Evolutionary patterns and ecological influences of venom function in Medusozoa (phylum Cnidaria)

Klompen, Anna Marie Louisa

Publication

Evolutionary patterns and ecological influences of venom function in Medusozoa (phylum Cnidaria)

Klompen, Anna Marie Louisa

Abstract

In my dissertation research, I have utilized molecular and computational approaches (e.g. phylogenetics, transcriptomics, molecular evolution), as well as transgenic approaches to study the evolution of toxins and their ecological role within medusozoan venoms. The clade Medusozoa includes the jellyfish-bearing lineages of the phylum Cnidaria, animals characterized by possession of specialized secretory products called cnidae that are housed in !stinging cells”or cnidocytes. The most ubiquitous of these cnidae types are called nematocysts, which contain a complex mixture of toxins known collectively as venom. In cnidarians, venom is deployed primarily (but not exclusively) for predation and defense. This dissertation research aims to explore how medusozoan venom systems respond to diverse ecological interactions within the context of complex life history traits. In Chapter 1, I presented a brief introduction to medusozoan venom systems and toxinology. Currently, little is known about how the composition and ecological role of medusozoan venoms may be altered across complex life history traits, such as division of labor within a colonial species. For example, within the hydrozoan Hydractinia symbiolongicarpus, the colony displays several morphologically and functionally distinct polyp types: feeding polyps (gastrozooids), reproductive polyps (gonozooids), and defensive/foraging polyps (dactylozooids). In Chapter 2, I established a nematocyst-specific transgenic line for H. symbiolongicarpus and integrate FACS, RNA-Seq, and differential expression analyses to show that the colony partitions nematocyst types and putative venom genes across the functionally-specialized polyps types. Within these differentially expressed venom gene candidates I found several putative !jellyfish toxins” (JFTs), which are dominant components in the venoms of box jellyfish (class Cubozoa) and known to be highly toxic to humans. In Chapter 3, I used phylogenetic and selection analyses to explore the evolutionary trajectory of JFTs across medusozoans, including relatively weaker stingers in the classes Hydrozoa (e.g. Hydractinia) and Scyphozoa. I found evidence of duplication followed by gene-wide episodic positive selection in the clade of JFTs derived from box jellyfish when compared to other clades, suggesting that the high potency of JFTs in cubozoan venoms has been a functional change driven by a combination of duplication and a change in selective pressure, possibly associated with a dietary switch to vertebrate prey. A survey of differential expression studies showed that JFTs are often upregulated in either developing or mature medusae or in tissues responsible for prey-capture, as in H. symbiolongicarpus. In Chapter 4, I documented the spatial expression patterns of H. symbiolongicarpus JFTs within the colony, and used these patterns to explore how partitioning of venoms occurs across functionally-distinct polyps and nematocyst types. Using localization techniques at both the level of RNA (in-situ hybridization) and protein (immunohistochemistry), in addition to my previously established transgenic line, I showed that partitioning of JFTs in H. symbiolongicarpus is both a product of modulating nematogenesis and nematocyst-type specific expression across tissues.