Comparative mitochondrial genome analysis of Varunidae and its phylogenetic implications
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Abstract: Complete mitochondrial genomes (mitogenomes) can indicate phylogenetic relationships, as well as useful information for gene rearrangement mechanisms and molecular evolution. Currently, the phylogenetic location of the genus Varuna (Brachyura: Varunidae) has not been well resolved mainly because of limited representatives (only two extant species). Here, we determined a new mitogenome of this genus (Varuna litterata) and added the published mitogenomes to reconstruct the phylogeny of Varunidae. The 16 368-bp mitogenome contains the entire set of 37 genes and a putative control region. The characteristics of this newly sequenced mitogenome were described and compared with the other 15 Varunidae mitogenomes. All 16 analyzed mitogenomes have identical gene order and similar molecular features. The sliding window and genetic distance analyses demonstrate highly variable nucleotide diversity, with comparatively low variability of COI and COII, and high variability of ND6. The nonsynonymous/synonymous substitution rates (dN/dS ratio) analysis shows that all 13 PCGs are under purifying selection and ATP8 gene evolves under the least selective pressure. Twelve tRNA genes, two rRNAs, one PCG, and the putative control region are found to be rearranged with respect to the pancrustacean ground pattern gene order. Tandem duplication/random loss model is adopted to explain the large-scale gene rearrangement events occurring in Varunidae mitogenomes. Phylogenetic analyses show that all Varunidae species are placed into one group, and form a sister clade with Macrophthalmidae. Nevertheless, the phylogenetic relationships within Varunidae are not completely consistent based on the two different datasets used in this study. These findings will contribute to a better understanding of gene rearrangement and molecular evolution in Varunidae mitogenomes, as well as provide insights into the phylogenetic studies of Brachyura.
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Key words:
- varunid crab /
- Varuna litterata /
- mitogenome /
- gene rearrangement /
- tandem duplication/random loss /
- phylogeny
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Figure 1. The base skews of 13 PCGs of 16 Varunidae mitogenomes. a. GC-skews, b. AT-skews.
Figure 2. Structure of control region in 16 Varunidae mitogenomes. The colored ovals indicate the tandem repeats; the remaining regions are shown with green boxes. The tandem repeat with copy number exceeding 7 is displayed in the format of (motif)n.
Figure 3. Sliding window analyses of 13 PCGs (green box) and 2 rRNAs (orange box) among 16 Varunidae mitogenomes (a). The red line shows the value of nucleotide diversity (Pi) in a sliding window analysis (a sliding window of 200 bp with a step size of 20 bp). Gene names and the Pi value of each gene are indicated above or below the graph. Genetic distance (on average) and nonsynonymous/synonymous substitution rates (dN/dS) of 13 PCGs among 16 Varunidae species (b).
Figure 4. Phylogenetic trees of Varunidae species inferred from 13 PCGs based on different methods. a. Nucleotide sequences based on maximum likelihood (ML) and Bayesian inference (BI) analysis; b. amino acid sequences based on ML analysis; c. amino acid sequences based on BI analysis. Node marked with a solid circle indicates 100 maximum likelihood bootstrap value and 100% supporting value.
Figure 5. Phylogenetic tree of Brachyuran species inferred from the nucleotide sequences of 13 PCGs based on maximum likelihood (ML) and Bayesian inference (BI) analysis. Node marked with a solid circle indicates 100 maximum likelihood bootstrap value and 100% supporting value.
Figure 6. Inferred intermediate steps between the ancestral gene arrangement of crustaceans and Varunidae mitogenomes. a. The ancestral gene arrangement of crustaceans; b. the results of one tandem duplication/random loss (TDRL) event and the ancestral gene arrangement of Brachyura; c. the results of two TDRL events and the final gene arrangement in Varuna litterata and 15 other varunid species. The duplicated gene block is underlined and the lost genes are labeled with gray.
Table 1. Features of the mitochondrial genome of Varuna litterata
Gene Position Length/
bpAmino
acidStart/Stop
codonAnticodon Intergenic
regionStrand From To COI 1 bp 1534 bp 1534 511 ATG/T – 0 H Leu (L2) 1535 bp 1600 bp 66 – – TAA 5 H COII 1606 bp 2310 bp 705 234 ATG/TAA – 12 H ATP8 2323 bp 2484 bp 162 53 ATG/TAA – −7 H ATP6 2478 bp 3152 bp 675 224 ATT/TAA – −1 H COIII 3152 bp 3943 bp 792 263 ATG/TAA – −1 H Gly (G) 3943 bp 4007 bp 65 – – TCC 0 H ND3 4008 bp 4358 bp 351 116 ATT/TAA – 1 H Ala (A) 4360 bp 4422 bp 63 – – TGC 2 H Arg (R) 4425 bp 4487 bp 63 – – TCG −1 H Asn (N) 4487 bp 4551 bp 65 – – GTT 0 H Ser (S1) 4552 bp 4618 bp 67 – – TCT 22 H Thr (T) 4641 bp 4705 bp 65 – – TGT 2 H Pro (P) 4708 bp 4771 bp 64 – – TGG 20 L ND1 4792 bp 5727 bp 936 311 ATG/TAA – 31 L Leu (L1) 5759 bp 5825 bp 67 – – TAG 0 L 16S 5826 bp 7198 bp 1373 – – – 0 L 12S 7199 bp 8087 bp 889 – – – 0 L His (H) 8088 bp 8150 bp 63 – – GTG 6 L ND5 8157 bp 9890 bp 1734 577 ATA/TAA – 126 L Val (V) 10 017 bp 10 089 bp 73 – – TAC 0 L CR 10 090 bp 11 185 bp 1096 – – – 0 H Gln (Q) 11 186 bp 11 254 bp 69 – – TTG 11 L Cys (C) 11 266 bp 11 328 bp 63 – – GCA 0 L Tyr (Y) 11 329 bp 11 393 bp 65 – – GTA 2 L Lys (K) 11 396 bp 11 465 bp 70 – – TTT −2 H Asp (D) 11 464 bp 11 531 bp 68 – – GTC 6 H Glu (E) 11 538 bp 11 602 bp 65 – – TTC 2 H Phe (F) 11 605 bp 11 669 bp 65 – – GAA 14 L ND4 11 684 bp 13 021 bp 1338 445 ATG/TAG – −7 L ND4L 13 015 bp 13 326 bp 312 103 ATA/TAA – 87 L ND6 13 414 bp 13 923 bp 510 169 ATT/TAA – −1 H Cyt b 13 923 bp 15 057 bp 1135 378 ATG/T – 0 H Ser (S2) 15 058 bp 15 124 bp 67 – – TGA 20 H Ile (I) 15 145 bp 15 209 bp 65 – – GAT 4 H Met (M) 15 214 bp 15 281 bp 68 – – CAT 0 H ND2 15 282 bp 16 292 bp 1011 336 ATC/TAG – −2 H Trp (W) 16 291 bp 16 358 bp 68 – – TCA 9 H Note: – represents no data. CR is abbreviation of control region. 
