1.3. Theory: the evolution of systems with multiple required components
The standard answer to this question was put forward by Darwin. Mivart (1871) argued that the “incipient stages of useful structures” could not have evolved gradually by variation and natural selection, because the intermediate stages of complex systems would have been nonfunctional. Darwin replied in the 6th edition of Origin of Species (Darwin, 1872) by emphasizing the importance of change of function in evolution. Although Darwin’s most famous discussion of the evolution of a complex system, the eye, was an example of massive improvement of function from a rudimentary ancestor (Salvini-Plawen and Mayr, 1977; Nilsson and Pelger, 1994), Darwin gave equal weight to examples of functional shift in evolution. These included the complex reproductive devices of orchids and barnacles, groups with which he was particularly familiar (Darwin, 1851, 1854, 1862). Intricate multi-component systems such as these could not have originated by gradual improvement of a single function, but if systems and components underwent functional shift, then selection could have preserved intermediates for a function different from the final one. The equal importance of improvement of function and change of function for understanding the evolutionary origin of novel complex systems has been similarly emphasized by later workers (Maynard Smith, 1975; Mayr, 1976). Recent studies give cooption of structures a key role in the origin of feathers (Prum and Brush, 2002), and novel organs (Pellmyr and Krenn, 2002); Mayr (1976) gives many other examples. Computer simulations also show the importance of cooption for the origin of complex systems with multiple required parts (Lenski et al., 2003).
Do these common insights from classical, organismal evolutionary biology help us to understand the solution to the puzzle Macnab put forward regarding the origin of flagellum? Cooption at the molecular level is in fact as well-documented at it is at the macroscopic level (Ganfornina and Sanchez, 1999; Thornhill and Ussery, 2000; True and Carroll, 2002). It has been implicated in origin of ancient multi-component molecular systems such as the Krebs cycle (Melendez-Hevia et al., 1996) as well as the rapid origin of multi-component catabolic pathways for abiotic toxins that humans have recently introduced into the environment, such as pentachlorophenol (Anandarajah et al., 2000; Copley, 2000), atrazine (de Souza et al., 1998; Sadowsky et al., 1998; Seffernick and Wackett, 2001), and 2,4-dinitrotoluene (Johnson et al., 2002); many other cases of catabolic pathway evolution exist (Mortlock, 1992). All of these systems absolutely require multiple protein species for proper function. Even for some molecular systems equaling the flagellum in complexity, reasonably detailed reconstructions of evolutionary origins exist. Generally these are available for systems which originated relatively recently in geological history, which are well-studied due to medical importance, and where phylogeny is relatively well resolved; examples include the vertebrate blood-clotting cascade (Doolittle and Feng, 1987; Hanumanthaiah et al., 2002; Jiang and Doolittle, 2003) and the vertebrate immune system (Muller et al., 1999; Pasquier and Litman, 2000).
Thornhill and Ussery (2000) summarized the general pathways by which systems with multiple required components may evolve. They delineate three gradual routes to such systems: parallel direct evolution (coevolution of components), elimination of functional redundancy (“scaffolding,” the loss of once necessary but now unnecessary components) and adoption from a different function (“cooption,” functional shift of components); a fourth route, serial direct evolution (change along a single axis), could not produce multiple-components-required systems. However, Thornhill and Ussery’s analysis did not distinguish between the various levels of biological organization at which these pathways might operate. The above-cited literature on the evolution of complex molecular systems indicates that complex systems usually originate by a key shift in function of an ancestral system, followed by an intensive period of improvement of the originally crudely functioning design. At the level of the system, cooption is usually the key event in the origin of the modern system with the function of interest. However, a great deal of the complexity in terms of numbers of parts is added to the system after origination. These accessory parts get added by duplication and cooption of novel genes (for reviews of gene duplication in evolution, see Long, 2001; Chothia et al., 2003; Hooper and Berg, 2003) and/or duplication and subfunctionalization (Force et al., 1999) of genes already involved in the crudely-functioning system. Cooption of whole subsystems, linking them to the “core” system, may also occur.
Therefore, improvement of function at the system level might be implemented by cooption at the level of a protein or subsystem. Change of function at the system level might occur without any lower level cooption of new components. Thornhill and Ussery’s four routes can be reduced to the two major pathways proposed by Darwin: improvement of current function (optimization) and shift of function (cooption). Cooption remains its own category, while the other three routes (serial direct evolution, parallel direct evolution, and elimination of functional redundancy) can be considered as three versions of functional improvement, with the lower-level components undergoing optimization, coevolutionary optimization, or loss, respectively. This conceptual framework is basically equivalent to the patchwork model for the evolution of metabolic pathways (Melendez-Hevia et al., 1996; Copley, 2000), where components are recruited from diverse sources and functional improvement or functional shift might occur at any organizational level, e.g. system, subsystem, protein, or protein domain.
