Mitogenomic Phylogeny and Adaptive Evolution of Snailfishes (Liparidae) Reveal Correlation Between tRNA...

The snailfish family (Liparidae) represents one of the most rapidly speciating and ecologically diverse lineages of marine fishes, with species distributed across a broad bathymetric range from intertidal zones to the hadal depths. Despite their ecological and evolutionary significance, phylogenetic relationships and adaptive mechanisms within Liparidae remain poorly resolved due to morphological conservatism, phenotypic plasticity, and limited genomic resources due to challenges such as sampling difficulties and a reliance on partial mtDNA markers. In this study, we sequenced, assembled, and annotated the complete mitochondrial genomes of two snailfish species, Liparis chefuensis and Liparis tanakae, collected from the Yellow Sea. The mitogenome of L. chefuensis is 18,870 bp in length, encoding 13 protein-coding genes (PCGs), 2 rRNAs, and 22 tRNAs, while that of L. tanakae spans 17,485 bp and contains 13 PCGs, 2 rRNAs, and 23 tRNAs. Phylogenetic reconstruction based on the concatenated sequences of 13 mitochondrial PCGs from 15 liparid species revealed that L. chefuensis clusters within the subgenus Lyoliparis, contradicting its previous classification under Careliparis and suggesting a need for taxonomic reassessment. Notably, we identified distinct patterns of tRNA gene rearrangement in the cluster between ND2 and COI, which suggest a link to both phylogeny and habitat depth. Shallow-water species (<30 m) possess the tRNA^Trp-tRNA^Tyr-tRNA^Ala-tRNA^Asn-tRNA^Cys (WYANC) arrangement, whereas deep-water species (>100 m) display the derived tRNA^Trp-tRNA^Asn-tRNA^Cys-tRNA^Tyr-tRNA^Ala-tRNA^Cys/tRNA^Ala (WNCYAC/A) configurations. These rearrangements are hypothesized to originate from tandem duplication events followed by random gene loss, potentially reflecting adaptive evolution to deep-sea environments. Additionally, L. tanakae exhibits a markedly higher number of non-canonical G-U and A-C base pairs in its tRNA secondary structures, indicating substantial structural divergence. Our findings not only provide essential mitogenomic resources for snailfish systematics and species identification but also propose that tRNA rearrangements in mitochondrial genomes may serve as genomic innovations facilitating deep-sea colonization. This study enhances our understanding of mitochondrial genome evolution and environmental adaptation in marine fishes.