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Article

Complete Mitochondrial Genome and Phylogenetic Analysis of Tarsiger indicus (Aves: Passeriformes: Muscicapidae)

by
Guanwei Lan
1,2,†,
Jiaojiao Yu
2,†,
Juan Liu
3,
Yue Zhang
3,
Rui Ma
2,
Yanshan Zhou
2,
Biqing Zhu
3,
Wei Wei
1,
Jiabin Liu
2,4,* and
Guilan Qi
5,*
1
Key Laboratory of Southwest China Wildlife Resources Conservation (Ministry of Education), China West Normal University, Nanchong 637009, China
2
Sichuan Key Laboratory of Conservation Biology for Endangered Wildlife, Chengdu Research Base of Giant Panda Breeding, Chengdu 610081, China
3
Administrative Bureau of Baihe National Nature Reserve, Ngawa 623400, China
4
Institute of Wildlife Conservation, Central South University of Forestry and Technology, Changsha 410004, China
5
Animal Husbandry Institute, Chengdu Academy of Agriculture and Forestry Sciences, Chengdu 611130, China
*
Authors to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Genes 2024, 15(1), 90; https://doi.org/10.3390/genes15010090
Submission received: 9 November 2023 / Revised: 26 December 2023 / Accepted: 26 December 2023 / Published: 11 January 2024
(This article belongs to the Section Animal Genetics and Genomics)
Browse Figures
Versions Notes

Abstract

:
Tarsiger indicus (Vieillot, 1817), the White-browed Bush Robin, is a small passerine bird widely distributed in Asian countries. Here, we successfully sequenced its mitogenome using the Illumina Novaseq 6000 platform (Illumina, San Diego, CA, USA) for PE 2 × 150 bp sequencing. Combined with other published mitogenomes, we conducted the first comprehensive comparative mitogenome analysis of Muscicapidae birds and reconstructed the phylogenetic relationships between Muscicapidae and related groups. The T. indicus mitogenome was 16,723 bp in size, and it possessed the typical avian mitogenome structure and organization. Most PCGs of T. indicus were initiated strictly with the typical start codon ATG, while COX1 and ND2 were started with GTG. RSCU statistics showed that CUA, CGA, and GCC were relatively high frequency in the T. indicus mitogenome. T. cyanurus and T. indicus shared very similar mitogenomic features. All 13 PCGs of Muscicapidae mitogenomes had experienced purifying selection. Specifically, ATP8 had the highest rate of evolution (0.13296), whereas COX1 had the lowest (0.01373). The monophylies of Muscicapidae, Turdidae, and Paradoxornithidae were strongly supported. The clade of ((Muscicapidae + Turdidae) + Sturnidae) in Passeriformes was supported by both Bayesian Inference and Maximum likelihood analyses. The latest taxonomic status of many passerine birds with complex taxonomic histories were also supported. For example, Monticola gularis, T. indicus, and T. cyanurus were allocated to Turdidae in other literature; our phylogenetic topologies clearly supported their membership in Muscicapidae; Paradoxornis heudei, Suthora webbiana, S. nipalensis, and S. fulvifrons were formerly classified into Muscicapidae; we supported their membership in Paradoxornithidae; Culicicapa ceylonensis was originally classified as a member of Muscicapidae; our results are consistent with a position in Stenostiridae. Our study enriches the genetic data of T. indicus and provides new insights into the molecular phylogeny and evolution of passerine birds.

