Evolution of sex ratio through gene loss.

Abstract

The maintenance of males at intermediate frequencies is an important evolutionary problem. Several species of <i>Caenorhabditis</i> nematodes 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 the <i>male secreted short</i> (<i>mss</i>) gene family to male mating success, sex ratio, and population growth. The <i>mss</i> family is essential for sperm competitiveness in gonochoristic species, but has been lost in parallel in androdioecious species. Using a transgene to restore <i>mss</i> function to the androdioecious <i>Caenorhabditis briggsae,</i> we examined how mating system and population subdivision influence the fitness of the <i>mss</i><i>+</i> genotype. Consistent with theoretical expectations, when <i>mss+</i> and <i>mss</i><i>-</i>null (i.e., wild type) genotypes compete, <i>mss+</i> 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 of <i>mss+</i>, it is insufficient to explain its parallel loss. However, in genetically homogenous androdioecious populations, <i>mss+</i> both increases male frequency and depresses population growth. We propose that the lack of inbreeding depression and the strong subdivision that characterize natural <i>Caenorhabditis</i> populations impose selection on sex ratio that makes loss of <i>mss</i> adaptive after self-fertility evolves.