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Article

Mitochondrial Genome and Phylogenetic Analysis of the Narrownose Smooth-Hound Shark Mustelus schmitti Springer, 1939

by
Walter Nisa-Castro-Neto
1,2,
Paulo Guilherme Carniel Wagner
1,3,
Diéssy Kipper
4,
Vinicius Proença da Silveira
4,
André Salvador Kazantzi Fonseca
4,
Nilo Ikuta
4 and
Vagner Ricardo Lunge
2,4,*
1
Organização para a Pesquisa e a Conservação de Esqualos no Brasil (PRÓ-SQUALUS), Torres 905560-000, RS, Brazil
2
Instituto de Biotecnologia/Programa de Pós-Graduação em Biotecnologia (PPGBIO), Universidade de Caxias do Sul (UCS), Caxias do Sul 95070-560, RS, Brazil
3
Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis (IBAMA/RS)/Centro de Triagem de Animais Silvestres (CETAS/RS), Porto Alegre 90160-070, RS, Brazil
4
Simbios Biotecnologia, Cachoeirinha 94950-000, RS, Brazil
*
Author to whom correspondence should be addressed.
Animals 2024, 14(23), 3396; https://doi.org/10.3390/ani14233396
Submission received: 16 September 2024 / Revised: 7 November 2024 / Accepted: 20 November 2024 / Published: 25 November 2024
(This article belongs to the Section Animal Genetics and Genomics)
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Simple Summary

The Southwest Atlantic Ocean (SAO) is a biodiversity hotspot for elasmobranchs. This marine subclass of animals is deeply threatened by anthropogenic activities and many species are at imminent risk of extinction, such as sharks of the genus Mustelus. Scientific reports on the biology, ecology and genetic identity of the narrownose (Mustelus schmitti), the smalleye (Mustelus higmani) and the striped (Mustelus fasciatus) smooth-hound sharks from the family Triakidae are few in the literature. This study describes the sequencing of the first complete mitochondrial genome of a Chondrichthyes from the SAO coast (Mustelus schmitti, a shark classified as critically endangered by the International Union for Conservation of Nature—IUCN) and presents the phylogenetic analysis of this species. The scientific knowledge obtained here will help in elasmobranch conservation programs, in future studies on population ecology and genetics and in fisheries control for this and other small coastal shark species at risk in SAO.

Abstract

Southern Brazil is home to a large biodiversity of elasmobranchs from the Brazilian coast. Several genera and species of small sharks of the Triakidae family live in this marine environment. Studies on these shark species are scarce, with few genetic data and little information on animal population structures. The present study aimed to sequence the complete mitochondrial genome (mtDNA) of the endangered species Mustelus schmitti (narrownose smooth-hound shark) and to perform a phylogenetic analysis of the Triakidae family. The mtDNA sequenced here was 16,764 bp long and possessed the usual 13 mitochondrial protein coding genes (PCGs), 22 tRNAs, two rRNAs (12S and 16S) and a large D-loop DNA sequence, presenting an overall organization similar to other species from the genus Mustelus. Phylogenetic analyses were performed using a dataset containing this new mtDNA and 59 other mitochondrial genomes of the Carcharhiniformes species (including 14 from the Triakidae family), using the Maximum Likelihood (ML) method. All the species of the Triakidae family were clustered into a monophyletic topology group. In addition, polyphyly was observed in Galeorhinus galeus, Hemiatrakis japanica, Triakis megalopterus and Triakis semifasciata. In conclusion, this study contributes to a deeper understanding of the genetic diversity of sharks and represents an important step towards the conservation of these endangered animals.

