Drifting fronds and drifting alleles: Range dynamics, local dispersal and habitat isolation shape the population structure of the estuarine seaweed Fucus ceranoides

Journal of Biogeography

Volumn 39, Issue 6, 2012, Pages 1167-1178

  Neiva, João ^a,b   Pearson, Gareth A ^a   Valero, Myriam ^b   Serrão, Ester A ^a  

^a UNIVERSITY OF ALGARVE   (Portugal)

^b STATION BIOLOGIQUE DE ROSCOFF   (France)

Author keywords

Estuary; Fucus ceranoides; Microsatellites; North eastern Atlantic; Pleistocene refugium; Population structure; Post glacial expansion; Rafting

Indexed keywords

ALLELE; DISPERSAL; ESTUARINE ENVIRONMENT; GENE FLOW; GENETIC DRIFT; GENETIC MARKER; GENETIC VARIATION; ISOLATED POPULATION; LAST DEGLACIATION; LATITUDINAL GRADIENT; METAPOPULATION; MITOCHONDRIAL DNA; PHYLOGEOGRAPHY; POPULATION STRUCTURE; POSTGLACIAL; RANGE EXPANSION; RANGE SIZE; REFUGIUM; SEAWEED;

ATLANTIC OCEAN; ATLANTIC OCEAN (NORTHEAST);

FUCUS; FUCUS CERANOIDES;

EID: 84861186032     PISSN: 03050270     EISSN: 13652699     Source Type: Journal    
DOI: 10.1111/j.1365-2699.2011.02670.x     Document Type: Article

References (90)

