheles gambiae and Anopheles coluzzii," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    2. Xiao Zhang & Mark Blaxter & Jonathan M. D. Wood & Alan Tracey & Shane McCarthy & Peter Thorpe & Jack G. Rayner & Shangzhe Zhang & Kirstin L. Sikkink & Susan L. Balenger & Nathan W. Bailey, 2024. "Temporal genomics in Hawaiian crickets reveals compensatory intragenomic coadaptation during adaptive evolution," Nature Communications, Nature, vol. 15(1), pages 1-19, December.

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