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SYMBIOSIS AS A MECHANISM OF ADAPTATION AND AS A SOURCE OF PHENOTYPIC COMPLEXITY

An alternative to incorporating foreign genes directly into a recipient genome is to develop a close relationship with a species able to provide some beneficial product or process. Symbiotic associations that are mutually beneficial raise immediate issues involving evolutionary stability—issues that Darwin noted and also addressed in The Origin of Species: “Natural Selection cannot possibly produce any modification in a species exclusively for the good of another species; although throughout nature one species incessantly takes advantage of, and profits by, the structures of others” (Darwin, 1859a, p. 201). Because different species possess different capabilities, such as different abilities to use substrates or to produce required metabolic compounds, it is now evident that one species can profit through associations with another species and that this benefit can be mutual; that is, providing a benefit to another species need not entail a cost. These differences in capabilities have become more defined through genomic data, which allow us to use genome sequences to map many metabolic capabilities onto the branches of the tree of life. In many circumstances, one symbiotic partner immediately profits from providing some benefit to the other partner; for example, a compound available in excess to one species might act as a limiting substrate to its partner, which in turn can generate from this substrate additional compounds needed by the first species. Because of the different capabilities of different species, mutually beneficial associations can arise de novo from organisms that are not coevolved, and these associations can then become stabilized through natural selection acting within each species. Mutual advantage often can be enhanced by natural selection when the two lineages are associated across generations, although heritability of the symbiosis is not a requirement for mutual benefit (Sachs et al., 2004). Genomic data inform us that many symbioses are founded on the differences in metabolic capabilities that are enforced by differences in gene content of genomes.

Symbiosis binds organisms from all domains of life and has produced extreme modifications in genomes and structure (e.g., von Dohlen et al., 2001; Waters et al., 2003; Gilson et al., 2006; Nakabachi et al., 2006). In addition, symbiosis affects genome evolution by facilitating gene transfer from one genome to another and by facilitating the loss from one genome of genes that are present in both symbiotic partners. Both of these events can cause a facultative symbiosis to become an obligate one because one partner becomes dependent on products of genes that are restricted to the genome of the other partner. The result is a complex, fused metaorganism, with different compartments for different portions of its required genes, mechanisms for transporting compounds and gene products between compartments, complex development maintaining the different cell types



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