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Table 2. The percentage content of composition and skewness of Varuna litterata mitogenome
A/% T/% G/% C/% (A+T)/% AT-skew GC-skew Length/bp Mitogenome 35.2 36.2 10.8 17.8 71.4 −0.014 −0.243 16 368 PCGs 28.2 40.3 15.6 16.0 68.4 −0.177 −0.011 11 195 COI 27.8 35.2 16.9 20.1 63.0 −0.118 −0.088 1539 COII 32.5 34.8 12.8 20.0 67.2 −0.034 −0.221 705 ATP8 35.8 48.8 3.7 11.7 84.6 −0.153 −0.520 162 ATP6 28.9 39.0 11.7 20.4 67.9 −0.148 −0.272 675 COIII 26.8 37.0 15.2 21.1 63.8 −0.160 −0.164 792 ND3 30.8 41.6 10.3 17.4 72.4 −0.150 −0.258 351 ND1 25.4 43.5 20.7 10.4 68.9 −0.262 0.333 936 ND5 28.1 40.7 20.9 10.3 68.8 −0.184 0.342 1734 ND4 28.1 42.6 19.7 9.6 70.7 −0.205 0.342 1338 ND4L 27.9 47.4 18.6 6.1 75.3 −0.260 0.506 282 ND6 26.7 47.5 6.9 19.0 74.1 −0.280 −0.470 549 Cyt b 26.9 37.5 14.4 21.2 64.4 −0.166 −0.193 1135 ND2 29.5 43.7 8.1 18.7 73.2 −0.195 −0.395 1011 16S rRNA 40.4 39.0 13.6 7.0 79.4 0.018 0.322 1373 12S rRNA 41.4 38.7 12.7 7.2 80.1 0.034 0.277 889 tRNAs 38.0 35.8 14.9 11.3 73.8 0.031 0.134 1454 CR 38.0 42.2 11.1 8.7 80.2 −0.053 0.124 1096
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Table 3. The percentage content of composition and skewness of mitogenome in 16 Varunidae species
Species A/% T/% G/% C/% (A + T)/% AT-skew GC-skew Length/bp Cyclograpsus granulosus 33.1 36.1 11.2 19.5 69.3 −0.043 −0.272 16 300 Pseudohelice subquadrata 34.2 33.5 10.5 21.7 67.7 0.010 −0.347 16 898 Helicana wuana 33.0 35.5 11.5 20.0 68.4 −0.037 −0.269 16 359 Helice latimera 34.0 35.1 11.0 19.9 69.1 −0.017 −0.290 16 246 Helice tientsinensis 33.9 35.1 11.0 19.9 69.1 −0.017 −0.289 16 212 Cyclograpsus intermedius 34.7 35.9 10.7 18.7 70.6 −0.017 −0.270 16 184 Eriocheir hepuensis 35.1 36.4 10.8 17.7 71.5 −0.018 −0.245 16 335 Eriocheir sinensis 35.3 36.4 10.7 17.7 71.6 −0.015 −0.248 16 354 Eriocheir japonica 35.2 36.5 10.7 17.7 71.6 −0.018 −0.245 16 352 Neoeriocheir leptognathus 35.6 39.0 10.1 15.3 74.6 −0.046 −0.206 16 143 Hemigrapsus penicillatus 34.1 36.4 11.4 18.1 70.5 −0.033 −0.229 16 486 Hemigrapsus sanguineus 34.3 35.5 11.2 19.1 69.8 −0.018 −0.260 16 275 Metaplax longipes 37.6 33.8 10.6 17.9 71.4 0.053 −0.257 16 305 Varuna litterata 35.2 36.2 10.8 17.8 71.4 −0.014 −0.243 16 368 Varuna yui 35.7 36.5 10.2 17.6 72.2 −0.011 −0.265 15 915 Gaetice depressus 35.4 37.6 10.5 16.5 73.0 −0.030 −0.223 16 288
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