Extensive transcriptional differentiation and specialization of a parasite across its host's metamorphosis

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 dissimilar 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 occupy single and multiple host species. However, many parasites can experience significant niche shifts in a single host. To explore the potential for a hosts metamorphosis to shape divergence between stages across its parasites 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 the O. elektroscirrha exceeded even that of its host. However, because of its greater gene content, the monarch exhibited greater total transcriptional turnover than its parasite. These findings highlight that synthesis of evolutionary theory pertaining to free-living and parasitic life cycles could be facilitated by more nuanced and continuous descriptions of life cycle complexity.