Abstract
Sexually dimorphic differentiation of sex-shared behaviors is observed across the animal world, but the underlying neurobiological mechanisms are not fully understood. Here we report sexual dimorphism in neurotransmitter release at the neuromuscular junctions (NMJs) of adult Caenorhabditis elegans. Studying worm locomotion confirms sex differences in spontaneous locomotion of adult animals, and quantitative fluorescence analysis shows that excitatory cholinergic synapses, but not inhibitory GABAergic synapses exhibit the adult-specific difference in synaptic vesicles between males and hermaphrodites. Electrophysiological recording from the NMJ of C. elegans not only reveals an enhanced neurotransmitter release but also demonstrates increased sensitivity of synaptic exocytosis to extracellular calcium concentration in adult males. Furthermore, the cholinergic synapses in adult males are characterized with weaker synaptic depression but faster vesicle replenishment than that in hermaphrodites. Interestingly, T-type calcium channels/CCA-1 play a male-specific role in acetylcholine release at the NMJs in adult animals. Taken together, our results demonstrate sexually dimorphic differentiation of synaptic mechanisms at the C. elegans NMJs, and thus provide a new mechanistic insight into how biological sex shapes animal behaviors through sex-shared neurons and circuits.
Highlights
Behavioral sex differences are observed in most, if not all animal species
Caenorhabditis elegans sinusoidal movement results from the alternating contraction and relaxation of body wall muscle cells, which are triggered by ACh and GABA released at the neuromuscular junctions (NMJs), respectively
Since SNB-1 is presynaptic vesicle-associated protein required for versicle release, these results suggested that adult males host more presynaptic vesicles at NMJs than adult hermaphrodites
Summary
Dimorphic behaviors are the result of the presentation of specific neurons and synaptic connections exclusive in one sex, and/or sex-biased functional modulation of shared neurons in both sexes (Ngun et al, 2011; Portman, 2017; Choleris et al, 2018). Similar to other model organisms, C. elegans processes a number of sex-specific anatomical features in the nervous system, including male- and hermaphrodite-specific neurons and synaptic connections, which encode sex-specific behaviors, and drive sexually dimorphic traits in behaviors developed in both sexes (Portman, 2017; Barr et al, 2018). Low expression of the food-associated chemoreceptor ODR-10 in AWA sensory neuron of well-fed males, one of the core sensory neurons in both sexes, promotes mate-search search (Ryan et al, 2014)
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