Gene expression profiling across the three-host life cycle of <i>Schistocephalus solidus</i> : how decoupled are the life stages?

Parasites with complex life cycles infect multiple hosts, adapting to different ecological niches using a single genome. The adaptive decoupling hypothesis suggests that different life stages should be genetically independent, meaning selection in one life stage does not affect traits in another. We tested this hypothesis using the tapeworm Schistocephalus solidus. Transcriptome sequencing was performed from all life phases, representing the entire life cycle of the parasite, such that differential gene expression could be examined between hosts (e.g., first vs. second intermediate host) as well as functionally equivalent phases across hosts (e.g., transmission vs. growth). Gene set enrichment analysis assessed whether similar biological functions in different hosts relied on common genes.Our findings show that the strongest correlation was observed in consecutive phases. Instead, in the rest of the life cycle, gene expression in each phase is distinct, with no positive correlation between functionally similar stages or those in the same host. When genes are upregulated in one stage, they are downregulated or not differentially expressed in others, even within the same host or when performing similar tasks. When some gene ontology terms matched in functionally similar stages, they were encoded by different genes, which uncovers another layer of decoupling: same biological processes but different gene sets used.These results support the decoupling hypothesis in parasitic worms, demonstrating that complex life cycles are maintained through stage-specific gene regulation rather than shared functional gene expression. This provides insights into the mechanisms leading to multi-host life cycles.