Smith, John Maynard, and Eors Szathmary. “Symbiosis.” In The Major Transitions in Evolution . Oxford University Press, 1997.

The establishment of a permanent and obligate coexistence of genetic entities that were once capable of independent existence played an important part in the origin of the eukaryotes, and, if our earlier speculations are correct, in the origin of cells and chromosomes. In this chapter, we discuss other examples of symbiosis. The term is used to include all cases in which two or more different kinds of organism live in close association: thus it extends from parasitism to mutualism. Mutualism has been defined as a relationship from which both partners benefit. However, as will become clearer below, it is hard to measure, or even to define, ‘benefits’: in what sense is a mitochondrion today better off than its once free-living ancestors? The two questions that we shall ask are: • What are the selective force acting on the two partners in present-day symbioses? • Could such selective forces lead to the establishment of permanent and obligate coexistence? First, however, we review briefly some of the ecologically more important symbioses (for further examples, see Pirozynski & Hawksworth, 1988; Margulis & Fester, 1991). We mention only a fraction of the known mutualistic associations. Others, including cases of interaction between animals and prokaryotes, are discussed below. It is striking that symbiotic relationships have been important in the utilization by plants of nutrient-poor soils, the colonization of bare rock, life in deep-sea vents, the construction of coral reefs, and the utilization of plant material by several groups of insects. Sonea (1991; see also Sonea & Panisset, 1983) has pictured the world of bacteria as a single superorganism, whose individual component cells rely for their survival on ecological exchange of metabolites, and on genetic exchange via plasmids and phages. This picture has the virtue of emphasizing the important role played by plasmids and temperate phages in conferring on individual bacterial cells capacities needed in particular environments—for example, resistance to antibiotics, tolerance of heavy metals and new metabolic abilities. But the picture suffers from the drawback that is fatal to all holistic models of evolution, from the Gaia hypothesis downwards, of losing all sight of the units of selection, and hence of lacking any model of the dynamics of evolutionary change.

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