The whale shark genome reveals patterns of vertebrate gene family evolution

• Authors: Milton Tan, University of Illinois Urbana-Champaign; Anthony K Redmond, Trinity College Dublin; Helen Dooley, University of Maryland School of Medicine; Ryo Nozu, Okinawa Churashima Foundation; Keiichi Sato, Okinawa Churashima Foundation; Shigehiro Kuraku, RIKEN Center for Biosystems Dynamics Research (BDR); Sergey Koren, National Human Genome Research Institute, National Institutes of Health, Bethesda; Adam M Phillippy, National Human Genome Research Institute, National Institutes of Health, Bethesda; Alistair DM Dove, Georgia Aquarium; Timothy Read, Emory University
• Journal Title: ELIFE
• Volume: Volume 10
• Publisher: eLIFE SCIENCES PUBL LTD | 2021-08-19
• Type of Work: Article | Final Publisher PDF
• Publisher DOI: http://doi.org/10.7554/eLife.65394
• Keywords: Science & Technology; Life Sciences & Biomedicine; Biology; Life Sciences & Biomedicine - Other Topics; whale shark; Rhincodon typus; chondrichthyes; vertebrate; gnathostome; fish; Other; TOLL-LIKE RECEPTORS; FIBRILLAR COLLAGEN; PROVIDES INSIGHT; IMMUNE RECEPTORS; MOLECULAR CLOCK; DEATH EVOLUTION; SPOTTED GAR; SEQUENCE; ALIGNMENT; TREE

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.