title: Diverse feather shape evolution enabled by coupling anisotropic signalling modules with self-organizing branching programme.
abstract: Adaptation of feathered dinosaurs and Mesozoic birds to new ecological niches was potentiated by rapid diversification of feather vane shapes. The molecular mechanism driving this spectacular process remains unclear. Here, through morphology analysis, transcriptome profiling, functional perturbations and mathematical simulations, we find that mesenchyme-derived GDF10 and GREM1 are major controllers for the topologies of rachidial and barb generative zones (setting vane boundaries), respectively, by tuning the periodic-branching programme of epithelial progenitors. Their interactions with the anterior-posterior WNT gradient establish the bilateral-symmetric vane configuration. Additionally, combinatory effects of CYP26B1, CRABP1 and RALDH3 establish dynamic retinoic acid (RA) landscapes in feather mesenchyme, which modulate GREM1 expression and epithelial cell shapes. Incremental changes of RA gradient slopes establish a continuum of asymmetric flight feathers along the wing, while switch-like modulation of RA signalling confers distinct vane shapes between feather tracts. Therefore, the co-option of anisotropic signalling modules introduced new dimensions of feather shape diversification.
authors.affiliation: Department of Pathology, University of Southern California, Los Angeles, California 90033, USA.
authors.forename: Ang
authors.initials: A
authors.lastname: Li
authors.affiliation: Department of Biomedical Engineering, University of California, Irvine, California 92627, USA.
authors.forename: Seth
authors.initials: S
authors.lastname: Figueroa
authors.affiliation: Department of Pathology, University of Southern California, Los Angeles, California 90033, USA.
authors.forename: Ting-Xin
authors.initials: TX
authors.lastname: Jiang
authors.affiliation: Department of Pathology, University of Southern California, Los Angeles, California 90033, USA.
authors.forename: Ping
authors.initials: P
authors.lastname: Wu
authors.affiliation: Department of Pathology, University of Southern California, Los Angeles, California 90033, USA.
authors.forename: Randall
authors.initials: R
authors.lastname: Widelitz
authors.affiliation: Department of Biomedical Engineering, University of California, Irvine, California 92627, USA.|Department of Mathematics, University of California, Irvine, California 92697, USA.
authors.forename: Qing
authors.initials: Q
authors.lastname: Nie
authors.affiliation: Department of Pathology, University of Southern California, Los Angeles, California 90033, USA.|Integrative Stem Cell Center, China Medical University, Taichung 404, Taiwan.|Center for the Integrative and Evolutionary Galliformes Genomics, National Chung Hsing University, Taichung 402, Taiwan.|Research Center for Developmental Biology and Regenerative Medicine, National Taiwan University, Taipei 10617, Taiwan.
authors.forename: Cheng-Ming
authors.initials: CM
authors.lastname: Chuong
mesh_terms: D000818:Animals; D005075:Biological Evolution; D001717:Birds / Q000033:anatomy & histology*; D025061:Dinosaurs; D004847:Epithelial Cells; D005241:Feathers / Q000033:anatomy & histology*; D055413:Growth Differentiation Factor 10 / Q000235:genetics; D059630:Mesenchymal Stem Cells; D018168:Receptors, Retinoic Acid / Q000235:genetics; D050697:Retinal Dehydrogenase / Q000235:genetics; D000072516:Retinoic Acid 4-Hydroxylase / Q000235:genetics; D014212:Tretinoin / Q000378:metabolism; D051153:Wnt Proteins / Q000235:genetics
chemical_list: D055413:Growth Differentiation Factor 10; D018168:Receptors, Retinoic Acid; D051153:Wnt Proteins; D014212:Tretinoin; D000072516:Retinoic Acid 4-Hydroxylase; D050697:Retinal Dehydrogenase