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Article

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

by
Ruxiang Wang
1,2,
Ang Li
1,
Shuai Che
1,
Huan Wang
1 and
Shufang Liu
1,*
1
State Key Laboratory of Mariculture Biobreeding and Sustainable Goods, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao 266071, China
2
College of Environmental Science and Engineering, Ocean University of China, Qingdao 266100, China
*
Author to whom correspondence should be addressed.
Biology 2026, 15(4), 295; https://doi.org/10.3390/biology15040295
Submission received: 30 December 2025 / Revised: 5 February 2026 / Accepted: 5 February 2026 / Published: 7 February 2026
(This article belongs to the Special Issue Genetics and Evolutionary Biology of Aquatic Organisms)
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Simple Summary

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.

Abstract

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.

1. Introduction

The typical vertebrate mitochondrial DNA (mtDNA) is a double-stranded, circular molecule, 15–20 kb in length, usually containing 13 protein-coding genes (PCGs), 2 rRNA genes, 22 tRNA genes, and 2 main non-coding regions: the control region (D-loop) and the origin of light-strand replication (OL) [1]. Fish mitochondrial genomes are generally highly conserved in structure, particularly in gene order, which is a key reason for the widespread use of mtDNA as a molecular marker in fish systematics (e.g., for population identification, phylogeography, evolution, and phylogenetic reconstruction) [2,3,4,5]. While advancements in sequencing technology and the expansion of genomic databases have led to increased reporting of mitochondrial gene rearrangements in fishes [6,7], these events remain relatively rare across the group. Although such rearrangements have now been documented in at least 34 teleost families, they collectively represent a small proportion of known species diversity and are often concentrated within specific evolutionary lineages, such as the order Anguilliformes, Notothenioidei and the genus Parupeneus [7,8,9,10]. Mitochondrial gene rearrangements can harbor significant phylogenetic information, as demonstrated in numerous terrestrial vertebrates [11,12,13,14]. In contrast, reported cases in teleost fish remain limited and taxonomically restricted; consequently, studies utilizing gene rearrangements to investigate fish systematics and evolution are still relatively rare.
Mitochondria are central to cellular energy metabolism, producing ATP via the electron transport chain—a process dependent on all 13 protein-coding genes encoded in the mitochondrial DNA (mtDNA) [15]. Functional constraints on these mtDNA genes have been shown to influence adaptation across diverse environments, including those related to locomotion, climate, and elevation [16,17,18]. Of particular relevance to deep-sea colonization, the extreme conditions of high hydrostatic pressure, low temperature, and often limited oxygen availability impose strong selective pressures on energy metabolism [19]. Consequently, adaptive evolution in mitochondrial function has been considered as a key mechanism enabling survival in the deep sea, highlighting the critical link between mtDNA evolution and adaptation to abyssal environments [15].
The snailfish family (Liparidae; Teleostei: Scorpaeniformes: Cottoidei) exhibits extremely high species diversity, comprising 32 genera and over 520 species, making it one of the most rapidly speciating lineages of marine fishes [20,21,22]. Snailfishes are globally distributed, inhabiting depths from the intertidal to the hadal zone in temperate and cold regions, primarily concentrated in the North Pacific, North Atlantic, and polar seas. They are also found in deep-sea bottoms of tropical and subtropical regions near the equator [23,24,25,26]. The two most diverse genera, Careproctus and Paraliparis, are distributed in both Hemispheres, while the genus Liparis is restricted to the Northern Hemisphere [26]. North Pacific waters, particularly near Alaska, harbor an extraordinary diversity of Liparidae, with over 85 species described or known but awaiting formal description [27,28,29]. The discovery and description of new species and new geographic records are ongoing [30,31,32,33,34,35]. However, due to high morphological similarity, phenotypic plasticity, rapid evolutionary rates, broad distributions, and difficulties in obtaining deep-sea samples, taxonomic research on Liparidae has progressed slowly, and the phylogenetic relationships of many species remain controversial [26].
Currently, complete mitochondrial genome data are publicly available for only 13 liparid species [36,37,38], representing merely 2.5% of the family’s diversity, indicating a significant data gap. Liparis chefuensis and Liparis tanakae both belong to the genus Liparis. The former is endemic to the Yellow Sea residing in areas shallower than 30 m [39], while the latter is the only dominant liparid species in Chinese waters residing around 100–121 m [40], making both significant for regional biodiversity studies. However, the lack of complete and accurate mitochondrial genome sequences for these species has impeded phylogenetic and evolutionary studies of Liparidae. Therefore, it is necessary to sequence and analyze their complete mitochondrial genomes to supplement and improve the family’s genomic database.
In summary, this study aims to:
  • Sequence, assemble, and annotate the complete mitochondrial genomes of L. chefuensis and L. tanakae, analyzing their structural characteristics (base composition, codon usage bias, tRNA structure);
  • Construct phylogenetic trees based on mitochondrial PCGs from 15 Liparidae species to clarify their evolutionary relationships;
  • Investigate tRNA rearrangement in the mitochondrial genomes of the genus Liparis, explore their association with phylogeny and habitat depth, and analyze potential formation mechanisms and functional impacts.
Our results provide essential data for the biological research of L. chefuensis and L. tanakae, re-examine liparid phylogenetic relationships, and offer new insights into the deep-sea adaptation mechanisms within the family.

