crustacean research, no. 39: 1 - 10, 2010 Phylogenetic relationships of superfamily () 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 , 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 , was large family ; 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 , 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 , 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) 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) 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 (linked to the EMBL and and 2, respectively. Two equally parsimonious GenBank databases) under accession numbers trees were obtained (726 steps, CI = 0.530, AB432946–AB432981. RI = 0.539), and the strict consensus of these trees is shown in Fig. 3. Although the three Phylogenetic analyses trees differ slightly in topology, the following The nucleotide sequences were aligned relationships are congruent among them, with the multiple alignment algorithm in with bootstrap values > 50%. (i) Members CLUSTAL W (Thompson et al., 1994) with of superfamily Gammaroidea are divided default settings (gap opening cost = 15, gap into two main clades, one consisting of extension cost = 6.66, transition weight = 0.5). Anisogammaridae, and the other containing Alignment gaps were treated as missing data. the remaining five families (Crangonyctidae, Phylogenetic relationships were reconstructed Gammaridae, Luciobliviidae, Melitidae, by three methods: (i) maximum-parsimony and Mesogammaridae) included in the (MP) implemented in MEGA ver. 3.0 study. (ii) The seven anisogammarid species software (Kumar et al., 2004), with gaps comprise a monophyletic group, as do the treated as missing data, equal weighting for three mesogammarid species, with each all characters, and heuristic searches of 100 clade having high bootstrap support. (iii) random-addition replicates using the close- In Anisogammaridae, the three species of neighbor-interchange (CNI) algorithm; (ii) Eogammarus form a monophyletic group. neighbor-joining (NJ) (Saitou & Nei, 1987) (iv) In Melitidae, three species (Maera danae, implemented in MEGA ver. 3.0 software, Maera sp., and Quadrimaera pacifica) form a using Kimura’s two-parameter substitution monophyletic group. model (Kimura, 1980); and (iii) maximum- In contrast, the following relationships likelihood (ML) implemented in PAUP* were supported only by the ML analysis, (Swofford, 2002), based on the substitution with high bootstrap support. (v) The four model and phylogenetic parameters identified melitid species form a monophyletic as optimal by MODELTEST 3.06 (Posoda & group (98% support). (vi) Maera danae is Crandall, 1998). The ML analysis used the phylogenetically closer to Quadrimaera transversion model (TVM + I + G) for the parcifica than to the congenic species Maera 4 K. Tomikawa et al.

Fig. 1. Maximum likelihood (ML) tree for the combined 16S and 28S data, based on the TVM + I + G substitution model. Bootstrap values >50% are shown, based on 100 pseudoreplicates. Black circles indicate marine species, double circles indicate brackish water species, open circles indicate freshwater species, and asterisks indicate interstitial species. Black and white vertical bars to right of species names indicate families and superfamilies, respectively.

sp. (85% support). shallow concavity in the proximal element. To date, gammarid-type calceolus has been one of the most important diagnostic features Discussion of Gammaroidea (Tomikawa et al., 2007b). Phylogenetics and at the suprafamilial Recent studies of amphipod phylogeny level have reached conflicting conclusions on Superfamily Gammaroidea (Bousfield, whether superfamily Gammaroidea is 1977) was originally not well defined, monophyletic. The studies by Englisch because it was defined by characters et al. (2003) and Tomikawa et al. (2007) typically found in suborder Gammaridea supported monophyly for Gammaroidea, (Williams & Barnard, 1988). In a review on the basis of 18S and 28S rRNA gene of the morphology of calceolus, Lincoln sequences, respectively. In contrast, the study & Hurley (1981) showed that members of by Macdonald et al. (2005) based on 16S, Gammaroidea have gammarid-type calceolus, 18S, and COI data did not find monophyly for which is characterized by a discrete stalk and Gammaroidea: in a strict consensus MP tree, PHYLOGENY OF GAMMAROIDEA AND ALLIED TAXA 5

Fig. 2. Neighbor-joining (NJ) tree for the combined 16S and 28S data. Bootstrap values >50% are shown, based on 1000 pseudoreplicates. Black and white vertical bars to right of species names indicate families and superfamilies, respectively.