1. Alberto, F., Raimondi, P.T., Reed, D.C., Coelho, N.C., Leblois, R., Whitmer, A. & Serrão, E.A. (2010) Habitat continuity and geographic distance predict population genetic differentiation in giant kelp. Ecology, 91, 49-56.
2. Araújo, R., Serrão, E.A., Sousa-Pinto, I. & Aberg, P. (2011) Phenotypic differentiation at southern limit borders: the case-study of two fucoid macroalgal species with different life-history traits. Journal of Phycology, 47, 451-462.
3. Arnaud-Haond, S., Migliaccio, M., Diaz-Almela, E., Teixeira, S., van de Vliet, M.S., Alberto, F., Procaccini, G., Duarte, C.M. & Serrão, E.A. (2007) Vicariance patterns in the Mediterranean Sea: east-west cleavage and low dispersal in the endemic seagrass Posidonia oceanica. Journal of Biogeography, 34, 963-976.
4. Arrontes, J. (1993) Nature of the distributional boundary of Fucus serratus on the north shore of Spain. Marine Ecology Progress Series, 93, 183-193.
5. Arrontes, J. (2002) Mechanisms of range expansion in the intertidal brown alga Fucus serratus in northern Spain. Marine Biology, 141, 1059-1067.
6. Attrill, M.J. & Rundle, S.D. (2002) Ecotone or ecocline: ecological boundaries in estuaries. Estuarine Coastal and Shelf Science, 55, 929-936.
7. Austerlitz, F., Jung-Muller, B., Godelle, B. & Gouyon, P.-H. (1997) Evolution of coalescence times, genetic diversity and structure during colonization. Theoretical Population Biology, 51, 148-164.
8. Belkhir, K., Borsa, P., Chikhi, L., Raufaste, N. & Bonhomme, F. (19962004) GENETIX 4.05, logiciel sous Windows TM pour la génétique des populations. Laboratoire Génome, Populations, Interactions, CNRS UMR 5171, Université de Montpellier II, Montpellier.
9. Bennett, K.D. & Provan, J. (2008) What do we mean by 'refugia'? Quaternary Science Reviews, 27, 2449-2455.
10. Bhagwat, S.A. & Willis, K.J. (2008) Species persistence in northerly glacial refugia of Europe: a matter of chance or biogeographical traits? Journal of Biogeography, 35, 464-482.
11. Billard, E., Daguin, C., Pearson, G.A., Serrão, E.A., Engel, C. & Valero, M. (2005a) Genetic isolation between the three closely related taxa: Fucus vesiculosus, F. spiralis and F. ceranoides. Journal of Phycology, 41, 900-905.
12. Billard, E., Serrao, E.A., Pearson, G.A., Engel, C.R., Destombe, C. & Valero, M. (2005b) Analysis of sexual phenotype and prezygotic fertility in natural populations of Fucus spiralis, F. vesiculosus (Fucaceae, Phaeophyceae) and their putative hybrids. European Journal of Phycology, 40, 397-407.
13. Billot, C., Engel, C.R., Rousvoal, S., Kloareg, B. & Valero, M. (2003) Current patterns, habitat discontinuities and population genetic structure: the case of the kelp Laminaria digitata in the English Channel. Marine Ecology Progress Series, 253, 111-121.
14. Brochmann, C., Gabrielsen, T.M., Nordal, I., Landvik, J.Y. & Elven, R. (2003) Glacial survival or tabula rasa? The history of North Atlantic biota revisited. Taxon, 52, 417-450.
15. Cavalli-Sforza, L.L. & Edwards, A.W.F. (1967) Phylogenetic analysis models and estimation procedures. American Journal of Human Genetics, 19, 233-257.
16. Chapman, A.R.O. (1995) Functional ecology of fucoid algae: 23years of progress. Phycologia, 34, 1-32.
17. Coleman, M.A. & Brawley, S.H. (2005) Are life history characteristics good predictors of genetic diversity and structure? A case study of the intertidal alga Fucus spiralis (Heterokontophyta; Phaeophyceae). Journal of Phycology, 41, 753-762.
18. Cowen, R.K. & Sponaugle, S. (2009) Larval dispersal and marine population connectivity. Annual Review of Marine Science, 1, 443-466.
19. Coyer, J.A., Peters, A.F., Stam, W.T. & Olsen, J.L. (2003) Post-ice age recolonization and differentiation of Fucus serratus L. (Phaeophyceae; Fucaceae) populations in Northern Europe. Molecular Ecology, 12, 1817-1829.
20. Coyer, J.A., Hoarau, G., Sjotun, K. & Olsen, J.L. (2008) Being abundant is not enough: a decrease in effective population size over eight generations in a Norwegian population of the seaweed Fucus serratus. Biology Letters, 4, 755-757.
21. Coyer, J.A., Hoarau, G., Beszteri, B., Pearson, G. & Olsen, J.L. (2009) Expressed sequence tag-derived polymorphic SSR markers for Fucus serratus and amplification in other species of Fucus. Molecular Ecology Resources, 9, 168-170.
