Abstract
Documenting the scale of movement among populations is an important challenge for marine ecology. Using nine microsatellite markers, evidence of genetic structure in a marine kelp, the sea palm Postelsia palmaeformis Ruprecht, was examined in the vicinity of Cape Flattery, Washington state, USA (48° 24′ N, 124°44′ W). Genetic clustering analysis implemented without reference to geographic structure strongly suggested that a number of distinct genetic clusters existed among the 245 plants sampled in August in the years 1997–2001. Subsequent analysis showed that clustering was associated with geographically defined populations both among (km scale) and within (m scale) sampling sites. F st analysis of geographically defined populations revealed significant genetic differentiation among populations of plants as little as 5 m apart, evidence of genetic structuring at even smaller scales, and a sharp increase in F st across populations separated by up to 23 m. F st values were also high and approximately unchanging (F st=0.470) for populations separated by greater distances (up to 11 km), consistent with a scenario of rare dispersal by detached, floating plants carried by variable currents. The results corroborate natural history observations suggesting that P. palmaeformis has extremely short (1–3 m) spore dispersal distances, and indicate that the dynamics of sea palm populations are more affected by local processes than recruitment from distant populations.
Similar content being viewed by others
References
Abbott IA, Hollenberg GJ (1976) Marine algae of California. Stanford University Press, Stanford
Avise JC (2004) Molecular markers, natural history and evolution. Sinauer Press, Sunderland
Billot C, Engel CR, 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. Mar Ecol Prog Ser 253:111–121
Bohonak AJ (1999) Dispersal, gene flow, and population structure. Q Rev Biol 74:21–45
Coleman MA, Brawley SH (2004) Spatial and temporal variability in dispersal and population genetic structure in a marine metapopulation. Abstract presented at the Ecological Society of America annual meeting, Portland, Oregon http://www.abstracts.co.allenpress.com/pweb/esa2004/document/?ID=35254
Coleman MA, Brawley SH (2005) Are life history characteristics good predictors of genetic diversity and structure? A case study of the intertidal alga Fucus spiralis (Heterokontophyta; Phaeophyceae). J Phycol 41:753–762
Colin PL (2003) Larvae retention: genes or oceanography? Science 300:1657
Coyer JA, Olsen JL, Stam WT (1997) Genetic variability and spatial separation in the sea palm kelp Postelsia palmaeformis (Phaeophyceae) as assessed with M13 fingerprints and RAPDS. J Phycol 33:561–568
Dayton PK (1973) Dispersion, dispersal. And persistence of the annual intertidal alga, Postelsia palmaeformis Ruprecht. Ecology 54:433–438
Duffy JE (1993) Genetic population structure in two tropical sponge-dwelling shrimps that differ in dispersal potential. Mar Biol 116:459–470
Deysher L, Norton TA (1982) Dispersal and colonisation in Sargassum muticum (Yendo) Fensholt. J Exp Mar Biol Ecol 56:179–195
Engel CR, Wattier R, Destombe C, Valero M (1999) Performance of non-motile male gametes in the sea: analysis of paternity and fertilization success in a natural population of a red seaweed, Glacilaria gracilis. Proc R Soc Lond B 266:1879–1886
Fain SR, Druehl LD, Baillie DL (1988) Repeat and single copy chloroplast DNA. J Phycol 24:292–302
Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587
Grosberg R, Cunningham CW (2001) Genetic structure in the sea: from populations to communities. In: Bertness MD, Gaines SD, Hay ME (eds) Marine community ecology. Sinauer, Sunderland, pp 61–84
Grosberg RK (1991) Sperm-mediated gene flow and the genetic structure of a population of the colonial ascidian Botryllus schlosseri. Evolution 45:130–142
Hedrick PW (1999) Perspective: highly variable loci and their interpretation in evolution and conservation. Evolution 53:313–318
Hellberg ME (1994) Relationships between inferred levels of gene flow and geographic distance in a philopatric coral, Balanophyllia elegans. Evolution 48:1829–1854
