Condition-dependent lifetime sperm investment induced by juvenile population density in a sperm-heteromorphic moth

Individual condition is a critical factor influencing fitness variation in animal populations. However, how adult condition, mating behavior, and lifetime sperm allocation interplay to determine fitness outcomes remains poorly understood. We investigated these relationships in the Mediterranean flour moth (Ephestia kuehniella Zeller), a polygamous, sperm-heteromorphic species. We manipulated larval density to produce high-condition (from low density) and low-condition (from high density) adults. Using a factorial design, we paired males and females of varying conditions daily until male death, measuring body weight, pre-mating behavior, lifetime fertile (eupyrene) and infertile (apyrene) sperm transfer, mating frequency, and longevity. Our results demonstrate that high-density rearing significantly reduced adult body weight in both sexes. Supporting condition-dependence theory, high-condition males ejaculated significantly greater total quantities of both sperm types over their lifetime than low-condition males, irrespective of female condition. Furthermore, males of both conditions strategically allocated more sperm when paired with high-condition females, resulting in a faster decline of sperm reserves. This demonstrates cryptic male choice via condition-dependent sperm allocation. Despite these differences in sperm quantity, the fertile-to-infertile sperm ratio remained constant across all treatments, suggesting an optimal ratio. Notably, male condition did not affect lifetime mating frequency or longevity, suggesting low-condition males may trade body size for reproductive investment. These findings reveal that male reproductive investment is a dynamic, lifelong strategy, shaped not only by an individual’s own developmental history but also by the quality of each partner encountered.