1. Introduction

Chondrichthyes are a group of vertebrates with an ancestral evolutionary history dating back 400 million years [1,2]. The order Carcharhiniformes is the largest, most diverse and widely distributed taxon of sharks in the world’s seas and oceans, containing 10 families and approximately 291 species [3]. The genus Mustelus of the family Triakidae includes 28 species of small demersal sharks found in temperate and tropical waters of the continental shelves of all oceans [4]. In the Southwest Atlantic Ocean (SAO), animals of this genus can be found from Rio de Janeiro, Brazil, to Patagonia, Argentina [5]. Five species of Mustelus are frequently observed on the Brazilian coast: Mustelus canis, Mustelus fasciatus, Mustelus higmani, Mustelus norrisi and Mustelus schmitti [6]. These shark species are under varying levels of threat along the entire Brazilian coast [7,8].
In southern Brazil, fishing for large sharks was quite intensive in the 1980s [9]. As a consequence, populations of these animals declined in the 1990s and fishing became economically unviable, mainly for the more traditional fisheries. Therefore, fishermen directed their efforts to smaller and more coastal shark species, such as Squatina spp., Squalus spp., Galeorhinus galeus, Rhizoprionodon spp., Carcharhinus spp., Sphyrna spp. and the three main species of the genus Mustellus (M. canis, M. fasciatus and M. schimitti) [9,10]. The large reduction in populations of several shark species in the SAO resulted in conservation efforts for these ecologically important and vulnerable animals in Brazil [11,12]. Sharks were classified into risk of extinction and/or legal protection categories in 2004 (Normative Instruction 005/2004, Brazil). Two Mustelus species (M. fasciatus and M. schmitti) are sharks with small distribution and endemic to SAO [13,14]. They should be protected to avoid a collapse in shark populations, as observed in other oceans [15,16,17,18,19,20,21].
The narrownose smooth-hound shark (M. schmitti) is a coastal species (ICMBio, Brazil and IUCN) living in the seas from southern Brazil to Argentina [22,23,24]. The reproductive cycle is annual, and gestation takes between 11 and 12 months [25]. M. schmitti has slow growth and low fecundity, limiting recruitment and increasing vulnerability to overfishing. Catches in southern Brazil occur mainly in the winter and, in Uruguay, during summer and fall [26]. There is segregation of sexes and life stages [25,27]. Other information about behavior and reproduction was described previously [28].
Recent scientific articles have reported the sharks’ population structures [29,30,31]. Some studies emphasize the importance of sequencing genes and genomes to understand the population structure of many shark species [32,33,34,35]. The evolutionary history of chondrichthyans is also being elucidated with genetic data [1,36,37,38,39]. Most phylogenetic reports are based on a restricted number of nuclear and/or mitochondrial genes [37,40,41]. Next-generation sequencing (NGS) techniques have enabled reliable and accurate analysis of mitochondrial genomes (mtDNA) in recent years [42,43]. mtDNA data can be especially useful for identifying chondrichthyans, as well as for elucidating the occurrence of population units and understanding migratory flows [44,45]. All this genetic information is demonstrating more clearly the phylogeny of Chondrichthyes, as well as providing precise insights into the evolutionary relationships of these animals [46,47].
The present study sequenced the mitochondrial genome of the narrownose smooth-hound shark M. schmitti and performed a more complete phylogenetic analysis of the family Triakidae. The results reported here will help to elucidate the evolution of this endangered shark species and its relationship with other chondrichthyans.

2. Materials and Methods

2.1. Specimen Collection

One juvenile specimen of M. schmitti was collected from Praia de Mostardas, Mostardas, Rio Grande do Sul, Brazil (-30.864777 S/-50.595253 W) on 30th May 2023. The catch was accidental, using a coastal gillnet, positioned about 70 m from the beach line perpendicular to the shore. The net had been in place since 7:00 AM and was removed at 4:00 PM (Figure 1). Ethical procedures were adopted according international guidelines [48] and permission to perform this research was obtained from ICMBio/SISBIO (no. 71583) and SISGEN (no. ACA1D5C).

2.2. DNA Extraction, Sequencing and mtDNA Assembly

Genomic DNA was extracted using the PureLinkTM Genomic DNA Mini Kit according to the manufacturer’s instructions. Genome sequencing of M. schmitti was performed by Neoprospecta (Florianópolis, Brazil) using the MiSeq platform and a 305/205 paired-end library approach and prepared using the Illumina DNA Prep Kit. Trimmomatic v. 0.33 [49] was used to trim raw sequence reads and remove low-quality bases. The quality of trimmed reads was assessed using FastQC v. 0.11.2 (http://www.bioinformatics.babraham.ac.uk/projects/fastqc/, accessed on 31 June 2024). The reads were mapped against a reference mitogenome from a closely related species in Geneious Prime® v. 2024.0.5 (Biomatters, Auckland, New Zealand, www.geneious.com). The reference mtDNAs are presented in Table 1. Subsequently, the mapped Illumina reads were assembled de novo using SPAdes v. 3.6.0 [50]. The quality of draft genomes was evaluated using QUAST v. 4.0 [51]. As a final step, the total DNA-seq reads and assembly were mapped to the mtDNA from a closely related species in Geneious Prime software to confirm the quality of the assembly, correct potential assembly gaps and finally close the circular molecule.

