Ossification patterns in the tetrapod limb – conservation and divergence from morphogenetic events

Abstract

Two different patterns of the condensation and chondrification of the limbs of tetrapods are known from extensive studies on their early skeletal development. These are on the one hand postaxial dominance in the sequential formation of skeletal elements in amniotes and anurans, and on the other, preaxial dominance in urodeles. The present study investigates the relative sequence of ossification in the fore- and hindlimbs of selected tetrapod taxa based on a literature survey in comparison to the patterns of early skeletal development, i.e. mesenchymal condensation and chondrification, representing essential steps in the late stages of tetrapod limb development. This reveals the degree of conservation and divergence of the ossification sequence from early morphogenetic events in the tetrapod limb skeleton. A step-by-step recapitulation of condensation and chondrification during the ossification of limbs can clearly be refuted. However, some of the deeper aspects of early skeletal patterning in the limbs, i.e. the general direction of development and sequence of digit formation are conserved, particularly in anamniotes. Amniotes show a weaker coupling of the ossification sequence in the limb skeleton with earlier condensation and chondrification events. The stronger correlation between the sequence of condensation/chondrification and ossification in the limbs of anamniotes may represent a plesiomorphic trait of tetrapods. The pattern of limb ossification across tetrapods also shows that some trends in the sequence of ossification of their limb skeleton are shared by major clades possibly representing phylogenetic signals. This review furthermore concerns the ossification sequence of the limbs of the Palaeozoic temnospondyl amphibian Apateon sp. For the first time this is described in detail and its patterns are compared with those observed in extant taxa. Apateon sp. shares preaxial dominance in limb development with extant salamanders and the specific order of ossification events in the fore- and hindlimb of this fossil dissorophoid is almost identical to that of some modern urodeles.

Salamander limb development: Integrating genes, morphology, and fossils

“…Variation within urodeles appears to exceed that seen in other clades of tetrapod (Shubin and Alberch, 1986;Blanco and Alberch, 1992;Vorobyeva and Hinchliffe, 1996;Shubin and Wake, 2003;Franssen et al, 2005;Fröbisch, 2008).…”

“…The ontogenetic series for the branchiosaurid Apateon is extraordinary in its completeness, but can only provide insights into the sequence of ossification rather than earlier events in skeletogenesis, because only bony tissues are fossilized. Nevertheless, it has been demonstrated that although ossification is not a recapitulation of the sequence of events in early skeletogenesis, the general direction and polarity of digit development is preserved in the ossification sequence, with a close correlation in particular in anamniotes (Fröbisch, 2008). The ossification sequence can therefore provide insights into the early patterning of the limbs of this extinct clade despite the fact that the sequence of chondrogenesis, being of soft tissue, cannot be preserved.…”

“…The recent discoveries of preaxial dominance in limb development in the Lower Permian branchiosaurids (Fröbisch et al, 2007;Fröbisch, 2008) and a basale commune in the Middle Permian amphibamid Gerobatrachus add further data points for the evolution of this developmental pathway deep in the evolutionary history of amphibians (Fig. 6).…”

“…They lack limbs altogether as tadpoles and develop limbs only with the onset of metamorphosis (Duellman and Trueb, 1986). A delay of limb development is thought to be plesiomorphic for modern amphibians as indicated by the fossil record of Paleozoic amphibians, including branchiosaurids, which share other features of limb development with salamanders (Fröbisch et al, 2007, see below;Fröbisch, 2008). The late onset of limb development in amphibians may have been a crucial factor for the evolution of regenerative ability in salamanders and frogs, because the lag of limb development after other patterning processes in the embryo meant a freeing of the interactions with transient structures and the acquirement of a semiautonomous state of the limb (Galis et al, 2003b).…”

A case study of developmental palaeontology in <i>Stereosternum tumidum</i> (Mesosauridae, Parareptilia)

“…If preserved, they provide valuable insight into the life history of extinct taxa, as well as evolutionary trajectories. To date, ossification sequences in fossils are available for some "fish" (Cloutier, 2010), temnospondyl and lepospondyl amphibians (Fröbisch, 2008;Fröbisch et al, 2010Fröbisch et al, , 2015, "younginiforms" (sensu Bickelmann et al, 2009) (Currie, 1981;Caldwell, 2002), mosasaurs (Caldwell, 2002), sauropterygians (Hugi and Scheyer, 2012), ichthyosaurs (Caldwell, 1997), sauropsids (Delfino and Sánchez-Villagra, 2010) and mammals (Sánchez-Villagra, 2010). Most of this information is derived from secondarily aquatic taxa, which is the result of a taphonomic bias (Fröbisch et al, 2010).…”