Advertisement

Marine Biology

, Volume 156, Issue 5, pp 901–911 | Cite as

Geographical genetic structure and phylogeography of the Sargassum horneri/filicinum complex in Japan, based on the mitochondrial cox3 haplotype

  • Shinya Uwai
  • K. Kogame
  • G. Yoshida
  • H. Kawai
  • T. Ajisaka
Original Paper

Abstract

The genetic structure and phylogeography of the brown seaweed Sargassum horneri/filicinum complex in Japan were studied based on the mitochondrial cox3 haplotype. The cox3 haplotypes found were divided into three clades in a statistical parsimony network, among which there were large numbers of steps. Contrary to the reported large amount of drifting S. horneri along the Japanese coast, the three clades were dividedly distributed on the Japanese coast: the northern Pacific, the central Pacific, and western Japan. The western Japan S. horneri had haplotypes that were phylogenetically closer to those of S. filicinum than to the northern and central Pacific S. horneri populations. The S. filicinum populations were included within the western Japan clade and grouped together with the S. horneri samples from western Japan. Taken together with the unstable morphological diagnosis, this result suggests that S. filicinum should be reduced into a synonymy of S. horneri. The TMRCA analysis suggested that the divergence time of each clade may go back to the last interglacial period and a skyline plot suggested that the last glacial maximum had only a small effect on the population size of S. horneri. The geographic subdivision of the three groups, in spite of a large amount of drifting mats, suggests a limited contribution of drifting mats to gene flow on a large geographic scale. On a small geographic scale, a small number of haplotypes were shared between S. horneri-type and S. filicinum-type populations. This result suggests that populations of these two types are partially, though not completely, isolated from each other, possibly by selfing in S. filicinum-type populations or by a difference in peak reproduction.

Keywords

Tsushima Current Bayesian Skyline Plot Japanese Coast Small Geographic Scale Japan Coast 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

We would like to express our sincere gratitude to the late Professor emeritus Takeo Okuda who re-recognized S. filicinum and gave us many suggestions at the beginning of this study. We are also grateful for the critical comments to our manuscript by J.A. Coyer. We also thank to following for their help in sampling; M. Aoki, Y. Haga, M. Iima, A. Kijima, S. Kirihara, T. Komatsu, K. Kuwano, A. Mikami, H. Shimabukuro, A. Tanaka, K. Tatsukawa, R. Terada, and W.D. Wang.

