Seascape analysis reveals regional gene flow patterns among populations of a marine planktonic diatom

Proceedings of the Royal Society B: Biological Sciences

Volumn 280, Issue 1773, 2013, Pages

  Godhe, Anna ^a   Egardt, Jenny ^a   Kleinhans, David ^a,b   Sundqvist, Lisa ^a   Hordoir, Robinson ^c   Jonsson, Per R ^d  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b UNIVERSITY OF OLDENBURG   (Germany)

^c SWEDISH METEOROLOGICAL AND HYDROLOGICAL INSTITUTE   (Sweden)

^d GÖTEBORG UNIVERSITY   (Sweden)

Author keywords

Bacillariophyceae; Microsatellites; Oceanographic connectivity; Skeletonema marinoi

Indexed keywords

CONNECTIVITY; DIATOM; GENE FLOW; GENETIC MARKER; GENETIC STRUCTURE; MARINE ENVIRONMENT; OCEANIC CIRCULATION; PHYTOPLANKTON; PRIMARY PRODUCTION;

ATLANTIC OCEAN; NORTH SEA; SCANDINAVIA; SKAGERRAK;

BACILLARIOPHYCEAE; BACILLARIOPHYTA; NITZSCHIA ALBA; SKELETONEMA MARINOI;

EID: 84886999162     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2013.1599     Document Type: Article

References (59)

