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Article

Chromosome-Level Genome Assembly of the Rough-Toothed Dolphin (Steno bredanensis)

by
Haiyu Gao
1,2,†,
Hui Kang
1,2,†,
Yaolei Zhang
3,
Jiahao Wang
3,
Wenzhi Lin
1,
Peijun Zhang
1,
Mingli Lin
1,
Mingming Liu
1,
Guangyi Fan
3 and
Songhai Li
1,*
1
Marine Mammal and Marine Bioacoustics Laboratory, Institute of Deep-sea Science and Engineering, Chinese Academy of Sciences, Sanya 572000, China
2
University of Chinese Academy of Sciences, Beijing 100049, China
3
BGI (Beijing Genomics Institute)-Qingdao, BGI (Beijing Genomics Institute)-Shenzhen, Qingdao 266555, China
*
Author to whom correspondence should be addressed.
†
These authors contributed equally to this work.
J. Mar. Sci. Eng. 2023, 11(2), 418; https://doi.org/10.3390/jmse11020418
Submission received: 21 December 2022 / Revised: 4 February 2023 / Accepted: 10 February 2023 / Published: 15 February 2023
(This article belongs to the Special Issue Recent Advances in Marine Mammal Research in Indo-Pacific Area)
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Abstract

:
The rough-toothed dolphin (Steno bredanensis), the single extant species of the genus Steno, inhabits tropical and subtropical oceans. It is an attractive species for studying aquatic adaptation and evolution. The latest advances in high-throughput sequencing are transforming the study of marine mammals and contributing to understanding various phenomena at the species and population level by determining high-quality genomes. Here, to comprehensively understand the genetic features and explore the molecular basis of aquatic adaption, the chromosome-level genome assembly and comparative genomics analyses of S. bredanensis were performed. The 2.30 Gb final genome assembly of S. bredanensis (scaffold N50 length of 105.53 Mb) was obtained using single-tube long fragment read (stLFR) and Hi-C technologies. The genome assembly clearly revealed the preservation of large chromosomal fragments between S. bredanensis and the melon-headed whale (Peponocephala electra). The S. bredanensis genome contained 19,451 predicted protein-coding genes, of which about 92.33% have functional annotations. The genome assembly and gene sets showed high completeness, with a BUSCO score of 90.6% and 97.3%, respectively. We also identified several positively selected genes specific to S. bredanensis, which may be related to fat cell differentiation, tooth morphogenesis, and immunoregulatory activity. Finally, the demographic dynamics of S. bredanensis were estimated by the pairwise sequentially Markovian coalescent (PSMC) model and found that the population was affected by the climate at the time. We demonstrated that improved continuity and accuracy of the assembled sequence warranted the adoption of this chromosome-level genome as the reference genome and advanced the understanding of genetic features of the rough-toothed dolphin, which will be essential for future evolutionary studies and the protection of this species.

