Molecular Phylogeny and Taxonomy of the Aegagropila Clade (Cladophorales, Ulvophyceae), Including the Description of Aegagropilopsis Gen
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J. Phycol. 48, 808–825 (2012) Ó 2012 Phycological Society of America DOI: 10.1111/j.1529-8817.2012.01145.x MOLECULAR PHYLOGENY AND TAXONOMY OF THE AEGAGROPILA CLADE (CLADOPHORALES, ULVOPHYCEAE), INCLUDING THE DESCRIPTION OF AEGAGROPILOPSIS GEN. NOV. AND PSEUDOCLADOPHORA GEN. NOV.1 Christian Boedeker 2 School of Biological Sciences, Victoria University of Wellington, Kelburn Parade, Wellington 6140, New Zealand Charles J. O’Kelly Friday Harbor Laboratories, University of Washington, 620 University Road, Friday Harbor, Washington 98250, USA Wim Star Netherlands Centre for Biodiversity Naturalis (section NHN), Leiden University, Einsteinweg 2, 2300 RA Leiden, The Netherlands and Frederik Leliaert Phycology Research Group, Biology Department, Ghent University, Krijgslaan 281 S8, 9000 Ghent, Belgium The Aegagropila clade represents a unique group Abbreviations: bp, base pairs; BI, Bayesian infer- of cladophoralean green algae occurring mainly in ence; ML, maximum likelihood; MP, maximum brackish and freshwater environments. The clade is parsimony; s.s., sensu stricto sister to the species-rich and primarily marine Clado- phora and Siphonocladus lineages. Phylogenetic analy- ses of partial LSU and SSU nrDNA sequences reveal The Cladophorales is a species-rich order of ulvo- four main lineages within the Aegagropila clade, and phycean green algae with a siphonocladous organi- allow a taxonomic reassessment. One lineage con- zation that is widespread in marine and freshwater sists of two marine ‘Cladophora’ species, for which environments from tropical to polar regions. The the new genus Pseudocladophora and the new family Cladophorales have evolved in three main clades Pseudocladophoraceae are proposed. For the other (Fig. 1, Hanyuda et al. 2002, Leliaert et al. 2003, lineages, the family name Pithophoraceae is rein- Yoshii et al. 2004, Leliaert et al. 2012). The Siphono- stated. Within the Pithophoraceae, the earliest cladus clade (=Siphonocladales s.s.) is morphologi- diverging lineage includes Wittrockiella and Cladopho- cally diverse and mainly distributed in marine rella calcicola, occurring mainly in brackish and sub- tropical waters (Leliaert et al. 2007). Members of aerial habitats. The two other lineages are restricted the Cladophora clade (=Cladophorales s.s. or Clado- to freshwater. One of them shows a strong tendency phoraceae sensu Wille) are morphologically simpler, for epizoism, and consists of Basicladia species and consisting of branched or unbranched filaments, Arnoldiella conchophila. The other lineage includes and have a distribution that extends into cold tem- Aegagropila, Pithophora and a small number of tropi- perate and polar waters. The Aegagropila clade is sis- cal ‘Cladophora’ species. The latter are transferred ter to the Cladophora and Siphonocladus clades, and to the new genus Aegagropilopsis. Previously, polypy- has not yet received a formal taxonomic rank, despite ramidal pyrenoids had been suggested to be apo- robustness in previous phylogenetic studies (Hanyu- morphous for this clade, but we report the finding da et al. 2002, Yoshii et al. 2004). A fourth lineage, of both polypyramidal and bilenticular pyrenoids in Okellyaceae, is sister to the three main clades members of the Pithophoraceae, and thus show that (Fig. 1) and only includes Okellya curvata, an unbran- this character has no diagnostic value. ched, microfilamentous species occurring in temper- Key index words: Arnoldiella; Basicladia; Cladopho- ate marine subtidal habitats (Leliaert et al. 2009a). rella; freshwater; molecular phylogenetics; Pitho- The Aegagropila clade encompasses six species- phoraceae; Pseudocladophoraceae; ribosomal poor or monotypic genera and a small number of DNA; systematics; Wittrockiella freshwater Cladophora species (Hanyuda et al. 2002, Yoshii et al. 2004, Rindi et al. 2006). Hanyuda et al. (2002) suggested that the presence of loraxanthin, chitin and polypyramidal pyrenoids are diagnostic for the Aegagropila clade. Although molecular evi- 1Received 25 March 2011. Accepted 26 January 2012. 