Abstract
Salamanders are the only tetrapods capable of fully regenerating their limbs throughout their entire lives. Much data on the underlying molecular mechanisms of limb regeneration have been gathered in recent years allowing for new comparative studies between salamanders and other tetrapods that lack this unique regenerative potential. By contrast, the evolution of animal regeneration just recently shifted back into focus, despite being highly relevant for research designs aiming to unravel the factors allowing for limb regeneration. We show that the 300-million-year-old temnospondyl amphibian Micromelerpeton, a distant relative of modern amphibians, was already capable of regenerating its limbs. A number of exceptionally well-preserved specimens from fossil deposits show a unique pattern and combination of abnormalities in their limbs that is distinctive of irregular regenerative activity in modern salamanders and does not occur as variants of normal limb development. This demonstrates that the capacity to regenerate limbs is not a derived feature of modern salamanders, but may be an ancient feature of non-amniote tetrapods and possibly even shared by all bony fish. The finding provides a new framework for understanding the evolution of regenerative capacity of paired appendages in vertebrates in the search for conserved versus derived molecular mechanisms of limb regeneration.
Highlights
Regeneration of missing body parts occurs in most animal phyla, whereas regenerative capabilities vary extensively even between closely related taxa [1,2,3]
Much data on the underlying molecular mechanisms of limb regeneration have been gathered in recent years allowing for new comparative studies between salamanders and other tetrapods that lack this unique regenerative potential
We show that the 300-million-year-old temnospondyl amphibian Micromelerpeton, a distant relative of modern amphibians, was already capable of regenerating its limbs
Summary
Regeneration of missing body parts occurs in most animal phyla, whereas regenerative capabilities vary extensively even between closely related taxa [1,2,3]. While grafting experiments and some molecular studies indicated that contrary to initial limb development, during regeneration the distal tip of the stump is specified first, followed by intercalary growth [17,18,19], more recent studies point towards a proximo-distal sequence of cell specification during regeneration, indicating that similar patterning modes may be used in development and regeneration [20,21]. Frogs display some regenerative capacity and can fully regenerate their limbs until the tadpole reaches metamorphic climax and similar molecular markers controlling certain aspects of the regeneration cascade have been found in premetamorphic frogs and salamanders [8,23,24]. Limb regeneration is considered one of the most complex regenerative modes, and recent studies have identified a number of specific molecular markers that seem to be unique to salamander limb regeneration [24,27,28,29,30]
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