The effect of mating history on male reproductive ageing in Drosophila melanogaster

Mating bears costs, but how these costs affect the senescence of reproductive traits in males has received relatively little attention. Males of many species show reduced benefits from pre- and post-copulatory reproductive traits during ageing. Senescence of post-copulatory reproductive traits is often linked to a reduction in sperm quantity and quality, but can also be a consequence of changes in seminal fluid proteins that are transferred alongside sperm during mating. Here we investigated how mating history affects male reproductive ageing, especially at the post-copulatory level, using Drosophila melanogaster, a species in which links between seminal fluid proteins and male reproductive traits are well established. Besides a male cohort kept virgin until the start of the experiment we also included a cohort of males kept together with females allowing for ample mating opportunities. With these males we conducted a series of behavioral experiments covering several aspects of male reproductive success with males ranging in age from 4 days to 6 weeks after eclosion. Additionally, we investigated the storage capacity of male accessory glands (AG), the production site of the majority of seminal fluid proteins. We found male reproductive success to decline with increasing male age and, most importantly, males with prior matings showed a reduced performance in pre-copulatory success. However, our data suggest a constant short-term cost of mating rather than an accelerated senescence of pre-copulatory traits. In contrast, senescence of post-copulatory reproductive traits differed between mated and virgin males, hinting at mating costs in males altering the ageing process. We could not find any differences in the capacity of the AG to store seminal fluid proteins, however, our data suggest that old males transfer fewer seminal fluid proteins in a single mating. We conclude that a variety of traits is affected by male reproductive ageing in D. melanogaster with the cost of mating varying in its impact on senescence in these traits.