Sandra C. Lindstrom

A NEW LOOK AT AN ANCIENT ORDER: GENERIC REVISION OF THE BANGIALES (RHODOPHYTA)†

The red algal order Bangiales has been revised as a result of detailed regional studies and the development of expert local knowledge of Bangiales floras, followed by collaborative global analyses based on wide taxon sampling and molecular analyses. Combined analyses of the nuclear SSU rRNA gene and the plastid RUBISCO LSU (rbcL) gene for 157 Bangiales taxa have been conducted. Fifteen genera of Bangiales, seven filamentous and eight foliose, are recognized. This classification includes five newly described and two resurrected genera. This revision constitutes a major change in understanding relationships and evolution in this order. The genus Porphyra is now restricted to five described species and a number of undescribed species. Other foliose taxa previously placed in Porphyra are now recognized to belong to the genera Boreophyllum gen. nov., Clymene gen. nov., Fuscifolium gen. nov., Lysithea gen. nov., Miuraea gen. nov., Pyropia, and Wildemania. Four of the seven filamentous genera recognized in our analyses already have generic names (Bangia, Dione, Minerva, and Pseudobangia), and are all currently monotypic. The unnamed filamentous genera are clearly composed of multiple species, and few of these species have names. Further research is required: the genus to which the marine taxon Bangia fuscopurpurea belongs is not known, and there are also a large number of species previously described as Porphyra for which nuclear SSU ribosomal RNA (nrSSU) or rbcL sequence data should be obtained so that they can be assigned to the appropriate genus.

A NEW LOOK AT AN ANCIENT ORDER: GENERIC REVISION OF THE BANGIALES (RHODOPHYTA)(1).

The red algal order Bangiales has been revised as a result of detailed regional studies and the development of expert local knowledge of Bangiales floras, followed by collaborative global analyses based on wide taxon sampling and molecular analyses. Combined analyses of the nuclear SSU rRNA gene and the plastid RUBISCO LSU (rbcL) gene for 157 Bangiales taxa have been conducted. Fifteen genera of Bangiales, seven filamentous and eight foliose, are recognized. This classification includes five newly described and two resurrected genera. This revision constitutes a major change in understanding relationships and evolution in this order. The genus Porphyra is now restricted to five described species and a number of undescribed species. Other foliose taxa previously placed in Porphyra are now recognized to belong to the genera Boreophyllum gen. nov., Clymene gen. nov., Fuscifolium gen. nov., Lysithea gen. nov., Miuraea gen. nov., Pyropia, and Wildemania. Four of the seven filamentous genera recognized in our analyses already have generic names (Bangia, Dione, Minerva, and Pseudobangia), and are all currently monotypic. The unnamed filamentous genera are clearly composed of multiple species, and few of these species have names. Further research is required: the genus to which the marine taxon Bangia fuscopurpurea belongs is not known, and there are also a large number of species previously described as Porphyra for which nuclear SSU ribosomal RNA (nrSSU) or rbcL sequence data should be obtained so that they can be assigned to the appropriate genus.

PHYLOGENY OF THE DUMONTIACEAE (GIGARTINALES, RHODOPHYTA) AND ASSOCIATED FAMILIES BASED ON SSU rDNA AND INTERNAL TRANSCRIBED SPACER SEQUENCE DATA

