phylomitogenomics of malacostraca (arthropoda: crustacea)

Phylomitogenomics of Malacostraca (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, China

2 Beijing Institutes of Life Science, Chinese Academy of Sciences, Beijing 100101, China3 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 themitochondrial genomes, the number of metazoan mitochondrial genomes reported has a tremendous growth inthe past decades. Phylomitogenomics—reconstruction of phylogenetic relationships based on mitochondrialgenomic data—is now possible across large animal groups. Crustaceans in the class Malacostraca display a highdiversity of body forms and include large number of ecologically and commercially important species. In thisstudy, comprehensive and systematic analyses of the phylogenetic relationships within Malacostraca wereconducted based on 86 mitochondrial genomes available from GenBank. Among 86 malacostracan mitochondrialgenomes, 54 species have identical major gene arrangement (excluding tRNAs) to pancrustacean ground pattern,including six species from Stomatopoda, three species from Amphipoda, two krill, seven species fromDendrobranchiata (Decapoda), and 36 species from Pleocyemata (Decapoda). However, the other 32mitochondrial genomes reported exhibit major gene rearrangements. Phylogenies based on Bayesian analyses ofnucleotide sequences of the protein-coding genes produced a robust tree with 100% posterior probability atalmost all nodes. The results indicate that Amphipoda and Isopoda cluster together (Edriophthalma) (BPP=100).Phylomitogenomic analyses strong support that Euphausiacea is nested within Decapoda, and closely related toDendrobranchiata, which is also consistent with the evidence from developmental biology. Yet the taxonomicsampling of mitochondrial genome from Malacostraca is very biased to the order Decapoda, with no completemitochondrial genomes reported from 11 of the 16 orders. Future researches on sequencing the mitochondrialgenomes from a wide variety of malacostracans are necessary to further elucidate the phylogeny of this importantgroup of animals. With the increase in mitochondrial genomes available, phylomitogenomics will emerge as animportant 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). ActaOceanologica Sinica, 34(2): 84–92, doi: 10.1007/s13131-015-0583-1

1 IntroductionComplete mitochondrial genomes of human (Homo sapiens)

and mouse (Mus musculus) were sequenced in 1981 (Anderson etal., 1981; Bibb et al., 1981), which are the first ones available inMetazoa. The number of metazoan mitochondrial genomes re-ported reaches 127 by the end of the year 2000. However, from2001 to the present, along with the sequencing technology devel-opment and the continued enthusiasm of researchers on mito-chondrial genomes, the number of metazoan mitochondrial gen-omes reported increases tremendously. The metazoan mito-chondrial genomes available from GenBank have reached 3 653by the end of 2013 (Fig. 1). Phylomitogenomics, the use of mito-chondrial genomic data in resolving phylogenetic relationships,has emerged to be an important approach in phylogenetic recon-struction.

When mitochondrial genomes of one or several new specieswere obtained, the researchers often compare them with those of

close related species so that there is a lack of large-scale andcomparison in many major animal groups. As the genome data-bases now contain thousands of animal mitochondrial genomes,it allows comprehensive analysis and evaluation of existing datain a major group based on a large number of taxa. To assess andanalyze the existing mitochondrial genomic information, whichnot only help to reconstruct animal phylogeny based on mito-chondrial genomes, but also help to pinpoint the gaps in the cur-rent mitochondrial genomic data, and thus provide guidance forfuture researches. As a case study, this study examines the situ-ation in malacostracans from the viewpoint of phylomitogenom-ics.

The class Malacostraca is the largest of the six classes of crus-taceans, containing about 25 000 extant species, and is dividedinto 16 orders. Malacostracans display a high diversity of bodyforms, and include shrimp, crabs, krill, lobsters, woodlice, mantisshrimp and many other species (Martin and Davis, 2001).

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]

Foundation item: The National Natural Science Foundation of China under contract Nos 41476146 and 40906067; Hong Kong ScholarsProgram under contract No. XJ2012056; China Postdoctoral Science Foundation under contract Nos 2012M510054 and 2012T50218; a projectfunded by the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD).*Corresponding author, E-mail: [email protected]

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

Malacostracans not only contain a wide variety of taxa, but alsoinclude many species with high ecological and economic values.In the past hundreds of years, there have been many studies fo-cused on its systematic and evolutionary relationships. Literat-ures exploring the malacostracan relationships based on mor-phological and molecular data are numerous. Evolutionary rela-tionships among the various groups of Malacostraca was for a

long time a hotly debated issue (Richter and Scholtz, 2001; vonReumont et al., 2012). In this paper, comprehensive analyses ofthe phylogenetic relationships within Malacostraca were con-ducted based on 86 mitochondrial genomes available. In addi-tion, the knowledge gaps of the current mitochondrial genomicdata are also noted to guide future researches.

