Evolution of Insect Parasitism in Rhabditid and Diplogastrid Nematodes

Insect-parasitic nematodes, which obtain nutrients from a living host, arose independently in more than 20 lineages and in different geological periods since Silurian times. Except for Mermithidae, all these are Secernentea, which in various lineages exhibit different degrees between the first steps towards parasitism and obligate parasitism. Only in some tylenchids the transition passed through an ectoparasitc phase. From knowledge about the life cycles of parasitic and closely related free-living species of “Rhabditidae” and Diplogastridae associated with insects, hypotheses are formulated about how obligate parasites could have evolved. Prerequisites include the evolution of a dauer juvenile (J3) in the ancestral lineage of Secernentea and special adaptations as inhabitants of patchily distributed and rapidly changing saprobious habitats on land formed by decaying material, including phoretic behavior on insects. The preadaptation concept, i.e., that several problems for life as a parasitic nematode are “solved” by adaptations to a saprobiontic life in ephemeral habitats, requires further research in more detail. Several steps are included in this preadatation hypothesis, including the transformation of a dauer stage, the association with an insect, the acquisition of special behavioral traits and recognition mechanisms of the J3, the ability to invade animal tissue, the reaction to triggers from organisms and habitats, etc. In particular, endo-phoretic behavior (transportation inside the carrier) was one of the key innovations facilitating the transition to different types of associations like entoecy, necromeny, entomopathogeny (shown to be a special case of parasitoidy), and larval parasitism. The different associations are classified, and the gliding transitions between, e.g., necromeny and entomopathogeny, facultative and obligate parasitism, or uncontrollable relationships called “facultative parasitoidy” are highlighted. Multiple pathways occurred from free-living bacterial feeding nematodes to insect-parasitic ones. Nevertheless, the infective stage always emerged from the third-stage juvenile, constrained by the existence of a dauerlarva which changed its behavior. The physiological and reproductive preadaptations and required adaptations for the transitions between different types of intimate associations with insects are worked out. A diagram depicts the reconstructed evolutionary steps towards different modes of parasitic UDC 595.7:575.8:576.89 Advances in Arachnology and Developmental Biology. Papers dedicated to Prof. Dr. Božidar Ćurčić. S. E. Makarov & R. N. Dimitrijević (Eds.) 2008. Inst. Zool., Belgrade; BAS, Sofia; Fac. Life Sci., Vienna; SASA, Belgrade & UNESCO MAB Serbia. Vienna — Belgrade — Sofia, Monographs, 12, 143-161. 144 S. E. Makarov & R. N. Dimitrijević (Eds.) life of nematodes in insects: larval parasitism, adult parasitism, and a monoxenous or a heteroxenous parasitic life cycle. Three possibilities for the evolution of a heteroxenous life cycle of vertebrate-parasitizing nematodes that utilizes insects as paratenic or intermediate host are discussed, thus placing the J3 in the food chain of the definitive host, are discussed.