Advertisement

Seaweed Phylogeography from 1994 to 2014: An Overview

  • Zi-Min HuEmail author
  • De-Lin Duan
  • Juan Lopez-Bautista

Abstract

Molecular phylogeographic approaches employed for studying genetic diversity and evolution of seaweeds experienced noticeable growth since the mid-1990s and have greatly expanded our understanding of factors and processes contributing to biodiversity, adaptation, and population genetic variation of seaweeds. Herein, we present a numerical synthesis of 126 published references on seaweed phylogeography during the past two decades. We summarize the progress, research hotspots, regional distribution of outputs, potential deficiencies, and future tendencies in this field at a global scale. We also highlight the importance of integrating a statistically rigorous and comparative phylogeographic framework with species distribution models (SDM) and model-based phylogeographic inferences, when exploring cryptic speciation and evolution of seaweeds in response to global climate change, environmental shift, and human interference.

Keywords

Coastal ecosystem Ecological adaptation Habitat heterogeneity Phylogeography Population genetics Seaweed 

Notes

Acknowledgements

We would like to thank Ceridwen Fraser and an anonymous reviewer for valuable comments on this chapter. This study was partially supported by National Natural Science Foundation of China (31370264) granted to Z.M. Hu.

References

  1. Adey WH, Hayek LA. Elucidating marine biogeography with macrophytes: quantitative analysis of the North Atlantic supports the thermogeographic model and demonstrates a distinct Sub-Arctic region in the northwestern Atlantic. Northeast Nat. 2011;18:1–125.CrossRefGoogle Scholar
  2. Adey WH, Steneck RS. Thermogeography over time creates biogeographic regions: a temperature/space/time-integrated model and an abundance-weighted test for benthic marine algal. J Phycol. 2001;37:677–98.CrossRefGoogle Scholar
  3. Adey WH, Lindstrom SC, Hommersand MH, Müller KM. The biogeographic origin of Arctic endemic seaweeds: a thermogeographic view. J Phycol. 2008;44:1384–94.CrossRefGoogle Scholar
  4. Andreakis N, Procaccini G, Maggs CA, Kooisra WHCF. Phylogeography of the invasive seaweed Asparagopsis (Bonnemaisoniales, Rhodophyta) reveals cryptic diversity. Mol Ecol. 2007;16:2285–99.PubMedCrossRefGoogle Scholar
  5. Andreakis N, Kooistra WHCF, Procaccini G. High genetic diversity and connectivity in the polyploid invasive seaweed Asparagopsis taxiformis (Bonnemaisoniales) in the Mediterranean, explored with microsatellite alleles and multilocus genotypes. Mol Ecol. 2009;18:212–26.PubMedCrossRefGoogle Scholar
  6. Arbogast BS, Kenagy GJ. Comparative phylogeography as an integrative approach to historical biogeography. J Biogeogr. 2001;28(7):819–25.CrossRefGoogle Scholar
  7. Avise JC. Phylogeography: the history and formation of species. Cambridge: Harvard University Press; 2000.Google Scholar
  8. Avise JC. Phylogeography: retrospect and prospect. J Biogeogr. 2009;36:3–15.CrossRefGoogle Scholar
  9. Avise JC, Arnold J, Ball RM, Bermingham E, Lamb T, Neigel JE, Reeb CA, Saunders NC. Intraspecific phylogeography: the mitochondrial DNA bridge between population genetics and systematics. Ann Rev Ecol Syst. 1987;18:489–522.CrossRefGoogle Scholar
