Spatiotemporal changes in the genetic diversity of harmful algal blooms caused by the toxic dinoflagellate Alexandrium minutum

Molecular Ecology

Volumn 23, Issue 3, 2014, Pages 549-560

  Dia, A ^a   Guillou, L ^a   Mauger, S ^a   Bigeard, E ^a   Marie, D ^a   Valero, M ^a   Destombe, C ^a  

^a STATION BIOLOGIQUE   (France)

Author keywords

bloom dynamics; clonality; linkage disequilibrium; population genetics; resting cyst; sexual reproduction

Indexed keywords

ALEXANDRIUM MINUTUM; ALGAE; DINOPHYCEAE;

MICROSATELLITE DNA;

ALGAL BLOOM; ALLELE; ARTICLE; BLOOM DYNAMICS; CLONAL VARIATION; DINOFLAGELLATE; DNA SEQUENCE; ESTUARY; GENE LINKAGE DISEQUILIBRIUM; GENETIC VARIABILITY; GENETICS; GENOTYPE; POPULATION GENETICS; REPRODUCTION; RESTING CYST; SPATIOTEMPORAL ANALYSIS;

BLOOM DYNAMICS; CLONALITY; LINKAGE DISEQUILIBRIUM; POPULATION GENETICS; RESTING CYST; SEXUAL REPRODUCTION;

ALLELES; DINOFLAGELLIDA; ESTUARIES; GENETIC VARIATION; GENETICS, POPULATION; GENOTYPE; HARMFUL ALGAL BLOOM; LINKAGE DISEQUILIBRIUM; MICROSATELLITE REPEATS; SEQUENCE ANALYSIS, DNA; SPATIO-TEMPORAL ANALYSIS;

EID: 84892958902     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/mec.12617     Document Type: Article

References (62)

