ScienceWeek

EVOLUTION: ON THE EVOLUTION OF BIOLOGICAL COMPLEXITY

The following points are made by Christoph Adami (Science 2006 312:61):

1) If an elaborate lock fits an equally elaborate key, we immediately sense the purpose of design: The key was crafted with the idea of the lock in mind. We would not entertain the possibility that the match is accidental. When we come upon such lock-and-key pairs in nature, it is natural to ask how these pairs could have evolved via Darwinian evolution. At first glance, it seems that the key can only evolve to fit the lock if the lock is already present, and the lock cannot evolve except in the presence of the key (because without the key, it does not open). New work [1] takes a closer look at this puzzle and discovers a different answer in the molecular evolution of hormone-receptor interactions.

2) Charles Darwin was fully aware of the problems that such lock-and-key systems -- should they exist in biology -- would present to his theory because the theory relies upon step-by-step changes to a trait. Building a lock-and-key system appears to require at least two changes to happen simultaneously. He famously remarked that "if it could be demonstrated that any complex organ existed which could not possibly have been formed by numerous successive slight modifications, my theory would absolutely break down" [2]. This concern has been seized upon by proponents of an "intelligent design" alternative to Darwinian evolution that proposes that complex systems -- like those that display lock-and-key complexity -- cannot evolve. The premise for the argument is that systems of a lock-and-key nature cannot evolve and are thus "irreducibly complex" [3], implying that only the lock-and-key combination, but not its parts, is complex. The argument continues that because such systems do exist in nature, and cannot have evolved, they must have been "designed".

3) Darwin already saw how such thorny issues could be resolved. He further explains in THE ORIGIN OF SPECIES that "if we look to an organ common to all the members of a large class in order to discover the early transitional grades through which the organ has passed, we should have to look to very ancient ancestral forms, long since become extinct." In other words, Darwin suspected that viewing only the extant complex forms will obscure the path of evolution, and present an incomplete picture. But while the fossil record has yielded many intermediate forms that suggest a continuous evolution of traits, it is too often incomplete, and does not allow us to retrace the molecular history of a gene. Reconstructing the complete evolutionary history of a complex genetically encoded function (albeit a "computational" one) was achieved recently [4], and it experimentally vindicated Darwin's idea that the target of natural selection constantly changes, so that the complex feature of today may share very little with the original function. But while such computational investigations can be very satisfying, they might not convince everybody. It is therefore gratifying that it is now possible to reconstruct the ancestral genes of an existing species so that, as Darwin urged us to do, we can "look exclusively to its lineal ancestors" to understand a gene's evolution.

4) Bridgham et al [1] address one of the central concepts of the intelligent design argument. They did not study just any gene, but precisely a system that looks irreducibly complex: a hormone-receptor pair that we can think of as a biological lock and key. In vertebrates, the regulation of many cellular processes is controlled by steroid-receptor interactions that are highly specific. For example, cortisol activates the glucocorticoid receptor to regulate metabolism, inflammation, and immunity. In contrast, the mineralocorticoid receptor is activated by aldosterone, and controls electrolyte homeostasis, among other effects. This specificity is important, because the activation of the glucocorticoid receptor by aldosterone, for example, would be highly detrimental. Phylogeny tells us that an ancestral corticoid receptor gave rise to the glucocorticoid receptor and the mineralocorticoid receptor in a gene-duplication event more than 450 million years ago. However, aldosterone evolved much later. Without aldosterone present, how could the mineralocorticoid receptor evolve to be activated by it? Doesn't the pair's specificity require the evolution of two traits at the same time, an event that appears highly unlikely? Bridgham et al [1] took Darwin's advice and followed the line of descent to the ancestral corticoid receptor. Modern phylogenetic methods make it possible to reconstruct such inferred sequences and study the properties of these molecules in the laboratory. What the authors find is a surprise: Not only is the ancestral corticoid receptor sensitive to cortisol as expected, it is also activated by 11-deoxycorticosterone (DOC) and aldosterone. Because aldosterone was not present at the time, this sensitivity must be a by-product of sensitivity to another steroid, a promiscuity that can be exploited by evolution [5].

References (abridged):

1. J. T. Bridgham, S. M. Carroll, J. W. Thornton, Science 312, 97 (2006)

2. C. Darwin, The Origin of Species (John Murray, London, ed. 6, 1872)

3. M. J. Behe, Darwin's Black Box: The Biochemical Challenge to Evolution (Free Press, New Jersey, 1994)

4. R. E. Lenski, C. Ofria, R. T. Pennock, C. Adami, Nature 423, 139 (2003)

5. A. Aharoni et al., Nat. Genet. 37, 73 (2004)

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