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Evolutionary Aspects of Gobioid Fishes Based Upon a Phylogenetic Analysis of Mitochondrial Cytochrome B Genes

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Evolutionary Aspects of Gobioid Fishes Based Upon a Phylogenetic Analysis of Mitochondrial Cytochrome B Genes Gene 259 (2000) 5–15 www.elsevier.com/locate/gene Evolutionary aspects of gobioid fishes based upon a phylogenetic analysis of mitochondrial cytochrome b genes Akihito a, Akihisa Iwata b, Takanori Kobayashi c, Kazuho Ikeo d, Tadashi Imanishi d, Hiroaki Ono d, Yumi Umehara d, Chika Hamamatsu d, Kayo Sugiyama e, Yuji Ikeda e, Katsuichi Sakamoto e, Akishinonomiya Fumihito f, Susumu Ohno g,1, Takashi Gojobori d,* a The Imperial Residence, 1-1 Chiyoda Chiyoda-ku, Tokyo 100-0001, Japan b Graduate School of Asian and African Area Studies, Kyoto University, 46 Shimoadachi-cho, Yoshida, Sakyo-ku, Kyoto 606-8501, Japan c Fish Genetics Division, National Research Institute of Aquaculture, 422-1 Nakatsuhamaura, Nansei-cho, Watarai-gun, Mie 516-0108, Japan d Center for Information Biology, National Institute of Genetics, Mishima, Shizuoka 411-8540, Japan e Imperial Household Agency, 1-1 Chiyoda Chiyoda-ku, Tokyo 100-8111, Japan f Yamashina Institute for Ornithology, 115 Tsutsumine-aza, Konoyama, Abiko-shi, Chiba 270-1145, Japan g Beckman Research Institute of the City of Hope, 1450 East Duarte Road, Duarte, CA 91010-3000, USA Accepted 13 October 2000 Received by G. Bernardi Abstract The Gobioidei is a large suborder in the order Perciformes and consists of more than 2000 species belonging to about 270 genera. The vast number of species and their morphological specialization adapted to diverse habits and habitats makes the classification of the gobioid fishes very diYcult. A comprehensive estimation of the evolutionary scenario of all gobioid fishes using only morphological information is diYcult for two major reasons: first, in addition to wide ecological diversification, there is a trend towards specialization and degeneration of morphological characters among these species; second, an appropriate outgroup of gobioid fishes has not been recognized. Based upon nucleotide sequence comparisons of gobioid mitochondrial cytochrome b genes, we established the phylogenetic relationships of their diVerentiation into many groups of morphological and ecological diversity. The phylogenetic trees obtained show that most species examined have diverged from each other almost simultaneously or during an extremely short period of time. © 2000 Elsevier Science B.V. All rights reserved. Keywords: Evolution; Gobioid fishes; Mitochondrial cytochrome b; Phylogeny 1. Introduction of Akihito et al. (2000) (Table 2), which is close to that of Nelson (1994) except for the Gobiidae. Nelson (1994) The Gobioidei is a large suborder in the order recognized five subfamilies in the Gobiidae, which Perciformes comprising about 268 genera and approxi- included about 212 genera and roughly 1875 species, mately 2121 species (Nelson, 1994), and they have been but he remarked that his classification of subfamilies of variously classified into families and subfamilies in recent the Gobiidae was provisional. As the classification needs times as detailed data on them accumulated. These further study, no subfamilies are recognized in the classifications are shown in Table 1 (Miller, 1973; Hoese, Gobiidae in this paper. 