References

  1. Aguilar-Rosas LE, Aguilar-Rosas R, Kawai H, Uwai S, Valenzuela-Espinoza E (2007) New record of Sargassum filicinum Harvey (Fucales, Phaeophyceae) in the Pacific Coast of Mexico. Algae 22:17–21CrossRefGoogle Scholar
  2. Ajisaka T, Uwai S (2005) On the morphological variations of vesicles and receptacles in Sargassum horneri/filicinum-group. Kaiyo Mon 37:460–465 (in Japanese)Google Scholar
  3. Avise JC (2000) Phylogeography. The history and formation of species. Harvard University Press, Cambridge, Massachusetts, LondonGoogle Scholar
  4. Chinzei K, Fujioka K, Kitazono H, Koizumi I, Oba T, Oda M, Okada H, Sakai T, Tanimura Y (1987) Postglacial environmental change of the Pacific Ocean off the coasts of central Japan. Mar Micropaleontol 11:273–291. doi: https://doi.org/10.1016/0377-8398(87)90002-8 CrossRefGoogle Scholar
  5. Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659. doi: https://doi.org/10.1046/j.1365-294x.2000.01020.x CrossRefGoogle Scholar
  6. Comes HP, Kadereit J (1998) The effect of Quaternary climatic changes on the plant distribution and evolution. Trends Plant Sci 3:432–438. doi: https://doi.org/10.1016/S1360-1385(98)01327-2 CrossRefGoogle Scholar
  7. Coyer JA, Peters AF, Stam WT, Olsen JL (2003) Post-ice age recolonization and differentiation of Fucus serratus L. (Phaeophyceae; Fucales) populations in Northern Europe. Mol Ecol 12:1817–1829. doi: https://doi.org/10.1046/j.1365-294X.2003.01850.x CrossRefGoogle Scholar
  8. Drummond AJ, Rambaut A, Shapiro B, Pybus OG (2005) Bayesian coalescent inference of past population dynamics from molecular sequences. Mol Biol Evol 22:1185–1192. doi: https://doi.org/10.1093/molbev/msi103 CrossRefGoogle Scholar
  9. Dupanloup I, Schneider S, Excoffier L (2002) A simulated annealing approach to define the genetic structure of populations. Mol Ecol 11:2571–2581. doi: https://doi.org/10.1046/j.1365-294X.2002.01650.x CrossRefGoogle Scholar
  10. Engel C, Daguin C, Serrao EA (2005) Genetic entities and mating system in hermaphroditic Fucus spiralis and its close dioecious relative F. vesiculosus (Fucaceae, Phaeophyceae). Mol Ecol 14:2003–2046. doi: https://doi.org/10.1111/j.1365-294X.2005.02558.x CrossRefGoogle Scholar
  11. Engelen AH, Olsen JL, Breeman AM, Stam WT (2001) Genetic differentiation in Sargassum polyceratium (Fucales: Phaeophyceae) around the island of Curaçao (Netherlands, Antilles). Mar Biol (Berl) 139:267–277. doi: https://doi.org/10.1007/s002270100586 CrossRefGoogle Scholar
  12. Gorbarenko SA, Southon JR (2000) Detailed Japan Sea paleoceanography during the last 25 kyr; constrains from AMS dating and δ18O of planktonic foraminifera. Palaeogeogr Palaeoclimatol Palaeoecol 156:177–193. doi: https://doi.org/10.1016/S0031-0182(99)00137-6 CrossRefGoogle Scholar
  13. Helmuth B, Veit RR, Holberton R (1994) Long-distance dispersal of a subarctic brooding bivalve (Gaimardia trapesina) by kelp-rafting. Mar Biol (Berl) 120:421–426. doi: https://doi.org/10.1007/BF00680216 CrossRefGoogle Scholar
  14. Hendry AP, Day T (2005) Population structure attributable to reproductive time: isolation by time and adaptation by time. Mol Ecol 14:901–916. doi: https://doi.org/10.1111/j.1365-294X.2005.02480.x CrossRefGoogle Scholar
  15. Hewitt GM (1996) Some genetic consequence of ice age, and their role in divergence and speciation. Biol J Linn Soc Lond 58:247–276CrossRefGoogle Scholar
  16. Hoarau G, Coyer JA, Veldsink JH, Stam WT, Olsen JL (2007) Glacial refugia and recolonization pathways in the brown seaweed Fucus serratus. Mol Ecol 16:3606–3616. doi: https://doi.org/10.1111/j.1365-294X.2007.03408.x CrossRefGoogle Scholar
  17. Huelsenbeck JP, Ronquist F (2001) MRBAYES: Baysian inference of phylogeny. Bioinfomatics 17:754–755. doi: https://doi.org/10.1093/bioinformatics/17.8.754 CrossRefGoogle Scholar