  10. Bae DY, Ang PO Jr, Boo SM. Mitochondrial cox3 and trnW-I sequence diversity of Sagassum mticum. Aquat Bot. 2013;104:220–3.CrossRefGoogle Scholar
  11. Bakker FT, Olsen JL, Stam WT. Global phylogeography in the cosmopolitan species Cladophora vagabunda (Chlorophyta) based on nuclear rDNA internal transcribed spacer sequences. Eur J Phycol. 1995;30:197–208.CrossRefGoogle Scholar
  12. Beheregaray LB. Twenty years of phylogeography: the state of the field and the challenges for the Southern Hemisphere. Mol Ecol. 2008;17:3754–74.PubMedGoogle Scholar
  13. Bergström L, Tatarenkov A, Johannesson K, Jönsson RB, Kautsky L. Genetic and morphological identification of Fucus radicans sp. nov. (Fucales, Phaeophyceae) in the brackish Baltic Sea. J Phycol. 2005;41(5):1025–38.CrossRefGoogle Scholar
  14. Braga JC, Martin JM, Riding R. Internal structure of segment reefs: Halimeda algal mounds in the Mediterranean Miocene. Geology. 1996;24:35–8.CrossRefGoogle Scholar
  15. Brawley SH, Coyer JA, Blakeslee AMH, Hoarau G, Johnson L, Byers JE, Stam WT, Olsen JL. Historical invasions of the intertidal zone of Atlantic North America associated with distinctive patterns of trade and emigration. Proc Nat Acad Sci USA. 2009;106(20):8239–44.PubMedCentralPubMedCrossRefGoogle Scholar
  16. Buchanan J, Zuccarello GC. Decoupling of short- and long-distance dispersal pathways in the endemic New Zealand seaweed Carpophyllum maschalocarpum (Phaeophyceae, Fucales). J Phycol. 2012;48:518–29.CrossRefGoogle Scholar
  17. Chan SW, Cheang CC, Chirapart A, Gerung G, Tharith C, Ang PO Jr. Homogeneous population of the brown alga Sargassum polycystum in Southeast Asia: possible role of recent expansion and asexual propagation. PLoS ONE. 2013;8(10):e77662.PubMedCentralPubMedCrossRefGoogle Scholar
  18. Chan SW, Cheang CC, Yeung CW, Chirapat A, Gerung G, Ang PO Jr. Recent expansion led to the lack of genetic structure of Sargassum aquifolium populations in Southeast Asia. Mar Biol. 2014;161:785–95.CrossRefGoogle Scholar
  19. Cheang CC, Chu KH, Ang PO Jr. Morphological and genetic variation in the populations of Sargassum hemiphyllum (Phaeophyceae) in the northwestern Pacific. J Phycol. 2008;44:855–65.CrossRefGoogle Scholar
  20. Cheang CC, Chu KH, Ang PO Jr. Phylogeography of the marine marcoalga Sargassum hemiphyullum (Phaeophyceae, Heterokontophyta) in the Northwestern Pacific. Mol Ecol. 2010a;19:2933–48.PubMedCrossRefGoogle Scholar
  21. Cheang CC, Chu KH, Fujita D, Yoshida G, Hiraoka M, Critchley AT, Choi HG, Duan DL, Serisawa Y, Ang PO Jr. Low genetic variability of Sargassum muticum (Phaeophyceae) revealed by a global analysis of native and introduced populations. J Phycol. 2010b;46:1063–74.CrossRefGoogle Scholar
  22. Coll M, Piroddi C, Steenbeek J, Kaschner K, Lasram FBR, Aguzzi J, Ballesteros E, Bianchi CN, Corbera J, Dailianis T, Danovaro R, Estrada M, Froglia C, Galil BS, Gasol JM, Gertwagen R, Gil J, Guihaumon F, Kesner-Reyes K, Kitsos M-S, Koukouras A, Lampadariou N, Laxamana E, Lopez-Fe CM, Lotze HK, Martin D, Mouillot D, Oro D, Raicevich S, Rius-Barile J, Saiz-Salinas JL, Vicente CS, Somot S, Templado J, Turon X, Vafidis D, Villanueva R, Voultsiadou E. The biodiversity of the Mediterranean Sea: estimates, patterns, and threats. PLoS ONE. 2010;5(8):e11842.PubMedCentralPubMedCrossRefGoogle Scholar
