Evolution of complex systems

Nick Matzke rounds up the arguments and evidence, beginning with Darwin’s work, that explains how complex systems needing multiple parts can evolve:

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).

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