Biodiversity Science ›› 2013, Vol. 21 ›› Issue (3): 306-314.doi: 10.3724/SP.J.1003.2013.09029

• Orginal Article • Previous Article     Next Article

Population genetics and demographic history of red seaweed, Palmaria palmata, from the Canada-northwest Atlantic

Jingjing Li1, 2, Jie Zhang1, 2, Zimin Hu1, *(), Delin Duan1, *()   

  1. 1 Institute of Oceanology, Chinese Academy of Sciences, Qingdao, Shandong 266071
    2 University of Chinese Academy of Sciences, Beijing 100049
  • Received:2013-01-30 Accepted:2013-03-28 Online:2013-06-05
  • Hu Zimin,Duan Delin;

The paleoclimate change (e.g. the glacial fluctuation in the late Pleistocene) played an important role in shaping species’ population genetic structure, geographic distribution patterns, and gradient of diversity and composition. In this study, we sampled eight populations (138 individuals) of Palmaria palmata, a commercially and ecologically important red macroalga found on both sides of the North Atlantic coast, aiming to assess the genetic structure and demographic history through the integration of mitochondrial cox2-3 spacer and RAPD variation. Eleven mtDNA cox2-3 haplotypes were detected, one of which (C3) was common and located centrally in a haplotype network. It is shared by all populations and is regarded as ancestral. Two northern populations from the Gulf of St. Lawrence had highest levels of genetic diversity, and were significantly divergent from all other populations. AMOVA showed that highest genetic variation for cox2-3 occurred within populations, while less existed among groups. This was consistent with the results of a STRUCTURE clustering analysis of RAPD data. Our genetic diversity and haplotype network analyses indicated that multiple glacial refugia might have existed for the species along the Canada-north- west Atlantic coast. Furthermore, Bayesian skyline plot analysis based on cox2-3 spacer sequences indicated that population size underwent a slight increase over temporal and spatial scales. This occurred in approximately 0.18-0.13 million years ago. Pairwise genetic distance (K2P) between populations from the Gulf of St. Lawrence and the Bay of Fundy was 0.2%, indicating that they diverged from their common ancestor since about 0.36 million years ago. The evidence from our study suggests that climatic oscillations during the late Pleistocene had a drastic influence on the demography and genetic diversity of P. palmatain the Canada-northwest Atlantic.

Key words: Palmaria palmata, the Last Glacial Maximum, cox2-3, genetic structure, genetic diversity

Fig. 1

Morphological characters of Palmaria palmata. (a) Living intertidal habitat of P. palmata from County Clare, Ireland in 2008. It is frequently found living on thallus of red marcroalga Chondrus crispus and brown macroalga Fucus serratus; (b) Purple morphological features of P. palmata from Bonne Bay, Canada."

Table 1

Sampling details of eight Palmaria palmata populations, including abbreviation codes, geographic location, sample size (N), number of haplotypes (Nh), types of haplotype (H), haplotype diversity (h), and nucleotide diversity (π)"

h (SD)
π (SD)
Gulf of St. Lawrence
LA L’Anse Amour, Canada 52.32°N, 56.60°W 25 3 C1, C2, C3 0.640 (0.052) 0.0024 (0.0020)
BB Bonne Bay, Canada 49.51°N, 57.92°W 31 3 C1, C3, C4 0.540 (0.043) 0.0018 (0.0017)
GP Gaspe, Canada 48.88°N, 64.50°W 11 1 C3 0.000 (0.000) 0.0000 (0.0000)
RS Rimouski, Canada 48.47°N, 68.51°W 24 2 C3, C5 0.083 (0.075) 0.0002 (0.0005)
Bay of Fundy
MB Maces Bay, Canada 45.11°N, 66.75°W 8 2 C3, C6 0.250 (0.180) 0.0008 (0.0011)
VB Victoria Beach, Canada 44.69°N, 65.75°W 9 3 C3, C7, C8 0.417 (0.191) 0.0014 (0.0016)
LT Letete, Canada 45.06°N, 66.89°W 12 2 C3, C9 0.303 (0.148) 0.0009 (0.0012)
WH White Head, Canada 44.63°N, 66.72°W 18 3 C3, C10, C11 0.451 (0.117) 0.0015 (0.0015)

Fig. 2

Distribution of mitochondrial cox2-3 haplotypes of Palmaria palmata populations and median-joining haplotype network. Population codes correspond to those in Table 1."

Table 2

Molecular variance (AMOVA) of Palmaria palmata populations. The eight populations were clustered into two groups: the Gulf of St. Lawrence and the Bay of Fundy."

