Abstract
Although benthic marine algae are essential components of marine coastal systems that have been influenced profoundly by past and present climate change, our knowledge of seaweed phylogeography is limited. The brown alga Ishige okamurae Yendo occurs in the northwest Pacific, where it occupies a characteristic belt in the exposed intertidal zone. To understand the patterns of genetic diversity and the evolutionary history of this species, we analyzed mitochondrial cox3 from 14 populations (221 individuals) throughout its range. The 17 haplotypes found in this study formed five distinct clades, indicating significant genetic structure. The high differentiation and number of unique (private) haplotypes may result from the recolonization of the species from glacial refugia. Three putative refugia, each with high genetic diversity, were identified: southern Korea (including Jeju Island), northern Taiwan, and central Pacific Japan. Recolonization of I. okamurae was probably determined by ocean currents and changes in sea level during the last glacial period.
Similar content being viewed by others
References
Ajisaka T (1989) Plurilocular sporangia and the development of plurispores in Ishige okamurae Yendo (Phaeophyceae) from the Kada coast, Wakayama Prefecture in Japan. Jap J Phycol 37:17–22
Avis JC (2009) Phylogeography: retrospect and prospect. J Biogeogr 36:3–15
Boo SM, Lee KM, Cho GY, Nelson W (2011) Colpomenia claytoniae (Scytosiphonaceae, Phaeophyceae) based on morphology and cox3 sequences. Bot Mar 54:159–167
Cho GY, Lee SH, Boo SM (2004) A new brown algal order, Ishigeales (Phaeophyceae), established on the basis of plastid protein-coding rbcL, psaA, and psbA region comparison. J Phycol 40:921–936
Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate genealogies. Mol Ecol 9:1657–1659
Coyer JA, Hoarau G, Schaik JV, Luijckx P, Olsen JL (2011a) Trans-Pacific and trans-Arctic pathways of the intertidal macroalga Fucus distichus L. reveal multiple glacial refugia and colonizations from the North Pacific to the North Atlantic. J Biogeogr 38:756–771
Coyer JA, Hoarau G, Costa JF, Hoderdiik B, Serrao EA, Billard E, Valero M, Pearson G, Olsen JL (2011b) Evolution and diversification within the intertidal brown macroalgae Fucus spiralis/F. vesiculosus species complex in the North Atlantic. Mol Phylogenet Evol 58:283–296
Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetic analyses under Linux and Windows. Mol Ecol Resour 10:564–567
Fraser CI, Nikula R, Spencer HG, Waters JM (2009) Kelp genes reveal effects of subantarctic sea ice during the Last Glacial Maximum. Proc Natl Acad Sci USA 106:3249–3253
Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925
Grant WAS, Bowen BW (1998) Shallow population histories in deep evolutionary lineages of marine fishes: insights from sardines and anchovies and lessons for conservation. J Hered 89:415–426
Harpending HC (1994) Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution. Hum Biol 66:591–600
Heo SJ, Kim JP, Jung WK, Lee NH, Kang HS, Jun EM, Park SH, Kang SM, Lee YJ, Park PJ, Jeon YJ (2008) Identification of chemical structure and free radical scavenging activity of diphlorethohydroxycarmalol isolated from a brown alga, Ishige okamurae. J Microbiol Biotechn 18:676–681
Hewitt GM (2000) The genetic legacy of the quaternary ice ages. Nature 405:907–913
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
Hu ZM, Uwai S, Yu SH, Komatsu T, Ajisaka 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 20:3894–3909
Kim JM, Kennett J (1998) Paleoenvironmental changes associated with the Holocene marine transgression, Yellow Sea (Hwanghae). Mar Micropaleontol 34:71–89
Kimura M (1996) Quaternary paleogeography of the Ryukyu Arc. J Geogr 105:259–285
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
Lee YP (2008) Marine algae of Jeju. Academy Science, Seoul, pp 1–177