22. Crawford, N.G. (2010) SMOGD: software for the measurement of genetic diversity. Molecular Ecology Resources, 10, 556-557.
23. Dawson, M.N., Staton, J.L. & Jacobs, D.K. (2001) Phylogeography of the tidewater goby, Eucyclogobius newberryi (Teleostei, Gobiidae), in coastal California. Evolution, 55, 1167-1179.
24. Dudgeon, S., Kubler, J.E., Wright, W.A., Vadas, R.L. & Petraitis, P.S. (2001) Natural variability in zygote dispersal of Ascophyllum nodosum at small spatial scales. Functional Ecology, 15, 595-604.
25. Engel, C.R., Brawley, S.H., Edwards, K.J. & Serrão, E.A. (2003) Isolation and cross-species amplification of microsatellite loci from the fucoid seaweeds Fucus vesiculosus, F. serratus and Ascophyllum nodosum (Heterokontophyta, Fucaceae). Molecular Ecology Notes, 3, 180-182.
26. Evanno, G., Regnaut, S. & Goudet, J. (2005) Detecting the number of clusters of individuals using the software structure: a simulation study. Molecular Ecology, 14, 2611-2620.
27. Excoffier, L. & Ray, N. (2008) Surfing during population expansions promotes genetic revolutions and structuration. Trends in Ecology and Evolution, 23, 347-351.
28. Excoffier, L., Foll, M. & Petit, R.J. (2009) Genetic consequences of range expansions. Annual Review of Ecology, Evolution, and Systematics, 40, 481-501.
29. Falush, D., Stephens, M. & Pritchard, J.K. (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics, 164, 1567-1587.
30. Fernández, C. & Anadón, R. (2008) La cornisa Cantábrica: un escenario de cambios de distribución de comunidades intermareales. Algas, 39, 30-32.
31. Fraser, C.I., Nikula, R., Spencer, H.G. & Waters, J.M. (2009) Kelp genes reveal effects of subantarctic sea ice during the Last Glacial Maximum. Proceedings of the National Academy of Sciences USA, 106, 3249-3253.
32. Fraser, C.I., Thiel, M., Spencer, H.G. & Waters, J.M. (2010) Contemporary habitat discontinuity and historic glacial ice drive genetic divergence in Chilean kelp. BMC Evolutionary Biology, 10, 203.
33. Gibbard, P.L. & Lautridou, J.P. (2003) The Quaternary history of the English Channel: an introduction. Journal of Quaternary Science, 18, 195-199.
34. Gómez, A. & Lunt, D.H. (2007) Refugia within refugia: patterns of phylogeographic concordance in the Iberian Peninsula. Phylogeography of southern European refugia (ed. by S. Weiss and N. Ferrand ), pp. 155-188. Springer, Dordrecht.
35. Gómez, A., Hughes, R.N., Wright, P.J., Carvalho, G.R. & Lunt, D.H. (2007) Mitochondrial DNA phylogeography and mating compatibility reveal marked genetic structuring and speciation in the NE Atlantic bryozoan Celleporella hyalina. Molecular Ecology, 16, 2173-2188.
36. Graham, M.H., Dayton, P.K. & Erlandson, J.M. (2003) Ice ages and ecological transitions on temperate coasts. Trends in Ecology and Evolution, 18, 33-40.
37. Gysels, E.S., Hellemans, B., Pampoulie, C. & Volckaert, F.A.M. (2004) Phylogeography of the common goby, Pomatoschistus microps, with particular emphasis on the colonization of the Mediterranean and the North Sea. Molecular Ecology, 13, 403-417.
38. Hampe, A. & Petit, R.J. (2005) Conserving biodiversity under climate change: the rear edge matters. Ecology Letters, 8, 461-467.
39. Harley, C.D.G., Hughes, A.R., Hultgren, K.M., Miner, B.G., Sorte, C.J.B., Thornber, C.S., Rodriguez, L.F., Tomanek, L. & Williams, S.L. (2006) The impacts of climate change in coastal marine systems. Ecology Letters, 9, 228-241.
40. Hewitt, G.M. (1999) Post-glacial re-colonization of European biota. Biological Journal of the Linnean Society, 68, 87-112.
41. Hewitt, G.M. (2000) The genetic legacy of the Quaternary ice ages. Nature, 405, 907-913.
42. Hoarau, G., Coyer, J.A., Veldsink, J.H., Stam, W.T. & Olsen, J.L. (2007) Glacial refugia and recolonization pathways in the brown seaweed Fucus serratus. Molecular Ecology, 16, 3606-3616.
43. Hoek, C. (1987) The possible significance of long-range dispersal for the biogeography of seaweeds. Helgoländer Meeresunters, 41, 261-272.
44. Hofreiter, M. & Stewart, J. (2009) Ecological change, range fluctuations and population dynamics during the Pleistocene. Current Biology, 19, R584-R594.
