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Citation: | Ying Zhang, Lei Meng, Liming Wei, Bingjian Liu, Liqin Liu, Zhenming Lü, Yang Gao, Li Gong. Comparative mitochondrial genome analysis of Sesarmidae and its phylogenetic implications[J]. Acta Oceanologica Sinica, 2022, 41(8): 62-73. doi: 10.1007/s13131-021-1911-2 |
The mitochondrial genome (mitogenome) is typically circular in metazoans, with a size of 14–20 kb. This genome contains 13 protein-coding genes (PCGs), 22 transfer RNA genes (tRNAs), two ribosomal RNA genes (12S and 16S) and an AT-rich region (also called control region, CR) (Boore, 1999). The mitogenome is featured by high abundance in the cell, maternal inheritance, small genome size, conserved gene content, low level of recombination, and fast rate of evolution (Gyllensten et al., 1991; Sato and Sato, 2013), thus being regarded as an ideal tool for population genetics, comparative genomics and phylogenetic studies (Ma et al., 2015; Sanchez et al., 2016; Tan et al., 2018). Besides, comparative analyses of the complete mitogenomes of closely related taxa can deepen the understanding of gene rearrangements and evolutionary relationships (Ren et al., 2020; Zhang et al., 2020c). With the advent of next-generation sequencing technologies, comparative mitogenomics has become an important method for molecular evolution and phylogenetic analysis (Wang et al., 2020b; Zhang et al., 2020b).
Generally, gene order in most vertebrate mitogenomes is considered highly conserved, e.g., about 4% rearrangement ratio in fish mitogenomes (Gong et al., 2013). However, extensive gene rearrangements have been observed in invertebrate mitogenomes, such as in bivalves (Wu et al., 2012), cephalopods (Xin et al., 2018), insects (Liu et al., 2017), and crabs (Wang et al., 2019). So far, five main mechanisms have been proposed to account for mitogenomic rearrangements, including tandem duplication/random loss (TDRL) model (Moritz et al., 1987), tRNA mis-priming model (Cantatore et al., 1987), intra-mitochondrial recombination model (Poulton et al., 1993), tandem duplication/non-random loss model (Lavrov et al., 2002), and dimer-mitogenome and non-random loss model (Luo et al., 2019). One of the most commonly accepted hypotheses is the TDRL model, which assumes that the rearranged gene order occurs via tandem duplications followed by random deletion of certain duplications (Moritz et al., 1987; Arndt and Smith, 1998). It has accounted for numerous rearrangements in a variety of animal mitogenomes (Ma et al., 2015; Sun et al., 2019; Yang et al., 2019).
The infraorder Brachyura is the largest clade Decapod Crustacea, with over 7 250 known species inhabiting marine, freshwater, and terrestrial habitats (Zhang, 2011; Basso et al., 2017; Chen et al., 2018). Owing to the extreme morphological and ecological diversity, morphological identification and phylogenetic relationships within Brachyura are complicated (Tan et al., 2018; Wang et al., 2020a, b). Up to now, a comprehensive analysis of the overall phylogeny of Brachyura is still lacking. Wherein the sesarmid crabs (Sesarmidae) play an important ecological role colonizing the mangroves of the Indo-Pacific, Pacific, and Atlantic regions (Lee, 1998; Gillikin and Schubart, 2004). According to WoRMS (
To better understand this model species from the molecular perspective, we firstly sequenced and described the complete mitogenome of P. eumolpe. Combined with this newly sequenced mitogenome, a comparative analysis of 11 Sesarmidae mitogenomes were conducted to reveal the genomic evolution. Gene rearrangements in 11 sesarmid crab mitogenomes were compared and possible mechanisms of rearrangement were discussed. Additionally, the most comprehensive molecular phylogenetic analysis of 107 brachyuran species was conducted based on the nucleotide and amino acid sequences of 13 PCGs. These results will help to understand the features of Sesarmidae mitogenomes and lay a foundation for further evolutionary relationships within Brachyura.