gammaroidean Ramellogammarus derived from them. Schmitz (1992) considered vancouverensis, Eogammarus confervicolus, the gammarid type to represent one of the and E. oclairi are closely related with simplest and most basic anatomical patterns pontoporeioidean Monoporeia affinis rather among the nine structural types of calceoli than other gammaroideans; and in a ML recognized by Lincoln & Hurley (1981), tree, gammaroidean R. vancouverensis, E. favoring the latter hypothesis. In contrast, confervicolus, and E. oclairi formed a cluster Bousfield (2001) regarded the calceolus of including pontoporeioidean M. affinis and Crangonyctoidea as the most plesiomorphic. melphidippoidean Gammarellus angulosus The calceolus within Crangonyctoidea rather than other gammaroideans. These consists of a basal stalk and elongate body conflicting results may have arisen from the that bears many (more than 20) elements of small number of taxa included, especially similar simple structure (Bousfield, 2001). To in the former two studies. Although the clarify the evolution of calceolus, exhaustive present study also treated selected species, study of molecular phylogenetic relationships our results did not support the monophyly of within Amphipoda are required. Gammaroidea and were consistent with the The transverse cephalothorax apodemes study by Macdonald et al. (2005). were discovered by Coleman (2002) as Gammarid-type calceolus may not significant taxonomic features of amphipods. be synapomorphic for Gammaroidea, He found that the apodemes in Gammaridae suggesting two alternative hypotheses: (1) and Melitidae are fused into a complete gammarid-type calceolus is the result of cuticular bridge. However, close relationships convergent and/or parallel evolution; (2) between Gammaridae and Melitidae were gammarid-type calceolus is plesiomorphic in not supported by molecular analyses (e.g. Amphipoda, and other types of calceoli were Englisch et al., 2003; Macdonald et al., 2005; 6 K. Tomikawa et al.

Fig. 3. Maximum parsimony (MP) strict consensus tree for the combined 16S and 28S data. Bootstrap values >50% are shown, based on 1000 pseudoreplicates. Black and white vertical bars to right of species names indicate families and superfamilies, respectively.

present study). Studies of the transverse 1979]. Recently, it has been found that the cephalothorax apodemes of amphipods are sequence of Crangonyx serratus in their study limited and further study is needed. was a contamination and this result is in error (GenBank; Macdonald, pers. comm.). Phylogenetics and taxonomy at levels below On the basis of morphological characters, the family Tomikawa et al. (2007b) proposed that Family Anisogammaridae is confined to Mesogammaridae is monophyletic, the North Pacific rim region, occurring in and recognized two distinct lineages marine, brackish, and freshwater habitats. within this family on morphological and Members are characterized by having sexually ecological grounds: 1) Mesogammarus dimorphic gnathopods, the first being larger; and Paramesogammarus, a marine group, in males the palms are vertical and lined with characterized by having well-developed striated, peg-like setae; and the coxal gills eyes, a stout propodus and smooth palmar bear accessory lobes. Anisogammaridae has margin of the gnathopods, and unstalked been considered a well-defined family among coxal gills; 2) Eoniphargus and Octopupilla, Amphipoda since the work of Barnard & a group inhabiting freshwater subterranean Barnard (1983). The present results supported waters, characterized by having reduced the monophyly of Anisogammaridae. eyes, a feeble propodus of the gnathopods, Macdonald et al. (2005) did not support the palmar margin with small triangular monophyly of Anisogammaridae, but instead protuberances, and pedunculate coxal gills. In found a crangonyctid species [Crangonyx the present study, we analyzed all species of serratus (Embody, 1911)] embedded within Mesogammaridae except Paramesogammarus a paraphyletic group of three anisogammarid americanus Bousfield, 1979 and found that species [Ramellogammarus vancouverensis Eoniphargus kojimai was the sister group to Bousfield, 1979; Eogammarus confervicolus Octopupilla felix, which is consistent with the (Stimpson, 1856); and E. oclairi Bousfield, previous study by Tomikawa et al. (2007). PHYLOGENY OF GAMMAROIDEA AND ALLIED TAXA 7