  18. Ijiri A, Wang L, Oba T, Kawahata H, Huang C-Y, Huang C-Y (2005) Paleoenvironmental changes in the northern area of the East China Sea during the past 42,000 years. Palaeogeogr Palaeoclimatol Palaeoecol 219:239–261. doi: https://doi.org/10.1016/j.palaeo.2004.12.028 CrossRefGoogle Scholar
  19. Kogame K, Uwai S, Shimada S, Masuda M (2005) A study of sexual and asexual populations of Scytosiphon lomentaria (Scytosiphonaceae, Phaeophyceae) in Hokkaido, northern Japan, using molecular markers. Eur J Phycol 40:313–322. doi: https://doi.org/10.1080/09670260500193008 CrossRefGoogle Scholar
  20. Kojima S, Segawa R, Hayashi I (1997) Genetic differentiation among populations of the Japanese turban shell Turbo (Batillus) cornutus corresponding to warm currents. Mar Ecol Prog Ser 150:149–155. doi: https://doi.org/10.3354/meps150149 CrossRefGoogle Scholar
  21. Kojima S, Hayashi I, Kim D, Iijima A, Furuta T (2004) Phylogeography of an intertidal direct-developing gastropod Batillaria cumingi around the Japanese islands. Mar Ecol Prog Ser 276:161–172. doi: https://doi.org/10.3354/meps276161 CrossRefGoogle Scholar
  22. Komatsu T, Tatsukawa K, Filippi JB, Sagawa T, Matsubaga D, Mikami A, Ishida K, Ajisaka T, Tanaka K, Aoki M, Wang W-D, Liu H-F, Zhang S-D, Zhou M-D, Sugimoto T (2007) Distribution of drifting seaweeds in eastern East China Sea. J Mar Syst 67:245–252. doi: https://doi.org/10.1016/j.jmarsys.2006.05.018 CrossRefGoogle Scholar
  23. Miller KA, Engel J, Uwai S, Kawai H (2007) First Report of the Asian Seaweed Sargassum filicinum Harvey (Fucales) in California, USA. Biol Invasions 9:609–613. doi: https://doi.org/10.1007/s10530-006-9060-2 CrossRefGoogle Scholar
  24. Oba T, Murayama M (2004) Sea-surface temperature and salinity changes in the northwest Pacific since the Last Glacial Maximum. J Quat Sci 19:335–346. doi: https://doi.org/10.1002/jqs.843 CrossRefGoogle Scholar
  25. Oba T, Kato M, Kitazato H, Koizumi I, Omura A, Sakai T, Takayama T (1991) Paleoenvironmental changes in the Japan Sea during the last 85,000 years. Paleoceanography 6:499–518. doi: https://doi.org/10.1029/91PA00560 CrossRefGoogle Scholar
  26. Ohno M (1984) Observation on the floating seaweed on the near-shore waters of the southern Japan. Hydrobiologia 116/117:408–412. doi: https://doi.org/10.1007/BF00027711 CrossRefGoogle Scholar
  27. Okuda T (1977) Sargassum filicinum; its new findings in sexuality and distribution around Japan. Bull Jap Soc Phycol 25(Suppl):265–269Google Scholar
  28. Okuda T (1987) Monoecism and autumn-fruiting of Sargassum horneri. Jap J Phycol 35:221–225 (in Japanese with English summary)Google Scholar
  29. Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817–818. doi: https://doi.org/10.1093/bioinformatics/14.9.817 CrossRefGoogle Scholar
  30. Posada D, Crandall KA, Templeton AR (2000) GEODIS: a program for cladistic nested analysis of the geographical distribution of genetic haplotypes. Mol Ecol 9:487–488. doi: https://doi.org/10.1046/j.1365-294x.2000.00887.x CrossRefGoogle Scholar
  31. Reed DC, Laur DR, Abeling AW (1988) Variation in algal dispersal and recruitment: the importance of episodic event. Ecol Monogr 58:321–335. doi: https://doi.org/10.2307/1942543 CrossRefGoogle Scholar
  32. Sawada T (1955) Some observations on Sargassum filicinum Harvey. Sci Bull Fac Agr Kyushu Univ 15:71–76 (in Japanese with English abstract)Google Scholar
  33. Schneider S, Roessli D, Excoffier L (2000) ARLEQUIN: a software for population genetics data analysis. ver. 2.00. Genetics and Biometry Lab, Department of Anthropology, University of GenevaGoogle Scholar
  34. Stieger V, Horiguch T, Yoshida T, Coleman AW, Masuda M (2003) Phylogenetic relationships within the genus Sargassum (Fucales, Phaeophyceae), inferred from ITS-2 nrDNA, with an emphasis on the taxonomic subdivision of the genus. Phycol Res 51:1–10. doi: https://doi.org/10.1111/j.1440-1835.2003.tb00164.x CrossRefGoogle Scholar
  35. Swofford DL (2002) PAUP*: phylogenetic analysis using parsimony (and other methods). ver. 4.0b. Sinauer Associates, Sunderland, MassachusettsGoogle Scholar
