Phylogenomics shows that novel tapeworm-like traits of haplozoan parasites evolved from within the Peridiniales (Dinoflagellata)

Abstract

Haplozoans are intestinal parasites of marine annelids with bizarre traits, including a differentiated and dynamic trophozoite stage that resembles the scolex and strobila of tapeworms. Described originally as “Mesozoa”, comparative ultrastructural data and molecular phylogenetic analyses have shown that haplozoans are aberrant dinoflagellates; however, these data failed to resolve the phylogenetic position of haplozoans within this diverse group of protists. Several hypotheses for the phylogenetic position of haplozoans have been proposed: (1) within the Gymnodiniales based on tabulation patterns on the trophozoites, (2) within the Blastodiniales based on the parasitic life cycle, and (3) part of a new lineage of dinoflagellates that reflects the highly modified morphology. Here, we demonstrate the phylogenetic position of haplozoans by using three single-trophozoite transcriptomes representing two species: Haplozoon axiothellae and two isolates of H. pugnus collected from the Northwestern and Northeastern Pacific Ocean. Unexpectedly, our phylogenomic analysis of 241 genes showed that these parasites are unambiguously nested within the Peridiniales, a clade of single-celled flagellates that is well represented in marine phytoplankton communities around the world. Although the intestinal trophozoites of Haplozoon species do not show any peridinioid characteristics, we suspect that uncharacterized life cycle stages may reflect their evolutionary history within the Peridiniales.