Abstract
The origin and evolution of new microRNAs (miRNAs) is important because they can impact the transcriptome broadly. As miRNAs can potentially emerge constantly and rapidly, their rates of birth and evolution have been extensively debated. However, most new miRNAs identified appear not to be biologically significant. After an extensive search, we identified 12 new miRNAs that emerged de novo in Drosophila melanogaster in the last 4 million years (Myrs) and have been evolving adaptively. Unexpectedly, even though they are adaptively evolving at birth, more than 94% of such new miRNAs disappear over time. They provide selective advantages, but only for a transient evolutionary period. After 30 Myrs, all surviving miRNAs make the transition from the adaptive phase of rapid evolution to the conservative phase of slow evolution, apparently becoming integrated into the transcriptional network. During this transition, the expression shifts from being tissue-specific, predominantly in testes and larval brain/gonads/imaginal discs, to a broader distribution in many other tissues. Interestingly, a measurable fraction (20–30%) of these conservatively evolving miRNAs experience “evolutionary rejuvenation” and begin to evolve rapidly again. These rejuvenated miRNAs then start another cycle of adaptive – conservative evolution. In conclusion, the selective advantages driving evolution of miRNAs are themselves evolving, and sometimes changing direction, which highlights the regulatory roles of miRNAs.
Highlights
MicroRNAs are a class of small, endogenous RNAs that regulate gene expression post-transcriptionally [1,2]
We found most new adaptive miRNAs disappear over long periods of time; the miRNA repertoire stays close to that of a steady state
We sequenced five additional libraries from D. simulans and D.pseudoobscura to ensure that all Drosophila species in this survey included samples from testes and ovaries
Summary
MicroRNAs (miRNAs) are a class of small, endogenous RNAs that regulate gene expression post-transcriptionally [1,2]. Waddington [8,9], canalization contributes to developmental stability and, in a recent interpretation, it may contribute to evolvability via hidden genetic variations [10,11] Due to their small size, miR-producing hairpins can form readily and de novo emergence of miRNAs from non-miRNA transcripts is a frequent phenomenon [12,13]. There are hundreds of thousands of potential miRNA structures in each Drosophila genome [12] and millions in a mammalian genome [14] Given such a propensity for new miRNAs to emerge, the birth, death and adaptation of new miRNAs are a significant part of understanding the evolution of transcriptional regulation [12]. Local duplication or retrotransposition [15], rather than de novo origination, is the common mode for the formation of coding genes
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