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Acta Oceanol. Sin., 2015, Vol. 34, No. 2, P. 84–92 DOI: 10.1007/s13131-015-0583-1 http://www.hyxb.org.cn E-mail: [email protected] Phylomitogenomics of (Arthropoda: Crustacea) SHEN Xin1, 2, 3*, TIAN Mei1, YAN Binlun1, CHU Kahou3 1 Jiangsu Key Laboratory of Marine Biotechnology/College of Marine Science, Huaihai Institute of Technology, Lianyungang 222005, 2 Beijing Institutes of Life Science, Chinese Academy of Sciences, Beijing 100101, China 3 Simon F. S. Li Marine Science Laboratory, School of Life Sciences, The Chinese University of Hong Kong, Hong Kong, China Received 25 February 2014; accepted 29 August 2014

©The Chinese Society of Oceanography and Springer-Verlag Berlin Heidelberg 2015

Abstract Along with the sequencing technology development and continual enthusiasm of researchers on the mitochondrial genomes, the number of metazoan mitochondrial genomes reported has a tremendous growth in the past decades. Phylomitogenomics—reconstruction of phylogenetic relationships based on mitochondrial genomic data—is now possible across large groups. in the class Malacostraca display a high diversity of body forms and include large number of ecologically and commercially important . In this study, comprehensive and systematic analyses of the phylogenetic relationships within Malacostraca were conducted based on 86 mitochondrial genomes available from GenBank. Among 86 malacostracan mitochondrial genomes, 54 species have identical major gene arrangement (excluding tRNAs) to pancrustacean ground pattern, including six species from Stomatopoda, three species from , two , seven species from (), and 36 species from (Decapoda). However, the other 32 mitochondrial genomes reported exhibit major gene rearrangements. Phylogenies based on Bayesian analyses of nucleotide sequences of the protein-coding genes produced a robust with 100% posterior probability at almost all nodes. The results indicate that Amphipoda and cluster together (Edriophthalma) (BPP=100). Phylomitogenomic analyses strong support that Euphausiacea is nested within Decapoda, and closely related to Dendrobranchiata, which is also consistent with the evidence from developmental biology. Yet the taxonomic sampling of mitochondrial genome from Malacostraca is very biased to the Decapoda, with no complete mitochondrial genomes reported from 11 of the 16 orders. Future researches on sequencing the mitochondrial genomes from a wide variety of malacostracans are necessary to further elucidate the phylogeny of this important group of . With the increase in mitochondrial genomes available, phylomitogenomics will emerge as an important component in the Tree of Life researches. Key words: Malacostraca, Crustacea, Phylomitogenomics, gene arrangement, mitochondrial genome Citation: Shen Xin, Tian Mei, Yan Binlun, Chu Kahou. 2015. Phylomitogenomics of Malacostraca (Arthropoda: Crustacea). Acta Oceanologica Sinica, 34(2): 84–92, doi: 10.1007/s13131-015-0583-1

1 Introduction close related species so that there is a lack of large-scale and Complete mitochondrial genomes of human (Homo sapiens) comparison in many major animal groups. As the genome data- and mouse (Mus musculus) were sequenced in 1981 (Anderson et bases now contain thousands of animal mitochondrial genomes, al., 1981; Bibb et al., 1981), which are the first ones available in it allows comprehensive analysis and evaluation of existing data Metazoa. The number of metazoan mitochondrial genomes re- in a major group based on a large number of taxa. To assess and ported reaches 127 by the end of the year 2000. However, from analyze the existing mitochondrial genomic information, which 2001 to the present, along with the sequencing technology devel- not only help to reconstruct animal phylogeny based on mito- opment and the continued enthusiasm of researchers on mito- chondrial genomes, but also help to pinpoint the gaps in the cur- chondrial genomes, the number of metazoan mitochondrial gen- rent mitochondrial genomic data, and thus provide guidance for omes reported increases tremendously. The metazoan mito- future researches. As a case study, this study examines the situ- chondrial genomes available from GenBank have reached 3 653 ation in malacostracans from the viewpoint of phylomitogenom- by the end of 2013 (Fig. 1). Phylomitogenomics, the use of mito- ics. chondrial genomic data in resolving phylogenetic relationships, The class Malacostraca is the largest of the six classes of crus- has emerged to be an important approach in phylogenetic recon- taceans, containing about 25 000 extant species, and is divided struction. into 16 orders. Malacostracans display a high diversity of body When mitochondrial genomes of one or several new species forms, and include , , krill, , woodlice, mantis were obtained, the researchers often compare them with those of shrimp and many other species (Martin and Davis, 2001).

