Abstract
In order to elucidate the evolutionary process of deep-sea Bathymodiolus mussels, we investigated the phylogenetic relationships of 16 species worldwide by analyzing nucleotide sequences of the mitochondrial COI and ND4 genes. Deep-sea mussels were clustered into three groups by basal trichotomous divergence. The first was composed of four species found in Japanese waters and one species from the Gulf of Mexico, which contain methanotrophic endosymbiotic bacteria. The second included nine species distributed in the West and East Pacific, Indian, and Atlantic Oceans. Members of the second group were trichotomously divided into the Indo-West Pacific, Atlantic, and East Pacific subclusters. The Indo-West Pacific subcluster was composed of three very closely related species with mutual genetic distances at the intraspecific level (av. 0.019 in COI and 0.009 in ND4 relative to av. 0.156 in COI and 0.265 in ND4 among Bathymodiolus species other than Cluster A species), suggesting some gene flow among these species. The third consisted of two West Pacific species. Species in the second and third groups contain mainly thioautotrophic endosymbionts, including some species harboring both methanotrophs and thioautotrophs.
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References
Arevalo E, Davis SK, Sites JWJ (1994) Mitochondrial DNA sequence divergence and phylogenetic relationships among eight chromosome races of the Sceloperus grammicus complex (Phrynosomatidae) in Central Mexico. Syst Biol 43:387–418
Bielawski JP, Gold JR (1996) Unequal synonymous substitution rates within and between two protein-coding mitochondrial genes. Mol Biol Evol 13:889–892
Cary SC, Giovannoni SJ (1993) Transovarial inheritance of endosymbiotic bacteria in clams inhabiting deep-sea hydrothermal vents and cold seeps. Proc Natl Acad Sci USA 90:5695–5699
Cavanaugh CM, Levering PR, Maki JS, Mitchell R, Lidstrom ME (1987) Symbiosis of methylotrophic bacteria and deep-sea mussels. Nature 325:346–348
Childress JJ, Fisher CR, Brooks JM, Kennicutt II MC, Bidigare R, Anderson AE (1986) A methanotrophic marine molluscan (Bivalvia, Mytilidae) symbiosis; mussels fueled by gas. Science 233:1306–1308
Cosel R.von (2002) A new species of bathymodiolinae mussel (Mollusca, Bivalvia, Mytilidae) from Mauritania (West Africa), with comments on the genus Bathymodiolus Kenk & Wilson, 1985. Zoosystema 24:259–271
Cosel R.von, Olu K (1998) Gigantism in Mytilidae. A new Bathymodiolus from cold seep areas on the Barbados accretionary Prism. C R Acad Sci Paris Sci de la Vie 321:655–663
Cosel R.von, Marshall BA (2003) Two new species of large mussels (Bivalvia: Mytilidae) from active submarine volcanoes and a cold seep off the eastern North Island of New Zealand, with description of a new genus. Nautilus 117:31–46
Cosel R.von, Métivier B, Hashimoto J (1994) Three new species of Bathymodiolus (Bivalvia: Mytilidae) from hydrothermal vents in the Lau Basin and the North Fiji Basin, Western Pacific, and the Snake Pit area, Mid-Atlantic Ridge. Veliger 37:374–392
Cosel R.von, Comtet T, Krylova EM (1999) Bathymodiolus (Bivalvia: Mytilidae) from hydrothermal vents on the Azores Triple Junction and the Logatchev hydrothermal field, Mid-Atlantic Ridge. Veliger 42:218–248
Distel DL, Lane DJ, Olsen GJ, Giovannoni SJ, Pace B, Pace NR, Stahl DA, Felbeck H (1988) Sulfur-oxidizing bacterial endosymbionts: analysis of phylogeny and specificity by 16S rRNA sequences. J Bacteriol 170:2506–2510
Distel DL, Lee HK-W, Cavanaugh CM (1995) Intracellular coexistence of methano- and thioautotrophic bacteria in a hydrothermal vent mussel. Proc Natl Acad Sci USA 92:9598–9602
Distel DL, Baco AR, Chuang E, Morrill W, Cavanaugh CM, Smith CR (2000) Do mussels take wooden steps to deep-sea vents? Nature 403:725–726