1. Rynearson TA, Armburst EV. 2004 Genetic differentiation among populations of the planktonic marine diatom Ditylum brightwellii (Bacillariophyceae). J. Phycol. 40, 34-43. (doi:10.1046/j.1529-8817.2004.03089.x)
2. Nagai S, Nishitani G, Sakamoto S, Sugaya T, Lee C, Kim C, Itakura S, Yamaguchi M. 2009 Genetic structururing and transfer of marine dinoflagellate Cochlodinium polykrikoides in Japanese and Korean coastal waters revealed by microsatellites. Mol. Ecol. 18, 2337-2352. (doi:10.1111/j.1365-294X.2009.04193.x)
3. Evans KM, Kuhn SF, Hayes PK. 2005 High levels of genetic diversity and low levels of genetic differentiation in North Sea Pseudo-nitzschia pungens (Bacillariophyceae) populations. J. Phycol. 41, 506-514. (doi:10.1111/j.1529-8817. 2005.00084.x)
4. Godhe A, Härnström K. 2010 Linking the planktonic and benthic habitat: genetic structure of the marine diatom Skeletonema marinoi. Mol. Ecol. 19, 4478-4490. (doi:10.1111/j.1365-294X.2010.04841.x)
5. White C, Delkoe KA, Watson J, Siegel DA, Zacherl DC, Toonen RJ. 2010 Ocean currents help explain population genetic structure. Proc. R. Soc. B 277, 1685-1694. (doi:10.1098/rspb.2009.2214)
6. Casabianca S, Penna A, Pecchioli E, Jordi A, Basterretxea G, Vernesi C. 2012 Population genetic structure and connectivity of the harmful dinoflagellate Alexandrium minutum in the Mediterranean Sea. Proc. R. Soc. B 279, 129-138. (doi:10.1098/rspb.2011.0708)
7. Wright S. 1951 The genetical structure of populations. Ann. Eugenics 15, 323-354. (doi:10. 1111/j.1469-1809.1949.tb02451.x)
8. Treml EA, Halpin PN, Urban DL, Pratson LF. 2008 Modeling population connectivity by ocean currents, a graph-theoretic approach for marine conservation. Landscape Ecol. 23, 19-36. (doi:10.1007/s10980-007-9138-y)
9. Yasuda N, Nagai S, Hamaguchi M, Okaji K, Gerard K, Nadaoka K. 2009 Gene flow of Acanthaster planci (L.) in relation to ocean currents revealed by microsatellite analysis. Mol. Ecol. 18, 1574-1590. (doi:10.1111/mec.2009.18.issue-8)
10. Serra IA, Innocenti AM, Maida GD, Calvo S, Migliaccio M, Zambianchi E, Pizzigalli C, Arnaud-Haond S, Duarte CM. 2010 Genetic structure in the Mediterranean seagrass Posidonia oceanica: disentangling past vicariance events from contemporary patterns of gene flow. Mol. Ecol. 19, 557-568. (doi:10.1111/j.1365-294X.2009.04462.x)
11. McQuoid MR, Godhe A, Nordberg K. 2002 Viability of phytoplankton resting stages in the sediments of a coastal Swedish fjord. Eur. J. Phycol. 37, 191-201. (doi:10.1017/S0967026202003670)
12. Hairston NG, Vanbrunt RA, Kerrns CM, Engstrom DR. 1995 Age and survivorship of diapausing eggs in a sediment egg bank. Ecology 76, 1706-1711. (doi:10.2307/1940704)
13. Anderson DM, Fukuyo Y, Matsuoka K. 1995 Cyst methodologies. In Manual on harmful marine microalgae (eds GM Hallegraeff, DM Anderson, AD Cembella), pp. 229-249. IOC Manuals and Guides. Paris, France: UNESCO
14. Tahvanainen P, Figueroa RI, Alpermann TJ, John U, Hakanen P, Nagai S, Blomster J, Kremp A. 2012 Patterns of post-glacial genetic differentiation in marginal populations of a marine microalga. PLoS ONE 7, e53602. (doi:10.1371/journal.pone.0053602)
15. Sarno D, Kooistra W, Balzano S, Hargraves P, Zingone A. 2007 Diversity in the genus Skeletonema (Bacillariophyceae). III. Phylogenetic position and morphological variability of Skeletonema costatum and Skeletonema grevillei, with the description of Skeletonema ardens sp. nov. J. Phycol. 43, 156-170. (doi:10.1111/j.1529-8817.2006.00305.x)
16. Ellegaard M, Godhe A, Härnström K, McQuoid M. 2008 The species concept in a marine diatom: LSU rDNA-based phylogenetic differentiationin Skeletonema marinoi/dohrnii (Bacillariophyceae) is not reflected in morphology. Phycologia 47, 156-167. (doi:10.2216/07-79.1)
17. Saravanan V, Godhe A. 2010 Physiologic differentiation and genetic heterogeneity among seasonally separated clones of Skeletonema marinoi (Bacillariophyceae) in Gullmar Fjord, Sweden. Eur. J. Phycol. 45, 177-190. (doi:10.1080/ 09670260903445146)