1984; Akihito et al., 1984; Hoese and Gill, 1993; Pezold, The gobioid fishes are generally small fishes and 1993; Nelson, 1994; Akihito et al., 2000). The classifica- rarely exceed 50 cm. The smallest of all the fishes is tion of the gobioid fishes used in this paper follows that found among them, i.e a species identified as Trimmatom of the Gobiidae whose matured females are 8–10 mm * Corresponding author. in standard length (Winterbottom and Emery, 1981). E-mail address: [email protected] (T. Gojobori) The geographical distribution of the gobioid fishes is 1 Deceased. worldwide, and they are absent only from the Arctic 0378-1119/00/$ - see front matter © 2000 Elsevier Science B.V. All rights reserved. PII: S0378-1119(00)00488-1 6 Akihito et al. / Gene 259 (2000) 5–15 Table 1 Seven patterns of the classification of families and subfamilies of the Gobioidei in recent time Miller (1973) 2 families (7 subfamilies) Rhyacichthyidae, Gobiidae (Eleotrinae, Pirskeninae, Xenisthminae, Gobionellinae, Tridentigerinae, Gobiinae, Kraemeriinae) Hoese (1984) 6 families (6 subfamilies) Rhyacichthyidae, Eleotrididae, Xenisthmidae, Kraemeriidae, Microdesmidae (Microdesminae, Ptereleotrinae), Gobiidae (Oxudercinae, Amblyopinae, Sicydiinae, Gobiinae) Akihito et al. (1984) 3 families (2 subfamilies) Rhyacichthyidae, Gobiidae (Eleotridinae, Gobiinae), Gunnellichthyidae Hoese and Gill (1993) 6 families (5 subfamilies) Rhyacichthyidae, Odontobutidae, Gobiidae (Butinae, Eleotrinae, Gobiinae), Xenisthmidae, Kraemeriidae, Microdesmidae (Microdesminae, Ptereleotrinae) Pezold (1993) 2 superfamilies {6 families (5 subfamilies)} Rhyacichthyoidea {Rhyacichthyidae}, Gobioidea {Eleotrididae, Kraemeriidae, Microdesmidae, Xenisthmidae, Gobiidae (Amblyopinae, Gobiinae, Gobionellinae, Oxudercinae, Sicydiinae)} Nelson (1994) 8 families (9 subfamilies) Rhyacichthyidae, Odontobutidae, Eleotridae (Butinae, Eleotrinae), Gobiidae (Oxudercinae, Amblyopinae, Sicydiinae, Gobionellinae, Gobiinae), Kraemeriidae, Xenisthmidae, Microdesmidae (Microdesminae, Ptereleotrinae), Schindleriidae Akihito et al. (2000) 8 families (4 subfamilies) Rhyacichthyidae, Odontobutidae, Eleotridae (Butinae, Eleotrinae), Xenisthmidae, Gobiidae, Kraemeriidae, Microdesmidae (Microdesminae, Ptereleotrinae), Schindleriidae Table 2 Species of gobioid groups examined in the present study Accession Species Family and subfamily Collecting locality Collection Habitata no. date AB021230 Rhyacichthys aspro (Ra) Rhyacichthyidae Iriomote Island, Okinawa, Japan 13 July 1996 F AB021231 Bostrychus sinensis (Bs) Eleotridae Butinae Ishigaki Island, Okinawa, Japan 14 July 1996 B AB021232 Butis amboinensis (Ba) Eleotridae Butinae Iriomote Island, Okinawa, Japan 12 July 1996 B AB021233 Calumia godeVroyi (Cg) Eleotridae Eleotrinae Amami Island, Kagoshima, Japan 1998 S AB021234 Dormitator maculatus (Dm) Eleotridae Eleotrinae (purchased from aquarium shop) May 1998 F AB021235 Eleotris acanthopoma (Ea) Eleotridae Eleotrinae Ishigaki Island, Okinawa, Japan 7 April 1996 F AB021236 Eleotris fusca (Ef ) Eleotridae Eleotrinae Iriomote Island, Okinawa, Japan 30 May 1996 F AB021237 Eleotris melanosoma (Em) Eleotridae Eleotrinae Ishigaki Island, Okinawa, Japan 