Evolution of parasitism-related traits in nematodes

Summary The abundant resources provided by the host provide an evolutionary rationale for parasitism and drive the metabolic and developmental divergence of parasitic and free-living animals. Two evolutionally distant nematode genera, Steinernema and Heterorhabditis, independently evolved an entomopathogenic lifestyle, in which they invade insects and kill them with the assistance of specifically associated symbiotic pathogenic bacteria. It had been generally assumed that the worm, being a bacterivore, feeds on its symbiotic bacteria, which rapidly reproduce while consuming the insect host. The evolutionary adaptations of entomopathogenic nematodes to a parasitic lifestyle developmentally, and the symbiotic relationships of entomopathogenicity, remain largely unknown. We developed an axenic culture medium that allows for robust and sustained growth of Steinernema hermaphroditum, allowing finite control of nutrients available to the nematodes. We found that, uniquely among nematodes tested, the hatchlings of S. hermaphroditum cannot endure in a nutrient-poor environment; this ability is impaired but still present in Heterorhabditis bacteriophora. Similarly, the ability to forage for food is completely lost in H. bacteriophora hatchlings and severely compromised in S. hermaphroditum. We reasoned that these traits were lost because they are unnecessary to obligate parasites that always hatch in a resource-rich host. We further found that Steinernema and, to a limited extent, Heterorhabditis nematodes can successfully invade, develop, and reproduce inside a living insect host independent of their symbiotic bacteria, apparently feeding on the hemolymph, and emerge carrying bacteria found within, explaining the evolutionary origins of entomopathogenic nematodes. Highlights A simple but robust axenic culturing method for the emerging model nematode Steinernema hermaphroditum and other invertebrate parasitic nematodes. Convergent evolution led to the loss of hatchling survival traits in entomopathogenic nematodes. Nematode adaptation to parasitism is associated with changes in modes of feeding. Entomopathogenic nematodes evolved from parasitoid ancestors. Graphical abstract