Dubilier N, Windoffer R, Giere O (1998) Ultrastructure and stable carbon isotope composition of the hydrothermal vent mussels Bathymodiolus brevior and B. sp. affinis brevior from the North Fiji Basin, western Pacific. Mar Ecol Prog Ser 165:187–193
Fiala-Médioni A, McKiness ZP, Dando P, Boulegue J, Mariotti A, Alayse-Danet AM, Robinson JJ, Cavanaugh CM (2002) Ultrastructural, biochemical, and immunological characterization of two populations of the mytilid mussel Bathymodiolus azoricus from the Mid-Atlantic Ridge: evidence for a dual symbiosis. Mar Biol 141:1035–1043
Fisher CR, Brooks JM, Vodenichar JS, Zande JM, Childress JJ, Burke Jr RA (1993) The co-occurrence of methanotrophic and chemoautotrophic sulfur-oxidizing bacterial symbionts in a deep-sea mussel. Mar Ecol 14:277–289
Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299
Fujikura K, Kojima S, Fujiwara Y, Hashimoto J, Okutani T (2000) New distribution records of vesicomyid bivalves from deep-sea chemosynthesis-based communities in Japanese waters. Venus 59:103–121
Fujiwara Y, Takai K, Uematsu K, Tsuchida S, Hunt JC, Hashimoto J (2000) Phylogenetic characterization of endosymbionts in three hydrothermal vent mussels: influence on host distributions. Mar Ecol Prog Ser 208:147–155
Goffredi SK, Hurtado LA, Hallam S, Vrijenhoek RC (2003) Evolutionary relationships of deep-sea vent and cold seep clams (Mollusca: Vesicomyidae) of the “ pacifica/lepta” species complex. Mar Biol 142:311–320
Gustafson RG, Turner RD, Lutz RA, Vrijenhoek RC (1998) A new genus and five new species of mussels (Bivalvia: Mytilidae) from deep-sea sulfide/hydrocarbon seeps in the Gulf of Mexico. Malacologia 40:63–112
Hashimoto J (2001) A new species of Bathymodiolus (Bivalvia: Mytilidae) from hydrothermal vent communities in the Indian Ocean. Venus 60:141–149
Hashimoto J, Okutani T (1994) Four new mytilid mussels associated with deepsea chemosynthetic communities around Japan. Venus 53:61–83
Hashimoto J, Yamane T (2005) A new species of Gigantidas (Bivalvia: Mytilidae) from a vent site on the Kaikata Seamount southwest of the Ogasawara (Bonin) Islands, southern Japan. Venus 64:1–10
Jollivet D (1996) Specific and genetic diversity at deep-sea hydrothermal vents: an overview. Biodiv Conserv 5:1619–1653
Kenk VC, Wilson BR (1985) A new mussel (Bivalvia, Mytilidae) from hydrothermal vents in the Galapagos Rift Zone. Malacologia 26:253–271
Kimura M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120
Kojima S, Ohta S, Yamamoto T, Miura T, Fujiwara Y, Hashimoto J (2001a) Molecular taxonomy of vestimentiferans of the western Pacific and their phylogenetic relationships to species of the eastern Pacific. I. Family Lamellibrachiidae. Mar Biol 139:211–219
Kojima S, Segawa R, Fujiwara Y, Fujikura K, Ohta S, Hashimoto J (2001b) Phylogeny of hydrothermal-vent-endemic gastropods Alviniconcha spp. from western Pacific revealed by mitochondrial DNA sequences. Biol Bull 200:298–304
Kojima S, Ohta S, Yamamoto T, Miura T, Fujiwara Y, Fujikura K, Hashimoto J (2002) Molecular taxonomy of vestimentiferans of the western Pacific and their phylogenetic relationship to species of the eastern Pacific. II. Families Escarpiidae and Arcovestiidae. Mar Biol 141:57–64
Kojima S, Ohta S, Yamamoto T, Yamaguchi T, Miura T, Fujiwara Y, Fujikura K, Hashimoto J (2003) Molecular taxonomy of vestimentiferans of the western Pacific, and their phylogenetic relationship to species of the eastern Pacific. III. Alaysia-like vestimentiferans and relationship among families. Mar Biol 142:625–635
Kojima S, Fujikura K, Okutani T (2004) Multiple trans-Pacific migrations of deep-sea vent/seep-endemic bivalves in the family Vesicomyidae. Mol Phylogenet Evol 32:396–406
Lutz RA, Jablonski D, Rhoads DC, Turner RD (1980) Larval dispersal of a deep-sea hydrothermal vent bivalve from the Galápagos Rift. Mar Biol 57:127–133
Lutz RA, Bouchet P, Jablonski D, Turner RD, Waren A (1986) Larval ecology of mollusks at deep-sea hydrothermal vents. Am Malac Bull 4:49–54