  23. Couceiro L, Maneiro I, Ruiz JM, Barreiro R. Multiscale genetic structure of an endangered seaweed Ahnfeltiopsis pusilla (Rhodophyta): implications for its conservation. J Phycol. 2011;47(2):259–68.CrossRefGoogle Scholar
  24. Coyer JA, Olsen JL, Stam WT. Genetic variability and spatial separation of the sea palm kelp, Postelsia palmaeformis (Phaeophyceae) as assessed with M13 fingerprints and RAPDs. J Phycol. 1997;33:561–8.CrossRefGoogle Scholar
  25. Coyer JA, Peters AF, Hoarau G, Stam WT, Olsen JL. Hybridization of the marine seaweeds, Fucus serratus and Fucus evanescens (Heterokontophyta: Phaeophyceae) in a 100-year-old zone of secondary contact. Proc R Soc B. 2002;269:1829–34.PubMedCentralPubMedCrossRefGoogle Scholar
  26. Coyer JA, Peters AF, Stam WT, Olsen JL. Post-ice age recolonization and differentiation of Fucus serratus L. (Phaeophyceae; Fucaceae) populations in Northern Europe. Mol Ecol. 2003;12:1817–29.PubMedCrossRefGoogle Scholar
  27. Coyer JA, Hoarau G, Costa JF, Hogerdijk B, Serrão EA, Billard E, Valero M, Pearson GA, Olsen JL. Evolution and diversification within the intertidal brown macroalgae Fucus spiralis/F. vesiculosus species complex in the North Atlantic. Mol Phylogenet Evol. 2011a;58:283–96.PubMedCrossRefGoogle Scholar
  28. Coyer JA, Hoarau G, Pearson G, Mota C, Jüterbock A, Alpermann T, John U, Olsen JL. Genomic scans detect signatures of selection along a salinity gradient in populations of the intertidal seaweed Fucus serratus on a 12 km scale. Mar Genom. 2011b;4:41–9.CrossRefGoogle Scholar
  29. Coyer JA, Hoarau G, Skage M, Stam WT, Olsen JL. Origin of Fucus serratus (Heterokontophyta; Fucaceae) populations in Iceland and the Faroes: a microsatellite-based assessment. Eur J Phycol. 2006;41:235–46.Google Scholar
  30. Faugeron S, Valero M, Destombe C, Martínez EA, Correa JA. Hierarchical spatial structure and discriminant analysis of genetic diversity in the red alga Mazzaella laminarioides (Gigartinales, Rhodophyta). J Phycol. 2001;37:705–16.Google Scholar
  31. Fraser CI, Nikula R, Spencer HG, Waters JM. Kelp genes reveal effects of subantarctic sea ice during the last glacial maximum. Proc Nat Acad Sci USA. 2009a;106(9):3249–53.PubMedCentralPubMedCrossRefGoogle Scholar
  32. Fraser CI, Hay CH, Spencer GH, Waters JM. Genetic and morphological analyses of the southern bull kelp Durvillaea antarctic (Phaeophyceae: Durvillaeales) in New Zealand reveal cryptic species. J Phycol. 2009b;45:436–43.CrossRefGoogle Scholar
  33. Fraser CI, Nikula R, Waters JM. Oceanic rafting by a coastal community. Proc R Soc B. 2011;278:649–55.PubMedCentralPubMedCrossRefGoogle Scholar
  34. Fraser CI, Zuccarello GC, Spencer HG, Salvatore LC, Garcia GR, Waters JM. Genetic affinities between trans-oceanic populations of non-buoyant macroalgae in the high latitudes of the southern hemisphere. PLoS ONE. 2013;8(7):e69138.PubMedCentralPubMedCrossRefGoogle Scholar
  35. Freile D, Milliman JD, Hillis L. Leeward bank margin Halimeda meadows and draperies and their sedimentary importance on the western Great Bahama bank slope. Coral Reefs. 1995;14:27–33.CrossRefGoogle Scholar
  36. Griffiths CL, Robinson TB, Lange L, Mead A. Marine biodiversity in South Africa: an evaluation of current states of knowledge. PLoS ONE. 2010;5(8):e12008.PubMedCentralPubMedCrossRefGoogle Scholar
  37. Guillemin M, Valero M, Faugeron S, Nelson W, Destombe C. Tracing the trans-Pacific evolutionary history of a domesticated seaweed (Gracilaria chilensis) with Archaeological and genetic data. PLoS ONE. 2014;9(12):e114039.PubMedCentralPubMedCrossRefGoogle Scholar
