Glial expression of a steroidogenic enzyme underlies natural variation in hitchhiking behavior.

Abstract

Phoresy is an interspecies interaction that facilitates spatial dispersal by attaching to a more mobile species. Hitchhiking species have evolved specific traits for physical contact and successful phoresy, but the regulatory mechanisms involved in such traits and their evolution are largely unexplored. The nematode <i>Caenorhabditis elegans</i> displays a hitchhiking behavior known as nictation during its stress-induced developmental stage. Dauer-specific nictation behavior has an important role in natural <i>C. elegans</i> populations, which experience boom-and-bust population dynamics. In this study, we investigated the nictation behavior of 137 wild <i>C. elegans</i> strains sampled throughout the world. We identified species-wide natural variation in nictation and performed a genome-wide association mapping. We show that the variants in the promoter of <i>nta-1</i>, encoding a putative steroidogenic enzyme, underlie differences in nictation. This difference is due to the changes in <i>nta-1</i> expression in glial cells, which implies that glial steroid metabolism regulates phoretic behavior. Population genetic analysis and geographic distribution patterns suggest that balancing selection maintained two <i>nta-1</i> haplotypes that existed in ancestral <i>C. elegans</i> populations. Our findings contribute to further understanding of the molecular mechanism of species interaction and the maintenance of genetic diversity within natural populations.