2.3. Annotation and Sequence Analysis

The complete M. schmitti mtDNA was annotated using MitoAnnotator on the MitoFish website (http://mitofish.aori.u-tokyo.ac.jp/annotation/input.html (accessed on 31 June 2024) [52]. The programs RNAmmer (https://services.healthtech.dtu.dk/services/RNAmmer-1.2/ (accessed on 31 June 2024)) [53] and tRNA scan-SE (http://lowelab.ucsc.edu/tRNAscan-SE/ (accessed on 31 June 2024)) [54] were used to confirm the ribosomal RNA (rRNA) and the transfer RNA (tRNA) annotation results, respectively. The boundaries of the protein-coding genes (PCGs), rRNA genes and tRNA genes were refined manually by comparison with the annotated elasmobranch mtDNAs from GenBank. The complete mitochondrial genome obtained here was deposited in GenBank under the accession number PQ182775.
The assembled genome of M. schmitti was initially annotated using the MitoAnnotator and the nucleotide composition and genetic distance of the entire mitochondrial genome were analyzed using the MEGA11 v. 11.0.6 software [55].

2.4. Phylogenetic Analyses

A total of 59 complete mtDNAs of Carcharhiniformes species (14 Triakidae) were obtained from NCBI [45] and used to construct the dataset (Table 1). Chiloscyllium griseum (NC_017882), from the family Hemiscylliidae, and Lamna ditropis (NC_024269), from the family Lamnidae, were used as outgroups. The complete sequences (including D-loops) were aligned using the CLUSTAL W algorithm [56] plugin in the Geneious Prime® v. 2024.0.5. The phylogenetic relationships were reconstructed with the Maximum Likelihood (ML) method implemented in W-IQ-TREE web server [57], the optimal nucleotide substitution model selected using ModelFinder (GTR + F + I + G4) [58] and 1000 replicates of the ultrafast bootstrap approximation [59]. In addition, a Bayesian Inference (BI) phylogenetic tree was constructed in Geneious Prime® v. 2024.0.5, under 2 parallel runs and 2,000,000 generations. The initial 10% of sampled data was discarded as burn-in with default settings. FigTree v. 1.4.4 (http://tree.bio.ed.ac.uk/software/figtree/, accessed on 31 June 2024) was used to annotate the resulting phylogeny.

3. Results

3.1. Genome Structure, Composition and Asymmetry

The complete mtDNA of M. schmitti is 16,764 base pairs (bp) long, which is about the expected size for a shark genus. It also contains the typical genes, including 13 PCGs, 22 tRNAs, two rRNAs (12S and 16S) and a large D-loop. The gene order and the gene transcription directions in the complete M. schmitti mtDNA are consistent with those demonstrated for most vertebrate mtDNAs (Figure 2 and Table 2).
The overall percentages of the base composition are 30.7% A, 24.5% C, 14% G and 30.7% T. In a gene-by-gene comparison, the AT content is greater than the GC content in most genes. The AT ranged from 57% (tRNA-Thr) to 79.7% (tRNA-His), while the GC ranged from 30% (tRNA-Gly) to 56.5% (tRNA-Pro) (Table 2).

3.2. Protein Coding Regions, Transfer RNA and Ribosomal RNA

The 13 PCGs totaled 11,429 bp in length, accounting for 68.2% of the mtDNA and encoding a total of 3800 amino acids. All the PCGs are encoded by the heavy strand (H-strand), except for the ND6 gene, encoded by the light strand (L-strand). The length of the PCGs ranges from 168 bp (ATPase8) to 1830 bp (ND5) (Table 2). All the PCGs started with an ATG codon, except the COXI (GTG) and ND6 (CTA) genes, and finished with the three traditional stop codons (TAA, TAG, TGA), except ND6, which was terminated by a rare CAT codon (Figure 2, Table 2).
The 22 tRNA genes ranged from 67 bp (tRNA-Ser2) to 75 bp (tRNALeu1) in length and were located between rRNAs and PCGs. The total length of the tRNAs genes is 1553 bp, accounting for 9.3% of the whole mtDNA. Fourteen tRNAs are encoded on the H-strand and the remaining tRNAs are encoded on the L-strand. All tRNAs have a high AT content (79.7%) (Table 2).
The 12S and 16S rRNA genes are 953 bp and 1670 bp long, respectively. They are located between tRNA-Phe and tRNA-Leu, and separated by tRNA-Val, similar to most fish mtDNAs. All rRNAs have a high AT content (62.5%) (Table 2).
An additional analysis was performed within the 13 shark species from the family Triakidae. All the Triakidae mtDNAs contained the same 13 PCGs: ND1, ND2, COX1, COX2, ATP8, ATP6, COX3, ND3, ND4L, ND4, ND5, ND6 and Cytb. ND5 was the longest (1830 bp), while the ATP8 was the shortest (168 bp). These mtDNAs also had a small rRNA subunit (12S) and another large rRNA subunit (16S), ranging from 951 to 954 bp and 1648 to 1672 bp in length, respectively. Twelve mtDNAs had 22 tRNA genes, but Galeorhinus galeus (GenBank access ON652874) presented 23 genes (the tRNA-Thr gene is duplicated). The differences in the mtDNA sizes among species from Triakidae family are due to length of the control regions (D-loops). The D-loops ranged from 974 bp in Triakis semifasciata (GenBank access NC077588) to 1.786 bp in G. galeus (GenBank access ON652874) (Figure 3).