The crab specimen used in the present study was marine captured and purchased from Hainan Province, China (18°20′18″N, 109°30′50″E). The species was not involved in the endangered list of the International Union for Conservation of Nature (
The SQ Tissue DNA Kit (OMEGA, USA) was used to extract the total genomic DNA from muscle tissue of a single sample following the manufacturer’s instructions. The mitogenome of P. eumolpe was sequenced using the Illumina HisSeq 4000 platform with 150 bp paired-end reads (Shanghai Origingene Bio-pharmTechnology Co. Ltd., China). Adapters and low-quality bases were removed using Cutadapt v1.16 (Martin, 2011) with the following parameters: q, 20; m, 20. Trimmed reads shorter than 50 bp were discarded. Quality control of the raw and trimmed reads was performed using FastQC v0.11.5 (
The complete mitogenome was manually annotated using the software of Sequin (v15.10,
A total of 108 complete mitogenome sequences downloaded from the GenBank database (
The complete mitogenome of P. eumolpe (GenBank accession number MT193720) is a closed-circular molecule of 15 646 bp in length (Fig. S1), which contains 13 PCGs, two rRNAs, 22 tRNAs, as well as a putative CR (Fig. 1, Table 1). Except four PCGs (ND5, ND4, ND4L, and ND1), eight tRNAs (tRNA-His, Phe, Pro, Leu1, Val, Gln, Cys, and Tyr) and two rRNAs, which are distributed on the light (L-) strand, the rest of mitochondrial genes are distributed on the heavy (H-) strand (Table 1, Fig. S1). The genome sizes of 11 sesarmid crabs are relatively conserved, ranging from 15 611 bp (P. pictum) to 15 920 bp (Chiromantes neglectum) (Table S1). The maximum length diversification is detected in the rapidly evolving CR, which ranges from 528 bp (P. tripectinis) to 833 bp (Metopaulias depressus) and is largely responsible for the mitogenome length differences. Also, the overlapping regions and intergenic spacers are partially associated with the genome sizes (Fig. 1, Table S1).
Gene | Position | Length/bp | Amino acid | Start/Stop codon | Anticodon | Intergenic region/bp | Strand | |
From | To | |||||||
COI | 1 bp | 1 534 bp | 1 534 | 511 | ATG/T | − | 1 | H |
Leu (L2) | 1 536 bp | 1 604 bp | 69 | − | − | TAA | 6 | H |
COII | 1 611 bp | 2 298 bp | 688 | 229 | ATG/T | − | 0 | H |
Lys (K) | 2 299 bp | 2 367 bp | 69 | − | − | TTT | 0 | H |
Asp (D) | 2 368 bp | 2 435 bp | 68 | − | − | GTC | 0 | H |
ATP8 | 2 436 bp | 2 594 bp | 159 | 52 | ATG/TAA | − | −4 | H |
ATP6 | 2 591 bp | 3 262 bp | 672 | 223 | ATA/TAA | − | −1 | H |
COIII | 3 262 bp | 4 053 bp | 792 | 263 | ATG/TAA | − | −1 | H |
Gly (G) | 4 053 bp | 4 117 bp | 65 | − | − | TCC | −3 | H |
ND3 | 4 115 bp | 4 468 bp | 354 | 117 | ATA/TAA | − | 2 | H |
Ala (A) | 4 471 bp | 4 538 bp | 68 | − | − | TGC | 6 | H |
Arg (R) | 4 545 bp | 4 610 bp | 66 | − | − | TCG | 2 | H |
Asn (N) | 4 613 bp | 4 680 bp | 68 | − | − | GTT | 0 | H |
Ser (S1) | 4 681 bp | 4 747 bp | 67 | − | − | TCT | 0 | H |
Glu (E) | 4 748 bp | 4815 bp | 68 | − | − | TTC | 3 | H |
His (H) | 4 819 bp | 4 883 bp | 65 | − | − | GTG | 0 | L |
Phe (F) | 4 884 bp | 4 949 bp | 66 | − | − | GAA | 1 | L |
ND5 | 4 951 bp | 6 681 bp | 1 731 | 576 | ATG/TAA | − | 43 | L |
ND4 | 6 725 bp | 8 074 bp | 1 350 | 449 | ATG/TAA | − | −7 | L |
