The whale shark genome reveals patterns of vertebrate gene family evolution
- University of Illinois Urbana-Champaign, United States
- Trinity College Dublin, Ireland
- University of Maryland School of Medicine, United States
- Okinawa Churashima Research Center, Japan
- National Institute of Genetics, Japan
- National Center for Biotechnology Information, United States
- Georgia Aquarium, United States
- Emory University School of Medicine, United States
Abstract
Chondrichthyes (cartilaginous fishes) are fundamental for understanding vertebrate evolution, yet their genomes are understudied. We report long-read sequencing of the whale shark genome to generate the best gapless chondrichthyan genome assembly yet with higher contig contiguity than all other cartilaginous fish genomes, and studied vertebrate genomic evolution of ancestral gene families, immunity, and gigantism. We found a major increase in gene families at the origin of gnathostomes (jawed vertebrates) independent of their genome duplication. We studied vertebrate pathogen recognition receptors (PRRs), which are key in initiating innate immune defense, and found diverse patterns of gene family evolution, demonstrating that adaptive immunity in gnathostomes did not fully displace germline-encoded PRR innovation. We also discovered a new Toll-like receptor (TLR29) and three NOD1 copies in the whale shark. We found chondrichthyan and giant vertebrate genomes had decreased substitution rates compared to other vertebrates, but gene family expansion rates varied among vertebrate giants, suggesting substitution and expansion rates of gene families are decoupled in vertebrate genomes. Finally, we found gene families that shifted in expansion rate in vertebrate giants were enriched for human cancer-related genes, consistent with gigantism requiring adaptations to suppress cancer.
Data availability
Raw genome sequencing data have been deposited to SRA under SRX3471980. Raw transcriptome sequence sequence data are available at NCBI BioProject ID PRJDB8472 and DDBJ DRA ID DRA008572. The assembly has been deposited to GenBank and is accessioned as GCA_001642345.2.
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Whale shark blood cell transcriptomeBioProject, PRJDB8472.
Article and author information
Author details
Funding
George Aquarium
- Alistair DM Dove
Emory School of Medicine Development
- Timothy Read
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Dario Riccardo Valenzano, Max Planck Institute for Biology of Ageing, Germany
Version history
- Received: December 2, 2020
- Accepted: August 18, 2021
- Accepted Manuscript published: August 19, 2021 (version 1)
- Version of Record published: September 21, 2021 (version 2)
Copyright
This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.
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The whale shark genome reveals patterns of vertebrate gene family evolution
eLife 10:e65394.
https://doi.org/10.7554/eLife.65394
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