Male mating is among the most complex behaviors executed byC. elegans. This multi-step program requires two genes that are homologs of human polycytins, PC-1/lov-1 and PC-2/pkd-2, for the initiation of mating (the response to contact step) and to locate the hermaphrodite vulva. We identified
cwp-5, a novel gene expressed in exactly the same set of male specific neurons as the C. elegans polycystins. CWP-5 is a single pass transmembrane protein, with enrichment in sensory cilia in the ray RnB and head CEM neurons of adult male nematodes. A recessive, loss of function, deletion mutation in
cwp-5(
tm1893) animals produces a profound disruption of the ability of males to initiate mating by responding to hermaphrodite contact. We found that
cwp-5(
tm1893) enhanced the mating defects of both
lov-1(
sy582) and
pkd-2(
sy606) males, but not
lov-1;
pkd-2 double mutant males. This data implies that
cwp-5 acts in a polycystin dependent pathway to promote male mating behavior. Moreover, we observed a significant difference between
cwp-5; polycystin double mutants' behavior and that of
lov-1;
pkd-2;
cwp-5 triple mutants, such that the loss of the remaining polycystin in these animals resulted in a robust improvement in mating efficiency. These data suggest that both polycystins have a latent capacity to repress sensory transduction during male mating, and that this effect is actively repressed by
cwp-5. Additional studies suggest potential functional interactions between
cwp-5 and the polycystins; both PKD-2 and CWP-5 require LOV-1 for proper ciliary targeting. Localization defects of CWP-5::YFP in a
lov-1 mutant background are attenuated by removing
pkd-2, while PKD-2::GFP localization defects are alleviated by removing
cwp-5. Taken together, our work identifies a new gene,
cwp-5, whose function in male mating behavior has revealed a novel mechanism of polycystin regulation of sensory signaling in C. elegans males. Our results may have relevance to the understanding or treatment of human polycystic kidney disease, in which loss of PC-1 or PC-2 function leads to severe kidney failure. If the repression of sensory transduction observed in C. elegans by
lov-1 and
pkd-2 is conserved in human polycystins, interventions aimed at blocking the antagonistic activities of the remaining polycystin may be of value to PKD patients.