2 Materials and methods

2.1 Data acquisitionA total of 3 653 metazoan mitochondrial genomes were

downloaded (ftp://ftp.ncbi.nlm.nih.gov/genomes/). Then 86malacostracan mitochondrial genomes were obtained by self-written PERL script. The taxa are shown in Table 1, including rep-resentatives from five orders, with 60 species from Decapoda(Wilson et al., 2000; Yamauchi et al., 2002; Yamauchi et al., 2003;Miller et al., 2004; Yamauchi et al., 2004; Miller et al., 2005; Placeet al., 2005; Segawa and Aotsuka, 2005; Sun et al., 2005; Ivey andSantos, 2007; Shen et al., 2007; Yang et al., 2008; Ki et al., 2009;Peregrino-Uriarte et al., 2009; Shen et al., 2009; Liu and Cui,2010a; Yang et al., 2010; Ma et al., 2011; Qian et al., 2011;Jondeung et al., 2012; Kim et al., 2012a; Kim et al., 2011; Kim etal., 2012b; Lin et al., 2012; Liu and Cui, 2011; Shi et al., 2012; Yanget al., 2012; Kim et al., 2013a; Kim et al., 2013b; Ma et al., 2013;Shen et al., 2013; Yang et al., 2013; Wang et al., 2014), two fromEuphausiacea (Shen et al., 2010; Shen et al., 2011), six from Sto-matopoda (Cook, 2005; Miller and Austin, 2006; Liu and Cui,2010b), sixteen from Amphipoda (Bauza-Ribot et al., 2009; Ito etal., 2010; Ki et al., 2010; Kilpert and Podsiadlowski, 2010b; Bauza-Ribot et al., 2012; Krebes and Bastrop, 2012; Shin et al., 2012), andtwo from Isopoda (Kilpert and Podsiadlowski, 2006; Kilpert andPodsiadlowski, 2010a).

2.2 Comparison of major gene arrangementsDue to the high frequency of translocations and inversions of

the transfer RNA (tRNA) genes in animal mitochondrial gen-omes, major coding gene (protein-coding genes and ribosomalRNA genes) arrangement may provide more reliable informationthan tRNA genes when we focus on the comparison of higherlevel taxa. In this paper, the major gene arrangement of the 86malacostracan mitochondrial genomes were analyzed and com-pared systematically.

2.3 Phylomitogenomic analysisNucleotide sequences of each of the 13 protein-coding genes

(atp6, atp8, cob, cox1-3, nad1-4, nad4L, nad5 and nad6) wereseparately aligned using Clustal X 1.83 (Thompson et al., 1997)(default parameters) and then concatenated as a single dataset of11 584 base pairs (bp) for analysis. Model selection for the nucle-otide acid dataset was done with jModelTest (Darriba et al., 2012)and the best model was GTR matrix and the Gamma+Invar mod-el. Phylogenetic analysis was performed using MrBayes 3.1 (Ron-quist and Huelsenbeck, 2003). Four Markov chains of 1 000 000generations were run with sampling every 1 000 generations. Thefirst quarter (250 000 generations) was excluded from the analys-is as “burn-in”. After omitting the first 250 “burn in” trees, the re-maining 750 sampled trees were used to estimate the consensustree and the Bayesian posterior probability (BPP).

Gene rearrangement information was indicated in the phylo-genetic tree constructed using the protein-coding gene se-quences. Thus information from mitochondrial genomes as awhole (including sequence information and gene arrangement)were used for exploring the phylogenetic relationships of the tar-get groups, which is basic requirement of phylomitogenomicanalyses.

