Dispersal Ability and Genetic Structure in Mytilid Mussels of Whale-Fall Communities

Youki Fukasawa¹, Haruna Kobayashi-Iwatani², Masaru Kawato³, Hideki Kobayashi⁴, Yoshihiro Fujiwara³, Jun-Ichi Miyazaki^2*

¹Graduate School of Medical and Engineering Science Department of Education, University of Yamanashi, Kofu, Japan.
²Faculty of Education and Human Sciences, University of Yamanashi, Kofu, Japan.
³Department of Marine Biodiversity Research, Japan Agency for Marine-Earth Science and Technology, Yokosuka, Japan.
⁴Department of Environmental Geochemical Cycle Research, Japan Agency for Marine-Earth Science and Technology, Yokosuka, Japan.

DOI: 10.4236/ojms.2015.53025                

Abstract

Since organic falls are ephemeral and distributed sporadically, organisms in organic-fall communities must acquire high dispersal ability to migrate from one organic fall to another. However, the dispersal ability of obligate organic-fall organisms has not been investigated thoroughly and the stability of the genetic structure of their communities is unknown. In this study, in order to elucidate the dispersal ability and genetic structure in the organic-fall communities, we carried out population genetic analyses based on sequences of mitochondrial NADH dehydrogenase subunit 4 in two mytilid mussels. Adipicola pacifica was obtained from whale and cow bones artificially settled in Japanese waters off Cape Noma (CN) and in the Nansei-Shoto Trench (NS) and Sagami Bay (SB), and Benthomodiolus geikotsucola from natural whale bones in the Torishima Seamount (TS); both species are symbiotic with chemoautotrophic bacteria. Genetic differentiation (F_st) indicated almost no annual change in genetic structure between 2003, 2004, 2005, and 2007 collections of A. pacificafrom CN (depth 225 - 229 m), although the 2010 collection had somewhat different genetic structure from the others. Similarly, there was not significant genetic differentiation between 1993 and 2005 collections of B.geikotsucola from TS (depth 4020 m). The F_st and gene bidirectional mean rate of gene flow (Nm) indicated high gene flow and no significant genetic differentiation between A. pacifica specimens collected from CN, NS, and SB. The results suggest that the genetic structure is stable and A. pacifica has high dispersal ability. The mismatch distribution suggests that A. pacificaexpanded their distribution from SB to NS via CN, as expansion time (τ = 2ut) decreased from SB to CN and NS.

Keywords

Chemosynthesis-Based Community, Mitochondrial DNA, Organic Falls, Stepping Stone Hypothesis

