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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.

SUBMITTER: Clarkson CS

PROVIDER: S-EPMC4086683 | biostudies-literature | 2014 Jun

REPOSITORIES: biostudies-literature

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

Clarkson Chris S CS Weetman David D Essandoh John J Yawson Alexander E AE Maslen Gareth G Manske Magnus M Field Stuart G SG Webster Mark M Antão Tiago T MacInnis Bronwyn B Kwiatkowski Dominic D Donnelly Martin J MJ

Nature communications 20140625

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 mutati ...[more]

PMID: 24963649

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Project description:BackgroundThe sibling species of the malaria mosquito, Anopheles gambiae (sensu stricto) and Anopheles coluzzii co-exist in many parts of West Africa and are thought to have recently diverged through a process of ecological speciation with gene flow. Divergent larval ecological adaptations, resulting in Genotype-by-Environment (G × E) interactions, have been proposed as important drivers of speciation in these species. In West Africa, An. coluzzii tends to be associated with permanent man-made larval habitats such as irrigated rice fields, which are typically more eutrophic and mineral and ammonia-rich than the temporary rain pools exploited by An. gambiae (s.s.) METHODS: To highlight G × E interactions at the larval stage and their possible role in ecological speciation of these species, we first investigated the effect of exposure to ammonium hydroxide and water mineralisation on larval developmental success. Mosquito larvae were exposed to two water sources and increasing ammonia concentrations in small containers until adult emergence. In a second experiment, larval developmental success was compared across two contrasted microcosms to highlight G × E interactions under conditions such as those found in the natural environment.ResultsThe first experiment revealed significant G × E interactions in developmental success and phenotypic quality for both species in response to increasing ammonia concentrations and water mineralisation. The An. coluzzii strain outperformed the An. gambiae (s.s.) strain under limited conditions that were closer to more eutrophic habitats. The second experiment revealed divergent crisscrossing reaction norms in the developmental success of the sibling species in the two contrasted larval environments. As expected, An. coluzzii had higher emergence rates in the rice paddy environment with emerging adults of superior phenotypic quality compared to An. gambiae (s.s.), and vice versa, in the rain puddle environment.ConclusionsEvidence for such G × E interactions lends support to the hypothesis that divergent larval adaptations to the environmental conditions found in man-made habitats such as rice fields in An. coluzzii may have been an important driver of its ecological speciation.

Project description:BackgroundWhen integrated with insecticide-treated bed nets, larval control of Anopheles mosquitoes could fast-track reductions in the incidence of human malaria. However, larval control interventions may deliver suboptimal outcomes where the preferred breeding places of mosquito vectors are not well known. This study investigated the breeding habitat choices of Anopheles mosquitoes in southern Nigeria. The objective was to identify priority sites for mosquito larval management in selected urban and periurban locations where malaria remains a public health burden. METHODS: Mosquito larvae were collected in urban and periurban water bodies during the wet-dry season interface in Edo, Delta, and Anambra States. Field-collected larvae were identified based on PCR gel-electrophoresis and amplicon sequencing, while the associations between Anopheles larvae and the properties and locations of water bodies were assessed using a range of statistical methods.ResultsMosquito breeding sites were either man-made (72.09%) or natural (27.91%) and mostly drainages (48.84%) and puddles (25.58%). Anopheles larvae occurred in drainages, puddles, stream margins, and a concrete well, and were absent in drums, buckets, car tires, and a water-holding iron pan, all of which contained culicine larvae. Wild-caught Anopheles larvae comprised Anopheles coluzzii (80.51%), Anopheles gambiae sensu stricto (s.s.) (11.54%), and Anopheles arabiensis (7.95%); a species-specific PCR confirmed the absence of the invasive urban malaria vector Anopheles stephensi among field-collected larvae. Anopheles arabiensis, An. coluzzii, and An. gambiae s.s. displayed preferences for turbid, lowland, and partially sunlit water bodies, respectively. Furthermore, An. arabiensis preferred breeding sites located outside 500 m of households, whereas An. gambiae s.s. and An. coluzzii had increased detection odds in sites within 500 m of households. Anopheles gambiae s.s. and An. coluzzii were also more likely to be present in natural water bodies; meanwhile, 96.77% of An. arabiensis were in man-made water bodies. Intraspecific genetic variations were little in the dominant vector An. coluzzii, while breeding habitat choices of populations made no statistically significant contributions to these variations.ConclusionSibling malaria vectors in the An. gambiae complex display divergent preferences for aquatic breeding habitats in southern Nigeria. The findings are relevant for planning targeted larval control of An. coluzzii whose increasing evolutionary adaptations to urban ecologies are driving the proliferation of the mosquito, and An. arabiensis whose adults typically evade the effects of treated bed nets due to exophilic tendencies.

Dataset Information

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

Publications

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

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