Silver chimaera genome highlights lineage-specific sex chromosome and opsin gene evolution in holocephalans

Cartilaginous fishes are divided into holocephalans and elasmobranchs, and they offer valuable systems for analysing the genetic basis of adaptation to diverse habitats and the evolution of chromosomal organization. Genomic studies on cartilaginous fishes were initiated early with holocephalans because of their compact genomes, but have concentrated primarily on the family Callorhinchidae. Here, we focused on the most species-rich holocephalan family Chimaeridae and characterized the genome of its member, silver chimaera (Chimaera phantasma), in pursuit of genomic traces of adaptation to deep-sea vision. The resulting genome assembly exhibited high continuity and completeness, enabling the first chromosome-level comparison among holocephalans. They displayed substantial intragenomic variation in chromosome length, correlated with intron size, alongside a high degree of one-to-one chromosomal homology. Our search for silver chimaera photoreceptor genes revealed a shrunken set of opsin genes, including rhodopsin exhibiting a sequence signature typical of deep-sea adaptation. We also performed whole-genome resequencing of multiple silver chimaera individuals of both sexes, which identified a putative X-chromosome fragment. This is the first evidence of a holocephalan sex chromosome and suggests male heterogametic sex determination. Our findings contribute to a deeper understanding of vertebrate genome diversity and lay the groundwork for future genetic studies on this species.