A neurotransmitter atlas of the Caenorhabditis elegans male nervous system reveals sexually dimorphic neurotransmitter usage

Abstract

The nervous system of most animals is sexually dimorphic but such dimorphisms are generally poorly mapped on an anatomical, cellular, and molecular level. The adult nervous system of the nematode Caenorhabditis elegans displays a number of clearly defined anatomical sexual dimorphisms, but molecular features of sexually dimorphic neurons remain sparse. In this resource paper, we provide a comprehensive atlas of neurotransmitters used in the nervous system of the male and compare it to that of the hermaphrodite. Among the three major neurotransmitter systems, acetylcholine (ACh) is the most frequently used, followed by glutamate (Glu), and lastly g-aminobutyric acid (GABA). Many male-specific neurons utilize multiple neurotransmitter systems. Interestingly, we find that neurons that are present in both sexes alter their neurotransmitter usage depending on the sex of the animal. One neuron scales up its usage of ACh, another becomes serotonergic in males, and another one adds a new neurotransmitter (glutamate) to its nonsex-specific transmitter (ACh). In all these cases, neurotransmitter changes are correlated with substantial changes in synaptic connectivity. We assembled the neurotransmitter maps of the male-specific nervous system into a comprehensive atlas that describes the anatomical position of all the neurons of the male-specific nervous system relative to the sex-shared nervous system. We exemplify the usefulness of the neurotransmitter atlas by using it as a tool to define the expression pattern of a synaptic organizer molecule in the male tail. Taken together, the male neurotransmitter atlas provides an entry point for future functional and developmental analysis of the male nervous system.