Ossification patterns of the carpus and tarsus in salamanders and impacts of preaxial dominance on the fin-to-limb transition

Abstract

Early limb skeletogenesis in salamanders is characterized by preaxial elements, digits I and II forming earlier than their postaxial counterparts (digits III to V), a phenomenon known as preaxial dominance, whereas in amniotes and anurans, these developmental sequences are reversed. This pattern characterizes the late skeletogenesis of digits and zeugopodium of anamniote tetrapods but remains unknown in carpals/tarsals. To correct this gap in knowledge, we investigate the ossification patterns of the carpals/tarsals in six salamander families/clades based on micro–computed tomography scans. We found that preaxial dominance is seen in the distal carpals/tarsals of several salamander clades and diverse early tetrapods, such as temnospondyls and amniotes. This distribution suggests that preaxial dominance is a primitive developmental pattern in tetrapods. Our results demonstrate that the distal carpals/tarsals are developmentally and evolutionarily independent in the autopodium, and preaxial dominance facilitates stabilization of the number of distal carpals/tarsals during fin-to-limb transition and digit reduction in early tetrapods.

Morphology and ontogeny of carpus and tarsus in stereospondylomorph temnospondyls

“… Jia et al (2022) recently conducted a large-scale analysis of the mesopodial ossification patterns in a great number of salamander taxa in a variety of clades. They found preaxial polarity in the ossification sequence of the distal carpals and tarsals ( i.e ., the digital arch mesopodials) in most clades of salamanders, whereas others, like plethodontids and salamandrids, show postaxial polarity.…”

“…To compare the mesopodial ossification patterns in stereospondylomorphs among each other, but also with other temnospondyls, salamanders and amniotes, we follow Jia et al (2022) who used the scheme of Goette (1879) in dividing the salamander mesopodium into three different columns. These columns contain, in the case of a “generalized” salamander mesopodium like that of Dicamptodon ( Shubin & Wake, 2003 ), the following elements: (1) radiale/tibiale and element y in the preaxial column, (2) intermedium and centrale in the central column, and (3) ulnare/fibulare in the postaxial column.…”

“…2 ). The row of distal carpals and distal tarsals, respectively, or digital arch mesopodials sensu Jia et al (2022) , are treated separately from these columns.…”

“…Recently, Jia et al (2022) provided a comprehensive study of the ossification patterns in the mesopodium of a variety of salamander clades and compared their results with published descriptions of incompletely ossified carpals and tarsals of a few selected early tetrapods. The authors found preaxial dominance in the ossification of distal carpals and tarsals in most salamander taxa and suggested this pattern to be plesiomorphic for tetrapods, in line with previous studies suggesting a plesiomorphic state of preaxial polarity in limb development based on ossification of the long bones and digits ( Fröbisch, Carroll & Schoch, 2007 ; Fröbisch, 2008 ; Fröbisch, Bickelmann & Witzmann, 2014 ; Fröbisch et al, 2015 ).…”

The salamander limb: a perfect model to understand imperfect integration during skeletal regeneration

“…The last elements to ossify are the ones in the mesopodium (carpals and tarsals). These elements ossify late during post-embryonic development or remain cartilaginous for the entire life ( Fröbisch, 2008 ; Jia et al, 2022 ). In axolotls, a variable ossification of these elements was reported in animals older than 5-years-old ( Riquelme-Guzmán et al, 2021 ).…”