1. Introduction

The rough-toothed dolphin (Steno bredanensis; Cuvier in Lesson, 1828) was distributed mainly in tropical and subtropical waters around the world, where it is generally found in deep waters (1000–3000 m) [1], but populations in certain places also live in the shallow nearshore waters [2]. S. bredanensis are relatively robust compared to other dolphins, with long narrow beaks, well-developed dorsal fins and flippers, and extremely fast swimming speeds [3]. A possible morphological adaptation to preying upon mahimahi may have led to the development of uniquely rugose teeth in S. bredanensis. Similar to other dolphins, S. bredanensis possess some aquatic adaptations, such as a thick layer of insulating fat under the skin needed to regulate body temperature to adapt to changes in the temperature of seawater at different depths. They usually occur in groups of 10–20, with reports of up to more than 100 individuals. In addition, they are sociable and curious cetaceans with complex interspecific relationships [3,4]. As a worldwide species, S. bredanensis is listed by the IUCN as a species of Least Concern [5]. Despite this listing, a large number of stranding events have been recorded and may have greater impacts than are currently known [6].
As sequencing technology advances, it is increasingly recognized that reference genomes make important contributions to the identification, characterization, and conservation of biodiversity [7,8,9], especially for naturally rare species, such as marine mammals. Meanwhile, genome information of marine mammals is of interest for further investigation, as these species could contribute to understanding the distinct morphological or physiological adaptations by uncovering the genomic features, which improved our understanding of evolutionary relatedness and aided efforts for species conservation and management.
Previous studies on S. bredanensis mainly used the mitochondrial genome and traditional molecular genetic markers (such as microsatellites) to discover the genetic structure and differentiation time of different populations [10,11,12]; however, information about the S. bredanensis genome is limited. Therefore, a chromosomal-level assembly of S. bredanensis was sequenced and assembled with a combination of single-tube long fragment read (stLFR) and Hi-C sequencing technologies, which allowed us to compare the genomic structure between dolphins and infer the population history of the species. We also verified the quality of genome assembly and discovered evolutionary events by collinearity analysis of S. bredanensis and melon-headed whale and cattle. In addition, the study focused on the expansion or contraction gene family and positive selection genes, demonstrating the possibility of finding genes involved in aquatic adaptation in the rough-toothed dolphin. In this study, a high-quality assembly of the genome of S. bredanensis was conducted to further understand its genetic characteristics and explore the molecular mechanism of its aquatic adaptation.

2. Materials and Methods

2.1. Sample Collection and Genome Sequencing

A stranded adult male rough-toothed dolphin (S. bredanensis) individual muscle tissue was collected in June 2019, in Sanya, China (18 °N, 109 °E), for genome sequencing. The dolphin was about 2.20 m in length and 73.50 kg in weight. All sample collection and use protocols were approved by the Institute of Deep-sea Science and Engineering, Chinese Academy of Sciences (ethical statement number: IDSSE-SYLL-MMMBL-01). The DNA of S. bredanensis was then extracted using the approach of cetyltrimethylammonium bromide (CTAB) [13].
The quality and quantity of DNA were examined using Pulsed Field Gel Electrophoresis (PFGE) and Qubit Fluorometer, where high-quality purified DNA with an average length of 50 Kb was further used to construct a stLFR library using the MGIEasy stLFR Library Prep kit (PN: 1000005622), according to the instructions [14]. Hi-C library was constructed with muscle tissue of the same individual [15]. On each dataset, pair-end sequencing, with a read length of 100 bp on the BGISEQ-500, was performed.

2.2. Genome Assembly

Before the genome assembly, jellyfish (v2.2.6) [16] was used to measure the total occurrences of 17-mer in both strands of the stLFR sequence, and GenomeScope (v2.0) [17] was used to calculate the size, heterozygosity, and repeat content of the S. bredanensis genome. Supernova (v2.1.1) [18] was first used to assemble S. bredanensis genomes with default parameters based on the stLFR2 Supernova pipeline (https://github.com/BGI-Qingdao/stlfr2supernova_pipeline) (accessed on 15 July 2021). Next, Redundans (v0.14a) [19] was used to selectively remove alternative heterozygous sequences, and then stLFR-GapCloser (https://github.com/BGI-Qingdao/stLFR_GapCloser) (accessed on 10 August 2021) [20] was used for filling gaps. For the Hi-C data, we used Hic-Pro pipeline [21] with default parameters to identify all valid paired reads, combined them with filled genome sequences, and assembled them at the chromosome level. Then, we used the 3D-DNA pipeline [22] to sort and orient assembled DNA fragments.

