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...

Between-individual variance in potential reproductive rate theoretically creates a load in reproducing populations by driving sexual selection of male traits for winning competitions, and female traits for resisting the costs of multiple mating. Here, using replicated experimental evolution under divergent operational sex ratios (OSR, 9:1 or 1:6 ♀:♂) we empirically identified the parallel reproductive fitness consequences for females and males in the promiscuous flour beetle Tribolium castaneum. Our results revealed clear evidence that sexual conflict resides within the T. castaneum mating system. After 20 generations of selection, females from female-biased OSRs became vulnerable to multiple mating, and showed a steep decrease in reproductive fitness with an increasing number of control males. In contrast, females from male-biased OSRs showed no change in reproductive fitness, irrespective of male numbers. The divergence in reproductive output was not explained by variation in female mortality. Parallel assays revealed that males also responded to experimental evolution: individuals from male-biased OSRs obtained 27% greater reproductive success across 7-day competition for females with a control male rival, compared to males from the female-biased lines. Subsequent assays suggest that these differences were not due to postcopulatory sperm competitiveness, but to precopulatory/copulatory competitive male mating behavior. K E Y W O R D S :Cost of mating, flour beetles, male mating behavior, mating strategies, polyandry, sperm competition.

The widespread phenomenon of polyandry (mating by females with multiple males) is an evolutionary puzzle, because females can sustain costs from promiscuity, whereas full fertility can be provided by a single male. Using the red flour beetle, Tribolium castaneum, we identify major fitness benefits of polyandry to females under inbreeding, when the risks of fertilization by incompatible male haplotypes are especially high. Fifteen generations after inbred populations had passed through genetic bottlenecks, we recorded increased levels of female promiscuity compared with noninbred controls, most likely due to selection from prospective fitness gains through polyandry. These data illustrate how this common mating pattern can evolve if population genetic bottlenecks increase the risks of fitness depression due to fertilization by sperm carrying genetically incompatible haplotypes.