1. The mechanistic basis for and adaptive significance of variation in female sperm storage organs are important for a range of questions concerning sexual selection and speciation, as such variation influences the evolutionary trajectories of male fertilization related traits and may facilitate speciation through its effects on gamete recognition.
2. Female yellow dung flies (Scathophaga stercoraria) usually develop three sperm storage compartments, and this subdivision may be an adaptation for sorting sperm during postcopulatory choice.
3. Using lines artificially selected to express four spermathecae (4s), we explored the fitness consequences of the novel phenotype relative to the naturally prevalent three-spermatheca (3s) phenotype by manipulating the opportunity for postcopulatory sexual selection (females mated either with three or only one male prior to oviposition). In addition, we examined the developmental plasticity of spermathecal number in response to different larval food environments and estimated its genetic correlation with growth rate.
4. Mating treatments with and without the opportunity for postcopulatory sexual selection revealed no significant fitness differences between alternative spermathecal phenotypes within selection lines despite overall benefits associated with multiple mating, and moderate egg-to-adult survival costs in response to artificial selection for 4s. Manipulations of the larval food environment revealed that the expression of 4s is highly plastic and tightly linked to environmental conditions promoting fast somatic growth and development. Likewise, siblings with fast intrinsic (genetic) growth were more likely to express 4s within and across food environments.
5. The present results highlight a great potential for rapid evolutionary change in female sperm storage morphology through indirect selection on life-history traits, and further suggest genetic assimilation as a potential mechanism facilitating phylogenetic transitions in spermatheca number as frequently observed within the Dipterans.