Kirschman Lucas J, McCue Marshall D, Boyles Justin G, Warne Robin W
Department of Zoology, Southern Illinois University, Carbondale, IL 62901, USA
Department of Biological Sciences, St. Mary's University, San Antonio, TX 78228, USA.
J Exp Biol. 2017 Sep 15;220(Pt 18):3391-3397. doi: 10.1242/jeb.164830. Epub 2017 Jul 20.
Variation in environmental conditions during larval life stages can shape development during critical windows and have lasting effects on the adult organism. Changes in larval developmental rates in response to environmental conditions, for example, can trade off with growth to determine body size and condition at metamorphosis, which can affect adult survival and fecundity. However, it is unclear how use of energy and nutrients shape trade-offs across life-stage transitions because no studies have quantified these costs of larval development and metamorphosis. We used an experimental approach to manipulate physiological stress in larval amphibians, along with respirometry and C-breath testing to quantify the energetic and nutritional costs of development and metamorphosis. Central to larval developmental responses to environmental conditions is the hypothalamic-pituitary-adrenal/interrenal (HPA/I) axis, which regulates development, as well as energy homeostasis and stress responses across many taxa. Given these pleiotropic effects of HPA/I activity, manipulation of the HPA/I axis may provide insight into costs of metamorphosis. We measured the energetic and nutritional costs across the entire larval period and metamorphosis in a larval amphibian exposed to exogenous glucocorticoid (GC) hormones - the primary hormone secreted by the HPA/I axis. We measured metabolic rates and dry mass across larval ontogeny, and quantified lipid stores and nutrient oxidation via C-breath testing during metamorphosis, under control and GC-exposed conditions. Changes in dry mass match metamorphic states previously reported in the literature, but dynamics of metabolism were influenced by the transition from aquatic to terrestrial respiration. GC-treated larvae had lower dry mass, decreased fat stores and higher oxygen consumption during stages where controls were conserving energy. GC-treated larvae also oxidized greater amounts of C-labelled protein stores. These results provide evidence for a proximate cause of the physiological trade-off between larval growth and development, and provide insight into the energetic and nutrient costs that shape fitness trade-offs across life stages.
幼体生命阶段环境条件的变化会在关键窗口期影响发育，并对成年生物体产生持久影响。例如，幼体发育速率对环境条件的变化会与生长相互权衡，从而决定变态时的体型和状况，进而影响成年后的生存和繁殖力。然而，目前尚不清楚能量和营养物质的利用如何在生命阶段转换中形成权衡，因为尚无研究对幼体发育和变态的这些成本进行量化。我们采用实验方法来操纵幼体两栖动物的生理应激，并通过呼吸测量法和碳呼吸测试来量化发育和变态的能量及营养成本。幼体对环境条件的发育反应的核心是下丘脑 - 垂体 - 肾上腺/肾间（HPA/I）轴，该轴调节发育以及许多分类群的能量稳态和应激反应。鉴于HPA/I活动的这些多效性作用，操纵HPA/I轴可能有助于深入了解变态的成本。我们测量了暴露于外源性糖皮质激素（GC）激素（HPA/I轴分泌的主要激素）的幼体两栖动物在整个幼体期和变态过程中的能量和营养成本。我们在对照和GC暴露条件下，测量了幼体个体发育过程中的代谢率和干重，并通过变态过程中的碳呼吸测试量化了脂质储存和营养物质氧化。干重的变化与先前文献报道的变态状态相符，但代谢动态受从水生呼吸向陆生呼吸转变的影响。在对照幼体保存能量的阶段，经GC处理的幼体干重较低、脂肪储存减少且耗氧量较高。经GC处理的幼体还氧化了更多的碳标记蛋白质储存。这些结果为幼体生长和发育之间生理权衡的直接原因提供了证据，并深入了解了影响生命阶段适应性权衡的能量和营养成本。
