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Deep-time evolution of regeneration and preaxial polarity in tetrapod limb development
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Deep-time evolution of regeneration and preaxial polarity in tetrapod limb development
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Journal Article
Deep-time evolution of regeneration and preaxial polarity in tetrapod limb development
2015
Overview
Salamanders are the only tetrapod that can fully regenerate their limbs and tail, a capacity that might be linked to their unique preaxial mode of limb development; here, data from fossils reveal the existence of preaxial polarity in various amphibians from the Carboniferous and Permian periods, suggesting that salamander-like regeneration is an ancient feature of tetrapods that was subsequently lost at least once in the lineage leading to amniotes.
Regeneration came early in amphibians
Salamanders are unique among tetrapods in that they can fully regenerate their limbs and tail, a capacity that might be linked to their unique preaxial mode of limb development, in which the first and second digits tend to develop before the others. Nadia Fröbisch and colleagues demonstrate the existence of preaxial polarity in various amphibians from the Carboniferous and Permian periods. Limb regeneration has also been reported in one of these forms, demonstrating that both features were present together in amphibians 290 million years ago. These findings suggest that salamander-like regeneration is an ancient feature of tetrapods that was subsequently lost at least once in the lineage leading to amniotes. Salamanders are the only modern tetrapods that retained regenerative capacities and preaxial polarity in limb development.
Among extant tetrapods, salamanders are unique in showing a reversed preaxial polarity in patterning of the skeletal elements of the limbs, and in displaying the highest capacity for regeneration, including full limb and tail regeneration. These features are particularly striking as tetrapod limb development has otherwise been shown to be a highly conserved process
1
,
2
. It remains elusive whether the capacity to regenerate limbs in salamanders is mechanistically and evolutionarily linked to the aberrant pattern of limb development; both are features classically regarded as unique to urodeles
3
. New molecular data suggest that salamander-specific orphan genes play a central role in limb regeneration and may also be involved in the preaxial patterning during limb development
4
,
5
. Here we show that preaxial polarity in limb development was present in various groups of temnospondyl amphibians of the Carboniferous and Permian periods, including the dissorophoids
Apateon
and
Micromelerpeton
, as well as the stereospondylomorph
Sclerocephalus
. Limb regeneration has also been reported in
Micromelerpeton
6
, demonstrating that both features were already present together in antecedents of modern salamanders 290 million years ago. Furthermore, data from lepospondyl ‘microsaurs’ on the amniote stem indicate that these taxa may have shown some capacity for limb regeneration and were capable of tail regeneration
7
, including re-patterning of the caudal vertebral column that is otherwise only seen in salamander tail regeneration. The data from fossils suggest that salamander-like regeneration is an ancient feature of tetrapods that was subsequently lost at least once in the lineage leading to amniotes. Salamanders are the only modern tetrapods that retained regenerative capacities as well as preaxial polarity in limb development.
Publisher
Nature Publishing Group UK,Nature Publishing Group
