An endocrine–based model for developmental and morphogenetic diversification in metamorphic and paedomorphic urodeles

Abstract

Mechanistic interpretations of the diversity in urodele cranial ontogenies have focused largely on the primary distinctions of metamorphic versus paedomorphic forms and obligate versus facultative expressions of the latter. These distinctions, however, do not address the underlying spectrum of developmental and morphogenetic patterns in thyroid hormone (TH)‐mediated tissues. This study integrates empirical and comparative observations on TH–mediated remodelling to formulate a new endocrine–based model to explain cranial diversification within and between metamorphic and paedomorphic urodeles. The dose–dependent remodelling induced by TH in a metamorphic urodele, the hemidactyliine plethodontid Eurycea bislineata , is compared against ontogenetic and phylogenetic variation in the same remodelling across Urodela. Immersion of Eurycea larvae in a T 4 concentration within the range of plasma T 4 levels found in natural Eurycea metamorphs results in rapid, synchronous, and complete metamorphic tissue responses as in natural plethodontid development. In contrast, lower doses produce gradual, incomplete remodelling patterns that bear greater resemblance to nonplethodontid development. A large proportion of remodelling events shows a strong correspondence between their sensitivity to TH in Eurycea and both their range of occurrence and developmental sequence in nonplethodontids. Also, the morphogenesis exhibited by certain tissues at low TH, although aberrant for plethodontids, is similar to natural development in nonplethodontids. These findings suggest that the widespread dissociation evinced by urodele cranial ontogenies may owe more to variable thyroid activity than previously realized. In particular, the abruptly metamorphic ontogeny of plethodontids and the varying degrees of metamorphic remodelling exhibited by facultative and obligate paedomorphs would seem to be explained more parsimoniously by specific changes in the profile of TH activity than by independent changes in individual tissue sensitivities. The corollary, that tissue sensitivity is largely conserved in urodeles, raises important implications for understanding character evolution, homology, and dissociation in metamorphic systems.