Evolution of Animal Parasitism in Nematodes of the Suborder Spirurina

The phylum Nematoda includes species adapted to nearly every environment on Earth, ranging from free-living forms to parasites of plants and animals. Parasitism has evolved multiple times independently within the phylum, and the suborder Spirurina is particularly notable because all of its members are obligate animal parasites. In this study, we conducted a molecular phylogenetic analysis of Spirurina, integrating ancestral state reconstruction (ASR) to clarify higher-level relationships and to trace the evolutionary origins of parasitism. Our analysis suggested that the parasitic origin of Spirurina, which arose from free-living nematodes within Rhabditida that had adapted to terrestrial environments, is bifurcated. One is associated with early-dividing lineages of aquatic invertebrates (Gnathostomatomorpha and Seuratoidea), while the other is associated with millipedes belonging to a large terrestrial clade that includes the suborders Oxyuridomorpha, Rhigonematomorpha, Ascaridomorpha, Camallanomorpha, and Spiruromorpha. Comparative examination of life cycles across infraorders indicates that parasitic strategies evolved from simple, single-host infection cycles to complex life cycles requiring intermediate hosts. These complex cycles appear to have originated in freshwater environments, where copepods and other crustaceans served as ancestral intermediate hosts in aquatic lineages. Importantly, our findings identify millipedes as a pivotal ancestral host group that shaped the early terrestrial evolution of parasitism within Spirurina. Together, these findings provide a comprehensive framework for understanding the evolutionary pathways that gave rise to the remarkable diversity of parasitic strategies within Spirurina.