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J.1529-8817.1988.Tb04480.X.Pdf J. Phycol. 24, 377-385 (1988) A PRELIMINARY INVESTIGATION OF THE PHYLOGENETIC RELATIONSHIPS AMONG THE FRESHWATER, APICAL PORE FIELD-BEARING CYMBELLOID AND GOMPHONEMOID DIATOMS (BACILLARIOPHYCEAE) John P. KocioEek2 and Eugene F. Stoerrner Great Lakes Research Division, 2200 Bonisteel Boulevard, The University of Michigan, Ann Arbor, Michigan 48 109 ABSTRACT shape and most assume a stalked growth habit via Relationships among the apical pore jeld-bearing dia- mucilage exuded through apical pore fields (APF’s). tom genera Brebissonia, Cymbella, Gomphonema, Gomphoneis, Didymosphenia, Gomphocymbella, CLADISTIC ANALYSIS and Reimeria and their close ally Encyonema were Terminal taxa. Included in this group of diatoms evaluated using cladistics. These biraphid genera are a are those taxa which are asymmetrical to the trans- polythetic group dejned by chloroplast number and type, apical axis (Gomphonema Ehrenb., Gomphoneis Cleve, mode of sexual reproduction, valve orientation and pres- Didymosphenia M. Schm.), asymmetrical to the trans- ence of apical porejelds. Character states of valve as well apical and apical axes (Gomphocymbella 0. Mull.) and as non-siliceousfeatures were described and then polarized those taxa asymmetrical to the apical axis. Members using the outgroup method, with the naviculoid genera of this latter group had previously been included in Anomoeoneis and Placoneis sewing as outgroups. The three genera, based on differences in growth habit. cladistic analysis suggests two groups of terminal taxa, Cocconema Ehrenb. represented those cymbelloid corresponding to to a predominantly cymbelloid lineage diatoms which grow at the ends of mucilaginous and a goniphonemoid lineage. Didyrnosphenia, previ- stalks, whereas Encyonema Kiitz. species grow within ously thought to be closely allied to gomphonemoid diatoms, mucilaginous tubes. The genus Cymbella C.A. Ag. is shown to be more closely related to Cymbella. Gom- originally contained free-living species. These three phonema appears to be without distinguishing charac- genera were combined into Cymbella by Heiberg teristics. Relationships of the other genera are described. (1863) who argued that growth habit alone was not The systematic position of small, doubly-punctate Gom- sufficient to base taxonomic differences at the genus phonema species is discussed. level. This view predominated until recently when Krammer (1982b) showed the stalked forms (which Key index words: Bacillariophyeae; Brebissonia; cla- have nomenclatural priority to the name Cymbella) distics; Cymbella; diatoms; Didymosphenia; Encyo- differ substantially from those species which grow nema; evolution; Gomphocymbella; Gomphoneis; in tubes. Krammer (198213) recognized Cymbella and Gomphonema; phylogeny; Reimeria Encjonema as distinct groups (subgenera of Cymbella); they are treated here at the level of genus. The Although diatoms have been observed with light remaining cymbelloid diatoms that fit neither into microscopy for over 275 years (Anonymous 1703, Cymbella nor Encyonema constitute a heterogenous Leeuwenhoek 1703) and with electron microscopy group, called Cymbopleura by Krammer (1982b). Lit- for over 50 years (Krause 1936), little is known about tle is known about their ultrastructure. From this genealogical relationships in some groups, particu- heterogenous group of cymbelloid diatoms Kociolek larly at the generic level. Many authors have inves- and Stoermer (1987) erected the genus Reirneria, tigated relationships at this level of hierarchy; how- which includes the former Cymbella sinuata Greg. ever, more recent works have concentrated almost and its allies. Thus, of the cymbelloid diatoms, Cym- exclusively on marine and freshwater centric dia- bella sensu stricto, Encyonema and Reimeria are rec- toms. ognized as natural groups and included as terminal Relationships among pennate diatom genera have taxa in the analysis. only recently been explored through the cladistic Also included in the analysis is the genus Brebis- approach. Williams (1985) based his view of rela- Sonia Grun., a small group described originally as tionships among members of the family Diatoma- having naviculoid symmetry (Grunow 1860) but re- ceae on results of a cladistic analysis, and Kociolek cently reported to be slightly asymmetrical to the and Stoermer (1986a) used cladistics to evaluate re- apical axis (Mahoney and Reimer 1986). lationships among monoraphid diatoms. In this re- Diagrammatic interpretations of the eight genera port we attempt to evaluate phylogenetic relation- included in the cladistic analysis are presented in ships in one group of freshwater biraphid diatoms. Figure 1. Members of this group exhibit asymmetry in valve Two of the genera, Cymbella and Gomphoneis, are subdivided. The subdivisions include: (1) Cymbella I Accepted: 6 May 1988. mexicana (Ehrenb.) Cleve separated from Cymbella S. Address for reprint requests. s. based on Krammer’s (1982b) observations of dif- 377 378 JOHN P. KOCIOLEK AND EUGENE F. STOERMER BREBISSONIA ities between most species with regard to pattern of reduction