Forty Years of Erratic Insecticide Resistance Evolution in the Mosquito Culex pipiens

Labbé, Pierrick; Berticat, Claire; Berthomieu, Arnaud; Unal, Sandra; Bernard, Clothilde; Weill, Mylène; Lenormand, Thomas

doi:10.1371/journal.pgen.0030205

Cited by 139 publications

(150 citation statements)

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“…However, duplications are often costly, either through structural problems (breakpoints), hitch‐hiking deleterious mutations, metabolic overproduction costs, and/or due to the disruption of biochemical balances for the products of the duplicated genes (Kondrashov & Kondrashov, 2006; Labbé, Berticat et al., 2007; Milesi, Assogba et al., 2017). The chromosomal segment concerned by the duplication can indeed far exceed the gene of interest so that the resulting amplicons contain several other genes, as shown for example in Saccharomyces cerevisiae (Koszul, Caburet, Dujon, & Fischer, 2004), D. melanogaster (Remnant et al., 2013), and An.…”

Section: Introductionmentioning

confidence: 99%

Adaptive deletion in resistance gene duplications in the malaria vector Anopheles gambiae

Assogba

Alout

Koffi

et al. 2018

Evolutionary Applications

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While gene copy‐number variations play major roles in long‐term evolution, their early dynamics remains largely unknown. However, examples of their role in short‐term adaptation are accumulating: identical repetitions of a locus (homogeneous duplications) can provide a quantitative advantage, while the association of differing alleles (heterogeneous duplications) allows carrying two functions simultaneously. Such duplications often result from rearrangements of sometimes relatively large chromosome fragments, and even when adaptive, they can be associated with deleterious side effects that should, however, be reduced by subsequent evolution. Here, we took advantage of the unique model provided by the malaria mosquito Anopheles gambiae s.l. to investigate the early evolution of several duplications, heterogeneous and homogeneous, segregating in natural populations from West Africa. These duplications encompass ~200 kb and 11 genes, including the adaptive insecticide resistance ace‐1 locus. Through the survey of several populations from three countries over 3–4 years, we showed that an internal deletion of all coamplified genes except ace‐1 is currently spreading in West Africa and introgressing from An. gambiae s.s. to An. coluzzii. Both observations provide evidences of its selection, most likely due to reducing the gene‐dosage disturbances caused by the excessive copies of the nonadaptive genes. Our study thus provides a unique example of the early adaptive trajectory of duplications and underlines the role of the environmental conditions (insecticide treatment practices and species ecology). It also emphasizes the striking diversity of adaptive responses in these mosquitoes and reveals a worrisome process of resistance/cost trade‐off evolution that could impact the control of malaria vectors in Africa.

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Section: Introductionmentioning

confidence: 99%

Adaptive deletion in resistance gene duplications in the malaria vector Anopheles gambiae

Assogba

Alout

Koffi

et al. 2018

Evolutionary Applications

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“…While the majority of duplicated genes are not retained, undergo pseudogenation, or exhibit distinct negative effects (Lynch and Conery, 2000;Demuth and Hahn, 2009;Tang and Amon, 2013), gene duplication has facilitated evolution in diverse organisms (Kondrashov et al, 2002;Conant and Wolfe, 2008). For one of the simplest types of copy number variation, gene duplication, a wide range of resulting adaptations to changing local environmental conditions has been characterized (Triglia et al, 1991;Labbé et al, 2007;Schmidt et al, 2010;Dassanayake et al, 2011;Heinberg et al, 2013; for review, see Kondrashov, 2012). Single gene copy number amplification has also been observed as an adaptive response to selective pressures (Bass and Field, 2011).…”

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Distinct Copy Number, Coding Sequence, and Locus Methylation Patterns UnderlieRhg1-Mediated Soybean Resistance to Soybean Cyst Nematode

