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. variegatadisplays 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 inB. variegata; moreover, the development of all elements of the axial and limb skeleton is affected by THs. The more accentuated hormonal control of skeletogenesis inB. variegatademonstrates 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.
Highlights
The amphibian life cycle consisting of water-dwelling larvae and terrestrial adults is unique among vertebrate animals
The degree of variability in the timing and sequence of cranial bone appearance is comparable with that found in B. orientalis (Hanken and Hall, 1988a)
On a large-scale comparison within anurans with a biphasic life history, B. variegata displays a rather typical cranial ossification sequence, with the frontoparietal, parasphenoid, and exoccipital arising first and dentary, quadratojugal, and pterygoid are among the last bones to arise (Trueb and Alberch, 1985; Weisbecker and Mitgutsch, 2010)
Summary
The amphibian life cycle consisting of water-dwelling larvae and terrestrial adults is unique among vertebrate animals. Caecilians, a very specialized group of fossorial or aquatic amphibians, display only moderate morphological reorganization limited mainly to the loss of gills and rebuilding of the palatal region of the skull and hyobranchium (Wake, 1989; Reiss, 1996). Urodelans retain the overall larval body plan, undergo profound changes in the external and internal morphology. Resorption of the external gills and caudal fins is accompanied by changes in the skull structure: larval provisory bones disappear, and adult bones appear (Rose, 2003). Metamorphic transformation is extremely profound and results in the remodeling of the body plan: fish-like aquatic larvae transform into tailless terrestrial animals adapted to jumping. The larval cartilaginous jaw apparatus is replaced by an adult bony apparatus, suspensorium undergoes rebuilding, and the jaw joint shifts posteriorly (Rocek, 2003)
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