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.

SUMMARY 19"Reproduction through sex carries substantial costs, mainly because only half of sexual 20" adults produce offspring 1 . It has been theorised that these costs could be countered if 21" sex allows sexual selection to clear the universal fitness constraint of mutation load 2-4 . 22"Under sexual selection, competition between (usually) males, and mate choice by 23" (usually) females create important intraspecific filters for reproductive success, so that 24" only a subset of males gains paternity. If reproductive success under sexual selection is 25" dependent on individual condition, which depends on mutation load, then sexually 26" selected filtering through 'genic capture' 5 could offset the costs of sex because it 27" provides genetic benefits to populations. Here, we test this theory experimentally by 28" comparing whether populations with histories of strong versus weak sexual selection 29" purge mutation load and resist extinction differently. After evolving replicate 30" populations of the flour beetle Tribolium castaneum for ~7 years under conditions that 31" differed solely in the strengths of sexual selection, we revealed mutation load using 32" inbreeding. Lineages from populations that had previously experienced strong sexual 33" selection were resilient to extinction and maintained fitness under inbreeding, with 34" some families continuing to survive after 20 generations of sib × sib mating. By contrast, 35" lineages derived from populations that experienced weak or non-existent sexual 36" selection showed rapid fitness declines under inbreeding, and all were extinct after 37" generation 10. Multiple mutations across the genome with individually small effects can 38" be difficult to clear, yet sum to a significant fitness load; our findings reveal that sexual 39" selection reduces this load, improving population viability in the face of genetic stress. 40"3"Sexual selection is a widespread evolutionary force giving rise to a striking diversity of sights, 41" sounds and smells that filter reproductive success away from less competitive or attractive 42" individuals, frequently at the expense of survival 6 . Sexual selection will operate to varying 43" degrees whenever sexual reproduction exists, and its significance as a potent force 44" profoundly influencing reproductive fitness of individuals is long established 6 . In contrast, 45"limited empirical work has been directed at measuring the consequences of sexual selection 46" for the fitness of populations. This lack of attention is surprising for two reasons: first, 47"because population viability is vital for biodiversity maintenance and ecosystem stability, 48"especially under modern anthropogenic stress 7,8 ; and second, because it is predicted that the allows sexual selection to operate, reducing the universal handicap of mutation load 3,4 .51" 52"Population or lineage health will always suffer at some level from mutation load -the 53"difference in fitness betw...

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.

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