Molecular evidence for the coexistence of two sibling species in Pylaiella littoralis (Ectocarpales, Phaeophyceae) along the Brittany coast

Journal of Phycology

Volumn 51, Issue 3, 2015, Pages 480-489

  Geoffroy, Alexandre ^a,b   Mauger, Stéphane ^a,b   De Jode, Aurélien ^a,b   Le Gall, Line ^c   Destombe, Christophe ^a,b  

^a SORBONNE UNIVERSITÉ   (France)

^b STATION BIOLOGIQUE DE ROSCOFF   (France)

^c MUSÉUM NATIONAL D'HISTOIRE NATURELLE   (France)

Author keywords

Pylaiella littoralis; Gene flow; Microsatellite; Multilocus barcode; Sibling species

Indexed keywords

ECTOCARPALES; PHAEOPHYCEAE; PYLAIELLA; PYLAIELLA LITTORALIS;

EID: 84931560731     PISSN: 00223646     EISSN: 15298817     Source Type: Journal    
DOI: 10.1111/jpy.12291     Document Type: Article

References (56)

1. Bandelt, H. J., Forster, P. & Röhl, A. 1999. Median-joining networks for inferring intraspecific phylogenies. Mol. Biol. Evol. 16:37-48.
2. Belkhir, K., Borsa, P., Chikhi, L., Raufaste, N. & Bonhomme, F. 2003. GENETIX 4.05, logiciel sous Windows TM pour la génétique des populations. Available at: at: www.genetix.univmontp2.fr.
3. Bickford, D., Lohman, D. J., Sodhi, N. S., Ng, P. K. L., Meier, R., Winker, K., Ingram, K. K. & Das, I. 2007. Cryptic species as a window on diversity and conservation. Trends Ecol. Evol. 22:148-55.
4. Billard, E., Daguin, C., Pearson, G., Serrão, E., Engel, C. & Valero, M. 2005. Genetic isolation between three closely related taxa: Fucus vesiculosus, F. spiralis, and F. ceranoïdes (Phaophyceae). J. Phycol. 41:900-5.
5. Billard, E., Serrão, E., Pearson, G., Destombe, C. & Valero, M. 2010. Fucus vesiculosus and spiralis species complex: a nested model of local adaptation at the shore level. Mar. Ecol. Prog. Ser. 405:163-74.
6. Bolton, J. J. 1979a. The taxonomy of Pilayella littoralis (L.) Kjellm. (Phaeophyta, Ectocarpales) in the British Isles, a numerical approach. Br. Phycol. J. 14:317-25.
7. Bolton, J. J. 1979b. Estuarine adaptation in populations of Pilayella littoralis (L.) Kjellm. (Phaeophyta, Ectocarpales). Estuar. Coast. Mar. Sci. 9:273-80.
8. Cock, J. M., Sterck, L., Rouzé, P., Scornet, D., Allen, A. E., Amoutzias, G., Anthouard, V. et al. 2010. The Ectocarpus genome and the independent evolution of multicellularity in brown algae. Nature 465:617-21.
9. Coyer, J. A., Hoarau, G., Costa, J. F., Hogerdijk, B., Serrão, E. A., Billard, E., Valero, M., Pearson, G. A. & Olsen, J. L. 2011. Evolution and diversification within the intertidal brown macroalgae Fucus spiralis/F. vesiculosus species complex in the North Atlantic. Mol. Phylogenet. Evol. 58:283-96.
10. Coyer, J. A., Hoarau, G., Stam, W. T. & Olsen, J. L. 2007. Hybridization and introgression in a mixed population of the intertidal seaweeds Fucus evanescens and F. serratus. J. Evol. Biol. 20:2322-33.
11. Engel, C. R., Billard, E., Voisin, M. & Viard, F. 2008. Conservation and polymorphism of mitochondrial intergenic sequences in brown algae (Phaeophyceae). Eur. J. Phycol. 43:195-205.
12. Engel, C. R., Daguin, C. & Serrão, E. A. 2005. Genetic entities and mating system in hermaphroditic Fucus spiralis and its close dioecious relative F. vesiculosus (Fucaceae, Phaeophyceae). Mol. Ecol. 14:2033-46.
13. Feldmann, J. 1954. Inventaire de la flore marine de Roscoff. Algues, champignons, lichens et spermatophytes. Travaux de la Station Biologique de Roscoff, suppl. 6. Editions de la station biologique de Roscoff, Roscoff, 152 pp.
14. Fritsch, F. E. 1952. The Structure and Reproduction of the Algae, vol. 2. Cambridge University Press, London, 939 pp.
15. Goudet, J. 1999. PCA-GEN: Principal Component Analysis on Gene Frequency Data, version 1.2. Population Genetics Laboratory, University of Lausanne, Switzerland.
