Sexually reproducing animals display sex-specific behaviors wired onto dimorphic connectivity patterns in the nervous system (Jarrell et al., 2012). The mechanisms underlying the development of sexually dimorphic nervous systems that consists mainly of shared neuronal types remain largely unknown.
Here we dissect the regulatory programs that specify sexually dimorphic neuron identity. Specifically, we focus on the PHB sensory neurons, which function as chemosensory cells that negatively modulate reversals to odorant repellents (Hilliard et al., 2002). In hermaphrodites, PHBs synapse heavily onto command interneurons (AVAs) that control locomotion. Using in vivo trans-synaptic labeling (Feinberg et al., 2008), we confirm the EM data from Jarrell et al. that demonstrates these connections are absent in adult males, and instead, connections are made with AVG and LUA interneurons and male specific motor neurons. We find that PHBs in males do not process the same sensory cues as in hermaphrodites, but instead are repurposed to process cues involved in mating behavior. Inducible neuronal silencing of PHBs results in defective contact-induced backward locomotion of males during mating, as well as defective vulva location. Strikingly, we find that PHB-AVA synaptic connections are shared by both sexes at the L1 stage, therefore resulting in the sensory modulation of locomotion by repellents in both sexes. Later in development, the PHBs synapses to AVA interneurons are pruned in males, generating a sexually diverged synaptic state that generates dimorphic behaviors. Using cell-specific neuronal masculinization, we show that the pre-synaptic cell autonomously controls sex-specific pruning. Conversely, PHB-AVA synapses are pruned in hermaphrodites with masculinized PHBs, and the antagonistic behavior is lost. The regulatory programs that trigger this specific dimorphic connectivity are controlled by several members of the evolutionary conserved family of DM domain Zn-finger transcription factors, which function in neuron-type specific modules. dmd-5 and dmd-11 are dimorphically expressed in the male AVG neuron and are required for synaptic connectivity and male mating behavior.
Our results suggest that sexual identity of individual neurons defines sex-specific synaptic targets and allows for diversification of behavioral outputs with a limited set of shared neurons.
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