2.3. Genome Annotation

The repetitive sequence annotation method of this study is divided into de novo prediction and homologous sequence alignment. The de novo prediction for sequences and interspersed repeats were completed by default parameters of software RepeatModeler (v1.0.8) [23] and LTR_FINDER (v1.0.6) [24] (for long terminal repeats, LTRs). Then, we adopted RepeatMasker (v4.0.5) [23] to identify and classify repeat elements based on predicted sequences from the de novo prediction. In homology-based detection, DNA and protein transposable elements (TEs) were identified using RepeatMasker (v4.0.5) and RepeatProteinMask (v4.0.5) to search the Repbase database [25], respectively. Tandem repeats were predicted by Tandem Repeat Finder (v4.0.7) [26].
In order to perform TEs identification at DNA and protein levels, we identified sequences that were similar to known repeated sequences. We used two approaches to predict the gene structure—homology prediction and de novo annotation. For de novo prediction, Augustus (v3.3) [27] and Genescan (v1.0) [28] were used. The homology prediction used the GeneWise (v2.4.1) [29] to align the nonredundant protein sequences of eight species, including common bottlenose dolphin (Tursiops truncatus), killer whale (Orcinus orca), sperm whale (Physeter macrocephalus), common minke whale (Balaenoptera acutorostrata), baiji (Lipotes vexillifer), narrow-ridged finless porpoise (Neophocaena asiaeorientalis), cattle (Bos taurus), and goat (Capra hircus). The final consensus protein-coding gene set was generated by integrating all predicted gene models using EvidenceModeler (EVM) [30].
The protein sequences of the rough-toothed dolphin were compared with the commonly used protein databases, including SwissProt [31], KEGG [32], TrEMBL [31], InterPro [33], Non-redundant (NR) [34], and Gene Ontology (GO) [35].

2.4. Assessment of the Assembly and Annotation

The SOAP (v2.27) [36] was used to compare the sequences fragment library with the assembled genome, and a sequencing depth distribution map was then generated. If the actual sequencing depth consists of the sequencing depth estimated by k-mer, it means that the assembled genome size of S. bredanensis has sufficient integrity for analysis. The Benchmarking Universal Single-Copy Orthologs (BUSCO, v3.0) [37] and mammalia_odb9 lineage datasets were used to assess the quality and integrity of the final genome assembly and gene set. To show the accuracy of genome assembly, we aligned our assembly to the melon-headed whale (Peponocephala electra) and cattle (B. taurus) using Lastz (v1.02.00) (http://www.bx.psu.edu/miller_lab/dist/) (accessed on 20 September 2021) [38] and visualized using RectChr (v1.30) (https://github.com/BGI-shenzhen/RectChr) (accessed on 20 September 2021).

2.5. Evolution Analysis

In order to reveal the evolutionary status of S. bredanensis in cetaceans, we constructed homologous gene sets and carried out genome phylogenetic analysis with several cetaceans. The genome data include ten toothed whales and one Baleen whale: Risso’s dolphin (Grampus griseus), false killer whale (Pseudorca crassidens), narrow-ridged finless porpoise (N. asiaeorientalis), baiji (L. vexillifer), Commerson’s dolphin (Cephalorhynchus commersonii), killer whale (O. orca), melon-headed whale (P. electra), rough-toothed dolphin (S. bredanensis), narwhal (Monodon monoceros), Atlantic white-sided dolphin (Lagenorhynchus acutus), and common minke whale (B. acutorostrata) (see Table S1 for details). Gene families were identified using TreeFam with default parameters [39]. We used 5715 single-copy orthologous genes to construct a phylogenetic tree by PhyML [40], with B. acutorostrata as an outgroup. Divergence times were estimated by MCMCTREE (v4.4) [41], and calibration divergence times were used between O. orca and L. acutus (6.3~10.7 Mya) and B. acutorostrata and L. vexillifer (35.4~42.5 Mya) [42,43]. Computational Analysis of gene Family Evolution (CAFÉ) (v2.1) [44] was used to perform the expansion and contraction of each gene family. The p-values were calculated, and the expanded or contracted gene families were considered significant when p-values < 0.05. To identify positive selection genes (PSGs) in the S. bredanensis genome, we selected S. bredanensis as the foreground branch with the other ten cetaceans as the background branch. The branch-site likelihood ratio test was performed using codeml’s free ratio model in PAML (v4.8) [41]. Genes with p-values less than 0.05 were considered as candidates for positive selection.

