Natural variation in Caenorhabditis elegans collective behavior reveals potential adaptation to novel environments

Animal behavior can diverge in natural populations in response to different environmental conditions, but if and how natural selection also shapes the evolution of collective behavior in groups of animals remains underexplored. With their cosmopolitan distribution and known collective behaviours, wild populations of Caenorhabditis elegans provide a powerful system to address how collective behavior could evolve across natural habitats on a global scale. We screened a panel of 196 genetically diverse C. elegans strains sampled from around the world, conducting aggregation behavior experiments and analysis to quantify natural variation among these populations. We found substantial variation in the spatial magnitude and the temporal dynamics of aggregation across strains, which were significantly explained by the elevation of the source habitats. Accounting for neutral evolutionary processes, our maximum likelihood population effects (MLPE) models further support a role of selection on aggregation. Furthermore, the two behavioral traits are highly heritable, and genome-wide association studies (GWAS) revealed a quantitative trait locus (QTL) containing several candidate genes associated with oxygen response and foraging behaviors. Our results showcase C. elegans aggregation as a collective behavior that has diverged globally across elevational gradients, and support that natural selection has shaped the evolution of this collective behavior.