Independent recruitment of F box genes to regulate hermaphrodite development during nematode evolution

Elucidating the molecular mechanisms that created ancient complex traits like insect wings is difficult. Fortunately, some complex traits have arisen recently. For example, hermaphroditic reproduction evolved independently many times during recent nematode evolution. Although C. elegans hermaphrodites require fog-2, which encodes an F box protein that regulates the translation of tra-2 mRNAs, the related species C. briggsae lacks fog-2. We identified a critical regulator of hermaphrodite development in C. briggsae, named she-1. Analysis of double mutants indicates that she-1 acts upstream of tra-2 in C. briggsae, just as fog-2 does in C. elegans. Molecular cloning shows that she-1 encodes a novel F box protein that was created by a recent gene duplication. Whereas FOG-2 acts through GLD-1 in C. elegans, SHE-1 does not bind GLD-1 in C. briggsae. Thus, both species recruited F box genes produced by recent duplication events into the sex-determination pathway to control hermaphrodite development, but these genes have distinct activities. This result implies that some gene families are more likely to give rise to novel regulatory genes than other families. Finally, we note that null mutations of she-1 are temperature sensitive, so C. briggsae might once have been a facultative hermaphrodite.