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Constancea 83.9: Phylogeny of Osmundea 12/17/2002 06:46:34 PM Constancea 83, 2002 University and Jepson Herbaria P.C

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Constancea 83.9: Phylogeny of Osmundea 12/17/2002 06:46:34 PM Constancea 83, 2002 University and Jepson Herbaria P.C Constancea 83.9: Phylogeny of Osmundea 12/17/2002 06:46:34 PM Constancea 83, 2002 University and Jepson Herbaria P.C. Silva Festschrift Phylogenetic Analysis of the Geographically Disjunct Genus Osmundea Stackhouse (Rhodomelaceae, Rhodophyta) Lynne McIvor1, Christine A. Maggs2, Michael D. Guiry1, and Max H. Hommersand3 1 Department of Botany, Martin Ryan Institute, The National University of Ireland, Galway, Galway, Ireland. 2 School of Biology and Biochemistry, The Queen's University of Belfast, Medical Biology Centre, 97 Lisburn Road, Belfast, U. K. BT9 7BL. 3 Department of Biology, Coker Hall, University of North Carolina, Chapel Hill, NC 27599−3280, USA. ABSTRACT Despite numerous studies, the phylogeny and taxonomy of much of the Laurencia Lamouroux complex still remains obscure. Previous phylogenetic analyses of the genus Osmundea based on comparative morphology and sequences of the plastid−encoded rbcL gene indicated two potentially phylogenetically informative characters. The presence or absence of secondary pit connections in the epidermis and the shape of spermatangial receptacles (urn−shaped or cup−shaped) were synapomorphies for some clades in European species. Osmundea Stackhouse has a markedly disjunct distribution, being confined to Atlantic and Mediterranean coasts of Europe and Pacific North America. The major goal of this study was to extend taxon sampling to Californian species (the “Spectabilis group”) which show character combinations that differ from any European species. In addition, we investigated whether the basionym Fucus oederi Gunnerus might be available for the taxonomically and nomenclaturally confused species Osmundea ramosissima Athanasiadis. The tribe Laurencieae, represented by Chondrophycus, Laurencia, and Osmundea, was well supported, with Chondrophycus papillosus and the type species of Laurencia, L. obtusa, positioned basally. All species currently placed in the genus Osmundea formed a monophyletic group with robust support. 1/11 Constancea 83.9: Phylogeny of Osmundea 12/17/2002 06:46:34 PM Within Osmundea, three clades representing different geographical areas were observed (North Pacific, Atlantic Europe, Mediterranean + Atlantic Europe), with good (91% to 100%) bootstrap support. This phylogeny is interpreted as indicating that the genus may have originated in the late Tethys. The Californian clade and the European Osmundea clades exhibit contrasting stability of characters. The Californian species showed a fixed urn−shaped spermatangial receptacle shape and showed a variable number of epidermal secondary pit connections. In contrast, among the European species, the shape of the spermatangial receptacle shows character reversals and appears to be actively evolving in Mediterranean species. The two distinct European clades of Osmundea are clearly separable by the presence or absence of secondary pit connections. This comparative biogeographical approach to a morphological/molecular phylogenetic investigation has therefore yielded results that challenge the use solely of morphological characters for future generic subdivision in Osmundea. INTRODUCTION The Laurencia Lamouroux complex (Laurencieae, Rhodomelaceae) contains numerous species that are widely distributed in tropical and temperate waters (McDermid 1988, 1989). Members of this complex are readily identifiable within the Rhodomelaceae by a unique combination of vegetative features, such as their extensive cortex, a central axis recognizable only near the apical cell, and apical cells sunk in apical pits of the branchlets (Kylin 1956). The taxonomic history of Laurencia sensu lato has been summarized by Furnari and Serio (1995) and Furnari et al. (2001). One of the most significant contributions was made by Yamada (1931), who proposed an arrangement of Laurencia into four sections based on gross morphology and anatomical characters. Saito (1967) described some additional anatomical characters, including the presence or absence of secondary pit connections between epidermal cells. In a revision based primarily on Japanese species, he divided the genus into two subgenera, Laurencia (sections Laurencia, Pinnatifidae, Forsterianae) and Chondrophycus Tokida &Saito (sections Chondrophycus, Palisadae). Saito (1969) then proposed the “Spectabilis group” for a number of Californian species, which differed from the existing sections by a combination of adaxial tetrasporangia, urn−shaped “indeterminate” spermatangial receptacles, and (mistakenly) a lack of secondary pit connections between epidermal cells. Later, Furnari and Serio (1993a) pointed out errors in Saito's (1982) treatment of