1. Introduction

Passerines (Aves: Passeriformes) include a large number of species and are adapted to various ecological environments. The latest data show that the group has 145 families and 6695 species, accounting for 60% of all bird species; moreover, Muscicapidae is the third-largest family after Tyrannidae and Thraupidae, with 351 species from 53 genera [1]. Tarsiger indicus (Vieillot, 1817) (Figure 1), the White-browed Bush Robin, is a small Muscicapidae bird widely distributed in Asian countries, including India, Nepal, Bhutan, Myanmar, Vietnam, and China [2]. In China, T. indicus is found in Sichuan, Gansu, Shanxi, Hubei, Yunnan, Tibet, and Taiwan [3,4,5]. It generally inhabits the coniferous forests and the mixed broadleaf–conifer forests between alpine rock valleys at altitudes of 2440–4270 m above sea level in western China; in addition, it also inhabits the bottom shrubland of dense forests at altitudes of 2300–3200 m above sea level in Taiwan Island of China. In the past, the White-browed Bush Robin has been divided into three subspecies, including T. indicus indicus, T. i. yunnanensis, and T. i. formosanus [3]. Recently, an integrative taxonomic investigation found the Taiwan endemic T. i. formosanus to be distinctive in genetics, song, and morphology from T. i. indicus and T. i. yunnanensis of the Sino-Himalayan mountains [6]. In view of this, the T. i. formosanus subspecies has been suggested to be upgraded to the species T. formosanus, named the Taiwan Bush Robin [6,7]. In addition, T. indicus has been included in the updated List of Terrestrial Wild Animals of Important Ecological, Scientific, and Social Value in China [8]. Due to its wide geographical distribution and large population size, the conservation status of T. indicus is Least Concern in both the IUCN Red List of Threatened Species [2] and the Red List of China’s Vertebrates [9].
Vertebrate mitochondrial genomes (mitogenomes) are circular, typically 14,000–20,000 bp, and contain 13 protein-coding genes (PCGs), two ribosomal RNA (rRNAs), 22 transfer RNA genes (tRNAs), and one large non-coding D-loop region [10,11]. The mitogenome has been extensively used in population genetics, population dynamics, and adaptive evolution studies of various animal groups [12,13,14,15,16], particularly in phylogenetic reconstruction among animal species [14,16,17,18,19]. It is worth emphasizing that mitochondrial genomes are more reliable in phylogenetic reconstruction than a single mitochondrial gene [20,21,22]. However, the mitogenomes of the Muscicapidae family, a complex lineage of passerines, has been studied very little. So far, complete mitochondrial genomes of only 24 species (ca. 7% of the overall clade) from 15 genera (ca. 28%) within Muscicapidae family have published in the GenBank database (Table 1), mainly focusing on simple mitogenomic descriptions [23,24,25,26,27,28,29].
Genetic data on T. indicus are currently rare. In the GenBank database, only 39 nucleotide sequences have been uploaded as of August 2023, including 16 sequences of mitochondrial Cytb and ND2 genes. An accurate understanding of phylogeny is an important prerequisite for many studies of ecology and evolution [6,48]. However, in terms of phylogenetic status, T. indicus was previously placed into the genus Luscinia [49] and is now still placed into the Turdidae family in some publications [50].
In order to better understand the mitogenome characteristics and the phylogenetic relationship of T. indicus, we sequenced its mitochondrial genome through high-throughput sequencing technology here. Combined with other published data, we conduct the first comprehensive comparative mitogenome analysis of Muscicapidae birds and reconstruct the phylogenetic relationships between Muscicapidae and related groups using a mitogenomic approach.

2. Materials and Methods

2.1. Materials

A subadult window victim, which was found dead, was collected from Yingjing Area of the Giant Panda National Park, Scihuan Province, China (29°33′39.50″ N, 102°51′4.10″ E, 2428 m above sea level) on 30 July 2022, and it was identified as T. indicus by morphological characters and mitochondrial Cytb blast. The extraction of genomic DNA from a pectoral muscle was carried out using the Rapid Animal Genomic DNA Isolation Kit (Sangon Biotech Co., Ltd., Shanghai, China), according to the manufacturer’s protocol. The specimen and its DNA were deposited at the Chengdu Research Base of Giant Panda Breeding (Dr. Jiabin Liu, [email protected]) with the voucher number PB2022027.

2.2. Mitogenome Sequencing, Assembly, and Annotation

With the assistance of Sangon Biotech Co., Ltd. (Shanghai, China), we sequenced the mitochondrial genome through a high-throughput sequencing technique. Library preparation, mitogenome sequencing, and mitogenome assembly were performed as previously described [51]. Mitogenome annotations were implemented using MITOS WebServer (http://mitos2.bioinf.uni-leipzig.de/index.py, accessed on 15 August 2023) [52] and MitoAnnotator (http://mitofish.aori.u-tokyo.ac.jp/annotation/input/, accessed on 15 August 2023) [53]. Based on their proposed cloverleaf secondary structures and anticodon sequences, the tRNAs were rechecked using ARWEN online services (http://130.235.244.92/ARWEN/, accessed on 15 August 2023) [54]. The mitogenome visualization map was generated using Chloroplot (https://irscope.shinyapps.io/Chloroplot/, accessed on 18 August 2023) [55].

