Loss of behavioral stress response in blind cavefish reduces energy expenditure

Zool Res. 2023 Jul 18;44(4):678-692. doi: 10.24272/j.issn.2095-8137.2022.354.

Abstract

The stress response is essential for animal self-defense and survival. However, species may exhibit stress response variation depending on their specific environmental and selection pressures. Blind cavefish dwell in cave environments, which differ markedly in stressors and resource availability compared to surface aquatic environments. However, whether blind cavefish exhibit differences in stress response as an adaptation to their cave environments remains unclear. Here, we investigated differences in stress response in six closely related Triplophysa species, including three blind cavefish (T. longibarbata, T. jiarongensis, and T. rosa) and three normal-sighted river fish (T. nasobarbatula, T. dongsaiensis, and T. bleekeri). Results showed that blind cavefish exhibited a range of distinct behavioral responses compared to sighted river fish, including greater levels of activity, shorter duration of freezing, absence of erratic movements or thrashing behavior, and opposite behavioral trends over time. Furthermore, the cavefish species demonstrated attenuated increases in metabolic rate in response to stressors related to novel environments. Cave-dwelling T. rosa also exhibited lower basal hypothalamic-pituitary-inter-renal (HPI) axis-related gene expression levels and stress hormone concentrations compared to river-dwelling T. bleekeri. These results suggest that blind cavefish may have lost their behavioral stress response, potentially mediated by a reduction in basal activity of the HPI axis, thus enabling the conservation of energy by reducing unnecessary expenditure in energy-limited caves.

应激反应对于动物的自卫和生存至关重要,在不同的物种或种群间可能存在差异,与环境特征和选择压力有关。洞穴水环境在应激源和食物资源等方面与地表水环境差异明显。那么,洞穴鱼是否会有独特的应激反应呢?该研究选用高原鳅属(Triplophysa)的六种鱼为对象,包括三种眼退化的典型洞穴鱼:长须盲高原鳅(T. longibarbata)、佳荣盲高原鳅(T. jiarongensis)和玫瑰高原鳅(T. rosa),和三种眼发育正常的地表鱼:鼻须高原鳅(T. nasobarbatula)、洞腮高原鳅(T. dongsaiensis)和贝氏高原鳅(T. bleekeri),以研究洞穴鱼和地表鱼间应激反应的差异。结果发现,与地表鱼相比,进入新环境后洞穴鱼的应激反应明显不同,其活跃性较高,冻结性较低,没有不规则运动和剧烈扭动行为,且行为指标随时间的变化趋势发生颠转,相对代谢率和相对应激后过量耗氧也较低。此外,洞穴鱼玫瑰高原鳅的下丘脑-垂体-肾间质轴的关键基因基础表达量和应激激素基础水平均比地表鱼贝氏高原鳅低。结果表明,洞穴鱼失去了新环境诱导的应激行为反应,可能由HPI轴的基础活性减弱介导,这有利于在资源有限的洞穴环境中节约应激反应相关的能量消耗。.

Keywords: Behavior; Cavefish; Metabolic rate; Stress responses.

MeSH terms

  • Adaptation, Physiological
  • Animals
  • Biological Evolution
  • Caves
  • Characidae* / physiology
  • Cypriniformes* / genetics
  • Energy Metabolism

Grants and funding

This study was supported by the National Natural Science Foundation of China (32070438)