The Deep Evolution of Metazoans and Metazoan Micrornas

microRNAs, ~22nt non-coding RNA regulatory genes, are key players in cellular differentiation and homeostasis. They might also play important roles in shaping metazoan macroevolution. Previous studies have shown that miRNAs are continuously being added to metazoan genomes through time, and once integrated into gene regulatory networks show only rare mutations to the primary sequence of the mature gene product and are only rarely secondarily lost. However, because the conclusions from all of these studies were based on phylogenetic conservation of miRNAs between model systems like Drosophila and vertebrates and the taxon of interest, it was unclear if these trends would describe most miRNAs in most metazoan phyla. Here, we explore the miRNA repertoires of ten different phyla by combining 454 sequencing of small RNA libraries with genomic searches from taxa whose divergence times are known from either the fossil record and/or a molecular clock. We show that the evolutionary trends elucidated from the model systems are generally true for all miRNA families and metazoan taxa explored: the continuous addition of miRNA families with only rare substitutions to the mature sequence and only rare instances of secondary losses. Further, we describe a novel miRNA type in demosponges that, although shows a different pre-miRNA structure, still shows the same evolutionary dynamics as eumetazoan miRNAs. We propose that miRNAs might be excellent phylogenetic markers, and suggest that the advent of morphological complexity might have its roots in miRNA innovation.