Hellberg ME (1996) Dependence of gene flow on geographic distance in two solitary corals with different larval dispersal capabilities. Evolution 50:1167–1175
Jones GP, Milicich MJ, Emslie MJ, Lunow C (1999) Self-recruitment in a coral reef fish population. Nature 402:802–804
Kain JM (1964) Aspects of the biology of Laminaria hyperborea. III. Survival and growth of gametophytes. J Mar Biol Assoc UK 44:415–433
Kalvass PE (1994) The effect of different harvest methods on sea palm (Postelsia palmaeformis) sporophyll growth. California Fish Game 80:57–67
Klautau M, Russo CAM, Lazoski C, Boury-Esnault N, Thorpe JP, Sole-Cava AM (1999) Does cosmopolitanism result from overconservative systematics? A case study using the marine sponge Chondrilla nucula. Evolution 53:1414–1422
Kusumo HT, Druehl LD (2000) Variability over space and time in the genetic structure of the winged kelp Alaria marginata. Mar Biol 136:397–409
Kusumo HT, Pfister CA, Wootton JT (2004) Dominant (AFLP) and codominant (microsatellite) markers for the kelp Postelsia palmaeformis (Laminariales). Mol Ecol Notes 4:372–375
Kyle CJ, Boulding EG (2000) Comparative population genetic structure of marine gastropods (Littorina spp.) with and without pelagic larval dispersal. Mar Biol 137:835–845
Leigh EG Jr, Paine RT, Quinn JF, Suchanek TH (1987) Wave energy and intertidal productivity. Proc Natl Acad Sci USA 84:1314–1318
Levinton JS, Suchanek TH (1979) Geographic variation, niche breadth, and genetic differentiation at different geographic scales in the mussels Mytilus californianus and Mytilus edulis. Mar Biol 49:363–376
Lindstrom SC, Olsen JL, Stam WT (1997) Postglacial recolonization and the biogeography of Palmaria mollis (Rhodophyta) along the Northeast Pacific coast. Can J Bot 75:1887–1896
Martínez EA, Cárdenas L, Pinto R (2003) Recovery and genetic diversity of the intertidal kelp Lessonia nigrescens (Phaeophyceae) 20 years after El Niño 1982/83. J Phycol 39:504–508
Lu TT, Williams SL (1994) Genetic diversity and genetic structure in the brown alga Halidrys dioica (Fucales: Cystoseiraceae) in Southern California. Mar Biol 121:363–371
McFadden CS (1997) Contributions of sexual and asexual reproduction to population structure in the clonal soft coral, Alcyonium rudyi. Evolution 51:112–126
Olson RR (1985) The consequences of short distance larval dispersal in a sessile marine invertebrate. Ecology 66:30–39
Paine RT (1979) Disaster, catastrophe, and local persistence of the sea palm Postelsia palmaeformis. Science 205:685–687
Paine RT (1988) Habitat suitability and local population persistence of the sea palm Postelsia palmaeformis. Ecology 69:1787–1794
Palumbi SR (1994) Genetic divergence, reproductive isolation, and marine speciation. Ann Rev Ecol Syst 25:547–572
Palumbi SR (1995) Using genetics as an indirect estimator of larval dispersal. In: McEdward L (ed) Ecology of marine invertebrate larvae. CRC Press, New York, pp 369–387
Palumbi SR, Warner RR (2003) Why gobies are like hobbits. Science 299:51–52
Palumbi SR, Wilson AC (1990) Mitochondrial DNA diversity in the sea urchins Strongylocentrotus purpuratus and Strongylocentrotus droebachiensis. Evolution 44:403–415
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Reed DC, Amsler CD, Ebeling AW (1992) Dispersal in kelps:factors affecting spore swimming and competency. Ecology 73:1577–1585
Reusch TBH (2002) Microsatellites reveal high population connectivity in eelgrass (Zostera marina) in two contrasting coastal areas. Limnol Oceanogr 47:78–85
Reusch TBH, Stam WT, Olsen JL (2000) A microsatellite-based estimation of clonal diversity and population subdivision in Zostera marina, a marine flowering plant. Mol Ecol 9:127–140
Roughgarden J, Gaines SD, Possingham H (1988) Recruitment dynamics in complex life cycles. Science 241:1460–1466
Ruckelshaus M (1998) Spatial scale of genetic structure and an indirect estimate of gene flow in eelgrass, Zostera marina. Evolution 52:330–343
