Search

Parasitic life-strategies in the phylum Nematoda (roundworms) are remarkably diverse and intricate in terms of evolution and taxonomy. By analysing novel rDNA data obtained on rare host-associated groups with unusual biology, we reveal paraphyly of the last major taxon with uncertain higher-rank classification that united solely parasitic nematodes (Marimermithida) to show that primarily marine parasitism only emerged independently and repeatedly in a few free-living lineages. We report secondary seaward ingression of land-based parasites (Mermithida) via invading hosts in the subtidal zone to illustrate the host-borne scenario of oceanic fish and mammal colonization by primarily terrestrial parasites (Spiruria). We also present the first molecular data on marine nematodes from unicellular hosts (foraminiferan protozoans) to demonstrate the independent origins of exploitative nematode associations at a microscopic scale. We argue that, in contrast with primarily intestinal associations arising from saprotrophy and commensalism, non-intestinal host capture (colonization of host body cavity or internal organs) is likely to be a primary route of transition to truly exploitative parasitism in roundworms. Predispositions to host capture in nematode morphology, ecology and life cycles imply its evolution as part of innate pre-adaptations to crossing environmental boundaries to enable multiple successful transitions to parasitism in the phylum history.

Nematodes (roundworms) are ubiquitous animals commonly dominating in ecological communities and networks, with many parasites and pathogen vectors of great economic and medical significance. Nematode parasites are remarkably diverse in life strategies and adaptations at a great range of hosts and dimension scales, from whales to protozoan cells. Their life history is intricate and requires understanding to study the genomic, structural and ecological bases of successful transitions to parasitism. Based on analyses of rDNA for a representative sampling of host-associated and free-living groups, we dismiss the last higher-rank nematode taxon uniting solely parasitic forms (Marimermithida) and show that primarily marine parasitism emerged independently and repeatedly within only few free-living lineages. We re-evaluate the significance of some traditionally important phenotypic characters and report the phenomenon of dramatic adaptation to parasitism on very short evolutionary timescales. A cross-phylum character interpretation vindicates that non-intestinal (in-tissue or cavitary) host capture was likely a primary route of transition to truly exploitive parasitism (vs. intestinal commensalism) in roundworms, and extant nematode parasitoids (larval parasites) infesting the host body cavity or internal organs realise this primary lifestyle. Parasitism may have evolved in nematodes as part of innate pre-adaptations to crossing environmental boarders, and such transitions have been accomplished multiple times successfully in the phylum history.