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Laminariales, Phaeophyceae) Supports Substantial Taxonomic Re-Organization1

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Laminariales, Phaeophyceae) Supports Substantial Taxonomic Re-Organization1 J. Phycol. 42, 493–512 (2006) r 2006 Phycological Society of America DOI: 10.1111/j.1529-8817.2006.00204.x A MULTI-GENE MOLECULAR INVESTIGATION OF THE KELP (LAMINARIALES, PHAEOPHYCEAE) SUPPORTS SUBSTANTIAL TAXONOMIC RE-ORGANIZATION1 Christopher E. Lane,2 Charlene Mayes Centre for Environmental and Molecular Algal Research, University of New Brunswick, Fredericton, NB, Canada E3B 6E1 Louis D. Druehl Bamfield Marine Sciences Centre, Bamfield, BC, Canada V0R 1B0 and Gary W. Saunders Centre for Environmental and Molecular Algal Research, University of New Brunswick, Fredericton, NB, Canada E3B 6E1 Every year numerous ecological, biochemical, Key index words: Costariaceae; Laminariales; long and physiological studies are performed using branch attraction; nested analyses; phylogenetics; members of the order Laminariales. Despite the Saccharina fact that kelp are some of the most intensely stud- ied macroalgae in the world, there is significant de- bate over the classification within and among the The order Laminariales Migula, commonly called three ‘‘derived’’ families, the Alariaceae, Lamina- kelp, includes the largest algae in the world, reaching riaceae, and Lessoniaceae (ALL). Molecular phylo- up to 50 m in length (Van den Hoek et al. 1995). Kelp genies published for the ALL families have are ubiquitous in coastal waters of cold-temperate re- generated hypotheses strongly at odds with the cur- gions from the Arctic to the Antarctic, and their size rent morphological taxonomy; however, conflicting and biomass establishes a unique and essential habitat phylogenetic hypotheses and consistently low levels for hundreds of species (Steneck et al. 2002). They are of support realized in all of these studies have re- used as a food source in Asia and Europe, and are also sulted in conservative approaches to taxonomic re- economically important for their extracts (Chapman visions. In order to resolve relationships within this 1970, Ohno and Crithchley 1998), which are used in group we have sequenced over 6000 bp from re- consumer and medical products. gions in the nuclear, chloroplast, and mitochondrial There are approximately 30 genera within the genomes and included 42 taxa in Bayesian, neigh- Laminariales, many of which are monotypic, whereas bor-joining, and parsimony analyses. The result is a few contain a large number of species [ca. 45 species the first comprehensive and well-supported molec- in Laminaria (Kain 1971), 12 species in Alaria ular phylogeny for the ALL complex of the Lami- (Widdowson 1971, Kraan et al. 2001)]. Nearly 100 nariales. We maintain the three recognized families species of kelp are currently recognized across the or- (Alariaceae, Laminariaceae, and Lessoniaceae), but der, with the majority of them occurring in the North with vastly different compositions, as well as pro- Pacific, where 40 species are currently recognized from pose the Costariaceae fam. nov. for Agarum, Cost- the coast of North America (Druehl 1970), and ca.41 aria, Dictyoneurum, and Thalassiophyllum, the only from Asia (Yoshida 1998, Kawai and Sasaki 2000, genera in the Laminariales with flattened, occasion- Kawai et al. 2000). The North Atlantic contains only ally terete, stipes and either a perforate or reticulate a fraction of the diversity seen in the Pacific, with only blade. In addition, our data strongly support a split eight kelp species recognized (South and Tittley 1986, of the genus Laminaria. We resurrect the genus Sac- Kawai and Sasaki 2000). However, these species span a charina Stackhouse for the Laminaria clade that taxonomic range equal to that among the 40 species on does not contain L. digitata (Hudson) J.V. Lam- the West Coast of North America. The Southern Hemi- ouroux, the type of the genus. sphere kelp species are limited to Eisenia galapagensis (near the equator), two species of Laminaria, three spe- cies of Macrocystis, the introduced species Undaria pin- natifida (also introduced in Europe, but originally from East Asia), and the largely Southern Hemisphere gen- era Ecklonia and Lessonia (Womersley 1987, Adams 1Received 4 July 2005. Accepted 29 December 2005. 