Acetylcholinesterase genes within the Diptera: takeover and loss in true flies

Author:

Huchard Elise1,Martinez Michel2,Alout Haoues1,Douzery Emmanuel J.P1,Lutfalla Georges3,Berthomieu Arnaud1,Berticat Claire1,Raymond Michel1,Weill Mylène1

Affiliation:

1. Institut des Sciences de l'Evolution (UMR 5554 CNRS), C.C. 065, Université de Montpellier II34095 Montpellier cedex 5, France

2. INRA, Unité d'Ecologie animale et Zoologie agricole2, place Pierre Viala, 34060 Montpellier Cedex 01, France

3. UMR 5124 CNRS, C.C.86, Université de Montpellier II34095 Montpellier cedex 5, France

Abstract

It has recently been reported that the synaptic acetylcholinesterase (AChE) in mosquitoes is encoded by theace-1gene, distinct and divergent from theace-2gene, which performs this function inDrosophila. This is an unprecedented situation within the Diptera order because bothacegenes derive from an old duplication and are present in most insects and arthropods. Nevertheless,Drosophilapossesses only theace-2gene. Thus, a secondary loss occurred during the evolution of Diptera, implying a vital function switch from one gene (ace-1) to the other (ace-2). We sampled 78 species, representing 50 families (27% of the Dipteran families) spread over all major subdivisions of the Diptera, and looked forace-1andace-2by systematic PCR screening to determine which taxonomic groups within the Diptera have this gene change. We show that this loss probably extends to all true flies (or Cyclorrhapha), a large monophyletic group of the Diptera. We also show thatace-2plays a non-detectable role in the synaptic AChE in a lower Diptera species, suggesting that it has non-synaptic functions. A relative molecular evolution rate test showed that the intensity of purifying selection onace-2sequences is constant across the Diptera, irrespective of the presence or absence oface-1, confirming the evolutionary importance of non-synaptic functions for this gene. We discuss the evolutionary scenarios for the takeover oface-2and the loss oface-1, taking into account our limited knowledge of non-synaptic functions ofacegenes and some specific adaptations of true flies.

Publisher

The Royal Society

Subject

General Agricultural and Biological Sciences,General Environmental Science,General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine

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