Marine Biology

, Volume 160, Issue 6, pp 1407–1414 | Cite as

Asymmetric genetic exchange in the brown seaweed Sargassum fusiforme (Phaeophyceae) driven by oceanic currents

  • Zi-Min Hu
  • Jie Zhang
  • Juan Lopez-Bautista
  • De-Lin Duan
Original Paper
First Online:
Received:
Accepted:

Abstract

Geological phenomena (e.g. drastic sea level fluctuations during the Quaternary Ice Age in the Northern Hemisphere) have been demonstrated to intensively affect the biogeographic patterns and tempo-spatial compositions of genetic diversity of marine organisms. However, it is poorly understood whether contemporary factors such as oceanic surface currents have also shaped inter-regional population genetics of specific coastal marine flora, with or without limited dispersal capability. In this study, we determined mtDNA Cox1 gene sequences of the brown seaweed Sargassum fusiforme from nine populations along the Chinese coast and one population from the west coast of South Korea, in an effort to understand what factors are contributing to their current genetic structure and geographic distribution patterns. Genetic analyses indicated a deep genetic break between the Yellow-Bohai Sea (YBS) and the other two marginal seas, the East China Sea (ECS) and the South China Sea (SCS). In particular, the amount of genetic exchange from the SCS to each of the ECS and YBS was significantly higher than that from the opposite directions. Our analyses supports the hypothesis that biogeographic patterns of genetic variation in S. fusiforme are probably an interactive consequence of post-glacial colonization from two scattered refugia driven by the offshore Kuroshio Current and asymmetric gene flow among adjacent sea margins.

Keywords

Brown Seaweed Warm Current Kuroshio Current Genetic Connectivity Taiwan Warm Current 
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.
This is a preview of subscription content, log in to check access.

Notes

Acknowledgments

We thank engineer Ji-Dong Liu for his kind help on field collection. We are grateful to Michael Scott DePriest (The University of Alabama) for assistance to improve the English-writing and two anonymous reviewers for their valuable and constructive comments on the original version of this manuscript. This study was supported in part by National Natural Science Foundation of China (No. 31000103) granted to Z.M. Hu and the US National Science Foundation Assembling the Tree of Life Program (No. DEB-1036495) granted to JMLB.

Supplementary material

227_2013_2192_MOESM1_ESM.doc (39 kb)
Supplementary material 1 (DOC 39 kb)
227_2013_2192_MOESM2_ESM.pdf (9 kb)
Fig. S1 Plots of isolation by distance (IBD) analysis, a reduced major axis regression to calculate interpret and slope of genetic and geographic distance (Km). (Z = 21227.581, R2 = 0.174, r = 0.4175, one-sided P = 0.9580) (PDF 9 kb)
227_2013_2192_MOESM3_ESM.tif (1.2 mb)
Fig. S2 Posterior probability of effective population size (θ) for each of the three marginal-scale populations (TIFF 1252 kb)