the section Pinnatifidae, and merged the emended Pinnatifidae with the “Spectabilis group” into the subgenus Saitoa Furnari & Serio, nom. illeg. However, many details of the vegetative and reproductive structures of all the subgenera (Laurencia, Chondrophycus, and Saitoa) were still lacking. During the last decade, further major changes have been made. The genus Osmundea Stackhouse (1809) has been resurrected (Nam et al. 1994) for a group of species largely corresponding to the subgenus Saitoa. The section Chondrophycus has also been elevated to generic status (Garbary and Harper 1998). Both taxonomic changes were proposed on the basis of a suite of morphological characters (Nam et al. 1994; Nam and Saito 1995; Garbary and Harper 1998; Nam 1999). The genus Osmundea was defined by (1) the development of spermatangia on filaments formed by apical and epidermal cells rather than on spermatangial trichoblasts formed by axial cells, (2) tetrasporangia formed by random epidermal cells rather than particular pericentral cells (Nam et al. 1994), and (3) the formation of two pericentral cells in vegetative axial filaments (Nam 1999). Molecular studies, based on rbcL sequence data, have corroborated the morphological evidence for the separation of Osmundea from Laurencia (Nam et al. 2000). The species currently assigned to Osmundea have a markedly disjunct distribution, being confined to Atlantic and Mediterranean coasts of Europe and Pacific North America (Serio et al. 1999). In contrast, the genera Laurencia and Chondrophycus are more widely distributed, although the majority of species are found in the Southern Hemisphere (McDermid 1988). There have been only two previous phylogenetic studies of the genus Osmundea. The morphological cladistic analysis of Garbary and Harper (1998) placed O. hybrida basal in the genus, and linked European and Californian species together in pairs such as O. truncata with O. spectabilis. Nam et al.'s (2000) study assessed the phylogenetic significance of several morphological characters in Osmundea by comparative morphological and molecular analyses, but was confined to the European species. The type of spermatangial pits, previously thought to be significant (Saito 1982), was shown to be homoplasious. Urn−shaped spermatangial pits are found only in Osmundea (Nam et al. 1994), but Nam et al. (2000) were 2/11 Constancea 83.9: Phylogeny of Osmundea 12/17/2002 06:46:34 PM unable to determine whether these or cup−shaped spermatangial receptacles are ancestral within the European species of Osmundea. Additional taxa were required to evaluate the level of phylogenetic informativeness of male receptacle shape. In contrast, the presence vs. absence of secondary pit connections between epidermal cells was found to be a synapomorphy for the two clades of European Osmundea species. Again, however, the phylogenetic significance of these characters could not be fully assessed because species from the North Pacific were not available for inclusion in the analyses. The North Pacific species of Osmundea show character combinations that differ from any European species: all have urn− (pocket−) shaped spermatangial receptacles, but only Osmundea spectabilis is reported to have some (rare) secondary pit connections between the epidermal cells (Nam et al. 1994; Serio et al. 1999). It was the main purpose, therefore, of this study to widen our previous phylogenetic analysis of Osmundea to include species that are found in Pacific North America, particularly O. spectabilis, in order to clarify the phylogenetic significance and character evolution of secondary pit connections and spermatangial receptacle shape. The gene chosen for analyses was rbcL, as there is data available for a number of European species of Osmundea. In addition, previous studies have shown this gene to give good resolution of red algal relationships at the species to genus level (e.g., Freshwater et al. 1994; Hommersand et al. 1994; McIvor et al. 2001). We have sequenced eight of the fifteen Osmundea species currently recognized: O. blinksii, O. hybrida, O. osmunda, O. pinnatifida, O. ramosissima, O. spectabilis, O. splendens, and O. truncata, with most of the remaining seven [O. crispa (Hollenberg) Nam, O. maggsiana Serio, Cormaci & Furnari, O. multibulba (Dawson, Neushul & Wildman) Nam, O. pelagiensis (Cormaci, Furnari & Serio) Furnari, O. pelagosae (Schiffner) Nam, O. sinicola (Setchell & Gardner) Nam, and O. verlaquei (Cormaci, Furnari & Serio) Furnari] being of relatively restricted occurrence. In addition to this, we wished to clarify the nomenclatural position of one of the two European species confused until recently under the name Osmundea truncata (Kützing) Nam & Maggs. The second of the sister species was referred to O. ramosissima by Nam et al. (2000), who recognized Osmundea ramosissima Athanasiadis (1996, p. 119) as a valid name for the polynomial Fucus ramosissimus
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