|A. Evolutionary Discontinuities
We usually begin our game of "Twenty Questions" with the query "Animal, Vegetable or Mineral?". Natural philosophers often like to "divide and conquer" the spheres of nature in tres partes , like Caesar dismembering Gaul. Lately, the organic world has been sorted into a popular triplet of Archaea, Bacteria and Eukaryota (Woese 1987). I challenge this tripartition of life, not as incorrect, but as obfuscatory.
The most important understanding of natural diversity achieved within the 20th century may have been the recognition of the deep chasm between the Prokaryotes and the Eukaryotes. Anyone who has entered biology after that division can scarcely appreciate the impact of the concept. it is not superseded by the discovery of deep phylogenetic separations among the prokaryotes. Nor is it threatened by continuing disputes about the pattern of emergence of eukaryotic branches. The prokaryotic/eukaryotic disjunction is of much greater significance in terms of complex evolutionary innovations (Maynard Smith and Szathmary, 1995), and a greater challenge to explanation.
A brief review of some of the major biological innovations shared by all the Eukaryotes may be helpful in posing the problem. These features set Eukaryotes apart from both the Archaea and the Bacteria. One is the eukaryotic chromosome, and the associated equipment required to manage its enhanced genetic burden. The most primitive invention within this complex set of tools is perhaps the nucleosome, the set of histones and associated chromosomal proteins that serve as spools to store the much larger sets of genetic instructions in the eukaryotes, to distribute them in orderly fashion to daughter cells, and to regulate their deployment in appropriate contexts.
Another set of biological innovations consists of the fiber systems within eukaryotic cells employed to give shape and motility to both cells and to parts of cells. The premier manifestation of these fiber systems is in the remarkably complex organelle referred to variously as a flagellum, a cilium, an undulipodium, or - in the case of sperm cells - the tail. Understanding the ubiquity of the eukaryotic signature of 9 + 2 symmetry within these structures was an early triumph of electron microscopy. No comparable structures are known among the Archaea and Bacteria, though some of the molecules have prokaryotic homologues
A third set of eukaryotic distinctions is associated with the electrically excitable cell membrane that surrounds all eukaryotic cells, and provides an order of magnitude greater sensitivity in knowing their environment and in communicating with each other. The properties of the eukaryotic cell membranes are essential for the manifestation of the characteristic eukaryotic phenomena of mulicellular development and nervous activity.
Other distinctive properties of the eukaryotic cell membrane have also been noted, particularly the capacity for ingesting and egesting foreign elements in vacuolar packages. This biological capacity may, indeed, have been responsible for the capture (in plastids and mitochondria) of alternative respiratory and synthetic capabilities from prokaryotes, and for establishing functionally distinctive intracellular environments. We need not, however, summarize all the distinctive features of eukaryotes. Rather, these commonly mentioned characteristics serve as a platform for introducing the biological innovation that has not been generally recognized as perhaps the most distinctively eukaryotic invention of all -- the biological species.
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 Sonneborns explanation for the multiplicity of ciliate species. Specifically he linked Sonneborns 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).
C. Morphological vs Molecular Conservatism
The familiar juxtaposition of Tempos and Modes (Simpson,1942) was inserted into the evolutionary chat room early and provided a focus for dealing with some of the diverse processes and events of evolutionary history. Simpsons major contribution was to deploy fossils to stretch the evolutionary time scale beyond the commonplace verities of the modern world which preoccupied (and still preoccupy) many specialists. But even fossils provide samples of only the last few moments in the history of life on the earth, and consist primarily of eukaryotic remains. The fossils tell us little about the long prehistory assigned to prokaryotes, and the residues of most of the eukaryotic protists are not much more enlightening. Consequently the verities wrested from studies of modern plants and animals are projected uncertainly upon the evolutionary processes of an earlier and very different world.
Expanding the Modern Synthesis to include the protists requires a reorientation of perspectives. The reductionistic technology of genetics manifests its ultimate success in the attribution of a visible morphological difference between two organisms to a difference between allelic mendelian genes, then to differences between sites on a particular chromosome, and finally to a base substitution in a particular DNA sequence. That powerful but flawed perspective leads to the understandable but expensive errors embodied in concepts such as the gene for schizophrenia. The implicit cause and effect argument is so powerful, that a well-trained modern biologist can scarcely imagine that organisms so nearly identical in their microscopic anatomy as Tetrahymena thermophila and T. pyriformis, can be as different in their DNA sequences as a kangaroo and a chimpanzee. Though a significant reciprocity between genotype and phenotype on the evolutionary scale can be argued (Nanney 1982), its acceptance requires a fundamental shift from the anthropic bias of the MES.