Lynne McIvor

rbcL sequences reveal multiple cryptic introductions of the Japanese red alga Polysiphonia harveyi

In Europe, the last 20 years have seen a spectacular increase in accidental introductions of marine species, but it has recently been suggested that both the actual number of invaders and their impacts have been seriously underestimated because of the prevalence of sibling species in marine habitats. The red alga Polysiphoniaharveyi is regarded as an alien in the British Isles and Atlantic Europe, having appeared in various locations there during the past 170 years. Similar or conspecific populations are known from Atlantic North America and Japan. To choose between three competing hypotheses concerning the origin of P. harveyi in Europe, we employed rbcL sequence analysis in conjunction with karyological and interbreeding data for samples and isolates of P. harveyi and various congeners from the Pacific and North Atlantic Oceans. All cultured isolates of P. harveyi were completely interfertile, and there was no evidence of polyploidy or aneuploidy. Thus, this biological species is both morphologically and genetically variable: intraspecific rbcL divergences of up to 2.1% are high even for red algae. Seven rbcL haplotypes were identified. The four most divergent haplotypes were observed in Japanese samples from Hokkaido and south‐central Honshu, which are linked by hypothetical ‘missing’ haplotypes that may be located in northern Honshu. These data are consistent with Japan being the centre of diversity and origin for P. harveyi. Two non‐Japanese lineages were linked to Hokkaido and Honshu, respectively. A single haplotype was found in all North Atlantic and Mediterranean accessions, except for North Carolina, where the haplotype found was the same as that invading in New Zealand and California. The introduction of P. harveyi into New Zealand has gone unnoticed because P. strictissima is a morphologically indistinguishable native sibling species. The sequence divergence between them is 4–5%, greater than between some morphologically distinct red algal species. Two different types of cryptic invasions of P. harveyi have therefore occurred. In addition to its introduction as a cryptic sibling species in New Zealand, P. harveyi has been introduced at least twice into the North Atlantic from presumed different source populations. These two introductions are genetically and probably also physiologically divergent but completely interfertile.

Taxonomy and phylogeny of Osmundea (Rhodomelaceae, Rhodophyta) in Atlantic Europe

Two species of Osmundea Stackhouse (Rhodomelaceae, Rhodophyta) that occur in Atlantic Europe have been confused under the names Osmundea ramosissima (Oeder) Athanasiadis and Osmundea truncata (Kützing) Nam et Maggs, regarded until now as a synonym of O. ramosissima. An epitype from its type locality (Stavanger, Norway) is selected for Osmundea ramosissima Athanasiadis, recognized here as a valid name for Fucus ramosissimus Oeder, nom. illeg. Details of vegetative and reproductive morphology of O. ramosissima are reported, based on material from France, the British Isles, and Helgoland. Osmundea ramosissima resembles other species of Osmundea in its vegetative axial segments with two pericentral cells and one trichoblast, spermatangial development from apical and epidermal cells (filament type), the formation of five pericentral cells in the procarp‐bearing segment of the female trichoblast, and tetrasporangial production from random epidermal cells. Among the species of Osmundea, O. ramosissima is most similar to O. truncata. Both species have discoid holdfasts, secondary pit connections between epidermal cells, and cup‐shaped spermatangial pits. They differ in that: (a) O. ramosissima lacks lenticular wall thickenings and refractive needle‐like inclusions in medullary cells, both of which are present in O. truncata; (b) O. ramosissima has branched spermatangial filaments that terminate in a cluster of several cells, whereas in O. truncata the unbranched spermatangial filaments have a single large terminal sterile cell; and (c) cystocarps of O. ramosissima lack protuberant ostioles but ostioles are remarkably protuberant in O. truncata. Phylogenetic analyses of rbcL sequences of Laurencia obtusa (Hudson) Lamouroux and all five Atlantic European species of Osmundea, including the type species, strongly support the generic status of Osmundea. Osmundea ramosissima and O. truncata are closely related (5.2% sequence divergence) and form a well‐supported clade sister to a clade consisting of O. pinnatifida (Hudson) Stackhouse, O. osmunda Stackhouse and O. hybrida (A. P. de Candolle) Nam. The formation of secondary pit connections between epidermal cells is a synapomorphy for the O. ramosissima+O. truncata clade. The close relationship between species with cup‐shaped spermatangial pits (Osmundea hybrida) and urn‐shaped pits (Osmundea pinnatifida and Osmundea osmunda) shows that spermatangial pit shape is not an important phylogenetic character. Parsimony analysis of a morphological data set also supports the genus Osmundea but conflicts with the molecular trees in infrageneric relationships, placing O. hybrida basal within the Osmundea clade and grouping O. osmunda and O. pinnatifida but not O. truncata and O. ramosissima. A key to Osmundea species is presented.

