The tiger shark, Galeocerdo cuvier (Peron & Lesueur, 1822), genome reveals genomic and epigenomic signatures of shark evolution and demographic history

Abstract

Cartilaginous fishes (Chondrichthyes) represent one of the oldest extant vertebrate lineages, persisting for over 450 million years, yet genomic resources remain limited for many species despite widespread conservation concern. The tiger shark, Galeocerdo cuvier (Peron & Lesueur, 1822), the sole surviving member of the family Galeocerdonidae, is a circumglobally cosmopolitan predator vital in ecosystem regulation but is experiencing population declines. Here, we generated the first chromosome-scale haplotype-phased reference genome for the tiger shark and integrated comparative and population genomics with methylomics to characterise its genome architecture and evolutionary history. This assembly presented the first evidence of male heterogamety in this species. Comparative analyses revealed lineage-specific transposable element expansions across the chondrichthyan class suggesting ongoing genome restructuring in Carcharhiniform sharks. We report the first hydroxymethylome in a chondrichthyan, higher than that of other vertebrates, hinting at novel DNA evolutionary and regulatory pathways in an early-diverging lineage of jawed vertebrates. We identified genomic signatures of prolonged population decline that correlated with historical climate fluctuations and have resulted in sustained low levels of genetic heterozygosity in this species. These findings offer new insights into shark and broader vertebrate genomic and epigenomic evolution while providing valuable resources for conservation genomics of one of the world's most widespread top-order predators in the face of accelerating environmental change.