Variation in the post-mating fitness landscape in fruitflies

Sperm competition is pervasive and fundamental to determining a male’s overall fitness. Sperm traits and seminal fluid proteins (Sfps) are key factors. However, studies of sperm competition may often exclude females that fail to remate during a defined period. Hence, the resulting datasets contain fewer data from the potentially fittest males that have most success in preventing female remating. It is also important to consider a male’s reproductive success before entering sperm competition, which is a major contributor to fitness. The exclusion of these data can both hinder our understanding of the complete fitness landscapes of competing males and lessen our ability to assess the contribution of different determinants of reproductive success to male fitness. We addressed this here, using the Drosophila melanogaster model system, by (i) capturing a comprehensive range of intermating intervals that define the fitness of interacting wild type males, and (ii) analysing outcomes of sperm competition using selection analyses. We conducted additional tests using males lacking the sex peptide (SP) ejaculate component versus genetically matched (SP+) controls. This allowed us to assess the comprehensive fitness effects of this important Sfp on sperm competition. The results showed a signature of positive, linear selection in wild type and SP+ control males on the length of the intermating interval and on male sperm competition defense. However, the fitness surface for males lacking SP was distinct, with local fitness peaks depending on contrasting combinations of remating intervals and offspring numbers. The results suggest that there are alternative routes to success in sperm competition and provide an explanation for the maintenance of variation in sperm competition traits.