3.3. Phylogenetic Analysis

The phylogenetic tree included 60 species from the seven main families of ground sharks (Carcharhiniformes): Carcharhinidae, Hemigaleidae, Proscylliidae, Pseudotriakidae, Scyliorhinidae, Sphyrnidae and Triakidae. The topology of the ML tree was consistent, presenting well-supported clades with high bootstrap probabilities (BPs). In addition, all the species from same families clustered together as expected (Figure 4).
Specifically, the family Triakidae presented G. galeu separately in a basal branch. The remaining twelve species clustered into three well separated branches. The M. schmitti mtDNA sequenced here clustered within four other species: M. palumbes, M. asterias, M. manazo and T. megalopterus. The remaining five Mustelus species (M. griseus, M. mosis, M. mustelus, M. norrisi and M. canis) clustered together in another branch, while Hemitriakis japanica and Triakis semifasciata clustered in a third one. Therefore, sister groups were observed within the members of the genus Mustelus (Figure 4).
The phylogenetic tree also demonstrated the paraphyly of the genera Mustelus and Triakis, since T. megalopterus occupied an initial branching position. T. semifasciata, which was also included in the phylogenetic analysis and was established as a sister group of the M. schmitti clade containing M. manazo, M. asterias and M. palumbis.

4. Discussion

The use of molecular genetic methods to characterize new marine animal species (including sharks) has increased substantially in the last decades [60]. Scientific studies identified and classified many new species, as well as demonstrating the genetic diversities and their gene flows [42,44,45]. It is necessary to study each species separately to reduce the risk of these animals’ extinction [61,62]. However, only ≅10% of the elasmobranchs were well-studied for genetic identity and population structures.
In the present study, the complete mtDNA from a M. schmitti specimen was originally sequenced (GenBank Accession PQ182775). Regarding general characteristics, M. schmitti’s mtDNA length and overall organization are similar to those of other sharks from the same family (Triakidae). The complete mtDNA of M. schmitti is 16,764 bp, the expected size for shark genomes (ranging from 16,677 bp in C. falciformis to 19,100 bp in H. buergeri) and in agreement with the mtDNA conservancy among elasmobranchs [43]. In addition, the overall genomic organization, with the presence of 13 PCGs, 22 tRNAs, two rRNAs and a large D-loop region, is typical of other vertebrates [63,64]. The overall nucleotide composition is also consistent with other studies and suggests a conservative trend throughout chondrichthyan evolution [65,66,67,68,69].
A more detailed comparative analysis within the family Triakidae demonstrated that the mtDNAs lengths and compositions of the different species were almost the same as those previously reported [43,45,70]. The base composition of M. schmitti differs from those of M. canis and M. norrisi, suggesting paraphilia of these triakid species, even though they occur in synchronous areas of the South Atlantic [71,72]. The conservation of the length and composition of the mtDNA from this family suggests evolutionary stability due to the strong selective pressure maintaining the mitochondrial gene order and sequences among chondrichthyans [73,74]. This highly conserved gene organization of M. schmitti PCGs in the mtDNA also highlights the similarity with other members of the same taxonomic order [75,76]. Notably, the presence of 13 PCGs is a pattern observed in many other shark species [77], with H-strand coding for most proteins, except for ND6 (coded L-strand) [66,72]. The variation in the length of the PCGs, from 168 bp (ATPase8) to 1830 bp (ND5), is also in line with other studies [78,79]. All this distribution has already been hypothesized to help in mitochondrial gene expression [80,81]. Finally, 12S and 16S rRNA genes are inserted between tRNA-Phe and tRNA-Leu, similarly to what has been observed in many elasmobranch mtDNAs [82]. The organization of rRNAs is fundamental for regulating gene expression and maintaining mitochondrial functionality [61].
The phylogenetic tree for Charchariniforms (updated with M. schmitti) provided a more comprehensive view of the relationships within the family Triakidae. First, all the genera and species clustered into a unique clade with 100% BPs, highlighting the taxonomic robustness of this family [66,83]. Second, the position of G. galeus in the basal branch of the Triakidae clade suggests a distant relationship with the other Mustelus species, consistent with the broad distribution patterns of this species across all oceans [42,70]. This polyphyletic arrangement is further supported by the vicariant processes and gene flows that have occurred throughout the taxon’s evolution [32,84,85]. However, the presence of polyphyletic arrangements among genera within the Triakidae clade reveals some unsolved questions [43,44,45]. Furthermore, the occurrence of sister groups among Mustelus spp. highlights the genetic proximity and overlap of the areas where these species occur in the oceans [36]. These results corroborated the importance of studying the geographical distributions of the elasmobranchs [45]. The evidence of paraphyly in the genera Mustelus and Triakis, with T. megalopterus occupying a basal position and grouping as a well-supported sister clade with the other Mustelus species, also suggests that these genera have undergone distinct and complex evolutionary processes. The separation of T. semifasciata as a sister group to the clade of M. schmitti, M. manazo, M. asterias and M. palumbis, with strong support, may also indicate historical events and fixation in coastal areas, and with limitations to single regions [66,78].
In a wider view of the phylogenetic tree, the clusters for Carcharhinidae and Triakidae exhibit interesting intra-familial relationships, suggesting some lineages may have undergone recent rapid radiations [42,86,87]. The difficulties in resolving these relationships are due to an incomplete sorting of the lineages, since not enough time has passed to reliably resolve some of these knots, because the permanent genetic variation of the ancestral species inherited by the immediate descendant species was not separated before speciation [88,89]. In this context, excess partitioning can reduce the number of informative sites needed to accurately group these taxa [90,91,92,93]. These findings highlight the need for more studies integrating phylogenetic, ecological and geographic data for a comprehensive understanding of evolution and diversification within the Triakidae [94,95].
It is also important to analyze the vicariance/gene flow processes that occurred throughout the evolution of Charchariniformes, especially for hound sharks [96,97,98]. M. canis and M. norrisi are found in the same geographic areas of the western Atlantic coast, M. mosis occurs on the eastern coast of the Indian Ocean and M. griseus in the western Pacific Ocean. M. mosis is distributed from the southern Indian Ocean along the western coast of Africa to the Mediterranean. They grouped into a single clade, highlighting the wide distribution of their ancestral species by the continental distribution and circulation of the Atlantic Ocean during the Turonian Period (93.9 million and 89.8 million years ago Ma). In contrast, the other two species of this family (H. japanica and T. semifasciata) grouped into another clade. These species now live in the Pacific Ocean and probably originated in this geographic area in the Turonian Period [99,100].
Regarding reproductive mode, M. schmitti fits into the same group as the species that exhibit aplacental viviparity [5]. This result is consistent with previous studies suggesting that shared reproductive modes are important features in the phylogenetic organization of elasmobranchs [101,102]. Aplacental viviparity, a reproductive mode in which embryos develop inside the mother’s body without the formation of a placenta, is a significant adaptation that can influence the survival and reproductive success of species [103]. These findings are corroborated by studies showing that reproductive characteristics can be used to trace evolutionary relationships between shark and ray species [78,84]. The inclusion of M. schmitti in the same clade as other species with aplacental viviparity suggests that this reproductive mode may have evolved once in a common ancestor, being maintained throughout evolution due to its adaptive advantages [32,42].
One of the factors limiting the phylogenetic analysis of the family Triakidae is the lack of mtDNAs of other species, mainly those from SAO. It is still challenging to differentiate species, as well as to study population structures within the same species. Therefore, the M. schmitti mtDNA sequenced here provides the genetic identity for an important species living in SAO. As more efficient taxonomic classification methods are developed, these species can be more easily monitored and tracked, also making it possible to implement actions to reinforce coastal inspection to prevent predatory fishing. In addition, specific species populations can be estimated to determine specific time series of catches in Brazilian waters.
Finally, the monophyletic organization of M. schmitti and its association with other aplacental viviparous species highlight the importance of reproductive characteristics in the phylogenetic structuring of the Triakidae [103]. These results highlight the need to integrate morphological, ecological and molecular data for a comprehensive understanding of the evolutionary trajectories of these sharks, aiding in the development of effective management and conservation strategies.

5. Conclusions

These results provide an understanding of the M. schmitti mtDNA, with complete mitochondrial genome sequence and structure. The phylogenetic analysis clarifies the evolutionary relationships within the Triakidae family, reinforcing that Mustelus and Triakis are not monophyletic. These findings are important for accurate species identification, contributing to the conservation and management of shark and other coastal species, which are under heavy pressure due to commercial fishing.

