Broad phylogenetic analyses of the four major plant-parasitic nematode lineages reveal essentially distinct origins and diversification patterns

Four major nematode clades are discerned within which plant parasitism arose at least once. The distinct levels of diversification within the individual clades are reflected by their systematics: plant parasites in the basal Clades 1 and 2 reside in (just) two families (Trichodoridae and Longidoridae). Meanwhile, in Clades 10 and 12 parasitic nematodes are allocated in a superfamily (Aphelenchoidoidea) and an order (Tylenchida). By taking the coverage of the next lower taxonomic level as a measure, 60, 80, 100 and 85% of the diversity was included in our phylogenetic analyses. Individual clades represented by 93 (Clade 1), 171 (Clade 2), 320 (Clade 10), and 1,089 (Clade 12) nearly full-length small subunit ribosomal DNA sequences (≈ 1,700 bp each) were analyzed using Bayesian and Maximum likelihood-based inferences. Diversification patterns among these Clades are distinct. Clades 1 and 2 exclusively harbor ectoparasites, of which a subset transmits Tobra (Trichodoridae) or Nepo-viruses (Longidoridae). Superposition of current virus-transmission data on phylogenetic trees revealed 3 (Trichodoridae) and > 5 clusters (Longidoridae) suggesting that minor modifications in the virus-pharynx interface suffice to acquire this capability. Endoparasitism arose exclusively in Clades 10 and 12, resulting in disparate life strategies in each of these clades. Plant parasitism within Clade 10 arose at least 4 times from insect-vectored fungivorous lineages (occasionally with secondary loss of the insect association) and resulted almost exclusively in endoparasites of above-ground plant parts, in the absence of (intermediate) ectoparasites. Our analyses point at a single common origin of all predominantly below-ground feeding plant parasites in Clade 12, whereas sedentary endoparasitism arose at least five times. Numerous origins and shapes of plant parasitism-relevant characteristics such as the development of plant parasitism per se, of sedentary endoparasitism, and of virus-vectoring capacities point at an unexpected flexibility within this morphologically conserved phylum.