18. Taylor R, Abrahamsson K, Godhe A, Wängberg S-Å. 2009 Seasonal variability in polyunsaturated aldehyde production potential between strains of Skeletonema marinoi (Bacillariophyceae). J. Phycol. 45, 46-53. (doi:10.1111/j.1529-8817. 2008.00625.x)
19. Migita S. 1967 Sexual reproduction of centric diatom Skeletonema costatum. Bull. Jpn Soc. Sci. Fish. 33, 392-398. (doi:10.2331/suisan.33.392)
20. Godhe A, McQouid M, Karunasagar I, Karunasagar I, Rehnstam-Holm A-S. 2006 Comparison of three common molecular tools for distinguishing among geographically separated clones of the diatom Skeletonema marinoi Sarno et Zingone (Bacillariophyceae). J. Phycol. 42, 280-291. (doi:10.1111/j.1529-8817.2006.00197.x)
21. Schunter C, Carreras-Carbonell J, Macpherson E, Tintoré J, Vidal-Vijande E, Pascual A, Guidetti P, Pascual M. 2011 Matching genetics with oceanography: directional gene flow in a Mediterranean fish species. Mol. Ecol. 20, 5167-5181. (doi:10.1111/j.1365-294X.2011. 05355.x)
22. Lindahl O, Belgrano A, Davidsson L, Hernroth B. 1998 Primary production, climatic oscillation, and physio-chemical processes: the Gullmar Fjord timeseries data set (1985-1996). ICES J. Mar. Sci. 55, 723-729. (doi:10.1006/jmsc.1998.0379)
23. Gustafsson M, Nordberg K. 1999 Benthic foraminifera and their response to hydrography, periodic hypoxic conditions and primary production in the Koljö Fjord on the Swedish west coast. J. Sea Res. 41, 163-178. (doi:10.1016/S1385-1101(99)00002-7)
24. Guillard RRL. 1975 Culture of phytoplankton for feeding marine invertebrates. In Culture of marine invertebrate animals (eds W Smith, M Chanley), pp. 29-60. New York, NY: Plenum Press.
25. Kooistra WHCF, DeStefano M, Mann DG, Salma N, Medlin LK. 2003 Phylogenetic position of Toxarium, a pennate-like lineage within centric diatoms (Bacillariophyceae). J. Phycol. 39, 185-197. (doi:10. 1046/j.1529-8817.2003.02083.x)
26. Almany GR et al. 2009 Permanent genetic resources added to molecular ecology resources database 1 May 2009-31 July 2009. Mol. Ecol. Resour. 9, 1460-1466. (doi:10.1111/j.1755-0998.2009.02759.x)
27. Raymond M, Rousset F. 1995 GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J. Hered. 86, 248-249.
28. Rice WR. 1989 Analyzing tables of statistical tests. Evolution 43, 223-225. (doi:10.2307/2409177)
29. Park SDE. 2001 Trypanotolerance in West African Cattle and the population genetic effects of selection. PhD thesis, University of Dublin, Dublin, Ireland.
30. van Oosterhout C, Weetman D, Hutchinson WF. 2006 Estimation and adjustment of microsatellite null alleles in nonequilibrium populations. Mol. Ecol. Notes 6, 255-256. (doi:10.1111/ j.1471-8286.2005.01082.x)
31. Brookfield JFY. 1996 A simple new method for estimating null allele frequency from heterozygote deficiency. Mol. Ecol. 5, 453-455. (doi:10.1111/j. 1365-294X.1996.tb00336.x)
32. Excoffier L, Laval G, Schneider S. 2005 Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol. Bioinform. Online 1, 47-50.
33. Jost L. 2008 GST and its relatives do not measure differentiation. Mol. Ecol. 17, 4015-4026. (doi:10. 1111/j.1365-294X.2008.03887.x)
34. Gerlach G, Jueterbock A, Kraemer P, Deppermann J, Harmand P. 2010 Calculations of population differentiation based on GST and D: forget GST but not all of statistics! Mol. Ecol. 19, 3845-3852. (doi:10.1111/j.1365-294X.2010.04784.x)
35. Sundqvist L, Zackrisson M, Kleinhans D. 2013 Directional genetic differentiation and asymmetric migration. J. Theor. Biol. (http://arxiv.org/abs/1304.0118)
36. Madec G. 2010 Nemo ocean engine, v. 3.3. Technical report, IPSL, Paris, France.
37. Hordoir R, Dieterich C, Basu C, Dietze H, Meier HEM. 2013 Freshwater outflow of the Baltic Sea and transport in the Norwegian current: a statistical correlation analysis based on a numerical experiment. Cont. Shelf Res. 64, 1-9. (doi:10.1016/ j.csr.2013.05.006)
