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

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.

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

“…No other major introgressed regions were detected (SI Appendix, Fig. S3), in agreement with the results reported by Clarkson et al (19). Individual mosquito whole-genome sequencing revealed two recombinant individuals (samples 24 and 99) collected in 2012, both of which were r/r while reestablishing the A. coluzzii sequence in the first 2 Mb of chromosome 2L (Fig.…”

“…The most well-characterized animal examples include warfarin resistance in European house mice (36) and melanism in North American gray wolves (37). Adaptive introgression of an insecticide-resistance gene between A. gambiae and A. coluzzii has been reported in numerous papers (12,19,(38)(39)(40)(41). These examples suggest that reproductive barriers between animal species break down facilitating adaptation to changes in the environment.…”

Pollutants and insecticides drive local adaptation in African malaria mosquitoes

“…This selective sweep is characterized by a prominent depression of Tajima's D (1.5 Mb in width) and contains 80 genes including the pyrethroid knockdown resistance gene (kdr). Although it is difficult to precisely identify the specific gene that has been influenced by selection in this region, the voltage-gated sodium channel gene (kdr), which is a pervasive target of selection in Anopheles mosquitoes (Clarkson et al 2014;Norris et al 2015), represents the strongest candidate in our populations. Three mutations of the para-type sodium channel conferring knockdown resistance (1014F, 1014L, and 1014S) are widespread in Cameroon .…”

Genomic insights into adaptive divergence and speciation among malaria vectors of theAnopheles niligroup

“…These changeswhich involve local adaptation and genetic differentiation, introgressive hybridization, and selective sweeps across loci conferring resistance to xenobiotics-are particularly evident in the most anthropophilic species (Barnes et al, 2017;Clarkson et al, 2014;Norris et al, 2015).…”