Gene duplications: a role in adaptive evolution

Author(s): Labbé P, Milesi P, Weill M, Lenormand T

Summary:

Evolutionary potential is limited by the number and type of genes present, but how these limits shape the evolution of new functions remains a matter of debate. In this context, gene duplications are thought to be the main source of raw material for new evolutionary features: duplications are essentially envisioned as genomic substrates for long-term adaptation. Their early evolution is thus often neglected, notably how gene-dosage modifications affect fitness and condition their first steps. The evolution of insecticide resistance in the mosquito Culex pipiens is one of the few examples of contemporary duplications. Resistance represents a genetic adaptation to the environmental changes induced by insecticides, and as such, provides evolutionary biologists with a contemporary model for studying parameters that influence ongoing adaptation. The ace-1 gene encodes the acetylcholinesterase (AChE1), the target of organophosphate (OP) insecticides. A mutation in this gene causes high resistance levels in many mosquito species. However, a strong genetic constraint drives resistance evolution, as the degree of resistance and the ability to degrade ACh trade off. Recently, we identified in Cx. pipiens new ace-1 alleles that carry one susceptible and one resistant copy associated on the same chromosome. These different duplicated alleles show different dynamics in the field. We propose that duplications are selected to disentangle the two functions, i.e., by improving synapse signaling and mosquito’s fitness while maintaining resistance. I will present our recent work investigating 1) the duplication origin at the molecular level and 2) the complex gene-dosage/fitness relations and their impact in the field dynamics of these innovations. Our work stresses the role of duplications as immediate adaptive features, but shows that their fate is checked by natural selection early on: only those passing its short-term sieve can become seeds for future evolution.