2.3. Comparative Mitogenomic Analyses

The complete mitogenome of T. indicus and 24 other Muscicapidae birds belonging to 15 genera were used for comparative mitogenomic analyses (Table 1). The 13 PCGs, two rRNAs, and whole mitogenomes were aligned in batches with MAFFT v7.505 [56]. Nucleotide composition and relative synonymous codon usage (RSCU) were calculated using MEGA v11.0.9 [57]. Nucleotide composition biases were determined from the formulas AT-skew = (A − T)/(A + T) and GC-skew = (G − C)/(G + C). The nucleotide diversity (Pi), the non-synonymous substitution rate (Ka), and the synonymous substitution rate (Ks) were calculated using DnaSP v6.12.03 [58].
Data visualization was performed using OmicStudio tools (https://www.omicstudio.cn/tool, accessed on 25 August 2023) [59].

2.4. Mitogenomic Phylogenetic Analyses

Two rRNAs and 13 PCGs of T. indicus and 40 other Passeriformes birds belonging to 26 genera and seven families were used for mitogenomic phylogenetic analyses (Table 1). The taxonomy of all birds is based on the IOC World Bird List v13.2 [1]. Pitta sordida (Passeriformes: Pittidae) was used as an outgroup based on its well-documented distant phylogenetic position from the ingroup [60,61,62]. Two rRNA sequences were aligned in batches with MAFFT v7.505 [56] using ‘–auto’ strategy and normal alignment mode, and 13 PCGs sequences were aligned in batches using the codon-aware program MACSE v2.06 [63], which preserves reading frame and allows incorporation of sequencing errors or sequences with frameshifts. Ambiguously aligned fragments of these 15 alignments were removed in batches using Gblocks v0.91b [64] with the following parameter settings: minimum number of sequences for a conserved/flank position (22/22), maximum number of contiguous non-conserved positions (8), minimum length of a block (10), allowed gap positions (with half). The 15 alignments were eventually concatenated into one multi-gene dataset consisting of a 13,893 bp sequence using PhyloSuite v1.2.3 [65]. The concatenated multi-gene dataset was used to clarify the phylogeny using Bayesian Inference (BI) and Maximum Likelihood (ML) methods. A best-fit partition model (edge-linked) was selected by ModelFinder v2.2.0 [66] using a BIC criterion, and the results are shown in Table S1. BI phylogenies were inferred using MrBayes v3.2.6 [67] under a partition model (2 parallel runs, ten million generations, sampling every one thousand generations), in which the initial 25% of sampled data were discarded as burn-in. ML phylogenies were inferred using IQ-TREE v2.2.0 [68] under an edge-linked partition model for one hundred thousand ultrafast [69] bootstraps.
High-quality figures of phylogenetic trees were produced using FigTree v.1.4.4 (http://tree.bio.ed.ac.uk/software/figtree/, accessed on 31 August 2023).

3. Results and Discussion

3.1. Structure and Organization of the T. indicus Mitogenome

Herein, the complete mitogenome of T. indicus (GenBank accession number: OR459825) was successfully sequenced and annotated. It was a circular and double-stranded DNA molecule, consisting of a typical structure with 13 PCGs, 2 rRNAs, 22 tRNAs, and a major non-coding D-loop region (Table 2; Figure 2). Among these 37 genes, 28 were located on the heavy strand, while the remaining nine genes, including eight tRNAs (trnQ, trnA, trnN, trnC, trnY, trnS2, trnE and trnP) and one PCG (ND6), were located on the light strand (Table 2; Figure 2). T. indicus showed the typical avian mitogenome order [21,70], which was also the ancestral avian arrangement found in many lineages of Passeriformes [21]. The mitogenome structure and organization of T. indicus was consistent with those of T. cyanurus, but the T. indicus mitogenome (16,723 bp) was smaller in size than the T. cyanurus mitogenome (16,803 bp), and the interspecific difference was mainly caused by the size difference in the D-loop region located between trnE and trnF (Table 2).