Cook¹,

Bayless²,

et al. 2014

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Copy number variation of kilobase-scale genomic DNA segments, beyond presence/absence polymorphisms, can be an important driver of adaptive traits. Resistance to Heterodera glycines (Rhg1) is a widely utilized quantitative trait locus that makes the strongest known contribution to resistance against soybean cyst nematode (SCN), Heterodera glycines, the most damaging pathogen of soybean (Glycine max). Rhg1 was recently discovered to be a complex locus at which resistance-conferring haplotypes carry up to 10 tandem repeat copies of a 31-kb DNA segment, and three disparate genes present on each repeat contribute to SCN resistance. Here, we use whole-genome sequencing, fiber-FISH (fluorescence in situ hybridization), and other methods to discover the genetic variation at Rhg1 across 41 diverse soybean accessions. Based on copy number variation, transcript abundance, nucleic acid polymorphisms, and differentially methylated DNA regions, we find that SCN resistance is associated with multicopy Rhg1 haplotypes that form two distinct groups. The tested high-copy-number Rhg1 accessions, including plant introduction (PI) 88788, contain a flexible number of copies (seven to 10) of the 31-kb Rhg1 repeat. The identified low-copy-number Rhg1 group, including PI 548402 (Peking) and PI 437654, contains three copies of the Rhg1 repeat and a newly identified allele of Glyma18g02590 (a predicted α-SNAP [α-soluble N-ethylmaleimide–sensitive factor attachment protein]). There is strong evidence for a shared origin of the two resistance-conferring multicopy Rhg1 groups and subsequent independent evolution. Differentially methylated DNA regions also were identified within Rhg1 that correlate with SCN resistance. These data provide insights into copy number variation of multigene segments, using as the example a disease resistance trait of high economic importance.

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“…gambiae. However, insecticide resistance is a rapidly evolving trait (13,14) and, particularly in large populations, new mutations can arise frequently (15).…”

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confidence: 99%

Footprints of positive selection associated with a mutation ( N1575Y ) in the voltage-gated sodium channel of Anopheles gambiae

Jones

Liyanapathirana²,

Agossa³

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

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Insecticide resistance is an ideal model to study the emergence and spread of adaptative variants. In the African malaria mosquito, Anopheles gambiae, this is complemented by a strong public health rationale. In this insect, resistance to pyrethroid and DDT insecticides is strongly associated with the mutations L1014F and L1014S within the para voltage-gated sodium channel (VGSC). Across much of West Africa, 1014F frequency approaches fixation. Here, we document the emergence of a mutation, N1575Y, within the linker between domains III-IV of the VGSC. In data extending over 40 kbp of the VGSC 1575Y occurs on only a single long-range haplotype, also bearing 1014F. The 1014F-1575Y haplotype was found in both M and S molecular forms of An. gambiae in West/ Central African sample sites separated by up to 2,000 km. In Burkina Faso M form, 1575Y allele frequency rose significantly from 0.053 to 0.172 between 2008 and 2010. Extended haplotype homozygosity analysis of the wild-type 1575N allele showed rapid decay of linkage disequilibrium (LD), in sharp contrast to the extended LD exhibited by 1575Y. A haplotype with long-range LD and high/increasing frequency is a classical sign of strong positive selection acting on a recent mutant. 1575Y occurs ubiquitously on a 1014F haplotypic background, suggesting that the N1575Y mutation compensates for deleterious fitness effects of 1014F and/or confers additional resistance to insecticides. Haplotypic tests of association suggest the latter: The 1014F-1575Y haplotype confers a significant additive benefit above 1014F-1575N for survival to DDT (M form P = 0.03) and permethrin (S form P = 0.003).kdr | selective sweep | inactivation particle

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Forty Years of Erratic Insecticide Resistance Evolution in the Mosquito Culex pipiens

Cited by 139 publications

References 45 publications

Adaptive deletion in resistance gene duplications in the malaria vector Anopheles gambiae

Adaptive deletion in resistance gene duplications in the malaria vector Anopheles gambiae

Distinct Copy Number, Coding Sequence, and Locus Methylation Patterns UnderlieRhg1-Mediated Soybean Resistance to Soybean Cyst Nematode

Footprints of positive selection associated with a mutation ( N1575Y ) in the voltage-gated sodium channel of Anopheles gambiae

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