The bowfin genome illuminates the developmental evolution of ray-finned fishes

Andrew W Thompson; M Brent Hawkins; Elise Parey; Dustin J Wcisel; Tatsuya Ota; Kazuhiko Kawasaki; Emily Funk; Mauricio Losilla; Olivia E Fitch; Qiaowei Pan; Romain Feron; Alexandra Louis; Jérôme Montfort; Marine Milhes; Brett L Racicot; Kevin L Childs; Quenton Fontenot; Allyse Ferrara; Solomon R David; Amy R McCune; Alex Dornburg; Jeffrey A Yoder; Yann Guiguen; Hugues Roest Crollius; Camille Berthelot; Matthew P Harris; Ingo Braasch

doi:10.1038/s41588-021-00914-y

The bowfin genome illuminates the developmental evolution of ray-finned fishes

Nat Genet. 2021 Sep;53(9):1373-1384. doi: 10.1038/s41588-021-00914-y. Epub 2021 Aug 30.

Authors

Andrew W Thompson^{1

2}, M Brent Hawkins^{3

4

5

6}, Elise Parey⁷, Dustin J Wcisel⁸, Tatsuya Ota⁹, Kazuhiko Kawasaki¹⁰, Emily Funk^{11

12}, Mauricio Losilla^{1

2}, Olivia E Fitch^{1

2}, Qiaowei Pan¹³, Romain Feron^{13

14}, Alexandra Louis⁷, Jérôme Montfort¹⁵, Marine Milhes¹⁶, Brett L Racicot¹, Kevin L Childs¹⁷, Quenton Fontenot¹⁸, Allyse Ferrara¹⁸, Solomon R David¹⁸, Amy R McCune¹¹, Alex Dornburg¹⁹, Jeffrey A Yoder^{8

20

21}, Yann Guiguen¹⁵, Hugues Roest Crollius⁷, Camille Berthelot⁷, Matthew P Harris^{3

4}, Ingo Braasch^{22

23}

Affiliations

¹ Department of Integrative Biology, Michigan State University, East Lansing, MI, USA.
² Ecology, Evolution & Behavior Program, Michigan State University, East Lansing, MI, USA.
³ Department of Genetics, Harvard Medical School, Boston, MA, USA.
⁴ Department of Orthopedic Research, Boston Children's Hospital, Boston, MA, USA.
⁵ Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA, USA.
⁶ Museum of Comparative Zoology, Harvard University, Cambridge, MA, USA.
⁷ Institut de Biologie de l'ENS (IBENS), Département de Biologie, École Normale Supérieure, CNRS, INSERM, Université PSL, Paris, France.
⁸ Department of Molecular Biomedical Sciences, NC State University, Raleigh, NC, USA.
⁹ Department of Evolutionary Studies of Biosystems, SOKENDAI (the Graduate University for Advanced Studies), Hayama, Japan.
¹⁰ Department of Anthropology, Pennsylvania State University, University Park, PA, USA.
¹¹ Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, NY, USA.
¹² Animal Science Department, University of California Davis, Davis, CA, USA.
¹³ Department of Ecology and Evolution, University of Lausanne, Lausanne, Switzerland.
¹⁴ Swiss Institute of Bioinformatics, Lausanne, Switzerland.
¹⁵ INRAE, LPGP, Rennes, France.
¹⁶ GeT-PlaGe, INRAE, Genotoul, Castanet-Tolosan, France.
¹⁷ Department of Plant Biology, Michigan State University, East Lansing, MI, USA.
¹⁸ Department of Biological Sciences, Nicholls State University, Thibodaux, LA, USA.
¹⁹ Department of Bioinformatics and Genomics, University of North Carolina at Charlotte, Charlotte, NC, USA.
²⁰ Comparative Medicine Institute, NC State University, Raleigh, NC, USA.
²¹ Center for Human Health and the Environment, NC State University, Raleigh, NC, USA.
²² Department of Integrative Biology, Michigan State University, East Lansing, MI, USA. [email protected].
²³ Ecology, Evolution & Behavior Program, Michigan State University, East Lansing, MI, USA. [email protected].

Abstract

The bowfin (Amia calva) is a ray-finned fish that possesses a unique suite of ancestral and derived phenotypes, which are key to understanding vertebrate evolution. The phylogenetic position of bowfin as a representative of neopterygian fishes, its archetypical body plan and its unduplicated and slowly evolving genome make bowfin a central species for the genomic exploration of ray-finned fishes. Here we present a chromosome-level genome assembly for bowfin that enables gene-order analyses, settling long-debated neopterygian phylogenetic relationships. We examine chromatin accessibility and gene expression through bowfin development to investigate the evolution of immune, scale, respiratory and fin skeletal systems and identify hundreds of gene-regulatory loci conserved across vertebrates. These resources connect developmental evolution among bony fishes, further highlighting the bowfin's importance for illuminating vertebrate biology and diversity in the genomic era.

Publication types

Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

Animals
Biological Evolution*
Chromatin / genetics
Evolution, Molecular*
Fishes
Genome / genetics*
Skates, Fish / genetics*
Skates, Fish / immunology
Skates, Fish / physiology*
Whole Genome Sequencing

Substances

Chromatin

Grants and funding

R01 OD011116/OD/NIH HHS/United States