3.2. Codon Usage

Among the 13 PCGs, the smallest one was ATP8, and the largest one was ND5, ranging from 168 bp to 1818 bp (Table 2). Most PCGs of T. indicus were initiated with the typical start codon ATG, while COX1 and ND2 were started with GTG (Table 2). The unusual start codon GTG was also observed in COX1 from other bird groups, such as Sittidae [71,72], Accipitridae [73,74], Phasianidae [75], Columbidae [76], and other Passeriformes species [24,25,30,36,45]. The stop codons of 13 PCGs were quite varied in T. indicus. ATP6, ATP8, COX2, Cytb, ND3, ND4L, and ND6 were terminated with the representative stop codon TAA or TAG, COX1, ND1, and ND5 ended with AGA or AGG, while COX3, ND2, and ND4 were occasionally terminated with the truncated stop codon TA or T (Table 2). The incomplete stop codons TA and T are common in metazoan mitogenomes [19,20,51,72], and they can be converted to TAA by post-transcriptional modifications during the mRNA maturation process [77]. The start and stop codons of the 13 PCGs were very similar in the mitogenomes of T. indicus and T. cyanurus, and the only difference was the stop codon of the ND6 gene: the former was TAG, while the latter was AGG (Table 2).
The T. indicus mitogenome contained a total of 3797 codons in its protein-coding regions (Table S2). The three most frequently used codons were CUA (Leu1), AUC (Ile), and UUC (Phe), which were used 347, 217, and 181 times, respectively, and the five least-used codons were UGU (Cys), AGU (Ser1), ACG (Thr), CGG (Arg), and AAG (Lys), which were used 6, 6, 6, 4, and 4 times, respectively (Table S2). As in other birds [76,78,79], amino acids with high frequency encoded by PCGs were Leu (664), Thr (327), and Ala (323) (Table S2).
In addition, RSCU is a reference value to evaluate the frequency of codons encoding the same amino acid [80]. When the RSCU ratio was greater than 1, it indicated that the codon occurred many times [80]. Statistics on the RSCU showed that CUA (3.14), CGA (2.34), and GCC (2.18) were relatively high-frequency in T. indicus mitogenome (Figure 3; Table S2). RSCU values of T. cyanurus mitogenome was also summarized and compared with T. indicus, and these two mitogenomes had very similar characteristics of utilization rate of synonymous codon of single amino acids (Figure 3; Table S2).

3.3. Nucleotide Composition, Diversity, and Evolution

The overall nucleotide composition of the T. indicus mitogenome was 32.88% C, 29.63% A, 22.75% T, and 14.73% G, indicating that the mitogenomes were biased towards C and A bases, which had also been the case in previous studies of avian mitochondrial genomes [18,81]. Its overall G + C content was 47.62%, which was similar to the 47.03% of the T. cyanurus mitogenome (Figure 4). Similar to most other birds [18,37,72], overall G + C content of the whole mitogenomes of all 25 Muscicapidae birds was slightly lower than their overall A + T content (Table S3). In terms of a single mitochondrial gene of Muscicapidae species including T. indicus, the individual G + C contents were very close to 50% (Table S3; Figure 4 and Figure 5). Although T. indicus and T. cyanurus were closely related species, their individual G + C content had an inconsistent trend among all genes (Figure 4).
We also calculated the nucleotide skew of mitochondrial gene in 25 Muscicapidae species. The AT-skew values of the entire genome, concatenated rRNAs, concatenated PCGs, and single rRNA and PCG (except ND6) were positive, while the GC-skew values were negative (Figure 5), as was common in mitogenomes of Strigiformes [18] and Accipitriformes [74], indicating that Cs were more abundant than Gs, and As were more abundant than Ts. AT-skew and GC-skew were due to the different distribution of nucleotides between the two DNA strands, which further led to an asymmetry in the DNA strands [51,80]. We also analyzed the correlation between nucleotide content and corresponding skew of all mitogenomes of Muscicapidae (Figure 5), but the correlation was weak and further confirmation was needed with more data.
The nucleotides varied greatly among different genes (Figure 6). The average nucleotide diversity values for individual genes ranged from 0.04264 (rrnS) to 0.16538 (ND2), and the percentage of nucleotide variable sites ranged from 18.05% (rrnL) to 52.93% (ND2) (Figure 6A), indicating that rrnL and rrnS were slow-evolving genes, ND2 was a fast-evolving gene.
To further understand the role of selective pressure on the mitochondrial PCGs among the Muscicapidae species, we calculated and compared the average Ka/Ks ratio for each PCG (Figure 6B). Ka/Ks ratio = 1 denotes neutral mutations, Ka/Ks ratio < 1 denotes negative selection, and Ka/Ks ratio > 1 denotes positive selection [82,83]. Here, the average Ka/Ks ratio for all PCGs were consistently far lower than 1, indicating that all PCGs of Muscicapidae mitogenomes had experienced purifying selection. Among the 13 PCGs, ATP8 had the highest rate of evolution (0.13296), whereas COX1 had the lowest (0.01373) (Figure 6B), which was congruent with the previous studies in Passeriformes [51,71], Piciformes [79], Strigiformes [18], and penguins [84], as well as frogs [85]. Therefore, our findings confirmed that COX1 experienced the strongest purifying selection and COX1 might play important roles in the evolution of avian mitogenomes.

