Schmitz, JF and Chain, F and Bornberg-Bauer, E
Evolution of novel genes in three-spined stickleback populations
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Eukaryotic genomes frequently acquire new protein coding genes which may significantly impact anorganism’s fitness. Novel genes can be created, for example, by duplication of large genomic regionsorde novo, from previously non-coding DNA. Either way, creation of a novel transcript is an essentialearly step during novel gene emergence. Most studies on the gain-and-loss dynamics of novel genesso far have compared genomes between species, constraining analyses to genes that have remainedfixed over long time scales. However, the importance of novel genes for rapid adaptation amongpopulations has recently been shown. Therefore, since little is known about the evolutionary dynamicsof transcripts across natural populations, we here study transcriptomes from several tissues and ninegeographically distinct populations of an ecological model species, the three-spined stickleback. Ourfindings suggest that novel genes typically start out as transcripts with low expression and high tissuespecificity. Early expression regulation appears to be mediated by gene-body methylation. Althoughmost young and narrowly expressed genes are rapidly lost, those that survive and subsequently spreadthrough populations tend to gain broader and higher expression levels. Independent of their genomicorigin, the properties of the encoded proteins, such as disorder and aggregation propensity, hardlychange. Correspondingly, young novel genes are not preferentially under positive selection but oldernovel genes more often overlap with FSToutlier regions. Taken together, expression of the few survivingnovel genes is rapidly regulated, while structural properties of encoded proteins are non-debilitatingand might only change much later.