The maintenance of males at intermediate frequencies is an important evolutionary problem. Several species ofCaenorhabditisnematodes have evolved a mating system in which selfing hermaphrodites and males coexist. While selfing produces XX hermaphrodites, cross-fertilization produces 50% XO male progeny. Thus, male mating success dictates the sex ratio. Here, we focus on the contribution of themale secreted short(mss) gene family to male mating success, sex ratio, and population growth. Themssfamily is essential for sperm competitiveness in gonochoristic species, but has been lost in parallel in androdioecious species. Using a transgene to restoremssfunction to the androdioeciousCaenorhabditis briggsae,we examined how mating system and population subdivision influence the fitness of themss+genotype. Consistent with theoretical expectations, whenmss+andmss-null (i.e., wild type) genotypes compete,mss+is positively selected in both mixed-mating and strictly outcrossing situations, though more strongly in the latter. Thus, while sexual mode alone affects the fitness ofmss+, it is insufficient to explain its parallel loss. However, in genetically homogenous androdioecious populations,mss+both increases male frequency and depresses population growth. We propose that the lack of inbreeding depression and the strong subdivision that characterize naturalCaenorhabditispopulations impose selection on sex ratio that makes loss ofmssadaptive after self-fertility evolves.