3 Results and discussion

3.1 Characteristics of malacostracan mitochondrial genomesThe length of decapod mitochondrial genomes ranges from

14 316 bp (H. gammarus) to 18 197 bp (G. dehaani) (Table 1). Thetwo krill mitochondrial genomes are 15 498 bp and 16 898 bp inlength for E. superba (incomplete) and E. pacifica, respectively.The length of mantis shrimp mitochondrial genomes ranges from15 714 bp (H. harpax) to 16 325 bp (L. maculata). In Amphipoda,the length of mitochondrial genomes varies between 14 113 bp(M. longipes) and 18 424 bp (G. antarctica). The length of two iso-pod mitochondrial genomes is 15 289 bp (L. oceanica) and 14 994bp (E. sp.14 FK-2009), respectively.

In Decapoda, the A + T contents of the mitochondrial heavychain are between 60.2% (A. distinguendus) and 74.9% (G. de-haani) (Table 1). The values for two krill mitochondrial genomesare 68.1% and 72.0% for E. superba and E. pacifica, respectively.

SHEN Xin et al. Acta Oceanol. Sin., 2015, Vol. 34, No. 2, P. 84–92 85

And the values for mantis shrimps are between 63.8% (L. macu-lata) and 70.8% (O. oratoria). As for Amphipoda, the A + T con-tents of mitochondrial genomes are between 64.0% (G. duebeni)and 76.9% (M. repens). And values for the two isopods are 60.8%(L. oceanica) and 69.6% (E. sp.14 FK-2009).

The gene content of malacostracan mitochondrial genomes isconserved. Among the 86 malacostracan mitochondrial gen-omes, 76 of them encode 13 protein-coding genes, two ri-bosomal RNA genes and 22 tRNA genes typical to metazoans.However, there are variation in the number tRNA genes in ten

species, including A. chinensis (Decapoda: Sergestoidea), S. cros-nieri (Decapoda: Anomura), E. occidentalis (Decapoda: As-tacidea), H. gammarus (Decapoda: Astacidea), G. dehaani (Deca-poda: Brachyura), S. hispidus (Decapoda: Stenopodidea), N. ja-ponica (Decapoda: Axiidea), E. superba (Euphausiacea: Eu-phausiidae), M. longipes (Amphipoda: Hadzioidea) and L. ocean-ica (Isopoda: Diplocheta). Most surprisingly, one astacid H. gam-marus lost a protein-coding gene (nad2), which is very rare incrustacean mitochondrial genomes (Shen et al., 2013) (Table 1).

Table 1. Basic information of 86 malacostracan mitochondrial genomes

Taxonomy OrganismAccession

No.Length/

bpProtein rRNA tRNA

A+T/%

Reference

Decapoda Penaeoidea Farfantepenaeuscaliforniensis

NC_012738 15 975 13 2 22 67.0 Peregrino-Uriarte etal. (2009)

Fenneropenaeuschinensis

NC_009679 16 004 13 2 22 68.9 Shen et al. (2007)

Litopenaeusvannamei

NC_009626 15 990 13 2 22 67.7 Shen et al. (2007)

Litopenaeusstylirostris

NC_012060 15 988 13 2 22 68.6 Peregrino-Uriarte etal. (2009)

Marsupenaeusjaponicus

NC_007010 15 968 13 2 22 66.5 Yamauchi et al.(2004)

Penaeus monodon NC_002184 15 984 13 2 22 70.6 Wilson et al. (2000)

Sergestoidea Acetes chinensis NC_017600 15 740 13 2 23 70.6 Kim et al. (2012a)

Achelata Panulirus 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)

Panulirus ornatus NC_014854 16 105 13 2 22 66.7 Qian et al. (2011)

Panulirus homarus NC_016015 15 665 13 2 22 67.1 unpublished

Panulirus versicolor NC_017868 15 700 13 2 22 66.7 Shen et al. (2013)

Scyllarides 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)

Neopetrolisthesmaculatus

NC_020024 15 324 13 2 22 71.3 Shen et al. (2013)

Paralithodescamtschaticus

NC_020029 16 720 13 2 22 73.9 Kim et al. (2013b)

Astacidea Cambaroides similis NC_016925 16 220 13 2 22 71.7 Kim et al. (2012c)

Procambarus clarkii 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)

Enoplometopusoccidentalis

NC_020027 15 111 13 2 19 72.7 Shen et al. (2013)

Homarus americanus NC_015607 16 432 13 2 22 69.5 Kim et al. (2012b)

