Phylogenetic Relationships of Superfamily Gammaroidea (Amphipoda) and Its Allies from Japan
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CRUSTACEAN RESEARCH, NO. 39: 1 - 10, 2010 Phylogenetic relationships of superfamily Gammaroidea (Amphipoda) and its allies from Japan Ko Tomikawa, Norio Kobayashi and Shunsuke F. Mawatari Abstract.– The current superfamilial Bulycheva (1957) was the first to classification of suborder Gammaridea, at attempt to group families of Gammaridea least of the Japanese members, requires by superfamily, establishing the superfamily a full reassessment of their phylogenetic Talitroidea. This was followed by Barnard relationships. We investigated 17 (1972, 1973), who filled out Talitroidea and species representing six families in three began using Corophioidea to encompass superfamilies from Japan, based on several families. Bousfield (1977, 1983) partial sequences of the mitochondrial subsequently rearranged all families into 19 16S rRNA and nuclear 28S rRNA genes. superfamilies, and later (Bousfield, 2001) Members of superfamily Gammaroidea modified his classification system, including are characterized by having gammarid- at least 90 families and additional unnamed type calceolus on their antennae, but groups in 21 superfamilies, but he did not our molecular analyses did not support give substantial reasons for the modification. the monophyly of Gammaroidea. The Superfamily Gammaroidea was erected unique gammarid-type calceolus found in by Bousfield (1977), prior to which species Gammaroidea may not be a synapomorphy of Gammaroidea and allied taxa had usually for this group. Monophyly of the families been recognized as members of the extremely studied, except for Melitidae, was large family Gammaridae; for example, supported by neighbor-joining, maximum Stebbing (1906) and Schellenberg (1942) parsimony, and maximum likelihood included crangonyctid, gammarid, and melitid analyses. The molecular analyses revealed taxa in Gammaridae. Although these taxa that during their evolutionary history, appeared not to be closely related to each gammaroidean amphipods repeatedly other, this familial arrangement persisted for switched between marine and freshwater a long time. Bousfield (1977) split the old habitats. Gammaridae into 25 families arranged in six superfamilies, including 18 new families and five new superfamilies. Unfortunately, none Introduction of Bousfield’s diagnoses of superfamilies Gammaridean amphipods are one of was fully discrete (Barnard & Barnard, 1983; the most diverse groups of crustaceans, Williams & Barnard, 1988); the status of with more than 7,000 species in about 130 Gammaroidea is especially controversial, families described (Barnard & Karaman, because this group comprises morphologically 1991; Bousfield & Shih, 1994). Gammaridea diverse species and has few clear diagnostic comprises species inhabiting marine, brackish, features. or freshwater habitats, and some species have Many authors have studied the Japanese adapted to living in material stranded on gammaroidean fauna (Tattersall, 1922; the seashore, in forest litter, or in hypogean Schellenberg, 1937; Uéno, 1940; Karaman, waters. Amphipods are a very conspicuous 1979, 1986; Bousfield, 1977; Morino, 1984, and important part of many freshwater and 1985, 1986, 1993; Tomikawa & Morino, marine ecosystems (Bousfield, 1979; Barnard 2003; Tomikawa et al., 2003, 2006, 2007b; & Barnard, 1983). Tomikawa, 2008). To date, 28 species 2 K. TOMIKAWA ET AL. have been recorded from Japan. All known Melitidae, on the basis of analyses of partial Japanese gammaroidean genera and species sequences of mitochondrial and nuclear genes have been assigned to four families, of which from Japanese amphipods. We also briefly Gammaridae is holarctic in distribution, and discuss the direction of evolutionary changes Anisogammaridae, Mesogammaridae, and in habitats among gammaroidean species. Luciobliviidae are endemic to the North Pacific rim region (Bousfield, 1977, 1979; Materials and Methods Tomikawa et al., 2007b; Tomikawa, 2008). Although phylogenetic relationships Sampling design within Gammaridea are still poorly Nucleotide sequences of parts of the understood, several authors have conducted mitochondrial 16S and nuclear 28S rRNA relevant molecular phylogenetic studies genes were examined for 18 specimens (Meyran et al., 1997; Ogarkov et al., from 17 species of amphipods, including 1997; Sherbakov et al., 1998; Sherbakov seven anisogammarids, four melitids, three et al., 1999; Englisch & Koeneman, 2001; mesogammarids, and one species each Englisch et al., 2003; Lörz & Held, 2004; representing Crangonyctidae, Gammaridae, Macdonald et al., 2005; Hou et al., 2007; and Luciobliviidae (Table 1). Among these Tomikawa et al., 2007a). Most recently, species, Maera sp. from the Nansei Islands Tomikawa et