Juvenile population density induces condition‐dependent lifetime sperm investment in a sperm‐heteromorphic moth

Abstract Individual condition is a critical factor influencing fitness variation in animal populations. However, how adult condition, mating behaviour and lifetime sperm allocation interplay to determine fitness outcomes of males 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 unmated females of varying conditions daily until male death, measuring body weight, pre‐mating behaviour, lifetime fertile (eupyrene) and infertile (apyrene) sperm transfer, mating frequency and longevity. High‐density rearing reduced adult body weight in both sexes. Male and female conditions independently influenced lifetime sperm investment, with no significant interaction between the two. High‐condition males possessed a greater baseline capacity, transferring significantly more sperm than low‐condition males. Concurrently, males, regardless of their conditions, employed a universal strategy of transferring significantly more sperm of both types to high‐condition females compared to low‐condition females. This resulted in a faster decline of sperm reserves in these pairings, demonstrating cryptic male choice via strategic sperm allocation. Despite these differences in sperm quantity, the infertile‐to‐fertile sperm ratio remained constant at approximately 6:1 across all treatments. This suggests either a fixed physiological constraint on sperm composition or a ratio selected to maximise fertilisation success in unmated females. Adult condition affected distinct stages of the pre‐mating sequence. The time taken to initiate courtship was driven primarily by female condition, with males, regardless of their own condition, taking significantly longer to court high‐condition females. However, mating latency was independently influenced by both sexes, that is, low‐condition males and females initiated copulation early, potentially representing a time‐minimisation strategy to ensure reproductive success under resource limitation. Our study adds important nuance to condition‐dependence theory, demonstrating that although high phenotypic condition increases overall reproductive capacity, the targeted allocation of those resources is independently driven by mate quality. For capital breeders constrained by finite resources, this highlights that reproductive strategies are shaped by the independent, additive effects of an individual's developmental history and their immediate social context.