Source of variations
Variance components
% of variation
Fixation indices
群组间 Among groups 1 0.0409 10.12 FCT = 0.10118NS
种群间 Among populations within groups 6 0.1246 34.09 Fsc = 0.37928***
种群内 Within populations 130 0.2075 55.79 FST = 0.44509***

Fig. 3

Population structuring analysis based on RAPD data with STRUCTURE. Each vertical bar indicates the multi-locus genotype of one individual, and colors represent the K virtual clusters. Population codes are the same as Table 1."

Fig. 4

Demographic history of Palmaria palmata. (a) Mismatch distributions of Palmaria palmata populations. The abscissa indicates the number of pairwise differences between compared sequences. The ordinate is the frequency for each value. Bars represent the observed distribution of pairwise differences, while the solid line shows the expected distribution; (b) Bayesian skyline plots show effective population size as a function of time. The upper and lower limits of grey trend represent the 95% confidence intervals of higher probability density (HPD) analysis."

22 Krebes L, Blank M, Bastrop R (2011) Phylogeography, historical demography and postglacial colonization routes of two amphi-Atlantic distributed amphipods. Systematics and Biodiversity, 9, 259-273.
23 Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25, 1451-1452.
24 Lindstrom SC, Olsen JL, Stam WT (1996) Recent radiation of the Palmariaceae (rhodophyta). Journal of Phycology, 32, 457-468.
25 Lindstrom SC, Olsen JL, Stam WT (1997) Postglacial recolonization and the biogeography of Palmaria mollis (Rhodophyta) along the Northeast Pacific coast. Canadian Journal of Botany, 75, 1887-1896.
26 Lister A, Hewitt GM (2004) Genetic consequences of climatic oscillations in the Quaternary. Philosophical Transactions of the Royal Society B: Biological Sciences, 359, 183-195.
27 Maggs CA, Castilho R, Foltz D, Henzler C, Jolly MT, Kelly J, Olsen J, Perez KE, Stam W, Väinölä R, Viard F, Wares J (2008) Evaluating signatures of glacial refugia for North Atlantic benthic marine taxa. Ecology, 89, S108-S122.
28 Olsen JL, Zechman FW, Hoarau G, Coyer JA, Stam WT, Valero M, Åberg 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.
29 Panova M, Blakeslee AMH, Miller AW, Mäkinen T, Ruiz GM, Johannesson K, André C (2011) Glacial history of the North Atlantic marine snail, Littorina saxatilis, inferred from distribution of mitochondrial DNA lineages. PLoS ONE, 6, e17511.
30 Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics, 14, 817-818.
31 Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics, 155, 945-959.
32 Provan J, Bennett KD (2008) Phylogeographic insights into cryptic glacial refugia. Trends in Ecology and Evolution, 23, 564-571.
33 Provan J, Wattier RA, Maggs CA (2005) Phylogeographic analysis of the red seaweed Palmaria palmata reveals a Pleistocene marine glacial refugium in the English Channel. Molecular Ecology, 14, 793-803.
34 Ray N, Currat M, Excoffier L (2003) Intra-deme molecular diversity in spatially expanding populations. Molecular Biology and Evolution, 20, 76-86.
35 Riggs SR, Snyder SW, Hine AC, Mearns DL (1996) Hardbottom morphology and relationship to the geologic framework: mid-Atlantic continental shelf. Journal of Sedimentary Research, 66, 830-846.
36 Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Molecular Biology and Evolution, 9, 552-569.
37 Saunders GW (2004) A chronicle of the convoluted systematics of the red algal orders Palmariales and Rhodymeniales (Florideophyceae, Rhodophyta). CEMAR Occasional Notes in Phycology, 1, 1-16.
38 Strimmer K, Pybus OG (2001) Exploring the demographic history of DNA sequences using the generalized skyline plot. Molecular Biology and Evolution, 18, 2298-2305.
39 Svendsen JI, Alexanderson H, Astakhov VI, Demidov I, Dowdeswell JA, Funder S, Gataullin V, Henriksen M, Hjort C, Houmark-Nielsen M, Hubberten HW, Ingólfsson O, Jakobsson M, Kjaer KH, Larsen E, Lokrantz H, Lunkka JP, Lyså A, Mangerud J, Matiouchkov A, Murray A, Möller P, Niessen F, Nikolskaya O, Polyak L, Saarnisto M, Siegert C, Siegert MJ, Spielhagen RF, Stein R (2004) Late quaternary ice sheet history of northern Eurasia. Quaternary Science Reviews, 23, 1229-1271.
40 Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics, 123, 585-595.
41 Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution, 28, 2731-2739.
42 Teasdale BW, Klein AS (2010) Genetic variation and biogeographical boundaries within the red alga Porphyra umbilicalis (Bangiales, Rhodophyta). Botanica Marina, 53, 417-431.