division and sexual reproduction. Mann (1983a) observed that the genera Cymbella s. l., Gom- phonema and Didymosphenia, among others, produce ENCYONEMA valves of cis orientation only, and similar observa- tions have been made for Gomphoneis (Kociolek 1988). This provides further evidence that these genera are closely related. Dawson (1973b, c), COX (1977), Kociolek and Rosen (1984), Mahoney and Reimer (1986) and Kociolek and Stoermer (1987) have noted similarities between most of these genera based on APF structure. Representatives from all genera except Encyonema form mucilaginous stalks. REIMERIA Thus, similarities of chloroplast shape, sexual re- production, and APF structure and function suggest these genera form a monophyletic lineage. GOMPHOCYMBELLA Previous interpretations of phylogenetic relationships. - Previous classification schemes for the cymbelloid ? e and gomphonemoid genera considered here have traditionally been based on valve symmetry. Cym- MOSPHENIA belloid diatoms were previously classified together, and gomphonemoid diatoms were thought to form a separate natural group, based on their symmetry features (Muller 1905, Karsten 1928, Patrick and Reimer 1975). The genus Brebissonia has occupied a primitive place in this group, owing to its navic- uloid symmetry, whereas Gomphocymbella, which is asymmetrical to both the apical and transapical axes, has been suggested to be intermediate between cym- belloid and gomphonemoid forms. Very little evidence, other than symmetry consid- FIG. 1. Schematic representation of valve (left) and cytological erations, has been offered to suggest phylogenetic (right) features of the eight genera serving as terminal taxa in relationships between the cymbelloid and gompho- the cladistic analysis. At right, dark circles represent nuclei, dot- nemoid diatoms. Cleve (1894) and Yermoloff (19 18) ted circles represent pyrenoids. pointed to members of the genus Navicula Bory as possible ancestors of the genus Cymbella. The pos- sibility of Navicula-like progenitors to the cymbel- ferences in the structure of foramina, stigmata and loid diatoms has been strengthened by the work of APF’s, and (2) separation of Gomphoneis into two Cox (1979) and Krammer (1982b) which shows at- groups, namely G. elegans (Grun.) Cleve and its allies tributes of the Navicula lineolatae group in cymbel- and G. herculeana and its allies. Distinction between loid diatoms. Mann (1983b) has also suggested the the two groups represents those species without and possible origin of cymbelloid forms from Navicula. with an axial plate, respectively. Some authors have suggested that gomphonemoid A complete listing of terminal taxa is presented diatoms may have arisen from the cymbelloids. Cleve in Table 1. (1894) indicates that gomphocymbelloid diatoms may The freshwater APF-bearing cymbelloid and gompho- be intermediate between the two groups, while nemoid diatoms and their close allies as a monophyletic Krammer and Lange-Bertalot (1985:38) state that lineage. The hypothesis that the terminal taxa form Reimeria sinuata (Greg.) Kociolek & Stoermer is, a monophyletic group is suggested by cytoplasmic, “eine(r) transitorische(n) Art zwischen Cymbella und reproductive, valve and growth habit characteris- Gomphonema. ” tics. As early as 1871 Pfitzer noted similarities in Characters and character polarity. Characters used cytoplasmic features and modes of reproduction be- in the cladistic analysis are described below. Defi- tween species of Cymbella s.1. and Gomphonema. Mer- nitions and distribution of character states are taken eschkowsky (1902- 1903) grouped most of these largely from previously published observations. Po- genera together based on similarities of chloroplasts larity of character states was determined by the out- and, although Gomphoneis was not included in Mer- group method. This criterion for establishing char- eschkowsky’s treatment, unpublished observations acter polarity assumes features found within the indicate G. herculeana has a similarly-shaped chlo- group under investigation (the ingroup) and in sister roplast (Kociolek 1988). Hauptfleisch (1 895), Stein- taxa (the outgroups) were also found in the ancestor ecke (193 l), and Geitler (1973) have noted similar- of the groups and therefore are primitive. Features PHYLOGENETIC RELATIONSHIPS OF DIATOMS 379 TABLE1. Coding of character statesfor the ten terminal taxa. 0 = primitive, I, 2 = derived, 9 = missinglunknown. * represents characters with unordered states. See text for description of features. Tam ~~ DtdpOS- Gom ho Gomphoneu Features Brebrrsonia Cymbella C. mencana phenta Encyonema cym&ll~ elegnns hernrleana Gomphonema Rnmena 1. 0 1 1 1 1 1 0 0 0 1 2. 1 0 0 1 0 1 1 1 1 0 3. 0 0 0 1 0 1 1 1 1 0 4. 0 0 0 1 0 1 1 1 1 0 5. 0 1 1 1 0 0 0 0 0 0 6. 1 0 0 0 0 1 0 1 1 0 7. 0 1 0 0 0 0 0 0 0 0 8. 0 0 1 1 0 0 0 0 0 0 9. 0 0 1 1 0 0 0 0 0 0 10. 0 1 1 1 0 1 0 1 1 0 11. 0 0 0 0 0 0 0 0 0 1 12. 0 0 0 0 0 0 1 1 0 0 13. 0 0 0 0 0 0 1 1 0 0 14. 0 0 0 0 0 0 1 1 0 0 15. 0 0 0 0 0 0 0 1 0 0 16. 0 1 1 1 0 0 0 0 0 0 17.* 9 2 2 2 1 1 9 1 1 1 18.* 9 2 2 2 1 1 9 1 1 1 19.* 9 2 2 2 1 9 9 1 1 1 20.
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