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

Author:

Jia Jia123ORCID,Anderson Jason S.2ORCID,Jiang Jian-Ping4ORCID,Wu Wenhao5ORCID,Shubin Neil H.6ORCID,Gao Ke-Qin1ORCID

Affiliation:

1. School of Earth and Space Sciences, Peking University, 5 Yiheyuan Road, Beijing 100871, China.

2. Department of Comparative Biology and Experimental Medicine, University of Calgary, 3330 Hospital Drive, Calgary, Alberta T2N 1N4, Canada.

3. State Key Laboratory of Palaeobiology and Stratigraphy (Nanjing Institute of Geology and Palaeontology, CAS), 39 East Beijing Road, Nanjing, Jiangsu Province 210008, China.

4. Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu, Sichuan Province 610041, China.

5. Research Center of Palaeontology and Stratigraphy, College of Earth Sciences, Jilin University, Changchun, Jilin Province 130061, China.

6. Department of Organismal Biology and Anatomy, Biological Sciences, The University of Chicago, Chicago, IL 60637, USA.

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.

Publisher

American Association for the Advancement of Science (AAAS)

Subject

Multidisciplinary

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