Morphology, rbcL phylogeny and distribution of distromatic Ulva (Ulvophyceae, Chlorophyta) in Ireland and southern Britain

C.J. Loughnane, L.M. McIvor, F. Rindi, D.B. Stengel and M.D. Guiry. 2008. Morphology, rbcL phylogeny and distribution of distromatic Ulva (Ulvophyceae, Chlorophyta) in Ireland and southern Britain. Phycologia 47: 416–429. DOI: 10.2216/07-61.1 Species of Ulva occur worldwide in all aquatic habitats from freshwater through brackish to fully saline environments. The scarcity of stable morphological characters and the morphological plasticity linked to environmental conditions typical of species referred to this genus make identification and circumscription problematic. In Ireland and Britain the taxonomy of Ulva species has been uncertain, and only three species have been reported: Ulva lactuca, U. rigida and U. olivascens (later reassigned to Umbraulva olivascens). We reassessed the taxonomic status of this genus by combining morphological investigations with analyses of rbcL sequence data for 24 selected specimens from the Irish and southern British shores. This combination of methods allowed the identification of seven lineages, which were considered to represent the following species: Ulva rigida, U. scandinavica, U. lactuca, U. gigantea, U. rotundata, U. californica and Umbraulva olivascens. Of these, U. scandinavica, U. gigantea, U. rotundata and U. californica are newly reported; the distribution of U. olivascens was shown to be much wider than previously thought. The use of morphological features proved to be largely inconclusive and of limited value for circumscription of species. In the rbcL phylogeny, U. olivascens formed a sister clade to all other species. The results support the conspecificity of U. rigida, U. scandinavica and U. armoricana and the conspecificity of U. pseudocurvata and U. compressa already suggested in previous studies.

Using rbcL sequence data to reassess the taxonomic position of some Grateloupia and Dermocorynus species (Halymeniaceae, Rhodophyta) from the north-eastern Atlantic

Grateloupia is one of the most taxonomically complex genera of the Cryptonemiales. Of four species reported to occur in Ireland and Britain, only G. filicina (J.V. Lamouroux) C. Agardh and G. dichotoma J. Agardh are considered as native, with Grateloupia filicina var. luxurians A. Gepp & E.S. Gepp and G. doryphora (Montagne) Howe thought to be recent introductions. Sequence data from the plastid-encoded rbcL gene have been used to assist in clarifying the taxonomic position of these and other members of the Halymeniaceae from Ireland, Britain and neighbouring coasts. Molecular and morphological evidence indicate that the introduced alga G. filicina var. luxurians is only distantly related to the type species, G. filicina. It is here raised to species status as G. luxurians (A. Gepp & E.S. Gepp) R.J. Wilkes, L.M. McIvor & Guiry, stat. nov. A further species, Grateloupia minima P.L. Crouan & H.M. Crouan, has also been reported in the north-eastern Atlantic, but is currently considered as a seasonal or juvenile form of G. filicina. Based on morphological evidence and sequence data, G. minima is distinct from G. filicina, and is hereby reinstated. Although rarely reported, the closely related taxon, Dermocorynus montagnei P. L. Crouan & H. M. Crouan was also included in this study. Molecular and morphological data place Dermocorynus in a clade of Grateloupia species and we therefore propose that Dermocorynus be placed in synonymy with Grateloupia. The relationship between morphology and phylogeny within Grateloupia is discussed in the light of these results.

Reappraisal of the type species of Polysiphonia (Rhodomelaceae, Rhodophyta)

