Transcriptomic analysis of avian digits reveals conserved and derived digit identities in birds

Morphological characters are the result of developmental gene expression. The identity of a character is ultimately grounded in the gene regulatory network directing development and thus whole-genome gene expression data can provide evidence about character identity. This approach has been successfully used to assess cell-type identity(1-3). Here we use transcriptomic data to address a long-standing uncertainty in evolutionary biology, the identity of avian wing digits(4,5). Embryological evidence clearly identifies the three wing digits as developing from digit positions 2, 3 and 4 (ref. 6), whereas palaeontological data suggest that they are digits I, II and III7. We compare the transcriptomes of the wing and foot digits and find a strong signal that unites the first wing digit with the first foot digit, even though the first wing digit develops from embryological position 2. Interestingly, our transcriptomic data of the posterior digits show a higher degree of differentiation among forelimb digits compared with hindlimb digits. These data show that in the stem lineage of birds the first digit underwent a translocation from digit position 1 to position 2, and further indicate that the posterior wing digits have unique identities contrary to any model of avian digit identity proposed so far(5,8).