Abstract

BackgroundGene families typically evolve by gene duplication followed by the adoption of new or altered gene functions. A different way to evolve new but related functions is alternative splicing of existing exons of a complex gene. The chemosensory gene families of animals are characterised by numerous loci of related function. Alternative splicing has only rarely been reported in chemosensory loci, for example in 5 out of around 120 loci in Drosophila melanogaster. The gustatory receptor gene Gr39a has four large exons that are alternatively spliced with three small conserved exons. Recently the genome sequences of eleven additional species of Drosophila have become available allowing us to examine variation in the structure of the Gr39a locus across a wide phylogenetic range of fly species.Methodology/Principal FindingsWe describe a fifth exon and show that the locus has a complex evolutionary history with several duplications, pseudogenisations and losses of exons. PAML analyses suggested that the whole gene has a history of purifying selection, although this was less strong in exons which underwent duplication.Conclusions/SignificanceEstimates of functional divergence between exons were similar in magnitude to functional divergence between duplicated genes, suggesting that exon divergence is broadly equivalent to gene duplication.

Highlights

  • Gustatory receptor (Gr) genes comprise a large fraction (,50%) of the Drosophila chemosensory receptor gene superfamily [1], encoding 7-transmembrane (7TM) proteins involved in taste and smell

  • E-mail: ag91@st-andrews.ac. uk Chemosensory receptor repertoires among different insects show great divergence, for instance only a few orthologous groups were identified when the complete olfactory and gustatory receptor repertoires of the fruit fly, honeybee and mosquito were compared [4,5,13]

  • Several structural changes have occurred to Gr39a, including the loss of exon C in D. willistoni and the species of Drosophila subgenus, and multiple duplications of exon A in D. pseudoobscura, Figure 4

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Summary

Introduction

Gustatory receptor (Gr) genes comprise a large fraction (,50%) of the Drosophila chemosensory receptor gene superfamily [1], encoding 7-transmembrane (7TM) proteins involved in taste and smell. Much of the diversity of the chemoreceptor family has evolved through widespread and repeated whole-gene duplications, followed by functional divergence of those duplicates that do not degrade to pseudogenes [2,3]. Another mechanism that enlarges the eukaryotic protein repertoire in general is alternative splicing. Analysis of the Gr repertoire in 12 Drosophila species allowed us to identify the orthologues of the Gr39a genes in these species [7] This locus showed an unusual pattern of structural changes compared with other Grs. Here we investigate in detail the evolution of the Gr39a gene using a comparative, bioinformatic approach. Estimates of functional divergence between exons were similar in magnitude to functional divergence between duplicated genes, suggesting that exon divergence is broadly equivalent to gene duplication

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