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Parasitism is a common life strategy throughout the eukaryotic tree of life. Many devastating human pathogens, including the causative agents of malaria and toxoplasmosis, have evolved from a photosynthetic ancestor. However, how an organism transitions from a photosynthetic to a parasitic life history strategy remains mostly unknown. This is largely because few systems present the opportunity to make meaningful comparisons between a parasite and a close free-living relative. Parasites have independently evolved dozens of times throughout the Florideophyceae (Rhodophyta), and often infect close relatives. The accepted evolutionary paradigm proposes that red algal parasites arise by first infecting a close relative and over time diversify and infect more distantly related species. This provides a natural evolutionary gradient of relationships between hosts and parasites that share a photosynthetic common ancestor. Elegant microscopic work in the late 20th century provided detailed insight into the infection cycle of red algal parasites and the cellular interactions between parasites and their hosts. Those studies led to the use of molecular work to further investigate the origins of the parasite organelles and reveal the evolutionary relationships between hosts and their parasites. Here we synthesize the research detailing the infection methods and cellular interactions between red algal parasites and their hosts. We offer an alternative hypothesis to the current dogma of red algal parasite evolution and propose that red algae can adopt a parasitic life strategy through multiple evolutionary pathways, including direct infection of distant relatives. Furthermore, we highlight potential directions for future research to further evaluate parasite evolution in red algae.

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