Neuroendocrinology of Fish Metamorphosis and Puberty: Evolutionary and Ecophysiological Perspectives

Metamorphosis and puberty are two major events of the postembryonic development in Vertebrates. Based on some examples from fish species, we review the definition, role and regulation of these events, analyze their common and different features, as well as their impact on the evolution and diversity of life cycles. The term of puberty, firstly defined in humans, has been subsequently extended to the first acquisition of the capacity to reproduce in all mammalian and non-mammalian vertebrates as well as in invertebrates. By definition, puberty occurs only once in the life cycle. However, some similarities may be found with other events, such as annual re-activation of the reproductive function in seasonal breeders or sex-change in adults, as observed in some fish species. Metamorphosis allows the transition from one developmental stage in a specific environment to the next stage in a different environment, and includes a migration between the two habitats. Metamorphosis corresponds to drastic changes in body shape, physiology and behavior, and, unlike puberty, is encountered only in some phyla/species. In Vertebrates, the most described metamorphosis is the transformation in Amphibians of the aquatic larva (tadpole) into the terrestrial juvenile. Larval metamorphosis is also encountered in some other Vertebrates, such as lampreys and some teleosts (Elopomorphes and Pleuronectiformes). Less drastic morphological, physiological and behavioral changes occur in juveniles of some migratory teleosts. This is the case of smoltification in salmons and silvering in eels, which are referred to as ”secondary metamorphoses”. Investigations on the regulation of puberty and metamorphoses in Vertebrates reveal the crucial roles of the neuroendocrine axes. In all Vertebrates, puberty is triggered by the activation of the gonadotropic axis, constituted of brain neuropeptide (gonadotropin-releasing hormone, GnRH), pituitary glycoprotein hormones (gonadotropins: luteinizing hormone, LH and follicle stimulating hormone, FSH) and gonadal steroids. Sex steroids induce the morpho-physiological and behavioral transformations characteristic of puberty. Metamorphosis in Amphibians is triggered by the thyrotropic axis, constituted of brain neuropeptide corticotropin-releasing hormone (CRH), instead of thyrotropin-releasing hormone, (TRH), pituitary glycoprotein hormone (thyrotropin, TSH) and thyroid hormones (TH: thyroxine, T4 and triiodothyronine, T3), which play a key-role in the induction of morpho-physiological and behavioral changes. A similar control is suggested for larval metamorphosis in teleosts. Studies on smoltification also indicate an important role of thyroid hormones in secondary metamorphoses in teleosts, even though other hormones such as growth hormone (GH) and corticosteroids may be of prime importance. In contrast, recent investigations in the eel reveal that the gonadotropic axis, and ultimately sex steroids would be the major triggering control of silvering. The similarities of the morpho-physiological and behavioral changes between the two species indicate remarkable evolutionary convergences in the morphogenetic roles and target tissues of TH and sex steroids for the induction of secondary metamorphoses. In all cases, the possible synergistic role of cortisol is highlighted. Comparison of puberty and metamorphosis may also favor our understanding of the internal and environmental triggering signals of these postembryonic developmental events. In teleosts, the large plasticity in the occurrence and timing of metamorphosis and puberty, which contributes to the high diversity of fish life cycles, may provide new and relevant models to such investigations.