Understanding heatwave damage through reproduction in insect systems

最近的长期实地调查显示，昆虫数量的“灾难性”下降，即使在免受栖息地丧失和杀虫剂影响的地区也是如此。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的了解仍然“令人不安地有限”（Cahill et al 2013）。这个项目将检验一个关键的驱动因素，通过测试一个假设，即生殖过程中异常的热敏性可以解释昆虫数量下降的原因。在气候变化的背景下，热浪等极端气候条件变得更加频繁和严重，这种热变化对生物多样性的破坏可能大于平均变化。男性对热的生殖敏感性在恒温动物中是众所周知的，但异温动物却很少受到关注，尽管它们构成了生物多样性的大部分，并直接受到热环境的影响。在最近的NERC项目中，我们在Tribolium甲虫模型中发现，繁殖对变暖异常敏感：高于种群最佳温度5-7摄氏度的热浪会损害雄性生育能力和精子功能，第二次热浪几乎会使雄性完全不育（Sales等人，2018：实验热浪会损害精子功能并导致模型昆虫的跨代损伤。）自然审稿)。相比之下，雌性生殖对热有弹性，但由于雌性储存的精子受到热损伤而受到损害。除了这些直接影响外，我们还发现，如果父亲或受精精子（在雌性储存中）经历过热浪，对后代的生殖健康和寿命的跨代损害就不那么明显了。因为a)繁殖对种群生存能力至关重要，b)热浪变得越来越频繁和严重，c)地球上的大多数物种都是昆虫，它们的数量正在令人担忧地下降，我们建议测量实验性热浪如何影响：1)一组热带和温带昆虫物种的繁殖；2)不同寿命阶段的热脆弱性以及是否存在永久性损伤；3)热浪对种群恢复力、生存力和灭绝的影响。根据最近专家评论的建议，我们将通过三个互补的工作包进行系统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。基于我们对Tribolium甲虫的研究结果，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繁殖。我们选择了代表一些主要目和生态的物种，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。将模拟热浪条件，在繁殖期间，温度超过当地平均温度50摄氏度，持续5天。2)测量不同生命阶段对热浪条件的敏感性。对Tribolium甲虫进行的实验表明，热浪条件（比最佳温度高5-7摄氏度，持续5天）会使成熟雄性和它们的精子的繁殖量减半。新的试验数据现在显示，在相同的条件下，未成熟的雄性会完全不育，蛹的死亡率很高。因此，我们将在甲虫和飞蛾模型中测量胚胎、幼虫、蛹和成虫生命阶段对热浪的相对脆弱性，并评估对两性的生存、发育、繁殖和跨代效应的影响，以及这种损害是否永久性。3)测量热浪对昆虫种群活力的影响。利用三角甲虫和倍蛾模型（已被证明对跟踪长期的、整个种群的影响有价值），并结合2)中阶段敏感性的信息，随着项目的进展，我们将测量和模拟热浪如何导致复制种群的长期下降和灭绝，从而更广泛地了解极端天气如何影响生命阶段的昆虫生物多样性。

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.