16. Guiry, M. D. & Guiry, G. M. 2014. AlgaeBase. world-wide electronic publication. Available at: http://www.algaebase.org (last accessed 15 April 2014).
17. Hoarau, G., Coyer, J. A. & Olsen, J. L. 2009. Paternal leakage of mitochondrial DNA in a Fucus (Phaeophyceae) hybrid zone. J. Phycol. 45:621-4.
18. Jakobsson, M. & Rosenberg, N. A. 2007. CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801-6.
19. Kato, Y., Kogame, K., Nagasato, C. & Motomura, T. 2006. Inheritance of mitochondrial and chloroplast genomes in the isogamous brown alga Scytosiphon lomentaria (Phaeophyceae). Phycol. Res. 54:65-71.
20. Kiirikki, M. & Lehvo, A. 1997. Life strategies of filamentous algae in the northern Baltic proper. Sarsia 82:259-67.
21. Knight, M. 1923. Studies in the Ectocarpaceae I. The life-history and cytology of Pylaiella littoralis (L.) Kjellm. Trans. R. Soc. Edinburgh 53:353-61.
22. Kornmann, P. 1990. Pilayella macrocarpa Foslie (Ectocarpales, Phaeophyceae) in Helgoland and the rejection of Pilayella varia Kjellman. Bot. Mar. 33:257-9.
23. Kornmann, P. & Sahling, P.-H. 1977. Meeresalgen von Helgoland. Helgoländer Wiss. Meeresunters 29:1-289.
24. Kylin, H. 1933. Über die entwicklungsgeschichte der Phaeophyceen, von Harald Kylin. H. Ohlssons Buchdruckerei, Lund, 102 pp.
25. Leliaert, F., Verbruggen, H., Vanormelingen, P., Steen, F., López-Bautista, J. M., Zuccarello, G. C. & De Clerck, O. 2014. DNA-based species delimitation in algae. Eur. J. Phycol. 49:179-96.
26. Levitan, D. R., Fukami, H., Jara, J., Kline, D., McGovern, T. M., McGhee, K. E., Swanson, C. A. & Knowlton, N. 2004. Mechanisms of reproductive isolation among sympatric broadcast-spawning corals of the Montastraea annularis species complex. Evolution 58:308-23.
27. 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 Res. Biotechnol. 2:40-6.
28. Mayden, R. L. 1997. A hierarchy of species concepts: the denouement in the saga of the species problem. In Claridge, M. F., Dawah, H. A. & Wilson, M. R. [Eds.] Species: The Units of Biodiversity. Chapman and Hall, New York, pp. 381-424.
29. Mcneill, J., Barrie, F. R., Buck, W. R., Demoulin, V., Greuter, W., Hawksworth, D. L., Herendeen, P. S. et al. [Eds.]. 2012. International Code of Nomenclature for Algae, Fungi, and Plants (Melbourne Code) Adopted by the Eighteenth International Botanical Congress Melbourne, Australia, July 2011. Koeltz Scientific Books, Melbourne, 240 pp.
30. Monteiro, C. A., Serrão, E. A. & Pearson, G. A. 2012. Prezygotic barriers to hybridization in marine broadcast spawners: reproductive timing and mating system variation. PLoS ONE 7:e35978.
31. Müller, D. G. & Stache, B. 1989. Life history studies on Pilayella littoralis (L.) Kjellman (Phaeophyceae, Ectocarpales) of different geographical origin. Bot. Mar. 32:71-8.
32. Newton, L. 1931. A Handbook of the British Seaweeds. British Museum (Natural History), London, 478 pp.
33. Palumbi, S. R., Cipriano, F. & Hare, M. P. 2001. Predicting nuclear gene coalescence from mitochondrial data: the three-times rule. Evolution 55:859-68.
34. Peakall, R. & Smouse, P. E. 2012. GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics 28:2537-9.
35. Peters, A. F., Couceiro, L., Tsiamis, K., Küpper, F. C. & Valero, M. 2015. Barcoding of cryptic stages of marine brown algae isolated from incubated substratum reveals high diversity in Acinetosporaceae (Ectocarpales, Phaeophyceae). Cryptogam. Algol. 36:3-29.
36. Peters, A. F., Scornet, D., Müller, D. G., Kloareg, B. & Cock, J. M. 2004. Inheritance of organelles in artificial hybrids of the isogamous multicellular chromist alga Ectocarpus siliculosus (Phaeophyceae). Eur. J. Phycol. 39:235-42.