2. Materials and Methods

2.1. Sample Collection, DNA Extraction, and Quality Assessment

Liparis chefuensis was collected from the intertidal zone of the Yellow River Estuary in July 2022 at a depth of 4 m and Liparis tanakae was collected during an autumn survey cruise in the Yellow Sea in September 2021 at a depth of about 110 m. Due to logistical constraints during the research cruise, samples were temporarily stored at −20 °C for the 5–7 day transit period. Upon return, muscle tissue was immediately dissected for DNA extraction.
Genomic DNA was extracted using a TIANamp Marine Animal DNA Kit (Tiangen, Beijing, China). DNA integrity and quality were assessed by 1% agarose gel electrophoresis, and concentration was detected using a Nano-300 nano spectrophotometer (Allsheng, Hangzhou, China).

2.2. Library Construction, Sequencing, and Data Filtering

Libraries were constructed and sequenced on the DNBSEQ platform (MGI, Shenzhen, China). Briefly, DNA was sheared by ultrasonication into 300–400 bp fragments, end-repaired, and ligated to adapters. Following PCR amplification and circularization of the products, libraries were sequenced. Library construction and sequencing were performed by the BGI Genomics Co., Ltd. (Shenzhen, China).
Raw sequencing data with about 45X average depth were processed with SOAPnuke (v1.5.3) [41] to remove adapter sequences, reads shorter than 150 bp, reads with polyX length exceeding 50 bp, reads with N content exceeding 1%, and other low-quality reads, yielding clean data for subsequent assembly.

2.3. Mitochondrial Genome Assembly and Annotation

De novo assembly of the mitochondrial genome was performed using Novoplasty (v4.3.5) [42], with K-mer set to 33 and using the mitochondrial COI gene sequence of L. chefuensis and L. tanakae as a seed (a common choice given its high conservation and utility for anchoring vertebrate mitogenome assemblies). Annotation and visualization of the mitochondrial genome were conducted on MitoFish (v2025.06) [43] using the vertebrate mitochondrial genetic code.
MEGA X (v10.2) [44] was used for base composition statistics and base bias calculation, where GC-skew = (G − C)/(G + C) and AT-skew = (A − T)/(A + T). EMBOSS (v6.6.0) [45] was used for codon usage bias analysis of the whole genome, tRNAs, rRNAs, the control region, and protein-coding genes.
MITOS2 (v2.1.10) [46] was used for annotation and secondary structure prediction of mitochondrial tRNAs, and visualization was performed using VARNA (v3-93) [47].

2.4. Phylogenetic Analysis

Complete mitochondrial genome sequences and annotation files for 13 additional Liparidae species were downloaded from NCBI (Table 1). To ensure consistent and accurate annotation, all downloaded sequences were re-annotated using MitoFish (v2025.06) [43] with the vertebrate mitochondrial genetic code and compared against the original annotations. The 13 PCG sequences for each species were extracted, stop codons were removed, and the genes were concatenated per species to create a dataset for phylogenetic analysis. MAFFT (v7.487) [48] was used for sequence alignment of the concatenated PCGs dataset. IQ-Tree (v2.4.0) [49] was used to construct the ML tree with a codon position partition scheme, automatically selecting the best-fit evolutionary model (GTR + F + I + G4), with parameters -bb 1000 and -alrt 1000 for 1000 ultrafast bootstrap replicates to assess branch support and SH-like aLRT test for branch reliability, respectively. PAUP* (v4.0a169) and MrModeltest2 (v.2.4) were used to find the best model for BI analysis. MrBayes (v3.2.7a) [50] was used to construct the BI tree under the best model GTR + I + G, running 2 independent MCMC chains for 107 generations, sampling every 1000 generations, discarding the first 25% as burn-in, ensuring the average standard deviation of split frequencies was <0.01. Cottus dzungaricus was selected as the outgroup, that belongs to the suborder Cottoidei, and includes the family Liparidae.

