Transcriptional signatures of sexual selection, stress, and development in salmon lice (lepeophtheirus salmonis)

ABSTRACT\nThe salmon louse (Lepeophtheirus salmonis) is an important ectoparasitic copepod of wild and farmed salmon. Management of this parasite in Atlantic salmon aquaculture relies on chemicals administered as baths or in the feed. Unfortunately, multiple-drug resistance has now been reported in all major salmon producing countries, threatening the sustainability of the industry. The development of novel treatments for sea lice has been challenging due to a lack of functional studies and genomic characterization for this non-model species. These knowledge gaps have also impeded progress in finding markers to detect and monitor resistance in the field as part of drug management. In this thesis, a characterization of approximately 20,000 L. salmonis transcripts is described across studies monitoring physiological differences related to chemical exposure. Basal expression differences between sexes, populations, stages, and microsporidian infection are also integrated with these data to both characterize known phenotypes and explore novel responses. An accumulation of gene expression data from different projects described herein were also combined with previously published L. salmonis transcriptomic datasets to make cross-study comparisons and consensus-based gene annotation and characterization. \nMeta-analysis of male and female L. salmonis transcriptomes revealed important insights on sexual selection and its relationship with sexually dimporphic traits in lice. Markers were identified for both reproduction and the sexually dimorphic nature of drug resistance, immunity, mobility, and energy expenditure, among other traits. Additionally, male-biased genes appear to be evolving faster than female-biased or unbiased genes, potentially explaining sex differences related to drug resistance. The physiology of lice when exposed to two commonly used delousing drugs, cypermethrin and emamectin benzoate (EMB), was also assessed and characterized across baseline variables such as sex and population. The presence of a novel, vertically-transmitted microsporidian infection was also described in relation to EMB exposed lice, revealing sophisticated patterns of gene expression that included stress-specific genes, general stress genes, and genes that respond non-additively to stress. From a broader perspective, data from multiple studies was used to provide robust annotation of genes involved in stress, including 50 secretory and excretory protein (SEP) genes that respond concordantly to chemical exposures, microsporidian infection, and other environmental challenges such as hyposalinity. These genes are overexpressed in feeding lice compared to starved, and have annotations for digestion, host-immunomodulation, and antimicrobial effects. Other stress markers include heat shock proteins Hsp27 and Hsp70, which respond to stress generally, and could have important roles in future L. salmonis studies. Finally, the efficacy, ultrastructural impacts, and molecular responses of L. salmonis to the most recently licensed therapeutant, lufenuron, was described for the first time. Lufenuron is a chitin synthesis inhibitor and the first new louse drug on the market in nearly two decades. In this work, novel assays were designed to test the physiological responses of lice to this drug without using salmon hosts, and transcriptomic and metabolomic responses were integrated with observations from transmission electron microscopy to describe the failed molting process. Altogether, the work described in this dissertation represents the most comprehensive analysis of gene function in L. salmonis, offering new targets for parasite control, drug resistance monitoring, and stress detection for future work.

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