3.4. Mitochondrial Phylogenomics

The ML and BI trees of the 13PCGs + 2rRNAs dataset had similar topologies, and most nodes were supported by high bootstrap percentages (BP) and Bayesian posterior probabilities (BPP) (Figure 7 and Figure S1).
Our results showed that Muscicapidae, Turdidae, and Paradoxornithidae were clustered into two monophyletic groups, and species of the same genus were clustered together with a high degree of confidence. Muscicapidae and Turdidae were sister groups (BP = 85, BPP = 1.00), and they clustered together with Sturnidae (BP = 100, BPP = 1.00), which was consistent with a previous study [38]. T. indicus and T. cyanurus were clustered together with high confidence (BP = 100, BPP = 1.00). These two Tarsiger birds were previously placed in the genus Luscinia [49]. Although many species of Muscicapidae, such as M. gularis, T. indicus, and T. cyanurus were allocated to Turdidae in some older works [50,86] and the up-to-date NCBI taxonomy database; our phylogenetic topologies clearly supported their membership in the Muscicapidae family. It is important to note that the phylogenetic relationships between some genera within Muscicapidae are problematic between our study and a previous study [23]. The position of C. semirufa in our ML and BI trees was not consistent, and different from the ML tree based on a 13 PCGs dataset in a Yang et al. study [23], and the degree of confidence of related branches was not high (Figure 7 and Figure S1). Our ML and BI trees showed consistent topology (Calliope + Larvivora) + Ficedula (Figure 7 and Figure S1); however, the ML tree of the Yang et al. study showed the diametrical topology Calliope + (Ficedula + Larvivora) with low bootstrap percentages [23]. Complete mitogenomes may provide more accurate signals than gene fragments for phylogenetic reconstruction. Overall, the current 25 species represent only 7% of the old-world flycatchers group, so, in order to better resolve the phylogenetic relationships within Muscicapidae, it is still necessary to obtain more mitochondrial genome sequences of old-world flycatchers.
In addition, P. heudei, S. webbiana, S. nipalensis, and S. fulvifrons were classified into Muscicapidae in previous studies [57,71] and the NCBI taxonomy database, but our results showed that these species clustered into the Paradoxornithidae family [87]. The taxonomic history of C. ceylonensis was also complex [72]. C. ceylonensis was originally classified into the Muscicapidae family based on external morphology, reproductive habits, and nesting characteristics [86]. Subsequently, it was classified into the family Rhipiduridae [88]. Lately, the phylogenetic analyses based on multilocus sequence data revealed that C. ceylonensis was in fact a member of the Stenostiridae family [62]. Here, we also clarified its taxonomic validity based on mitochondrial genome approach.

4. Conclusions

In this study, we successfully sequenced the mitogenome of T. indicus using the Illumina Novaseq 6000 platform with a paired-end read length of 150 bp. We also annotated and summarized its mitogenomic characteristics in detail. Importantly, we conducted the first comprehensive mitogenome analysis of Muscicapidae. The mitogenome of T. indicus mitogenome contained the typical avian mitochondrial gene arrangement. T. cyanurus and T. indicus shared very similar mitogenomic features. All 13 PCGs of the mitogenomes of Muscicapidae had experienced purifying selection. The monophylies of Muscicapidae, Turdidae, and Paradoxornithidae were strongly supported. The clade of ((Muscicapidae + Turdidae) + Sturnidae) in Passeriformes was supported by both BI and ML analyses. The current taxonomic status of many passerine birds with complex taxonomic histories were also supported. Our study provides the first complete mitochondrial genome of T. indicus to enrich its genetic data. A large number of studies on the mitochondrial genome of Muscicapidae are still needed in the future to further solve some phylogenetic problems.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/genes15010090/s1, Table S1: The partition and best-fit partition models used in this study; Table S2: The codon usage in the mitogenomes of T. indicus and T. cyanurus; Table S3: The nucleotide composition and skew in the mitogenomes of 25 species of Muscicapidae; Figure S1: The phylogenetic relationships of Passeriformes inferred by BI method based on the 13PCGs + 2rRNAs dataset. Numbers on nodes are the Bayesian posterior probabilities.