ND4L | 8 068 bp | 8 370 bp | 303 | 100 | ATG/TAA | − | 8 | L |
Thr (T) | 8 379 bp | 8 445 bp | 67 | − | − | TGT | 0 | H |
Pro (P) | 8 446 bp | 8 511 bp | 66 | − | − | TGG | 2 | L |
ND6 | 8 514 bp | 9 017 bp | 504 | 167 | ATT/TAA | − | 2 | H |
Cyt b | 9 020 bp | 10 151 bp | 1 132 | 377 | ATA/T | − | 0 | H |
Ser (S2) | 10 152 bp | 10 218 bp | 67 | − | − | TGA | 15 | H |
ND1 | 10 234 bp | 11 181 bp | 948 | 315 | GTG/TAA | − | 24 | L |
Leu (L1) | 11 206 bp | 11 271 bp | 66 | − | − | TAG | 0 | L |
16S | 11 272 bp | 12 603 bp | 1 332 | − | − | − | 0 | L |
Val (V) | 12 604 bp | 12 676 bp | 73 | − | − | TAC | 0 | L |
12S | 12 677 bp | 13 494 bp | 818 | − | − | − | 0 | L |
CR | 13 495 bp | 14 178 bp | 684 | − | − | − | 0 | H |
Gln (Q) | 14 179 bp | 14 246 bp | 68 | − | − | TTG | 50 | L |
Ile (I) | 14 297 bp | 14 363 bp | 67 | − | − | GAT | 6 | H |
Met (M) | 14 370 bp | 14 436 bp | 67 | − | − | CAT | 0 | H |
ND2 | 14 437 bp | 15 444 bp | 1 008 | 335 | ATG/TAG | − | −2 | H |
Trp (W) | 15 443 bp | 15 511 bp | 69 | − | − | TCA | 3 | H |
Cys (C) | 15 515 bp | 15 579 bp | 65 | − | − | GCA | 0 | L |
Tyr (Y) | 15 580 bp | 15 645 bp | 66 | − | − | GTA | 0 | L |
Note: − represents no data. CR is abbreviation of control region. |
The genes in P. eumolpe mitogenome are arranged both with interval and overlapping phenomena. There are 16 intergenic spacers with a total length of 174 bp, with the longest one (50 bp) located between tRNA-Gln and tRNA-Ile (Table 1). Simultaneously, a total of 18 bp overlapping sites are identified at six junctions. Two overlaps therein (1 bp between ATP6 and COIII, 7 bp between ND4 and ND4L) (Table 1) are also generally found in other crabs (Gong et al., 2019, 2020b; Lu et al., 2020).
The overall nucleotide composition of P. eumolpe is as follows: 36.7% A, 38.8% T, 9.8% G, and 14.7% C, respectively, with a high AT bias (75.5%) (Table S2). The skewness metrics of the mitogenome show negative AT-skew (−0.027) and negative GC-skew (−0.198) (Table S3). Also, the nucleotide composition of our newly sequenced mitogenome is compared with the other 10 Sesarmidae mitogenomes (Table S3). All the mitogenomes are rich in As and Ts, with the A+T content ranging from 74.2% (P. tripectinis) to 77.7% (Nanosesarma minutum). The base skewness is also highly congruent. The AT-skew ranges from −0.032 (P. pictum) to −0.010 (Chiromantes neglectum and Chiromantes dehaani), and the GC-skew ranges from −0.232 (Metopaulias depressus) to −0.194 (P. pictum) (Table S3). The negative AT-skew and GC-skew values among analyzed mitogenomes indicate that Ts and Cs are more abundant than As and Gs.
The mitogenome of P. eumolpe contains 13 PCGs in the typical order found in brachyuran species, consisting of seven NADH dehydrogenases (ND1−ND6 and ND4L), three cytochrome c oxidases (COI−COIII), two ATPases (ATP6 and ATP8), and one cytochrome b (Cyt b). All PCGs are initiated by the start codon ATN (ATA, ATG, and ATT), with an exception (GTG) in ND1. The majority of the 13 PCGs terminate with TAA or TAG, whereas three other PCGs (COI, COII, and Cyt b) use a single T as a stop codon (Table 1). Incomplete stop codons are common in both invertebrate and vertebrate mitochondrial genes and may be recovered via post-transcriptional polyadenylation (Ojala et al., 1981).
