Abstract
The independent origins of plant parasitism in nematodes offer a classic model for studying the evolution of parasitic adaptations. Using comparative genomics, we analyzed representative nematodes from the superfamilies Aphelenchoidea and Tylenchoidea within the suborder Tylenchina, uncovering the genetic basis of cross-superfamily molecular convergence and lineage-specific divergence. Overall, sequence-level molecular convergence was relatively weak, reflecting dilution of evolutionary contrast by closely related ancestral genetic backgrounds and the diverse genetic mechanisms by which different lineages attain the plant-parasitic phenotype. Nevertheless, these two independently evolved parasitic lineages exhibited a predictable, general-purpose molecular arsenal for breaching host physical and immune barriers. At the metabolic level, the unsaturated fatty acid biosynthesis pathway (ko01040) underwent concordant and significant contraction across plant-parasitic lineages throughout the suborder, suggesting a possible shift toward greater reliance on host-derived lipids, although this remains to be functionally tested. At the sequence level, the two superfamilies displayed strong site-level convergence in core genes including host recognition (GRK, Tr-type G), effector protein folding (PDI), plant nitrogen assimilation (asparagine synthetase), and interfacial stress perception (DOMON, alkaline ceramidase), which may contribute to the molecular framework for breaching parasitic barriers and warrant further experimental validation. Building on this foundation, life-history and niche differentiation drove a dual-track paradigm. The Tylenchoidea lineage, represented by sedentary endoparasites, followed a path of large-scale genome-wide streamlining, with extensive outsourcing and degeneration of autonomous metabolic pathways, highly adapted to the stable internal environment of specialized root feeding sites. In contrast, the migratory parasitic Aphelenchoidea displayed a dual paradigm of conserved genome-wide metabolic versatility coupled with precise micro-level remodeling of stress-resistance networks, which we propose, as candidate hypotheses, may facilitate adaptation to the high-stress aerial environment and multiple hosts through micro-scale remodeling of mitochondrial stress responses, host-lipid utilization, and medium-sensing proteins. This contrast between macro-scale degeneration and micro-scale specialization provides a genomic perspective that may help inform future work on the origin and evolutionary radiation of parasitism in invertebrates.