Developmental alterations of the C. elegans male anal depressor morphology and function require sex-specific cell autonomous and cell non-autonomous interactions

We studied the Caenorhabditis elegans anal depressor development in larval males and hermaphrodites to address how a differentiated cell sex-specifically changes its morphology prior to adulthood. In both sexes, the larval anal depressor muscle is used for defecation behavior. However in the adult males, the muscle's sarcomere is reorganized to facilitate copulation. To address when the changes occur in the anal depressor, we used YFP:actin to monitor, and mutant analysis, laser-ablation and transgenic feminization to perturb the cell's morphological dynamics. In L1 and L2 stage larva, the muscle of both sexes has similar sarcomere morphology, but the hermaphrodite sex-determination system promotes more growth. The male anal depressor begins to change in the L3 stage, first by retracting its muscle arm from the neurons of the defecation circuit. Then the muscle's ventral region develops a slit that demarcates an anterior and posterior domain. This demarcation is not dependent on the anal depressor's intrinsic genetic sex, but is influenced by extrinsic interactions with the developing male sex muscles. However, subsequent changes are dependent on the cell's sex. In the L4 stage, the anterior domain first disassembles the dorsal-ventral sarcomere region and develops filopodia that elongates anteriorly towards the spicule muscles. Later, the posterior domain dissembles the remnants of its sarcomere, but still retains a vestigial attachment to the ventral body wall. Finally, the anterior domain attaches to the sex muscles, and then reassembles an anterior-posteriorly oriented sarcomere. Our work identifies key steps in the dimorphic re-sculpting of the anal depressor that are regulated by genetic sex and by cell-cell signaling.