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Evol Appl. 2018 Mar 25;11(8):1245-1256. doi: 10.1111/eva.12619. eCollection 2018 Sep.

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

Author information

1
Institut des Sciences de l'Evolution de Montpellier (UMR 5554, CNRS-UM-IRD-EPHE) Université de Montpellier Montpellier France.
2
Disease Control and Elimination Department Medical Research Council, Unit The Gambia Banjul The Gambia.
3
Institut Régional de Santé Publique Université d'Abomey Calavi Cotonou Benin.
4
Faculté des Sciences et Techniques Laboratoire de Biologie et de Typage Moléculaire en Microbiologie Université d'Abomey Calavi Cotonou Bénin.
5
Institut Pierre Richet (IPR)/Institut National de Santé Publique (INSP) Bouaké Côte d'Ivoire.
6
Institut de Recherche pour le Développement (IRD) UMR MIVEGEC Montpellier France.

Abstract

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.

KEYWORDS:

adaptive trajectory; fitness cost; gene duplication; genome evolution; insecticide resistance; malaria vector

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