| The evolutionary history of animals covers a broad spectrum of body plans and morphological complexity. There are two periods in evolutionary history marked by major transitions in morphology, first at the base of "Bilateria" ∼670 mya, and second, at the base of Vertebrata ∼500 mya when several characters were gained such as the neural crest. The causal bases for these changes have been sought in the genome. Whole genome duplication events (GDE), gene family expansions, and gene regulatory innovations have been shown to coincide with changes in animal complexity. MicroRNAs (miRNAs) are a viable causal factor in increasing organismal complexity by regulating gene expression. The two periods in animal history marked by an increase in complexity, "Bilateria" and Vertebrata, are also marked by major expansions of the microRNA gene repertoire. By surveying the microRNA complement of animals across Metazoa we have identified three characteristics of microRNA gene evolution, 1. miRNAs are continuously being added to the animalian genomes, 2. Once integrated into a gene regulatory network, they are strongly conserved in primary sequence and 3. They are rarely secondarily lost. These qualities make microRNAs excellent phylogenetic markers as well. We show that vertebrates evolved 46 new miRNA families with shared organ expression profiles between lamprey, hagfish and gnathostomes, suggesting these genes as potential drivers of vertebrate innovations. As well, the microRNA repertoire of these three taxa resolved the phylogenetic relationship of Cyclostomata as monophyletic. The genomic position of miRNA paralogues in humans, together with gene trees incorporating lamprey orthologues, indicates that GDEs cannot account for the origin of these novel families themselves. We hypothesize that lying behind the origin of animal complexity is the expansion of the noncoding RNA inventory including miRNAs. |