Foundation item: The National Natural Science Foundation of China under contract Nos 41476146 and 40906067; Hong Kong Scholars Program under contract No. XJ2012056; China Postdoctoral Science Foundation under contract Nos 2012M510054 and 2012T50218; a project funded by the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD). *Corresponding author, E-mail: [email protected] SHEN Xin et al. Acta Oceanol. Sin., 2015, Vol. 34, No. 2, P. 84–92 85

Malacostracans not only contain a wide variety of taxa, but also long time a hotly debated issue (Richter and Scholtz, 2001; von include many species with high ecological and economic values. Reumont et al., 2012). In this paper, comprehensive analyses of In the past hundreds of years, there have been many studies fo- the phylogenetic relationships within Malacostraca were con- cused on its systematic and evolutionary relationships. Literat- ducted based on 86 mitochondrial genomes available. In addi- ures exploring the malacostracan relationships based on mor- tion, the knowledge gaps of the current mitochondrial genomic phological and molecular data are numerous. Evolutionary rela- data are also noted to guide future researches. tionships among the various groups of Malacostraca was for a

Fig. 1. Growth curve of metazoan mitochondrial genomes released in GenBank.

2 Materials and methods (atp6, atp8, cob, cox1-3, nad1-4, nad4L, nad5 and nad6) were separately aligned using Clustal X 1.83 (Thompson et al., 1997) 2.1 Data acquisition (default parameters) and then concatenated as a single dataset of A total of 3 653 metazoan mitochondrial genomes were 11 584 base pairs (bp) for analysis. Model selection for the nucle- downloaded (ftp://ftp.ncbi.nlm.nih.gov/genomes/). Then 86 otide acid dataset was done with jModelTest (Darriba et al., 2012) malacostracan mitochondrial genomes were obtained by self- and the best model was GTR matrix and the Gamma+Invar mod- written PERL script. The taxa are shown in Table 1, including rep- el. Phylogenetic analysis was performed using MrBayes 3.1 (Ron- resentatives from five orders, with 60 species from Decapoda quist and Huelsenbeck, 2003). Four Markov chains of 1 000 000 (Wilson et al., 2000; Yamauchi et al., 2002; Yamauchi et al., 2003; generations were run with sampling every 1 000 generations. The Miller et al., 2004; Yamauchi et al., 2004; Miller et al., 2005; Place first quarter (250 000 generations) was excluded from the analys- et al., 2005; Segawa and Aotsuka, 2005; Sun et al., 2005; Ivey and is as “burn-in”. After omitting the first 250 “burn in” , the re- Santos, 2007; Shen et al., 2007; Yang et al., 2008; Ki et al., 2009; maining 750 sampled trees were used to estimate the consensus Peregrino-Uriarte et al., 2009; Shen et al., 2009; Liu and Cui, tree and the Bayesian posterior probability (BPP). 