The genus Polysiphonia Greville, nom. cons., has had a long and confused nomenclatural history. At present, Polysiphonia has a wide circumscription, including at least 200 species, but it is heterogeneous in many vegetative and reproductive developmental features. Central to any re-evaluation of the genus is a detailed examination of the type species of Polysiphonia, P. urceolata (Lightfoot ex Dillwyn) Greville, which is conspecific with P. stricta (Dillwyn) Greville. We here report on the vegetative and reproductive morphology of P. stricta, including P. urceolata, based on type and other material from the British Isles. Thalli consist of prostrate and erect ecorticate axes with four pericentral cells, attached by unicellular rhizoids remaining in open connection with pericentral cells. Prostrate axes lack vegetative trichoblasts ; trichoblasts occur seasonally on erect axes. Branch initials are cut off from the subapical cell at intervals of four or five segments in dichotomous and alternating pairs rather than being formed from each axial cell in the spiral pattern typical of most species of Polysiphonia. Spermatangial branch initials, which are trichoblast homologues, are produced directly from each axial cell at the tips of erect branches, not subtended by trichoblasts, and have two- to five-celled sterile tips when mature. The mature carpogonial branch is four-celled with a two-celled first sterile group and a one-celled second sterile group. Following presumed fertilization, direct fusion apparently takes place between carpogonium and auxiliary cell; mature cystocarps are usually urceolate. Tetrasporangia are formed from the third pericentral cell, in straight series, and have two pre-sporangial cover cells. Previous accounts of a third, post-sporangial cover cell could not be substantiated. P. stricta and a small group of other Polysiphonia species differ in several important respects from most members of the genus, which have rhizoids cut off from pericentral cells by a cell division, abundant trichoblasts, spirally arranged tetrasporangia and a post-sporangial cover cell. The branching pattern of P. stricta highlights the difficulties of distinguishing between the tribes Polysiphonieae and Pterosiphonieae.

Gayliella gen. nov in the tribe Ceramieae (Ceramiaceae, Rhodophyta) based on molecular and morphological evidence

On the basis of comparative morphology and phylogenetic analyses of rbcL and LSU rDNA sequence data, a new genus, Gayliella gen. nov., is proposed to accommodate the Ceramium flaccidum complex (C. flaccidum, C. byssoideum, C. gracillimum var. byssoideum, and C. taylorii), C. fimbriatum, and a previously undescribed species from Australia. C. transversale is reinstated and recognized as a distinct species. Through this study, G. flaccida (Kützing) comb. nov., G. transversalis (Collins et Hervey) comb. nov., G. fimbriata (Setchell et N. L. Gardner) comb. nov., G. taylorii comb. nov., G. mazoyerae sp. nov., and G. womersleyi sp. nov. are based on detailed comparative morphology. The species referred to as C. flaccidum and C. dawsonii from Brazil also belong to the new genus. Comparison of Gayliella with Ceramium shows that it differs from the latter by having an alternate branching pattern; three cortical initials per periaxial cell, of which the third is directed basipetally and divides horizontally; and unicellular rhizoids produced from periaxial cells. Our phylogenetic analyses of rbcL and LSU rDNA gene sequence data confirm that Gayliella gen. nov. represents a monophyletic clade distinct from most Ceramium species including the type species, C. virgatum. We also transfer C. recticorticum to the new genus Gayliella.

Molecular analyses elucidate the taxonomy of fully corticated, nonspiny species of Ceramium (Ceramiaceae, Rhodophyta) in the British Isles

Abstract Four fully corticated nonspiny species of Ceramium are currently recognized in the British Isles, all formerly confused under the illegitimate name Ceramium rubrum (Hudson) C. Agardh. One of these species was known briefly as C. nodulosum (Lightfoot) Ducluzeau but, in 1996, P.C. Silva and others [Univ. Calif. Publ. Bot. 79] showed that this is a later homonym of C. nodulosum de Candolle and advocated conserving C. rubrum with a neotype. As an alternative to this, we investigated whether the name C. virgatum Roth 1797 might be available for this species. The aim of the present study was to typify C. virgatum, in the context of better characterizing this and the other fully corticated species of Ceramium that occur in the British Isles, by analysis of plastid DNA (cpDNA) restriction fragment length polymorphism (RFLP) or rbcL sequences (or both) of each species from various sites, including their type localities. The lectotype of C. virgatum is Roths illustration of a Ceramium specimen from Eckwarden, North Sea, which could represent any member of the ‘C. rubrum’ group. Material resembling Roths from the North Sea island of Helgoland is here designated as an epitype of C. virgatum. Its rbcL sequence was aligned with sequences of al1 C. rubrum-like species in the British Isles, viz. C. secundatum, C. botryocarpum, C. pallidum and ‘C. nodulosum’. The Helgoland material was clearly conspecific with the alga previously identified as C. nodulosum from Ireland (0.08% rbcL divergence, compared to a minimum between-species divergence of 1.8%). We therefore suggest that the name C. virgatum Roth should be employed for this species. Each of the four fully corticated species can be identified by morphological features, in particular the number of axial segments between branches. Phylogenetic analyses of rbcL sequences and cpDNA RFLP data showed C. pallidum to be basal among the North Atlantic C. rubrum-like species and indicated a close relationship between C. secundatum and C. botryocarpum.

