Ribosomal RNA phylogeny and the primary lines of evolutionary descent.

Over the past decade, developments in molecular phylogeny using ribosomal RNA (rRNA) sequences have revealed the outlines of the master phylogenetic tree relating all known life-forms. This serves as a framework within which we can begin to understand evolutionary diversity, the evolution of intermediary metabolism, and a host of other biological principles. We provide here a brief overview of some of the findings, which at times offer a different perspective than textbook versions of the evolutionary history of life. As pointed out by Zuckerkandl and Pauling (J. Theoret. Biol. 8, 357-366, 1965) macromolecular sequence comparisons are the most accurate and reliable basis from which to infer phylogenetic relationships. Sequence data are preferable to other molecular methods for assessing evolutionary relatedness (e.g., nucleic acid hybridizations and immunological tests) because they permit straightforward, quantitative interpretation and, importantly, because they form a growing data base for subsequent reference. Moreover, use of sufficiently lengthy sequences avoids mistaking relationships because of “convergence” of phenotypes. There is not necessarily a “best” molecule for comparative sequence studies. The only requirements are that the molecules sequence does not undergo genetic transfer between species, that its function is as strictly constant as possible, and that it contains a sufficient number of residues which change at a rate commensurate with the evolutionary distance considered. The 16Slike and 23Slike rRNAs meet these criteria and are sufficiently conservative in structure that they can be used to establish the most ancient relationships among all organisms. The 5s rRNAs and tRNAs also are conservative in structure, but they contain too few independently varying nucleotide positions to establish the more distant relationships accurately. About four hundred full and partial 16Slike rRNA sequences, mostly prokaryotic, have been determined. The figure shows an unrooted phylogenetic tree (Fitch and Margoliash, Science 755, 279-284, 1967) based on approximately one thousand unambiguously homologous characters (nucleotides) in 18S-like rRNAs. Extant organisms are seen to fall into three, phylogenetically coherent groups, the eukaryotes, the eubacteria, and the archaebacteria (Fox et al., Science 209, 457-463, 1980). These are the primary lines of evolutionary descent-the three “primary kingdoms:’ The exact root of this tree Cannot be placed because that requires a more deeply branching sequence, which cannot exist in a universal phylogeny. It is noteworthy that the line segments connecting the various modern organisms to their common ancestors are not the same length. This means that the lines of descent represented have not evolved at the same rate, a fact evident from comparisons of protein sequences, as well. Therefore, an assumption of isochronicity cannot be used to establish the root of the tree. It often has been supposed that the eukaryotic lineage arose relatively recently, l-2 billion years ago, from a prokaryotic ancestry. This age for the eukaryotes is loosely based on an absence of earlier, eukaryote-like fossils and on extended extrapolations of protein sequence comparisons. However, the figure shows that the eukaryotic nuclear line of descent did not arise from within either of the bacterial lines; rather, it seems as ancient as the bacterial lines. Regardless of the root position in the tree, deep branchings among the eukaryotes attest to this (Sogin et al., PNAS 83, 1383-1387, 1986). On the other hand, the molecular phylogenetic data (not only from rRNA) prove beyond reasonable doubt that the mitochondria and chloroplasts are of eubacterial origins (below). The organisms most familiar to us, the multicellular plants and animals, occupy a rather shallow domain within the eukaryotic line of descent. The developmental programs of the multicellular forms engender incredible