Abstract

Author SummaryOur upper limbs differ from fish fins, notably by their subdivision into arm and hand regions, which are separated by a complex articulation, the wrist. The development of this anatomy is associated with two distinct waves of expression of the Hoxa and Hoxd genes during development. Would such a shared expression pattern be sufficient to infer homology between fish fins and mouse limbs? We investigated this question here, looking at whether the two phases of Hox gene transcription that are observed during tetrapod limb development also occur during zebrafish fin development. We find the answer is “not quite.” For although the mechanisms that regulate the expression of Hoxa and Hoxd are comparable between zebrafish fins and mouse limbs, when the genomic regions that regulate Hox gene expression in fish fins are introduced into transgenic mice, they trigger Hox gene expression in only the proximal limb segment (the segment nearest the body) and not in the presumptive digits. We conclude that although fish have the Hox regulatory toolkit to produce digits, this potential is not utilized as it is in tetrapods, and as a result we propose that fin radials—the bony elements of fins—are not homologous to tetrapod digits.

Highlights

  • The tetrapod limb is made out of a proximal-to-distal series of long bones, the stylopod, zeugopod in the arm, and the digits in the hand, the latter of which are separated from the former two by the mesopodium, an articulation based on an array of small roundish bones [1,2,3,4]

  • Would such a shared expression pattern be sufficient to infer homology between fish fins and mouse limbs? We investigated this question here, looking at whether the two phases of Hox gene transcription that are observed during tetrapod limb development occur during zebrafish fin development

  • We find the answer is ‘‘not quite.’’ For the mechanisms that regulate the expression of Hoxa and Hoxd are comparable between zebrafish fins and mouse limbs, when the genomic regions that regulate Hox gene expression in fish fins are introduced into transgenic mice, they trigger Hox gene expression in only the proximal limb segment and not in the presumptive digits

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Summary

Introduction

The tetrapod limb is made out of a proximal-to-distal series of long bones, the stylopod, zeugopod in the arm, and the digits in the hand, the latter of which are separated from the former two by the mesopodium, an articulation based on an array of small roundish bones [1,2,3,4]. This skeletal organisation evolved during the Devonian as an adaptation to the buoyancy-lacking environment of the land [5,6]. The existence of distinct regulatory modules for long bones on either side of the mesopodial articulation (the wrist and ankle), together with the separated evolutionary trajectories of these elements, has supported the view that tetrapod limbs are genetically organized following a specific bimodal pattern of proximal (arm and forearm) and distal (digits) long bones, which as such is not present in fish fins (refs. in [1])

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