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els, Population Variation, and Trends and Patterns in Plant Evolution.

Early Evolution and the Origin of Cells

Darwin noticed the sudden appearance of several major animal groups in the oldest known fossiliferous rocks. “If [my] theory be true, it is indisputable that before the lowest Cambrian stratum was deposited . . . the world swarmed with living creatures,” he wrote, noting that he has “no satisfactory answer” to the “question why we do not find rich fossiliferous deposits belonging to these assumed earliest periods” (ref. 10, ch. 10). In his colloquium article, J. William Schopf (11) points out that, one century later, one decade after the publication of Stebbins' Variation and Evolution in Plants (1), the situation had not changed. The known history of life extended only to the beginning of the Cambrian Period, about 550 million years ago. This state would soon change, notably due to three papers published in Science in 1965 by E. S. Barghoorn and S. A. Tyler (12), Preston Cloud (13), and E. S. Barghoorn and J. W. Schopf (14). Schopf speaks of the predecessors who anticipated or made possible the work reported in the three papers, and of his own and others ' contributions to current knowledge, which places the oldest fossils known, in the form of petrified cellular microbes, nearly 3,500 million years ago, seven times older than the Cambrian and reaching into the first quarter of the age of the Earth.

Lynn Margulis, M. F. Dolan, and R. Guerrero set their thesis in the title of their contribution: “The chimeric eukaryote: Origin of the nucleus from the karyomastigont in amitochondriate protists” (15). The karyomastigont is an organellar system composed of at least a nucleus with protein connectors to one (or more) kinetosome. The ancestral eukaryote cell was a chimera between a thermoacidophilic archaebacterium and a heterotrophic eubacterium, a bacterial consortium that evolved into a heterotrophic cell, lacking mitochondria at first. Cells with free nuclei evolved from karyomastigont ancestors at least five times, one of them becoming the mitochondriate aerobic ancestor of most eukaryotes. These authors aver that only two major categories of organisms exist: prokaryotes and eukaryotes. The Archaea, making a third category according to Carl Woese and others (16), should be considered bacteria and classified with them.

The issue of shared genetic organelle origins is also indirectly a subject of the colloquium paper by Jeffrey D. Palmer and colleagues (17). The mitochondrial DNA (mtDNA) of flowering plants (angiosperms) can be more than 100 times larger than mtDNA of animals. Plant mitochondrial genomes evolve rapidly in size, by growing and shrinking. Within the cucumber family, for example, mtDNA varies more than sixfold. Palmer and collaborators have investigated more than 200 angiosperm species and uncovered enormous pattern heterogeneities, some of which are lineage specific. The authors reveal numerous losses of mitochondrial ribosomal protein genes (but only rare losses of respiratory genes), virtually all in some lineages, yet most ribosomal protein genes have been retained in other lineages. High rates of functional transfer of mt ribosomal protein genes to the nucleus account for many of the losses. The authors show that plant mt genomes can increase in size, acquiring DNA sequences by horizontal transfer. Their striking example is a group I intron in the mt cox1 gene, an invasive mobile element that may have transferred between species more than 1,000 independent times during angiosperm evolution. For more than a decade, we have known that the rate of nucleotide substitution in angiosperm mtDNA is very low, 50–100 times lower than that in vertebrate mtDNA. Palmer et al. have now discovered fast substitution rates in Pelargonium and Plantago, two distantly related angiosperms.

Viral and Bacterial Models

Andrés Moya and colleagues (18) point out advantages offered by RNA viruses for the experimental investigation of evolution; notably, the phenotypic features (“phenotypic space”) map fairly directly onto the “genetic space.” In other organisms, from bacteria to humans, the expression of the genetic make-up in the phenotype is mediated, to a lesser or greater degree, but always importantly, by complex interactions between genes, between cells, and the environment. The model that these authors use is the vesicular stomatitis virus (VSV), a rhabdovirus containing 11.2 kb of RNA encoding five proteins. The authors grow different viral clones under variable demographic and environmental conditions, and measure the evolution of fitness in these clones by competition with a control clone. Fitness generally decreases through the serial viral transfers from culture to culture, particularly when bottlenecks associated with transfers are small. Fitness may, however, increase when the transmission rates are high, although the response varies from clone to clone. Moya et al. conclude with an examination of the advantages and disadvantages of traditional population genetics theory for the description of viral evolution vis-à-vis the quasi-species concept, which proposes that the target of natural selection is not a single genotype but rather a cloud of mutants distributed around a most frequent one, the “master sequence.”

Robin M. Bush and colleagues (19) had noticed in their earlier reconstruction of the phylogeny of influenza A virus, based on the hemagglutinin gene, an excess of nonsilent nucleotide substitutions in the terminal branches of the tree. They explore two likely hypotheses to account for this excess. The first is that these nucleotide replacements are host-mediated mutations that have appeared or substantially increased in frequency during passage of the virus in the embryonated eggs in which they are cultured; this hypothesis can account at most for 59 (7.9%) of the 745 nonsilent substitutions observed. The second is that sampling bias is induced by the preference of investigators for sequencing antigenetically dissimilar strains for the purpose of identifying new variants that might call for updating the vaccine, which seems to be the main factor accounting for the replacement excess in terminal branches. The authors point out that the matter is of consequence in vaccine development and that host-mediated mutations should be removed before making decisions about influenza evolution.

Bruce R. Levin and Carl T. Bergstrom (20) note that adaptive evolution in bacteria compared to plants and animals is different in three respects. The two most important factors are (i) the frequency of homologous recombination, which is low in bacteria but high in sexual eukaryotes, and (ii) the phylogenetic range of gene exchange, which is broad in bacteria but narrow (typically, intraspecific) in eukaryotes. A third factor is that the role of viruses, plasmids, and other infectiously transmitted genetic elements is nontrivial in the adaptive evolution of bacteria, while it is negligible in eukaryotes.

Protoctist Models

The mitochondrial genome of kinetoplasts is a highly derived genome in which frameshift errors in reading frames are corrected at the mRNA level. “RNA editing” refers to these posttranscriptional modifications, of which two types are known. One consists of the precise insertion or deletion of U residues, so as to produce open reading frames in the mRNAs encoded in the organelle DNA known as the maxicircle. The other editing system is a modification of 34 Cs into 34 Us in the anticodon of tRNA molecules that can decode the UGA stop codon as tryptophan. Larry Simpson and colleagues (21) seek to unravel the evolution of these two peculiar genetic systems. With support from computer simulations, the authors elaborate an evolutionary scenario that proposes an ancient but unique evolutionary



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