3. Results

3.1. Mitochondrial Genome Sequencing and Assembly

Sequencing of L. chefuensis yielded 40,080,591 clean reads, with a Q20 of 97.92%. The final assembled mitochondrial genome was 18,870 bp in length (GenBank accession: PX718959), containing 37 genes: 13 PCGs, 22 tRNA genes, 2 rRNA genes (12S rRNA and 16S rRNA), and 2 main non-coding regions (D-loop and OL) (Figure 1A).
Sequencing of L. tanakae yielded 48,034,225 clean reads, with a Q20 of 98.18%. The final assembled mitochondrial genome was 17,485 bp in length (GenBank accession: PX718960), containing 38 genes: 13 PCGs, 23 tRNA genes, 2 rRNA genes, and 2 main non-coding regions. Compared to the typical vertebrate mitochondrial genome, it possesses one extra tRNA gene, which is a novel structural feature (Figure 1B).

3.2. Phylogenetic Analysis

The ML and BI trees based on 13 PCGs from 15 Liparidae species showed congruent topologies (Figure 2). Species of the genus Liparis formed a monophyletic clade, while species of Pseudoliparis, Crystallichthys, and Careproctus together formed a sister clade. Within the Liparis clade, the subgenus Lyoliparis (represented by L. tessellatus) clustered with L. punctulatus and L. chefuensis, while species of the subgenus Careliparis formed a distinct cluster.
Although some internal nodes received moderate support (Bootstrap < 95%, Posterior Probability < 0.95), the consistent topology between ML and BI analyses suggests the current subgeneric classification of L. chefuensis may require re-evaluation.

3.3. Mitochondrial Genome Structure Comparison and tRNA Rearrangement

Comparative analysis revealed tRNA gene rearrangements in the tRNA gene cluster region between ND2 and COI in all eight studied Liparis species, displaying three distinct patterns (Figure 3):
  • Pattern 1 (Pink branch): Found in shallow-water species (<30 m: L. chefuensis, L. punctulatus, L. tessellatus), with the order tRNATrp-tRNATyr-tRNAAla-tRNAAsn-tRNACys (WYANC);
  • Pattern 2 (Red branch): Found in deep-water Careliparis species (>100 m: L. agassizii, L. bathyarcticus, L. ochotensis, L. gibbus), with the order tRNATrp-tRNAAsn-tRNACys-tRNATyr-tRNAAla-tRNACys (WNCYAC);
  • Pattern 3 (Purple branch): Unique to the deep-water Careliparis species L. tanakae (100–121 m), with the order tRNATrp-tRNAAsn-tRNACys-tRNATyr-tRNAAla-tRNAAla (WNCYAA);
  • Typical Pattern (Black branch): Genera outside Liparis (Pseudoliparis, Crystallichthys, Careproctus) retained the classic vertebrate tRNATrp-tRNAAla-tRNAAsn-tRNACys-tRNATyr (WANCY) arrangement.
Based on the Tandem Duplication and Random Loss (TDRL) model, these patterns can be plausibly explained (Figure 3): The ancestral WANCY cluster likely underwent one or two tandem duplications, followed by random loss of specific genes, giving rise to the observed arrangements. For instance, Pattern 1 could arise from a single duplication followed by loss of the ANC, W, and Y copies. Pattern 2 might result from a single duplication with loss of A, W, N, and Y copies. The complex Pattern 3 in L. tanakae may require two duplications followed by loss of A, W, NCYW, and NCY copies.

3.4. tRNA Structure Analysis

The 22 tRNAs of L. chefuensis had a total length of 1549 bp (66–74 bp per tRNA) and exhibited typical cloverleaf secondary structure (Figure 4). Non-Watson-Crick pairs included 29 G-U and 9 A-C pairs.
The 23 tRNAs of L. tanakae had a total length of 1612 bp (63–74 bp per tRNA) and also formed typical cloverleaf structures (Figure 5). Notably, they contained significantly more non-standard pairs: 44 G-U and 25 A-C pairs.