Homarus gammarus NC_020020 14 316 12 2 19 68.6 Shen et al. (2013)

Cherax destructor NC_011243 15 894 13 2 22 62.4 Miller et al. (2004)

Brachyura Austinograearodriguezensis

NC_020312 15 611 13 2 22 68.8 Yang et al. (2013)

Austinograeaalayseae

NC_020314 15 620 13 2 22 66.8 Yang et al. (2013)

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)

Xenograpsustestudinatus

NC_013480 15 798 13 2 22 73.9 Ki et al. (2009)

Ilyoplax deschampsi NC_020040 15 460 13 2 22 69.6 unpublished

Callinectes sapidus 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)

Portunustrituberculatus

NC_005037 16 026 13 2 22 70.2 Yamauchi et al.(2003)

Scylla serrata NC_012565 15 775 13 2 22 72.5 Jondeung et al.(2012)

to be continued

86 SHEN Xin et al. Acta Oceanol. Sin., 2015, Vol. 34, No. 2, P. 84–92

Continued from Table 1Scylla tranquebarica NC_012567 15 833 13 2 22 73.8 unpublished

Scylla olivacea NC_012569 15 723 13 2 22 69.4 unpublished

Scyllaparamamosain

NC_012572 15 825 13 2 22 73.0 Ma et al. (2013)

Geothelphusadehaani

NC_007379 18 197 13 2 23 74.9 Segawa and Aotsuka(2005)

Pseudocarcinus gigas NC_006891 15 515 13 2 22 70.5 Miller et al. (2005)

Caridea Alpheusdistinguendus

NC_014883 15 700 13 2 22 60.2 Qian et al. (2011)

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)

Alvinocarislongirostris

NC_020313 16 050 13 2 22 62.2 Yang et al. (2013)

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)

Exopalaemoncarinicauda

NC_012566 15 730 13 2 22 63.6 Shen et al. (2009b)

Macrobrachiumrosenbergii

NC_006880 15 772 13 2 22 62.3 Miller et al. (2005)

Macrobrachiumlanchesteri

NC_012217 15 694 13 2 22 67.1 unpublished

Macrobrachiumnipponense

NC_015073 15 806 13 2 22 66.0 Ma et al. (2011)

Polychelida Polycheles typhlops NC_020026 16 221 13 2 22 67.5 Shen et al. (2013)

Stenopodidea Stenopus hispidus 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)

Corallianassacoutierei

NC_020025 15 481 13 2 22 64.7 Shen et al. (2013)

Nihonotrypaeathermophila

NC_019610 15 240 13 2 22 69.6 Lin et al. (2012)

Nihonotrypaeajaponica

NC_020351 15 274 13 2 20 70.3 Kim et al. (2013a)

Gebiidea 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)

Thalassina kelanang NC_019608 15 528 13 2 22 66.3 Lin et al. (2012)

Euphausiacea Euphausiidae Euphausia 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 Gonodactyluschiragra

NC_007442 16 279 13 2 22 67.5 unpublished

Lysiosquillidae Lysiosquillinamaculata

NC_007443 16 325 13 2 22 63.8 unpublished

Squillidae Harpiosquillaharpax

NC_006916 15 714 13 2 22 69.7 Miller and Austin(2006)

Oratosquilla oratoria NC_014342 15 783 13 2 22 70.8 Liu and Cui (2010b)

Squilla mantis 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 Gondogeneiaantarctica

NC_016192 18 424 13 2 22 70.1 Shin et al. (2012)

Gammaroidea Pseudoniphargusdaviui

NC_019662 15 155 13 2 22 68.7 Bauza-Ribot et al.(2012)

Gammarus duebeni NC_017760 15 651 13 2 22 64.0 Krebes and Bastrop(2012)

Hadzioidea Metacrangonyxlongipes


Metacrangonyxrepens


Metacrangonyxdominicanus


Metacrangonyxgoulmimensis


to be continued


Continued from Table 1Metacrangonyxilvanus


Metacrangonyxspinicaudatus


Metacrangonyxlongicaudus


Metacrangonyxpanousei


Metacrangonyxremyi


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 andPodsiadlowski (2006)

Phreatoicidae Eophreatoicus sp.14FK-2009

NC_013976 14 994 13 2 22 69.6 Kilpert and Podsiad-lowski (2010a)

Note: 1) incomplete.

