Symbiosis of the Millipede Parasitic Nematodes Rhigonematoidea and Thelastomatoidea with Evolutionary Different Origins

Abstract

BackgroundHow various host-parasite combinations have been established is an important question in evolutionary biology. We have previously described two nematode species, Rhigonema naylae and Travassosinema claudiae, which are parasites of the Xystodesmidae millipede Parafontaria laminata in Aichi Prefecture, Japan. Rhigonematoidea belongs to the infraorder Rhigonematomorpha and is phylogenetically close to the Ascaridomorpha, which includes the roundworm parasite in animals. Thelastomatoidea spp. belong to the infraorder Oxyuridomorpha, which comprises a wide variety of parasites in many vertebrates and invertebrates. These nematodes were isolated together with high prevalence; however, the phylogenetic, evolutionary, and ecological relationships between these two parasitic nematodes and between host-parasites are not well known.ResultsWe collected nine species (11 isolates) of Xystodesmidae millipede from seven different locations in Japan and found that all species were co-infected with the parasitic nematodes Rhigonematoidea spp. and Thelastomatoidea spp. Rhigonematoidea spp. is exclusively a millipede parasite, and combinations of parasitic nematode groups and host genera seem to be fixed, supporting the hypothesis of their co-speciation. Intriguingly, Thelastomatoidea spp. were isolated, and the host-parasite relationship was not clarified, clearly indicating the broad host range of these nematode groups. Although the infection prevalence and population of Rhigonematoidea spp. were higher than those of Thelastomatoidea spp., these parasites were not competitive. The population of Rhigonematoidea spp. was not negatively affected by co-infection with Thelastomatoidea spp.ConclusionsPhylogenetic analysis supported our hypothesis that, during the evolution of parasitic nematode diversity in millipedes, the Rhigonematoidea spp. first established relationships with millipedes and were followed by the Thelastomatoidea spp.. The ancestor of the latter nematode might have moved from other host arthropods such as cockroaches.