From water-breathing nymphs to air-breathing adults: Insects as a model system to investigate the physiological challenges associated with the transition of life from water to land

从呼吸水的若虫到呼吸空气的成虫：昆虫作为模型系统来研究与生命从水到陆地的转变相关的生理挑战

• 批准号: RGPIN-2014-05794
• 负责人: Matthews, Philip
• 金额: $ 2.84万
• 依托单位: University of British Columbia
• 依托单位国家: 加拿大
• 项目类别: Discovery Grants Program - Individual
• 财政年份: 2016
• 资助国家: 加拿大
• 起止时间: 2016-01-01 至 2017-12-31
• 项目状态: 已结题
• 来源: https://www.nserc-crsng.gc.ca/ase-oro/Details-Detailles_eng.asp?id=611850
• 关键词: water; breathing; nymphs; air; adults

This Discovery Program will take the novel approach of using aquatic insects to examine the physiological challenges associated with the transition from breathing water to breathing air. Aquatic insects support valuable freshwater ecosystems and fisheries, but are highly susceptible to changes in water quality, so understanding their physiology is of crucial importance for successful environmental management. Our current understanding of the respiratory challenges associated with moving between water and air comes from studying how aquatic animals, particularly vertebrates, have adapted their morphology and physiology to function on land. From this perspective, water-breathing is the ancestral condition and air-breathing is a derived state. The insects, however, have performed this feat in reverse, adapting their terrestrial air-breathing physiology to function in water. Although all adult insects are air-breathers, representatives of nine insect orders have evolved to be developmentally amphibious, spending the juvenile proportion of their life cycle as aquatic nymphs or larvae that possess gills and breathe water. These insect groups provide an exceptional opportunity to examine the evolution of adaptations associated with aquatic respiration, and to determine whether environmental constraints have caused gill-bearing insects to converge on a respiratory physiology comparable to other aquatic animals, or whether the phylogenetic constraints of their terrestrial ancestry have resulted in a respiratory physiology similar to air-breathing animals. The physiological consequences of the insects’ return to water are not well understood, but there is tantalizing evidence that water-breathing nymphs possess elevated internal CO2 levels commonly associated with breathing air, an observation that cannot be explained by current textbook dogma. Furthermore, we know nothing of the mechanisms and physiological shifts that enable these insects, during metamorphosis, to change rapidly from breathing with gills to using an air-filled respiratory system. My research program aims to identify and compare the respiratory and acid-base strategies used by water-breathing juvenile insects with those of the air-breathing adults, and to explore the physiological changes that occur during their rapid transition from water to land. I will use a range of techniques, including respirometry, morphometry and histology, to reveal the different strategies used by the aquatic and terrestrial life stages to regulate their internal oxygen and carbon dioxide levels, and their acid-base balance. Thus, this research program addresses a fundamental gap in our understanding of insect physiology and provides insight into the evolution of respiratory adaptations underlying the transition from water to land.

这个发现计划将采取使用水生昆虫的新方法来研究从呼吸水到呼吸空气的转变所带来的生理挑战。水生昆虫支持宝贵的淡水生态系统和渔业，但对水质变化非常敏感，因此了解它们的生理机能对于成功的环境管理至关重要。我们目前对在水和空气之间移动所带来的呼吸挑战的理解来自于研究水生动物，特别是脊椎动物，如何适应它们的形态和生理机能在陆地上发挥作用。从这个角度来看，水呼吸是祖先的状态，空气呼吸是一种衍生状态。然而，昆虫却反过来完成了这一壮举，使它们的陆地呼吸生理适应了水中的功能。虽然所有的成年昆虫都是呼吸空气的，但有9个昆虫目的代表已经进化成发育中的两栖动物，它们的生命周期中的幼年部分是水生的，或者是拥有鳃和呼吸水的幼虫。这些昆虫群体提供了一个特殊的机会，以研究与水生呼吸适应的演变，并确定是否环境的限制导致鳃轴承昆虫收敛在呼吸生理学可比其他水生动物，或是否其陆地祖先的系统发育的限制导致呼吸生理学类似于呼吸空气的动物。昆虫回到水中的生理后果还没有得到很好的理解，但有诱人的证据表明，呼吸水的昆虫具有通常与呼吸空气相关的内部二氧化碳水平升高，这一观察结果无法用目前的教科书教条来解释。此外，我们对这些昆虫在变态过程中从用鳃呼吸迅速转变为使用充满空气的呼吸系统的机制和生理变化一无所知。我的研究项目旨在确定和比较呼吸水的幼年昆虫与呼吸空气的成年昆虫所使用的呼吸和酸碱策略，并探索它们从水到陆地快速过渡期间发生的生理变化。我将使用一系列的技术，包括呼吸测量，形态测量和组织学，揭示水生和陆生生命阶段使用的不同策略来调节其内部的氧气和二氧化碳水平，以及酸碱平衡。因此，这项研究计划解决了我们对昆虫生理学理解的根本差距，并提供了从水到陆地过渡的呼吸适应演变的见解。