2.6. Demographic History

We estimated effective population size (Ne) over time using the pairwise sequentially Markovian coalescent (PSMC) [45]. Diploid genome reference was constructed using “samtools mpileup -C50” and “vcfutils.pl vcf2fq − d 5 − D 1000”. We inferred the demographic history using PSMC with parameters ‘−N25 − t15 − r5 − p4 + 25*2 + 4 + 6′ and tested the robustness of effective population size estimates using 100 bootstrap replicates. The estimated generation time (g) and mutation rate per generation per site (μ) were set to 19.6 [46] and 1.3 × 10−8 (estimated using r8s) [47].

3. Results and Discussion

We generated 302.31 Gb raw data (~131×) using the stLFR sequencing strategy (Table S2) and then filtered the raw reads, retrieving a total of 155.41 Gb clean data, and this clean data was used for later assembly. Before assembling the genome, the genome size of S. bredanensis was estimated to be 2.54 Gb and its heterozygosity was 0.31% (Figure S1). We assembled a draft genome sequence of 2.30 Gb, in which contig N50 was 99.39 Kb and scaffold N50 was 43.88 Mb, respectively. The single peak distribution of sequencing depth as a function of GC content (Figure S2) indicates that the assembly was not contaminated and did not have redundancy. Based on 154.96 Gb Hi-C data, we obtained a chromosome-level genome assembly with a total length of 2.30 Gb (scaffold N50 of 105.53 Mb and contig N50 of 99.30 Kb), and 98.17% of the assembled genome was anchored onto 22 chromosomes, consistent with the general Delphinidae karyotype [48] (Figure 1, Table S3). The chromosomes ranged from 35.26 Mb to 182.78 Mb (Table S4) and had a high consistency in length with the karyotypes (Figure 1). These data could show that chromosomes were anchored in good quality. The assembled genome of this study was similar in size to the published S. bredanensis genome, with some statistics such as scaffold N50 and most chromosome lengths being slightly longer than the published genome (Tables S3 and S4). A comparison of the high-quality genome of P. electra with that of S. bredanensis showed good coverage and synteny, indicating the accuracy of the S. bredanensis genome at the chromosome level (Figure 2). Comparing S. bredanensis and B. taurus, we found several fission and fusion events. For example, Chr16 in the S. bredanensis genome is a fusion of Chr26 and Chr28 in B. taurus (Figure 2). Additionally, the number of syntenic blocks suggested that the X chromosome is conserved between cetaceans and B. taurus (Figure 2).
Approximately 36.58% of the assembled S. bredanensis genome was annotated as transposable elements (TEs), including long interspersed nuclear elements (LINEs; 33.28%), short interspersed nuclear elements (SINEs; 0.41%), Long Terminal Repeat (LTRs; 6.26%), and DNA transposons (1.37%) (Table S5). The LINEs are the most abundant transposable elements. After masking the identified repeat elements, 19,451 protein-coding genes were predicted for the S. bredanensis genome (Table S6). The average mRNA, coding sequence, exon, and intron length distribution were like those of other cetaceans (Figure S3). Of the 19,451 predicted genes, ~92.33% were functionally annotated to at least one of the databases such as InterPro, GO, and KEGG (Table S7), indicating the high accuracy of gene prediction. The completeness of the rough-toothed genome assembly and gene set was evaluated as 90.6% and 97.3% (Table S8), with BUSCO, which was in the expected range for a high-quality mammalian genome and comparable to the genomes of several other marine mammals [43]. Thus, the S. bredanensis genome is a well-assembled and nearly complete reference genome, which is highly accurate for subsequent evolutionary analysis.
To identify the relationships between S. bredanensis and other related species, we constructed a maximum likelihood (ML) tree using 5715 single-copy genes of 11 species (Figure 3). All branches had 100/100 bootstrap support and showed that S. bredanensis was closely related to G. griseus and C. commersonii. This tree is consistent with the recent large-scale phylogenomic analysis of cetaceans [49,50]. For example, McGowen et al. constructed the phylogenomic tree, resulting in 3191 separate partitions by gene to show the same topologies of S. bredanensis, G. griseus, and C. commersonii. Based on reference time points from previous studies [42,43], we estimated that S. bredanensis and G. griseus diverged ~7.0 Mya. By comparing eleven cetaceans, we discovered that 153 gene families were expanded or contracted in S. bredanensis (p < 0.05). We observed expansion genes enriched in several GO terms, including “social behavior (GO:0035176)”, “neuromuscular process (GO:0050905)”, and “brain development (GO:0007420)” (p < 0.01) using Metascape [51] (www.metascape.org, accessed on 20 September 2021) (Figure S4), which may reflect relevant adaptations in S. bredanensis. Of these gene families, we found the NADH-ubiquinone oxidoreductase chain 5 (MT-ND5) gene expanded with 11 copies in S. bredanensis. MT-ND5 is important for creating adenosine triphosphate (ATP), which may be related to the high ATP demands and high-energy behaviors of S. bredanensis, such as chases.
Using evolutionary pressure analysis, we found that relative to the other ten cetaceans, 175 positively selected genes (PSGs) exist in S. bredanensis (Table S9). These genes were significantly (p < 0.01) enriched in some GO terms such as “fat cell differentiation (GO:0045444)” and “T cell differentiation (GO:0030217)” (Table S10). Seven genes ((BBS1 (Bardet-Biedl syndrome 2 protein), BBS2 (Bardet-Biedl syndrome 2 protein), TCF7L2 (transcription factor 7-like 2), RETREG1 (Reticulophagy regulator 1), OSBPL11 (Oxysterol-binding protein-related protein 11), C1QTNF3 (Complement C1q tumor necrosis factor-related protein 3), and METRNL (Meteorin-like protein)) associated with “fat cell differentiation (GO:0045444)” were found to be under positive selection in the S. bredanensis genome, suggesting that these genes might contribute to the adipogenesis in S. bredanensis. Phenotypic observations in marine mammals have previously shown that all marine mammals