1. Agapow P-M, Burt A, (2001) Indices of multilocus linkage disequilibrium. Molecular Ecology Notes, 1, 101-102.
2. Alpermann TJ, Beszteri B, John U, Tillmann U, Cembella AD, (2009) Implications of life-history transitions on the population genetic structure of the toxigenic marine dinoflagellate Alexandrium tamarense. Molecular Ecology, 18, 2122-2133.
3. Anderson DM, Alpermann TJ, Cembella AD, Collos Y, Masseret E, Montresor M, (2012) The globally distributed genus Alexandrium: multifaceted roles in marine ecosystems and impacts on human health. Harmful Algae, 14, 10-35.
4. Arnaud-Haond S, Belkhir K, (2007) GenClone 1.0: a new program to analyse genetics data on clonal organisms. Molecular Ecology Notes, 7, 15-17.
5. Barreto FS, Tomas CR, McCartney MA, (2011) AFLP fingerprinting shows that a single Prymnesium parvum harmful algal bloom consists of multiple clones. Journal of Heredity, 102, 747-752.
6. Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F, (1996 -2004) GENETIX 4.05, logiciel sous Windows TM pour la génétique des populations. Laboratoire Génome, Populations, Interactions, CNRS UMR 5171, Université de Montpellier II, Montpellier, France.
7. Bell G, (1982) The Masterpiece of Nature: The Evolution and Genetics of Sexuality. University of California Press, Berkeley.
8. Bengtsson BO, (2003) Genetic variation in organisms with sexual and asexual reproduction. Journal of Evolutionary Biology, 16, 189-199.
9. Bravo I, Isabel Figueroa R, Garcès E, Fraga S, Massanet A, (2010) The intricacies of dinoflagellate pellicle cysts: the example of Alexandrium minutum cysts from a bloom-recurrent area (Bay of Baiona, NW Spain). Deep Sea Research Part II: Topical Studies in Oceanography, 57, 166-174.
10. Brown AH, Feldman MW, Nevo E, (1980) Multilocus structure of natural populations of Hordeum spontaneum. Genetics, 96, 523-536.
11. Burt A, Carter DA, Koenig GL, (1996) Molecular markers reveal cryptic sex in the human pathogen Coccidioides immitis. Proceedings of the National Academy of Sciences, USA, 93, 770-773.
12. Casabianca S, Penna A, Pecchioli E, et al,. (2011) Population genetic structure and connectivity of the harmful dinoflagellate Alexandrium minutum in the Mediterranean Sea. Proceedings of the Royal Society B: Biological Sciences, 279, 129-138.
13. Casteleyn G, Leliaert F, Backeljau T, et al,. (2010) Limits to gene flow in a cosmopolitan marine planktonic diatom. Proceedings of the National Academy of Sciences, USA, 107, 12952-12957.
14. Cermeno P, Falkowski PG, (2009) Controls on diatom biogeography in the ocean. Science, 325, 1539-1541.
15. Chambouvet A, Morin P, Marie D, Guillou L, (2008) Control of toxic marine dinoflagellate blooms by serial parasitic killers. Science, 322, 1254-1257.
16. Cloern JE, (1991) Tidal stirring and phytoplankton bloom dynamics in an estuary. Journal of Marine Research, 49, 203-221.
17. Crawford NG, (2010) SMOGD: software for the measurement of genetic diversity. Molecular Ecology Resources, 10, 556-557.
18. De Meeûs T, Guégan JF, Teriokhin AT, (2009) MultiTest V. 1.2, a program to binomially combine independent tests and performance comparison with other related methods on proportional data. BMC Bioinformatics, 10, 443.
19. Deng H-W, Lynch M, (1996) Change of genetic architecture in response to sex. Genetics, 143, 203-212.
20. Eckert CG, (2001) The loss of sex in clonal plants. Evolutionary Ecology, 15, 501-520.
21. Erdner DL, Richlen M, McCauley LAR, Anderson DM, (2011) Diversity and dynamics of a widespread bloom of the toxic dinoflagellate Alexandrium fundyense. PLoS ONE, 6, e22965.
22. Estrada M, Solé J, Anglès S, Garcés E, (2010) The role of resting cysts in Alexandrium minutum population dynamics. Deep Sea Research Part II: Topical Studies in Oceanography, 57, 308-321.
23. 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.
24. Figueroa RI, Garcés E, Bravo I, (2007) Comparative study of the life cycles of Alexandrium tamutum and Alexandrium minutum (Gonyaulacales, Dinophyceae) in culture. Journal of Phycology, 43, 1039-1053.
25. Figueroa RI, Garcés E, Camp J, (2010) Reproductive plasticity and local adaptation in the host parasite system formed by the toxic Alexandrium minutum and the dinoflagellate parasite Parvilucifera sinerae. Harmful Algae, 10, 1-8.
26. Figueroa RI, Vázquez JA, Massanet A, Murado MA, Bravo I, (2011) Interactive effects of salinity and temperature on planozygote and cyst formation of Alexandrium minutum (Dinophyceae) in culture. Journal of Phycology, 47, 13-24.
27. Finlay BJ, Fenchel T, (2004) Cosmopolitan metapopulations of free-living microbial eukaryotes. Protist, 155, 237-244.
28. Garcés E, Bravo I, Vila M, Figueroa RI, Maso M, Sampedro N, (2004) Relationship between vegetative cells and cyst production during Alexandrium minutum bloom in Arenys de Mar harbour (NW Mediterranean). Journal of Plankton Research, 26, 637-645.
29. Gómez A, Carvalho GR, (2000) Sex, parthenogenesis and genetic structure of rotifers: microsatellite analysis of contemporary and resting egg bank populations. Molecular Ecology, 9, 203-214.
30. Goudet J, (1999) PCA-GENE, version 1.2. Available from http://www2.unil.ch/popgen/softwares/pcagen.htm (Accessed 8 April 2013).
31. Goudet J, (2001) Fstat, a program to estimate and test gene diversities and fixation indices (version 2.9.3.2). Available from http://www2.unil.ch/ popgen/softwares/fstat.htm (Accessed8 April 2013).