  38. Hewitt GM. The genetic legacy of the Quaternary ice ages. Nature. 2000;40:907–13.CrossRefGoogle Scholar
  39. Hickerson MJ, Meyer C. Testing comparative phylogeographic models of marine vicariance and dispersal using a hierarchical Bayesian approach. BMC Evol Biol. 2008;8:322.PubMedCentralPubMedCrossRefGoogle Scholar
  40. Hoarau G, Coyer JA, Veldsink JH, Stam WT, Olsen JL. Glacial refugia and recolonization pathways in the brown seaweed Fucus serratus. Mol Ecol. 2007;16:3606–16.PubMedCrossRefGoogle Scholar
  41. Hu ZM. Intertidal population genetic dynamics at a microgeographic seascape scale. Mol Ecol. 2013;22:3191–4.PubMedCrossRefGoogle Scholar
  42. Hu ZM, Critchley AT, Gao TX, Zeng XQ, Morrell SL, Duan DL. Delineation of Chondrus (Gigartinales, Florideophyceae) in China and the origin of C. crispus inferred from molecular data. Mar Biol Res. 2007a;3:145–54.CrossRefGoogle Scholar
  43. Hu ZM, Zeng XQ, Critchley AT, Morrell SL, Duan DL. Phylogeography of the Northern Atlantic species Chondrus crispus (Gigartinales, Rhodophyta) inferred from nuclear rDNA internal transcribed spacer sequences. Hydrobiologia. 2007b;575(1):315–27.CrossRefGoogle Scholar
  44. Hu ZM, Guiry MD, Critchley AT, Duan DL. Phylogeographic patterns indicate trans-Atlantic migration from Europe to North America in the red seaweed Chondrus crispus (Gigartinales, Rhodophyta). J Phycol. 2010;46:889–900.CrossRefGoogle Scholar
  45. Hu ZM, Uwai S, Yu SH, Komatsu T, Ajisaka T, Duan DL. Phylogeographic heterogeneity of the brown macroalga Sargassum horneri (Fucaceae) in the northwestern Pacific in relation to late Pleistocene glaciation and tectonic configurations. Mol Ecol. 2011a;20:3894–909.PubMedCrossRefGoogle Scholar
  46. Hu ZM, Li W, Li JJ, Duan DL. Post-Pleistocene demographic history of the North Atlantic endemic Irish moss Chondrus crispus: glacial survival, spatial expansion and gene flow. J Evol Biol. 2011b;24:505–17.PubMedCrossRefGoogle Scholar
  47. Hu ZM, Zhang J, Lopez-Bautista J, Duan DL. Asymmetric genetic exchange in the brown seaweed Sargassum fusiforme (Phaeophyceae) driven by oceanic currents. Mar Biol. 2013;160(6):1407–14.CrossRefGoogle Scholar
  48. Ilves KL, Huang W, Wares JP, Hickerson MJ. Colonization and/or mitochondrial selective sweeps across the North Atlantic intertidal assemblage revealed by multi-taxa approximate Bayesian computation. Mol Ecol. 2010;19:4505–19.PubMedCrossRefGoogle Scholar
  49. Kerswell AP. Global biodiversity patterns of benthic marine algae. Ecology. 2006;87:2479–88.PubMedCrossRefGoogle Scholar
  50. Kidd KM, Ritchie MG. Phylogeographic information systems: putting the geography into phylogeography. J Biogeogr. 2006;33(11):1851–65.CrossRefGoogle Scholar
  51. Kim SY, Weinberer F, Boo SM. Genetic data hint at a common donor region for invasive Atlantic and Pacific populations of Gracilaria vermiculophylla (Gracilariales, Rhodophyta). J Phycol. 2010;46:1346–349.Google Scholar
  52. Kim KM, Hoarau G, Boo SM. Genetic structure and distribution of Gelidium elegans (Gelidiales, Rhodophyta) in Korea based on mitochondrial cox1 sequence data. Aquat Bot. 2012;98:27–33.CrossRefGoogle Scholar