Small subunit (SSU) rDNA was sequenced for 25 species in 19 genera of the Gigartinales (Rhodophyta). As well, the internal transcribed spacer (ITS) region was sequenced, and a data matrix of 36 morphological characters was constructed for 16 species of Dumontiaceae. Phylogenetic trees were calculated from a multiple alignment of the SSU sequence data to infer relationships between species of Dumontiaceae and other gigartinalean taxa. The SSU analysis produced a polyphyletic Dumontiaceae. Notably, Acrosymphyton failed to associate with the included Gigartinales, let alone the Dumontiaceae, supporting an earlier proposal to remove it to a new family. The analyses were equivocal about the phylogenetic affinities of Dudresnaya, which clustered with the Kallymeniaceae, and the affinities of the Indo‐West Pacific Gibsmithia, Kraftia, and Dasyphloea, the last‐mentioned clustering with the Antarctic Gainiaceae, and these four taxa with Portieria (Rhizophyllidaceae). Further investigations are necessary to resolve relationships among these taxa. Rhodopeltis, a genus recently moved to the Dumontiaceae from the Polyideaceae, showed a weak association with the remaining northern Dumontiaceae. The final group consisted of cold‐temperate Northern Hemisphere species. Phylogenetic analyses using a combination of SSU, ITS, and morphological data within this clade produced two strongly supported clades, a Dilsea/Neodilsea clade and a Cryptosiphonia/Dumontia clade. Dilsea is derived from a paraphyletic Neodilsea and may itself be polyphyletic. Atlantic and Pacific isolates of Dumontia contorta clearly showed sufficient divergence to warrant recognition as distinct species, and Dumontia alaskana, sp. nov. is proposed for the Pacific species.

rbcL gene sequences reveal relationships among north-east Pacific species of Porphyra (Bangiales, Rhodophyta) and a new species, P. aestivalis

Phylogenetic analyses of the rbcL (chloroplast Rubisco large subunit) gene from 23 newly sequenced species of Porphyra, primarily from the north‐east Pacific, one Bangia and previously published sequences from both genera resolve relationships among most species of Porphyra and reveal five clades of species with Porphyra‐type morphologies among a number of Bangia lineages: (1) P. papenfussii V. Krishnam; (2) P. mumfordii S. C. Lindstrom et K. M. Cole and P. rediviva Stiller et Waaland together with a group of north Atlantic species, including the type of the genus, P. purpurea (Wahl‐enb.) C. Agardh; (3) P. cuneiformis (Setch. et Hus) V. Krishnam., P. occidentalis Setch. et Hus, P. schizo‐phylla Hollenb., and P. variegata (Kjellm.) Kjellm. and their Atlantic sibling species, all distromatic; (4) P. aestivalis sp. nov. and its north Atlantic sibling, P. birdiae C. D. Neefus et A. C. Mathieson; and (5) a speciose clade containing both Pacific and Atlantic representatives. Close relationships are confirmed between sibling species previously identified by iso‐zymes, morphology and chromosomal features. The morphologically similar dioecious P. pseudolanceolata V. Krishnam., P. conwayae (S. C. Lindstrom et K. M. Cole) stat. nov., and P. lanceolata (Setch. et Hus) G. M. Smith occur in a strongly supported subclade in clade 5 together with the monoecious P. fallax S. C. Lindstrom et K. M. Cole. Results presented here highlight the need for intensive taxon sampling and for examination of different parts of the genome to understand more fully relationships among species and higher level taxa in the Bangiales.

New, resurrected and redefined species of Mastocarpus (Phyllophoraceae, Rhodophyta) from the northeast Pacific