32. Gsell AS, de Senerpont Domis LN, Przytulska-Bartosiewicz A, et al,. (2012) Genotype-by-temperature interactions may help to maintain clonal diversity in Asterionella formosa (Bacillariophyceae). Journal of Phycology, 48, 1197-1208.
33. Hairston NG Jr, Kearns CM, Ellner SP, (1996) Phenotypic variation in a zooplankton egg bank. Ecology, 77, 2382-2392.
34. Halim Y, (1960) Alexandrium minutum nov. g., nov. sp., a dinoflagellate causing red water. Vie et Milieu, 11, 102-105.
35. Jost L, (2008) G(ST) and its relatives do not measure differentiation. Molecular Ecology, 17, 4015-4026.
36. Lebret K, Kritzberg ES, Figueroa R, Rengefors K, (2012) Genetic diversity within and genetic differentiation between blooms of a microalgal species. Environmental Microbiology, 14, 2395-2404.
37. Lepelletier F, Karpov SA, Le Panse S, et al,. (2013) Parvilucifera rostrata sp. nov. (Perkinsozoa), a Novel Parasitoid that Infects Planktonic Dinoflagellates. Protist, 165, 31-49.
38. Marie D, Simon N, Guillou L, Partensky F, Vaulot D, (2001). DNA/RNA analysis of phytoplankton by flow cytometry. Current Protocols in Cytometry, 11, 11.12.1-11.12.14.
39. Mauger S, Couceiro L, Valero M, (2012) A simple and cost-effective method to synthesize an internal size standard amenable to use with a 5-dye system. Prime Journals, 2, 40-46.
40. Maynard-Smith J, (1978) The Evolution of Sex. Cambridge University Press, London, UK.
41. Maynard-Smith J, Hoekstra R, (1980) Polymorphism in a varied environment: how robust are the models? Genetic Research, 35, 45-57.
42. Maynard-Smith J, Smith NH, O'Rourke M, Spratt BG, (1993) How clonal are bacteria? Proceedings of the National Academy of Sciences, USA, 90, 4384-4388.
43. McCauley LAR, Erdner DL, Nagai S, Richlen ML, Anderson DM, (2009) Biogeographic analysis of the globally distributed harmful algal bloom species Alexandrium minutum (Dinophyceae) based on rRNA gene sequences and microsatellite markers. Journal of Phycology, 45, 454-463.
44. McCue K, Holtsford T, (1998) Seed bank influences on genetic diversity in the rare annual Clarkia springvillensis (Onagraceae). American Journal of Botany, 85, 30-36.
45. Montagnes D, Chambouvet A, Guillou L, (2008) Responsibility of microzooplankton and parasite pressure for the demise of toxic dinoflagellate blooms. Aquatic Microbial Ecology, 53, 211-225.
46. Moon-van der Staay SY, De Wachter R, Vaulot D, (2001) Oceanic 18S rDNA sequences from picoplankton reveal unsuspected eukaryotic diversity. Nature, 409, 607-610.
47. Nagai S, MCcauley L, Yasuda N, et al,. (2006) Development of microsatellite markers in the toxic dinoflagellate Alexandrium minutum (Dinophyceae). Molecular Ecology Notes, 6, 756-758.
48. Nagai S, Lian C, Yamaguchi S, et al,. (2007) Microsatellite markers reveal population genetic structure of the toxic dinoflagellate Alexandrium tamarense (Dinophyceae) in japanese coastal waters. Journal of Phycology, 43, 43-54.
49. Nei M, (1987) Molecular Evolutionary Genetics. Columbia University Press, New York, New York, USA.
50. Norris RD, (2000) Pelagic species diversity, biogeography, and evolution. Paleobiology, 26, 236-258.
51. Palumbi SR, (1994) Reproductive isolation, genetic divergence, and speciation in the sea. Annual Review of Ecology and Systematics, 25, 547-572.
52. Pitcher GC, Cembella AD, Joyce LB, Larsen J, Probyn RA, Sebastián R, (2007) The dinoflagellate Alexandrium minutum in Cape Town harbour (South Africa): Bloom characteristics, phylogenetic analysis and toxin composition. Harmful Algae, 6, 823-836.
53. Probert I, Lewis J, Erard-Le Denn E, (2002) Morphological details of the life history of Alexandrium minutum (Dinophyceae). Cryptogamie Algologie, 23, 343-355.
54. Richlen ML, Erdner DL, McCauley LAR, Libera K, Anderson DM, (2012) Extensive genetic diversity and rapid population differentiation during blooms of Alexandrium fundyense (Dinophyceae) in an isolated salt pond on Cape Cod, MA, USA. Ecology and Evolution, 2, 2588-2599.
55. Rispe C, Pierre JS, Simon JC, Gouyon PH, (1998) Models of sexual and asexual coexistence in aphids based on constraints. Journal of Evolutionary Biology, 11, 685-701.
56. Rynearson TA, Armbrust EV, (2000) DNA fingerprinting reveals extensive genetic diversity in a field population of the centric diatom Ditylum brightwellii. Limnology and Oceanography, 45, 1329-1340.
57. Rynearson TA, Armbrust EV, (2005) Maintenance of clonal diversity during a spring bloom of the centric diatom Ditylum brightwellii. Molecular Ecology, 14, 1631-1640.
58. Rynearson TA, Newton JA, Armbrust EV, (2006) Spring bloom development, genetic variation, and population succession in the planktonic diatom Ditylum brightwellii. Limnology and Oceanography, 51, 1249-1261.
59. Scholin CA, Anderson DM, (1994) Identification of group- and strain-specific genetic markers for globally distributed Alexandrium (Dinophyceae). I. Rflp analysis of SSU rRNA genes. Journal of Phycology, 30, 744-754.
60. Silvertown J, (2008) The evolutionary maintenance of sexual reproduction: evidence from the ecological distribution of asexual reproduction in clonal plants. International Journal of Plant Sciences, 169, 157-168.
61. Teriokhin AT, De Meeûs T, Guegan JF, (2007) On the power of some binomial modifications of the Bonferroni multiple test. Zhurnal Obshchei Biologii, 68, 332-340.
62. Wyatt T, Jenkinson IR, (1997) Notes on Alexandrium population dynamics. Journal of Plankton Research, 19, 551-575.