  53. Kim SY, Manghisi A, Morabito M, Yang EC, Yoon HS, Miller KA, Boo SM. Genetic diversity and haplotype distribution of Pachymeniopsis gargiuli sp. Nov. and P. lanceolata (Halymeniales, Rhodophyta) in Korea, with notes on their non-native distributions. J Phycol. 2014;50:885–96.CrossRefGoogle Scholar
  54. Knowles LL, Maddison WP. Statistical phylogeography. Mol Ecol. 2002;11:2623–35.PubMedCrossRefGoogle Scholar
  55. 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. Abundance of drifting seaweeds in eastern East China Sea. J Appl Phycol. 2008;20:801–9.CrossRefGoogle Scholar
  56. Kostamo K, Korpelainen H, Olsson S. Comparative study on the population genetics of the red algae Furcellaria lumbricalis occupying different salinity conditions. J Appl Phycol. 2012;159:561–71.Google Scholar
  57. Kooistra WHCF, Coppejans EGG, Payri C. Molecular systematics, historical ecology, and phylogeography of Halimeda (Bryopsidales). Mol Phylogenet Evol. 2002;24:121–38.PubMedCrossRefGoogle Scholar
  58. Kozak KH, Graham CH, Wiens JJ. Integrating GIS-based environmental data into evolutionary biology. Trends Ecol Evol. 2008;23:141–8.PubMedCrossRefGoogle Scholar
  59. Krueger-Hadfield SA, Collén J, Daguin-Thiebaut C, Valero M. Genetic population structure and mating system in Chondrus crispus (Rhodophyta). J Phycol. 2011;47:440–50.CrossRefGoogle Scholar
  60. Krueger-Hadfield SA, Roze D, Mauger S, Valero M. Intergametophytic selfing and microgeographic genetic structure shape populations of the intertidal red seaweed Chondrus crispus. Mol Ecol. 2013;22:3242–60.PubMedCrossRefGoogle Scholar
  61. Lee KM, Boo SM, Kain (Jones) JM, Sherwood AR. Cryptic diversity and biogeography of the widespread brown alga Colpomenia sinuosa (Ectocarpales, Phaeophyceae). Bot Mar. 2013;56:15–25.Google Scholar
  62. Leskinen E, Alström-Rapaport C, Pamilo P. Phylogeographical structure, distribution and genetic variation of the green algae Ulva intestinalis and U. compressa (Chlorophyta) in the Baltic Sea area. Mol Ecol. 2004;13:2257–65.PubMedCrossRefGoogle Scholar
  63. Li JJ, Hu ZM, Duan DL. Genetic data from the red alga Palmaria palmata reveal a mid-Pleistocene deep genetic split in the North Atlantic. J Biogeogr. 2015;42(5):902–13.CrossRefGoogle Scholar
  64. Li JJ, Hu ZM, Duan DL. Survival in glacial refugia vs. postglacial dispersal in the North Atlantic: the cases of red seaweeds. In: Hu ZM, Fraser CI editors. Seaweed phylogeography: adaptation and evolution of seaweeds under environmental change. Berlin, Heidelberg: Springer; 2016.Google Scholar
  65. Lindstrom SC. The Bering Strait connection: dispersal and speciation in boreal macroalgae. J Biogeogr. 2001;28:243–51.CrossRefGoogle Scholar
  66. Lindstrom SC. The biogeography of seaweeds in Southeast Alaska. J Biogeogr. 2009;36:401–9.CrossRefGoogle Scholar
  67. Lindstrom SC, Olsen JL, Stam WT. Recent radiation of the Palmariaceae (Rhodophyta). J Phycol. 1996;32:457–68.CrossRefGoogle Scholar
  68. Maggs CA, Castilho R, Foltz D, Henzler C, Jolly MT, Kelly J, Olsen JL, Perez KE, Stam WT, Väinölä R, Viard F, Wares J. Evaluating signatures of glacial refugia for North Atlantic benthic marine taxa. Ecology. 2008;89:S108–22.PubMedCrossRefGoogle Scholar
  69. McIvor L, Maggs CA, Provan J, Stanhope MJ. rbcL sequences reveal multiple cryptic introductions of the Japanese red alga Polysiphonia harveyi. Mol Ecol. 2001;10:911–9.PubMedCrossRefGoogle Scholar