Lee JH, Cho CH, Lee JH, Lee S, Tang Y (2000) Seasonal variation in the Cheju warm current in the Northern East China Sea. J Oceanogr 56:197–211
Lee EY, Lee IK, Choi HG (2003) Morphology and nuclear small-subunit rDNA sequences of Ishige (Ishigeaceae, Phaeophyceae) and its phylogenetic relationship among selected brown algal orders. Bot Mar 46:193–201
Lee KM, Boo GH, Risomena-Rodriquez R, Shin JA, Boo SM (2009) Classification of the genus Ishige (Ishigeales, Phaeophyceae) in the north Pacific Ocean with recognition of I. foliacea based on plastid rbcL and mitochondrial cox3 gene sequences. J Phycol 45:906–913
Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452
Liu JX, Gao TX, Wu SF, Zhang YP (2007) Pleistocene isolation in the Northwestern Pacific marginal seas and limited dispersal in a marine fish, Chelon haematocheilus, (Temminck & Schlegel, 1845). Mol Ecol 16:275–288
Maggs CA, Castilho R, Foltz DW, Henzler C, Jolly MT, Kelly J, Olsen JL, Perez KE, Stam WT, Vainola R, Viard F, Wares JP (2008) Evaluating signature of glacial refugia for north Atlantic benthic marine taxa. Ecology 89:S108–S122
Marko PB (2004) ‘What’s larvae got to do with it?’ Disparate patterns of post-glacial population structure in two benthic marine gastropods with identical dispersal potential. Mol Ecol 13:597–611
Papadopoulou A, Anastasiou I, Vogler AP (2010) Revisiting the insect mitochondrial clock: the mid-Aegean trench calibration. Mol Biol Evol 27:1659–1672
Procaccini G, Olsen JL, Reusch TBH (2007) Contribution of genetics and genomics to seagrass biology and conservation. J Exp Mar Biol Ecol 350:234–259
Rambaut A (2002) SeAl, v. 2.0. Institute of Evolutionary Biology, Ashworth Laboratories, Edinburgh
Ray N, Currat M, Excoffier L (2003) Intra-deme molecular diversity in spatially expanding populations. Mol Biol Evol 20:76–86
Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic difference. Mol Biol Evol 9:552–569
Schneider S, Excoffier L (1999) Estimation of past demographic parameters from the distribution of pairwise differences when the mutation rates vary among sites: application to human mitochondrial DNA. Genetics 152:1079–1089
Slatkin M, Hudson RR (1991) Pairwise comparisons of mitochondrial DNA sequences in stable and exponentially growing populations. Genetics 129:555–562
Sotka EE, Wares JP, Barth JA, Grosberg RK, Palumbi SR (2004) Strong genetic clines and geographical variation in gene flow in the rocky intertidal barnacle Balanus glandula. Mol Ecol 13:2143–2156
Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595
Tang B, Zhou K, Song D, Yang G, Dai Y (2003) Molecular systematics of the Asian mitten crabs, genus Eriocheir (Crustacea: Brachyura). Mol Phylogenet Evol 29:309–316
Tsukada M (1982) Cryptomeria japonica: glacial refugia and late-glacial and postglacial migration. Ecology 63:1091–1105
Wang J, Gao P, Kang M, Lowe AJ, Huang H (2009) Refugia within refugia: the case study of a canopy tree (Eurycorymbus cavaleriei) in subtropical China. J Biogeogr 36:2156–2164
Acknowledgments
This study was supported by a Korean Research Foundation (KRF) grant (MEST; 2009-0077972) and a grant from Marine Biotechnology Program funded by Ministry of Land, Transport, and Maritime Affairs of Korean government. We thank Gong Soo Chung, Youn Ho Lee, Dong Jin Lee, and Min Hur for their useful advice on paleogeography of the Korean peninsula, Paul John Geraldino and Ga Hun Boo for collections from Japan, and Put O. Ang, and Song Qin and Yang Rui for help in collections in Hong Kong and China, respectively.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by S. Uthicke.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Lee, K.M., Yang, E.C., Coyer, J.A. et al. Phylogeography of the seaweed Ishige okamurae (Phaeophyceae): evidence for glacial refugia in the northwest Pacific region. Mar Biol 159, 1021–1028 (2012). https://doi.org/10.1007/s00227-012-1882-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00227-012-1882-0