Comparative connectomics of parasite esophagus suggests evolutionary simplification of a nervous system

Abstract

Several prominent examples suggest that the evolution of parasitism is accompanied by nervous system simplification. However, it is unclear if this is a generalizable rule and whether parasite- associated simplification occurs at the level of synaptic connectivity. The nematode esophagus is a specialized neuromuscular feeding organ that varies with diet and lifestyle. Plant-parasitic nematodes are major agricultural pests that feed through a protrusible stylet and release of extensive glandular effectors; however, the neuronal mechanisms controlling parasite feeding are unclear. Here, we used serial-section electron microscopy to reconstruct the esophageal connectome of the infective second-stage juvenile of the soybean cyst nematode, Heterodera glycines, and compared it with those of the free-living species Caenorhabditis elegans and Pristionchus pacificus. Similar to these species, H. glycines has 20 esophageal neurons with relatively conserved cell body positions. Despite this conservation, the H. glycines chemical synaptic network is highly reduced in output to musculature. A unique ensheathment of neurons by a gland cell facilitates novel synaptic connectivity in H. glycines. The H. glycines esophageal network is strongly biased toward monadic synapses and shows a greater proportion of neuron- neuron and neuron-gland connections. Consistent with a reduction in motor output, network analysis indicates that the H. glycines esophageal network is smaller and less clustered than free-living species. Using centrality analysis and synthetic ablation, we predict that control of multiple feeding modules in H. glycines depends on distinct neurons compared to free-living species. These findings show how parasitism reshapes a feeding circuit and identify candidate species-specific circuits for parasite control. Significance statementAnimal nervous systems are tuned to the behaviors they support. Nematodes occupy diverse ecological niches, and their feeding organ, the esophagus, is specialized to their diet. Understanding the esophageal nervous system provides evolutionary insights into parasitism as well as pathways for future control targets. We present the esophageal connectome of the soybean cyst nematode Heterodera glycines, which causes devastating damage to soybean production worldwide. By comparing H. glycines and free-living species, which diverged over 350 million years ago, we identify evolutionarily conserved features of the feeding circuit and highlight parasite-specific circuits as candidate targets for control.