2010a; Yang et al., 2010; Ma et al., 2011; Qian et al., 2011; Gene rearrangement information was indicated in the phylo- Jondeung et al., 2012; Kim et al., 2012a; Kim et al., 2011; Kim et genetic tree constructed using the protein-coding gene se- al., 2012b; Lin et al., 2012; Liu and Cui, 2011; Shi et al., 2012; Yang quences. Thus information from mitochondrial genomes as a et al., 2012; Kim et al., 2013a; Kim et al., 2013b; Ma et al., 2013; whole (including sequence information and gene arrangement) Shen et al., 2013; Yang et al., 2013; Wang et al., 2014), two from were used for exploring the phylogenetic relationships of the tar- Euphausiacea (Shen et al., 2010; Shen et al., 2011), six from Sto- get groups, which is basic requirement of phylomitogenomic matopoda (Cook, 2005; Miller and Austin, 2006; Liu and Cui, analyses. 2010b), sixteen from Amphipoda (Bauza-Ribot et al., 2009; Ito et al., 2010; Ki et al., 2010; Kilpert and Podsiadlowski, 2010b; Bauza- 3 Results and discussion Ribot et al., 2012; Krebes and Bastrop, 2012; Shin et al., 2012), and two from Isopoda (Kilpert and Podsiadlowski, 2006; Kilpert and 3.1 Characteristics of malacostracan mitochondrial genomes Podsiadlowski, 2010a). The length of decapod mitochondrial genomes ranges from 14 316 bp (H. gammarus) to 18 197 bp (G. dehaani) (Table 1). The 2.2 Comparison of major gene arrangements two krill mitochondrial genomes are 15 498 bp and 16 898 bp in Due to the high frequency of translocations and inversions of length for E. superba (incomplete) and E. pacifica, respectively. the transfer RNA (tRNA) genes in animal mitochondrial gen- The length of mitochondrial genomes ranges from omes, major coding gene (protein-coding genes and ribosomal 15 714 bp (H. harpax) to 16 325 bp (L. maculata). In Amphipoda, RNA genes) arrangement may provide more reliable information the length of mitochondrial genomes varies between 14 113 bp than tRNA genes when we focus on the comparison of higher (M. longipes) and 18 424 bp (G. antarctica). The length of two iso- level taxa. In this paper, the major gene arrangement of the 86 pod mitochondrial genomes is 15 289 bp (L. oceanica) and 14 994 malacostracan mitochondrial genomes were analyzed and com- bp (E. sp.14 FK-2009), respectively. pared systematically. In Decapoda, the A + T contents of the mitochondrial heavy chain are between 60.2% (A. distinguendus) and 74.9% (G. de- 2.3 Phylomitogenomic analysis haani) (Table 1). The values for two krill mitochondrial genomes Nucleotide sequences of each of the 13 protein-coding genes are 68.1% and 72.0% for E. superba and E. pacifica, respectively. 86 SHEN Xin et al. Acta Oceanol. Sin., 2015, Vol. 34, No. 2, P. 84–92