3.5. General Mitochondrial Genome Features

Detailed structural features and nucleotide composition for L. chefuensis and L. tanakae are provided in Table 2, Table 3, Table 4 and Table 5. Both genomes showed negative GC-skew and positive AT-skew, and an A + T content higher than G + C content, consistent with typical vertebrate mitochondrial genomes.

3.6. Codon Usage Bias

Except for COXI (start GTG), all PCGs in both species used ATG as the start codon. Stop codon usage varied, with incomplete stop codons (T- or TA-) likely completed to TAA via polyadenylation [51].
Relative Synonymous Codon Usage (RSCU) analysis indicated a preference for A/T-ending codons and an avoidance of G/C-ending codons in both species (Figure 6). Leucine, Alanine, and Threonine were the most abundant amino acids.

4. Discussion

4.1. Phylogenetic Relationships and Taxonomic Implications

Our phylogenetic analysis provides new insights into liparid systematics. The distinct clustering of Liparis species separate from Pseudoliparis, Crystallichthys, and Careproctus is consistent with some previous studies using COI, RAD-seq, or morphology [18,52,53,54,55]. However, our results place L. chefuensis within the Lyoliparis clade, contradicting its previous classification in Careliparis [26]. This discrepancy may stem from past misidentification, potentially due to the sympatric distribution and morphological similarity between L. chefuensis and L. tanakae in the Yellow Sea. Morphometric data support this reclassification: the fin ray counts of L. chefuensis (dorsal 36–38, anal 29–31, pectoral 34–36 [40]) differ significantly from the characteristics ranges of Careliparis (dorsal 39–48, anal 31–37, pectoral 35–46 [55]) and do not fully align with Lyoliparis either. Therefore, the subgeneric placement of L. chefuensis warrants further investigation using additional molecular markers (e.g., nuclear genes) and detailed morphological re-examination.

4.2. tRNA Gene Rearrangements: A Putative Adaptive Innovation

While mitochondrial gene order is generally conserved in fishes, rearrangements are increasingly being documented, often in specific clusters like the one between ND2 and COI [4,10,12,13,56,57,58,59,60,61,62,63]. We identified a novel and phylogenetically correlated rearrangement of the WANCY tRNA cluster in Liparis. We hypothesize that the shift from the WYANC pattern observed in shallow-water species to the WNCYAC pattern found in deep-water species represents an important genomic innovation potentially link to adaptation to the deep-sea environment.

4.2.1. Phylogenetic Signal of Rearrangements

Mitochondrial gene rearrangements often contain phylogenetic information. The rearrangement patterns are highly consistent with the phylogenetic relationships within the genus Liparis: the subgenus Lyoliparis and its closely related species branch exhibit the WYANC arrangement, the subgenus Careliparis exhibits the WNCYA + A/C arrangement, while the three genera Pseudoliparis, Crystallichthys, and Careproctus conform to the typical vertebrate WANCY arrangement. Both the rearrangement pattern and the PCGs phylogenetic tree demonstrate the close relationship between L. chefuensis and the subgenus Lyoliparis, correcting the previous taxonomic placement within the subgenus Careliparis.
The perfect congruence between rearrangement patterns and the major phylogenetic clades within Liparis underscores the utility of mitochondrial gene order as a phylogenetic marker. The shared derived state (WNCYAC) unites the deep-water Careliparis species, while the distinct state (WYANC) characterizes the shallow-water clade. This provides independent evidence for the reclassification of L. chefuensis. However, caution is needed, as convergent rearrangements can occur [64], and more data from related taxa are essential.