Author Contributions

Conceptualization, J.L. (Jiabin Liu) and G.Q.; Data curation, J.Y.; Formal analysis, J.Y.; Funding acquisition, G.L. and J.L. (Jiabin Liu); Investigation, G.L., J.L. (Juan Liu) and Y.Z. (Yue Zhang); Methodology, G.L. and J.Y.; Project administration, J.L. (Jiabin Liu) and G.Q.; Resources, G.L.; Visualization, J.Y.; Writing—original draft, G.L. and J.Y.; Writing—review & editing, J.L. (Juan Liu), Y.Z. (Yue Zhang), R.M., Y.Z. (Yanshan Zhou), B.Z., W.W., J.L. (Jiabin Liu) and G.Q. All authors have read and agreed to the published version of the manuscript.

Funding

This work was financially supported by the National Natural Science Foundation of China (Grant No. U21A20193), the Sichuan Science and Technology Program (Grant No. 2023NSFSC1156), and the Capacity Building Project of Baihe National Nature Reserve in 2022 (Grant No. N5132252022000101-3).

Institutional Review Board Statement

Ethical review and approval were not required because the specimen used in this study was a subadult bird that crashed into a window and died.

Informed Consent Statement

Not applicable.

Data Availability Statement

The GenBank accession number of the newly determined Tarsiger indicus mitogenome sequence is OR459825. The BioProject, BioSample, and SRA accession numbers of metadata are PRJNA1006441, SAMN37041239, and SRR25670941, respectively.

Acknowledgments

We gratefully acknowledge Taifu Hu, a bird lover from Longcanggou Town of Yingjing County, for providing the photo of T. indicus. We truly thank HOME for Researchers (http://www.home-for-researchers.com/, accessed on 2 October 2023) for the linguistic assistance during the preparation of this manuscript.

Conflicts of Interest

The authors declare no conflicts of interest.

