Published June 25, 2025 | Version v1
Journal article Open

Ecological interactions and genomic innovation fueled the evolution of ray-finned fish endothermy

  • 1. University of California, San Diego
  • 2. Cornell University
  • 3. Temple University
  • 4. Université Claude Bernard Lyon 1
  • 5. University of Oklahoma
  • 6. National Research Collections Australia
  • 7. University of Minnesota Twin Cities
  • 8. Università degli Studi di Torino
  • 9. University of Basel Zoological Institute
  • 10. Natural History Museum and Institute
  • 11. University of Chicago
  • 12. Smithsonian Institution
  • 13. North Carolina State University
  • 14. The George Washington University

Description

Endothermy has independently evolved in several vertebrate lineages but remains rare among fishes. Using an integrated approach combining phylogenomic and ecomorphological data for 1051 ray-finned fishes, a time-dependent evolutionary model, and comparative genomic analyses of 205 marine vertebrates, we show that ecological interactions with modern cetaceans coincided with the evolution of endothermy in ray-finned fishes during the Eocene-Miocene. This result is supported by evidence of temporal and geographical overlap between cetaceans and endothermic fish lineages in the fossil record, as well as correlations between cetacean diversification and the origin of endothermy in fishes. Phylogenetic comparative analyses identified correlations between endothermy, large body sizes, and specialized swimming modes while challenging diet specialization and depth range expansion hypotheses. Comparative genomic analyses identified several genes under selection in endothermic lineages, including carnmt1 (involved in fatty acid metabolism) and dcaf6 (associated with development). Our findings advance the understanding of how ecological interactions and genomic factors shape key adaptations.

Data availability

All data needed to evaluate the conclusions in the paper are present in the paper and/or the Supplementary Materials. High-resolution versions of all figures that appear in the main manuscript are available in a Zenodo repository at https://doi.org/10.5281/zenodo.14934749. In addition, all supplementary tables (tables S1 to S27) and datasets (datasets S1 to S11) used in this study are available in a Dryad repository at https://doi.org/10.5061/dryad.ht76hdrpj. Raw sequence reads are available at the National Center for Biotechnology Information Sequence Read Archive BioProject (number PRJNA1262494) at https://ncbi.nlm.nih.gov/bioproject/PRJNA1262494. A repository containing all codes used for phylogenomic assembly and exon capture is available via the Dryad link provided above, as well as in the following repositories: https://github.com/lilychughes/FishLifeExonHarvesting and https://github.com/lilychughes/FishLifeExonCapture. The codes used for the comparative genomic analyses can be found at https://github.com/veg/Endothermy and https://github.com/veg/Endothermy/tree/main/RER.

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Additional details

Identifiers

DOI
10.1126/sciadv.ads8488
Other
oai:uchicago.tind.io:15555

Funding

National Science Foundation
DEB-2144325
National Science Foundation
DEB-2015404
National Science Foundation
DEB-1541491
National Science Foundation
DEB-2225130
National Science Foundation
DEB-1541552

UChicago Information

Division(s)
Biological Sciences Division
Department(s)
Organismal Biology and Anatomy