In order to invade and adapt to deep-sea environments, shallow-water organisms have to acquire tolerance to high hydrostatic pressure, low water temperature, toxic methane and hydrogen sulfide, and feeding strategies not relying on photosynthetic products. Our previous study showed that the “evolutionary stepping stone hypothe-sis”, which assumes that organic falls can act as stepping-stones to connect shallow sea with deep sea, was supported in Mytilidae. However, it is not known whether other bivalves constituting chemosynthetic communities experienced the same evolutionary process or different processes from mytilid mussels. Therefore, here, we performed phylogenetic analyses by sequencing the nuclear 18S rRNA and mitochondrial COI genes of solemyid and thyasirid bivalves. In Solemyidae, the two genera Solemya and Acharax formed each clade, the latter of which was divided into three subgroups. The Solemya clade and one of the Acharax subgroups diverged in the order of shallow-sea residents, whale-bone residents, and deep-sea vent/seep residents, which supported the “evolutionary stepping stone hypothesis”. Furthermore, in Thyasiridae, the two genera Thyasira and Maorithyas formed a paraphyletic group and the other genera, Adontorhina , Axinopsis , Axinulus , Leptaxinus , and Mendicula , formed a clade. The “evolu-tionary stepping stone hypothesis” was not seemingly supported in the other lineages of Solemyidae and Thyasiridae.
KeywordsWhale BoneDeep SeaNuclear DNAMitochondrial DNAStepping Stone Hypothesis
Corliss, J.B. and Ballard, R.D. (1977) Oases of Life in the Cold Abyss. National Geographic, 152, 440-453.
Lonsdale, P. (1977) Clustering of Suspension-Feeding Macrobenthos near Abyssal Hydrothermal Vents at Oceanic Spreading Centers. Deep Sea Research, 24, 857-863. https://doi.org/10.1016/0146-6291(77)90478-7
Paull, C.K., Hecker, B., Commeau, R., Freeman-Lynde, R.P., Neumann, C., et al. (1984) Biological Communities at the Florida Escarpment Resemble Hydrothermal Vent Taxa. Science, 226, 965-967. https://doi.org/10.1126/science.226.4677.965
Kennicutt, M.C.II, Brooks, J.M., Bidigare, R.R., Fay, R.A., Wade, T.L. and McDonald, T.J. (1985) Vent-Type Taxa in a Hydrocarbon Seep Region on the Louisiana Slope. Nature, 317, 351-353. https://doi.org/10.1038/317351a0
Smith, C.R., Kukert, R.A.,Wheatcroft, R.A., Jumars, P.A. and Deming, J.W. (1989) Vent Fauna on Whale Remains. Nature, 341, 27-28. https://doi.org/10.1038/341027a0
Distel, D.L., Baco, A.R., Chuang, E., Morrill, W., Cavanaugh, C., et al. (2000) Marine Ecology: Do Mussels Take Wooden Steps to Deep-Sea Vents? Nature, 403, 725-726. https://doi.org/10.1038/35001667
Miyazaki, J.-I., de Oliveria Martins, L., Fujita, Y., Matsumoto, H. and Fujiwara, Y. (2010) Evolutionary Process of Deep-Sea Bathymodiolus Mussels. PLoS ONE, 5, e10363. https://doi.org/10.1371/journal.pone.0010363
Lorion, J., Kiel, S., Faure, B., Kawato, M., Ho, S.Y.W., et al. (2013) Adaptive Radiation of Chemosymbiotic Deep-Sea Mussels. Proceedings of the Royal Society B: Biological Sciences, 280, No. 1770. https://doi.org/10.1098/rspb.2013.1243
Kyuno, A., Shintaku, M., Fujita, Y., Matsumoto, H., Utsumi, M., Watanabe, H., Fujiwara, Y. and Miyazaki, J.-I. (2009) Dispersal and Differentiation of Deep-Sea Mussels of the GenusBathymodiolus (Mytilidae, Bathymodiolinae). Journal of Marine Biology, 2009, Article ID: 625672. https://doi.org/10.1155/2009/625672
Fukasawa, Y., Kobayashi-Iwatani, H., Kawato, M., Kobayashi, H., Fujiwara, Y., et al. (2015) Dispersal Ability and Genetic Structure in Mytilid Mussels of Whale-Fall Communities. Open Journal of Marine Science, 5, 295-305. https://doi.org/10.4236/ojms.2015.53025
Pojeta, J.J. (1988) The Origin and Paleozoic Diversification of Solemyoid Pelecypods. New Mexico Bureau of Mines and Mineral Resources, Memoir 44, 201-271.
