Evolution of parasitism-related traits in nematodes

Abstract

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 evolutionarily 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 worms, being bacterivores, feed on their symbiotic bacteria, which rapidly reproduce as they consume 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 supports robust and sustained growth of Steinernema hermaphroditum, with finite control of nutrients available to the nematodes. We found that, uniquely among the nematodes tested, S. hermaphroditum hatchlings 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. HighlightsO_LIA simple but robust axenic culturing method for the emerging model nematode Steinernema hermaphroditum and other nematode parasites of invertebrates. C_LIO_LINematode adaptation to parasitism is associated with changes in modes of feeding. C_LIO_LIConvergent evolution led to the loss of hatchling survival traits in entomopathogenic nematodes. C_LIO_LIEntomopathogenic nematodes evolved from parasitoid ancestors and likely acquired their bacterial symbionts from their hosts. C_LI Graphical abstract O_FIG O_LINKSMALLFIG WIDTH=146 HEIGHT=200 SRC="FIGDIR/small/678730v2_ufig1.gif" ALT="Figure 1"> View larger version (32K): org.highwire.dtl.DTLVardef@880785org.highwire.dtl.DTLVardef@a5cbcforg.highwire.dtl.DTLVardef@e78671org.highwire.dtl.DTLVardef@2b9d99_HPS_FORMAT_FIGEXP M_FIG C_FIG