References

  1. Barkley RA (1970) The Kuroshio current. Science 6:54–60Google Scholar
  2. Bouza N, Caujapé-Castells J, González-Pérez MA, Sosa PA (2006) Genetic structure of natural populations in the red alga Gelidium canariense (Celidiales, Rhodophyta) investigated by random amplified polymorphic DNA (RAPD) markers. J Phycol 42:304–311CrossRefGoogle Scholar
  3. Casteleyn G, Leliaert F, Backeljau T, Debeer AE, Kotaki Y, Rhodes L, Lundholm N, Sabbe K, Vyverman W (2010) Limits to gene flow in a cosmopolitan marine planktonic diatom. Proc Natl Acad Sci USA 107:12952–12957CrossRefGoogle Scholar
  4. Cheang CC, Chu KH, Ang PO (2008) Morphological and genetic variation in the populations of Sargassum hemiphyllum (Phaeophyceae) in the Northwestern Pacific. J Phycol 44:855–865CrossRefGoogle Scholar
  5. Cheang CC, Chu KH, Ang PO (2009) The phylogeography of Sargassum fusiforme (Fucales, Heterokontophyta) in the northwestern Pacific. Joint Annual Meetings of the American Society of Plant Biologists and the Phycological Society of America, pp. 63. Honolulu, Hawaii, 18–22 July 2009Google Scholar
  6. Cheang CC, Chu KH, Ang PO (2010) Phylogeography of the marine marcoalga Sargassum hemiphyullum (Phaeophyceae, Heterokontophyta) in the Northwestern Pacific. Mol Ecol 19:2933–2948CrossRefGoogle Scholar
  7. Cheng YP, Hwang SY, Lin TP (2005) Potential refugia in Taiwan revealed by the phylogeographical study of Castanopsis carlesii Hayata (Fagaceae). Mol Ecol 14:2075–2085CrossRefGoogle Scholar
  8. Deng OE, Hazel W (2010) Population structure and phylogeography of an acorn barnacle with induced defense and its gastropod predator in the Gulf of California. Mar Biol 157:1989–2000CrossRefGoogle Scholar
  9. Drummond AJ, Rambaut A, Shapiro B, Pybus OG (2005) Bayesian coalescent inference of past population dynamics from molecular sequences. Mol Biol Evol 22:1185–1192CrossRefGoogle Scholar
  10. Excoffier L, Laval G, Schneider S (2005) Arlequin version 3.0: an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50Google Scholar
  11. FAO Fisheries Proceedings (2008) FAO/NACA Regional workshop on the future of mariculture: a regional approach for responsible development in the Asia-Pacific region. In: Lovatelli A, Phillips MJ, Arthur JR and Yamamoto K (eds). Guangzhou, China, 7–11 March 2006Google Scholar
  12. Felsenstein J (1984) Distance methods for inferring phylogenies: a justification. Evolution 38:16–24CrossRefGoogle Scholar
  13. Felsenstein J (2006) Accuracy of coalescent likelihood estimates: do we need more sites, more sequences, or more loci? Mol Biol Evol 23:691–700CrossRefGoogle Scholar
  14. Harpending H (1994) Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution. Hum Biol 66:591–600Google Scholar
  15. He LJ, Zhang AB, Weese D, Zhu CD, Jiang CJ, Qiao ZG (2010) Late Pleistocene population expansion of Scylla paramamosain along the coast of China: a population dynamic response to the last interglacial sea level highstand. J Exp Mar Biol Ecol 38:520–528Google Scholar
  16. Hewitt GM (2004) Genetic consequences of climatic oscillations in the quaternary. Phil Trans Roy Soc Lond B 359:183–195CrossRefGoogle Scholar
  17. Hu ZM, Duan DL (2013) Insufficient geographical sampling could severely influence phylogeographic interpretations: comment on phylogeography of the seaweed Ishige okamurae (Phaeophyceae): evidence for glacial refugia in the northwest Pacific region (Lee et al. Mar Biol 159:1021-1028, 2012). Mar Biol. doi:  10.1007/s00227-013-2198-4 Google Scholar
  18. Hu JY, Kawamura H, Hong HS, Qi YQ (2000) A review of the currents in the South China Sea: seasonal circulation, South China Sea Warm Current and Kuroshio intrusion. J Oceanogr 56:607–624CrossRefGoogle Scholar
  19. Hu ZM, Zeng XQ, Wang AH, Shi CJ, Duan DL (2004) An efficient method for DNA isolation from red algae. J Appl Phycol 16:161–166CrossRefGoogle Scholar
  20. Hu ZM, Uwai S, Yu SH, Komatsu T, Ajisata T, Duan DL (2011) Phylogeographic heterogeneity of the brown alga Sargassum horneri (Fucaeae) in the northwestern Pacific in relation to late Pleistocene glaciation and tectonic configurations. Mol Ecol 20:3894–3909CrossRefGoogle Scholar
  21. Hwang EK, Cho YC, Sohn CH (1999) Reuse of holdfasts in Hizikia fusiformis cultivation. J Korean Fish Soc 32:112–116 (In Korea with English abstract)Google Scholar
  22. Jensen JL, Bohonak AJ, Kelley ST (2005) Isolation by distance, web service. BMC Genet 6:13CrossRefGoogle Scholar
  23. Johansson G, Sosa PA, Snoeijs P (2003) Genetic variability and level of differentiation in North Sea and Baltic Sea populations of the green alga Cldophora rupestris. Mar Biol 142:1019–1027Google Scholar
  24. 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 40:313–322CrossRefGoogle Scholar
  25. Kojima S, Kamimura S, Iijima A, Kimura T, Kurozumi T, Furota T (2006) Molecular phylogeny and population structure of tideland snails in the genus Cerithidea around Japan. Mar Biol 149:525–535CrossRefGoogle Scholar
  26. Kokita T, Nohara K (2011) Phylogeography and historical demography of the anadromous fish Leucopsarion petersii in relation to geological history and oceanography around the Japanese Archipelago. Mol Ecol 20:143–164CrossRefGoogle Scholar
