A molecular mechanism for the origin of a key evolutionary innovation, the bird beak and palate, revealed by an integrative approach to major transitions in vertebrate history

Published on Jul 1, 2015in Evolution3.57
· DOI :10.1111/evo.12684
Bhart-Anjan S. Bhullar16
Estimated H-index: 16
Zachary S. Morris11
Estimated H-index: 11
(Harvard University)
+ 6 AuthorsArhat Abzhanov22
Estimated H-index: 22
(Imperial College London)
The avian beak is a key evolutionary innovation whose flexibility has permitted birds to diversify into a range of disparate ecological niches. We approached the problem of the mechanism behind this innovation using an approach bridging paleontology, comparative anatomy, and experimental developmental biology. First, we used fossil and extant data to show the beak is distinctive in consisting of fused premaxillae that are geometrically distinct from those of ancestral archosaurs. To elucidate underlying developmental mechanisms, we examined candidate gene expression domains in the embryonic face: the earlier frontonasal ectodermal zone (FEZ) and the later midfacial WNT-responsive region, in birds and several reptiles. This permitted the identification of an autapomorphic median gene expression region in Aves. To test the mechanism, we used inhibitors of both pathways to replicate in chicken the ancestral amniote expression. Altering the FEZ altered later WNT responsiveness to the ancestral pattern. Skeletal phenotypes from both types of experiments had premaxillae that clustered geometrically with ancestral fossil forms instead of beaked birds. The palatal region was also altered to a more ancestral phenotype. This is consistent with the fossil record and with the tight functional association of avian premaxillae and palate in forming a kinetic beak.
  • References (63)
  • Citations (43)
#1Stephen L. Brusatte (Edin.: University of Edinburgh)H-Index: 34
#2Graeme T. Lloyd (University of Oxford)H-Index: 22
Last.Mark A. Norell (AMNH: American Museum of Natural History)H-Index: 60
view all 4 authors...
119 CitationsSource
#1Michael S. Y. Lee (University of Adelaide)H-Index: 52
#2Andrea Cau (UNIBO: University of Bologna)H-Index: 15
Last.Gareth J. Dyke (University of Southampton)H-Index: 28
view all 4 authors...
108 CitationsSource
25 CitationsSource
#1Kevin J. Parsons (Glas.: University of Glasgow)H-Index: 18
#2A. Trent Taylor (UMass: University of Massachusetts Amherst)H-Index: 1
Last.R. Craig Albertson (UMass: University of Massachusetts Amherst)H-Index: 25
view all 4 authors...
47 CitationsSource
#1Günter P. WagnerH-Index: 66
156 Citations
#1Nathan M. Young (UCSF: University of California, San Francisco)H-Index: 26
#2Diane Hu (UCSF: University of California, San Francisco)H-Index: 32
Last.Ralph S. Marcucio (UCSF: University of California, San Francisco)H-Index: 36
view all 10 authors...
67 CitationsSource
54 CitationsSource
#1Amy M. Balanoff (SBU: Stony Brook University)H-Index: 16
#2Gabe S. Bever (NYIT: New York Institute of Technology)H-Index: 13
Last.Mark A. Norell (AMNH: American Museum of Natural History)H-Index: 60
view all 4 authors...
75 CitationsSource
#1Claudia Compagnucci (Guy's Hospital)H-Index: 7
#2Mélanie Debiais-Thibaud (Paris Diderot University)H-Index: 13
Last.Michael J. Depew (UCSF: University of California, San Francisco)H-Index: 18
view all 12 authors...
43 CitationsSource
#1John N. Griffin (Guy's Hospital)H-Index: 2
#2Claudia Compagnucci (Guy's Hospital)H-Index: 7
Last.Michael J. Depew (UCSF: University of California, San Francisco)H-Index: 18
view all 7 authors...
30 CitationsSource
Cited By43
#1David Jablonski (U of C: University of Chicago)H-Index: 60
2 CitationsSource
#1Ryan N. Felice (UCL: University College London)H-Index: 3
#2Akinobu Watanabe (New York Institute of Technology College of Osteopathic Medicine)H-Index: 6
Last.Anjali Goswami (UCL: University College London)H-Index: 32
view all 9 authors...
1 CitationsSource
#1Tatiana S. Bagaeva (MSU: Moscow State University)
#2Daria M. Kupaeva (MSU: Moscow State University)H-Index: 1
Last.S.V. Kremnyov (MSU: Moscow State University)H-Index: 5
view all 6 authors...
#1Zachary S. Morris (Harvard University)H-Index: 11
#2Kent A. Vliet (UF: University of Florida)H-Index: 18
Last.Stephanie E. Pierce (Harvard University)H-Index: 15
view all 4 authors...
8 CitationsSource
#1Alejandro Rico-Guevara (University of California, Berkeley)H-Index: 5
#2Diego Sustaita (CSUSM: California State University San Marcos)H-Index: 5
Last.Robert Dudley (University of California, Berkeley)H-Index: 43
view all 7 authors...
#1Vincent Bels (University of Paris)H-Index: 15
#2Anthony HerrelH-Index: 52
#1Qinwen Liu (U of C: University of Chicago)H-Index: 1
#2Pinar Onal (NYU: New York University)H-Index: 1
Last.Joseph W. Thornton (U of C: University of Chicago)H-Index: 37
view all 8 authors...
4 CitationsSource
#1Shiro Egawa (Tohoku University)H-Index: 4
#2Daisuke Saito (Tohoku University)H-Index: 11
Last.Koji Tamura (Tohoku University)H-Index: 35
view all 4 authors...
1 CitationsSource
View next paperBirds have paedomorphic dinosaur skulls