Author Contributions

Conceptualization, W.N.-C.-N.; methodology, W.N.-C.-N. and V.R.L.; software, D.K.; validation, W.N.-C.-N., V.R.L. and D.K.; formal analysis, W.N.-C.-N., V.R.L. and P.G.C.W.; investigation, W.N.-C.-N.; resources, W.N.-C.-N. and V.P.d.S.; data curation, W.N.-C.-N. and D.K.; writing—original draft preparation, W.N.-C.-N. and D.K.; writing—review and editing, W.N.-C.-N., N.I., A.S.K.F. and V.R.L.; visualization, W.N.-C.-N. and V.P.d.S.; supervision, V.R.L. and W.N.-C.-N.; project administration, W.N.-C.-N.; funding acquisition, P.G.C.W. and W.N.-C.-N. All authors have read and agreed to the published version of the manuscript.

Funding

Funding for sequencing the mitochondrial genome provided by PROJETO CARCHARIAS: mtDNA Elasmobranchii® of the PRÓ-SQUALUS. D.K. was supported by the Brazilian National Council for Scientific and Technological Development (CNPq), process number: 351240/2023-3. V.R.L. was also financially supported by the National Council for Scientific and Technological Development from Brazil (CNPq—Conselho Nacional de Desenvolvimento Científico e Tecnológico; process number 308445/2020-1).

Institutional Review Board Statement

The study was conducted in accordance with the Declaration of Helsinki. Ethical procedures were adopted according international guidelines and permission to perform this research was obtained from ICMBio/SISBIO (no. 71583) and SISGEN (no. ACA1D5C).

Informed Consent Statement

Not applicable.

Data Availability Statement

Data are contained within the article.

Acknowledgments

The authors would also like to express their gratitude to the fisherman–researcher Marco Antonio da Rosa Dias for his invaluable partnership over the years in marine conservation in Rio Grande do Sul and to Pereira Ferreira da Silva and Clarice Prade Carvalho (In memorian) for inspiring this work. W.N.-C.-N. also acknowledges Luiz Glock for his dedication and patience, transforming his educational and personal journey into an inspiring experience every day.

Conflicts of Interest

The authors declare no conflicts of interest.