37. Presting, G. G. 2006. Identification of conserved regions in the plastid genome: implications for DNA barcoding and biological function. Can. J. Bot. 84:1434-43.
38. Pritchard, J. K., Stephens, M. & Donnelly, P. 2000. Inference of population structure using multilocus genotype data. Genetics 155:945-59.
39. Puillandre, N., Lambert, A., Brouillet, S. & Achaz, G. 2011. ABGD, Automatic Barcode Gap Discovery for primary species delimitation. Mol. Ecol. 21:1864-77.
40. Raymond, M. & Rousset, F. 1995. GENEPOP (Version 1.2): Population Genetics Software for Exact Tests and Ecumenicism. J. Hered. 86:248-9.
41. Rosenberg, N. A. 2004. DISTRUCT: a program for the graphical display of population structure. Mol. Ecol. Notes 4:137-8.
42. Ruprecht, F. J. 1850. Algae Ochotenses: Die ersten sicheren Nachrichten über die Tange des Ochotskischen Meeres. Buchdruckerei der Kaiserlichen Akademie der Wissenschaften, St Petersburg, 243 pp.
43. Russell, G. 1963. A study in populations of Pylaiella littoralis. J. Mar. Biol. Assoc. United Kingdom 43:469-83.
44. Russell, G. 1967. The ecology of some free-living Ectocarpaceae. Helgol. Mar. Res. 15:155-62.
45. Siemer, B. L. & Pedersen, P. M. 1995. The taxonomic status of Pilayella littoralis, P. varia and P. macrocarpa (Pilayellaceae, Fucophyceae). Phycologia 34:257-66.
46. Silberfeld, T., Leigh, J. W., Verbruggen, H., Cruaud, C., de Reviers, B. & Rousseau, F. 2010. A multi-locus time-calibrated phylogeny of the brown algae (Heterokonta, Ochrophyta, Phaeophyceae): investigating the evolutionary nature of the "brown algal crown radiation". Mol. Phylogenet. Evol. 56:659-74.
47. Silva, P. C., Lamy, D., Loiseaux-de Goër, S. & de Reviers, B. 1999. Proposal to conserve the name Pylaiella bory (Phaeophyceae) with a conserved spelling. Taxon 48:139-40.
48. Sites, J. W. Jr & Marshall, J. C. 2003. Delimiting species: a Renaissance issue in systematic biology. Trends Ecol. Evol. 18:462-70.
49. Tellier, F., Faugeron, S. & Valero, M. 2011. Possible role of a mitochondrial genome rearrangement in maintaining the spatial segregation of two cryptic species of the Lessonia nigrescens species complex. Cah. Biol. Mar. 52:371-83.
50. Tellier, F., Meynard, A. P., Correa, J. A., Faugeron, S. & Valero, M. 2009. Phylogeographic analyses of the 30°S south-east Pacific biogeographic transition zone establish the occurrence of a sharp genetic discontinuity in the kelp Lessonia nigrescens: vicariance or parapatry? Mol. Phylogenet. Evol. 53:679-93.
51. Tronholm, A., Steen, F., Tyberghein, L., Leliaert, F., Verbruggen, H., Antonia Ribera Siguan, M. & De Clerck, O. 2010. Species delimitation, taxonomy, and biogeography of Dictyota in Europe (Dictyotales, Phaeophyceae). J. Phycol. 46:1301-21.
52. Valero, M., Destombe, C., Mauger, S., Ribout, C., Engel, C. R., Daguin-Thiebaut, C. & Tellier, F. 2011. Using genetic tools for sustainable management of kelps: a literature review and the example of Laminaria digitata. Cah. Biol. Mar. 52:467-83.
53. 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. J. Phycol. 40:1013-27.
54. Weir, B. S. & Cockerham, C. C. 1984. Estimating F-Statistics for the analysis of population structure. Evolution 38:1358-70.
55. Yang, E. C., Peters, A. F., Kawai, H., Stern, R., Hanyuda, T., Bárbara, I., Müller, D. G., Strittmatter, M., van Reine, W. F. P. & Küpper, F. C. 2014. Ligulate Desmarestia (Desmarestiales, Phaeophyceae) revisited: D. japonica sp. nov. and D. dudresnayi differ from D. ligulata. J. Phycol. 50:149-66.
56. Zardi, G. I., Nicastro, K. R., Canovas, F., Costa, J. F., Serrão, E. A. & Pearson, G. A. 2011. Adaptive traits are maintained on steep selective gradients despite gene flow and hybridization in the intertidal zone. PLoS ONE 6:e19402.