The amino acid composition and relative synonymous codon usage of 11 sesarmid crabs are roughly identical. The most frequently used amino acids are Leu, Ser, Phe, and Ile in these mitogenomes (Fig. S2). In consistent with other brachyuran species (Lu et al., 2020; Wang et al., 2020a, b), the usage of two- and four-fold degenerate codons in these sesarmid crabs is biased toward the use of codons abundant in A or T (Fig. 1, Table S2). In addition, the codons Arg (CGC) and Cys (UGC) are absent in Episesarma lafondii and P. pictum mitogenomes, and Arg (CGC) is also absent in the other five Sesarmidae species (Chiromantes dehaani, Chiromantes haematocheir, Clistocoeloma sinense, N. minutum, and P. affine) (Fig. S2, Table S2). Both of the missing codons are preferred to end with “C” in the third codon position.
The mitogenome of P. eumolpe contains 22 tRNA genes scattered throughout the genome. The tRNAs size range from 65 bp to 73 bp with a total length of 1 480 bp. Most tRNAs display a typical cloverleaf secondary structure except for tRNA-Ser (TCT) that lacks the dihydrouridine (DHU) arm (Fig. S3), which is thought to be a common phenomenon in metazoan mitogenomes (Lü et al., 2019; Ruan et al., 2020; Wang et al., 2020a). Except for the normal base pairing and G-U, three kinds of mismatches are found in tRNAs. One C-U base pair is predicted in tRNA-Lys, one C-A base pair is predicted in tRNA-Ser (S1) and two U-U base pairs are predicted in tRNA-His and tRNA-Leu (L1). The total length of the two rRNAs in P. eumople is 2 150 bp. Of the two genes, the 16S rRNA is 1 332 bp located between tRNA-Leu (L1) and tRNA-Val, while the 12S rRNA is 818 bp and resides between tRNA-Val and CR (Fig. S1, Table 1).
The CR of P. eumople is located between 12S rRNA and tRNA-Gln, with an extremely high AT content (81.7%). The CR is the most variable region because of a faster evolution rate compared with the other genes. Nevertheless, the alignment of 11 Sesarmidae CRs reveals five conserved sequence blocks (Fig. 1). Their consensus sequences are as follows: ATATATGTATAT (CSB-A), TACGGAT-ATATA (CSB-B), GTAATTTCAATGGTTTAGA (CSB-C), TCTAA-ACCAATGAAAT-TAC (CSB-D), and ATTATATTATATTTAA-TTAAATGTATATATA--TATATAT (CSB-E) (the underlined letters represent the fluctuant nucleotide among the 11 Sesarmidae species). Additionally, several tandem repeat units are detected in the CRs in almost all sesarmid crab mitogenomes except for P. affine and P. eumolpe (Fig. 2). The motif length and copy number of tandem repeat units present dramatic differences among these analyzed Sesarmidae mitogenomes. The longest motif is 72 bp occurred in N. minutum CR, followed by 38 bp in Chiromantes haematocheir CR; the largest copy number is 4 occurred in Chiromantes haematocheir and Metopaulias depressus CR. Notably, Chiromantes neglectum and Chiromantes dehanni CR share two identical tandem repeat units almost in the same location; however, no similar tandem repeat unit is detected in other CRs. So far, there have been few studies on the conserved blocks, especially their potential functions in invertebrate mitogenomes (Ray and Densmore, 2002; Guo et al., 2003; Zhao et al., 2011). Comparative analyses of more distantly related species and several imperative functional experiments are needed to uncover the conserved sequence blocks related to its function and further to illuminate the functional importance of CR.
To detect the selective pressure of 13 PCGs in sesarmid crabs, we conduct pairwise Ka/Ks analyses for each PCG. It is commonly accepted that Ka>Ks, Ka=Ks, and Ka<Ks generally indicate positive selection, neutral mutation, and purifying selection, respectively (Yang, 2006). The results show that all 13 PCGs among the 11 Sesarmidae mitogenomes are evolving under a purifying selection. COI gene exhibits the strongest purifying selection, whereas the NADH family genes (especially ND6) exhibits a slightly relaxed purifying selection; ATP8 is an outlier, with pairwise comparison values ranging from neutral selection (0.000) to positive selection (1.039) (Fig. 3). The lowest Ka/Ks ratio for COI gene indicates strong evolutionary conservation, which results in the COI gene often being used as a potential molecular marker (Hebert et al., 2003). In contrast, the ATP8 gene exhibits the highest evolutionary rate of all the PCGs, which implies that the ATP8 gene can be used to evaluate intraspecific relationships (Wang et al., 2015). Furthermore, the Ka/Ks values in Sesarmidae species reveal that the environment variation is not great enough to change their genetic function.
