New insights into the dynamics of de novo gene origin

The evolution of genes de novo from ancestrally nongenic sequences is a significant mechanism of gene origin. Many studies have focused on distant evolutionary comparisons, which bias the sample of de novo genes towards older genes that have acquired important functions and have been refined by selection. In this report, we focus on the earliest steps in de novo gene origin by identifying young, polymorphic transcripts that may be missed by other study designs. To accomplish this, we sequenced tissue-specific transcriptomes from a much larger sample of genotypes than have been used in previous analyses of de novo genes in Drosophila melanogaster. We identified 90 potential species-specific de novo genes expressed in the male accessory glands of 29 D melanogaster lines derived from the same natural population. We find that most young, unannotated transcripts are both rare in the population and transcribed at low abundance. Improved sampling of both ingroup and outgroup genotypes reveals that many young genes are polymorphic in more than one species, resulting in substantial uncertainty about the age and phylogenetic distribution of de novo genes. Among the genes expressed in the same tissue, gene age correlates with proximity to other tissue-specific genes, with the youngest genes being least likely to occur near established tissue-specific genes. This and other lines of evidence suggest that de novo genes do not commonly evolve by simply reutilizing pre-existing regulatory elements. Together, these results provide new insights into the origin and early evolution of de novo genes. Author SummaryGenes may be born and lost without any lasting evidence of their existence. The typical longevity may be especially limited for de novo genes - that is, genes that originate from ancestrally non-genic, untranscribed sequences, since most genomic regions are not expected to be beneficial when transcribed. To better capture the population biology of nascent de novo genes at points close to their origin, we sequenced tissue-specific transcriptomes from a large number of Drosophila melanogaster genotypes. Most de novo genes were expressed in very few genotypes, consistent with the expectation of transience and rapid turnover. However, many young genes showed polymorphic transcription in multiple species, suggesting that the combination of low frequency with limited sampling can lead us to underestimate how long de novo genes persist in populations. We identified several features that de novo genes come to share with established tissue-specific genes the longer they persist. This study highlights important challenges in reconstructing de novo gene origin and helps elucidate why some transcripts may survive long enough to acquire selectable functions.