Résumé
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), analyzed 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
heterogeneous duplicated alleles; it also favors 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.