Lindstrom S.C., Hughey J.R. and Martone P.T. 2011. New, resurrected and redefined species of Mastocarpus (Phyllophoraceae, Rhodophyta). Phycologia 50: 661–683. DOI: 10.2216/10-38.1 Recent molecular phylogenetic investigations of the red algal genus Mastocarpus from the northeast Pacific resolved numerous cryptic species. Although species were clearly defined through genetic analyses, the correct names to apply to the species remained unclear due to both morphological variability within species and morphological similarity between species. To determine the appropriate name for each entity, we analyzed DNA from type material of taxa previously ascribed to Mastocarpus. In combination with this analysis, an updated phylogeny based on a broad range of geographical and morphological collections is presented that includes data from nuclear (ribosomal internal transcribed spacers [ITS]), chloroplast (rbcL) and mitochondrial [cytochrome oxidase I (COI)] genomes. By analyzing partial ITS region sequences of type specimens, we are able to match currently accepted names (Mastocarpus papillatus, M. pacificus and M. jardinii) to modern collections. We resurrect the following specific epithets and propose the new combinations Mastocarpus cristatus, Mastocarpus latissimus and Mastocarpus agardhii, and we create new species for which we were unable to verify an existing name: Mastocarpus alaskensis, Mastocarpus intermedius, Mastocarpus vancouveriensis, Mastocarpus californianus and Mastocarpus rigidus. The species formerly included in M. papillatus are now identified as Mastocarpus alaskensis, M. papillatus, Mastocarpus intermedius, Mastocarpus cristatus, Mastocarpus vancouveriensis and Mastocarpus latissimus. The name M. jardinii applies to a species thus far collected only from Moss Beach in San Mateo County and the Monterey Peninsula, both in California. Specimens other than the type previously assigned to M. jardinii are now separated into three species: Mastocarpus rigidus, Mastocarpus californianus and Mastocarpus agardhii. Mastocarpus cristatus represents a species closely allied to Clade 3 (Mastocarpus intermedius), and M. pacificus represents Clade 7. Morphological and anatomical diagnoses, along with vertical distributions and geographic ranges, are provided for each species.

THE BIOGEOGRAPHIC ORIGIN OF ARCTIC ENDEMIC SEAWEEDS: A THERMOGEOGRAPHIC VIEW1

The Arctic is geologically and biogeographically young, and the origin of its seaweed flora has been widely debated. The Arctic littoral biogeographic region dates from the latest Tertiary and Pleistocene. Following the opening of Bering Strait, about 3.5 mya, the “Great Trans‐Arctic Biotic Interchange” populated the Arctic with a fauna strongly dominated by species of North Pacific origin. The Thermogeographic Model (TM) demonstrates why climate and geography continued to support this pattern in the Pleistocene. Thus, Arctic and Atlantic subarctic species of seaweeds are likely to be evolutionarily “based” in the North Pacific, subarctic species are likely to be widespread in the warmer Arctic, and species of Atlantic Boreal or warmer origin are unlikely in the Arctic and Subarctic. Although Arctic seaweeds have been thought to have a greater affinity with the North Atlantic, we have reanalyzed the Arctic endemic algal flora, using the Thermogeographic Model and evolutionary trees based on molecular data, to demonstrate otherwise. There are 35 congeneric species of the six, abundant Arctic Rhodophyta that we treat in this paper; 32 of these species (91%) occur in the North Pacific, two species (6%) occur in the Boreal or warmer Atlantic Ocean, and a single species is panoceanic, but restricted to the Subarctic. Laminaria solidungula J. Agardh, a kelp Arctic “endemic” species, has 18 sister species. While only eleven (61%) occur in the North Pacific, this rapidly dispersing and evolving genus is a terminal member of a diverse family and order (Laminariales) widely accepted to have evolved in the North Pacific. Thus, both the physical/time‐based TM and the dominant biogeographic pattern of relatives of Arctic macrophytes suggest strong compliance with the evidence of zoology, geology, and paleoclimatology that the Arctic marine flora is largely of Pacific origin.

Cryptic diversity, biogeography and genetic variation in Northeast Pacific species of Porphyra sensu lato (Bangiales, Rhodophyta)