45. Ibrahim, K.M., Nichols, R.A. & Hewitt, G.M. (1996) Spatial patterns of genetic variation generated by different forms of dispersal during range expansion. Heredity, 77, 282-291.
46. Irwin, D.E. (2002) Phylogeographic breaks without geographic barriers to gene flow. Evolution, 56, 2383-2394.
47. Jensen, J.L., Bohonak, A.J. & Kelley, S.T. (2005) Isolation by distance, web service. BMC Genetics, 6, 13.
48. ST and its relatives do not measure differentiation. Molecular Ecology, 17, 4015-4026.
49. Kelly, D.W., MacIsaac, H.J. & Heath, D.D. (2006) Vicariance and dispersal effects on phylogeographic structure and speciation in a widespread estuarine invertebrate. Evolution, 60, 257-267.
50. Kinlan, B.P. & Gaines, S.D. (2003) Propagule dispersal in marine and terrestrial environments: a community perspective. Ecology, 84, 2007-2020.
51. Kinlan, B.P., Gaines, S.D. & Lester, S.E. (2005) Propagule dispersal and the scales of marine community process. Diversity and Distributions, 11, 139-148.
52. Langella, O. (1999) POPULATIONS 1.2.30. Available at:
53. Lein, T.E. (1984) Distribution, reproduction, and ecology of Fucus ceranoides L. (Phaeophyceae) in Norway. Sarsia, 69, 75-81.
54. Lomolino, M.V., Riddle, B.R. & Brown, J.H. (2005) Biogeography, 3rd edn. Sinauer Associates, Sunderland, MA.
55. Lyons, D.A. & Scheibling, R.E. (2009) Range expansion by invasive marine algae: rates and patterns of spread at a regional scale. Diversity and Distributions, 15, 762-775.
56. Maggs, C.A., Castilho, R., Foltz, D., Henzler, C., Jolly, M.T., Kelly, J., Olsen, J., Perez, K.E., Stam, W., Väinölä, R., Viard, F. & Wares, J. (2008) Evaluating signatures of glacial refugia for North Atlantic benthic marine taxa. Ecology, 89, 108-122.
57. McKenzie, P.F. & Bellgrove, A. (2008) Dispersal of Hormosira banksii (Phaeophyceae) via detached fragments: reproductive viability and longevity. Journal of Phycology, 44, 1108-1115.
58. Ménot, G., Bard, E., Rostek, F., Weijers, J.W.H., Hopmans, E.C., Schouten, S. & Damste, J.S.S. (2006) Early reactivation of European rivers during the last deglaciation. Science, 313, 1623-1625.
59. Munda, I.M. (1999) The benthic algal vegetation of land-locked fjords in southeastern Iceland. Hydrobiologia, 393, 169-180.
60. Neiva, J., Pearson, G.A., Valero, M. & Serrão, E.A. (2010) Surfing the wave on a borrowed board: range expansion and spread of introgressed organellar genomes in the seaweed Fucus ceranoides L. Molecular Ecology, 19, 4812-4822.
61. Norton, T.A. (1992) Dispersal by macroalgae. British Phycological Journal, 27, 293-301.
62. Olsen, J.L., Stam, W.T., Coyer, J.A., Reusch, T.B.H., Billingham, M., Bostrom, C., Calvert, E., Christie, H., Granger, S., La Lumiere, R., Milchakova, N., Oudot-Le Secq, M.P., Procaccini, G., Sanjabi, B., Serrão, E., Veldsink, J., Widdicombe, S. & Wyllie-Echeverria, S. (2004) North Atlantic phylogeography and large-scale population differentiation of the seagrass Zostera marina L. Molecular Ecology, 13, 1923-1941.
63. Olsen, J.L., Zechman, F.W., Hoarau, G., Coyer, J.A., Stam, W.T., 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. Journal of Biogeography, 37, 842-856.
64. Pascual, M., Aquadro, C.F., Soto, V. & Serra, L. (2001) Microsatellite variation in colonizing and Palearctic populations of Drosophila subobscura. Molecular Biology and Evolution, 18, 731-740.
65. Pearson, G.A. & Serrão, E.A. (2006) Revisiting synchronous gamete release by fucoid algae in the intertidal zone: fertilization success and beyond? Integrative and Comparative Biology, 46, 587-597.
66. Pearson, G.A., Lago-Leston, A. & Mota, C. (2009) Frayed at the edges: selective pressure and adaptive response to abiotic stressors are mismatched in low diversity edge populations. Journal of Ecology, 97, 450-462.
67. Perrin, C., Daguin, C., van de Vliet, M., Engel, C.R., Pearson, G.A. & Serrão, E.A. (2007) Implications of mating system for genetic diversity of sister algal species: Fucus spiralis and Fucus vesiculosus (Heterokontophyta, Phaeophyceae). European Journal of Phycology, 42, 219-230.
68. Petit, R.J., Brewer, S., Bordacs, S. et al. (2002) Identification of refugia and post-glacial colonisation routes of European white oaks based on chloroplast DNA and fossil pollen evidence. Forest Ecology and Management, 156, 49-74.