And the values for mantis are between 63.8% (L. macu- species, including A. chinensis (Decapoda: ), S. cros- lata) and 70.8% (O. oratoria). As for Amphipoda, the A + T con- nieri (Decapoda: ), E. occidentalis (Decapoda: As- tents of mitochondrial genomes are between 64.0% (G. duebeni) tacidea), H. gammarus (Decapoda: ), G. dehaani (Deca- and 76.9% (M. repens). And values for the two isopods are 60.8% poda: Brachyura), S. hispidus (Decapoda: ), N. ja- (L. oceanica) and 69.6% (E. sp.14 FK-2009). ponica (Decapoda: ), E. superba (Euphausiacea: Eu- The gene content of malacostracan mitochondrial genomes is phausiidae), M. longipes (Amphipoda: Hadzioidea) and L. ocean- conserved. Among the 86 malacostracan mitochondrial gen- ica (Isopoda: Diplocheta). Most surprisingly, one astacid H. gam- omes, 76 of them encode 13 protein-coding genes, two ri- marus lost a protein-coding gene (nad2), which is very rare in bosomal RNA genes and 22 tRNA genes typical to metazoans. mitochondrial genomes (Shen et al., 2013) (Table 1). However, there are variation in the number tRNA genes in ten

Table 1. Basic information of 86 malacostracan mitochondrial genomes Accession Length/ A+T/ Organism Protein rRNA tRNA Reference No. bp % Decapoda NC_012738 15 975 13 2 22 67.0 Peregrino-Uriarte et californiensis al. (2009) Fenneropenaeus NC_009679 16 004 13 2 22 68.9 Shen et al. (2007) chinensis NC_009626 15 990 13 2 22 67.7 Shen et al. (2007) vannamei Litopenaeus NC_012060 15 988 13 2 22 68.6 Peregrino-Uriarte et stylirostris al. (2009) NC_007010 15 968 13 2 22 66.5 Yamauchi et al. japonicus (2004) monodon NC_002184 15 984 13 2 22 70.6 Wilson et al. (2000) Sergestoidea chinensis NC_017600 15 740 13 2 23 70.6 Kim et al. (2012a) japonicus NC_004251 15 717 13 2 22 64.5 Yamauchi et al. (2002) Panulirus stimpsoni NC_014339 15 677 13 2 22 65.6 Liu and Cui (2011) NC_014854 16 105 13 2 22 66.7 Qian et al. (2011) NC_016015 15 665 13 2 22 67.1 unpublished NC_017868 15 700 13 2 22 66.7 Shen et al. (2013) latus NC_020022 15 663 13 2 22 67.6 Shen et al. (2013) Anomura Shinkaia crosnieri NC_011013 15 182 13 2 18 72.9 Yang et al. (2008) Neopetrolisthes NC_020024 15 324 13 2 22 71.3 Shen et al. (2013) maculatus Paralithodes NC_020029 16 720 13 2 22 73.9 Kim et al. (2013b) camtschaticus Astacidea similis NC_016925 16 220 13 2 22 71.7 Kim et al. (2012c) NC_016926 15 928 13 2 22 72.9 Kim et al. (2012c) Procambarus fallax NC_020021 15 253 13 2 22 72.4 Shen et al. (2013) Enoplometopus NC_020027 15 111 13 2 19 72.7 Shen et al. (2013) occidentalis Homarus americanus NC_015607 16 432 13 2 22 69.5 Kim et al. (2012b) NC_020020 14 316 12 2 19 68.6 Shen et al. (2013) destructor NC_011243 15 894 13 2 22 62.4 Miller et al. (2004) Brachyura Austinograea NC_020312 15 611 13 2 22 68.8 Yang et al. (2013) rodriguezensis Austinograea NC_020314 15 620 13 2 22 66.8 Yang et al. (2013) alayseae Gandalfus yunohana NC_013713 15 567 13 2 22 69.9 Yang et al. (2010) Eriocheir sinensis NC_006992 16 354 13 2 22 71.6 Sun et al. (2005) Eriocheir japonica NC_011597 16 352 13 2 22 71.6 Wang et al. (2014) Eriocheir hepuensis NC_011598 16 335 13 2 22 71.5 Wang et al. (2014) Xenograpsus NC_013480 15 798 13 2 22 73.9 Ki et al. (2009) testudinatus Ilyoplax deschampsi NC_020040 15 460 13 2 22 69.6 unpublished NC_006281 16 263 13 2 22 69.1 Place et al. (2005) Charybdis japonica NC_013246 15 738 13 2 22 69.2 Liu and Cui (2010a) Portunus NC_005037 16 026 13 2 22 70.2 Yamauchi et al. trituberculatus (2003) serrata NC_012565 15 775 13 2 22 72.5 Jondeung et al. (2012) to be continued SHEN Xin et al. Acta Oceanol. Sin., 2015, Vol. 34, No. 2, P. 84–92 87

