Evolutionarily-conserved behavioral plasticity enables context-dependent performance of mating behavior in C. elegans

Behavioral plasticity helps humans and animals to achieve their goals by adapting their behaviors to different environments. Although behavioral plasticity is ubiquitous, many innate species-specific behaviors, such as mating, are often assumed to be stereotyped and unaffected by plasticity or learning, especially in invertebrates. Here, we describe a novel case of behavioral plasticity in the nematode C. elegans - under a different set of naturalistic conditions the male uses a unique, previously undescribed set of behavioral steps for mating. Under standard lab conditions (agar plates with bacterial food), the male performs parallel mating, a largely two-dimensional behavioral strategy where his body and tail remain flat on the surface and slide alongside the partner s body from initial contact to copulation. But when placed in liquid medium, the male performs spiral mating, a distinctly three-dimensional behavioral strategy where he winds around the partner s body in a helical embrace. The performance of spiral mating does not require a long-term change in growing conditions but it does improve with experience. This experience-dependent improvement involves a critical period - a time window around the L4 to early adult stage, which coincides with the development of most male-specific neurons. We tested several wild isolates of C. elegans and other Caenorhabditis species and found that most were capable of parallel mating on surfaces and spiral mating in liquids. We suggest that two- and three-dimensional mating strategies in Caenorhabditis are plastic, conditionally expressed phenotypes conserved across the genus, and which can be genetically "fixed " in some species.