Sensation in a Single Neuron Pair Represses Male Behavior in Hermaphrodites

Abstract

Summary Pheromones elicit innate sex-specific mating behaviors in many species. We demonstrate that in C. elegans, male-specific sexual attraction behavior is programmed in both sexes but repressed in hermaphrodites. Repression requires a single sensory neuron pair, the ASIs. To represses attraction in adults, the ASIs must be present, active, and capable of sensing the environment during development. The ASIs release TGF-β, and ASI function can be bypassed by experimental activation of TGF-β signaling. Sexual attraction in de-repressed hermaphrodites requires the same sensory neurons as in males. The sexual identity of both these sensory neurons and a distinct subset of interneurons must be male to relieve repression and release attraction. TGF-β may therefore act to change connections between sensory- and interneurons during development to engage repression. Thus, sensation in a single sensory neuron pair during development reprograms a common neural circuit from male to female behavior.

Genes and circuits of courtship behaviour in Drosophila males

“…Recent studies have indicated that this picture also holds in other organisms. For example, in Caenorhabditis elegans, male-specific sexual attraction behaviour is repressed in hermaphrodites by a single neuron pair, the ASIs, which release transforming growth factor-β during development to induce this repression 72 . Upon de-repression, hermaphrodites exhibit male behaviour using the same neuronal circuits as those used by males 72 .…”

Patterning of sexually dimorphic neurogenesis in the Caenorhabditis elegans ventral cord by Hox and TALE homeodomain transcription factors

“…Hermaphrodites, in contrast, have eight sex-specific neurons, all of which regulate egg laying (reviewed in Schafer, 2005). Furthermore, some neurons common to both sexes are functionally specialized to mediate sex-specific behaviors such as response to pheromones (Jang et al, 2012;White and Jorgensen, 2012).…”

Reciprocal inhibition between sensory ASH and ASI neurons modulates nociception and avoidance in Caenorhabditis elegans

“…Notably, the neurotransmitters, such as neuropeptides, serotonin (5-HT), tyramine (TA) and octopamine (OA), have been increasingly shown to be transmitters or modulators of ASH-mediated aversive behaviours [12][13][14][15] . ASI sensory neurons are reported to mediate dauer formation 16 , enable worms to learn to avoid the smell of pathogenic bacteria after ingestion via INS-6 signalling 17 , suppress male-specific sexual attraction behaviour 18 , respond to temperature stimuli to negatively modulate thermotaxis behaviour 19 , mediate diet-restriction-induced longevity 20 , modulate satiety quiescence 21 , regulate acute CO 2 avoidance 22 , repress exploratory behaviours that comprise spontaneous reversals and omega turns 5 , and inhibit ASH-mediated aversive responses to 100% 1-octanol 23 . These studies support the hypothesis that ASIs are important polymodal sensory neurons mediating or modulating worm behaviours and development.…”