The PVD neuron has male-specific structure and mating function in C. elegans

Abstract

Neurons display unique shapes and establish intricate networks, which may differ between sexes. In complex organisms, studying sex differences in structure and function of individual neurons is difficult. The nematode Caenorhabditis elegans hermaphrodites and males present an exceptional model for studying neuronal morphogenesis in a simple, sexually-dimorphic system. We focus on the polymodal sensory bilateral neuron pair PVD, which forms a complex but stereotypic dendritic tree composed of multiple subunits that resemble candelabra. PVD is well studied in hermaphrodites, but not in males. We show here that during larval development, male PVDs extend a similar architecture to the hermaphrodite utilizing the sexually-shared Menorin patterning mechanism. In early adulthood, however, male PVD develops a unique extension into the copulatory tail structure. Alongside established tail ray neurons RnA and RnB, we show PVD is a third, previously unrecognized, neuron within the tail rays. Unlike RnA and RnB, PVD extends anterogradely, branches and turns within the ray hypodermis, and is non-ciliated. This PVD sexually-dimorphic arborization is absent in mutant backgrounds which perturb the Menorin guidance complex. SAX-7/L1CAM, a hypodermal component of this complex, shows a male-specific expression pattern which precedes PVD extension, and its presence allows PVD to enter the tail rays. Further, our results reveal that genetically altered arborization or ablation of the PVD result in male mating behavioral defects, particularly as males turn around the hermaphrodite. These results uncover an adult-stage sexual dimorphism of dendritic branching and uncover a function for PVD in male sexual behavior.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

* We have extended our analysis of PVD dendritic trees in the male tail by employing mutants, genetic cell ablations, reporter genes, and advanced microscopy techniques, including confocal and electron microscopy. Firstly, we have confirmed that the tip processes of PVD are not ciliated. Secondly, we have shown that these processes do not invade the channel occupied by the other two neuronal dendrites, RnA and RnB. Thirdly, we demonstrate that the intra-ray PVD processes enter the rays in an anterograde manner during adulthood, whereas the RnA and RnB dendrites enter the channel in a retrograde fashion during the L4 stage. Fourthly, through the expression of human caspase in RnB, we establish that the ablation of this neuron does not hinder the entry and morphogenesis of the PVD within the rays. Lastly, we reveal that the PVD processes independently migrate, branch, and perform U-turns within the rays, independently from the channel. These additional characterizations of the sexually dimorphic PVD dendritic trees in males enhance and provide a more detailed and mechanistic understanding of our findings.