2Author for correspondence: e-mail christian.boedeker@ dence clearly indicates the polyphyletic nature of the vuw.ac.nz. genus Cladophora, only few nomenclatural changes 808 PHYLOGENY OF THE PITHOPHORACEAE 809 Okellyaceae The majority of the species in the Aegagropila -marine clade occurs in freshwater environments. The genus -temperate -monotypic Wittrockiella grows in brackish habitats, and Cladopho- -unbranched filaments ra horii C. Hoek (Fig. 2A) and C. conchopheria (Fig. 2B) are the only marine species. Wittrockiella currently encompasses three species, W. lyallii Aegagropila clade -mainly brackish & freshwater (Harv.) C. Hoek, Ducker et Womersley (Fig. 2C), -temperate to tropical W. salina V.J. Chapm. and W. amphibia (Collins) -to date 10 species included -branched filaments Boedeker et G.I. Hansen (Fig. 2F). In Wittrockiella, creeping prostrate axes give rise to upright, unbranched or sparsely branched filaments. A close Siphonocladus clade relationship between W. salina and the (sub)tropi- -exclusively marine cal, subaerial or freshwater species Cladophorella calci- -mainly tropical cola F.E. Fritsch (Fig. 2E) has been suggested by van -species-rich (>100 species) -morphologically most complex den Hoek et al. (1984) based on overall morpholog- ical similarity. The genus Basicladia consists of seven species and is characterized by branched or unbranched upright filaments (Fig. 2, G, I) arising Cladophora clade from an extensive prostrate, rhizome-like stratum -mainly marine consisting of coalescent, branched filaments -tropical-temperate-polar -species-rich (>100 species) (Fig. 2H), with a characteristic long basal cell -branched or unbranched filaments (Fig. 2J). Basicladia has a reputation for occurring on freshwater turtles, but culture experiments have Fig. 1. Schematic phylogenetic tree of the Cladophorales with shown that other substrates can be colonized as well gross information on habitat, species numbers, and morphology for the four main lineages. (Proctor 1958), and the recently included species B. okamurae (Fig. 2, G, H) and B. kosterae (Fig. 2, G, I) are actually only rarely encountered on turtles. have been proposed, namely the recent transfer of The diminutive and poorly known Arnoldiella concho- C. kosterae C. Hoek and C. okamurae (Ueda) C. Hoek phila V.V. Mill. has been found on shells of freshwater to the genus Basicladia (Garbary 2010) and the trans- bivalves (Miller 1928), freshwater gastropods (Kar- fer of C. amphibia Collins to Wittrockiella (Boedeker gupta 1994, Keshri and Hazra 2009) and a range of and Hansen 2010). Species of Cladophora are (still) other substrates (Cox Downing 1970). Pithophora distributed in the three main clades of the Clado- Wittr. is easily recognized by the characteristic aki- phorales (Fig. 1). The lectotype species of Cladophora netes (Fig. 2, K, L) and includes more than 35 taxa, is C. oligoclona (Setchell and Gardner 1920, van den but this number is likely inflated due to plastic mor- Hoek 1963), a synonym of C. rivularis, which is a phological characters (Ernst 1908, Mothes 1930, member of the Cladophora clade (Leliaert and Fott 1971, Pankow and Ta¨uscher 1980). This mainly Boedeker 2007). Thus, taxonomic changes of Clado- (sub)tropical freshwater genus only occurs unat- phora species in the Aegagropila clade and the Siphono- tached in relatively stagnant, nutrient-rich waters cladus clade are required. Cladophora species and can form extensive floating masses that can be (including earlier synonyms) that are part of the Aeg- local nuisances (Entwisle and Price 1992, Lembi agropila clade, as well as candidate Cladophora species 2003). The freshwater species Aegagropila linnaei for the Aegagropila clade (based on morphological or Ku¨tz. (Fig. 2P) is currently regarded as the sole ecological data) that were shown to have other affili- member of its genus (van den Hoek 1963, Hanyuda ations by molecular data, are listed in Table 1. et al. 2002), but a number of potentially closely The Aegagropila clade is interesting from both an related species have been identified (Boedeker et al. evolutionary and ecological perspective. It consti- 2010a). Aegagropila linnaei is the best-known repre- tutes a mainly freshwater ⁄ brackish lineage within sentative of the lineage and gained considerable sci- the predominantly marine Cladophorales. Several entific, cultural (in Japan), and economic members occur in highly specialized niches such as (aquarium trade) fame due to the peculiar lake on the carapaces of freshwater turtles (some mem- balls formed under specific conditions (Kurogi bers of Basicladia), on freshwater snails and bivalves 1980, Niiyama 1989, Boedeker et al. 2010b). (monotypic Arnoldiella and several Basicladia spe- Molecular phylogenetic studies based on SSU cies), as epi- or endophytes of salt marsh plants and rDNA sequence data provided the first insights into mangrove pneumatophores (some members of Witt- the relationships within the Aegagropila clade (Hanyuda rockiella), or on marine intertidal snails (Cladophora et al. 2002, Yoshii et al. 2004, Rindi et al. 2006). conchopheria Sakai). Recently, aerophytic unicells These studies showed that Cladophora conchopheria occurring on tree bark have been described and and C. horii form a sister clade to the rest of the included in this lineage based on DNA sequence Aegagropila clade. The relationships within that clade data (Spongiochrysis hawaiiensis, Rindi et al. 2006). were only partly resolved. Surprisingly, the 810 TABLE