Independent origins of fish endothermy converge on a developmental regulatory signature

Abstract

Why independent origins of the same complex physiological trait repeatedly produce similar body forms and physiological changes remains central in evolutionary biology. Endothermy, the internal production and retention of metabolic heat, evolved at least four times in ray-finned fishes, providing natural replicates for convergent genomic signatures. We present a chromosome-scale analysis of three transitions (opah, tunas, and swordfish), including a new chromosome-level genome of the rare, charismatic Pacific oarfish, analyzed with 31 other teleost genomes. The strongest signal is regulatory: of 253,680 conserved noncoding elements, 577 are rate-accelerated in endothermic lineages, with 67 accelerated in all three, exceeding matched ectothermic controls and enriched near developmental transcription factors and Wnt-signaling genes (e.g., irx1a, irx5a, her9, and lmo1). These elements overlap zebrafish developmental enhancers more than expected by chance but are not tied to genes emphasized by expression or coding-selection studies of endothermic lineages, marking a regulatory layer distinct from that metabolic layer. This convergence is part of a broader mosaic: endothermic lineages also share transition-biased substitution and convergent duplication signatures, including excess tandem duplications and lineage-specific gene-family expansion, whereas chromosome organization and protein-coding sequence change little. Endothermic convergence therefore leaves its clearest signal in regulatory remodeling, alongside shifts in substitution bias and gene-family evolution.