A molecular approach to questions in the phylogeny of planktonic sarcodines
Amaral-Zettler, Linda A.
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The Acantharea and the Polycystinea are two classes of sarcodines (Sarcodina) which are exclusively planktonic and occur strictly in oligotrophic marine environments. Although these protists have been the topic of research since Ernst Haeckel's systematic investigations of samples from the H. M. S. Challenger Expedition, many aspects of their phylogeny and systematics remain poorly resolved. Part of the problem is that the criteria used in systematics of these groups until now has emphasized morphological elements which may be similar due to convergence rather than common ancestry. The application of molecular biology to the field of biological oceanography offers alternative approaches to reexamining sarcodine phylogeny with the goal of producing classifications which reflect evolutionary history. The relationships of the Acantharea and the Polycystinea (order Spumellarida) to other protists were investigated using phylogenetic analyses of small-subunit ribosomal RNA (SSU rRNA) genes. Members of these two classes have been traditionally grouped into the common superclass Actinopoda based on their specialized pseudopodia called axopodia. Sequences from two orders of Acantharea (Symphyacanthida and Chaunacanthida) and four representatives from the order Spumellarida and the class Polycystinea (one solitary and three colonial spumellaria) were aligned against 25 other eukaryotic SSU rRNA sequences extracted from a data base of more than 800 eukaryotic sequences and subjected to distance, maximum parsimony and maximum likelihood analyses. SSU rRNA-based phylogenies do not support the common ancestry of the Acantharea and the Polycystinea, implying that the superclass Actinopoda is artificial and should be discarded. The respective monophyly of the Acantharea and the Polycystinea were supported in all analyses accomplished. The origin of the sequences was confirmed by in situ hybridization experiments. SSU rRNA gene sequences for the solitary spumellarian Thalassicolla nucleata were compared from individuals collected from the Sargasso Sea and the Pacific Ocean. Sequences from pooled individuals showed primary structure differences which were consistent with genus-level variation reported in the literature for unrelated taxa. These results indicate that there may be different strains of this genus which are morphologically identical or that perhaps there may be allelic variation within a given individual. The evolutionary relationships between the solitary T. nucleata and seven colonial spumellaria were analyzed to determine whether the two families of colonial spumellaria (Collosphaeridae and Sphaerozoidae) form a monophyletic evolutionary assemblage. Phylogenies inferred from distance and maximum likelihood methods did not support the monophyly of the colony-forming spumellaria. Parsimony methods did support the monophyly of the colonial spumellaria but with very low bootstrap support. The monophyly of members from the Collosphaeridae family was supported in all analyses with 100% bootstrap support while only distance analyses supported the monophyly of the Sphaerozoidae. The possibility that coloniality has evolved more than once in the Spumellarida has been suggested from observations of the fossil record. However, contrary conclusions have been reached from studies based on skeletal morphogenesis. The results obtained from molecular analyses question the utility of coloniality as a reliable phylogenetic marker. Sequence variation within the SSU rRNA genes of the Spumellarida appears to be sufficient enough for continued fine-scaled comparisons between existing morphospecies. The branching patterns within three of the four orders of the Acantharea were examined using additional SSU rRNA gene sequence data from representatives of the Symphyacanthida, Chaunacanthida and Arthracanthida. The results from this analysis revealed a phylogeny which placed one representative of the Symphyacanthida (Haliommatidium sp.) branching among the Arthracanthida. An examination of the cytological features of Haliommatidium sp. in the literature revealed morphological similarities it shares with the Arthracanthida that could corroborate this result. The variability within acantharian SSU rDNA was significantly less than that observed in spumellaria, and may prove less useful in establishing relationships at taxonomic categories below the order level.
Submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy at the Massachusetts Institute of Technology and the Woods Hole Oceanographic Institution September 1996
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