So far, three main types of gene rearrangement events have been observed in the mitogenomes of animal, including translocation, shuffling, and inversion (Thyagarajan et al., 1996; Macey et al., 1997; Tsaousis et al., 2005; Zhuang and Cheng, 2010). Here, two translocations are detected in P. eumolpe mitogenome. One is the translocation of tRNA-His (H). Compared with the gene order of the ancestor of Decapoda, the tRNA-His (H) is rearranged from the downstream of ND5 (Fig. 4a) to the position between tRNA-Glu (E) and tRNA-Phe (F), forming a new gene block (E-H-F-ND5-ND4) in P. eumolpe mitogenome (Fig. 4b). The translocation of tRNA-His gene is a relatively common event in brachyuran mitogenomes (Lu et al., 2020; Wang et al., 2020a, b). The other translocation is identified in tRNA-Gln (Q) when selecting the ancestral mitochondrial gene order of Brachyura as a reference. The typical IQM arrangement (tRNA-Ile-Gln-Met) is changed to QIM order (tRNA-Gln-Ile-Met), which is identical with other published Sesarmidae mitogenomes (Wang et al., 2018, 2019) (Fig. 4c).
How did the mitogenome structure of P. eumolpe emerge? Based on the rearrangement features and principle of parsimony, the TDRL is adopted to explain the rearrangement events in P. eumolpe mitogenome. The hypothesized intermediate steps are as follows, starting with the typical ancestral order of the Decapoda mitogenome (Fig. 4a). First, the F-ND5-H genes underwent a complete copy, forming a dimeric block (F-ND5-H)- (F′-ND5′-H'). Consecutive copies were then followed by a random loss of supernumerary genes, namely F-ND5-H-F′-ND5′-H′ (the underlined letters represent the deleted genes). Thus a new H-F-ND5 gene order was formed (Fig. 4b). In the following step, the gene order of the gene block (CR-I-Q-M) was changed to CR-Q-I-M through the same mechanism (Fig. 4c).
Considering these 11 Sesarmidae mitogenomes analyzed in this study share the same gene arrangement (Fig. 4c), which was resulted from the translocation of two tRNAs (tRNA-His and tRNA-Gln). So is there a universal mechanism to account for the rearrangement events? The TDRL model used in P. eumolpe mitogenome is generally featured by the presence of intergenic spacers as a result of incomplete deletion of the duplicated genes (Moritz et al., 1987; Arndt and Smith, 1998). Here, different levels of intergenic spacers were found in the two rearranged regions (H-F-ND5 and CR-Q-I-M) in these 11 Sesarmidae mitogenomes. The intergenic spacers in the rearranged regions are as follows: 1 bp to 9 bp between E and H (G1); 1 bp to 2 bp between H and F (G2); 1 bp to 7 bp between F and ND5 (G3); 15 bp to 50 bp between ND5 and ND4 (G4); 14 bp to 211 bp between Q and I (G5); and 6 bp to 63 bp between I and M (G6) (Fig. 4). These features in rearranged regions support that the novel gene order in Sesarmidae mitogenomes can be well explained by the TDRL model.
In this study, we reconstructed the phylogenetic relationships of Brachyura based on the nucleotide and amino acid sequences of 13 PCGs using ML and BI methods (Figs 5, S4 and S5). The phylogenetic trees (ML tree and BI tree) based on the nucleotide sequences produce an identical structure. Here, only one topology (BI) with both support values is displayed (Fig. 5). However, the phylogenetic trees based on the amino acid sequences are not consistent, and both trees are slightly different from the nucleotide trees (Figs S4−S6). In both the nucleotide and amino acid trees, all Sesarmidae species cluster into a clade and consist of two sister groups. Nevertheless, the phylogenetic position of Nanosesarma within this family is not consistent. The BI tree of the nucleotide sequences shows that N. minutum forms a sister clade with four Parasesarma species, while N. minutum interfuses the Parasesarma clade in the BI tree of the nucleotide sequences and the amino acid trees. Because the genus Nanosesarma has only one representative, long-branch attraction (Philippe, 2000; Boussau et al., 2014) may lead to this topology. Future researches that include more sample volume are essential to confirm the phylogenetic placement of Nanosesarma.