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Genes 15 00090 g001
Figure 1. Reference image of adult T. indicus. The photo was taken by Taihu Hu on 20 February 2022 in Yingjing County, Ya’an City, Sichuan Province, China.
Figure 1. Reference image of adult T. indicus. The photo was taken by Taihu Hu on 20 February 2022 in Yingjing County, Ya’an City, Sichuan Province, China.
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Genes 15 00090 g002
Figure 2. Graphical representation of Tarsiger indicus mitogenome. Genes outside the outer multicolored circle are located on the light strand counterclockwise, and those inside the outer circle are located on the heavy strand clockwise. Different colors indicate different types of genes and regions. The inner blue circle represents the local GC content.
Figure 2. Graphical representation of Tarsiger indicus mitogenome. Genes outside the outer multicolored circle are located on the light strand counterclockwise, and those inside the outer circle are located on the heavy strand clockwise. Different colors indicate different types of genes and regions. The inner blue circle represents the local GC content.
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Genes 15 00090 g003
Figure 3. The relative synonymous codon usage (RSCU) in mitogenomes of T. indicus and T. cyanurus.
Figure 3. The relative synonymous codon usage (RSCU) in mitogenomes of T. indicus and T. cyanurus.
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Genes 15 00090 g004
Figure 4. The G + C content (%GC) of T. indicus and T. cyanurus mitogenomes.
Figure 4. The G + C content (%GC) of T. indicus and T. cyanurus mitogenomes.
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Genes 15 00090 g005
Figure 5. Correlation between nucleotide content and corresponding skew in the mitogenomes of 26 species of Muscicapidae. (A) A + T content (%AT) vs. AT-skew; (B) G + C content (%GC) vs. GC-skew. Each dot represents a mitogenome.
Figure 5. Correlation between nucleotide content and corresponding skew in the mitogenomes of 26 species of Muscicapidae. (A) A + T content (%AT) vs. AT-skew; (B) G + C content (%GC) vs. GC-skew. Each dot represents a mitogenome.
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Genes 15 00090 g006
Figure 6. Evolutionary rates of mitochondrial genes of 25 species of Muscicapidae. (A) Nucleotide diversity and percentage of variable sites; (B)The ratio of non-synonymous substitution rate and synonymous substitution rate.
Figure 6. Evolutionary rates of mitochondrial genes of 25 species of Muscicapidae. (A) Nucleotide diversity and percentage of variable sites; (B)The ratio of non-synonymous substitution rate and synonymous substitution rate.
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Figure 7. The phylogenetic relationships of Passeriformes inferred by ML method based on the 13PCGs + 2rRNAs dataset. Numbers on nodes are the bootstrap percentages.
Figure 7. The phylogenetic relationships of Passeriformes inferred by ML method based on the 13PCGs + 2rRNAs dataset. Numbers on nodes are the bootstrap percentages.
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Table 1. List of 41 species used for the comparative mitogenomic analyses and the mitogenomic phylogenetic analyses in this study.
Table 1. List of 41 species used for the comparative mitogenomic analyses and the mitogenomic phylogenetic analyses in this study.
FamilySpeciesGenBank No.Mitogenome Size (bp)References
MuscicapidaeOenanthe isabellinaKU097327NC_04029016,812[30]
Oenanthe oenantheMN356231NC_05103616,826[31]
Copsychus saularisKU058637NC_03060316,827[32]
Copsychus sechellarumMN356447 16,839[31]
Muscicapa sibiricaMK770601NC_04537417,879[27]
Muscicapa sibiricaMK390479NC_04518117,897[15,28]
Muscicapa dauuricaMK770602NC_04537518,026[29]
Ficedula hyperythraMW795347NC_05832016,819[23]
Ficedula albicollisKF293721NC_02162116,787[33]
Ficedula zanthopygiaJN018411NC_01580216,794Unpublished
Phoenicurus auroreusKF997863NC_02606616,772[34]
Phoenicurus frontalisMT360379NC_05391716,776[24]
Calliope calliopeHQ690246NC_01507416,841Unpublished
Larvivora komadoriLC541462 16,812Unpublished
Larvivora akahigeLC541457 16,824Unpublished
Myophonus caeruleusMN564936 16,815Unpublished
Enicurus schistaceusOP998296NC_07212017,112Unpublished