Santelices B (1990) Patterns of reproduction, dispersal and recruitment in seaweeds. Oceanogr Mar Biol Annu Rev 28:177–276
Schneider S, Roessli D, Excoffier L (2000) Arlequin: a software for population genetics data analysis. Ver 2.000. Genetics and Biometry Lab, Department of Anthropology, University of Geneva
Shulman MJ, Bermingham E (1995) Early life histories, ocean currents, and the population genetics of Caribbean reef fishes. Evolution 49:897–910
Sousa WP (1984) Intertidal mosaics: patch size, propagule availability, and spatially variable patterns of succession. Ecology 65:1918–1935
Spight TM (1974) Sizes of populations of a marine snail. Ecology 55:712–729
Swearer SE, Caselle JE, Lea DW, Warner RR (1999) Larval retention and recruitment in an island population of a coral-reef fish. Nature 402:799–802
Taylor MS, Hellberg ME (2003) Genetic evidence for local retention of pelagic larvae in a Caribbean reef fish. Science 299:107–109
Thorson G (1950) Reproductive and larval ecology of marine bottom invertebrates. Biol Rev 25:1–45
van der Strate HJ, van de Zande L, Stam WT, Haroun RJ, Olsen JL (2003) Within-island differentiation and between-island homogeneity: Non-equilibrium population structure in the seaweed Cladophoropsis membranacea (Chlorophyta) in the Canary Islands. Eur J Phycol 38:15–23
Waples RS (1987) A multispecies approach to the analysis of gene flow in marine shore fishes. Evolution 41:385–400
Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370
Williams SL, Di Fiori RE (1996) Genetic diversity and structure in Pelvetia fastigata (Phaeophyta: Fucales): does a small effective neighborhood size explain fine-scale genetic structure? Mar Biol 126:371–382
Williams ST, Benzie JAH (1996) Genetic uniformity of widely separated populations of the coral reef starfish Linckia laevigata from the East Indian and West Pacific Oceans, revealed by allozyme electrophoresis. Mar Biol 126:99–107
Worcester SE (1994) Adult rafting versus larval swimming: dispersal and recruitment of a botryllid ascidian on eelgrass. Mar Biol 121:309–317
Wright JT, Zuccarello GC, Steinberg PD (2000) Genetic structure of the subtidal red alga Delisea pulchra. Mar Biol 136:439–448
Wright S (1951) The genetical structure of populations. Ann Eugen 15:323–353
Wright S (1965) The interpretation of population structure by F-statistics with special regard to systems of mating. Evolution 19:395–420
Yoshiyama RM, Sassaman C (1987) Geographical patterns of allozymic variation in three species of intertidal sculpins. Environ Biol Fish 20:203–218
Yund PO (1995) Gene flow via the dispersal of fertilizing sperm in a colonial ascidian (Botryllus schlosseri): the effect of male density. Mar Biol 122:649–654
Yund PO, O’Neil PG (2000) Microgeographic genetic differentiation in a colonial ascidian (Botryllus schlosseri) population. Mar Biol 137:583–588
Zuccarello GC, Yeates PH, Wright JT, Bartlett J (2001) Population structure and physiological differentiation of haplotypes of Caloglossa leprieurii (Rhodophyta) in a mangrove intertidal zone. J Phycol 37:235–244
Acknowledgements
We are indebted to the Makah Tribal Council for granting long-term access to Tatoosh Island and the mainland study sites. J. Salamunovitch, F. Stevens, K. Rose, B. Kordas, L. Weis, B. Scott, A. Miller, K. Edwards, J. Duke, and R. Paine provided essential field and laboratory assistance. We also thank R. Hudson, J. Gladstone, K. Tarvin, K. Feldheim, R. Grosberg, J. Pritchard, and M. Hellberg for helpful technical advice, and J. Bergelson and T. Carr for the use of equipment. The study was supported by NSF grant OCE-0117801, the University of Chicago Faculty Research Fund, and the Andrew W. Mellon Foundation.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by J.P. Grassle, New Brunswick
Rights and permissions
About this article
Cite this article
Kusumo, H.T., Pfister, C.A. & Wootton, J.T. Small-scale genetic structure in the sea palm Postelsia palmaeformis Ruprecht (Phaeophyceae). Mar Biol 149, 731–742 (2006). https://doi.org/10.1007/s00227-006-0254-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00227-006-0254-z