3 April 1996 B AB021238 Eleotris oxycephala (Eo) Eleotridae Eleotrinae Yoshida-cho, Shizuoka, Japan 1993 F AB021239 Gobiomorphus hubbsi (Gh) Eleotridae Eleotrinae Ashley River, New Zealand 28 July 1998 F AB021240 Hypseleotris compressa (Hc) Eleotridae Eleotrinae (purchased from aquarium shop) October 1997 F AB021241 Micropercops swinhonis (Ms) Odontobutidae Samrye-up, Chollabuk-do, Korea 8 May 1996 F AB021242 Mogurnda mogurnda (Mm) Eleotridae Eleotrinae (purchased from aquarium shop) December 1997 F AB021243 Odontobutis obscura (Oo) Odontobutidae Kochi, Japan 15 August 1995 F AB021244 Ophieleotris sp. Eleotridae Eleotrinae Iriomote Island, Okinawa, Japan 2 Nov. 1995 F (Akihito et al., 1984) (Osp) AB021245 Ophiocara porocephala (Op) Eleotridae Butinae Ishigaki Island, Okinawa, Japan 3 April 1996 B AB021246 Oxyeleotris marmorata (Om) Eleotridae Butinae Bangkok, Thailand June 1997 F AB021247 Tateurndina ocellicauda (Toc) Eleotridae Eleotrinae (purchased from aquarium shop) December 1997 F AB021248 Xenisthmus sp. ( Xsp) Xenisthmidae Zamami Island, Okinawa, Japan April 1997 S AB021249 Acanthogobius flavimanus (Af ) Gobiidae Chiba, Japan 3 November 1996 S AB021250 Kraemeria cunicularia ( Kc) Kraemeriidae Ishigaki Island, Okinawa, Japan 14 July 1996 B AB021251 Periophthalmus argentilineatus (Par) Gobiidae Ishigaki Island, Okinawa, Japan 14 July 1996 B AB021252 Ptereleotris heteroptera (Ph) Microdesmidae Iriomote Island, Okinawa, Japan 20 July 1997 S Ptereleotrinae AB021253 Taenioides limicola (Tl ) Gobiidae Iriomote Island, Okinawa, Japan 22 July 1997 B AB021254 Tridentiger bifasciatus (Tb) Gobiidae Lake Shinji, Shimane, Japan 2 December 1996 B AB021255 Tridentiger obscurus (Tob) Gobiidae Mie, Japan May 1997 B AB021256 Gunnellichthys monostigma (Gm) Microdesmidae Iriomote Island, Okinawa, Japan 20 July 1997 S Microdesminae AB021257 Protogobius attiti (Pat) Unassigned Province SUD, New Caledonia 10 November 1997 F a S: sea; F: fresh water; B: brackish water. Akihito et al. / Gene 259 (2000) 5–15 7 and Antarctic areas. Most gobioid fishes have bottom- 2.2. DNA amplification and sequencing dwelling habits in the sea and rivers, and their habitats show a wide spectrum, from the sea-floor at a depth of We extracted DNA from each of these 28 species of over 300 m to mountain streams. gobioid fishes. First, the tissue fragments were incubated The adaptations to these habitats have developed overnight at 60°C in TNES-6M buVer and proteinase various morphological specializations. A notable adap- K. Then, samples were deproteinized and total DNA tation to the benthic way of life is the development of was extracted from an individual sample, using the a sucker formed by uniting the pelvic fins to cling to a method of Asahida et al. (1996). We designed primers substratum. The sucker is found in a large number of specific to the cytochrome b gene that was used for PCR species of the Gobiidae. Sicyopterus japonicus has a (polymerase chain reaction) analysis (see Fig. 2). short round sucker whose adhesive power is extremely PCR reactions were conducted under the following strong, and it clings to the rocks in torrential streams conditions: 1 min at 94°C, followed by 30 cycles of 30 s by utilizing the sucker. It even climbs the walls of at 94°C,
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