We sequenced the chloroplast rubisco large subunit (rbcL) gene in 236 samples of Porphyra sensu lato from the northeast Pacific. Comparisons of sequences within the study area as well as comparisons with published sequences revealed up to five cryptic species among the 22 named species: a species closely related to Porphyra abbottiae, a species previously identified as P. pseudolinearis, a species closely related to P. pseudolanceolata and previously identified as that species, a previously unknown species from the eastern Aleutian Islands, and a species closely related to P. schizophylla and previously identified as that species. All of these previously unrecognized species had high bootstrap values separating them from the other species. In addition, our wide geographic sampling allowed us to extend, curtail or clarify the geographic ranges of a number of the species. We also provide published sequences for P. gardneri and P. smithii for the first time. We compared amount of sequence divergence within species grouped on the basis of sexuality (monoecious, sectored into separate male and female “halves”, or dioecious), habitat (high, mid, or low intertidal/subtidal), and seasonality (winter, spring, or summer) using Tukey’s HSD t test, but we observed no significant differences between species grouped in this manner. Different species showed different levels of genetic variation in the rbcL gene apparently unrelated to these traits. Also, we observed no differences in the patterns of genetic variation in a species based on whether the specimens were collected from outside or from within the region covered by ice during Pleistocene glaciations.

Misleading morphologies and the importance of sequencing type specimens for resolving coralline taxonomy (Corallinales, Rhodophyta): Pachyarthron cretaceum is Corallina officinalis.

Coralline red algae play a key role in the ecology of near shore marine ecosystems and are increasingly being used to study the effects of climate change in the marine environment. Corallines are very difficult to identify to species, and even to genus, using morpho‐anatomy, likely complicating studies of their ecology, physiology, and biodiversity. We sequenced a 296 base pair fragment of chloroplast DNA from a 187‐year‐old isolectotype specimen of Pachyarthron cretaceum, a morphologically distinct geniculate species, to demonstrate that coralline morphology is often misleading and that species names can only be applied unequivocally by comparing DNA sequences from type material with sequences from field‐collected specimens. Our results indicate that Pachyarthron cretaceum is synonymous with Corallina officinalis.

Isozymes in macroalgae (seaweeds): genetic differentiation, genetic variability and applications in systematics

Use of isozymes (including allozymes) in studies of population genetics and systematics of seaweeds has increased sufficiently in the last decade to allow some generalization. Only a single locus has been observed for about half the enzymes analysed in seaweeds, compared with 29% in vascular plants. Compared with higher plants, macroalgal species generally have low amounts of electrophoretically detectable genetic variation; the lowest levels of genetic variation found in natural populations are those reported for seaweeds. Nonetheless, seaweeds show an association between levels of genetic diversity as revealed by isozymes and species-specific attributes, such as mating system and predominance of asexual versus sexual reproduction. In systematic studies, isozymes have revealed cryptic species and identified pairs of sibling taxa. The quaternary structure of enzymes appears to be conserved at the phylum level. With the current availability of improved techniques for enzyme electrophoresis and for data int...

A new look at an ancient order: generic revision of the Bangiales

The red algal order Bangiales has been revised as a result of detailed regional studies and the development of expert local knowledge of Bangiales floras, followed by collaborative global analyses based on wide taxon sampling and molecular analyses. Combined analyses of the nuclear SSU rRNA gene and the plastid RUBISCO LSU (rbcL) gene for 157 Bangiales taxa have been conducted. Fifteen genera of Bangiales, seven filamentous and eight foliose, are recognized. This classification includes five newly described and two resurrected genera. This revision constitutes a major change in understanding relationships and evolution in this order. The genus Porphyra is now restricted to five described species and a number of undescribed species. Other foliose taxa previously placed in Porphyra are now recognized to belong to the genera Boreophyllum gen. nov., Clymene gen. nov., Fuscifolium gen. nov., Lysithea gen. nov., Miuraea gen. nov., Pyropia, and Wildemania. Four of the seven filamentous genera recognized in our analyses already have generic names (Bangia, Dione, Minerva, and Pseudobangia), and are all currently monotypic. The unnamed filamentous genera are clearly composed of multiple species, and few of these species have names. Further research is required: the genus to which the marine taxon Bangia fuscopurpurea belongs is not known, and there are also a large number of species previously described as Porphyra for which nuclear SSU ribosomal RNA (nrSSU) or rbcL sequence data should be obtained so that they can be assigned to the appropriate genus.