43 Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research, 25, 4876-4882.
44 Vermeij GJ (1991) Anatomy of an invasion: the trans-Arctic interchange. Paleobiology, 17, 281-307.
45 Victoria M, Miagostovich MP, Ferreira MSR, Vieira CB, Fioretti JM, Leite JPG, Colina R, Cristina J (2009) Bayesian coalescent inference reveals high evolutionary rates and expansion of Norovirus populations. Infection, Genetics and Evolution, 9, 927-932.
46 Wares JP (2002) Community genetics in the Northwestern Atlantic intertidal. Molecular Ecology, 11, 1131-1144.
47 Wares JP, Cunningham CW (2001) Phylogeography and historical ecology of the North Atlantic intertidal. Evolution, 55, 2455-2469.
48 Zuccarello GC, Burger G, West JA, King RJ (1999) A mitochondrial marker for red algal intraspecific relationships. Molecular Ecology, 8, 1443-1447.
49 Zuccarello GC, West JA (2002) Phylogeography of the Bostrychia calliptera-B. pinnata complex (Rhodomelaceae, Rhodophyta) and divergence rates based on nuclear, mitochondrial and plastid DNA markers. Phycologia, 41, 49-60.
1 Addison JA, Hart MW (2005) Colonization, dispersal, and hybridization influence phylogeography of North Atlantic sea urchins (Strongylocentrotus droebachiensis). Evolution, 59, 532-543.
2 Albaina N, Olsen JL, Couceiro L, Ruiz JM, Barreiro R (2012) Recent history of the European Nassarius nitidus (Gastropoda): phylogeographic evidence of glacial refugia and colonization pathways. Marine Biology, 159, 1871-1884.
3 Bandelt HJ, Forster P, Rohl A (1999) Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution, 16, 37-48.
4 Bigg GR, Cunningham CW, Ottersen G, Pogson GH, Wadley MR, Williamson P (2008) Ice-age survival of Atlantic cod: agreement between palaeoecology models and genetics. Proceedings of the Royal Society B: Biological Sciences, 275, 163-172.
5 Campo D, Molares J, Garcia L, Fernandez-Rueda P, Garcia- Gonzalez C, Garcia-Vazquez E (2010) Phylogeography of the European stalked barnacle (Pollicipes pollicipes): identification of glacial refugia. Marine Biology, 157, 147-156.
6 Charbit S, Ritz C, Philippon G, Peyaud V, Kageyama M (2007) Numerical reconstructions of the Northern Hemisphere ice sheets through the last glacial-interglacial cycle. Climate of the Past, 3, 15-37.
7 Drummond AJ, Rambaut A, Shapiro B, Pybus OG (2005) Bayesian coalescent inference of past population dynamics from molecular sequences. Molecular Biology and Evolution, 22, 1185-1192.
8 Drummond AJ, Ho SYW, Phillips MJ, Rambaut A (2006) Relaxed phylogenetics and dating with confidence. PLoS Biology, 4, 699-710.
9 Drummond AJ, Suchard MA, Xie D, Rambaut A (2012) Bayesian Phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution, 29, 1969-1973.
10 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.
11 Excoffier L (2004) Patterns of DNA sequence diversity and genetic structure after a range expansion: lessons from the infinite-island model. Molecular Ecology, 13, 853-864.
12 Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources, 10, 564-567.
13 Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics, 131, 479-491.
14 Flint RF (1940) Pleistocene features of the Atlantic Coastal Plain. American Journal of Science, 238, 757-787.
15 Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics, 147, 915-925.
16 Hewitt GM (1996) Some genetic consequences of ice ages, and their role in divergence and speciation. Biological Journal of the Linnean Society, 58, 247-276.
17 Hoarau G, Coyer JA, Veldsink JH, Stam WT, Olsen JL (2007) Glacial refugia and recolonization pathways in the brown seaweed Fucus serratus. Molecular Ecology, 16, 3606-3616.
18 Hu ZM, Guiry MD, Critchley AT, Duan DL (2010) Phylogeographic patterns indicate transatlantic migration from Europe to North America in the red seaweed Chondrus Crispus (Gigartinales, Rhodophyta). Journal of Phycology, 46, 889-900.
19 Hu ZM, Li W, Li JJ, Duan DL (2011) Post-Pleistocene demographic history of the North Atlantic endemic Irish moss Chondrus crispus: glacial survival, spatial expansion and gene flow. Journal of Evolutionary Biology, 24, 505-517.
20 Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution, 16, 111-120.
21 Kingman JFC (1982) On the genealogy of large populations. Journal of Applied Probability, 19, 27-43.
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[9] . [J]. Chin J Plan Ecolo, 2013, 37(3): 276 .
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