Convergent regulatory evolution and loss of flight in paleognathous birds.

Timothy B Sackton,Michele Clamp,Alison Cloutier,Allan J Baker,Nicole E Wheeler,Julia A Clarke,Phil Grayson,Jun S Liu,Zhirui Hu,Scott V Edwards,Paul P Gardner

doi:10.1126/science.aat7244

Abstract

A core question in evolutionary biology is whether convergent phenotypic evolution is driven by convergent molecular changes in proteins or regulatory regions. We combined phylogenomic, developmental, and epigenomic analysis of 11 new genomes of paleognathous birds, including an extinct moa, to show that convergent evolution of regulatory regions, more so than protein-coding genes, is prevalent among developmental pathways associated with independent losses of flight. A Bayesian analysis of 284,001 conserved noncoding elements, 60,665 of which are corroborated as enhancers by open chromatin states during development, identified 2355 independent accelerations along lineages of flightless paleognaths, with functional consequences for driving gene expression in the developing forelimb. Our results suggest that the genomic landscape associated with morphological convergence in ratites has a substantial shared regulatory component.

Highlights

Citable link Terms of UseTimothy B., Phil Grayson, Alison Cloutier, Zhirui Hu, Jun S
Whether convergent phenotypic evolution is driven by convergent molecular changes, in proteins or regulatory regions, are core questions in evolutionary biology
Developmental and epigenomic analysis of eleven new genomes of palaeognathous birds, including an extinct moa, to show that convergent evolution of regulatory regions, more so than protein-coding genes, is prevalent among developmental pathways associated with independent losses of flight

Summary

Citable link Terms of Use

Timothy B., Phil Grayson, Alison Cloutier, Zhirui Hu, Jun S. Using an electroporated b-actin/GFP enhancer construct assay, we identified a promising chicken region from among these candidates, consisting of the ATAC-seq peak containing the with convergent ratite-accelerated element mCE967994, which produced consistent strong enhancer activity in early chicken forelimbs (Fig. 4c-e) This element is located in the intron of the TEAD1 gene, which has been implicated in cell proliferation, cell survival, mesoderm patterning, and the epithelial-mesenchymal transition [57,58,59], and contains binding sites for TEF-1/TEAD1, suggesting it may play a role in TEAD1 autoregulation. Our unbiased statistical and functional screens, which emphasized genomic changes occurring in parallel on multiple lineages of ratites, suggest that convergent morphological evolution and loss of flight in ratites is associated more strongly with regulatory evolution in noncoding DNA than with evolutionary changes in protein-coding genes, and contrast with previous work, which emphasized protein-coding correlates of flightlessness in birds. Our results do not rule out a role for lineage-specific genomic drivers of flightlessness, they provide a template for future genome-wide studies of loss of flight and other convergent phenotypes across the Tree of Life

Elegant crested tinamou

Findings

Ratite mean