Continued from Table 1 Scylla tranquebarica NC_012567 15 833 13 2 22 73.8 unpublished Scylla olivacea NC_012569 15 723 13 2 22 69.4 unpublished Scylla NC_012572 15 825 13 2 22 73.0 Ma et al. (2013) paramamosain Geothelphusa NC_007379 18 197 13 2 23 74.9 Segawa and Aotsuka dehaani (2005) Pseudocarcinus gigas NC_006891 15 515 13 2 22 70.5 Miller et al. (2005) Alpheus NC_014883 15 700 13 2 22 60.2 Qian et al. (2011) distinguendus Halocaridina rubra NC_008413 16 065 13 2 22 63.2 Ivey and Santos (2007) Alvinocaris chelys NC_018778 15 910 13 2 22 63.4 Yang et al. (2012) Alvinocaris NC_020313 16 050 13 2 22 62.2 Yang et al. (2013) longirostris Opaepele loihi NC_020311 15 905 13 2 22 65.7 Yang et al. (2013) Rimicaris kairei NC_020310 15 900 13 2 22 65.8 Yang et al. (2013) Exopalaemon NC_012566 15 730 13 2 22 63.6 Shen et al. (2009b) carinicauda Macrobrachium NC_006880 15 772 13 2 22 62.3 Miller et al. (2005) rosenbergii Macrobrachium NC_012217 15 694 13 2 22 67.1 unpublished lanchesteri Macrobrachium NC_015073 15 806 13 2 22 66.0 Ma et al. (2011) nipponense Polycheles typhlops NC_020026 16 221 13 2 22 67.5 Shen et al. (2013) Stenopodidea NC_018097 15 528 13 2 23 70.6 Shi et al. (2012) Axiidea Neaxius glyptocercus NC_019609 14 909 13 2 22 67.4 Lin et al. (2012) Corallianassa NC_020025 15 481 13 2 22 64.7 Shen et al. (2013) coutierei Nihonotrypaea NC_019610 15 240 13 2 22 69.6 Lin et al. (2012) thermophila Nihonotrypaea NC_020351 15 274 13 2 20 70.3 Kim et al. (2013a) japonica Austinogebia edulis NC_019606 15 761 13 2 22 73.6 Lin et al. (2012) Upogebia major NC_019607 16 143 13 2 22 70.7 Lin et al. (2012) Upogebia pusilla NC_020023 15 680 13 2 22 70.8 Shen et al. (2013) kelanang NC_019608 15 528 13 2 22 66.3 Lin et al. (2012) Euphausiacea Euphausiidae superba1) EU583500 15 498 13 2 23 68.1 Shen et al. (2010) Euphausia pacifica NC_016184 16 898 13 2 22 72.0 Shen et al. (2011) Stomatopoda Gonodactylidae Gonodactylus NC_007442 16 279 13 2 22 67.5 unpublished chiragra Lysiosquillidae Lysiosquillina NC_007443 16 325 13 2 22 63.8 unpublished maculata Harpiosquilla NC_006916 15 714 13 2 22 69.7 Miller and Austin harpax (2006) NC_014342 15 783 13 2 22 70.8 Liu and Cui (2010b) NC_006081 15 994 13 2 22 70.2 Cook (2005) Squilla empusa NC_007444 15 828 13 2 22 68.4 unpublished Amphipoda Caprellida Caprella mutica NC_014492 15 427 13 2 22 68.0 Kilpert and Podsiad- lowski (2010b) Caprella scaura NC_014687 15 079 13 2 22 66.4 Ito et al. (2010) Eusiroidea Gondogeneia NC_016192 18 424 13 2 22 70.1 Shin et al. (2012) antarctica Gammaroidea Pseudoniphargus NC_019662 15 155 13 2 22 68.7 Bauza-Ribot et al. daviui (2012) Gammarus duebeni NC_017760 15 651 13 2 22 64.0 Krebes and Bastrop (2012) Hadzioidea Metacrangonyx NC_013032 14 113 13 2 21 76.0 Bauza-Ribot et al. longipes (2009) Metacrangonyx NC_019653 14 355 13 2 22 76.9 Bauza-Ribot et al. repens (2012) Metacrangonyx NC_019654 14 543 13 2 22 73.6 Bauza-Ribot et al. dominicanus (2012) Metacrangonyx NC_019655 14 507 13 2 22 69.7 Bauza-Ribot et al. goulmimensis (2012) to be continued 88 SHEN Xin et al. Acta Oceanol. Sin., 2015, Vol. 34, No. 2, P. 84–92

Continued from Table 1 Metacrangonyx NC_019656 14 770 13 2 22 74.6 Bauza-Ribot et al. ilvanus (2012) Metacrangonyx NC_019657 15 037 13 2 22 74.8 Bauza-Ribot et al. spinicaudatus (2012) Metacrangonyx NC_019658 14 711 13 2 22 75.8 Bauza-Ribot et al. longicaudus (2012) Metacrangonyx NC_019659 14 478 13 2 22 76.2 Bauza-Ribot et al. panousei (2012) Metacrangonyx NC_019660 14 787 13 2 22 70.8 Bauza-Ribot et al. remyi (2012) Lysianassoidea Onisimus nanseni NC_013819 14 734 13 2 22 70.3 Ki et al. (2010) Melitoidea Bahadzia jaraguensis NC_019661 14 657 13 2 22 69.7 Bauza-Ribot et al. (2012) Isopoda Diplocheta Ligia oceanica NC_008412 15 289 13 2 21 60.8 Kilpert and Podsiadlowski (2006) Phreatoicidae Eophreatoicus sp.14 NC_013976 14 994 13 2 22 69.6 Kilpert and Podsiad- FK-2009 lowski (2010a) Note: 1) incomplete.

