Abstract
In crown group tetrapods, individual digits are homologized in relation to a pentadactyl ground plan. However, testing hypotheses of digit homology is challenging because it is unclear whether digits represent distinct and conserved gene regulatory states. Here we show dramatic evolutionary dynamism in the gene expression profiles of digits, challenging the notion that five digits have conserved developmental identities across amniotes. Transcriptomics shows diversity in the patterns of gene expression differentiation of digits, although the anterior-most digit of the pentadactyl limb has a unique, conserved expression profile. Further, we identify a core set of transcription factors that are differentially expressed among the digits of amniote limbs; their spatial expression domains, however, vary between species. In light of these results, we reevaluate the frame shift hypothesis of avian wing evolution and conclude only the identity of the anterior-most digit has shifted position, suggesting a 1,3,4 digit identity in the bird wing.
Highlights
In crown group tetrapods, individual digits are homologized in relation to a pentadactyl ground plan
Studies aiming to test for homology of developmental identity predict that the identities were present in a common ancestor and are conserved, detectable through comparative study of transcription factor and signaling gene expression profiles, in descendent lineages
Comparative analyses of gene expression have found support for this hypothesis: in situ hybridization and transcriptomics have revealed similarity between the anterior digit of the adult avian wing, which develops in position D2, and D1 of other limbs[7,23], and cells in the zone of polarizing activity do not contribute to the skeletal tissues of the digits of the adult avian wing, a pattern consistent with digit D1–D3 of other limbs[24,25]
Summary
Individual digits are homologized in relation to a pentadactyl ground plan. The fossil record of theropod dinosaurs shows a clear pattern of reduction of the posterior two digits in the lineage leading to birds, yet digits in the wing have been described as developing in the middle three positions of a pentadactyl developmental ground plan[17,18,19,20,21,22]. To explain this discrepancy, the frame shift hypothesis was proposed[16]. Comparative analyses of gene expression have found support for this hypothesis: in situ hybridization and transcriptomics have revealed similarity between the anterior digit of the adult avian wing, which develops in position D2, and D1 of other limbs[7,23], and cells in the zone of polarizing activity do not contribute to the skeletal tissues of the digits of the adult avian wing, a pattern consistent with digit D1–D3 of other limbs[24,25]
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