Convergent subgenome dominance but with lineage-specific functional divergence of homoeologs during cave adaptation: insights from full-length transcriptomes of Sinocyclocheilus species

洞穴适应过程中同源基因的趋同亚基因组优势与谱系特异性功能分化:来自中华环唇螈属物种全长转录组的启示

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Abstract

Allopolyploidy creates duplicated genomes that drives evolutionary innovation and adaptive diversification under extreme environmental pressures. Although subgenomic architecture is recognized as pivotal in post-polyploid evolution, the mechanisms by which divergent subgenome dynamics shape adaptive potential remain unclear. We investigated how subgenome evolution relates to environmental adaptation in Sinocyclocheilus cavefish, an allotetraploid lineage that repeatedly colonized caves across the karst landscapes of Southwest China. We integrated full-length and short-read transcriptomes from a surface-dwelling species (S. angustiporus) and two independently cave-adapted species (S. microphthalmus and S. furcodorsalis). The two cave dweller species showed consistent B-subgenome dominance in homoeolog expression, whereas the surface species showed balanced expression. Functional enrichment analyses identified lineage-specific functional divergence of dominantly expressed homoeologs. In S. microphthalmus, subgenome-dominant genes were significantly enriched in immunological elements, suggesting an evolutionary shift in immune investment. In S. furcodorsalis, subgenome-dominant genes were significantly enriched in neuromodulatory and metabolic pathways, consistent with energy conservation and sensory regression in nutrient-poor caves. Together, these findings suggest that polyploidy can promote diversification through convergent subgenome dominance. Biased repurposing of distinct stress-responsive modules resolves ancestral genomic conflicts. This, in turn, drives the emergence of lineage-specific functions and links genome duplication to ecological adaptation.

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