3.2 Gene arrangementMolecular and morphological evidences show that hexapods

and crustaceans form a clade, which is referred to as Pancrusta-cea (Regier et al., 2005; von Reumont et al., 2012). The two groupsshare the same primitive pattern in mitochondrial gene arrange-ment (i.e., the pancrustacean ground pattern) (Boore et al., 1998;Shen et al., 2007). Among the 86 malacostracans mitochondrialgenomes, 54 species have identical major gene arrangement tothe pancrustacean ground pattern, including all six species fromStomatopoda: G. chiragra, L. maculata, H. harpax, O. oratoria, S.mantis and S. empusa, three species from Amphipoda: G. antarc-tica, G. duebeni and B. jaraguensis, both krill: E. superba and E.pacifica, all seven species from Dendrobranchiata (Decapoda): F.californiensis, F. chinensis, L. vannamei, L. stylirostris, M. ja-ponicus, P. monodon and A. chinensis, and 36 species from Pleo-cyemata (Decapoda): P. japonicus, P. stimpsoni, P. ornatus, P. ho-marus, P. versicolor, S. latus, E. occidentalis, H. americanus, A.rodriguezensis, A. alayseae, G. yunohana, I. deschampsi, C. sap-idus, C. japonica, P. trituberculatus, S. serrata, S. tranquebarica,S. olivacea, S. paramamosain, G. dehaani, P. gigas, A. distinguen-dus, H. rubra, A. chelys, A. longirostris, O. loihi, R. kairei, E. carini-cauda, M. rosenbergii, M. lanchesteri, M. nipponense, S. hispidus,A. edulis, U. major, U. pusilla and T. kelanang (Fig. 2). However,the other 32 mitochondrial genomes encountered major gene re-arrangements, including both species from Isopoda: L. oceanicaand E. sp.14 FK-2009, 13 species from Amphipoda: C. mutica, C.scaura, P. daviui, M. longipes, M. repens, M. dominicanus, M.goulmimensis, M. ilvanus, M. spinicaudatus, M. longicaudus, M.panousei, M. remyi and O. nanseni, and 17 species from Pleo-cyemata (Decapoda): S. crosnieri, N. maculatus, P. camtschaticus,C. similis, P. clarkii, P. fallax, H. gammarus, C. destructor, E. sin-ensis, E. japonica, E. hepuensis, X. testudinatus, P. typhlops, N.glyptocercus, C. coutierei, N. thermophila and N. japonica.

S. crosnieri (Decapoda: Anomura) has translocations of nad2and nad1- lrRNA- srRNA (genes encoded on the negative strandare underlined, same below) (Fig. 2). N. maculatus and P.camtschaticus (Decapoda: Anomura) share translocations ofnad3 and nad2. Four members of Astacidea (Decapoda), C. simil-is, P. clarkii, P. fallax and H. gammarus, share inversions of onegene block: srRNA- lrRNA- nad1- cob- nad6- nad4L- nad4- nad5.In addition, H. gammarus loses the nad2 gene as compared tothe typical gene content of metazoan mitochondrial genomes.The three mitten crabs E. sinensis, E. japonica and E. hepuensis(Decapoda: Brachyura) share translocations of nad1, lrRNA and

srRNA genes. X. testudinatus (Decapoda: Brachyura) exhibitstranslocations of nad6 and cob genes. P. typhlops (Decapoda:Polychelida) has rearrangements of nad5 and cob genes. N. glypt-ocercus, C. coutierei, N. thermophila and N. japonica (Decapoda:Axiidea) share translocation of nad3/cox3 gene. C. mutica and C.scaura (Amphipoda: Caprellidea) share translocations of nad4and nad4L genes, and they also have translocation and inversionof nad5 gene. P. daviui (Amphipoda: Gammaridea) has translo-cation of nad1 gene. M. longipes, M. repens, M. dominicanus, M.goulmimensis, M. ilvanus, M. spinicaudatus, M. longicaudus, M.panousei and M. remyi (Amphipoda: Gammaridea) share trans-location and inversion of cob gene. O. nanseni (Amphipoda:Gammaridea) has translocations of nad6 and cob genes. L.oceanica (Isopoda: Oniscidea) have translocations of nad1, sr-RNA, cob, nad5 and lrRNA genes. E. sp.14 FK-2009 (Isopoda:Phreatoicidea) encounters large scale gene rearrangements.

