Dufour Sylvie, Sachs Laurent, Martin Patrick, Rousseau Karine
UMR BOREA, Biologie des Organismes et Écosystèmes Aquatiques, Muséum National d'Histoire Naturelle, Sorbonne Université, CNRS, IRD, 75005 Paris, France.
UMR PhyMA, Physiologie Moléculaire et Adaptation, Muséum National d'Histoire Naturelle, CNRS, 75005 Paris, France.
Biol Aujourdhui. 2025;219(1-2):37-50. doi: 10.1051/jbio/2025002. Epub 2025 Jul 22.
The most emblematic metamorphoses in the animal kingdom remain those of the caterpillar into a butterfly and the tadpole into a frog. However, some other vertebrates also present, at one or more steps of their biological cycle, drastic changes in their morphology, physiology and behavior, allowing them to adapt to a new environment (habitat) and way of life, and thus considered as metamorphoses. This is the case within fish, for some representatives of teleosts (the largest group among vertebrates) and of cyclostomes (the most ancient group among vertebrates). Thus, a larval (or primary) metamorphosis takes place, as for amphibians, in pleuronectiformes (e.g. flatfish), elopomorphs (e.g. eels) and also in cyclostomes (e.g. lamprey). This larval metamorphosis is controlled, in all cases, by thyroid hormones. However, this regulation is remarkably opposite, stimulatory in teleosts as in amphibians, and inhibitory in the lamprey. These opposing regulations, as well as the presence of metamorphoses only in certain groups or even certain species, suggest that the recruitment of thyroid hormones for the control of metamorphoses would have occurred repeatedly and independently during the evolution of vertebrates. The neuroendocrine control of the production of thyroid hormones during larval metamorphosis is ensured in amphibians by the stimulatory control of pituitary thyrotropin, itself under the stimulatory control of hypothalamic corticotropin-releasing hormone instead of the thyrotropin-releasing hormone classically involved in the thyrotropic control of metabolism. A similar neuroendocrine control would also occur for teleost larval metamorphosis, but investigations are yet limited. Data are still lacking concerning the neuroendocrine control of the production of thyroid hormone which exerts an inhibitory control on lamprey metamorphosis. In some amphidromous migratory fishes, a so-called secondary metamorphosis, because it occurs at the juvenile stage, allows the passage from the freshwater (river) to the seawater (ocean). These are silvering in eels and smoltification in salmons. Salmon smoltification is a transition between two phases of juvenile body growth, under the positive control of thyroid hormones, as the larval metamorphosis of amphibians and teleosts. In contrast, eel silvering marks the end of the feeding and body growth phase as well as the initiation of the reproductive phase, and is controlled by the gonadotropic axis with sex steroids. The additional involvement of other hormones, such as cortisol for larval and secondary metamorphosis and growth hormone for smoltification, has also been demonstrated in the control of vertebrate metamorphoses. Overall, the larval (primary) and secondary metamorphoses observed in various vertebrates, and the recruitment of thyroid hormones and different neuroendocrine axes for their triggering, have contributed to the evolution of complex life cycles adapted to diverse habitats.
动物王国中最具代表性的变态现象仍然是毛虫变成蝴蝶以及蝌蚪变成青蛙。然而,其他一些脊椎动物在其生物周期的一个或多个阶段,其形态、生理和行为也会发生剧烈变化,使它们能够适应新的环境(栖息地)和生活方式,因此也被视为变态。鱼类中的一些硬骨鱼(脊椎动物中最大的群体)和圆口纲动物(脊椎动物中最古老的群体)就是这种情况。因此,像两栖动物一样,鲽形目(如比目鱼)、鳗鲡目(如鳗鱼)以及圆口纲动物(如七鳃鳗)会发生幼体(或初级)变态。在所有这些情况下,幼体变态都受甲状腺激素控制。然而,这种调节却明显相反,在硬骨鱼中与在两栖动物中一样具有刺激作用,而在七鳃鳗中则具有抑制作用。这些相反的调节方式,以及仅在某些群体甚至某些物种中存在变态现象,表明在脊椎动物的进化过程中,甲状腺激素被用于控制变态现象的情况可能反复且独立地发生过。在两栖动物幼体变态过程中,垂体促甲状腺激素的刺激控制确保了甲状腺激素产生的神经内分泌控制,而垂体促甲状腺激素本身又受到下丘脑促肾上腺皮质激素释放激素的刺激控制,而非经典的参与甲状腺对新陈代谢控制的促甲状腺激素释放激素。硬骨鱼幼体变态也会发生类似的神经内分泌控制,但相关研究仍然有限。关于对七鳃鳗变态起抑制作用的甲状腺激素产生的神经内分泌控制,目前仍缺乏相关数据。在一些降海洄游鱼类中,会发生一种所谓的次级变态,因为它发生在幼鱼阶段,使鱼能够从淡水(河流)进入海水(海洋)。这在鳗鱼中是银化现象,在鲑鱼中是洄游性幼鱼的形态变化。鲑鱼的洄游性幼鱼形态变化是幼鱼身体生长两个阶段之间的转变,如同两栖动物和硬骨鱼的幼体变态一样,受甲状腺激素的正向控制。相比之下,鳗鱼的银化标志着摄食和身体生长阶段的结束以及生殖阶段的开始,并且受性腺轴与性类固醇的控制。在脊椎动物变态的控制过程中,还证明了其他激素的额外参与,如皮质醇参与幼体和次级变态,生长激素参与洄游性幼鱼的形态变化。总体而言,在各种脊椎动物中观察到的幼体(初级)和次级变态,以及为引发变态而招募甲状腺激素和不同的神经内分泌轴,都促进了适应不同栖息地的复杂生命周期的进化。