4.2.2. Correlation with Habitat Depth and Putative Function

The biological function and significance of mitochondrial gene rearrangement phenomena remain unclear but may be related to the action of natural selection in specific habitats [12,52]. The gene rearrangement phenomenon in the genus Liparis might provide insights for related research: The genus Liparis is generally considered to comprise shallow-water fishes, but different subgenera exhibit significant differences in habitat depth: the subgenus Liparis (e.g., L. montagui and L. liparis [65]) are mostly distributed in shallow waters from 0–100 m [52]; whereas the subgenus Careliparis species tend towards deep-sea life, with most distributed in the mesopelagic zone at 400–800 m (e.g., L. bathyarcticus primarily inhabits 400–647 m [55], L. ochotensis has a depth limit of 761 m [66], L. gibbus has a depth limit of 647 m [39]), and a few in the 100–400 m transition zone (e.g., L. agassizii and L. tanakae have depth limits around 100–121 m [39]). These deep-water Careliparis species exhibit the derived WNCYAC rearrangement pattern. Conversely, species inhabiting depths shallower than 30 m (e.g., the subgenus Lyoliparis species L. tessellatus, L. punctulatus [39], and L. chefuensis [40]) all possess the WYANC arrangement.
Thus, we can see that, the correlation between rearrangement patterns and habitat depth is striking. Deep-sea conditions (high pressure, low temperature, hypoxia, low energy) impose extreme demands on energy metabolism. Mitochondria, as cellular power plants, are central to meeting these demands. We hypothesize that the derived gene arrangements (WNCYAC, WNCYAA) in deep-water Liparis species may confer a putative selective advantage by optimizing mitochondrial function. This optimization could occur through increased transcriptional efficiency, enhanced RNA stability, or altered interactions with nuclear-encoded factors, ultimately boosting energy production under extreme conditions. It is crucial to note that this correlation, while compelling, does not establish causality. The proposed adaptive significance of the tRNA rearrangements remains a hypothesis requiring functional validation.

4.2.3. The Unique Case of Liparis tanakae

According to the TDRL model, the formation process of the gene rearrangement in L. tanakae is species specific: compared to gene rearrangements in other Liparidae species, L. tanakae might have undergone one additional gene cluster duplication, resulting in the unique WNCYAA rearrangement pattern. This might be related to its unique adaptation to the Yellow Sea environment, making it the only dominant species of Liparidae in the Yellow Sea region.
Furthermore, the tRNA secondary structures of L. chefuensis contained 29 G-U pairs and 9 A-C non-standard pairs. L. tanakae had even more, with 44 G-U pairs and 25 A-C pairs. Although G-U pairs are non-standard, their stability is higher than other non-Watson-Crick pairs and they might represent intermediate states of compensatory mutations, playing an important role in maintaining RNA structure and function [55,56]. The elevated number of non-standard pairs in the tRNAs of L. tanakae suggests that its mitochondrial tRNAs have undergone notable structural changes during evolution. Such structural changes could potentially influence tRNA stability and might thereby contribute to adaptive capacity in complex marine environments.
This unique genomic structure, coupled with its exceptionally high number of tRNA non-standard base pairs (which may affect stability and function), might reflect a specialized or transitional adaptive state.
A limitation of this study is the lack of data from the nominal subgenus Liparis, typically comprising shallow-water species. Obtaining their mitochondrial genomes is crucial for robustly testing the hypothesis that WYANC is the ancestral shallow-water state.

5. Conclusions

We present the first complete mitochondrial genomes for Liparis chefuensis and Liparis tanakae. Phylogenomic analysis supports the reassignment of L. chefuensis to the subgenus Lyoliparis. Most significantly, we discovered phylogenetically correlated tRNA gene rearrangements within Liparis that are strongly associated with habitat depth. We propose the hypothesis that these rearrangements are not merely neutral markers but may represent genomic adaptations that enhance mitochondrial function, may facilitate the colonization of the deep sea.
This study provides fundamental genetic resources for snailfish research and opens new avenues for investigating the role of mitogenomic architecture in extreme environment adaptation. Future work should focus on: (1) Filling taxonomic gaps, especially sequencing the subgenus Liparis; (2) Broadening taxonomic sampling to test the generality of the depth-rearrangement correlation; (3) Elucidating the molecular mechanisms driving these rearrangements; (4) Employing integrated multi-omics approaches (comparative genomics, transcriptomics, proteomics) and physiological assays to directly test the functional consequences of these rearrangements on mitochondrial performance; and (5) future studies could incorporate comparative analyses of non-coding regions (e.g., the D-loop) to elucidate the mechanisms and evolutionary implications of the substantial size variation observed in liparid mitogenomes.

Author Contributions

S.L. conceived and designed the study, secured funding, and supervised the project; R.W. led the genome assembly, annotation, data analysis, visualization, and phylogenetic interpretation; A.L., S.C. and H.W. contributed to sample collection, data curation; S.L. guided the overall project administration and revised it critically for important intellectual content; R.W. drafted the manuscript with input from A.L., S.C., H.W. and S.L. All authors have read and agreed to the published version of the manuscript.

