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

这个探索项目将采用新颖的方法，利用水生昆虫来研究从呼吸水到呼吸空气的转变所带来的生理挑战。水生昆虫支持着宝贵的淡水生态系统和渔业，但它们极易受到水质变化的影响，因此了解它们的生理学对成功的环境管理至关重要。我们目前对与在水和空气之间移动有关的呼吸挑战的理解来自于研究水生动物，特别是脊椎动物，如何适应它们在陆地上的形态和生理功能。从这个角度来看，水呼吸是祖先的状态，空气呼吸是衍生的状态。然而，这些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在水中的功能。虽然所有的成虫都是呼吸空气的，但有九目昆虫的代表已经进化成两栖动物，在它们生命周期的幼年时期，它们是水生的若虫或幼虫，拥有鳃并呼吸水。这些昆虫类群提供了一个绝佳的机会来研究与水生呼吸有关的适应进化，并确定环境限制是否导致鳃昆虫趋同于与其他水生动物相似的呼吸生理，或者它们的陆地祖先的系统发育限制是否导致了与空气呼吸动物相似的呼吸生理。昆虫重返水中的生理后果尚不清楚，但有诱人的证据表明，呼吸水的若虫体内的二氧化碳水平升高，通常与呼吸空气有关，这一观察结果无法用目前的教科书教条来解释。此外，我们对使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。我的研究项目旨在识别和比较水呼吸幼虫与空气呼吸成虫的呼吸和酸碱策略，并探索它们从水到陆地的快速过渡过程中发生的生理变化。我将使用一系列的技术，包括呼吸测量、形态测量和组织学，来揭示水生和陆地生命阶段调节其内部氧气和二氧化碳水平以及酸碱平衡的不同策略。因此，该研究项目解决了我们对昆虫生理学理解的一个基本空白，并提供了从水到陆地过渡的呼吸适应进化的见解。

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.