have blubber, an insulating, subcutaneous layer of adipose tissue and connective tissue, which is critical for limiting heat loss [52]. In previous studies, BBS genes were shown to exhibit a unique and specific expression pattern during adipogenesis [53]. As the lipid metabolism-related gene, RETREG1, was expressed significantly higher in obese pigs, it has been demonstrated that the function of FAM134B causes obesity to happen in mice [54,55,56]. OSBPL11 is involved in regulating ADIPOQ and FABP4 levels in differentiating adipocytes and also in the regulation of triglyceride storage in adipocytes [57]. C1QTNF3, a member of the C1q/TNF-related protein family, was found in mice to be one of the most up-regulated genes encoding secreted proteins in tumor-related groin adipose tissue in obesity caused by a high-fat diet [58]. METRNL has been found in previous studies to be an adipokine that is plentiful in subcutaneous white adipose tissue [59,60], which can enhance white fat browning [61]. Notably, we found that TCF7L2, which is associated with odontogenesis of the dentin-containing tooth (GO:0042475) was under positive selection in S. bredanensis. One of the causes of human cartilage degeneration is the excessive expression of TCF7L2 orthologue (TCF4) in chondrocytes [62], thus, implying that TCF7L2 may be related to special tooth morphogenesis of irregular folds and furrows on the crown surface of S. bredanensis. Furthermore, five genes (CD74 (CD74 molecule), IL15 (Interleukin-15), LY9 (T-lymphocyte surface antigen Ly-9), LMBR1L (Protein LMBR1L), IL21 (Interleukin-21)) were identified as candidate positive selection genes related to the immunoregulatory activity. Cetaceans must have encountered dramatic changes in pathogens during the transition from terrestrial to marine environments. These challenges from changing environmental pathogens exerted intensified selection pressure on the genomes of cetaceans, particularly on genes related to the immune system, as previously reported [63,64]. CD74, as an MHC (major histocompatibility complex) class II chaperone, has several biological functions in physiological and pathological situations, such as participating in other non-MHC II protein trafficking and regulating T-cell and B-cell developments [65]. Previous studies using the immune-related genes MHC have shown that the immune system of cetaceans has undergone adaptive evolution, particularly in rapid radiation lineages, such as existing dolphins [66]. IL15 is a cytokine that plays an important role in immune responses to microbial invaders and parasites by modulating immune cells in the immune system [67]. In previous studies, IL15 was used to assess the immune status of marine mammals, such as pinnipeds [68]. LY9, the member of the signaling lymphocytic activation molecule family (SLAMF), is associated with the regulation of multiple events of both innate and adaptive immune responses [67]. Many studies have reported the interaction between cetacean morbillivirus (CeMV) and their major cellular receptor, the SLAM gene family [69,70]. LMBR1L has been reported to play an important role in lymphogenesis and lymphoid activation as a negative regulator of the Wnt/β-catenin pathway [71]. IL21 may play a role in stimulating interferon gamma production in T-cells and NK cells in synergy with IL15 [72,73]. Therefore, it is crucial to determine the putative function of PSGs of S. bredanensis in further studies.
PSMC analysis generated well-defined population dynamics over its evolutionary history, from 3000 to 10 thousand years ago (Kya). There is a higher peak at ~7000 Kya (Figure 4), although it is probably because this is the time of the split from G. griseus, such an ancient region of differentiation implies highly differentiated allelic fragments (highly heterozygous). These highly heterozygous fragments may also come from balanced selection [45]. After this time, there was a significant reduction in its historical population, similar to sperm whales and Chinese white dolphins (i.e., Indo-Pacific humpback dolphins, Sousa chinensis), as discussed in previous studies [74,75]. The other peak at ~200 Kya (Figure 4) occurred during the Pleistocene, probably because global climate change and associated sea level changes during this period altered sea surface temperature and current flow, resulting in a change in resource availability [76]. The management and continued monitoring efforts are essential to ensure the conservation of S. bredanensis along the South China Sea. The results may contribute to the formation of a benchmark for further research in the region.
Nonetheless, some of our data should be interpreted with caution. For example, more evidence is needed to show the relationship between some positive selection genes disclosed in our study and the specific tooth morphology, lipogenesis, and immunoregulatory activity of the rough-toothed dolphin, such as combination with transcriptome, regulatome, metabolome, and proteome data. Integrating multi-omics data could resolve the genetic basis of complex traits of aquatic adaptation, highlight key regulatory genes, and predict potentially important genes for future study. The other concern is the lack of functional experiments, which could validate these genes and further contribute to investigating the evolutionary mechanisms of these complex traits.
The successful implementation of species conservation plans depends on correctly determining the taxonomic status of conservation targets [77]. Whole genome resequencing (WGR) is a powerful way to solve fundamental evolutionary biology problems that have not been completely solved by traditional methods [78]. Our study on the genome of S. bredanensis enriched the resources of the cetacean genome, allowing us to better understand the evolutionary relationship among cetaceans; moreover, past effective population studies have helped us understand how climate affects species populations. We expect that this reference genome should also provide a useful tool for continued population studies of S. bredanensis and may contribute to the understanding and conservation of global biodiversity.