Funding

This study was supported by the National Key R&D Program of China (2024YFD2400401); the Qingdao Science and Technology Benefiting the People Demonstration Project (24-1-8-xdny-3-nsh); the Central Public-interest Scientific Institution Basal Research Fund, YSFRI, CAFS (NO. 20603022024023).

Institutional Review Board Statement

All fish experiments were conducted in strict accordance with the recommendations provided by the State Science and Technology Commission of the People’s Republic of China of Health Guidelines for the Care and Use of Laboratory Animals (http://www.gov.cn/gongbao/content/2011/content_1860757.htm, accessed on 15 May 2023). The study was approved by the Institutional Animal Care and Use Committee of the Yellow Sea Fisheries Research Institute (YSFRI), Chinese Academy of Fishery Sciences (Approval code: YS-FRI-2021029 in 10 September 2020).

Informed Consent Statement

Not applicable.

Data Availability Statement

The mitochondrial genome supporting this study has been deposited in GenBank (http://www.ncbi.nlm.nih.gov) (accessed on 17 December 2025) under the accession number PX718959-PX718960.

Conflicts of Interest

The authors declare no conflicts of interest.

Abbreviations

The following abbreviations are used in this manuscript:
PCGsProtein-Coding Genes
OLOrigin of Light-strand replication
mtDNAmitochondrial DNA
MLMaximum Likelihood
BIBayesian Inference
TDRLTandem Duplication and Random Loss
RSCURelative Synonymous Codon Usage