3.3 Phylomitogenomic analysesPhylogenetic analysis based on Bayesian inference of nucle-

otide sequences of the protein-coding gene produce a robust treewith almost all nodes having 100% posterior probability (Fig. 3).And gene arrangement information was also indicated in theevolutionary tree. The Isopoda and the Amphipoda are two of thelargest pericarid groups. The position of the Isopoda and the Am-phipoda within Malacostraca is debated. The phylogenetic treeshows that Amphipoda and Isopoda cluster together (Edrioph-thalma) with strong support (BPP=100). There have been manyhypotheses on the phylogenetic position of the krill (Sars, 1883;Calman, 1904; Richter and Scholtz, 2001; Casanova, 2003). Thephylogenetic tree shows that Euphausiacea is nested with Deca-poda, and closely related to Dendrobranchiata (BPP=100; withsix prawns from Penaeoidea and one northern mauxia shrimpfrom Sergestoidea included in the analysis). And all the nine spe-cies from the two groups (Euphausiacea and Dendrobranchiata)share identical major gene arrangement. In conclusion, phylo-mitogenomic analyses, which combine phylogenetic tree con-struction and gene arrangement information, strong support theclose relationship between Euphausiacea and Dendrobranchi-ata, making Decapoda paraphyletic. This result is also consistentwith the findings from developmental biology, that krill isgrouped with the family of prawns (Penaeidae) in the Decapodabased on developmental similarities (Gurney, 1942; Gordon,1955).


Fig. 2. Major genes arrangements (tRNAs excluded) of 86 malacostracan mitochondrial genomes. The underlined genes encodedon the negative strand and the shaded region indicates conserved gene block. Green and yellow colors indicate gene blocks withoutor with inversion, respectively as compared to the pancrustacean ground pattern.


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

Within Pleocyemata, monophyly of five infraorders (Achelata,

Caridea, Brachyura, Axiidea and Anomura) is affirmed, butmonophyly of Gebiidea and Astacidea is questionable. In addi-tion, Stenopus hispidus from Stenopodidea does not group withthe other members of Pleocyemata, but instead is the basal groupamong all members from Decapoda, thus making Pleocyemataparaphyletic. Other than, monophyly of the other four orderswith mitochondrial genomes available is supported.

Phylomitogenomic analyses show that major gene arrange-ment characters are conserved within Achelata, Caridea andAnomura. However, current mitochondrial genomic data indic-ate that gene arrangement is not conserved within Brachyura.The three species of Eriocheir (E. sinensis, E. japonica and E.hepuensis) from Brachyura share translocations of nad1, lrRNAand srRNA genes. Meanwhile, X. testudinatus (Brachyura) hastranslocations of nad6 and cob genes. As more mitochondrial


data from different groups of Malacostraca become available,variations in gene arrangements could be used to infer phylogen-etic relationships within this group. Furthermore, the differentevolutionary rates that are involved in mitochondrial gene re-arrangements among close related taxa are worthy of furtherstudies.

4 Future prospectsThere are more than three thousand animal mitochondrial

genomes released so far. However, the taxonomic sampling isvery biased, with no mitochondrial genome from many taxa. Inthe class Malacostraca, the taxonomic sampling is very biased tothe order Decopoda (accounted for about 70% of sequencedmalacostracan mitochondrial genomes), with no complete mito-chondrial genomes reported from 11 of the 16 orders. Future re-searches should get focus on more members in the classMalacostraca, especially from those orders without mitochondri-al genomic data, such as Nebaliacea, Cumacea, Tanaidacea andAnaspidacea. With the development of sequencing technology,dozens mitochondrial genomic DNA of different samples couldbe simultaneously sequenced with next-generation sequencingplatform (Jex et al., 2010; Maricic et al., 2010; Gillett et al., 2014).Thus, more mitochondrial genome data should lead to a compre-hensive understanding of the phylogenetic relationships withinMalacostraca, and between malacostracans and the other crusta-ceans. It is believed that a robust tree of life will be built based onmitochondrial genomes, in combination with nuclear genes.With the increase in mitochondrial genomes available, phylo-mitogenomics will emerge as an important component in theTree of Life researches.

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phylomitogenomics of malacostraca (arthropoda: crustacea)

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