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IntroductionWith 78 species, Sinocyclocheilus cavefish constitute the largest cavefish radiation in the world. They exhibit remarkable morphological diversity across three habitat types: surface (surface morphs, normal-eyed, variably colored), exclusively-cave-dwelling (stygobitic morphs, eyeless, depigmented), and intermediate between cave and surface (stygophilic morphs, micro-eyed, partially depigmented). Distinctive traits of Sinocyclocheilus include variations in eye and skin conditions associated with their habitat, despite the role of the skin in sensing environmental changes, its habitat correlates are less understood, compared to the well-studied eye conditions.MethodsHere, we analyzed the correlation between Sinocyclocheilus skin morphology and its habitat, utilizing morphological and transcriptomics-based methods. We generated skin RNA-sequencing data for nine species and integrated those with existing data from five additional species. These 14 species represent the primary clades and major habitats of these cavefish.ResultWe identified 7,374 orthologous genes in the skin transcriptome data. Using a comparative transcriptomics approach, 1,348 differentially expressed genes (DEGs) were identified in the three morphotypes. GO and KEGG enrichment analyses suggested that these genes were mainly involved in energy metabolism, immunity and oxidative stress-related functions. Genes related to immune, apoptotic, and necrotic functions were identified through positive selection analysis of orthologous genes. The maximum likelihood phylogenetic tree, based on 1,369, single-copy orthologous genes of the species, was largely concordant with the currently established RAD-seq and mt-DNA based phylogenies. Species with higher cave dependence present lighter coloration, fewer dark blotches, and diminished scale morphology and coverage. We also found that differences in skin gene expression and positive selection effects may have contributed to the degradation of skin color and scales.DiscussionOur study highlights the significance of habitat in shaping skin metabolism, pigmentation variation, and morphology while offering insights into the molecular mechanisms driving these habitat-specific adaptations in Sinocyclocheilus. These findings underscore the transcriptional variation in adapting to diverse environments and contribute to future studies on the evolution and ecology of cavefish.

Cavefish evolved a series of distinct survival mechanisms for adaptation to cave habitat. Such mechanisms include loss of eyesight and pigmentation, sensitive sensory organs, unique dietary preferences, and predation behavior. Thus, it is of great interest to understand the mechanisms underlying these adaptability traits of troglobites. The teleost genus Sinocyclocheilus (Cypriniformes: Cyprinidae) is endemic to China and has more than 70 species reported (including over 30 cavefish species). High species diversity and diverse phenotypes make the Sinocyclocheilus as an outstanding model for studying speciation and adaptive evolution. In this study, we conducted a comparative transcriptomics study on the brain tissues of two Sinocyclocheilus species (surface-dwelling species – Sinocyclocheilus malacopterus and semi-cave-dwelling species – Sinocyclocheilus rhinocerous living in the same water body. A total of 425,188,768 clean reads were generated, which contributed to 102,839 Unigenes. Bioinformatic analysis revealed a total of 3,289 differentially expressed genes (DEGs) between two species Comparing to S. malacopterus, 2,598 and 691 DEGs were found to be respectively, down-regulated and up-regulated in S. rhinocerous. Furthermore, it is also found tens of DEGs related to cave adaptability such as insulin secretion regulation (MafA, MafB, MafK, BRSK, and CDK16) and troglomorphic traits formation (CEP290, nmnat1, coasy, and pqbp1) in the cave-dwelling S. rhinocerous. Interestingly, most of the DEGs were found to be down-regulated in cavefish species and this trend of DEGs expression was confirmed through qPCR experiments. This study would provide an appropriate genetic basis for future studies on the formation of troglomorphic traits and adaptability characters of troglobites, and improve our understanding of mechanisms of cave adaptation.