Acute heat exposure induces lifetime shifts in non-fertilising sperm allocation in a sperm-heteromorphic insect.

Ectotherm reproduction is vulnerable to acute heat stress, yet the longitudinal impacts of transient thermal events on male reproduction remain poorly understood. Using the stored-product pest Plodia interpunctella, a sperm-heteromorphic moth, we investigated how acute thermal stress (4 h at 40°C) impacts males' lifetime reproductive resource allocation and offspring fitness. Heat-exposed adult males and controls (26°C) were paired daily with non-stressed females. We found that transient heat stress did not significantly impact pre-courtship duration, courtship duration, copulation latency, longevity, or lifetime mating frequency, nor did it alter offspring developmental duration. Total offspring production and lifetime eupyrene (fertile) sperm transfer also remained unaffected. However, heat-exposed males exhibited a massive hyper-allocation of non-fertilising sperm, ejaculating 53.4% more apyrene sperm at a 56.8% faster rate, increasing lifetime apyrene production by 41.0%. This hyper-allocation suggests that non-fertilising apyrene sperm act as a critical compensatory mechanism, buffering eupyrene sperm to maintain intact reproductive output following severe thermal stress. Although male reproductive performance proved resilient, we observed a subtle inter-generational cost: a 3.5% reduction in male offspring body weight. Our findings highlight a novel, potential adaptive role for sperm heteromorphism, demonstrating that sperm-heteromorphic insects can leverage plastic, morph-specific ejaculate tailoring to safeguard fertility against acute thermal extremes.