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Figure 1. Sampling place of the Mustelus schmitti specimen (white star) on the coast of Rio Grande do Sul (RS) state, south Brazil. Coastal isobaths of 15 to 75 m are shown. The Southwest Atlantic (SAO) can be seen in purple in the top left corner. The arrows mark the northern and southern limits of the sampling in this research study approval by ICMBio/SISBIO.
Figure 1. Sampling place of the Mustelus schmitti specimen (white star) on the coast of Rio Grande do Sul (RS) state, south Brazil. Coastal isobaths of 15 to 75 m are shown. The Southwest Atlantic (SAO) can be seen in purple in the top left corner. The arrows mark the northern and southern limits of the sampling in this research study approval by ICMBio/SISBIO.
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Figure 2. Circular mitochondrial genome map of the M. schmitti. Genomic map constructed with Geneious Prime software. Colors denote type annotations (Yellow: CDS; green: genes; red: rRNA; pink: tRNA). The content of ACTG is represented on the inside (red:A; blue:C; green:T; yellow:G).
Figure 2. Circular mitochondrial genome map of the M. schmitti. Genomic map constructed with Geneious Prime software. Colors denote type annotations (Yellow: CDS; green: genes; red: rRNA; pink: tRNA). The content of ACTG is represented on the inside (red:A; blue:C; green:T; yellow:G).
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Figure 3. Alignment of the Triakidae mtDNAs showing all Mustelus species. Colors denote type annotations (Yellow: CDS; red: rRNA; pink: tRNA; orange: D-loops).
Figure 3. Alignment of the Triakidae mtDNAs showing all Mustelus species. Colors denote type annotations (Yellow: CDS; red: rRNA; pink: tRNA; orange: D-loops).
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Figure 4. The phylogenetic tree of the Carcharhiniformes species. The orange square indicates the sequence species generated in this study (Mustelus schmitti). Bootstrap support (right = yellow) and Bayesian posterior probability (left = red) values of each main clade are displayed next to the nodes. Clades are colored according to families: blue = Carcharhinidae; sepia = Sphyrnidae; light blue = Galeocerdidae; red = Hemigaleidae; orange = Triakidae; yellow = Proscylliidae; purple = Pseudotriakidae; green = Scyliorhinidae. Chiloscyllium griseum and Lamna ditropis were used as outgroups.
Figure 4. The phylogenetic tree of the Carcharhiniformes species. The orange square indicates the sequence species generated in this study (Mustelus schmitti). Bootstrap support (right = yellow) and Bayesian posterior probability (left = red) values of each main clade are displayed next to the nodes. Clades are colored according to families: blue = Carcharhinidae; sepia = Sphyrnidae; light blue = Galeocerdidae; red = Hemigaleidae; orange = Triakidae; yellow = Proscylliidae; purple = Pseudotriakidae; green = Scyliorhinidae. Chiloscyllium griseum and Lamna ditropis were used as outgroups.
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Table 1. General information and nucleotide composition for the mtDNAs of shark species of the Carcharhiniform order and one outgroup.
Table 1. General information and nucleotide composition for the mtDNAs of shark species of the Carcharhiniform order and one outgroup.
FamilySpeciesSize (bp)AT%GenBank
Carcharhinidae:Carcharhinus acronotus16,71961.6NC_024055
Carcharhinus albimarginatus16,70661.4NC_047239
Carcharhinus amblyrhynchoides16,70561.8NC_023948
Carcharhinus amblyrhynchos16,70561.6NC_047238
Carcharhinus amboinensis16,70462.0NC_026696
Carcharhinus brachyurus16,70461.7NC_057525
Carcharhinus brevipinna16,70661.4NC_027081
Carcharhinus falciformis16,67761.4NC_042256
Carcharhinus leucas16,70462.6NC_023522
Carcharhinus limbatus16,70561.7NC_057057
Carcharhinus longimanus16,70661.5NC_025520
Carcharhinus macloti16,70160.8NC_024862
Carcharhinus melanopterus16,70661.4NC_024284
Carcharhinus obscurus16,70661.5NC_020611