3.2 Gene arrangement srRNA genes. X. testudinatus (Decapoda: Brachyura) exhibits Molecular and morphological evidences show that hexapods translocations of nad6 and cob genes. P. typhlops (Decapoda: and crustaceans form a clade, which is referred to as Pancrusta- Polychelida) has rearrangements of nad5 and cob genes. N. glypt- cea (Regier et al., 2005; von Reumont et al., 2012). The two groups ocercus, C. coutierei, N. thermophila and N. japonica (Decapoda: share the same primitive pattern in mitochondrial gene arrange- Axiidea) share translocation of nad3/cox3 gene. C. mutica and C. ment (i.e., the pancrustacean ground pattern) (Boore et al., 1998; scaura (Amphipoda: Caprellidea) share translocations of nad4 Shen et al., 2007). Among the 86 malacostracans mitochondrial and nad4L genes, and they also have translocation and inversion genomes, 54 species have identical major gene arrangement to of nad5 gene. P. daviui (Amphipoda: ) has translo- the pancrustacean ground pattern, including all six species from cation of nad1 gene. M. longipes, M. repens, M. dominicanus, M. Stomatopoda: G. chiragra, L. maculata, H. harpax, O. oratoria, S. goulmimensis, M. ilvanus, M. spinicaudatus, M. longicaudus, M. mantis and S. empusa, three species from Amphipoda: G. antarc- panousei and M. remyi (Amphipoda: Gammaridea) share trans- tica, G. duebeni and B. jaraguensis, both krill: E. superba and E. location and inversion of cob gene. O. nanseni (Amphipoda: pacifica, all seven species from Dendrobranchiata (Decapoda): F. Gammaridea) has translocations of nad6 and cob genes. L. californiensis, F. chinensis, L. vannamei, L. stylirostris, M. ja- oceanica (Isopoda: Oniscidea) have translocations of nad1, sr- ponicus, P. monodon and A. chinensis, and 36 species from Pleo- RNA, cob, nad5 and lrRNA genes. E. sp.14 FK-2009 (Isopoda: cyemata (Decapoda): P. japonicus, P. stimpsoni, P. ornatus, P. ho- ) encounters large scale gene rearrangements. marus, P. versicolor, S. latus, E. occidentalis, H. americanus, A. rodriguezensis, A. alayseae, G. yunohana, I. deschampsi, C. sap- 3.3 Phylomitogenomic analyses idus, C. japonica, P. trituberculatus, S. serrata, S. tranquebarica, Phylogenetic analysis based on Bayesian inference of nucle- S. olivacea, S. paramamosain, G. dehaani, P. gigas, A. distinguen- otide sequences of the protein-coding gene produce a robust tree dus, H. rubra, A. chelys, A. longirostris, O. loihi, R. kairei, E. carini- with almost all nodes having 100% posterior probability (Fig. 3). cauda, M. rosenbergii, M. lanchesteri, M. nipponense, S. hispidus, And gene arrangement information was also indicated in the A. edulis, U. major, U. pusilla and T. kelanang (Fig. 2). However, evolutionary tree. The Isopoda and the Amphipoda are two of the the other 32 mitochondrial genomes encountered major gene re- largest pericarid groups. The position of the Isopoda and the Am- arrangements, including both species from Isopoda: L. oceanica phipoda within Malacostraca is debated. The phylogenetic tree and E. sp.14 FK-2009, 13 species from Amphipoda: C. mutica, C. shows that Amphipoda and Isopoda cluster together (Edrioph- scaura, P. daviui, M. longipes, M. repens, M. dominicanus, M. thalma) with strong support (BPP=100). There have been many goulmimensis, M. ilvanus, M. spinicaudatus, M. longicaudus, M. hypotheses on the phylogenetic position of the krill (Sars, 1883; panousei, M. remyi and O. nanseni, and 17 species from Pleo- Calman, 1904; Richter and Scholtz, 2001; Casanova, 2003). The cyemata (Decapoda): S. crosnieri, N. maculatus, P. camtschaticus, phylogenetic tree shows that Euphausiacea is nested with Deca- C. similis, P. clarkii, P. fallax, H. gammarus, C. destructor, E. sin- poda, and closely related to Dendrobranchiata (BPP=100; with ensis, E. japonica, E. hepuensis, X. testudinatus, P. typhlops, N. six from Penaeoidea and one northern mauxia shrimp glyptocercus, C. coutierei, N. thermophila and N. japonica. from Sergestoidea included in the analysis). And all the nine spe- S. crosnieri (Decapoda: Anomura) has translocations of nad2 cies from the two groups (Euphausiacea and Dendrobranchiata) and nad1- lrRNA- srRNA (genes encoded on the negative strand share identical major gene arrangement. In conclusion, phylo- are underlined, same below) (Fig. 2). N. maculatus and P. mitogenomic analyses, which combine phylogenetic tree con- camtschaticus (Decapoda: Anomura) share translocations of struction and gene arrangement information, strong support the nad3 and nad2. Four members of Astacidea (Decapoda), C. simil- close relationship between Euphausiacea and Dendrobranchi- is, P. clarkii, P. fallax and H. gammarus, share inversions of one ata, making Decapoda paraphyletic. This result is also consistent gene block: srRNA- lrRNA- nad1- cob- nad6- nad4L- nad4- nad5. with the findings from developmental biology, that krill is In addition, H. gammarus loses the nad2 gene as compared to grouped with the of prawns () in the Decapoda the typical gene content of metazoan mitochondrial genomes. based on developmental similarities (Gurney, 1942; Gordon, The three mitten crabs E. sinensis, E. japonica and E. hepuensis 1955). (Decapoda: Brachyura) share translocations of nad1, lrRNA and SHEN Xin et al. Acta Oceanol. Sin., 2015, Vol. 34, No. 2, P. 84–92 89

