Beyond Selfish Genes

Nov 15, 04:32 AM

Current Headlines: By Pigliucci, Massimo

Richard Dawkins's classic book, The Selfish Gene (1976), presented to the public the astonishing idea that organisms are "lumbering robots" controlled in their actions by "selfish" pieces of DNA bent on ensuring dieir own reproduction, come what may. Dawkins's follow-up book, The Extended Phenotype (1982), attempted to meet some of die criticisms raised against The Selfish Gene, mosdy diat it presented far too simplistic a view of evolution, and that its tone and metaphors were too easily interpreted as fostering the myth of genetic determinism (despite Dawkins's denials over time that he subscribes to it). Yet the damage was done. Far more people read Dawkins's first book (which was aimed at the general public) than the second, more scholarly one. Moreover, although The Selfish Gene was largely a popularization of technical ideas by evolutionary biologists such as William Hamilton (Oxford University) and George Williams (Stony Brook University, New York), it began to be discussed in the literature as if it were a primary source, an unfortunate outcome both for Dawkins (who became a target for the sort of heavy criticism that is not usually aimed at popular books) and for the originators of the basic ideas themselves (who remained somewhat peripheral to the public discussion).

Be that as it may, it is time to lay the selfish gene metaphor to rest, or at least to seriously appreciate its strict limits. Dawkins's basic idea is that evolutionary biologists should adopt what he calls a "gene's eye view" of evolution, since the genes, not the organisms, species, or any other level of biological organization, are really the targets of natural selection and chief actors in the evolutionary drama. This shift in perspective, which followed the explosive success of molecular biology beginning with the discovery of the structure of DNA in 1953, was based on the simple idea that genes, not organisms, provide historical continuity since it is genes, not the traits of organisms, that are passed from one generation to the next. As Dawkins put it, evolution is about the "replicators" (the genes) though the latter's fate is mediated at each generation by the "interactors," i.e., the organisms that interact with the environment.

But a number of scientists and philosophers soon pointed out that things aren't quite that simple. One of the first criticisms leveled against the view of the centrality of the gene was a simple observation made by geneticist Richard Lewontin and philosopher Elliott Sober. They emphasized that genes are never found isolated inside organisms, they are parts of genomes, and genes have to interact (through their products-usually, but not always, proteins) with other genes. Based on this logic, it is easy to construct models showing that-at most-selection acts on an ensemble of genes (i.e., on genotypes), not on individual genes.

Dawkins responded with the interesting maneuver of treating every other gene as a part of "the environment" of any focal gene under study. While this in a sense rescues the selfish gene idea, it begins to show the clumsiness of the approach, because now the remainder of the genome behaves simultaneously as a set of replicators, a set of vehicles (because of other gene's interactions with the focal one), and part of the "environment."

Things got worse from that point on. Recent research by Mary Jane West-Eberhard (Smithsonian Institution) and others is helping to re- establish the classic Darwinian idea that selection acts (primarily) on organisms, not genes. Indeed, a phenomenon that had rarely been studied when The Selfish Gene came out, known as "phenotypic plasticity" (the ability of an organism to accommodate environmental variation by altering its own developmental trajectory) suggests that the first step in evolution may often be mediated by the phenotype, with genetic changes fallowing (as opposed to leading, as in the standard theory), eventually stabilizing whatever outcome is initially favored by natural selection.

An even broader challenge to the gene's eye view of things has been brought by the resurgence of the idea of group selection, which- in its naive version-was a primary target of some of Williams's original work that inspired Dawkins. Williams had convincingly shown that there is no such thing as selection for "the good of the species" (a still amazingly popular misreading of the theory of evolution). However, recent work spearheaded by David Sloan Wilson (Binghamton University, New York) and others has succeeded in outlining what realistic conditions can in fact yield group-level selection, and empirical research supporting some group-selective scenarios has begun to accumulate (this is particularly relevant to the understanding of human evolution, especially evolution mediated by cultural traits).

Finally, very recent evidence supporting the existence of an additional layer of heritable epi-genetic information (i.e., information that is not carried by the genes themselves) has even put in some doubt the sharpness of the original distinction between replicators and interactors, as pointed out by philosopher Paul Griffiths (University of Exeter, England) and biologist Eva Jablonka (Tel Aviv University), among others. All of this is greatly expanding our concept of what counts as hereditary material, to the point that biologists are seriously reconsidering what, if anything, genes really are.

As a result of these and other serious challenges, some biologists and philosophers of science have come to an understanding of evolution as a multilevel process, where natural selection can act directly on genes (there are truly selfish genetic elements that reproduce parasitically inside the genome itself), individual organisms (as in classical evolutionary theory), social groups within species, and possibly even groups of different species (known as clades). Some authors have suggested that genes may still retain a special role because whatever change happens at higher levels is bound to be reflected (however indirectly) in changes in gene frequencies. But this "bookkeeping" role of genes in evolutionary biology is a far cry from grand statements about their alleged causal centrality. Evolution is indeed a much more fascinating and complex process than we thought.

Massimo Pigliucci is professor of evolutionary biology and philosophy at Stony Brook University in New York, a fellow of the American Association for the Advancement of Science, and author of Denying Evolution: Creationism, Scientism and the Nature of Science. His essays can be found at www.rationallyspeaking.org.

Copyright The Committee for the Scientific Investigation of Claims of the Paranormal (SCICOP) Nov/Dec 2007

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