Understanding heatwave damage through reproduction in insect systems

最近的长期实地调查显示，昆虫数量出现了“灾难性”下降，即使是在受栖息地丧失和杀虫剂保护的地区。气候变化是可能的原因，但我们对全球变暖下生物多样性丧失的直接驱动因素仍然“令人不安的有限知识”（Cahill等人，2013年）。该项目将研究一个关键的驱动因素，通过测试繁殖过程中异常的热敏感性可以解释为什么昆虫种群正在下降的假设。在气候变化下，热浪等极端条件变得更加频繁和严重，这种热变化可能比平均变化对生物多样性的损害更大。雄性生殖对热的敏感性在恒温动物中是众所周知的，但外温动物很少受到关注，尽管包括大多数生物多样性，并直接受到热环境的影响。在最近的一个NERC项目中，我们在赤拟谷盗模型中发现，繁殖对变暖异常敏感：高于种群最佳温度5- 7 ℃的热浪持续5天会损害雄性生育力和精子功能，第二次热浪几乎完全使雄性不育（Sales et al. 2018：Experimental heatwaves compromise sperm function and cause transgenerational damage in a model insect.）。Nature Comms）。相比之下，雌性生殖对热有弹性，但在雌性储存中由于精子的热损伤而受到损害。除了这些直接影响，我们还发现，如果父亲或受精精子对后代的生殖健康和寿命造成的跨代损害不太明显，（在雌性储存中）经历过热浪。因为a）繁殖对种群生存至关重要，B）热浪变得越来越频繁和严重，c）地球上大多数物种都是令人担忧的昆虫，我们建议测量实验热浪如何影响：1）热带和温带昆虫物种的繁殖; 2）不同生命阶段的热脆弱性以及任何损害是否是永久性的; 3）热浪对种群恢复力，生存力和灭绝的影响。正如最近的专家评论所建议的那样，我们将通过三个互补的工作包进行系统的实验来解决这些重要问题：1）测量不同昆虫物种的生殖敏感性。基于我们从赤拟谷盗的研究结果，我们将研究热浪如何影响九个温带和热带昆虫模型系统的性别特异性和配子特异性生殖。我们选择的物种代表了一些主要的目的和生态，我们从经验中知道，这些物种在受控的实验室实验中很容易繁殖。当温度超过种群繁殖期间的平均当地温度5 ℃，持续5天时，将模拟热浪条件。2）测量不同生命阶段对热浪条件的敏感性。对赤拟谷盗的实验表明，热浪条件（5- 7 ℃，持续5天）使成熟雄性的生殖产量和精子减少了一半。新的试验数据现在显示，在同样的条件下，未成熟的雄性会完全不育，而蛹的死亡率很高。因此，我们将在甲虫和蛾模型中测量胚胎、幼虫、蛹和成虫生命阶段对热浪的相对脆弱性，并评估对两性生存、发育、生殖和代际效应的影响，以及损害是否是永久性的。使用Tribolium甲虫和Plodia蛾模型，这些模型已被证明对跟踪长期，整个种群的影响具有价值，并结合有关阶段敏感性的信息2）随着项目的进展，我们将测量和建模热浪如何导致长期下降和复制种群的灭绝，更广泛地了解极端天气如何影响昆虫的生物多样性。

Recent long-term field surveys have revealed 'catastrophic' declines in insects, even in areas protected from habitat loss and pesticides. Climate change is the likely cause, but we still have 'disturbingly limited knowledge' about proximate drivers of biodiversity loss under global warming (Cahill et al 2013). This project will examine one key driver, by testing the hypothesis that exceptional thermal sensitivities within reproduction can explain why insect populations are declining. Under climate change, extreme conditions such as heatwaves are getting more frequent and severe, and such thermal variation may damage biodiversity more than average change. Male reproductive sensitivity to heat is well known in endotherms, but ectotherms have received scant attention, despite comprising most of biodiversity, and being directly affected by the thermal environment. In a recent NERC project, we identified in our Tribolium beetle model that reproduction is exceptionally sensitive to warming: heatwaves at 5-7oC above the population optimum for 5 days damage male fertility and sperm function, and a second heatwave almost completely sterilises males (Sales et al. 2018: Experimental heatwaves compromise sperm function and cause transgenerational damage in a model insect. Nature Comms). Female reproduction, by contrast, is resilient to heat, but is compromised via thermal damage to sperm in female storage. In addition to these direct impacts, we also revealed less obvious transgenerational damage to reproductive fitness and lifespan of offspring if fathers or fertilising sperm (in female storage) had experienced heatwaves.Because a) reproduction is essential for population viability, b) heatwaves are becoming more frequent and severe, and c) most species on Earth are insects in worrying decline, we propose to measure how experimental heatwaves impact on: 1) reproduction across a suite of tropical and temperate insect species; 2) thermal vulnerabilities at different life stages and whether any damage is permanent; and 3) heatwave impacts on population resilience, viability and extinction. As proposed by recent expert reviews, we will tackle these important questions using systematic experiments across three complementary work packages:1) MEASURE REPRODUCTIVE SENSITIVITIES IN DIFFERENT INSECT SPECIES. Building on our results from Tribolium beetles, we will investigate how heatwaves impact on sex-specific and gamete-specific reproduction across nine temperate and tropical insect model systems. We have chosen species that represent some major Orders and ecologies, and which we know from experience will breed readily within controlled lab experiments. Heatwave conditions will be simulated where temperatures exceed the average local temperature during breeding for the population by >5oC for 5 days.2) MEASURE DIFFERENT LIFE STAGE SENSITIVITIES TO HEATWAVE CONDITIONS. Experimental work with Tribolium beetles revealed that heatwave conditions (5-7oC above the optimum for 5 days) halved the reproductive output of mature males and their sperm. New pilot data now reveal that immature males become completely sterile under the same conditions, and pupae suffer high mortality. We will therefore measure the relative vulnerabilities of embryonic, larval, pupal and adult life stages to heatwaves in beetle and moth models, and assess impacts on survival, development, reproduction and transgenerational effects in both sexes, and whether the damage is permanent.3) MEASURE HEATWAVE IMPACTS ON INSECT POPULATION VIABILITY. Using Tribolium beetle and Plodia moth models which have proven value for the tracking of longer-term, whole-population impacts, and incorporating information about stage sensitivities from 2) as the project progresses, we will measure and model how heatwaves cause longer-term declines and extinctions in replicated populations, gaining broader insight into how extreme weather across life stages influences insect biodiversity.