  36. Taberlet P, Fumagalli L, Wust-Saucy A-G (1998) Comparative phylogeography and postglacial colonization routes in Europe. Mol Ecol 7:453–464. doi: https://doi.org/10.1046/j.1365-294x.1998.00289.x CrossRefGoogle Scholar
  37. Takahata N, Nei M (1985) Gene genealogy and variance of interpopulational nucleotide differences. Genetics 110:325–344PubMedPubMedCentralGoogle Scholar
  38. Templeton AR (1998) Nested clade analyses of phylogeographic data: testing hypotheses about gene flow and population history. Mol Ecol 7:381–397. doi: https://doi.org/10.1046/j.1365-294x.1998.00308.x CrossRefGoogle Scholar
  39. Templeton AR, Routman E, Phillips CA (1995) Separating population structure from population history: a cladistic analysis of the geographical distribution of mitochondrial DNA haplotypes in the tiger salamander, Ambystoma tigrinum. Genetics 140:767–782PubMedPubMedCentralGoogle Scholar
  40. Uchida T (1993) The life cycle of Sargassum horneri (Phaeophyceae) in laboratory culture. J Phycol 29:231–235. doi: https://doi.org/10.1111/j.0022-3646.1993.00231.x CrossRefGoogle Scholar
  41. Uehara S, Taggart CT, Mitani T, Suthers IM (2006) The abundance of juvenile yellowtail (Seriola quinqueradiata) near the Kuroshio: the roles of drifting seaweed and regional hydrography. Fish Oceanogr 15:351–362. doi: https://doi.org/10.1111/j.1365-2419.2005.00382.x CrossRefGoogle Scholar
  42. Ujiie H, Ujiie Y (1999) Late quaternary course changes if the Kuroshio Current in the Ryukyu Arc region, northern Pacific Ocean. Mar Micropaleontol 37:23–40. doi: https://doi.org/10.1016/S0377-8398(99)00010-9 CrossRefGoogle Scholar
  43. Uwai S, Yotsukura N, Serisawa Y, Muraoka D, Hiraoka M, Kogame K (2006) Intraspecific genetic diversity of Undaria pinnatifida in Japan, based on the mitochondrial cox3 gene and the ITS1 of nrDNA. Hydrobiologia 553:345–356. doi: https://doi.org/10.1007/s10750-005-0883-0 CrossRefGoogle Scholar
  44. Wu C-I (1991) Inferences of species phylogeny in relation to segregation of ancient polymorphisms. Genetics 127:429–435PubMedPubMedCentralGoogle Scholar
  45. Xu X, Oda M (1999) Surface-water evolution of the eastern East China Sea during the last 36,000 years. Mar Geol 156:285–304. doi: https://doi.org/10.1016/S0025-3227(98)00183-2 CrossRefGoogle Scholar
  46. Yashima K (1994) A geomorphological study of the caldrons in the Seto Inland Sea. Rep Hydrogr Res 30:237–327 (in Japanese with English summary)Google Scholar
  47. Yoshida T (1963) Studies on the distribution and drift of the floating seaweeds. Bull Tohoku Reg Fish Lab 23:141–186 (in Japanese with English summery)Google Scholar
  48. Yoshida T (1983) Japanese species of Sargassum subgenus Bactrophycus (Phaeophyceae, Fucales). J Fac Sci Hokkaido Univ Ser V Bot 13:99–246Google Scholar
  49. Yoshida G, Arima S, Terawaki T (1998) Growth and maturation of the ‘autumn-fruiting type’ of Sargassum horneri (Fucales, Phaeophyceae) and comparisons with the ‘spring fruiting type’. Phycol Res 46:183–189. doi: https://doi.org/10.1111/j.1440-1835.1998.tb00112.x CrossRefGoogle Scholar
  50. Yoshida G, Murase N, Arai S, Terawaki T (2004) Ecotypic differentiation in maturation seasonality among Srgassum horneri (Fucales, Phaeophyta) populations in Hiroshima Bay, Seto Inland Sea, Japan. Phycologia 43:703–710CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Shinya Uwai
    • 1
    • 5
  • K. Kogame
    • 2
  • G. Yoshida
    • 3
  • H. Kawai
    • 1
  • T. Ajisaka
    • 4
  1. 1.Kobe University Research Center for Inland SeasKobeJapan
  2. 2.Department of Natural History Sciences, Faculty of ScienceHokkaido UniversitySapporoJapan
  3. 3.National Research Institute of Fisheries and Environment of Inland Sea, Fisheries Research AgencyHiroshimaJapan
  4. 4.Division of Applied Bioscience, Graduate School of AgricultureKyoto UniversityKyotoJapan
  5. 5.Department of Environmental Science, Faculty of ScienceNiigata UniversityNiigataJapan

Personalised recommendations