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The evolutionary fate of heterogeneous gene duplications: A precarious overdominant equilibrium between environment, sublethality and complementation
Univ Montpellier, EPHE, CNRS, ISEM,IRD, Montpellier, France..
Univ Montpellier, EPHE, CNRS, ISEM,IRD, Montpellier, France.;MRC Unit, Dept Dis Control & Eliminat, Banjul, Gambia..
Univ Montpellier, EPHE, CNRS, ISEM,IRD, Montpellier, France.;Univ Reunion, CNRS, INSERM, UMR,PIMIT,IRD, St Clothilde, Ile De La Reuni, France..
Univ Montpellier, CNRS, MIVEGEC, UMR,IRD, Montpellier, France.;Inst Pasteur Nouvelle Caledonie, URE EM, Noumea, New Caledonia..
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2018 (English)In: Molecular Ecology, ISSN 0962-1083, E-ISSN 1365-294X, Vol. 27, no 2, p. 493-507Article in journal (Refereed) Published
Abstract [en]

Gene duplications occur at a high rate. Although most appear detrimental, some homogeneous duplications (identical gene copies) can be selected for beneficial increase in produced proteins. Heterogeneous duplications, which combine divergent alleles of a single locus, are seldom studied due to the paucity of empirical data. We investigated their role in an ongoing adaptive process at the ace-1 locus in Culex pipiens mosquitoes. We assessed the worldwide diversity of the ace-1 alleles (single-copy, susceptible S and insecticide-resistant R, and duplicated D that pair one S and one R copy), analysed their phylogeography and measured their fitness to understand their early dynamics using population genetics models. It provides a coherent and comprehensive evolutionary scenario. We show that D alleles are present in most resistant populations and display a higher diversity than R alleles (27 vs. 4). Most appear to result from independent unequal crossing-overs between local single-copy alleles, suggesting a recurrent process. Most duplicated alleles have a limited geographic distribution, probably resulting from their homozygous sublethality (HS phenotype). In addition, heterozygotes carrying different HS D alleles showed complementation, indicating different recessive lethal mutations. Due to mosaic insecticide control practices, balancing selection (overdominance) plays a key role in the early dynamics of heterogeneous duplicated alleles; it also favours a high local polymorphism of HS D alleles in natural populations (overdominance reinforced by complementation). Overall, our study shows that the evolutionary fate of heterogeneous duplications (and their long-term role) depends on finely balanced selective pressures due to the environment and to their genomic structure.

Place, publisher, year, edition, pages
2018. Vol. 27, no 2, p. 493-507
Keywords [en]
acetylcholinesterase, balancing selection, Culex pipiens, genome evolution, natural populations, overdominance, recurrent adaptation
National Category
Evolutionary Biology
Identifiers
URN: urn:nbn:se:uu:diva-351065DOI: 10.1111/mec.14463ISI: 000428069400013PubMedID: 29230902OAI: oai:DiVA.org:uu-351065DiVA, id: diva2:1209586
Available from: 2018-05-23 Created: 2018-05-23 Last updated: 2018-05-23Bibliographically approved

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Milesi, Pascal

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