Of the 29 families included in the phylogenetic trees, the monophyly of each family is strongly supported except Xanthidae and Homolidae (Figs 5, S4 and S5). However, it is worth noting that the monophyly of Gecarcinidae is presented in the amino acid trees, whereas it consists of two clades in the nucleotide trees, one of which forms a sister clade with Sesarmidae. Viewed from a higher taxonomic level, the polyphyly of three superfamilies (Eriphioidea, Ocypodoidea, and Grapsoidea) is well supported in both the nucleotide and amino acid trees (Figs 5, S4 and S5). However, within the polyphyly of Ocypodoidea and Grapsoidea, the relationships among different families are inconsistent (Fig. S6). The ML tree of the amino acid sequences places Ocypodidae at a relatively basal position, which is in accord with Tan’s result (Ma et al., 2019). Whereas the nucleotide trees and the BI tree of the amino acid sequences show that Ocypodidae forms a sister clade with Xengrapsidae, which in turn affects the positions of the other families as well. Therefore, the interrelationships among these two taxa need further analysis by integrating more molecular data. Besides, the superfamily status of Portunoidea has been constantly debated, with its constituent families varying among different authors. The latest results support a more conservative classification of Portunoidea with three instead of eight extant families: Geryonidae (Geryonidae+Ovalipidae), Carcinidae (Carcinidae+Pirimelidae+Polybiidae+Thiidae+Coelocarcinus) and Portunidae (Evans, 2018). However, the current phylogeny suggests different relationships among the three major Portunoidea groups. Here, Ovalipidae and Geryonidae cluster together as sister groups, which supports the latest classification of Portunoidea. While in previous researches, Ovalipidae is revealed to be more closely related to the Carcinidae+Polybiidae clade (Ma et al., 2019) or Portunidae (Tsang et al., 2014).
Previous findings showed that the evolution process of mitogenomes could be revealed by the length of gap spacer in the rearranged area (Kumazawa and Nishida, 1995; McKnight and Shaffer, 1997; Gong et al., 2020a). In order to explore the relationship between the phylogeny of Sesarmidae species and the gaps in the CR-Q-I-M region, four phylogenetic trees (two nucleotide trees and two amino acid trees) were constructed including 11 sesarmid crabs (Fig. 6). Except for the phylogenetic position of N. minutum, the ML tree of the amino acid sequences has the same topology as the other three phylogenetic trees. Although the difference exists, an obvious correlation between the gaps in the rearranged CR-Q-I-M region and the phylogenetic position of each sesarmid crab is observed (Fig. 6). Our results show that with the evolution of sesarmid crabs, the gap spacers (G5 and G6) decrease progressively under the degradation pressure of non-functional genes.
In this study, the complete mitogenome of P. eumolpe was sequenced. The 15 646 bp mitogenome contains 37 genes and one AT-rich region, as is typical of metazoan mitogenome. Compared to other previously reported complete mitogenomes of Sesarmidae, all of them have similar molecular characteristics. Although all 13 PCGs evolve under purifying selection, the ATP8 gene evolves under a highly relaxed selection. All of these analyzed Sesarmidae mitogenomes capture the same gene rearrangements, which can be fully explained by the TDRL model. The most comprehensive molecular phylogenetic analysis of Brachyura was constructed, and the polyphyly of three superfamilies (Eriphioidea, Ocypodoidea, and Grapsoidea) is reconfirmed. However, large-scale taxonomic samplings are still needed to further investigate the genomic evolution within Sesarmidae and better understand the taxonomical and phylogenetic studies of Brachyura.