  70. Miller KA, Olsen JL, Stam WT. Genetic divergence correlates with morphological and ecological subdivision in the deep-water elk kelp Pelagophycus porra (Laminariales, Phaeophyceae). J Phycol. 2000;36:862–70.CrossRefGoogle Scholar
  71. Moalic Y, Arnaud-Haond S, Perrin C, Pearson GA, Serrão EA. Travelling in time with networks: revealing present day hybridization versus ancestral polymorphism between two species of brown algae, Fucus vesiculosus and F. spiralis. BMC Evol Biol. 2011;11:33.PubMedCentralPubMedCrossRefGoogle Scholar
  72. Montecinos A, Broitman BR, Faugeron S, Haye PA, Tellier F, Guillemin M. Species replacement along a linear coastal habitat: phylogeography and speciation in the red alga Mazzaella laminarioides along the southeast Pacific. BMC Evol Biol. 2012;12:97.PubMedCentralPubMedCrossRefGoogle Scholar
  73. Muangmai N, Fraser CI, Zuccarello GC. Contrasting patterns of population structure and demographic history in cryptic species of (Rhodomelaceae, Rhodophyta) from New Zealand. J Phcyol. 2015;51:574–85.CrossRefGoogle Scholar
  74. Muhlin JF, Brawley SH. Recent versus relic: discerning the genetic signature of Fucus vesiculosus (Heterokontophyta; Phaeophyceae) in the Northwestern Atlantic. J Phycol. 2009;45:828–37.CrossRefGoogle Scholar
  75. Muhlin JF, Engel CR, Stessel R, Weatherbee RA, Brawley SH. The influence of coastal topography, circulation patterns, and rafting in structuring populations of an intertidal alga. Mol Ecol. 2008;17:1198–210.PubMedCrossRefGoogle Scholar
  76. Neiva J, Pearson GA, Valero M, Serrão EA. Surfing the wave on a borrowed board: range expansion and spread of introgressed organellar genomes in the seaweed Fucus ceranoides L. Mol Ecol. 2010;19:4812–22.PubMedCrossRefGoogle Scholar
  77. Neiva J, Pearson GA, Valero M, Serrão EA. Drifting fronds and drifting alleles: range dynamics, local dispersal and habitat isolation shape the population structure of the estuarine seaweed Fucus ceranoides. J Biogeogr. 2012a;39:1167–78.CrossRefGoogle Scholar
  78. Neiva J, Pearson GA, Valero M, Serrão EA. Fine-scale genetic breaks driven by historical range dynamics and ongoing density-barrier effects in the estuarine seaweed Fucus ceranoides L. BMC Evol Biol. 2012b;12:78.PubMedCentralPubMedCrossRefGoogle Scholar
  79. Neiva J, Assis J, Fernandes F, Pearson GA, Serrão EA. Species distribution models and mitochondrial DNA phylogeography suggest an extensive biogeographical shift in the high-intertidal seaweed Pelvetia canaliculata. J Biogeogr. 2014;41:1137–48.CrossRefGoogle Scholar
  80. Neiva J, Serrão EA, Assis J, Pearson GA, Coyer JA, Olsen JL, Hoarau G, Valero M. Climate oscillations, range shifts and phylogeographic patterns of North Atlantic Fucaceae. In: Hu ZM, Fraser CI editors. Seaweed phylogeography: adaptation and evolution of seaweeds under environmental change. Berlin, Heidelberg: Springer; 2016.Google Scholar
  81. Nicastro KR, Zardi GI, Teixeira S, Neiva J, Serrão EA, Pearson GA. Shift happens: trailing edge contraction associated with recent warming trends threatens a distinct genetic lineage in the marine macroalga Fucus vesiculosus. BMC Biol. 2013;11:6.PubMedCentralPubMedCrossRefGoogle Scholar
  82. Ogawa T, Ohki K, Kamiya M. High heterozygosity and phenotypic variation of zoids in apomictic Ulva prolifera (Ulvophyceae) from brackish environments. Aquat Bot. 2015;120:185–92.CrossRefGoogle Scholar