Fig. 2. Major genes arrangements (tRNAs excluded) of 86 malacostracan mitochondrial genomes. The underlined genes encoded on the negative strand and the shaded region indicates conserved gene block. Green and yellow colors indicate gene blocks without or with inversion, respectively as compared to the pancrustacean ground pattern. 90 SHEN Xin et al. Acta Oceanol. Sin., 2015, Vol. 34, No. 2, P. 84–92

Fig. 3. Phylomitogenomic tree based on 13 protein-coding genes (nucleotide sequence) of 86 malacostracan mitochondrial genomes. Black branches indicate the taxa whose mitochondrial gene arrangements are identical to the pancrustacean ground pattern (tRNAs excluded) and blue ones indicate the taxa whose mitochondrial genes encountered rearrangement.

Within Pleocyemata, monophyly of five infraorders (Achelata, Phylomitogenomic analyses show that major gene arrange- Caridea, Brachyura, Axiidea and Anomura) is affirmed, but ment characters are conserved within Achelata, Caridea and monophyly of Gebiidea and Astacidea is questionable. In addi- Anomura. However, current mitochondrial genomic data indic- tion, Stenopus hispidus from Stenopodidea does not group with ate that gene arrangement is not conserved within Brachyura. the other members of Pleocyemata, but instead is the basal group The three species of Eriocheir (E. sinensis, E. japonica and E. among all members from Decapoda, thus making Pleocyemata hepuensis) from Brachyura share translocations of nad1, lrRNA paraphyletic. Other than, monophyly of the other four orders and srRNA genes. Meanwhile, X. testudinatus (Brachyura) has with mitochondrial genomes available is supported. translocations of nad6 and cob genes. As more mitochondrial SHEN Xin et al. Acta Oceanol. Sin., 2015, Vol. 34, No. 2, P. 84–92 91

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