38. Adcroft A, Campin J-M. 2004 Re-scaled height coordinates for accurate representation of free-surface fows in ocean circulation model. Ocean Model 7, 269-284. (doi:10.1016/j.ocemod. 2003.09.003)
39. Egbert G, Bennett A, Foreman M. 1994 Topex/ poseidon tides estimated using a global inverse model. J. Geophys. Res. Oceans 99, 24821-24852. (doi:10.1029/94JC01894)
40. Levitus S, Boyer TP. 1994 World Ocean Atlas 1994, vol. 5: salinity. NOAA Atlas. Washington, DC: US Government Printing Office.
41. Döös K. 1995 Inter-ocean exchange of water masses. J. Geophys. Res. Oceans 100, 13 499-13514. (doi:10.1029/95JC00337)
42. Rosenberg M, Anderson C. 2011 PASSaGE: pattern analysis, spatial statistics and geographic exegesis, v. 2. Method Ecol. Evol. 2, 229-232. (doi:10.1111/j. 2041-210X.2010.00081.x)
43. Mann DG. 1993 Patterns of sexual reproduction in diatoms. Hydrobiologia 269/270, 11-20. (doi:10. 1007/BF00027999)
44. Bengtsson BO. 2003 Genetic variation in organisms with sexual and asexual reproduction. J. Evol. Biol. 16, 189-199. (doi:10.1046/j.1420-9101.2003. 00523.x)
45. DeMeester L, Goméz A, Okamura B, Schwenk K. 2002 The monopolization hypothesis and the dispersal-gene flow paradox in aquatic organisms. Acta Oecol. 23, 121-135. (doi:10.1016/S1146-609X(02)01145-1)
46. Palsson S. 2000 Microsatellite variation in Daphnia pulex from both sides of the Baltic Sea. Mol. Ecol. 9, 1075-1088. (doi:10.1046/j.1365-294x. 2000.00969.x)
47. Campillo S, Garcia-Roger EM, Carmona MJ, Gomez A, Serra M. 2009 Selection on life-history traits and genetic population divergence in rotifers. J. Evol. Biol. 22, 2542-2553. (doi:10.1111/j.1420-9101. 2009.01871.x)
48. Sarno D, Zingone A, Montresor M. 2010 A massive and simultaneous sex event of two Pseudo-nitzschia species. Deep Sea Res. II 57, 248-255. (doi:10. 1016/j.dsr2.2009.09.012)
49. Round FE, Crawford RM, Mann DG. 1990 The diatoms. Cambridge, UK: Cambridge University Press, 747.
50. Gallagher JC. 1983 Cell enlargement in Skeletonema costatum (Bacillariophyceae). J. Phycol. 19, 539-542. (doi:10.1111/j.0022-3646.1983.00539.x)
51. Casteleyn G, Leliaert F, Backeljau T, Debeer A-E, Kotakai Y, Rhodes L, Lundholm N, Sabbe K, Vyverman W. 2010 Limits to gene flow in a cosmopolitan marine planktonic diatom. Proc. Natl Acad. Sci. USA 107, 12952-12957. (doi:10.1073/ pnas.1001380107)
52. Kenchington EL, Patwary MU, Zouros E, Bird CJ. 2006 Genetic differentiation in relation to marine landscape in a broadcast-spawning bivalve mollusc (Placopecten magellanicus). Mol. Ecol. 15, 1781-1796. (doi:10.1111/j.1365-294X.2006.02915.x)
53. Stipa T. 2002 Temperature as a passive isopycnal tracer in salty, spiceless oceans. Geophys. Res. Lett. 29, 1953-1957. (doi:10.1029/2001GL014532)
54. Lignell R. 1993 Fate of a phytoplankton spring bloom: sedimentation and carbon flowin the planktonic food web in the northern Baltic. Mar. Ecol. Prog. Ser. 94, 239-252. (doi:10.3354/meps094239)
55. Tiselius P, Kuylenstierna M. 1996 Growth and decline of a diatom spring bloom: phytoplankton species composition, formation of marine snow and 9 the role of heterotrophic dinoflagellates. J. Plankton Res. 18, 133-155. (doi:10.1093/plankt/18.2.133)
56. Ellegren H. 2004 Microsatellites: simple sequences with complex evolution. Nat. Rev. Genet. 5, 435-443. (doi:10.1038/nrg1348)
57. Tesson SVM, Legrand C, van Oosterhout C, Montresor M, Kooistra WHCF, Procaccini G. 2013 Mendelian inheritance pattern and high mutation rates of microsatellite alleles in the diatom Pseudo-nitzschia multistriata. Protist 164, 89-100. (doi:10.1016/j.protis.2012.07.001)
58. Thibert-Plante X, Hendry AP. 2010 When can ecological speciation be detected with neutral markers? Mol. Ecol. 19, 2301-2314. (doi:10.1111/j. 1365-294X.2010.04641.x)
59. Landguth EL, Fedy BC, Oyler-McCance SJ, Garey AL, Emel SL, Mumma M, Wagner HH, Fortin M-J, Cushman SA. 2011 Effects of sample size, number of markers, and allelic richness on the detection of spatial genetic pattern. Mol. Ecol. Resour. 12, 276-284. (doi:10.1111/j.1755-0998. 2011.03077.x)