Increasing Hormonal Control of Skeletal Development: An Evolutionary Trend in Amphibians

Abstract

The biphasic life history of amphibians includes metamorphosis, a complex developmental event that involves drastic changes in the morphology, physiology and biochemistry accompanying the transition from the larval to adult stage of development. Thyroid hormones (THs) are widely known to orchestrate this remodeling and, in particular, to mediate the development of the bony skeleton, which is a model system in evolutionary morphological studies of amphibians. Detailed experimental studies of the role of THs in the craniogenesis of diverse urodelan amphibians revealed that (i) these hormones affect both the timing and sequence of bone formation, (ii) TH involvement increases in parallel with the increase in divergence between larval and adult skull morphology, and (iii) among urodelans, TH-involvement in skull development changes from a minimum in basal salamanders (Hynobiidae) to the most pronounced in derived ones (Salamandridae and Plethodontidae). Given the increasing regulatory function of THs in urodelan evolution, we hypothesized a stronger involvement of THs in the control of skeletogenesis in anurans with their most complex and dramatic metamorphosis among all amphibians. Our experimental study of skeletal development in the hypo- and hyperthyroid yellow-bellied toad (Bombina variegata: Bombinatoridae) supports the greater involvement of THs in the mediation of all stages of anuran cranial and postcranial bones formation. Similar to urodelans, B. variegata displays enhancing TH involvement in the development of cranial bones that arise during larval ontogeny: while the hormonal impact on early larval ossifications is minimal, the skull bones forming during metamorphosis are strictly TH-inducible. However, in contrast to urodelans, all cranial bones, including the earliest to form, are TH-dependent in B. variegata; moreover, the development of all elements of the axial and limb skeleton is affected by THs. The more accentuated hormonal control of skeletogenesis in B. variegata demonstrates the advanced regulatory and inductive function of THs in the orchestration of anuran metamorphosis. Based on these findings, we discuss (i) changes in THs function in amphibian evolution and (ii) the role of THs in the evolution of life histories in amphibians.

Direct development of the catfish pectoral fin: An alternative pectoral fin pattern of teleosts

“…Furthermore, in the limb development of the salamanders (eg, Hynobiidae) displaying the most primitive ontogeny pattern among the recent tetrapods, TH plays a minor role increasing in more derived taxa of amphibians (Anura). [64][65][66] These facts suggest that TH regulation of the pectoral fin development in fishes is an advanced feature, while a weak hormonal participation is a basal trait inherent for the deep common ancestor.…”

“…In the basal ray‐finned fishes, such as bichir Polypterus sp., American paddlefish Polyodon spatula , and sturgeons Acipenser sp., the pectoral fin skeleton develops early, before the foraging onset and disappearance of the larval fin fold, 4,60‐63 and likely is not associated with the thyroid hormone increase, if the latter is present. Furthermore, in the limb development of the salamanders (eg, Hynobiidae) displaying the most primitive ontogeny pattern among the recent tetrapods, TH plays a minor role increasing in more derived taxa of amphibians (Anura) 64‐66 . These facts suggest that TH regulation of the pectoral fin development in fishes is an advanced feature, while a weak hormonal participation is a basal trait inherent for the deep common ancestor.…”

The salamander limb: a perfect model to understand imperfect integration during skeletal regeneration

“…The levels of these hormones increase closer to metamorphosis and reach their peaks at the height of the process, after which TH concentrations decrease to basal levels similar to the ones observed in larval stages ( Alberch et al, 1986 ; Larras-Regard et al, 1981 ). A connection between TH and the skeleton has been shown in salamanders, particularly for the skull ( Rose, 2021 ; Vassilieva and Smirnov, 2021 ); however, evidence for the appendicular skeleton remains scarce. To date, most of it comes from the facultative paedomorphic axolotl.…”

“…It is noteworthy that salamanders are a group that encompasses individuals with different life cycles. These variations include direct developers and paedomorphosis (facultative and obligate) and it remains unclear what influence TH has in these species and their skeletons ( Laudet, 2011 ; Vassilieva and Smirnov, 2021 ). Although some salamanders do not undergo metamorphosis, functional TH receptors are present in the axolotl ( Safi et al, 2004 ), which would render the appendicular skeleton sensitive to TH treatments.…”

Paedomorphic salamanders are larval in form and patterns of limb emergence inform life cycle evolution

“…Therefore, paleontological evidence suggests that metamorphosis evolved to be more dramatic in crown group amphibians, 42 which fits with models of increasing hormonal control of skeletal development in salamanders and frogs. 43 However, the larvae of branchiosaurs 42 and stem salamanders 44 had relatively well-developed limbs prior to metamorphosis, indicating limb emergence was ancestrally decoupled from metamorphosis.…”