Mass PA, O’Mullan GD, Lutz RA, Vrijenhoek RC (1999) Genetic and morphometric characterization of mussels (Bivalvia: Mytilidae) from Mid-Atlantic Hydrothermal vents. Biol Bull 196:265–272
Miyazaki J-I, Shintaku M, Kyuno A, Fujiwara Y, Hashimoto J, Iwasaki H (2004) Phylogenetic relationships of deep-sea mussels of the genus Bathymodiolus (Bivalvia: Mytilidae). Mar Biol 144:527–535
Okutani T, Fujikura K, Sasaki T (2004a) Two new species of Bathymodiolus (Bivalvia: Mytilidae) from methane seeps on the Kuroshima Knoll off the Yaeyama Islands, southwestern Japan. Venus 63:97–110
Okutani T, Fujiwara Y, Fujikura K, Miyake H, Kawato M (2004b) A mass aggregation of the mussel Adipicola pacifica (Bovalvia: Mytilidae) on submerged whale bone. Venus 63:61–64
Olu K, Duperret A, Sibuet M, Foucher J-P, Fiala-Medioni A (1996) Structure and distribution of cold seep communities along the Peruvian active margin: relationship to geological and fluid patterns. Mar Ecol Prog Ser 132:109–125
Pradillon F, Shillito B, Young CM, Gaill F (2001) Developmental arrest in vent worm embryos. Nature 413:698–699
Swofford DL (2002) PAUP*: phylogenetic analysis using parsimony (and Other Methods), version 4.0 bata 10. Sinauer Associates, Sunderland
Van Dover CL, Humphris SE, Fornari D, Cavanaugh CM, Collier R, Goffredi SK, Hashimoto J, Lilley MD, Reysenbach AL, Shank TM, Von Damm KL, Banta A, Gallant RM, Gotz D, Green D, Hall J, Harmer TL, Hurtado LA, Johnson P, McKiness ZP, Meredith C, Olson E, Pan IL, Turnipseed M, Won Y, Young III CR, Vrijenhoek RC (2001) Biogeography and ecological setting of Indian Ocean hydrothermal vents. Science 294:818–823
Vrijenhoek RC (1997) Gene flow and genetic diversity in naturally fragmented metapopulations of deep-sea hydrothermal vent animals. J Hered 88:285–293
Watanabe H, Tsuchida S, Fujikura K, Yamamoto H, Inagaki F, Kyo M, Kojima S (2005) Population history associated with hydrothermal vent activity inferred from genetic structure of neoverrucid barnacles around Japan. Mar Ecol Prog Ser 288:233–240
Won Y, Hallam SJ, O’Mullan GD, Pan IL, Buck KR, Vrijenhoek RC (2003) Environmental acquisition of thiotrophic endosymbionts by deep-sea mussels of the genus Bathymodiolus. Appl Environ Microbiol 69:6785–6792
Yamanaka T, Mizota C, Maki Y, Fujikura K, Chiba H (2000) Sulfur isotope composition of soft tissues of deep-sea mussels, Bathymodiolus spp., in Japanese waters. Benthos Res 55:63–68
Yamanaka T, Mizota C, Fujiwara Y, Chiba H, Hashimoto J, Gamo T, Okudaira T (2003) Sulfur-isotopic composition of the deep-sea mussel Bathymodiolus marisindicus from currently active hydrothermal vents in the Indian Ocean. J Mar Biol Ass UK 83:841–848
Acknowledgements
We wish to express our thanks to Drs. Shigeaki Kojima, Takashi Okutani, Chitoshi Mizota, and Motoo Utsumi for their useful advice and support throughout this work. We are also grateful to Drs. Nobuhiro Minaka and Hirohisa Kishino for helpful advice on phylogenetic analyses. Thanks are also extended to the operation teams of the submersibles “Shinkai 2000”, “Shinkai 6500”, “Dolphin 3K”, “Hyper Dolphin” and “Kaiko” and the officers and crew of the support vessels “Natsushima”, “Yokosuka” and “ Kairei” for their help in collecting samples. This study is supported in part by a grant from the Research Institute of Marine Invertebrates and grants from the Ministry of Education, Culture, Sports, Science and Technology of Japan (nos. 12NP0201 and 80229830).
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Communicated by S. Nishida, Tokyo
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Iwasaki, H., Kyuno, A., Shintaku, M. et al. Evolutionary relationships of deep-sea mussels inferred by mitochondrial DNA sequences. Mar Biol 149, 1111–1122 (2006). https://doi.org/10.1007/s00227-006-0268-6
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DOI: https://doi.org/10.1007/s00227-006-0268-6