However, we refrain here from establishing have repeatedly switched between marine a new family or subfamily for each clade and freshwater habitats. In the same way, because this would merely complicate the subterranean species such as Eoniphargus classification of Amphipoda at this early stage kojimai, Octopupilla felix, and Lucioblivio of study. kozaensis did not form monophyletic groups, Holsinger (1986) suggested that putative indicating their independent invasion to epigean freshwater ancestors of freshwater subterranean habitats. cave dwelling species of Gammarus (family Gammaridae) were probably derived from Acknowledgements relatively recent marine immigrants. In our study, Mesogammarus memelitoides was the We thank Mr. T. Torii of Kokudokankyou first diverged species in Mesogammaridae, Corp., Ms. N. Matsumoto of Hiratsuka indicating that the common ancestor of City Museum for donating the specimens Eoniphargus kojimai and Octopupilla felix examined in this study, and Dr. Matthew H. might have invaded freshwater subterranean Dick of Hokkaido University for valuable waters from marine surface waters through comments on the manuscript. Thanks are also surface freshwaters or marine interstitial due to Dr. Kenneth S. Macdonald of New environment. Since subterranean species are Mexico State University and an anonymous characterized morphologically by rudimentary reviewer for their critical reading and for eyes, reduced pigmentation, and feeble useful advice. This study was supported in pereopods (Holsinger, 1994), these regressive part by a Research Fellowship for Young features are probably an adaptation for life in Scientists to the first author from the Japan a subterranean environment. Society for the Promotion of Science, by the The diagnosis of family Melitidae is Research Institute of Marine Invertebrates, rather unsatisfactory, as it is based on and by Fujiwara Natural History Foundation. characters typically found in superfamily Hadzioidea (Bousfield, 1977). Englisch et Literature Cited al. (2003) did not find monophyly for the two melitid species they studied, and noted, Barnard, J. L., 1972. The marine fauna “it remains uncertain whether the Melitidae of New Zealand: algae-living littoral are monophyletic or not, because a long- Gammaridea (Crustacea Amphipoda). branch effect may be obscuring the real New Zealand Oceanographic Institute phylogenetic relationships”. Only our ML tree Memoir, 62: 7–216. (Fig. 1) supported monophyly for Melitidae, ­———, 1973. Revision of Corophiidae whereas the position of one melitid species, and related families (Amphipoda). Gammarella cyclodactyla, was unresolved Smithsonian Contributions to Zoology, in our NJ and MP trees. On the other hand, 151: 1–27. all three phylogenetic analyses supported ———, & Barnard, K. H., 1983. Freshwater monophyly for the three species of Melitidae Amphipoda of the World, I. Evolutionary other than G. cyclodactyla, though the Patterns and II. Handbook and relationships among these three species varied Bibliography. xix + 830 pp. Hayfield with the method of analysis. In our ML tree Associates, Mt. Vernon, VA. (Fig. 1), Maera was paraphyletic, whereas the ———, & Karaman, G. S., 1991. two species of Maera were sister taxa in the The families and genera of marine NJ tree (Fig. 2). Analyses including additional gammaridean Amphipoda (except marine species of Melitidae are needed. gammaroids). Parts 1 & 2. Records of Amphipods occur in various the Australian Museum Supplement, 13: environments, including marine, brackish, 1–866. and freshwater (Fig. 1). We found that neither Boom, R., Sol, C. J. A., Salimans, M. M. marine nor brackish + freshwater species M., Jansen, C. L., Wertheim-Van Dillen, formed monophyletic groups, indicating P. M. E., & Van Der Noordaa, J., 1990. that in their evolutionary history, amphipods Rapid and simple method for purification 8 K. Tomikawa et al.