Molecular systematics of Ceramium and Centroceras (Ceramiaceae, Rhodophyta) from Brazil

Morphological investigations identified 11 Ceramium Roth species, of the 18 previously reported from Brazil. Phylogenetic analyses of sequences of the chloroplast‐encoded rbcL gene confirmed the presence of seven of these species. Three other species are reported from Brazil for the first time. Ceramium affine Setchell & Gardner and C. filicula Harvey ex Womersley were previously known only from the Pacific Ocean (Mexico and Australia, respectively). A new species, C. fujianum Barros‐Barreto et Maggs sp. nov., is described here. Its general habit is similar to that of C. strictum sensu Harvey from Europe but it has one less periaxial cell than C. strictum; its cortical filament arrangement is closest to C. deslongchampsii Chauvin ex Duby, also from Europe, but whorled tetrasporangia partially covered by cortical cells differ strikingly from the naked protruding tetrasporangia of C. deslongchampsii. Ceramium species in which each periaxial cell cuts off transversely only a single basipetal cell formed a robust clade. The genus Ceramium as represented in Brazil is not monophyletic with respect to Centroceras Kützing and Corallophila Weber‐van Bosse; Ceramium nitens, which has axial cells completely covered by rounded cortical cells formed by acropetal and basipetal filaments, did not group with any Ceramium clade but was weakly allied to a species of Corallophila. All three Brazilian Centroceras sequences were attributed to a single species, C. clavulatum.

RbcL sequences indicate a single evolutionary origin of multinucleate cells in the red algal tribe Callithamnieae.

In the Ceramiaceae, one of the largest families of the red algae, there are from 1 to 4000 nuclei in each vegetative cell, but each tribe is homogeneous with respect to the uninucleate/multinucleate character state, except for the Callithamnieae. The goals of this study were to analyze rbcL gene sequences to clarify the evolution of taxa within the tribe Callithamnieae and to evaluate the potential evolutionary significance of the development of multinucleate cells in certain taxa. The genus Aglaothamnion, segregated from Callithamnion because it is uninucleate, was paraphyletic in all analyses. Callithamnion (including Aristothamnion) was monophyletic although not robustly so, apparently due to variations between taxa in rate of sequence evolution. Morphological synapomorphies were identified at different depths in the tree, supporting the molecular phylogenetic analysis. The uninucleate character state is ancestral in this tribe. The evolution of multinucleate cells has occurred once in the Callithamnieae. Multiple nuclei in each cell may combine the benefits of small C values (rapid cell cycle) with large cells (permitting morphological elaboration) while maintaining a constant ratio of nuclear volume: cytoplasmic volume.

Vegetative morphology and rbcL phylogeny of some members of the genera Botryocladia and Irvinea (Rhodymeniaceae, Rhodophyta)

R.J. Wilkes, L. McIvor and M.D. Guiry. 2006. Vegetative morphology and rbcL phylogeny of some members of the genera Botryocladia and Irvinea (Rhodymeniaceae, Rhodophyta). Phycologia 45: 481–494. DOI: 10.2216/05-11.1 Botryocladia is a genus of marine red algae (Rhodophyta) generally found in tropical, subtropical and warm temperate seas. There are currently 35 described species, but the taxonomic status of many of these remains confused. Recently, the genus was split into two genera, with the new genus, Irvinea, described based on morphological and molecular evidence. Only one species, I. ardreana, is currently assigned to the newer genus. For this study, a number of cultured Botryocladia and Irvinea strains from the Mediterranean and Caribbean were examined. Each was examined microscopically and the key features currently used for identification were evaluated. Up to 1277 bp of the rbcL gene was PCR amplified for each isolate and directly sequenced. The molecular data confirm that the species currently considered as Botryocladia do not form a monophyletic group. Botryocladia boergesenii grouped in a clade with I. ardreana with the remaining Botryocladia species in a separate grouping. We propose the transfer of B. boergesenii to the genus Irvinea on the basis of the molecular and morphological data. Morphological and molecular data for the other species examined were also evaluated although little correlation between the morphological features and the rbcL data was observed. The taxonomic utility of some of the morphological features is called into doubt, although clear differences between the genera Botryocladia and Irvinea can be seen. In addition to the morphological features currently regarded as important intergeneric characters, the presence of branched vesicles as an indicator for species of Irvinea should be added.