Developmental basis of limb homology in urodeles: heterochronic evidence from the primitive hynobiid family.

Abstract

The vertebrate limb is a classic example of homology, long assumed to be underpinned by a developmental 'bauplan' of the type proposed in the Shubin/Alberch branching and segmenting model. In the anuran/amniote pattern skeletogenesis proceeds in a proximodistal direction with digits forming from the posterior to the anterior. But in free-living larvae of 'advanced' urodeles, the pattern of skeletogenesis is distinctly different with digits 1 and 2 and the basal commune developing early, in an anterior/distal position. This different pattern is cited as evidence for a diphyletic theory of tetrapod evolution. Reassessing this problem, we analysed the pattern of early skeletogenesis of three genera (Salamandrella, Ranodon, Onychodactylus) of the 'basal' family of hynobiids, using immunofluorescence to localize chondroitin-6-SO4 in Salamandrella. Here the developmental sequence was more proximodistal (intermedium preceding basal commune; early formation of the digital arch). This pattern, also found in direct developing urodeles such as Bolitoglossa subpalmata, resembled that in anurans/amniotes. Uniquely amongst tetrapods, urodeles use their developing limbs for locomotion. We attribute the unusual pattern in 'advanced' urodeles to adaptive modification of the developing limb. Differences in the pattern between 'basic' and 'advanced' urodeles and between urodeles and anuran/amniotes are interpreted as heterochronic within an overall single tetrapod developmental bauplan.