Chromosomal Restructuring and Subgenome Divergence Drive Post-Polyploid Adaptive Diversification in Sinocyclocheilus Cavefish

Allopolyploidy generates extensive genomic potential, yet its role in adaptive diversification remains poorly understood. We assembled phased chromosome-level genomes of cave and surface ecotypes of Sinocyclocheilus, a rapidly diversifying cavefish lineage, the most species-rich in the world. Our analyses show that all species derive from the ancestral allotetraploidisation event common to all cyprinids without subsequent polyploidisation. Instead, diversification has been driven by chromosomal rearrangements and the emergence of subgenome asymmetry. The dominant D subgenome maintains more genes, exhibits higher expression, and is enriched for adaptive functions, while the submissive S subgenome is inclined towards housekeeping roles. This asymmetry is further reinforced by the accumulation of transposable elements near genes exhibiting expression biased toward the S-subgenome. We also identify a derived epigenetic mechanism in the cave ecotype, i.e., differential methylation of these elements, absent in the surface ecotype. These findings show how structural, regulatory, and epigenetic processes have interacted following allopolyploidy to produce ecological and phenotypic diversity in Sinocyclocheilus. Our findings also offer quantitative evidence that cave adaptation is a complex process characterised by an evolutionary trade-off - the regression of energetically expensive traits combined with the remodeling of neural and developmental pathways driven by natural selection.