Turning off metamorphosis: Thyroid hormone deregulation in the evolution of obligately paedomorphic salamanders

Amphibian metamorphosis is a dramatic thyroid hormone (TH) mediated process involving the transformation of aquatic larvae into more-terrestrial adults. But some salamanders, referred to as larval-form paedomorphs, completely or partially forgo metamorphosis, retaining their aquatic larval features and lifestyle into adulthood. This developmental pattern can be facultative or obligate and can manifest from lowering circulating TH and/or reducing TH-responsiveness of larval tissues. Obligate larval-form paedomorphs display varying degrees of responsiveness to TH-treatment; some species exhibit complete metamorphosis, while others show no overt transformation of larval-form tissues. Investigations of the latter species have shown that they have a functional TH-axis, but their tissues have become deregulated (decoupled) from ancestral TH-induced transformation. Obligate paedomorphosis is thought to evolve from facultative paedomorphosis through genetic assimilation followed by canalization. However, the developmental and physiological advantages of full TH-deregulation of larval-form tissues have not been discussed in detail. Since TH is intertwined with many processes such as stress-response, growth, and reproduction, we propose that directional selection for deregulation may allow TH and other interacting hormones to be utilized more effectively without compromising the larval-form. Furthermore, it is unclear whether facultative paedomorphosis is a necessary prerequisite step to becoming obligate. We propose alternative scenarios leading to TH-deregulation such as a rapid rate of directional selection after secondarily colonizing more divergent adaptive zones (e.g., aquifers), and relaxed selection from disusing ancestral TH-pathways for metamorphosis over many generations. Deregulating hormone pathways may be a more generalizable evolutionary phenomenon, reinforcing developmental evolution and perhaps generating novel signaling pathways.