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Female mate choice can result in direct benefits to the female or indirect benefits through her offspring. Females can increase their fitness by mating with males whose genes encode increased survivorship and reproductive output. Alternatively, male investment in enhanced mating success may come at the cost of reduced investment in offspring fitness. Here, we measure male mating success in a mating arena that allows for male–male, male–female and female–female interactions in Drosophila melanogaster. We then use isofemale line population measurements to correlate male mating success with sperm competitive ability, the number of offspring produced and the indirect benefits of the number of offspring produced by daughters and sons. We find that males from populations that gain more copulations do not increase female fitness through increased offspring production, nor do these males fare better in sperm competition. Instead, we find that these populations have a reduced reproductive output of sons, indicating a potential reproductive trade‐off between male mating success and offspring quality. [ABSTRACT FROM AUTHOR]

Polyandrous females allow for sexual selection to persist after mating. In the event that females successfully mate with more than one male, sperm competition can occur. Seminal fluid proteins can indirectly affect a male's success in sperm competition through reducing the remating behaviour of females and can directly influence sperm competition through directly displacing competitor sperm or inducing females to eject it. These direct effects on competitor sperm are thought to contribute to the 'second male advantage', whereby the second male to mate sires the majority of offspring. Here, we show an additional mechanism where seminal proteins already present within a mated female appear to enhance offspring production of later competitor males, and contribute to second male advantage. Counter to expectation, increased offspring production was not due to a priming effect of greater early female productivity, nor was it through a general and consistent increase in offspring production. Instead, enhanced productivity was solely through lengthening the time that offspring are sired by the second male, indicating that seminal proteins from the first male to mate may enhance second male advantage through a presumably unintended protective effect on subsequent competitor sperm. [ABSTRACT FROM AUTHOR]