Cyornis umbratilisON746672NC_06869416,805Unpublished
Cyornis magnirostrisON746663NC_06868716,816Unpublished
Cyornis hainanus/rubeculoidesHQ896033NC_01523216,802[15]
Niltava davidiKY024217NC_03953816,770[35]
Melaenornis chocolatinusMT017899NC_05284116,582Unpublished
Cossypha semirufaMT017889NC_05283916,564Unpublished
Tarsiger indicusOR459825 This study
Tarsiger cyanurusKF997864NC_02606716,803[34]
Monticola gularisKX506858NC_03353616,801[36]
TurdidaeTurdus ruficollisMT712159NC_05725016,737[37]
Turdus obscurusMZ337397 16,739[38]
Turdus cardisMN865118NC_04694816,761[39]
Zoothera aureaMT527192NC_05429816,712[40]
Geokichla sibiricaMK377247 16,766[41]
Myadestes myadestinusKU158194NC_03135216,641[42]
Catharus fuscescensMN356183NC_05101316,766[31]
SturnidaeSturnus vulgarisKT946691NC_02936016,793[43]
ParadoxornithidaeSuthora fulvifronsKT598466NC_02843617,059[44]
Suthora nipalensisKT598467NC_02843716,996Unpublished
Suthora webbianaKF725775NC_02453916,960[45]
Paradoxornis heudeiEU376027 16,928Unpublished
Psittiparus gularisKX397391NC_03953617,109[35]
PhylloscopidaePhylloscopus proregulusMG189603NC_03718916,880[46]
StenostiridaeCulicicapa ceylonensisMH880820NC_04219116,851[47]
PittidaePitta sordidaMN356273NC_05146317,733[31]
Table 2. The mitochondrial genome comparison between T. indicus and T. cyanurus.
Table 2. The mitochondrial genome comparison between T. indicus and T. cyanurus.
GeneLocationGene Length (bp)Start/Stop Codon
T. indicus
OR459825		T. cyanurus
KF997864		T. indicus
OR459825		T. cyanurus
KF997864		T. indicus
OR459825		T. cyanurus
KF997864
trnF (gaa)1–68: +1–68: +6868
rrnS69–1050: +69–1051: +982983
trnV (uac)1051–1120: +1052–1121: +7070
rrnL1121–2719: +1122–2723: +15991602
trnL2 (uaa)2720–2794: +2724–2798: +7575
ND12800–3777: +2804–3781: +978978ATG/AGAATG/AGA
trnI (gau)3787–3858: +3794–3865: +7272
trnQ (uug)3866–3936: −3873–3943: −7171
trnM (cau)3936–4004: +3943–4011: +6969
ND24005–5044: +4012–5051: +10401040GTG/TAGTG/TA
trnW (uca)5045–5115: +5052–5122: +7171
trnA (ugc)5117–5185: −5124–5192: −6969
trnN (guu)5190–5262: −5197–5269: −7373
trnC (gca)5263–5329: −5270–5336: −6767
trnY (gua)5329–5399: −5336–5406: −7171
COX15401–6951: +5408–6958: +15511551GTG/AGGGTG/AGG
trnS2 (uga)6943–7017: −6950–7024: −7575
trnD (guc)7021–7089: +7028–7096: +6969
COX27098–7781: +7104–7787: +684684ATG/TAAATG/TAA
trnK (uuu)7783–7850: +7789–7856: +6868
ATP87852–8019: +7858–8025: +168168ATG/TAAATG/TAA
ATP68010–8693: +8016–8699: +684684ATG/TAAATG/TAA
COX38699–9482: +8705–9488: +784784ATG/TATG/T
trnG (ucc)9483–9551: +9489–9557: +6969
ND39552–9902: +9558–9908: +351351ATG/TAAATG/TAA
trnR (ucg)9904–9973: +9910–9979: +7070
ND4L9975–10,271: +9981–10,277: +297297ATG/TAAATG/TAA
ND410,265–11,642: +10,271–11,648: +13781378ATG/TATG/T
trnH (gug)11,643–11,713: +11,649–11,719: +7171
trnS1 (gcu)11,714–11,780: +11,722–11,786: +6765
trnL1 (uag)11,780–11,850: +11,786–11,856: +7171
ND511,851–13,668: +11,857–13,674: +18181818ATG/AGAATG/AGA
Cytb13,677–14,819: +13,683–14,825: +11431143ATG/TAAATG/TAA
trnT (ugu)14,823–14,891: +14,829–14,897: +6969
trnP (ugg)14,899–14,968: −14,904–14,973: −7070
ND614,982–15,500: −14,990–15,508: −519519ATG/TAGATG/AGG
trnE (uuc)15,502–15,573: −15,510–15,581: −7272
D-loop15,574–16,723: +15,582–16,803: +11501222
+ represents heavy strand, and − represents light strand.
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MDPI and ACS Style

Lan, G.; Yu, J.; Liu, J.; Zhang, Y.; Ma, R.; Zhou, Y.; Zhu, B.; Wei, W.; Liu, J.; Qi, G. Complete Mitochondrial Genome and Phylogenetic Analysis of Tarsiger indicus (Aves: Passeriformes: Muscicapidae). Genes 2024, 15, 90. https://doi.org/10.3390/genes15010090

AMA Style

Lan G, Yu J, Liu J, Zhang Y, Ma R, Zhou Y, Zhu B, Wei W, Liu J, Qi G. Complete Mitochondrial Genome and Phylogenetic Analysis of Tarsiger indicus (Aves: Passeriformes: Muscicapidae). Genes. 2024; 15(1):90. https://doi.org/10.3390/genes15010090

Chicago/Turabian Style

Lan, Guanwei, Jiaojiao Yu, Juan Liu, Yue Zhang, Rui Ma, Yanshan Zhou, Biqing Zhu, Wei Wei, Jiabin Liu, and Guilan Qi. 2024. "Complete Mitochondrial Genome and Phylogenetic Analysis of Tarsiger indicus (Aves: Passeriformes: Muscicapidae)" Genes 15, no. 1: 90. https://doi.org/10.3390/genes15010090

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