of nucleic acids. Journal of Clinical amphipods. Hydrobiologia, 287: 131–145. Microbiology, 28: 495–503. Hou, Z., Fu, J., & Li, S., 2007. A molecular Bousfield, E. L., 1977. A new look at the phylogeny of the Gammarus systematics of gammaroidean amphipods (Crustacea: Amphipoda) based on of the World. Crustaceana Supplement, 4: mitochondrial and nuclear gene sequences. 282–316. Molecular Phylogenetics and Evolution, ———, 1979. A revised classification and 45: 596–611. phylogeny of amphipod crustaceans. Karaman, G. S., 1979. First discovery of Transactions of the Royal Society of genus Melitoides Tzv. in Japan with Canada, Series IV, XVI: 343–390. remarks on some Japanese Eogammarus ———, 1983. An updated phyletic species. Contribution to the knowledge classification and palaeohistory of the of the Amphipoda 98. Poljoprivreda I Amphipoda. In: F. R. Schram, (ed.), Šumarstvo, 25: 23–40. Phylogeny, Museum of ———, 1986. The genus Gammarus Fabr. in Natural History, San Diego, 257–277. Japan (fam. Gammaridae). Contribution ———, 2001. An updated commentary on to the knowledge of the Amphipoda 162. phyletic classification of the amphipod Poljoprivreda I Šumarstvo, 32: 81–97. Crustacea and its applicability to the Kimura, M., 1980. A simple method for North American fauna. Amphipacifica, 3: estimating evolutionary rates of base 49–119. substitutions through comparative studies ———, & Shih, C.-T., 1994. The phyletic of nucleotide sequences. Journal of classification of amphipod crustaceans: Molecular Evolution, 16: 111–120. problems in resolution. Amphipacifica, 1: Kumar, S., Tamura, K., & Nei, M., 2004. 76–134. MEGA3: Integrated software for Bulycheva, A., 1957. Morskie Bloxi Morej molecular evolutionary genetics analysis SSSR I Sopredel’nyx Vod (Amphipoda- and sequence alignment. Bioinformatics, Talitroidea). Opredeliteli po Faune SSSR, 5: 150–163. 65: 1–185. (In Russian) Lincoln, R. J., & Hurley, D. E., 1981. Coleman, C. O., 2002. The transverse The calceolus, a sensory structure of apodeme bridge from the cephalothorax gammaridean amphipods (Amphipoda: of Amphipoda (Crustacea) and its Gammaridea). Bulletin of the British significance for systematics. Journal of Museum, Natural History, Zoology, 40: Natural History, 36: 37–49. 103–116. Englisch, U., & Koenemann, S., 2001. Lörz, A., & Held, C., 2004. A preliminary Preliminary phylogenetic analysis molecular and morphological phylogeny of selected subterranean amphipod of the Antarctic and crustaceans, using small subunit rDNA (Crustacea, Amphipoda). gene sequences. Organisms Diversity and Molecular Phylogenetics and Evolution, Evolution, 1: 139–145. 31: 4–15. ———, Coleman, C. O., & Wägele, J. Macdonald, K. S., Yampolsky, L., & Duffy, W., 2003. First observations on the J. E., 2005. Molecular and morphological phylogeny of the families Gammaridae, evolution of the amphipod radiation of Crangonyctidae, Melitidae, , Lake Baikal. Molecular Phylogenetics and and Evolution, 35: 323–343. (Amphipoda, Crustacea), using small Meyran, J., Monnerot, M., & Taberlet, P., subunit rDNA gene sequences. Journal of 1997. Taxonomic status and phylogenetic Natural History, 37: 2461–2486. relationships of some species of the genus Felsenstein, J., 1985. Confidence limits Gammarus (Crustacea, Amphipoda) on phylogenies: an approach using the deduced from mitochondrial DNA bootstrap. Evolution, 39: 783–791. sequences. Molecular Phylogenetics and Holsinger, J. R., 1994. Pattern and process Evolution, 8: 1–10. in the biogeography of subterranean Morino, H., 1984. On a new freshwater PHYLOGENY OF GAMMAROIDEA AND ALLIED TAXA 9

