Extensive transcriptional differentiation and specialization of a single-host parasite aligns with niche turnover generated by its host's metamorphosis.

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Foundational theory on life cycle evolution suggests that given genetic independence, the phenotypes presented by different life stages will diverge more when they occupy more distinct niches. When divergence between stages is significant and punctual, we typically consider the life cycle complex. In parasites, the delineation between simple and complex life cycles is usually made between those that utilize single and multiple host species. However, many parasites can experience significant niche shifts in a single host. To explore the potential for a host's metamorphosis to shape divergence between stages across its parasite's life cycle, we quantified the transcriptional differentiation and specialization that the protozoan parasite Ophryocystis elektroscirrha exhibits across the metamorphosis of its host, the monarch butterfly. We found evidence that O. elektroscirrha differentiates in concordance with the ecological turnover imposed by monarch transitions to different stages, and that patterns of transcriptional decoupling across O. elektroscirrha exceeded even those of its host. However, due to its greater gene content, the monarch butterfly exhibited greater total transcriptional turnover than its parasite. These findings suggest that a deeper understanding of life cycle evolution for both free-living and parasitic lifestyles may be facilitated by more nuanced and continuous descriptions of life cycle complexity.