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How non-coding DNA gives rise to new protein-coding genes ( de novo  genes) is not well understood. Recent work has revealed the origins and functions of a few  de novo  genes, but common principles governing the evolution or biological roles of these genes are unknown. To better define these principles, we performed a parallel analysis of the evolution and function of six putatively protein-coding  de novo  genes described in  Drosophila melanogaster . Reconstruction of the transcriptional history of  de novo  genes shows that two  de novo  genes emerged from novel long non-coding RNAs that arose at least 5 MY prior to evolution of an open reading frame. In contrast, four other  de novo  genes evolved a translated open reading frame and transcription within the same evolutionary interval suggesting that nascent open reading frames (proto-ORFs), while not required, can contribute to the emergence of a new  de novo  gene. However, none of the genes arose from proto-ORFs that existed long before expression evolved. Sequence and structural evolution of  de novo  genes was rapid compared to nearby genes and the structural complexity of  de novo  genes steadily increases over evolutionary time. Despite the fact that these genes are transcribed at a higher level in males than females, and are most strongly expressed in testes, RNAi experiments show that most of these genes are essential in both sexes during metamorphosis. This lethality suggests that protein coding  de novo  genes in Drosophila quickly become functionally important.

De Novo ORFs in Drosophila Are Important to Organismal Fitness and Evolved Rapidly from Previously Non-coding Sequences