Climate change is affecting biodiversity, but proximate drivers remain poorly understood. Here, we examine how experimental heatwaves impact on reproduction in an insect system. Male sensitivity to heat is recognised in endotherms, but ectotherms have received limited attention, despite comprising most of biodiversity and being more influenced by temperature variation. Using a flour beetle model system, we find that heatwave conditions (5 to 7 °C above optimum for 5 days) damaged male, but not female, reproduction. Heatwaves reduce male fertility and sperm competitiveness, and successive heatwaves almost sterilise males. Heatwaves reduce sperm production, viability, and migration through the female. Inseminated sperm in female storage are also damaged by heatwaves. Finally, we discover transgenerational impacts, with reduced reproductive potential and lifespan of offspring when fathered by males, or sperm, that had experienced heatwaves. This male reproductive damage under heatwave conditions provides one potential driver behind biodiversity declines and contractions through global warming.

With climate change creating a more volatile atmosphere, heatwaves that create thermal stress for living systems will become stronger and more frequent. Using the flour beetleTribolium castaneum, we measure the impacts of thermal stress from experimental heatwaves in the laboratory on reproduction and survival across different insect life stages, and the extent and pace of any recovery. We exposed larvae, pupae, juvenile and mature adult male beetles to 5-day periods of heat stress where temperatures were maintained at either 40°C or 42°C, a few degrees above the 35°C optimum for this species' population productivity, and then measured survival and reproduction compared with controls at 30°C. Mortality due to thermal stress was greatest among juvenile life stages. Male reproductive function was specifically damaged by high temperatures, especially if experienced through pupal or immature life stages when complete sterility was shown at reproductive maturity; larval exposure did not damage adult male fertility. High temperatures impaired testis development and the production of viable sperm, with damage being strongest when experienced during pupal or juvenile adult stages. Despite this disruption, males recovered from heat stress and, depending on the stage of exposure, testis size, sperm production and fertility returned to normal 15–28 days after exposure. Our experiments reveal how thermal stress from heatwave conditions could impact on insect survival and reproduction across different life stages, and the potential and timescales of recovery.

It is the differences between sperm and eggs that fundamentally underpin the differences between the sexes within reproduction. For males, it is theorized that widespread sperm competition leads to selection for investment in sperm numbers, achieved by minimizing sperm size within limited resources for spermatogenesis in the testis. Here, we empirically examine how sperm competition shapes sperm size, after more than 77 generations of experimental selection of replicate lines under either high or low sperm competition intensities in the promiscuous flour beetle Tribolium castaneum. After this experimental evolution, populations had diverged significantly in their sperm competitiveness, with sperm in ejaculates from males evolving under high sperm competition intensities gaining 20% greater paternity than sperm in ejaculates from males that had evolved under low sperm competition intensity. Males did not change their relative investment into sperm production following this experimental evolution, showing no difference in testis sizes between high and low intensity regimes. However, the more competitive males from high sperm competition intensity regimes had evolved significantly longer sperm and, across six independently selected lines, there was a significant association between the degree of divergence in sperm length and average sperm competitiveness. To determine whether such sperm elongation is costly, we used dietary restriction experiments, and revealed that protein-restricted males produced significantly shorter sperm. Our findings therefore demonstrate that sperm competition intensity can exert positive directional selection on sperm size, despite this being a costly reproductive trait.

Rising and more variable global temperatures pose a challenge for biodiversity, with reproduction and fertility being especially sensitive to heat. Here, we assessed the potential for thermal adaptation in sperm and egg function using Tribolium flour beetles, a warm-temperate-tropical insect model. Following temperature increases through adult development, we found opposing gamete responses, with males producing shorter sperm and females laying larger eggs. Importantly, this gamete phenotypic plasticity was adaptive: thermal translocation experiments showed that both sperm and eggs produced in warmer conditions had superior reproductive performance in warmer environments, and vice versa for cooler production conditions and reproductive environments. In warmer environments, gamete plasticity enabled males to double their reproductive success, and females could increase offspring production by one-third. Our results reveal exciting potential for sensitive but vital traits within reproduction to handle increasing and more variable thermal regimes in the natural environment.