Bailey, J.B. (2011) Paleobiology, Paleoecology, and Systematics of Solemyidae (Mollusca: Bivalvia: Protobranchia) from the Mazon Creek Lagerstatte, Pennsylvanian of Illinois. Bulletins of American Paleontology, 382, 1-72.
Sasaki, T., Okutani, T. and Fujikura, K. (2005) Molluscs from Hydrothermal Vents and Cold Seeps in Japan: A Review of Taxa Recorded in Twenty Recent Years (1984-2004). Venus, 64, 87-133.
Fujiwara, Y., Kawato, M., Yamamoto, T., Yamanaka, T., Sato-Okoshi, W., et al. (2007) Three-Year Investigations into Sperm Whale-Fall Ecosystems in Japan. Marine Ecology, 28, 219-232. https://doi.org/10.1111/j.1439-0485.2007.00150.x
Dubilier, N., Bergin, C. and Lott, C. (2008) Symbiotic Diversity in Marine Animals: The Art of Harnessing Chemosynthesis. Nature Reviews Microbiology, 6, 725-740. https://doi.org/10.1038/nrmicro1992
Fisher, C.R. and Childress, J.J. (1986) Translocation of Fixed Carbon from Symbiotic Bacteria to Host tissues in the Gutless Bivalve Solemya reidi. Marine Biology, 93, 59-68. https://doi.org/10.1007/BF00428655
Conway, N.M., Hows, B.L., McDowell Capuzzo, J.E., Turner, R.D. and Cavanaugh, C.M. (1992) Characterization and Site Description of Solemya borealis (Bivalvia; Solemyidae), Another Bivalve-Bacteria Symbiosis. Marine Biology, 112, 601-613. https://doi.org/10.1007/BF00346178
Krueger, D.M., Gustafson, R.G. and Cavanaugh, C.M. (1996) Vertical Transmission of Chemoautotrophic Symbionts in the Bivalve Solemya velum (Bivalvia: Protobranchia). Biological Bulletin, 190, 195-202. https://doi.org/10.2307/1542539
Barry, J.P., Buck, K.R., Goffredi, S.K. and Hashimoto, J. (2000) Ultrastructure Studies of Two Chemosynthetic Invertebrate-Bacterial Symbioses (Lamellibranchia sp. and Acharax sp.) from the Hatsushima Cold Seep in Sagami Bay, Japan. Journal of Deep Sea Research I, Biology, 16, 91-99.
Fujiwara, Y. (2003) Symbiotic Adaptation for Deeper Habitats in Chemosynthetic Environments. Journal of Geography, 112, 302-308. (In Japanese) https://doi.org/10.5026/jgeography.112.2_302
Imhoff, J.F., Sahling, H., Suling, J. and Kath, T. (2003) 16S rDNA-Based Phylogeny of Sulphur-Oxidising Bacterial Endosymbionts in Marine Bivalves from Cold-Seep Habitats. Marine Ecology Progress Series, 249, 39-51. https://doi.org/10.3354/meps249039
Yamanaka, T., Mizota, C., Matsuyama-Serisawa, K., Kakegawa, T., Miyazaki, J.-I., et al. (2008) Stable Isotopic Characterization of Carbon, Nitrogen and Sulfur Uptake of Acharax japonica from Central Japan. Plankton and Benthos Research, 3, 36-41. https://doi.org/10.3800/pbr.3.36
Taylor, J.D., Williams, S.T. and Glover, E.A. (2007) Evolutionary Relationships of the Bivalve Family Thyasiridae (Mollusca: Bivalvia), Monophyly and Superfamily Status. Journal of the Marine Biological Association of the United Kingdom, 87, 565-574. https://doi.org/10.1017/S0025315407054409
Kiel, S., Amano, K. and Jenkins, P.G. (2008) Bivalves from Cretaceous Cold-Seep Deposits on Hokkaido, Japan. Acta Palaeontologica Polonica, 53, 525-537. https://doi.org/10.4202/app.2008.0310
Hammer, O., Nakrem, H.A., Little, C.T.S., Hryniewicz, K., Sandy, M.R., et al. (2011) Hydrocarbon Seeps from Close to the Jurassic-Cretaceous Boundary, Svalbard. Palaeogeography, Palaeoclimatology, Palaeoecology, 306, 15-26. https://doi.org/10.1016/j.palaeo.2011.03.019
Passos, F.D., de Lima CuriMeserani, G. and Gros, O. (2007) Structural and Ultrastructural Analysis of the Gills in the Bacterial-Bearing Species Thyasira falklandica (Bivalvia, Mollusca). Zoomorphology, 126, 153-162. https://doi.org/10.1007/s00435-007-0034-4
Kauffman, E.G. (1967) Cretaceous Thyasira from the Western Interior of North America. Smithsonian Miscellaneous Collections, 152, 1-159.