69. Pritchard, J.K., Stephens, M. & Donnelly, P. (2000) Inference of population structure using multilocus genotype data. Genetics, 155, 945-959.
70. Provan, J. & Maggs, C.A. (2012) Unique genetic variation at a species' rear edge is under threat from global climate change. Proceedings of the Royal Society B: Biological Sciences, 279, 39-47.
71. Provan, J., Wattier, R.A. & Maggs, C.A. (2005) Phylogeographic analysis of the red seaweed Palmaria palmata reveals a Pleistocene marine glacial refugium in the English Channel. Molecular Ecology, 14, 793-803.
72. Remerie, T., Vierstraete, A., Weekers, P.H.H., Vanfleteren, J.R. & Vanreusel, A. (2009) Phylogeography of an estuarine mysid, Neomysis integer (Crustacea, Mysida), along the north-east Atlantic coasts. Journal of Biogeography, 36, 39-54.
73. Roman, J. & Palumbi, S.R. (2004) A global invader at home: population structure of the green crab, Carcinus maenas, in Europe. Molecular Ecology, 13, 2891-2898.
74. Serrão, E.A., Kautsky, L. & Brawley, S.H. (1996) Distributional success of the marine seaweed Fucus vesiculosus L. in the brackish Baltic Sea correlates with osmotic capabilities of gametes. Oecologia, 107, 1-12.
75. Serrão, E.A., Kautsky, L., Lifvergren, T. & Brawley, S.H. (1997) Gamete dispersal and pre-recruitment mortality in Baltic Fucus vesiculosus. Phycologia, 36, 388.
76. Stewart, J.R. & Dalén, L. (2008) Is the glacial refugium concept relevant for northern species? A comment on Pruett and Winker 2005. Climatic Change, 86, 19-22.
77. Stewart, J.R. & Lister, A.M. (2001) Cryptic northern refugia and the origins of the modern biota. Trends in Ecology and Evolution, 16, 608-613.
78. Stewart, J.R., Lister, A.M., Barnes, I. & Dalen, L. (2010) Refugia revisited: individualistic responses of species in space and time. Proceedings of the Royal Society B: Biological Sciences, 277, 661-671.
79. Svenning, J.C., Normand, S. & Kageyama, M. (2008) Glacial refugia of temperate trees in Europe: insights from species distribution modelling. Journal of Ecology, 96, 1117-1127.
80. Taberlet, P., Fumagalli, L., Wust-Saucy, A.G. & Cosson, J.F. (1998) Comparative phylogeography and postglacial colonization routes in Europe. Molecular Ecology, 7, 453-464.
81. Tatarenkov, A., Jonsson, R.B., Kautsky, L. & Johannesson, K. (2007) Genetic structure in populations of Fucus vesiculosus (Phaeophyceae) over spatial scales from 10m to 800km. Journal of Phycology, 43, 675-685.
82. Thiel, M. & Haye, P.A. (2006) The ecology of rafting in the marine environment. III. Biogeographical and evolutionary consequences. Oceanography and Marine Biology: An Annual Review, 44, 323-429.
83. Toonen, R.J. & Hughes, S. (2001) Increased throughput for fragment analysis on an ABI PRISM (R) automated sequencer using a membrane comb and STRand software. BioTechniques, 31, 1320-1324.
84. Turner, T.F., Wares, J.P. & Gold, J.R. (2002) Genetic effective size is three orders of magnitude smaller than adult census size in an abundant, estuarine-dependent marine fish (Sciaenops ocellatus). Genetics, 162, 1329-1339.
85. Vernet, P. & Harper, J.L. (1980) The costs of sex in seaweeds. Biological Journal of the Linnean Society, 13, 129-138.
86. Viejo, R.M., Martinez, B., Arrontes, J., Astudillo, C. & Hernandez, L. (2010) Reproductive patterns in central and marginal populations of a large brown seaweed: drastic changes at the southern range limit. Ecography, 33, 1-10.
87. Wallace, A.L., Klein, A.S. & Mathieson, A.C. (2004) Determining the affinities of salt marsh fucoids using microsatellite markers: evidence of hybridization and introgression between two species of Fucus (Phaeophyta) in a Maine estuary. Journal of Phycology, 40, 1013-1027.
88. Wares, J.P. & Cunningham, C.W. (2001) Phylogeography and historical ecology of the North Atlantic intertidal. Evolution, 55, 2455-2469.
89. Weir, B.S. & Cockerham, C.C. (1984) Estimating F-statistics for the analysis of population structure. Evolution, 38, 1358-1370.
90. Wilson, G.A. & Rannala, B. (2003) Bayesian inference of recent migration rates using multilocus genotypes. Genetics, 163, 1177-1191.