UCLA

One phenomenon that has perplexed biologists for decades is the lack of correlation between genome size and organismal complexity, aka the ‘C-value paradox’. It is now generally accepted that the paradox is caused by repetitive, non-coding sequences such as transposable elements. These ‘selfish’ or ‘parasitic’ sequences have profound impacts on the host genome. For instance, DNA methylation is thought to have originated as a defense mechanism against these genome parasites. As one of the most conserved epigenetic modifications in eukaryotes, DNA methylation plays important regulatory roles in animals. However, the evolution of transposable elements and DNA methylation have rarely been studied in non-bilaterian animals. This dissertation explores genome regulation in Cnidaria, the sister group of Bilateria, and its potential role in the evolution of complex life histories. Chapter 1 studies the distribution of DNA methylation across Cnidaria using published genomes and transcriptomes of over 70 species. By analyzing a proxy of DNA methylation, I show this epigenetic modification is prevalent in Cnidaria with instances of loss in a group of endoparasitic species. I also show cnidarian DNA methylation shares many similarities with bilaterian invertebrates, supporting the hypothesis that gene body methylation is the ancestral state in Eumetazoa. Additionally, cnidarians with complex life cycles tend to have heavier methylation, and both gene body methylation and repeat methylation increase with genome sizes. Chapter 2 examines DNA methylation patterns across the life history of a scyphozoan jellyfish, Aurelia coerulea, via stage-specific whole-genome bisulfite sequencing. This work characterizes the distribution of DNA methylation on the Aurelia genome, the correlation between methylation and expression levels, and highlights that sparsely-methylated genes tend to be expressed dynamically. Moreover, many genes are differentially methylated across life history stages; however, methylation changes do not predict expression changes. This study indicates that the regulatory role of gene body methylation lies more in stabilizing expression, a notion emerging as the primary function of DNA methylation in animals. Chapter 3 studies transposable elements (TEs) in the Aurelia genus. TEs in 12 species are annotated and quantified using whole genome sequencing. One clade shows signatures of ancient TE expansion events, indicating the TEs have undergone different evolutionary histories. Based on the phylogeny within the genus, these expansion events predate the closure of the isthmus of panama which separated the two clades of Aurelia. Additionally, the genome size difference between Aurelia aurita and Aurelia coerulea is unlikely due to activities of known TEs; however, Aurelia genomes harbor many unique TEs that would be worth further exploring. Overall, this dissertation research shows that Cnidaria is one of the most fascinating systems to study the evolution of genome regulation. As the first animals with real tissue layers, neuro-sensory systems, and a wide variety of different life histories, Cnidaria can shed light on how the genome ‘dark matter’ plays a role in the evolution of animal complexity.