B. The Centrality of the Biological Species

The prokaryotic/ eukaryotic disjunction is characterized by the acquisition of a distinctive genetic economy, that which underlies the theoretical consolidation we often refer to as the “Modern Evolutionary Synthesis” (MES), anticipated by Fisher and Wright, consolidated by Theodosius Dobzhansky in 1937 and elaborated by Mayr, Simpson, Stebbins and others (Provine, 1985). The realization has only gradually emerged that the biological species concept (BSC) is inappropriate for Archaea and Bacteria. The prokaryotes do not have the biological properties required to sustain the closed gene pools essential for the species of the MES. The prokaryotic genetic systems maintain some coherence as integrated evolutionary units; Bacillus subtilis is not likely to be confused with Escherichia coli. But these evolutionary units are not comparable to the closed genetic units referred to as Drosophila melanogaster or Tetrahymena thermophila. The prokaryotic “species” are inherently “leaky”. Horizontal genetic transfer is an essential source of genetic diversity, supplementing mutation and recombination which are the source of genetic variation in the eukaryotic economy.

This point of view needs to be set into a larger evolutionary context. All modern forms of life on Earth utilize the same system of molecular information management, and are universally considered to have had a common origin. That origin is generally considered to have been very soon after the primitive Earth was formed, though some controversy still exists over the interpretation of the traces of life in the oldest rocks. The most generally acceptable phylogenies are those based on the conserved functional elements of the information processing system, especially the ribosomal RNAs. While techniques for constructing evolutionary trees from these conservative molecules are most effective for relatively recent evolutionary events, they yield less secure structures for more ancient junctions. Even the most sophisticated treeing procedures (Van de Peer, 2000) continue to be frustrated by the branching details at the base of the eukaryotes. All the major eukaryotes groups seem to have exploded simultaneously at a remote time in the history of the Earth - manifesting no clear branching pattern in the “eukaryotic crown”, and with all lineages retaining the fundamental eukaryotic “inventions”, however singularly they are employed in specialized habitats. Though the ribosomal tree of the eukaryotes connects to that of the prokaryotes, probably closer to the Archaea than to the Bacteria, little hint is available for the sources of the major eukaryotic innovations, though Margulis has sought assiduously for prokaryotic traces.

Woese (2002) has recently discussed some of the difficult issues associated with the appearance of the first cells from the proposed pools of replicating nucleic molecules. He projects the genetic leakiness of modern prokaryotes backward to a chaotic pool of replicating genetic elements from which local configurations only gradually acquired control of their horizontal movements and began to develop exclusion mechanisms. He proposes that eventually these local configurations acquired sufficient selective advantage to give their collective properties greater selective leverage than that of the individual components. At this point, which he refers to the Darwinian Threshold, he suggests that “vertical” evolutionary forces become significant, and the cell becomes a distinctive evolutionary entity. He suggests that a similar Darwinian Threshold was reached three time for three distinctive kinds of cells. We argue that the “threshold” at the base of the eukaryotes was substantially different from that for prokaryotic cells. The disjunction at the base of the eukaryotes was a saltatory episode, not a gradual accumulation of new properties.

The genetically leaky prokaryotic cell of modern times still does not have the properties of the eukaryotic cell, nor does the prokaryotic “species” have the features that made the “biological species concept” the foundation of the “Modern Synthesis”. The MES was petrified in 1940, and synthesized in fact only our understanding of eukaryotic evolution. At the beginning of another century, a new synthesis is required to encompass evolutionary mechanisms in prokaryotes.

This perspective implies that the distinctive tempos and modes of evolution described in the “evolutionary synthesis” came into place only half through the history of life on earth, and are projected only with caution upon earlier eras of life, and on modern prokaryotic microbes. This perspective bears upon the contentious issue of the units of selection. The Naked Gene was the primordial unit of selection during the early history of life. That primacy was gradually surrendered to more complex associations of molecules, but the lonely gene continues it have significant selective leverage in modern prokaryotes. But with the saltatory appearance of the eukaryotes on the evolutionary stage the gene pool displaced the gene from the center of the darwinian stage and opened up new evolutionary venues.

The closed gene pool owed its evolutionary success to its focus on genomic “coadapted gene complexes” suitable for the exploitation of the strategy of “divide and conquer” within the ecosystem. The “invention” of species allowed the environment to be divided into a much finer grained mosaic of subtly distinguished eco-niches, maintained and exploited by sophisticated genomic genetic strategies.

While this concept of the gene pool was the foundation of the MES, its application to protists and its ecological implications were first glimpsed by Tracy Sonneborn (1957) in his studies of the genetic economies of the sibling species of the Paramecium aurelia complex. His insights were misunderstood and challenged by Ernst Mayr (1957), who largely surpressed their incorporation into modern population genetics and systematics (See Schloegel, 1999).

Nanney (1980) briefly elaborated Sonneborn’s explanation for the multiplicity of ciliate species. Specifically he linked Sonneborn’s inbreeding-outbreeding classification of genetic economies to the familiar dialectic between specialist and generalist life styles. Inbreeders tend to be exploiters of small or temporary niches, while outbreeders are more likely to prosper in a wider range of environments, both geographic and physiological. The rationale for this linkage was based on a strategic balance in the use of the two alternative sources of genetic variety. Inbreeders are more dependent upon “mutational variety”, made more accessible through haploidy or (in diploids) frequent resort to autogamy or breeding with close relatives. Outbreeders are more dependent upon “recombinational variety”, which they achieve by maximizing mating with strangers over a relatively long life span. Neither strategy has permitted significant access to horizontal genetic transfer from other cellular systems throughout eukaryotic evolution (Stanhope et al., 2001).