The evolution of courtship behaviors through the origination of a new gene in Drosophila

Abstract

New genes can originate by the combination of sequences from unrelated genes or their duplicates to form a chimeric structure. These chimeric genes often evolve rapidly, suggesting that they undergo adaptive evolution and may therefore be involved in novel phenotypes. Their functions, however, are rarely known. Here, we describe the phenotypic effects of a chimeric gene, sphinx, that has recently evolved in Drosophila melanogaster. We show that a knockout of this gene leads to increased male-male courtship in D. melanogaster, although it leaves other aspects of mating behavior unchanged. Comparative studies of courtship behavior in other closely related Drosophila species suggest that this mutant phenotype of male-male courtship is the ancestral condition because these related species show much higher levels of male-male courtship than D. melanogaster. D. melanogaster therefore seems to have evolved in its courtship behaviors by the recruitment of a new chimeric gene.chimeric gene ͉ gene duplication ͉ new functions ͉ phenotype evolution C omparative genomic analyses in various eukaryotes often reveal new genes that have evolved throughout the combination of unrelated genes or their duplicates (1-3). These new genes have usually evolved rapidly with a pattern of evolution that was shaped by positive Darwinian selection (4-6), suggesting that these chimeric genes have novel functions. Previous studies of molecular functions in new gene duplicates revealed the origination of important molecular functions in animals (6-8). A new gene becomes fixed in its initial stage in natural populations and subsequently evolves under various evolutionary forces (9). Understanding of this process requires the knowledge of the phenotypic effects of new gene duplicates because such effects are usually the targets of the positive selection that would determine the fate of the new gene duplicates. However, the phenotypes of these new genes are almost never known.In a survey of species-specific genes, we identified a courtship gene, sphinx, that originated and became fixed in a single species, Drosophila melanogaster, within the last 2-3 million years (mys) (10, 11). The sphinx gene was previously identified as a newly evolved chimeric gene (10, 11). The sphinx gene was formed by the insertion of a retroposed sequence of the ATP synthase F-chain gene (ATPS-F) from chromosome 2 into the 102F region of chromosome 4, recruiting sequences upstream to form a new exon and intron, a region we refer to as 102F-EI (10). Two alternative transcripts in adult males were detected from this locus (10). The sphinx gene appears to be functional because the gene contains only indel polymorphisms in the nonexonic sequences; it has a rate of evolution significantly above neutral expectations, suggesting rapid adaptive evolution; and it has a very specific pattern of expression (10). However, although it is derived, in part, from a protein-coding gene, it is most likely a noncoding RNA (ncRNA) because its parental-inherited coding regions are disrupted b...

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