al. (2007b) examined the resembles M. serratipalma, but differs in phylogenetic relationships among selected details of morphology (unpublished data). Japanese gammaroideans using the nuclear All trees were rooted with Siriella okadai 28S rRNA gene focusing on families (Mysida), because the sister group of within Gammaroidea and suggested the Amphipoda is uncertain. monophyly of superfamily Gammaroidea and two families, Anisogammaridae and Preparation of DNA, PCR, and DNA sequencing Mesogammaridae, respectively. However, Total genomic DNA was extracted with they did not include any non-gammaridean the QIAmp Tissue Kit (Qiagen); the final outgroup taxa. volume of the unquantitated DNA solution In this paper, we reassess the validity following extraction was roughly 100 μl. of superfamily Gammaroidea as proposed Approximately 150-bp and 450-bp fragments by Bousfield (1977) and the status of of the 16S and 28S rRNA genes, respectively, Anisogammaridae, Mesogammaridae, and were amplified by PCR with primers Table 1. Families, superfamilies, accession numbers, and sampling sites for the taxa included in the phylogenetic analysis. Species Family Superfamily Accession No. Collection site 16S 28S Anisogammarus pugettensis Anisogammaridae Gammaroidea AB432946 AB432947 Off Mukawa River, Hokkaido, Japan (42º33´N, 141º54´E) Eogammarus kygi Anisogammaridae Gammaroidea AB432948 AB432949 Naibetsu River, Hokkaido, Japan (42º48´N, 141º35´E) E. possjeticus Anisogammaridae Gammaroidea AB432950 AB432951 Akkeshi Bay, Hokkaido, Japan (43º1´N, 144º50´E) E. tiuschovi Anisogammaridae Gammaroidea AB432952 AB432953 Lake Yudou, Hokkaido, Japan (42º36´N, 143º32´E) Jesogammarus jesoensis Anisogammaridae Gammaroidea AB432954 AB432955 Sapporo, Hokkaido, Japan (43º3´N, 141º20´E) Locustogammarus locustoides Anisogammaridae Gammaroidea AB432956 AB432957 Akkeshi Bay, Hokkaido, Japan (43º1´N, 144º50´E) Spasskogammarus spasskii Anisogammaridae Gammaroidea AB432958 AB432959 Akkeshi Bay, Hokkaido, Japan (43º1´N, 144º50´E) Gammarus nipponensis Gammaridae Gammaroidea AB432960 AB432961 Yao, Osaka, Japan (34º37´N, 135º39´E) G. nipponensis Gammaridae Gammaroidea AB432962 AB432963 Naka River, Fukuoka, Japan (33º24´N, 130º24´E) Mesogammarus melitoides Mesogammaridae Gammaroidea AB432964 AB432965 Muroran, Hokkaido, Japan (42º18´N, 140º58´E) Eoniphargus kojimai Mesogammaridae Gammaroidea AB432966 AB432967 Seto River, Shizuoka, Japan (34º52´N, 138º13´E) Octopupilla felix Mesogammaridae Gammaroidea AB432968 AB432969 Koza River, Wakayama, Japan (33º32´N, 135º47´E) Lucioblivio kozaensis Luciobliviidae Gammaroidea AB432970 AB432971 Seto River, Shizuoka, Japan (34º52´N, 138º13´E) Crangonyx floridanus Crangonyctidae Crangonyctoidea AB432972 AB432973 Furutone River, Saitama, Japan Gammarella cyclodactyla Melitidae Hadzioidea AB432974 AB432975 Takehara, Hiroshima, Japan (34º20´N, 132º55´E) Maera danae Melitidae Hadzioidea AB432976 AB432977 Akkeshi, Hokkaido, Japan (42º58´N, 144º52´E) Maera sp. Melitidae Hadzioidea AB432978 AB432979 Off Cape Toi, Miyazaki, Japan (31º15´N, 131º31´E) Quadrimaera pacifica Melitidae Hadzioidea AB432980 AB432981 Takehara, Hiroshima, Japan (34º20´N, 132º55´E) PHYLOGENY OF GAMMAROIDEA AND ALLIED TAXA 3 KT16Sh (5’- CGTGCTAAGGTAGCRTA-3’) combined data. This was the best-fit model (modified from Macdonald et al., 2005) and determined by the likelihood ratio test (hLRT) KT16St (5’- TDARDRGTYGAACARAC-3’) executed in MODELTEST, with the gamma (modified from Palumbi et al., 1991) for 16S, shape parameter estimated to be 0.998 and and Am-28S-H (5’- GACGCGCATGAATGG the proportion of invariant sites estimated ATTAACG-3’) and Am-28S-T (5’-TGAACA to be 0.421. Robustness of NJ, MP, and ML ATCCGACGCTTGGCG-3’) (Tomikawa tree topologies was assessed with bootstrap et al., 2007) for 28S. PCR reactions were analyses (Felsenstein, 1985), with 1000 performed in an iCycler thermal cycler pseudoreplicates for NJ and MP, and 100 (Bio-Rad Laboratories) in 10-μl volumes pseudoreplicates for ML. containing 1.0 μl of template solution, 2 mM MgCl2, 2.5 mM each dNTP, 10 pmol Results each primer, and 5 U/μl Taq polymerase (Takara Ex Taq®) in 1X buffer provided by Sequences the manufacturer. Amplification conditions Excluding gap sites, the aligned combined were 94ºC for 7 min; 35 cycles of 94ºC for data set including all samples was 591 bp 45 s, 40–42ºC for 1 min depending on the long (16S, 146 bp; 28S, 445 bp), with 231 primer set, and 72ºC for 1 min; and 72ºC for variable sites and 162 parsimony-informative 7 min. Amplification products were purified sites. by Boom’s (1990) method and sequenced directly with a Model 3100-Avant genetic Phylogenetic relationships analyzer (ABI-Hitachi). Nucleotide sequences The optimal maximum-likelihood and have been deposited in the DDBJ nucleotide- neighbor-joining trees are shown in Figs. 1 sequence database