Evolution of vertebrate gill covers via shifts in an ancient Pou3f3 enhancer

Whereas the gill chambers of jawless vertebrates open directly into the environment, jawed vertebrates evolved skeletal appendages that drive oxygenated water unidirectionally over the gills. A major anatomical difference between the two jawed vertebrate lineages is the presence of a single large gi...

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Bibliographic Details
Published in:Proceedings of the National Academy of Sciences - PNAS 2020-10, Vol.117 (40), p.24876-24884
Main Authors: Barske, Lindsey, Fabian, Peter, Hirschberger, Christine, Jandzik, David, Square, Tyler, Xu, Pengfei, Nelson, Nellie, Yu, Haoze Vincent, Medeiros, Daniel M., Gillis, J. Andrew, Crump, J. Gage
Format: Article
Language:English
Subjects:
Animals
Appendages
Biological Sciences
Chondrichthyes
Divergence
Enhancer Elements, Genetic
Enhancers
Evolution
Evolution, Molecular
Fishes - classification
Fishes - genetics
Fishes - growth & development
Gills
Gills - growth & development
Mutation
Pharynx
Phylogeny
POU Domain Factors - genetics
Sharks
Sharks - classification
Sharks - genetics
Sharks - growth & development
Vertebrates
Vertebrates - classification
Vertebrates - genetics
Vertebrates - growth & development
Zebrafish
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Summary:Whereas the gill chambers of jawless vertebrates open directly into the environment, jawed vertebrates evolved skeletal appendages that drive oxygenated water unidirectionally over the gills. A major anatomical difference between the two jawed vertebrate lineages is the presence of a single large gill cover in bony fishes versus separate covers for each gill chamber in cartilaginous fishes. Here, we find that these divergent patterns correlate with the pharyngeal arch expression of Pou3f3 orthologs. We identify a deeply conserved Pou3f3 arch enhancer present in humans through sharks but undetectable in jawless fish. Minor differences between the bony and cartilaginous fish enhancers account for their restricted versus pan-arch expression patterns. In zebrafish, mutation of Pou3f3 or the conserved enhancer disrupts gill cover formation, whereas ectopic pan-arch Pou3f3b expression generates ectopic skeletal elements resembling the multimeric covers of cartilaginous fishes. Emergence of this Pou3f3 arch enhancer >430 Mya and subsequent modifications may thus have contributed to the acquisition and diversification of gill covers and respiratory strategies during gnathostome evolution.
ISSN:0027-8424
1091-6490
DOI:10.1073/pnas.2011531117