2Author for correspondence and present address: Department of 1994, Stegenga et al. 1997). Biochemistry and Molecular Biology, Dalhousie University, 5850 Col- While morphology is highly variable among mem- lege St., Halifax, N.S., B3H 1X5, Canada. e-mail [email protected]. bers of the Laminariales, kelp are typically connected 493 494 CHRISTOPHER E. LANE ET AL to the substrate by a holdfast of branching haptera, gross morphology of the sporophyte by Setchell and rhizoids, or a disc. A stipe is borne centrally from the Gardner (1925). The Alariaceae was defined by the holdfast and has at its upper end an intercalary meri- presence of sporophylls (special blades for reproduc- stem at the ‘‘transition zone’’ between the stipe and the tive sori). The Laminariaceae have simple, single terminal blade. Extension of both the stipe and the blades, whereas representatives of the Lessoniaceae blade occur by growth in this transition zone, with display splitting at the transition zone (between the growth in girth produced by a superficial meristem, stipe and the blades). Some genera, however, do not fit the meristoderm (Bold and Wynne 1985). Kelp are the neatly into the morphological scheme. In fact, Setchell only seaweed with specialized cells (trumpet hyphae) and Gardner (1925) stated that the genus Lessoniopsis for the transport of nutrients, stored mainly as lami- (Fig. 1b), which has both sporophylls and splitting, naran and mannitol (Parker 1965, Lu¨ning 1990). An- could be placed either in the Alariaceae or the Lesson- other defining feature of the Laminariales is their iaceae and the decision to place this genus in the latter heteromorphic, diplohaplontic life cycle, which alter- family was based on its habit being more similar to nates between a microscopic haploid gametophyte and Lessonia than Alaria. Despite uncertainty as to the use- a macroscopic parenchymatous diploid sporophyte. fulness of the characters that define the ALL families, Whereas many kelp are annuals, some, such as Lamin- these taxa had remained largely unchallenged at the aria hyperborea, reportedly live up to 20 years (Van den familial level until the application of molecular tech- Hoek et al. 1995). niques to kelp systematics. Kelps are well studied seaweeds; the ISI Web of Fain et al. (1988) were the first to apply molecular Knowledge lists 376 papers in just a 3 year period tools to kelp systematics. They initiated a restriction (January 2003–December 2005) with ‘‘kelp’’ in the key fragment length polymorphism (RFLP) investigation words. Despite the conspicuous nature of kelp, and of the chloroplast genome for five species [Alaria mar- considerable attention they receive from both bio- ginata (Al), Laminaria saccharina (La), Lessoniopsis littora- chemical and ecological researchers, little considera- lis (Le), Nereocystis luetkeana (Le) and Macrocystis tion had been given to their systematics until recently. integrifolia (Le); Al 5 Alariaceae, La 5 Laminariaceae, Several molecular studies over the past 20 years have Le 5 Lessoniaceae] of the Laminariales, of which three called into question the widely accepted classification were members of the Lessoniaceae. Rather than system for the Laminariales (Fain et al. 1988, Saunders grouping together, members of the Lessoniaceae and Druehl 1993b, Druehl et al. 1997, Yoon and Boo were polyphyletic—Nereocystis (Le) consistently 1999, Kawai and Sasaki 2000, Sasaki et al. 2001, Yoon grouped with Laminaria (La), whereas Alaria (Al) was et al. 2001). In the past 5 years publications have variously resolved with Macrocystis (Le), or Lessoniopsis changed the three ‘‘ancestral’’ families that were tradi- (Le). tionally recognized, viz., the Chordaceae, Phyllaria- Subsequent to the chloroplast studies of Fain et al. ceae, and Pseudochordaceae. The Phyllariaceae was (1988), a number of publications directed at resolving moved out of the Laminariales based on its close mo- kelp systematics have focused on the nuclear ribosomal lecular affinity to the Tilopteridales (Kawai and Sasaki cistron using either the small subunit rDNA (SSU) 2000). The monotypic genus Halosiphon was, at the (Saunders and Druehl 1992, Boo et al. 1999) or the same time, elevated from the Chordaceae to familial internal transcribed spacer regions (ITS) (Saunders status (Halosiphonaceae) and moved out of the Lam- and Druehl 1993b, Druehl et al. 1997, Yoon et al. inariales, but left incertae sedis at the ordinal level. The 2001). Phylogenetic trees generated from the first monotypic family Akkesiphycaceae was then added to ITS region (ITS1) (Saunders and Druehl 1993b) add- the Laminariales (Kawai and Sasaki 2000). Subse- ed further evidence that the Lessoniaceae was polyp- quently, the Phyllariaceae and Halosiphonaceae were hyletic, and also indicated a similar situation for a placed in the Tilopteridales based on both nuclear and second family, the Alariaceae. Three groups were re- chloroplast DNA sequence data (Sasaki et al. 2001). solved by their data: Group 1 for Alaria (Al), Lessonio- Thus, the ‘‘ancestral’’ clade in the Laminariales con- psis (Le), and Pterygophora (Al); Group 2 for Costaria tinues to have three families, but with substantially dif- (La) and Dictyoneurum (Le); and Group 3 for Egregia ferent composition. (Al), Eisenia (Al), Lessonia (Le), Macrocystis (Le),Ne- The three ‘‘derived,’’ or ‘‘ALL’’ families (Saunders reocystis (Le), and Postelsia (Le). Only one member of and Druehl 1993b),
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