Southward, E.C. (1986) Gill Symbionts in Thyasirids and Other Bivalve Molluscs. Journal of the Marine Biological Association of the United Kingdom, 66, 889-914. https://doi.org/10.1017/S0025315400048517
Fujiwara, Y., Kato, C., Masui, N., Fujikura, K. and Kojima, S. (2001) Dual Symbiosis in the Cold-Seep Thyasirid Clam Maorithyas hadalis from the Hadal Zone in the Japan Trench, Western Pacific. Marine Ecology Progress Series, 214, 151-159. https://doi.org/10.3354/meps214151
Dufour, S.C. (2005) Gill Anatomy and the Evolution of Symbiosis in the Bivalve Family Thyasiridae. The Biological Bulletin, 208, 200-212. https://doi.org/10.2307/3593152
Tamura, K., Stecher, G., Peterson, D., Filipski, A. and Kumar, S. (2013) MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0. Molecular Biology and Evolution, 30, 2725-2729. https://doi.org/10.1093/molbev/mst197
Swofford, D.L. (2002) PAUP: Phylogenetic Analysis Using Parsimony (and Other Methods), Version 4.0 Beta 10. Sinauer Associates, Sunderland.
Kimura, M. (1980) A Simple Method for Estimating Evolutionary Rate of Base Substitutions through Comparative Studies of Nucleotide Sequences. Journal of Molecular Evolution, 16, 111-120. https://doi.org/10.1007/BF01731581
Huelsenbeck, J.P., Ronquist, F., Nielsen, R. and Bollback, J.P. (2003) Bayesian Inference of Phylogeny and Its Impact on Evolutionary Biology. Science, 294, 2310-2314. https://doi.org/10.1126/science.1065889
Nylander, J.A.A. (2004) MrModeltest V 2. Programme Distributed by the Author. Evolutionary Biology Centre, Uppsala University, Uppsala.
Miya, M. and Nishida, M. (2000) Use of Mitogenomic Information in Teleostean Molecular Phylogenetics: A Tree-Based Exploration under the Maximum-Parsimony Optimality Criterion. Molecular Phylogenetics and Evolution, 17, 437-455. https://doi.org/10.1006/mpev.2000.0839
Held, C. (2000) Phylogeny and Biogeography of Serolid Isopods (Crustacea, Isopoda, Serolidae) and the Use of Ribosomal Expansion Segments in Molecular Systematics. Molecular Phylogeny and Evolution, 15, 165-178. https://doi.org/10.1006/mpev.1999.0739
Tyler, P.A., Young, C.M. and Clarke, A. (2000) Temperature and Pressure Tolerances of Embryos and Larvae of the Antarctic Sea Urchin Sterechinus neumayeri (Echinodermata: Echinoidea): Potential for Deep-Sea Invasion from High Latitudes. Marine Ecology Progress Series, 192, 173-180. https://doi.org/10.3354/meps192173
Brey T., Dahm C., Gorny M., Klages M., Stiller M., et al. (1996) Do Antarctic Benthic Invertebrates Show an Extended Level of Eurybathy? Antarctic Science, 8, 3-6. https://doi.org/10.1017/S0954102096000028
Giribet, G., Carranza, S., Baguna, J., Ruitort, M. and Ribera, C. (1996) First Molecular Evidence for the Existence of a Tardigrada + Arthropoda Clade. Molecular Biology and Evolution, 13, 76-84. https://doi.org/10.1093/oxfordjournals.molbev.a025573
Whiting, M.F., Carpenter, J.C., Wheeler, Q.D. and Wheeler, W.C.(1997) The Strepsiptera Problem: Phylogeny of the Holometabolous Insect Orders Inferred from 18S and 28S Ribosomal DNA Sequences and Morphology. Systematic Biology, 46, 1-68.
Folmer, O., Black, M., Hoeh, W., Lutz, R. and Vrijenhoek, R. (1994) DNA Primers for Amplification of Mitochondrial Cytochrome c Oxidase Subunit I from Diverse Metazoan Invertebrates. Molecular Marine Biology and Biotechnology, 3, 294-299.