Department of Integrative Biology, University of Guelph, Guelph, ON N1G 2W1, Canada.
Department of Biological Sciences, University of Toronto Scarborough, Toronto, ON M1C 1A4, Canada.
J Exp Biol. 2022 Oct 1;225(19). doi: 10.1242/jeb.244236. Epub 2022 Oct 13.
Major ecological transitions such as the invasion of land by aquatic vertebrates may be facilitated by positive feedback between habitat choice and phenotypic plasticity. We used the amphibious fish Kryptolebias marmoratus to test the hypothesis that aquatic hypoxia, emergence behaviour and respiratory plasticity create this type of positive feedback loop that causes fish to spend increasing amounts of time on land. Terrestrially acclimated fish were more sensitive to aquatic hypoxia (emergence at higher PO2) and were less hypoxia tolerant (shorter time to loss of equilibrium) relative to water-acclimated fish, which are necessary conditions for positive feedback. Next, we tested the prediction that exposure to aquatic hypoxia causes fish to emerge frequently, reduce gill surface area, and become less hypoxia tolerant. Indeed, fish exposed to severe aquatic hypoxia spent almost 50% of the time out of water and coverage of the gill lamellae by an inter-lamellar cell mass almost doubled. Fish exposed to aquatic hypoxia that could emerge from water were also more sensitive to subsequent acute aquatic hypoxia and were less hypoxia tolerant than normoxia-exposed controls. These results are opposite those of fish that cannot escape from aquatic hypoxia and presumably arise owing to plastic changes that occur during air exposure. Together, these results indicate that emergence behaviour begets further emergence behaviour, driven by gill remodelling which reduces aquatic respiratory function. This type of positive feedback may explain how amphibious behaviour has repeatedly evolved in fishes that occupy hypoxic aquatic habitats despite the associated challenges of life on land.
主要的生态转变,如水生脊椎动物对陆地的入侵,可能会受到栖息地选择和表型可塑性之间的正反馈的促进。我们使用两栖鱼类 Kryptolebias marmoratus 来检验以下假设:即低氧环境、出水上陆行为和呼吸可塑性创造了这种正反馈循环,导致鱼类在陆地上花费越来越多的时间。与水栖鱼类相比,适应陆地环境的鱼类对水生低氧更敏感(在更高的 PO2 下出水上陆),且对低氧的耐受能力更低(失去平衡的时间更短),这是正反馈的必要条件。接下来,我们测试了这样一个预测:即暴露于低氧环境中会导致鱼类频繁出水上陆、减少鳃表面积,并降低对低氧的耐受能力。事实上,暴露于严重低氧环境中的鱼类有近 50%的时间处于离水状态,且相邻鳃片间细胞层覆盖的鳃片面积几乎增加了一倍。那些可以从水中出水上陆的鱼类,暴露于低氧环境中后,对随后的急性低氧环境更为敏感,且对低氧的耐受能力比正常氧暴露对照组更低。这些结果与那些无法逃避低氧环境的鱼类相反,这可能是由于在空气暴露期间发生的可塑性变化所致。总之,这些结果表明,出水上陆行为会引发进一步的出水上陆行为,这是由减少水生呼吸功能的鳃重塑驱动的。这种正反馈可能解释了为什么在鱼类占据低氧水生栖息地的情况下,两栖行为会反复进化,尽管在陆地上生活存在相关挑战。