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1]	Corliss, J.B. and Ballard, R.D. (1977) Oases of Life in the Cold Abyss. National Geographic, 152, 440-453.
[2]	Lonsdale, P. (1977) Clustering of Suspension-Feeding Macrobenthos near Abyssal Hydrothermal Vents at Oceanic Spreading Centers. Deep Sea Research, 24, 857-863. http://dx.doi.org/10.1016/0146-6291(77)90478-7
[3]	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. http://dx.doi.org/10.1126/science.226.4677.965
[4]	Kennicutt II, M.C., Brooks, J.M., Bidigare, R.R., Fay, R.A., Wade T.L., et al. (1985) Vent-Type Taxa in a Hydrocarbon Seep Region on the Louisiana Slope. Nature, 317, 351-353. http://dx.doi.org/10.1038/317351a0
[5]	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. http://dx.doi.org/10.1038/341027a0
[6]	Smith, C.R. and Baco, A.R. (2003) Ecology of Whale Falls at the Deep-Sea Floor. Oceanography and Marine Biology, an Annual Review, 41, 311-354.
[7]	Okutani, T., Fujiwara, Y., Fujikura, K., Miyake, H. and Kawato, M. (2003) A Mass Aggregation of the Mussel Adipicola pacifica (Bivalvia, Mytilidae) on Submerged Whale Bones. The Malacological Society of Japan, 63, 61-64.
[8]	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. http://dx.doi.org/10.1111/j.1439-0485.2007.00150.x
[9]	Naganuma, T., Wada, H. and Fujioka, K. (1996) Biological Community and Sediment Fatty Acids Associated with the Deep-Sea Whale Skeleton at the Torishima Seamount. Journal of Oceanography, 52, 1-15. http://dx.doi.org/10.1007/BF02236529
[10]	Okutani, T. and Miyazaki, J.-I. (2007) Benthomodiolus geikotsucola n. sp.: A Mussel Colonizing Deep-Sea Whale Bones in the Northwest Pacific (Bivalvia: Mytilidae). Venus, 66, 49-55.
[11]	Jollivet, D. (1996) Specific and Genetic Diversity at Deep-Sea Hydrothermal Vents: An Overview. Biodiversity and Conservation, 5, 1619-1653. http://dx.doi.org/10.1007/BF00052119
[12]	Hashimoto, J. and Okutani, T. (1994) Four New Mytilid Mussels Associated with Deepsea Chemosynthetic Communities around Japan. Venus, 53, 61-83.
[13]	Miyazaki, J.-I., Beppu, S., Kajio, S., Dobashi, A., Kawato, M., et al. (2013) Dispersal Ability and Environmental Adaptability of Deap-Sea Mussels Bathymodiolus (Mytilidae: Bathymodiolinae). Open Journal of Marine Science, 3, 31-39. http://dx.doi.org/10.4236/ojms.2013.31003
[14]	Kyuno, A., Shintaku, M., Fujita, Y., Matsumoto, H., Utsumi, M., et al. (2009) Dispersal and Differentiation of Deep-Sea Mussels of the Genus Bathymodiolus (Mytilidae, Bathymodiolinae). Journal of Marine Biology, 2009, Article ID: 625672.
[15]	Distel, D.L., Baco, A.R., Chuang, E., Morrill, W., Cavanaugh, C. and Smith, C.R. (2000) Marine Ecology: Do Mussels Take Wooden Steps to Deep-Sea Vents? Nature, 403, 725-726. http://dx.doi.org/10.1038/35001667
[16]	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. http://dx.doi.org/10.1371/journal.pone.0010363
[17]	Lorion, J., Kiel, S., Faure, B., Kawato, M., Ho, S.Y., et al. (2013) Adaptive Radiation of Chemosymbiotic Deep-Sea Mussels. Proceedings of the Royal Society of London B, 280, 1243. http://dx.doi.org/10.1098/rspb.2013.1243
[18]	Fujioka, K., Wada, H. and Okano, H. (1993) Torishima Whale Bone Deep-Sea Animal Community Assemblage—New Finding by Shinkai 6500. Journal of Geography, 102, 507-517. (In Japanese)
[19]	Wada, H. (1993) Torishima Whale Bone Animal Community (TOWBAC). Shizuoka Chigaku (Shizuoka Geology), 67, 1-3. (In Japanese with color plates).
[20]	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. http://dx.doi.org/10.1093/molbev/mst197
[21]	Excoffier, L. and Lischer, H.E.L. (2010) Arlequin Suite Ver 3.5: A New Series of Programs to Perform Population Genetics Analyses under Linux and Windows. Molecular Ecology Resources, 10, 564-567. http://dx.doi.org/10.1111/j.1755-0998.2010.02847.x
[22]	Amon, D.J. (2013) Bone-Eating Worms and Wood-Eating Bivalves: Characterising the Ecology of Deep-Sea Organic Falls from Multiple Ocean Basins. Ph.D. Thesis, University of Southampton Press, Southampton, 1-186.
[23]	Thubaut, J., Corbari, L., Gros, O., Duperron, S., Couloux, A., et al. (2013) Integrative Biology of Idas iwatakii (Habe, 1958), a “Model Species” Associated with Sunken Organic Substrates. PLoS ONE, 8, e69680. http://dx.doi.org/10.1371/journal.pone.0069680