Abstract
Social behaviours are frequently utilised for defence and stress avoidance in nature. Both Caenorhabditis elegans and Pristionchus pacificus nematodes display social behaviours including clumping and bordering, to avoid hyperoxic stress conditions. Additionally, both species show natural variation in social behaviours with “social” and “solitary” strains. While the single solitary C. elegans N2 strain has evolved under laboratory domestication due to a gain-of-function mutation in the neuropeptide receptor gene npr-1, P. pacificus solitary strains are commonplace and likely ancestral. P. pacificus therefore provides an opportunity to further our understanding of the mechanisms regulating these complex behaviours and how they evolved within an ecologically relevant system. Using CRISPR/Cas9 engineering, we show that Ppa-npr-1 has minimal influence on social behaviours, indicating independent evolutionary pathways compared to C. elegans. Furthermore, solitary P. pacificus strains show an unexpected locomotive response to hyperoxic conditions, suggesting a novel regulatory mechanism counteracting social behaviours. By utilising both forward and reverse genetic approaches we identified 10 genes of the intraflagellar transport machinery in ciliated neurons that are essential for this inhibition. Therefore, a novel cilia-mediated environmental input adds an additional level of complexity to the regulation of hyperoxia-induced social behaviours in P. pacificus, a mechanism unknown in C. elegans.
Highlights
Nematodes have a highly developed chemosensory system and are able to respond to a multitude of environmental cues
It has been suggested that clumping and bordering behaviours are instigated to avoid the hyperoxic stress conditions induced by the 21% oxygen concentration [O2] present in the laboratory[4], since both behaviours result in the nematodes being exposed to lower [O2]
These findings indicate that the locomotive response to hyperoxic stress conditions as seen in P. pacificus RS2333 has not been a result of domestication in the approximately 3,000 generations this strain is cultured under laboratory conditions, but rather represents a general feature of solitary P. pacificus strains under natural conditions
Summary
Nematodes have a highly developed chemosensory system and are able to respond to a multitude of environmental cues. Clade B strains may perform social behaviours to avoid hyperoxic conditions in the laboratory, but they behave as solitary strains when the O2 levels are similar to those that they experience in the wild, suggesting that all P. pacificus strains behave solitary in natural conditions. These observations may be related to the necromenic association of P. pacificus and its connection to scarab beetle hosts, in which the arrested dauer stage of the nematode colonizes the insect and resumes development only after the death of the beetle by feeding on the proliferating microbes on the beetles’ carcass[18]. The need for the nematodes to search for a new host may have favoured the emergence of a mechanism that induces solitary foraging and favours dispersion
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