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2015 Clathromorphum.Pdf J. Phycol. 51, 189–203 (2015) © 2014 Phycological Society of America DOI: 10.1111/jpy.12266 DNA SEQUENCING, ANATOMY, AND CALCIFICATION PATTERNS SUPPORT A MONOPHYLETIC, SUBARCTIC, CARBONATE REEF-FORMING CLATHROMORPHUM (HAPALIDIACEAE, CORALLINALES, RHODOPHYTA) Walter H. Adey,2 Jazmin J. Hernandez-Kantun Botany Department, National Museum of Natural History, Smithsonian Institution, Washington, D.C., USA Gabriel Johnson Laboratory of Analytical Biology, National Museum of Natural History, Smithsonian Institution, Washington, D.C., USA and Paul W. Gabrielson Department of Biology and Herbarium, University of North Carolina, Chapel Hill, North Carolina, USA For the first time, morpho-anatomical characters under each currently recognized species of that were congruent with DNA sequence data were Clathromorphum and Neopolyporolithon. used to characterize several genera in Hapalidiaceae Key index words: anatomy; Callilithophytum; ecology; — the major eco-engineers of Subarctic carbonate evolution; Leptophytum; Melobesioideae; Neopolypor- ecosystems. DNA sequencing of three genes (SSU, olithon; psbA; rbcL; SSU rbcL, ribulose-1, 5-bisphosphate carboxylase/ oxygenase large subunit gene and psbA, photosystem Abbreviations: BI, Bayesian inference; BP, bootstrap II D1 protein gene), along with patterns of cell value; GTR, general time reversible; MCMC, Mar- division, cell elongation, and calcification supported kov Chain Monte Carlo; ML, maximum likelihood; a monophyletic Clathromorphum. Two characters psbA, Photosystem II D1 protein gene; rbcL, ribu- were diagnostic for this genus: (i) cell division, lose-15-bisphosphate carboxylase/oxygenase large elongation, and primary calcification occurred only subunit gene in intercalary meristematic cells and in a narrow vertical band (1–2 lm wide) resulting in a “meristem split” and (ii) a secondary calcification of interfilament crystals was also produced. For the past 50 years, Adey and collaborators have Neopolyporolithon was resurrected for N. reclinatum, intensively researched the Subarctic shallow subtid- the generitype, and Clathromorphum loculosum was al, carbonate, reef-forming coralline algae domi- transferred to this genus. Like Clathromorphum, cell nated by species of Clathromorphum Foslie, but also division, elongation, and calcification occurred only including species in Lithothamnion Heydrich, Lepto- in intercalary meristematic cells, but in a wider phytum W.H. Adey, and Phymatolithon Foslie (Subarc- vertical band (over 10–20 lm), and a “meristem tic as used herein, includes the Arctic; see Adey and split” was absent. Callilithophytum gen. nov. was Steneck 2001). As a result, this is one of the best proposed to accommodate Clathromorphum parcum, studied shallow subtidal ecosystems globally with the obligate epiphyte of the northeast Pacific numerous papers on the ecology (Adey 1964, 1965, endemic geniculate coralline, Calliarthron. 1966a,b, 1970a,b, 1971, Adey and McKibbin 1970, Diagnostic for this genus were epithallial cells Adey and Adey 1973, Adey et al. 2005), physiology terminating all cell filaments (no dorsi-ventrality was (Adey 1970b, Adey and McKibbin 1970, Adey 1973, present), and a distinct “foot” was embedded in the Adey et al. 2013), and biogeography (Adey 1966b, host. Leptophytum, based on its generitype, L. laeve, Adey et al. 1976, 2008, Adey and Steneck 2001, Adey was shown to be a distinct genus more closely and Hayek 2011) of these reef-forming carbonate related to Clathromorphum than to Phymatolithon. All species. names of treated species were applied unequivocally Concomitantly, studies on the growth and anat- by linking partial rbcL sequences from holotype, omy of these species (Adey 1964, 1965, 1966a), and isotype, or epitype specimens with field-collected more recently, high magnification SEM studies material. Variation in rbcL and psbA sequences (Adey et al. 2005, 2013) have revealed patterns of suggested that multiple species may be passing cell division, elongation, and calcification that have not been incorporated into our knowledge of the phylogenetic relationships among these Subarctic 1Received 20 February 2014. Accepted 6 November 2014. and Boreal taxa. For example, all growth (cell divi- 2Author for correspondence: e-mail [email protected]. sion and cell elongation) and calcification in Sub- Editorial Responsibility: M. Vis (Associate Editor) arctic Clathromorphum species and in Neopolyporolithon 189 190 WALTER H. ADEY ET AL. W.H. Adey & H.W. Johansen occurs in the interca- walls. However, in Subarctic Clathromorphum species, lary meristem (Adey 1965, Adey and Johansen 1972, secondary vertically or diagonally oriented, large, Lebednik 1977, Adey et al. 2005, Fig. 1). Cells are angular (deltoid in shape) calcite crystals are em- cut-off from the