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

Nature volume 477, pages 583–586 (2011)Cite this article

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Abstract

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 identity1,2,3. Here we use transcriptomic data to address a long-standing uncertainty in evolutionary biology, the identity of avian wing digits4,5. 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 far5,8.

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Figure 1: Chicken embryonic digit transcriptomes identify forelimb and hindlimb digits I but no clear correspondence between posterior forelimbs and hindlimbs.
Figure 2: Expression of Zic3.
Figure 3: Expression of Socs2.

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Accession codes

Primary accessions

Gene Expression Omnibus

Data deposits

All mRNA-seq data are deposited in the Gene Expression Omnibus under accession number GSE28156.

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Acknowledgements

The authors thank J. Noonan for discussions on this project, K. Cooper for experimental assistance and N. Carriero for read-mapping assistance and C. Tabin for providing us with the Hoxd12 probe. The authors are also grateful for the technical support for this project by the Yale Center for Genomic Analysis. The financial support by the Yale Science Development Fund is gratefully acknowledged.

Author information

Authors and Affiliations

  1. and Department of Ecology and Evolutionary Biology, Yale Systems Biology Institute, Yale University, West Haven, 06516, Connecticut, USA

    Zhe Wang, Rebecca L. Young & Günter P. Wagner

  2. Department of Genetics, Yale University School of Medicine, New Haven, 06510, Connecticut, USA

    Huiling Xue

Authors
  1. Zhe Wang
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Contributions

Z.W. performed the experiments and data analysis and participated in design of the study. R.L.Y., H.X. and G.P.W. participated in data analysis. G.P.W. conceived and designed the study and supervised the work. All authors discussed the results and made substantial contributions to the manuscript.

Corresponding author

Correspondence to Günter P. Wagner.

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The authors declare no competing financial interests.

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This file contains Supplementary Figures 1-10 with legends, Supplementary Table 1, a Supplementary Discussion and Supplementary References. (PDF 989 kb)

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Wang, Z., Young, R., Xue, H. et al. Transcriptomic analysis of avian digits reveals conserved and derived digit identities in birds. Nature 477, 583–586 (2011). https://doi.org/10.1038/nature10391

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