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

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

doi:10.1038/s41588-021-00914-y

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.

Highlights

The monotypic bowfin, A. calva (Linnaeus, 1776), is a textbook example in comparative anatomy for its prototypical fish body plan and key phylogenetic position[1,2]
A de novo genome assembly was constructed with Meraculous[26] and further scaffolded with Chicago[27] and Hi-C approaches[28] using the HiRise software pipeline[27] (Supplementary Figs. 1 and 2)
Using whole-genome alignments (WGAs) generated with Progressive Cactus[55], we showed that more than 50% of bowfin non-coding OCRs (ncOCRs) were conserved in gar, and 3,844 core bowfin ncOCRs were conserved in gar, zebrafish, mouse

Summary

Introduction

The monotypic bowfin, A. calva (Linnaeus, 1776), is a textbook example in comparative anatomy for its prototypical fish body plan and key phylogenetic position[1,2]. The bowfin (Amiiformes) and seven gar species (Lepisosteiformes) represent the extant Holostei, the sister lineage of teleost fishes, together comprising the Neopterygii[4,5,6,7,8]. These eight holosteans, capture just a minor fraction of this once speciose lineage. A chromosomal bowfin genome assembly is essential to test these two alternative scenarios and to develop a comprehensive evolutionary framework for understanding phenotypic evolution among ray-finned fishes

Methods

Results

Conclusion