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Figure 1. Circular maps of the mitochondrial genomes of Liparis chefuensis (A) and Liparis tanakae (B). The outer and inner circles represent genes encoded by the heavy strand and light strand (dark green: D-loop, light green: rRNA, orange: PCGs, pink: tRNA), respectively. The small interior circles indicate GC skew (red: positive, green: negative).
Figure 1. Circular maps of the mitochondrial genomes of Liparis chefuensis (A) and Liparis tanakae (B). The outer and inner circles represent genes encoded by the heavy strand and light strand (dark green: D-loop, light green: rRNA, orange: PCGs, pink: tRNA), respectively. The small interior circles indicate GC skew (red: positive, green: negative).
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Figure 2. Phylogenetic relationships of Liparidae based on 13 mitochondrial protein-coding genes (red font: L. chefuensis and L. tanakae). The Maximum Likelihood (ML) and Bayesian Inference (BI) trees are shown. Numbers at branches represent ML bootstrap support values (right) and BI posterior probabilities (left).
Figure 2. Phylogenetic relationships of Liparidae based on 13 mitochondrial protein-coding genes (red font: L. chefuensis and L. tanakae). The Maximum Likelihood (ML) and Bayesian Inference (BI) trees are shown. Numbers at branches represent ML bootstrap support values (right) and BI posterior probabilities (left).
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Figure 3. Mitochondrial tRNA gene rearrangements and proposed evolutionary mechanism in Liparidae (red font: L. chefuensis and L. tanakae). Pink indicates Pattern 1, containing shallow-water species; red indicates Pattern 2, containing deep-water species; purple indicates Pattern 3, containing only the deep-water species L. tanakae and the black indicates the Classic pattern. Blue represents ND2 and COI genes. Orange, green, and gray represent tRNA genes (indicated by the single-letter abbreviation of their corresponding amino acid). Red line represents genes randomly lost during evolution.
Figure 3. Mitochondrial tRNA gene rearrangements and proposed evolutionary mechanism in Liparidae (red font: L. chefuensis and L. tanakae). Pink indicates Pattern 1, containing shallow-water species; red indicates Pattern 2, containing deep-water species; purple indicates Pattern 3, containing only the deep-water species L. tanakae and the black indicates the Classic pattern. Blue represents ND2 and COI genes. Orange, green, and gray represent tRNA genes (indicated by the single-letter abbreviation of their corresponding amino acid). Red line represents genes randomly lost during evolution.
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Figure 4. Predicted secondary structures of the 22 tRNAs of Liparis chefuensis. The D-loop, TΨC loop, and anticodon loop are highlighted in blue. The anticodon is marked by a red dot.
Figure 4. Predicted secondary structures of the 22 tRNAs of Liparis chefuensis. The D-loop, TΨC loop, and anticodon loop are highlighted in blue. The anticodon is marked by a red dot.
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Figure 5. Predicted secondary structures of the 23 tRNAs of Liparis tanakae. The D-loop, TΨC loop, and anticodon loop are highlighted in blue. The anticodon is marked by a red dot.
Figure 5. Predicted secondary structures of the 23 tRNAs of Liparis tanakae. The D-loop, TΨC loop, and anticodon loop are highlighted in blue. The anticodon is marked by a red dot.
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Figure 6. Codon usage analysis for Liparis chefuensis and Liparis tanakae. (a,d) Amino acid usage frequency. (b,e) Synonymous codon usage frequency. (c,f) Relative Synonymous Codon Usage (RSCU) values for the 13 mitochondrial PCGs. Asterisks (*) denote stop codons.
Figure 6. Codon usage analysis for Liparis chefuensis and Liparis tanakae. (a,d) Amino acid usage frequency. (b,e) Synonymous codon usage frequency. (c,f) Relative Synonymous Codon Usage (RSCU) values for the 13 mitochondrial PCGs. Asterisks (*) denote stop codons.
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Table 1. Sequence information for all species used in phylogenetic analysis.
Table 1. Sequence information for all species used in phylogenetic analysis.
GenusSpeciesLength (bp)Accession Number
LiparisLiparis agassizii17,896KX156765.1
Liparis bathyarcticus17,358NC_063119.1
Liparis chefuensis18,870PX718959
Liparis gibbus18,466CM082632.1
Liparis ochotensis17,522MG718032.1
Liparis punctulatus16,771LC493935.1
Liparis tanakae17,485PX718960
Liparis tessellatus16,447MK182380.1
CareproctusCareproctus cypselurus16,140LC493936.1
Careproctus phasma15,707OR582698.1
Careproctus rastrinus15,284MW401763.1