  27. Komatsu T, Matsunaga D, Mikami A, Sagawa T, Boisnier E, Tatsukawa K, Aoki M, Ajisaka T, Uwai S, Tanaka K, Ishida K, Tanoue H, Sugimoto T (2008) Abundance of drifting seaweeds in eastern East China Sea. J Appl Phycol 20:801–809CrossRefGoogle Scholar
  28. Kuhner MK (2006) LAMARC 2.0: maximum likelihood and Bayesian estimation of population parameters. Bioinformatics 22:768–770CrossRefGoogle Scholar
  29. Lambeck K, Esat TM, Potter EK (2002) Links between climate and sea levels for the past three million years. Nature 419:199–206CrossRefGoogle Scholar
  30. Lee KM, Yang EC, Coyer JA, Zuccarello GC, Wang WL, Choi CG, Boo SM (2012) Phylogeography of the seaweed Ishige okamurae (Phaeophyceae): evidence for glacial refugia in the northwest Pacific region. Mar Biol 159:1021–1028CrossRefGoogle Scholar
  31. Liu SV, Kokita T, Dai CF (2008) Population genetic structure of the neon damselfish (Pomacentrus coelestis) in the northwestern Pacific Ocean. Mar Biol 154:745–753CrossRefGoogle Scholar
  32. Mach ME, Sbrocco EJ, Hice LA, Duffy TA, Conover DO, Barber PH (2011) Regional differentiation and post-glacial expansion of the Atlantic silverside, Menidia menidia, an annual fish with high dispersal potential. Mar Biol 158:515–530CrossRefGoogle Scholar
  33. Ohno M (1984) Observation on the floating seaweed on the near-shore waters of the southern Japan. Hydrobiologia 116(117):408–412CrossRefGoogle Scholar
  34. Olsen JL, Zechman FW, Hoarau G, Coyer JA, Stam WT, Valero M, Aberg P (2010) The phylogeographic architecture of the fucoid seaweed Ascophyllum nodosum: an intertidal “marine tree” and survivor of more than one glacial-interglacial cycle. J Biogeogra 37:842–856CrossRefGoogle Scholar
  35. Palumbi SR (1994) Genetic divergence, reproductive isolation and marine speciation. Annu Rev Ecol Syst 25:547–572CrossRefGoogle Scholar
  36. Pang SJ, Shan TF, Zhang ZH, Sun JZ (2008) Cultivation of the intertidal brown alga Hizikia fusiformis (Harvey) Okamura: mass production of zygote-derived seedlings under commercial cultivation conditions, a case study experience. Aquac Res 39:1408–1415CrossRefGoogle Scholar
  37. Petit RJ, El Mousadik A, Pons O (1998) Identifying populations for conservation on the basis of genetic markers. Conserv Biol 12:844–855CrossRefGoogle Scholar
  38. Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256CrossRefGoogle Scholar
  39. Rodriguez-Lanetty M, Hoegh-Guldberg O (2002) The phylogeography and connectivity of the latitudinally widespread coral Plesiastrea versipora in the Western Pacific. Mol Ecol 11:1177–1189CrossRefGoogle Scholar
  40. Russell AL, Goodman SM, Fiorentino I, Yoder AD (2008) Population genetic analysis of Myzopoda (Chiroptera: Myzopodidae) in Madagascar. J Mammal 89:209–221CrossRefGoogle Scholar
  41. Slatkin M (1993) Isolation by distance in equilibrium and nonequilibrium populations. Evolution 47:264–279CrossRefGoogle Scholar
  42. Tajima F (1989) Statistical methods for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595Google Scholar
  43. Tamura K, Peterson D, Peterson N, Stecher C, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739CrossRefGoogle Scholar
  44. Teske PR, Papadopoulos I, Newman BK, Dworschak PC, McQuaid CD, Barker NP (2008) Oceanic dispersal barriers, adaptation and larval retention: an interdisciplinary assessment of potential factors maintaining a phylogeographic break between sister lineages of an African prawn. BMC Evol Biol 8:34CrossRefGoogle Scholar
  45. Thiel M, Haye PA (2006) The ecology of rafting in the marine environment. III. Biogeographical and evolutionary consequences. Oceanogr Mar Biol Annu Rev 44:323–429Google Scholar
  46. Tittensor DP, Mora C, Jetz W, Lotze HK, Richard D, Berghe EV, Worm B (2010) Global patterns and predictions of marine biodiversity across taxa. Nature 466:1098–1101CrossRefGoogle Scholar
  47. Tseng CK (1984) Common Seaweeds of China. Science Press, Beijing, pp 1–318Google Scholar
  48. Tulchinsky AY, Norenburg JL, Turbeville JM (2012) Phylogeography of the marine interstitial nemertean Ototyphlonemertes parmula (Nemertea, Hoplonemertea) reveals cryptic diversity and high dispersal potential. Mar Biol 159:661–674CrossRefGoogle Scholar
  49. Vermeij G (1987) The dispersal barrier in the tropical Pacific: implications for molluscan speciation and extinction. Evolution 41:1046–1058CrossRefGoogle Scholar
  50. Voris HK (2000) Maps of Pleistocene sea levels in Southeast Asia: shorelines, river systems and time durations. J Biogeogr 27:1153–1167CrossRefGoogle Scholar
  51. Wang PX (1990) The ice-age Sea-status and problems. Quat Sci 2:111–124 (In Chinese with English abstract)Google Scholar
  52. Yoshida T (1963) Studies on the distribution and drift of the floating seaweeds. Bull Tohoku Reg Fish Res Lab 23:141–186 (In Japanese with English Abstract)Google Scholar
  53. Zou DH, Gao KS, Ruan ZX (2006) Seasonal pattern of reproduction of Hizikia fusiformis (Sargassaceae, Phaeophyta) from Nanao Island, Shantou, China. J Appl Phycol 18:195–201CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Zi-Min Hu
    • 1
    • 2
  • Jie Zhang
    • 1
    • 3
  • Juan Lopez-Bautista
    • 2
  • De-Lin Duan
    • 1
  1. 1.Institute of OceanologyChinese Academy of SciencesQingdaoChina
  2. 2.Department of Biological SciencesThe University of AlabamaTuscaloosaUSA
  3. 3.Graduate University of Chinese Academy of SciencesBeijingChina

Personalised recommendations