meristem distally to form a photo- placed between filaments (interfilament crystals of synthetic epithallium and proximally to form an Adey et al. 2013; Figs. 2 and 3). These secondary in- extensive perithallium. Moreover, in these Subarctic terfilament crystals appear to have no organic Clathromorphum species, Adey et al. (2013), using framework, and they dissolve out more readily than high magnification SEM, showed that primary calci- the primary wall crystals when older tissue is fication occurred in a narrow, horizontal plane exposed by invertebrate borers; the calcite dissolu- (meristem split), a few lm thick, within the meri- tion accompanying such boring can allow cells to stem (Figs. 2 and 3). In Lithothamnion (Figs. 1 and fall out of the broader carbonate matrix as hollow 4; Adey et al. 2005) and Leptophytum (Fig. 1), cell “grains” of carbonate, the primary wall crystals division also occurs in the single layer of intercalary meristematic cells, but full cell elongation occurs over a depth of 15–40 lm into the perithallium. The Subarctic species of Clathromorphum (C. com- pactum (Kjellman) Foslie C. circumscriptum (Stromfelt)€ Foslie, and C. nereostratum Lebednik), unlike all other known nongeniculate corallines, have a unique double mode of calcification (Nash et al. 2012, Adey et al. 2013). The primary calcifica- tion, characteristic of all Corallinales and Sporolit- hales studied to date, is of metabolically emplaced, short, very fine, radially oriented and prismatic micro-calcite crystals, embedded in organic cell FIG. 2. Clathromorphum nereostratum SEM image at 92,000 showing meristem, with its break in calcification, and overlying epithallium and underlying perithallium. Thin, inner cell layer of radial calcite crystals (black arrow); mass of larger and more verti- cally oriented interfilament calcite crystals (gray arrow). From Adey et al. (2013). FIG. 1. Comparative meristem and upper perithallial mean cell dimensions of Lithothamnion lemoineae, Clathromorphum circumscrip- FIG. 3. Unfractured meristem cells of Clathromorphum nereostra- tum, and Leptophytum laeve (See Adey et al. 2005 for details). Sets of tum showing: IM – inner wall, inner membrane, and OM, outer meristem and perithallial size curves demonstrate three primary membrane; CZ – fractured calcification zone; and PC – precipita- cell elongation (growth) types (Leptophytum/Phymatolithon—pro- tion cavity. Note the great difference in size and orientation of gressive, Clathromorphum—only meristem, and Lithothamnion— the inner wall crystals as compared to the interfilament crystals. mixed) currently known for Subarctic Hapalidiaceae. From Adey et al. (2013). CLATHROMORPHUM PHYLOGENETIC ANALYSES 191 embedded in organic remains providing the struc- (Fig. 5), and in all cases they are characteristic of ture of the grains (Adey et al. 2013). these three genera (Adey 1966a, Adey et al. 1982, Most coralline genera have a single layer of super- 2005, Bahia et al. 2013). ficial nonphotosynthetic epithallial cells, and in the Herein, we focus on the genus Clathromorphum classical literature these were called cover cells (Frit- (Foslie 1898) restricting ourselves to the well-studied sch 1952) or deckzellen (Suneson 1937). Although and currently recognized northern hemisphere spe- they are usually thought of as being very thin-walled cies. This includes the dominant Subarctic, carbo- with minimal (if any) calcification, there is a wide nate, reef-forming species: C. compactum (Foslie) variety of structure that is generally uniform at the Foslie (the generitype), C. circumscriptum (Stromfelt)€ generic level. Subarctic Clathromorphum species, for Foslie and C. nereostratum Lebednik. Also included in example, develop a multilayered, calcified, photo- Clathromorphum in earlier publications have been thin- synthetic epithallium. In contrast, Lithothamnion spe- ner epilithic species, C. loculosum (Kjellman) Foslie cies have a single-layered, calcified and thick-walled, and the Boreal (as defined by Adey and Steneck 2001, “armored” epithallium (flared upper walls in some including British Columbian) epiphytic species, C. literature, e.g., Irvine and Chamberlain 1994) that parcum (Setchell & Foslie) W. H. Adey and C. reclina- are highly distinctive both in surface view and in tum (Foslie) W. H. Adey. We also demonstrate that section, in SEM (Fig. 4) and in decalcified, paraffin- Leptophytum and Phymatolithon are distinct genera, embedded microtome sections (Adey 1966a, Adey resolving a long-standing dispute over the recogni- and McKibbin 1970). Epithallial cells of Sporolit- tion of Leptophytum (Adey et al. 2001, Woelkerling hales (Sporolithon and Heydrichia) are similar et al. 2002, Athanasiadis and Adey 2003, 2006). FIG. 4. SEM at 93,000 of Lithothamnion tophiforme showing characteristic
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