# Mitogenomic Phylogeny and Adaptive Evolution of Snailfishes (Liparidae) Reveal Correlation Between tRNA Rearrangements and Deep-Sea Colonization

## TL;DR

This study shows that snailfishes' mitochondrial gene rearrangements are linked to their deep-sea adaptation, offering new insights into marine fish evolution.

## Contribution

The paper identifies a correlation between tRNA gene rearrangements and deep-sea colonization in snailfishes.

## Key findings

- Shallow-water snailfishes have a different tRNA gene order compared to deep-water species.
- tRNA rearrangements in deep-water snailfishes may result from duplication and gene loss events.
- L. tanakae shows structural divergence in tRNA secondary structures with non-canonical base pairs.

## Abstract

We sequenced and analyzed the complete mitochondrial genomes of two snailfish species, Liparis chefuensis and Liparis tanakae, from the Yellow Sea. Our study reveals that these fishes show unique rearrangements in their mitochondrial tRNA genes, which are closely linked to their habitat depths. Shallow-water species exhibit one gene order, while deep-water species show a different arrangement. This suggests that changes in mitochondrial gene organization may help these fishes adapt to extreme deep-sea environments. Our findings provide valuable genetic data for snailfish identification and deepen our understanding of how marine organisms evolve to survive in the deep ocean.

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 tRNATrp-tRNATyr-tRNAAla-tRNAAsn-tRNACys (WYANC) arrangement, whereas deep-water species (>100 m) display the derived tRNATrp-tRNAAsn-tRNACys-tRNATyr-tRNAAla-tRNACys/tRNAAla (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.