Teleost Metamorphosis: The Role of Thyroid Hormone

Abstract

In most teleosts, metamorphosis encompasses a dramatic post-natal developmental process where the free-swimming larvae undergo a series of morphological, cellular and physiological changes that enable the larvae to become a fully formed, albeit sexually immature, juvenile fish. In all teleosts studied to date thyroid hormones (TH) drive metamorphosis, being the necessary and sufficient factors behind this developmental transition. During metamorphosis, negative regulation of thyrotropin by thyroxine (T4) is relaxed allowing higher whole-body levels of T4 that enable specific responses at the tissue/cellular level. Higher local thyroid cellular signaling leads to cell-specific responses that bring about localized developmental events. TH orchestrate in a spatial-temporal manner all local developmental changes so that in the end a fully functional organism arises. In bilateral teleost species, the most evident metamorphic morphological change underlies a transition to a more streamlined body. In the pleuronectiform lineage (flatfishes), these metamorphic morphological changes are more dramatic. The most evident is the migration of one eye to the opposite side of the head and the symmetric pelagic larva development into an asymmetric benthic juvenile. This transition encompasses a dramatic loss of the embryonic derived dorsal-ventral and left-right axis. The embryonic dorsal-ventral axis becomes the left-right axis, whereas the embryonic left-right axis becomes, irrespectively, the dorsal-ventral axis of the juvenile animal. This event is an unparalleled morphological change in vertebrate development and a remarkable display of the capacity of TH-signaling in shaping adaptation and evolution in teleosts. Notwithstanding all this knowledge, there are still fundamental questions in teleost metamorphosis left unanswered: how the central regulation of metamorphosis is achieved and the neuroendocrine network involved is unclear; the detailed cellular and molecular events that give rise to the developmental processes occurring during teleost metamorphosis are still mostly unknown. Also in flatfish, comparatively little is still known about the developmental processes behind asymmetric development. This review summarizes the current knowledge on teleost metamorphosis and explores the gaps that still need to be challenged.

The Role of the Thyroid Axis in Fish

“…Fish metamorphosis refers to the dramatic changes seen in flatfish, lampreys, and eels, but also be applied to any irreversible post-embryonic developmental event that affects multiple physiological or morphological traits (excluding those related to sexual maturation, reproduction, or senescence) seen in several FW and marine species (56,186). THs are key regulators of teleost metamorphosis, which involves cellular and molecular remodeling that lead to developmental changes (16). Typically, thyroid activity is low during pre-metamorphosis (i.e., low TH levels, with reduced DIO and TR expression), increases during the metamorphic event, peaks during developmental changes (metamorphic climax), and decreases to pre-metamorphic levels (16,186).…”

“…THs are key regulators of teleost metamorphosis, which involves cellular and molecular remodeling that lead to developmental changes (16). Typically, thyroid activity is low during pre-metamorphosis (i.e., low TH levels, with reduced DIO and TR expression), increases during the metamorphic event, peaks during developmental changes (metamorphic climax), and decreases to pre-metamorphic levels (16,186).…”

“…Later studies compared the structure/location of the gland in different fish species [e.g., gill tissue in rainbow trout ( Oncorhynchus mykiss ) ( 12 )], and uncovered the role of the thyroid as a regulator of metabolic activity ( 13 ), and the role of the pituitary [sailfin molly ( Poecilia latipinna ) ( 14 )] and hypothalamus [African lungfish ( Protopterus annectens ) ( 15 )] in the regulation of thyroid function. Despite over a century of research, our knowledge of the physiology of the fish thyroid is still incomplete, and previously published reviews focus on teleosts and on specific functions of the thyroid [e.g., metamorphosis ( 16 ); reproduction ( 17 )].…”

Functional morphogenesis from embryos to adults: Late development shapes trophic niche in coral reef damselfishes

“…Although the larvae‐to‐juvenile transition in fishes frequently involves metamorphosis (i.e., rapid anatomical reorganization), in many species this transformation is more protracted, but thyroid hormone (TH) regulates both metamorphosis and metamorphosis‐like processes in large numbers of vertebrates (Das et al, ; Hu et al, ; Laudet, ; McMenamin & Parichy, ; Paris et al, ; Wojcicka, Bassett, & Williams, ) and sharp increases in TH production are known to accompany the larvae‐to‐juvenile transition in multiple fish species (Campinho, ; Chang et al, ; McMenamin & Parichy, ). TH is also known to play an important role in skull morphogenesis throughout development and to have large effects on the growth and remodeling of both endochondral and intramembranous bone (Bassett & Williams, ; Hanken & Hall, ; Harvey et al, ; Hirano, Akita, & Fujii, ; Waung, Bassett, & Williams, ; Wojcicka et al, ).…”

Hierarchical analysis of ontogenetic time to describe heterochrony and taxonomy of developmental stages

“…In other words, depending on the species, the hatching larva can either be already well developed (with an open mouth to feed, certain fins developed) or rather less developed (mouth closed, large yolk sac, no fins developed). Campinho 50 stressed that "teleost metamorphosis is still an understudied developmental event. " Thyroid hormone signaling is nevertheless a universal feature.…”