4. Conclusions

In summary, we have generated an improved high-quality genome assembly of S. bredanensis with additional insights into genome features, contributing to documenting the evolutionary history of S. bredanensis and other cetaceans. Furthermore, we identified hundreds of candidate positive selection genes, some of which were related to fat cell differentiation, tooth morphogenesis, and immunoregulatory activity. The genome assembly in this study will offer valuable references for comparative genomics available for cetaceans in future work.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/jmse11020418/s1. Figure S1: The k-mer analysis curve generated by GenomeScope; Figure S2: GC content and sequencing depth of S. bredanensis genome; Figure S3: Distribution of gene, CDS (coding sequences), exon, and intron lengths in genomes from S. bredanensis and other four cetaceans; Figure S4: Functional enrichment results of expansion genes in S. bredanensis genome; Table S1: Basic information on additional species used in this study; Table S2: Statistics of sequencing raw data for S. bredanensis; Table S3: Comparison of S. bredanensis genome with published genome; Table S4:Length of assembled 22 chromosomes of S. bredanensis genome compared to those previously published; Table S5: Summary of transposable elements in S. bredanensis genome; Table S6: Summary statistics of annotated genes in S. bredanensis genome; Table S7: Summary statistics of functional annotation for predicted genes in public databases; Table S8: Summary of BUSCO analysis matched to the 4104 mammalian BUSCOs; Table S9: 175 positive selection genes of S. bredanensis genome; Table S10: Gene enrichment analyses of positive selection genes in S. bredanensis.

