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1 The Problem of the Evolvability of Gene Regulation Networks Organisms are superbly well engineered to survive and reproduce in their environments. We humans have achieved a wide variety of engineering feats, from computers to space stations, and we have learned to manipulate natural organisms with biotechnology, but it remains well beyond our capacity to build from scratch even simple forms of life capable of surviving and reproducing in a natural environment. The engineering of complex organisms , such as vertebrates, probably will always remain beyond our reach. The only way we can produce a complex organism is the old-fashioned way. Explaining the adaptive complexity of organisms has always been a goal of biology. It was long believed that the characteristics of species remained static and must have been designed by God. In fact, the superb engineering of organisms was the foundation of the argument from design for the existence of God. This argument was most famously presented by the natural theologian William Paley (1743–1805), who used the analogy of a watch and its maker: In crossing a heath, suppose I pitched my foot against a stone, and were asked how the stone came to be there; I might possibly answer, that, for anything I knew to the contrary, it had lain there forever: nor would it perhaps be very easy to show the absurdity of this answer. But suppose I had found a watch upon the ground, and it should be inquired how the watch happened to be in that place; I should hardly think of the answer I had before given, that for anything I knew, the watch might have always been there. . . . There must have existed, at some time, and at some place or other, an artificer or artificers, who formed [the watch] for the purpose which we find it actually to answer; who comprehended its construction, and designed its use. . . . Every indication of contrivance, every manifestation of design, which existed in the watch, exists in the works of nature; with the difference, on the side of nature, of being greater or more, and that in a degree which exceeds all computation. (Paley 1802) 2 Chapter 1 If we can reason from the design of a watch to the existence of its designer, Paley argued, we can certainly reason from the design of an organism, which is finer than that of a watch “in a degree which exceeds all computation ,” to the existence of its designer—God. A number of thinkers would challenge this conventional wisdom. I will introduce some of them here, not as elements of a complete history of evolutionary theory, but rather as elements of a narrative that leads to the problem this book addresses: the problem of the evolvability of gene regulation networks. 1.1 Erasmus Darwin Erasmus Darwin (1731–1802)—physician, naturalist, and grandfather of Charles—proposed in his two-volume work Zoonomia, first published in 1794–1796, that every living organism on Earth had descended from a microscopic aquatic filament. All the various forms extant in Darwin’s day had “transmuted” from this common ancestor. “In some this filament in its advance to maturity has acquired hands and fingers, as in mankind.,” Darwin wrote (1801, p. 506). “In others it has acquired claws or talons, as in tygers and eagles. In others, toes with an intervening web, or membrane, as in seals and geese.” How can changes to a species come about, particularly changes that make an organism better suited to their environment by making them more complex? This is a major question for any evolutionary view of life. We would never expect pieces of metal to spontaneously come together to form a well-functioning complex system such as a watch. We would not even expect a damaged watch to spontaneously start working again. So how could organisms change from simple filaments to complex vertebrates? Darwin saw the many aspects of the world improving slowly as an unfolding of God’s plan. Society, geology, and even the cosmos progressed not because God regularly interfered, but because God had set up the laws of nature so as to result in constant improvement: Thus it would appear, that all nature exists in a state of perpetual improvement by laws impressed on the atoms of matter by the great CAUSE OF CAUSES; and that the world may still be in its infancy, and continue to improve FOR EVER AND EVER. (Darwin 1818, volume I, p. 437) [18.191.176.66] Project...

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