The evolution of endoparasitism and complex life cycles in parasitic platyhelminths

Abstract

Within flatworms, the vast majority of parasitism is innate to Neodermata, the most derived and diversified group of the phylum Platyhelminthes.1,2 The four major lineages of Neodermata maintain various combinations of life strategies.3 They include both externally (ecto-) and internally feeding (endo-) parasites. Some lineages complete their life cycles directly by infecting a single host, whereas others succeed only through serial infections of multiple hosts of various vertebrate and invertebrate groups. Food sources and modes of digestion add further combinatorial layers to the often incompletely understood mosaic of neodermatan life histories. Their evolutionary trajectories have remained molecularly unresolved because of conflicting evolutionary inferences and a lack of genomic data.4 Here, we generated transcriptomes for nine early branching neodermatan representatives and performed detailed phylogenomic analyses to address these critical gaps. Polyopisthocotylea, mostly hematophagous ectoparasites, form a group with the mostly hematophagous but endoparasitic trematodes (Trematoda), rather than sharing a common ancestor with Monopisthocotylea, ectoparasitic epithelial feeders. Phylogenetic placement of the highly specialized endoparasitic Cestoda alters depending on the model. Regardless of this uncertainty, this study brings an unconventional perspective on the evolution of platyhelminth parasitism, rejecting a common origin for the endoparasitic lifestyle intrinsic to cestodes and trematodes. Instead, our data indicate that complex life cycles and invasion of vertebrates' gut lumen, the hallmark features of these parasites, evolved independently within Neodermata. We propose the demise of the traditionally recognized class Monogenea and the promotion of its two subclasses to the class level as Monopisthocotyla new class and Polyopisthocotyla new class.