species of Anisogammaridae angrenzenden Meeresteile nach ihren (Gammaroidea: Amphipoda) from Merkmalen und nach ihrer Lebensweise. central Japan. Publications of the Itako G. Fischer, Stuttgart, Germany, 1–252. Hydrobiological Station, 1: 17–23. Schmitz, E. H., 1992. Amphipoda. In: F. ———, 1985. Revisional studies on W. Harrison, & A. G. Humes, (eds.), Jesogammarus–Annanogammarus Microscopic Anatomy of Invertebrates, group (Amphipoda: Gammaroidea) Volume 9: Crustacea, Wiley-Liss, New with descriptions of four new species York, 443–528. from Japan. Publications of the Itako Sherbakov, D.Y., Kamaltynov, R. M., Hydrobiological Station, 2: 9–55. Ogarkov, O. B., & Verheyen, E., 1998. ———, 1986. A new species of the subgenus Patterns of evolutionary change in Annanogammarus (Amphipoda: Baikalian gammarids inferred from DNA Anisogammaridae) from Lake Suwa, sequences (Crustacea, Amphipoda). Japan. Publications of the Itako Molecular Phylogenetics and Evolution, Hydrobiological Station, 3: 1–11. 10: 160–167. ———, 1993. A new species of the ———, ———, ———, ———, Vainio, genus Jesogammarus (Amphipoda: J. K., & Verheyen, E., 1999. On the Anisogammaridae) from brackish waters phylogeny of Lake Baikal amphipods in of Japan. Publications of the Itako the light of mitochondrial and nuclear Hydrobiological Station, 6: 9–16. DNA sequence data. Crustaceana, 72: Ogarkov, O. B., Kamaltynov, R. M., 911–919. Belikov, S. I., & Sherbakov, D. Y., Stebbing, T. R. R., 1906. Amphipoda I. 1997. Phylogenetic relatedness of the Gammaridea. Das Tierreich, 21: 1–806. Baikal Lake endemical [sic.] amphipods Swofford, D. L., 2002. PAUP*. Phylogenetic (Crustacea, Amphipoda) deduced from Analysis Using Parsimony (*and Other partial nucleotide sequences of the Methods), Version 4. Sinauer Associates, cytochrome oxidase subunit III genes. Sunderland, Massachusetts. Molecular Biology 31: 24–29. Tattersall, W. M., 1922. Zoological results of Palumbi, S. R., Martin, A., Romano, S., a tour in the Far East. Part 8. Amphipoda McMillan, W. V., Stice, L., & Grabowski, with notes on an additional species of G., 1991. The Simple Fool’s Guide to Isopoda. Memoirs of the Asiatic Society PCR. Version 2.0. Special Publication, of Bengal, 6: 435–459. Department of Zoology and Kewalo Thompson, J. D., Higgins, D. G., & Gibson, Marine Laboratory, University of Hawaii, T. J., 1994. CLASTAL W: improving Honolulu. the sensitivity of progressive multiple Posoda, D., & Crandall, K. A., 1998. sequence alignment through sequence MODELTEST: testing the model of DNA weighting, positions-specific gap penalties substitution. Bioinformatics, 14: 817–818. and weight matrix choice. Nucleic Acids Saitou, N., & Nei, M., 1987. The neighbor- Research, 22: 4673–4680. joining method: a new method for Tomikawa, K., 2008. Two new records of reconstructing phylogenetic trees. anisogammarid amphipods (Crustacea: Molecular Biology and Evolution, 4: 406– Amphipoda: Gammaridea) from Japan. 425. Species Diversity, 13: 35–51. Schellenberg, A., 1937. Schlüssel und Tomikawa, K., Kobayashi, N., Morino, Diagnosen der dem Süßwasser Gammarus H., Hou, Z., & Mawatari, S. F., 2007a. nahestehenden einheiten ausschließlich Phylogenetic relationships within der Arten des Baikalsees und Australiens. the genus Jesogammarus (Crustacea, Zoologischer Anzeiger, 117: 267–280. Amphipoda, Anisogammaridae) deduced ———, 1942. Teil. Krebstiere order from mitochondrial COI and 12S Crustacea. IV: Flohkrebse order sequences. Zoological Science, 24: 173– Amphipoda. In: F. Dahl, (ed.), Die 180. Tierwelt Deutschlands und der Tomikawa, K., Kobayashi, N., Morino, H., & 10 K. Tomikawa et al.

Mawatari, S.F., 2007b. New gammaroid Anisogammaridae), with a description of family, genera and species from a new species. Journal of Natural History, subterranean waters of Japan, and their 40: 1083–1148. phylogenetic relationships (Crustacea: Uéno, M., 1940. Some freshwater amphipods Amphipoda). Zoological Journal of the from Manchoukuo, Corea and Japan. Linnean Society, 149: 643–670. Bulletin of the Biogeographical Society of sequences. Zoological Science, 24: 173– Japan, 10: 63–85. 180. Williams, W. D., & Barnard, J. L., 1988. The Tomikawa, K., Kobayashi, N., Morino, H., & taxonomy of crangonyctoid Amphipoda Mawatari, S.F., 2007b. New gammaroid (Crustacea) from Australian fresh family, genera and species from waters: foundation studies. Records of subterranean waters of Japan, and their the Australian Museum Supplement, 10: phylogenetic relationships (Crustacea: 1–180. Amphipoda). Zoological Journal of the Linnean Society, 149: 643–670. ———, & Morino, H., 2003. Two new Addresses: (KT) Department of Science freshwater species of the genus Education, Graduate School of Education, Jesogammarus (Crustacea: Amphipoda: Hiroshima University, Higashi-Hiroshima, Anisogammaridae) from northern Japan. 739-8524, Japan; (NK) The Hokkaido Zoological Science, 20: 229–241. University Museum, Sapporo, 060-0810, ———, ———, & Mawatari, S.F., 2003. Japan; (SFM) Department of Natural History A new freshwater species of the genus Sciences, Faculty of Science, Hokkaido Jesogammarus (Crustacea: Amphipoda: University, Sapporo, 060-0810, Japan. Anisogammaridae) from northern Japan. E-mail: (KT) tomikawa@hiroshima-u. Zoological Science, 20: 925–933. ac.jp ———, ———, Toft, J., & Mawatari, S.F., 2006. A revision of Eogammarus Received: 2 July 2009. Birstein, 1933 (Crustacea, Amphipoda, Accepted: 4 January 2010.