Author Contributions

Conceptualization, S.L.; methodology, H.G., H.K. and Y.Z.; software, H.G., H.K., Y.Z., G.F. and J.W.; formal analysis, H.G. and H.K.; investigation, H.G.; resources, S.L.; data curation, S.L. and H.G.; writing—original draft preparation, H.G. and H.K.; writing—review and editing, W.L., P.Z., M.L. (Mingli Lin), M.L. (Mingming Liu) and S.L.; visualization, H.G.; supervision, S.L.; project administration, S.L. and H.G.; funding acquisition, S.L. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by Hainan Province Science and Technology Special Fund (ZDKJ2019011).

Institutional Review Board Statement

The animal study protocol was approved by the Institutional Ethics Committee of the Institute of Deep-sea Science and Engineering, Chinese Academy of Sciences (ethical statement number: IDSSE-SYLL-MMMBL-01).

Informed Consent Statement

Not applicable.

Data Availability Statement

Requests for the data presented in this article should be directed to S.L. ([email protected]).

Acknowledgments

The authors are deeply grateful to Zixin Yang, Xiaoming Tang, Wanxue Xu, Zhengzhi Wei, Yongchuan Li, Xiaoyu Huang, and Zhihuan Li for helping during the sample collection.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Hi-C heatmap of genomic interactions. Interactions between two locations are depicted by a dark blue pixel.
Figure 1. Hi-C heatmap of genomic interactions. Interactions between two locations are depicted by a dark blue pixel.
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Figure 2. Chromosome-level synteny analysis between S. bredanensis and P. electra and B. taurus.
Figure 2. Chromosome-level synteny analysis between S. bredanensis and P. electra and B. taurus.
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Figure 3. (Left) Phylogenetic tree constructed using the maximum likelihood based on 5715 single-copy genes. (Right) Gene family clusters among 11 cetaceans.
Figure 3. (Left) Phylogenetic tree constructed using the maximum likelihood based on 5715 single-copy genes. (Right) Gene family clusters among 11 cetaceans.
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Figure 4. Demographic history of S. bredanensis, constructed using the PSMC.
Figure 4. Demographic history of S. bredanensis, constructed using the PSMC.
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Gao, H.; Kang, H.; Zhang, Y.; Wang, J.; Lin, W.; Zhang, P.; Lin, M.; Liu, M.; Fan, G.; Li, S. Chromosome-Level Genome Assembly of the Rough-Toothed Dolphin (Steno bredanensis). J. Mar. Sci. Eng. 2023, 11, 418. https://doi.org/10.3390/jmse11020418

AMA Style

Gao H, Kang H, Zhang Y, Wang J, Lin W, Zhang P, Lin M, Liu M, Fan G, Li S. Chromosome-Level Genome Assembly of the Rough-Toothed Dolphin (Steno bredanensis). Journal of Marine Science and Engineering. 2023; 11(2):418. https://doi.org/10.3390/jmse11020418

Chicago/Turabian Style

Gao, Haiyu, Hui Kang, Yaolei Zhang, Jiahao Wang, Wenzhi Lin, Peijun Zhang, Mingli Lin, Mingming Liu, Guangyi Fan, and Songhai Li. 2023. "Chromosome-Level Genome Assembly of the Rough-Toothed Dolphin (Steno bredanensis)" Journal of Marine Science and Engineering 11, no. 2: 418. https://doi.org/10.3390/jmse11020418

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