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UW-Madison BOTANY 940 - Assessing red algal supraordinal diversity and taxonomy

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1494American Journal of Botany 91(10): 1494–1507. 2004.ASSESSING RED ALGAL SUPRAORDINAL DIVERSITY ANDTAXONOMY IN THE CONTEXT OF CONTEMPORARYSYSTEMATIC DATA1GARYW. SAUNDERS2,4ANDMAXH. HOMMERSAND32Centre for Environmental & Molecular Algal Research, Department of Biology, University of New Brunswick, Fredericton, NewBrunswick, Canada, E3B 6E1; and3Department of Biology, University of North Carolina, Chapel Hill,North Carolina 27599-3280 USAThe wondrously diverse eukaryotes that constitute the red algae have been the focus of numerous recent molecular surveys andremain a rich source of undescribed and little known species for the traditional taxonomist. Molecular studies place the red algae inthe kingdom Plantae; however, supraordinal classification has been largely confined to debate on subclass vs. class level status for thetwo recognized subgroups, one of which is widely acknowledged as paraphyletic. This narrow focus has generally masked the extentto which red algal classification needs modification. We provide a comprehensive review of the literature pertaining to the antiquity,diversity, and systematics of the red algae and propose a contemporary classification based on recent and traditional evidence.Key words: Bangiophyceae; Compsopogonophyceae; Cyanidiophyta; Eurhodophytina; Florideophyceae; Metarhodophytina; Rho-dophyta; Rhodoplantae.The biological significance of red algae is only beginning to beappreciated. Even among professional biologists, knowledge ofthese organisms is often minimal and based on cursory informa-tion contained in general botany textbooks (Woelkerling, 1990, p.1).Macroalgal systematics traces its ‘‘modern’’ era to ratherhumble beginnings, the multitude of diverse species assignedto a few genera in a subdivision (Algae) of the class Crypto-gamia, which also included the ferns, mosses and fungi, po-sitioned among 23 classes of cone-bearing and floweringplants in the plant kingdom (Linnaeus, 1753). This early clas-sification clearly underrepresented macroalgal diversity andsubstantial taxonomic refinements inevitably followed. La-mouroux (1813) was the first to use color to segregate algalassemblages when he removed certain red algae from theirrespective associations with species of like morphology to theFloride´es. Harvey (1836) took the ‘‘biochemical’’ marker fur-ther and established the Chlorospermae, Melanospermae, andRhodospermae for green, brown, and red algae, respectively;in essence establishing the three major groups of macroalgaethat are recognized today.Numerous taxonomic changes were implemented in the en-suing decades, but the relatively recent advent of ultrastruc-tural and molecular systematic data in particular have uncov-ered the bewildering diversity, as well as evolutionary affini-ties of the chlorophytic and chromophytic lineages. Recenttaxonomic treatments vary, but schemes including as many as10 classes in two phyla are now presented for the chlorophyticline (cf. Lewis and McCourt, 2004). The brown algae are in-cluded in a larger chromophytic lineage, Heterokontophyta,1Manuscript received 15 January 2004; revision accepted 17 June 2004.During preparation of this review, GWS was supported by funds from theNatural Sciences and Engineering Research Council of Canada and the Can-ada Research Chair Program and MHH was supported by NSF PEET grantDEB-0328491. We are indebted to P. Silva and M. J. Wynne for helpfuldiscussions regarding the ICBN, as well as P. Silva for drawing the work ofDoweld to our attention. We thank R. Moe for Latin translations. Commentsfrom J. D. Palmer and two anonymous reviewers were genuinely appreciatedand served to improve the clarity of this manuscript.4E-mail: [email protected] a wide diversity of lineages distributed among some15 classes (cf. Andersen, 2004). The Rhodophyta have notexperienced a similar explosion in taxonomic breadth with ourcurrent perspective on supraordinal relationships virtually un-changed since ca. 1900 and confined to a continuing debateas to whether the two constituent lineages, Bangiophyceae andFlorideophyceae, should be recognized as distinct classes orsubsumed as subclasses within a single class Rhodophyceae(cf. Dixon, 1973).The current system of red algal classification creates theillusion that this lineage is relatively limited in its diversitywhen compared to chlorophytes and chromophytes; this de-spite the wide range of morphology observed among red algaeand a wealth of contemporary ultrastructural and moleculardata that speak to the antiquity and diversity within Rhodo-phyta. This review sets as its aim to amass the available in-formation on red algal phylogeny, diversity, and antiquity andto use this to reform red algal taxonomy. It is not our intentto deal with the broader issue of red algal affinities relative tothe other major eukaryotic lines. The reader is directed to anoverview of that topic by Keeling (2004) in this issue.FOSSILS AND ANTIQUITY OF THE RED ALGAEThe red algae are a study in extremes. Morphologically more di-verse than any other group of algae, they range from single cellsto large ornate multicellular plants . . . Uniquely among (nonfun-gal) eukaryotes they lack both flagella and centrioles . . . and ex-hibit a remarkable, often bizarre range of reproductive strategies(Butterfield, 2000, p. 386).The earliest putative red algal fossils date to ca. 2 billionyears before present and are superficially similar to the extanttaxa of the Porphyridiales, Bangiophyceae (Tappan, 1976). Al-though the evolutionary scenario presented by Tappan, inwhich the red algae represent a direct link between the pro-karyotic cyanophytes and other eukaryotes, is widely rejectedin light of recent phylogenetic hypotheses (e.g., Ragan andGutell, 1995), the possibility that unicellular red algae did existat such an early stage (Fig. 1) is compatible with the fossilsOctober 2004] 1495SAUNDERS ANDHOMMERSAND—RED ALGAL SYSTEMATICSFig. 1. Geological time scale from a general biology text (Campbell and Reece, 2002), modified to place red algal fossils in context with other majorevolutionary events.observed by Tappan and other scientists. Most notable in thisregard is the old (1.2 billion years) and relatively advancedfossil taxon Bangiomorpha (Butterfield, 2000). Bangiomorphapubescens Butterfield (2000) was described from the 1200-million-year-old Hunting Formation in the Canadian Arcticand represents the earliest putative record for sex and taxo-nomically resolvable


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UW-Madison BOTANY 940 - Assessing red algal supraordinal diversity and taxonomy

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