Assembling the Puzzle of an Enigmatic Shark Tapeworm: a Comparative Genomic and Transcriptomic Approach

The evolution of novelty among closely related taxa is a phenomenon that has occurred repeatedly within parasitic clades, however, the mechanisms that underlie the evolution of such innovations is not fully understood. This dissertation explores one example of this phenomenon that occurs in a monogeneric order of tapeworms, the Litobothriidea, that infect lamniform sharks. The most recently described member of this group, Litobothrium aenigmaticum, lacks all the characters typically demonstrated by members of this group, yet it robustly nests within the genus Litobothrium with the barcoding gene 28S rDNA (D1-D3). The aim of this dissertation was to investigate which mechanisms may have allowed for the bizarre morphology and anatomy of L. aenigmaticum. To do this, I first needed to better understand the differences between L. aenigmaticum and the typical litobothrrideans. Therefore, in chapter 1 I used transmission electron microscopy to characterize the internal anatomy of L. aenigmaticum. This work revealed that there are 11 novel cell types within the anterior region of the scolex of L. aenigmaticum, all of which contain secretory vesicles; nothing similar to this structure has been observed in any other cestode. With a more complete picture of the novelty of L. aenigmaticum, I next needed to generate the resources necessary to examine the mechanisms that led to the evolution of this species. In chapter 2 I assembled and annotated genomes for L. aenigmaticum, L. daileyi, and L. amplifica (338–406 Mb in size) and assembled transcriptomes for L. aenigmaticum, L. daileyi, and L. nickoli. Finally, in chapter 3 I used the genomic resources to perform a synteny and gene family evolution analysis and the transcriptomic resources to perform a differential expression analysis. These analyses revealed that gene family expansions and contractions, differential regulation of translation, up- and downregulation of specific transcripts, and coding region changes may underlie the novelty of L. aenigmaticum. In the future, I hope to broaden this study by also examining whether co-option and/or developmental changes may also be involved in this system