  83. Olsen JL, Zechman FW, Hoarau G, Coyer JA, Stam WT, Valero M, Nilsson P, Åberg P. The phylogeographic architecture of the fucoid seaweed Ascophyllum nodosum: an intertidal “marine tree” and survivor of more than one glacial-interglacial cycle. J Biogeogr. 2010;37:842–56.CrossRefGoogle Scholar
  84. Pakker H, Klerk H, van Campen JH, Olsen JL, Breeman AM. Evolutionary and ecological differentiation in the pantropical to warm-temperate seaweed Digenea simplex (Rhodophyta). J Phycol. 1996;32:250–7.CrossRefGoogle Scholar
  85. Peters AF, van Oppen MJH, Wiencke C, Stam WT, Olsen JL. Phylogeny and historical ecology of the Desmarestiaceae (Phaeophyceae) support a southern hemisphere origin. J Phycol. 1997;33:294–309.CrossRefGoogle Scholar
  86. Provan J, Murphy S, Maggs CA. Tracking the invasive history of the green alga Codium fragile ssp. tomentosoides. Mol Ecol. 2005a;14:189–94.PubMedCrossRefGoogle Scholar
  87. Provan J, Wattier RA, Maggs CA. Phylogeographic analysis of the red seaweed Palmaria palmata reveals a Pleistocene marine glacial refugium in the English Channel. Mol Ecol. 2005b;14:793–803.PubMedCrossRefGoogle Scholar
  88. Provan J, Maggs CA. Unique genetic variation at a species’ rear edge is under threat from global climate change. Proc R Soc B. 2011;279:39–47.PubMedCentralPubMedCrossRefGoogle Scholar
  89. Provan J, Booth D, Todd NP, Beatty GE, Maggs CA. Tracking biological invasions in space and time: elucidating the invasive history of the green alga Codium fragile using old DNA. Divers Distrib. 2008;14:343–54.CrossRefGoogle Scholar
  90. Provan J, Glendinning K, Kelly R, Maggs CA. Levels and patterns of population genetic diversity in the red seaweed Chondrus crispus (Florideophyceae): a direct comparison of single nucleotide polymorphisms and microsatellites. Biol J Linn Soc. 2013;108:251–62.CrossRefGoogle Scholar
  91. Richards CL, Carstens BC, Knowles LL. Distribution modeling and statistical phylogeography: an integrative framework for generating and testing alternative biogeographic hypotheses. J Biogeogr. 2007;34:1833–45.CrossRefGoogle Scholar
  92. Reuter M, Piller WE, Richoz S. The dispersal of Halimeda in northern hemisphere mid-latitudes: paleobiogeographical insights. Perspec Plant Ecol Evol Syst. 2012;14:303–9.CrossRefGoogle Scholar
  93. Robuchon M, Gall LL, Mauger S, Valero M. Contrasting genetic diversity patterns in two sister kelp species co-distributed along the coast of Brittany, France. Mol Ecol. 2014;23:2669–85.PubMedCrossRefGoogle Scholar
  94. Shimada S, Yokoyama N, Arai S, Hiraoka M. Phylogeography of the genus Ulva (Ulvophyceae, Chlorophyta), with special reference to the Japanese freshwater and brackish taxa. J Appl Phycol. 2008;20:979–89.CrossRefGoogle Scholar
  95. Sherwood AR. Phylogeography of Asparagopsis taxiformis (Bonnemaisoniales, Rhodophyta) in the Hawaiian Islands: two mtDNA markers support three separate introductions. Phycologia. 2008;47(1):79–88.CrossRefGoogle Scholar
  96. Tatarenkov A, Jönsson RB, Kautsky L, Johannesson K. Genetic structure in populations of Fucus vesiculosus (Phaeophyceae) over spatial scales from 10 m to 800 km. J Phycol. 2007;43(4):675–85.CrossRefGoogle Scholar
  97. Thiel M, Haye PA. The ecology of rafting in the marine environment. III. Biogeographical and evolutionary consequences. Oceanogr Mar Biol Ann Rev. 2006;44:323–429.Google Scholar