Careproctus reinhardti18,218PV357204.1
Careproctus scottae15,707OR582695.1
CrystallichthysCrystallichthys cyclospilus15,711OR582692.1
PseudoliparisPseudoliparis swirei16,593NC_063120.1
CottusCottus dzungaricus16,525MT897993.1
Table 2. Nucleotide composition and base bias in the mitochondrial genome of L. chefuensis.
Table 2. Nucleotide composition and base bias in the mitochondrial genome of L. chefuensis.
RegionT%C%A%G%AT%GC Skew%AT Skew%
PCGs33.0826.6125.9514.3759.03−0.29868−0.12079
rRNA22.7724.7433.2619.2356.03−0.125310.18722
tRNA28.4120.2129.5721.8257.980.038310.02001
Control region31.9413.7143.2511.1075.19−0.10520.15042
Genome30.1624.7930.7514.3060.91−0.268360.00969
Table 3. Nucleotide composition and base bias in the mitochondrial genome of L. tanakae.
Table 3. Nucleotide composition and base bias in the mitochondrial genome of L. tanakae.
RegionT%C%A%G%AT%GC Skew%AT Skew%
PCGs30.5226.2126.2114.4356.73−0.28986−0.07597
rRNA22.7224.3232.4820.4855.20−0.085710.17681
tRNA28.0020.2729.1722.5657.170.053460.02047
Control region36.2920.4042.780.5379.07−0.949350.08208
Genome27.7728.1029.6414.4957.41−0.319560.03257
Table 4. Genome features of L. chefuensis.
Table 4. Genome features of L. chefuensis.
GeneStrandLocationSize
(bp)		Intergenics LengthAnticodonAmino
Acids		Start
Codon		Stop
Codon
tRNAPhe+1–68680GAA
12S rRNA+69–10119430
tRNAVal+1012–1083720TAC
16S rRNA+1084–277116880
tRNALeu+2772–28457489TAA
ND1+2935–39099753 324ATGTAA
tRNAIle+3913–398169−1GAT
tRNAGln−3981–405171−1TTG
tRNAMet+4051–4119690CAT
ND2+4120–516510460 348ATGTA-
tRNATrp+5166–523671171TCA
tRNATyr−5408–54746748TGC
tRNAAla−5523–5591691GTT
tRNAAsn−5593–56657336GCA
tRNACys−5702–57676646GTA
COXI+5814–735815456 514GTGTAA
tRNASer−7365–7435713TGA
tRNAAsp+7439–7511736GTC
COXII+7518–82086910 230ATGT-
tRNALys+8209–8282721TTT
ATPase8+8284–8451168−8 55ATGTAA
ATPase6+8442–91246830 227ATGTA-
COXIII+9125–99097850 261ATGTA-
tRNAGly+9910–9982710TCC
ND3+9983–10,3313490 116ATGT-
tRNAArg+10,332–10,400690TCG
ND4L+10,401–10,697297−7 98ATGTAA
ND4+10,691–12,07213820 460ATGT-
tRNAHis+12,073–12,141690GTG
tRNASer+12,142–12,208683GCT
tRNALeu+12,212–12,284730TAG
ND5+12,285–14,1231839−2 612ATGTAG
ND6−14,120–14,6415220 173ATGTAG
tRNAGlu−14,642–14,710694TTC
Cytb+14,715–15,85111373 378ATGAGA
tRNAThr+15,855–15,92672−1TGT
tRNAPro−15,926–15,995700TGG
Table 5. Genome features of L. tanakae.
Table 5. Genome features of L. tanakae.
GeneStrandLocationSize
(bp)		Intergenics LengthAnticodonAmino
Acids		Start CodonStop
Codon
tRNAPhe+1–68680GAA
12S rRNA+69–10129440
tRNAVal+1013–1084720TAC
16S rRNA+1085–277216880
tRNALeu+2773–284674600TAA
ND1+3447–44219753 324ATGTAA
tRNAIle+4425–449369−1GAT
tRNAGln−4493–456371−1TTG
tRNAMet+4563–4631690CAT
ND2+4632–567710460 348ATGTA-
tRNATrp+5678–57487154TCA
tRNAAsn−5803–58757336GTT
tRNACys−5912–5977661GCA
tRNATyr−5979–604567−4GTA
tRNAAla−6042–610463198TGC
tRNAAla−6303–637169160TGC
COXI+6532–807615456 514GTGTAA
tRNASer−8083–8153713TGA
tRNAAsp+8157–82297322GTC
COXII+8252–89426910 230ATGT-
tRNALys+8943–9016741TTT
ATPase8+9018–9185168−10 55ATGTAA
ATPase6+9176–98586830 227ATGTA-
COXIII+9859–10,6437850 261ATGTA-
tRNAGly+10,644–10,716730TCC
ND3+10,717–11,0653490 116ATGT-
tRNAArg+11,066–11,134690TCG
ND4L+11,135–11,431297−7 98ATGTAA
ND4+11,425–12,80513810 460ATGT-
tRNAHis+12,806–12,874690GTG
tRNASer+12,875–12,941673GCT
tRNALeu+12,945–13,017730TAG
ND5+13,018–14,8561839−4 612ATGTAA
ND6−14,853–15,3745220 173ATGTAA
tRNAGlu−15,375–15,443694TTC
Cytb+15,448–16,58811410 380ATGT-
tRNAThr+16,589–16,66072−1TGT
tRNAPro−16,660–16,729700TGG
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Wang, R.; Li, A.; Che, S.; Wang, H.; Liu, S. Mitogenomic Phylogeny and Adaptive Evolution of Snailfishes (Liparidae) Reveal Correlation Between tRNA Rearrangements and Deep-Sea Colonization. Biology 2026, 15, 295. https://doi.org/10.3390/biology15040295

AMA Style

Wang R, Li A, Che S, Wang H, Liu S. Mitogenomic Phylogeny and Adaptive Evolution of Snailfishes (Liparidae) Reveal Correlation Between tRNA Rearrangements and Deep-Sea Colonization. Biology. 2026; 15(4):295. https://doi.org/10.3390/biology15040295

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Wang, Ruxiang, Ang Li, Shuai Che, Huan Wang, and Shufang Liu. 2026. "Mitogenomic Phylogeny and Adaptive Evolution of Snailfishes (Liparidae) Reveal Correlation Between tRNA Rearrangements and Deep-Sea Colonization" Biology 15, no. 4: 295. https://doi.org/10.3390/biology15040295

APA Style

Wang, R., Li, A., Che, S., Wang, H., & Liu, S. (2026). Mitogenomic Phylogeny and Adaptive Evolution of Snailfishes (Liparidae) Reveal Correlation Between tRNA Rearrangements and Deep-Sea Colonization. Biology, 15(4), 295. https://doi.org/10.3390/biology15040295

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