Male animals often adjust their sperm investment in response to sperm competition environment. To date, only a few studies have investigated how juvenile sociosexual settings affect sperm production before adulthood and sperm allocation during the first mating. Yet, it is unclear whether juvenile sociosexual experience (1) determines lifetime sperm production and allocation in any animal species; (2) alters the eupyrene : apyrene sperm ratio in lifetime ejaculates of any lepidopteran insects, and (3) influences lifetime ejaculation patterns, number of matings and adult longevity. Here we used a polygamous moth, Ephestia kuehniella, to address these questions. Upon male adult emergence from juveniles reared at different density and sex ratio, we paired each male with a virgin female daily until his death. We dissected each mated female to count the sperm transferred and recorded male longevity and lifetime number of matings. We demonstrate for the first time that males ejaculated significantly more eupyrenes and apyrenes in their lifetime after their young were exposed to juvenile rivals. Adult moths continued to produce eupyrene sperm, contradicting the previous predictions for lepidopterans. The eupyrene : apyrene ratio in the lifetime ejaculates remained unchanged in all treatments, suggesting that the sperm ratio is critical for reproductive success. Male juvenile exposure to other juveniles regardless of sex ratio caused significantly shorter adult longevity and faster decline in sperm ejaculation over successive matings. However, males from all treatments achieved similar number of matings in their lifetime. This study provides insight into adaptive resource allocation by males in response to juvenile sociosexual environment.
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