Carcharhinus perezii16,70961.5MW528216
Carcharhinus plumbeus16,70661.2NC_024596
Carcharhinus sorrah16,70761.0NC_023521
Carcharhinus tjutjot16,70560.6NC_026871
Glyphis fowlerae16,70460.6NC_028342
Glyphis garricki16,70260.8NC_023361
Glyphis glyphis16,70161.0NC_021768
Lamiopsis temminckii16,70861.1NC_028341
Lamiopsis tephrodes16,70561.2NC_028340
Loxodon macrorhinus16,70261.1NC_029843
Prionace glauca16,70562.5NC_022819
Rhizoprionodon acutus16,69363.0NC_046016
Scoliodon laticaudus16,69563.1NC_042504
Scoliodon macrorhynchos16,69363.1NC_018052
Triaenodon obesus16,70061.1NC_026287
Galeocerdidae:Galeocerdo cuvier16,70363.1NC_022193
Hemigaleidae:Hemigaleus microstoma16,70160.1NC_029400
Hemipristis elongata16,69163.0NC_032065
Proscylliidae:Proscyllium habereri16,70862.1NC_030216
Pseudotriakidae:Pseudotriakis microdon16,70063.6NC_022735
Scyliorhinidae:Cephaloscyllium fasciatum16,70361.9MZ424309
Cephaloscyllium umbratile16,69862.1NC_029399
Galeus melastomus16,70663.2NC_049881
Halaelurus buergeri19,10061.1NC_031811
Parmaturus melanobranchus16,68762.5NC_056784
Poroderma pantherinum16,68661.1NC_043830
Scyliorhinus canicula16,69762.0NC_001950
Scyliorhinus torazame17,86161.8AP019520
Sphyrnidae:Eusphyra blochii16,72761.3NC_031812
Sphyrna lewini16,72660.5NC_022679
Sphyrna mokarran16,71961.4NC_035491
Sphyrna tiburo16,72360.7NC_028508
Sphyrna zygaena16,73161.7NC_025778
Triakidae:Galeorhinus galeus17,48862.0ON652874
Hemitriakis japanica17,30160.0KJ617039
Mustelus asterias *16,70861.5ON652873
Mustelus canis16,75860.8OP056805
Mustelus griseus *16,75461.0NC_023527
Mustelus manazo *16,70761.8NC_000890
Mustelus mosis16,75560.7ON075077
Mustelus mustelus *16,75560.8NC_039629
Mustelus norrisi16,76961.2OP056963
Mustelus palumbes *16,70861.5NC_077463
Mustelus schmitti **16,76461.4PQ182775
Triakis megalopterus16,74661.3ON075075
Triakis semifasciata16,61361.2NC_077588
HemiscylliidaeChiloscyllium griseum16,75563.9NC_017882
LamnidaeLamna ditropis16,70261.1NC_024269
* Reference mtDNA complete genomes used for assembling the M. schmitti; ** obtained in this study.
Table 2. Annotation of the complete mtDNAs of Mustelus schmitti.
Table 2. Annotation of the complete mtDNAs of Mustelus schmitti.
NameCodon StartCodon StopAnti-CodonAT%CG%TypePosition fromPosition toLengthStrand
D-loop 63.935.1D-loop15641167631123H
tRNA-Pro TGG43.556.5tRNA155721564069L
tRNA-Thr TGT57.043.0tRNA154981556972H
CytbATGTAG 59.340.7gene14353154971145H
tRNA-Glu TTC68.631.4tRNA142811435070L
ND6CTACAT 61.538.1gene1375914280522L
ND5ATGTAA 63.436.5gene11934137631830H
tRNA-Leu2 TAG59.740.2tRNA118621193372H
tRNA-Ser2 GCT49.350.8tRNA117951186167H
tRNA-His GTG79.720.3tRNA117261179469H
ND4ATGT- 62.437.6gene10345117251381H
ND4LATGTAA 58.341.7gene1005510351297H
tRNA-Arg TCG67.132.9tRNA99851005470H
ND3ATGTAG 56.443.5gene96369984349H
tRNA-Gly TCC70.030.0tRNA9566963570H
COXIIIATGTAA 57.942.1gene87789563786H
ATPase6ATGTAA 64.235.7gene80958777683H
ATPase8ATGTAA 72.027.9gene79378104168H
tRNA-Lys TTT60.839.2tRNA7862793574H
COXIIATGT- 61.838.2gene71717861691H
tRNA-Asp GTC62.937.2tRNA7094716370H
tRNA-Ser1 TGA53.546.5tRNA7020709071L
COXIGTGTAA 61.538.5gene546270181557H
tRNA-Tyr GTA47.250.0tRNA5391546070L
tRNA-Cys GCA49.250.7tRNA5321538969L
tRNA-Asn GTT61.638.4tRNA5213528573L
tRNA-Ala TGC66.633.3tRNA5144521269L
tRNA-Trp CCA67.632.4tRNA5072514271H
ND2ATGTAG 62.237.8gene402750711045H
tRNA-Met CAT57.942.0tRNA3958402669H
tRNA-Gln TTG65.334.7tRNA3886395772L
tRNA-Ile GAT54.345.7tRNA3815388470H
ND1ATGTAA 60.339.7gene28403814975H
tRNA-Leu1 TAA54.745.3tRNA2765283975H
16S rRNA 62.537.4rRNA109527641670H
tRNA-Val TAV56.943.0tRNA1023109472H
12S rRNA 58.241.8rRNA701022953H
tRNA-Phe GAA60.939.1tRNA16969H
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Nisa-Castro-Neto, W.; Wagner, P.G.C.; Kipper, D.; da Silveira, V.P.; Fonseca, A.S.K.; Ikuta, N.; Lunge, V.R. Mitochondrial Genome and Phylogenetic Analysis of the Narrownose Smooth-Hound Shark Mustelus schmitti Springer, 1939. Animals 2024, 14, 3396. https://doi.org/10.3390/ani14233396