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Gene | Position | Length/bp | Amino acid | Start/Stop codon | Anticodon | Intergenic region/bp | Strand | |
From | To | |||||||
COI | 1 bp | 1 534 bp | 1 534 | 511 | ATG/T | − | 1 | H |
Leu (L2) | 1 536 bp | 1 604 bp | 69 | − | − | TAA | 6 | H |
COII | 1 611 bp | 2 298 bp | 688 | 229 | ATG/T | − | 0 | H |
Lys (K) | 2 299 bp | 2 367 bp | 69 | − | − | TTT | 0 | H |
Asp (D) | 2 368 bp | 2 435 bp | 68 | − | − | GTC | 0 | H |
ATP8 | 2 436 bp | 2 594 bp | 159 | 52 | ATG/TAA | − | −4 | H |
ATP6 | 2 591 bp | 3 262 bp | 672 | 223 | ATA/TAA | − | −1 | H |
COIII | 3 262 bp | 4 053 bp | 792 | 263 | ATG/TAA | − | −1 | H |
Gly (G) | 4 053 bp | 4 117 bp | 65 | − | − | TCC | −3 | H |
ND3 | 4 115 bp | 4 468 bp | 354 | 117 | ATA/TAA | − | 2 | H |
Ala (A) | 4 471 bp | 4 538 bp | 68 | − | − | TGC | 6 | H |
Arg (R) | 4 545 bp | 4 610 bp | 66 | − | − | TCG | 2 | H |
Asn (N) | 4 613 bp | 4 680 bp | 68 | − | − | GTT | 0 | H |
Ser (S1) | 4 681 bp | 4 747 bp | 67 | − | − | TCT | 0 | H |
Glu (E) | 4 748 bp | 4815 bp | 68 | − | − | TTC | 3 | H |
His (H) | 4 819 bp | 4 883 bp | 65 | − | − | GTG | 0 | L |
Phe (F) | 4 884 bp | 4 949 bp | 66 | − | − | GAA | 1 | L |
ND5 | 4 951 bp | 6 681 bp | 1 731 | 576 | ATG/TAA | − | 43 | L |
ND4 | 6 725 bp | 8 074 bp | 1 350 | 449 | ATG/TAA | − | −7 | L |
ND4L | 8 068 bp | 8 370 bp | 303 | 100 | ATG/TAA | − | 8 | L |
Thr (T) | 8 379 bp | 8 445 bp | 67 | − | − | TGT | 0 | H |
Pro (P) | 8 446 bp | 8 511 bp | 66 | − | − | TGG | 2 | L |
ND6 | 8 514 bp | 9 017 bp | 504 | 167 | ATT/TAA | − | 2 | H |
Cyt b | 9 020 bp | 10 151 bp | 1 132 | 377 | ATA/T | − | 0 | H |
Ser (S2) | 10 152 bp | 10 218 bp | 67 | − | − | TGA | 15 | H |
ND1 | 10 234 bp | 11 181 bp | 948 | 315 | GTG/TAA | − | 24 | L |
Leu (L1) | 11 206 bp | 11 271 bp | 66 | − | − | TAG | 0 | L |
16S | 11 272 bp | 12 603 bp | 1 332 | − | − | − | 0 | L |
Val (V) | 12 604 bp | 12 676 bp | 73 | − | − | TAC | 0 | L |
12S | 12 677 bp | 13 494 bp | 818 | − | − | − | 0 | L |
CR | 13 495 bp | 14 178 bp | 684 | − | − | − | 0 | H |
Gln (Q) | 14 179 bp | 14 246 bp | 68 | − | − | TTG | 50 | L |
Ile (I) | 14 297 bp | 14 363 bp | 67 | − | − | GAT | 6 | H |
Met (M) | 14 370 bp | 14 436 bp | 67 | − | − | CAT | 0 | H |
ND2 | 14 437 bp | 15 444 bp | 1 008 | 335 | ATG/TAG | − | −2 | H |
Trp (W) | 15 443 bp | 15 511 bp | 69 | − | − | TCA | 3 | H |
Cys (C) | 15 515 bp | 15 579 bp | 65 | − | − | GCA | 0 | L |
Tyr (Y) | 15 580 bp | 15 645 bp | 66 | − | − | GTA | 0 | L |
Note: − represents no data. CR is abbreviation of control region. |