  98. Uwai S, Kogame K, Yoshida G, Kawai H, Ajisaka T. Geographical genetic structure and phylogeography of the Sargassum horneri/filicinum complex in Japan, based on the mitochondrial cox3 haplotype. Mar Biol. 2009;156:901–11.CrossRefGoogle Scholar
  99. van Oppen MJH, Diekmann OE, Wiencke C, Stam WT, Olsen JL. Tracking dispersal routes: phylogeography of the Arctic-Antarctic disjunct seaweed Acrosiphonia arcta (Chlorophyta). J Phycol. 1994;30(4):67–80.CrossRefGoogle Scholar
  100. van Oppen MJH, Draisma SGA, Olsen JL, Stam WT. Multiple trans-Arctic passages in the red alga Phycodrys rubens: evidence from nuclear rDNA ITS sequences. Mar Biol. 1995a;123:179–88.CrossRefGoogle Scholar
  101. van Oppen MJH, Olsen JL, Stam WT. Genetic variation within and among North Atlantic and Baltic populations of the benthic alga Phycodrys rubens (Rhodophyta). Eur J Phycol. 1995b;30:251–60.CrossRefGoogle Scholar
  102. Verbruggen H, De Clerck O, Kooistra WHCF, Coppejans E. Molecular and morphometric data pinpoint species boundaries in Halimeda section Rhipsalis (Bryopsidales, Chlorophyta). J Phycol. 2005;41:606–21.CrossRefGoogle Scholar
  103. Verbruggen H, Tyberghein L, Pauly K, Vlaeminck C, Nieuwenhuyze KV, Kooistra WHCF, Leliaert F, De Clerck O. Macroecology meets macroevolution: evolutionary niche dynamics in the seaweed Halimeda. Global Ecol Biogeogr. 2009;18:393–405.CrossRefGoogle Scholar
  104. Wang XL, Zhao FJ, Hu ZM, Critchley AT, Morrell SL, Duan DL. Inter-simple sequence repeat (ISSR) analysis of genetic variation of Chondrus crispus populations from North Atlantic. Aquat Bot. 2008;88:154–9.CrossRefGoogle Scholar
  105. Yang EC, Cho GY, Kogame K, Carlile AL, Boo SM. RuBisCo cistron sequence variation and phylogeography of Ceramium kondoi (Ceramiaceae, Rhodophyta). Bot Mar 2008;51:370–77.Google Scholar
  106. Yang EC, Lee SY, Lee WJ, Boo SM. Molecular evidence for recolonization of Ceramium japonicum (Ceramiaceae, Rhodophyta) on the west coast of Korea after the last glacial maximum. Bot Mar 2009;52:307–15.Google Scholar
  107. Zuccarello GC, West JA. Multiple cryptic species: molecular diversity and reproductive isolation in the Bostrychia radicans/B. moritziana complex (Rhodomelaceae, Rhodophyta) with focus on North American isolates. J Phycol. 2003;39:948–59.CrossRefGoogle Scholar
  108. Zuccarello GC, West JA, Kamiya M, King RJ. A rapid method to score plastid haplotypes in red seaweeds and its use in determining parental inheritance of plastids in the red alga Bostrychia (Ceramiales). Hydrobiologia. 1999;401:207–14.CrossRefGoogle Scholar
  109. Zuccarello GC, Buchanan J, West JA. Increased sample for inferring phylogeographic patterns in Bostrychia radicans/B. moritziana (Rhodomelaceae, Rhodophyta) in the Eastern USA. J Phycol. 2006;42:1349–52.CrossRefGoogle Scholar
  110. Zuccarello GC, Buchanan J, West JA, Pedroche FF. Genetic diversity of the mangrove-associated alga Bostychia radicans/B. moritziana (Ceramiales, Rhodophyta) from southern Central America. J Appl Phycol 2011;59:98–104.Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  1. 1.Key Laboratory of Experimental Marine BiologyInstitute of Oceanology, Chinese Academy of SciencesQingdaoChina
  2. 2.Qingdao National Laboratory for Marine Science and TechnologyQingdaoChina
  3. 3.Department of Biological SciencesThe University of AlabamaTuscaloosaUSA

Personalised recommendations