AMA Style

Nisa-Castro-Neto W, Wagner PGC, Kipper D, da Silveira VP, Fonseca ASK, Ikuta N, Lunge VR. Mitochondrial Genome and Phylogenetic Analysis of the Narrownose Smooth-Hound Shark Mustelus schmitti Springer, 1939. Animals. 2024; 14(23):3396. https://doi.org/10.3390/ani14233396

Chicago/Turabian Style

Nisa-Castro-Neto, Walter, Paulo Guilherme Carniel Wagner, Diéssy Kipper, Vinicius Proença da Silveira, André Salvador Kazantzi Fonseca, Nilo Ikuta, and Vagner Ricardo Lunge. 2024. "Mitochondrial Genome and Phylogenetic Analysis of the Narrownose Smooth-Hound Shark Mustelus schmitti Springer, 1939" Animals 14, no. 23: 3396. https://doi.org/10.3390/ani14233396

APA Style

Nisa-Castro-Neto, W., Wagner, P. G. C., Kipper, D., da Silveira, V. P., Fonseca, A. S. K., Ikuta, N., & Lunge, V. R. (2024). Mitochondrial Genome and Phylogenetic Analysis of the Narrownose Smooth-Hound Shark Mustelus schmitti Springer, 1939. Animals, 14(23), 3396. https://doi.org/10.3390/ani14233396

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