The evolutionary fate of heterogeneous gene duplications: A precarious overdominant equilibrium between environment, sublethality and complementation.

Milesi P, Assogba BS, Atyame CM, Pocquet N, Berthomieu A, Unal S, Makoundou P, Weill M, Labbé P

Mol. Ecol. 27 (2) 493-507 [2018-01-00; online 2017-12-29]

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.

Affiliated researcher

Pascal Milesi

PubMed 29230902

DOI 10.1111/mec.14463

Crossref 10.1111/mec.14463

GENBANK: KT002464
GENBANK: KT002468
GENBANK: JX007768
GENBANK: JX007770
GENBANK: JX007776
GENBANK: JX007778
GENBANK: JX007780
GENBANK: JX007782
GENBANK: JX007784
GENBANK: JX007786
GENBANK: JX007788
GENBANK: JX007790
GENBANK: KT002448
GENBANK: KT002449
GENBANK: KT002450
GENBANK: KT002451
GENBANK: KT002452
GENBANK: KT002455
GENBANK: KT002457
GENBANK: KT002462
GENBANK: KT002466
GENBANK: KT002467
GENBANK: JX007766
GENBANK: JX007772
GENBANK: JX007774
GENBANK: KT002447
GENBANK: KT002453
GENBANK: KT002454
GENBANK: KT002458
GENBANK: KT002459
GENBANK: KT002461


Publications 7.1.2