"Darwin Never Proved Natural Selection is the Driving Force of Evolution- Because It Isn't"

Dan Graur brought our attention to an interview of evolutionary biologist Masatoshi Nei published in Discover Magazine.

Mutation, Not Natural Selection, Drives Evolution

In the interview, Nei discussed his theory of mutation-driven evolution. We wanted to learn more and found a number of useful online resources. (The least informative of those is Facebook. Discover Magazine posted a link to the interview there and got a number of ‘popular’ responses. It is safe to say that judging science based on facebook ‘likes’ is not a good idea.)

Nei explained his theory in a PNAS paper published in 2007.

The new mutation theory of phenotypic evolution

Recent studies of developmental biology have shown that the genes controlling phenotypic characters expressed in the early stage of development are highly conserved and that recent evolutionary changes have occurred primarily in the characters expressed in later stages of development. Even the genes controlling the latter characters are generally conserved, but there is a large component of neutral or nearly neutral genetic variation within and between closely related species. Phenotypic evolution occurs primarily by mutation of genes that interact with one another in the developmental process. The enormous amount of phenotypic diversity among different phyla or classes of organisms is a product of accumulation of novel mutations and their conservation that have facilitated adaptation to different environments. Novel mutations may be incorporated into the genome by natural selection (elimination of preexisting genotypes) or by random processes such as genetic and genomic drift. However, once the mutations are incorporated into the genome, they may generate developmental constraints that will affect the future direction of phenotypic evolution. It appears that the driving force of phenotypic evolution is mutation, and natural selection is of secondary importance.

What is going on? Here is the basic idea. In the accepted version of evolutionary theory (modern synthesis), the process of generating the variations is random and isotropic, whereas the ‘natural selection’ plays the primary role in selecting traits. In Nei’s model, the variations caused by mutations are not phenotypically random, but lead to directional jumps (‘constraint-breaking mutations’). Following paper explains the difference more nicely.

The Changing Face of Evolutionary Thinking

Are the products of evolution better explained by selection or by mutation? What one means by explained by mutation needs to be fleshed out, because not even the most dedicated proponent of a selectionist model of evolution will deny that mutations are necessary for evolutionary change. Also, it is not always easy to understand the arguments in Nei s book, because in some places Nei asserts that mutation is necessary to explain some kind of phenomenon. But it is not clear how this assertion is different from the generally accepted idea that mutations have to occur for selection to effect change. This reviewer only came to fully appreciate the force of Nei s argument until Chapter 9, which is the synthesis of his thinking based on the historical review and the reviews of empirical evidence from molecular evolution to which the previous eight chapters are dedicated. **As far as I can see, the core idea in Nei s book, to which evolutionary biologists need to pay attention, is constraint-breaking mutations.

In the classical selection-based model of evolution, genetic variation is assumed to be abundant and supplied by mutations with little directional bias.** This idea is supported by genetic data on the heritability of quantitative characters like wing length and body size. For these characters, it is plausible that natural selection explains the kind and direction of evolutionary change, such as the latitudinal variation of body size in mammals. This is plausible because of the abundance of genetic variation available for these traits in outbred populations. The alternative view, applicable to characters other than body size or wing length, is that patterns of evolutionary change can either be enabled or directed by the mutational process itself and thus properly be explained by mutation rather than natural selection. What it means to say is explained by mutation can be specified as meaning explained by the specific mutational mechanisms involved in specific cases, rather than by the abstract concept of mutation. To me three bodies of knowledge support the notion of mutation-driven evolution; most convincingly, namely, evolution of large-scale genomic features as explained by Michale Lynch s model of genome evolution, experimental studies of protein function evolution, and studies on the evolution of development.

Briefly, Michael Lynch shows that large-scale patterns of genome evolution can, to a surprising extent, be explained by the interplay of random genetic drift and the molecular biases of mutational change. If this model turns out to be correct, at least in a substantial set of cases, we would have a broad swat of evolutionary phenomenology that is driven by mutation rather than selection.

A good discussion of the differences <a href=”http://sandwalk.blogspot.ca/2010/08/mutationism-myth-vi-back-to- future.html

“>can be found in sandwalk blog, where Arlin Stoltzfus presents mutationism through six blog posts.

The Mendelians allowed that evolutionary change could be initiated by an event of mutation, and they interpreted this to mean that mutation was (to an unknown degree) a source of initiative, discontinuity, creativity and direction in evolution. The MS represents a very deliberate rejection of this view, and proposes instead that evolution is a complex sorting out of available variation to achieve a new multi-locus equilibrium, literally by “shifting gene frequencies” in the “gene pool”. The rate of evolution, in this view, does not depend on mutation, which merely supplies the “gene pool” with variation; evolution is not shaped by mutation, which is the “ultimate” source of variation, but not the proximate source.

When I made this distinction at a 2007 symposium in honor of W. Ford Doolittle, Joe Felsenstein was in the audience and pointed out that, while Fisher may have looked at things in this way, Wright’s stochastic view took into account random events, like new mutations. It’s true that Wright’s “shifting balance” model assigns a prominent role to random genetic drift, while Fisher’s view was deterministic. However, these are just two different flavors of the same “shifting gene frequencies” paradigm: neither view incorporates new mutations. The absence of new mutations from Wright’s shifting balance process is apparent from the fact that Patrick Phillips (1996) extended it to include a new starting phase (“phase 0”) of “waiting for a compensatory mutation”.

The fact that contemporary evolutionary biologists, for the most part, don’t understand this aspect of their intellectual heritage is not evidence of a cover-up. Scientists don’t get much chance to learn history. The history that they absorb is mainly from stories that appear in scientific writings, like the Mutationism Myth and the Essentialism Story, stories that represent Synthesis Historiography (Amundsen, 2005), the discipline of telling history in ways that make things turn out right for the Modern Synthesis. Synthesis Historiography teaches us that “saltationism” (Mayr’s pejorative term for the Mendelian view) and other alternatives to neo-Darwinism are nonsensical, “doomed rivals”, supported only by “typologists”, creationists, vitalists and other crazies. That is, Synthesis Historiography teaches the TINA doctrine: There Is No Alternative.

As contemporary research drifts away from the “gene pool” theory and the Darwinian doctrines of the MS, each evolutionary biologist remains confident that, due to the TINA doctrine, his own view must be “neo-Darwinian”. In reality, alternatives are being explored with increasing vigor in molecular evolution, evo-devo, and evolutionary genetics.

A few folks today are in the reverse situation of being familiar with MS orthodoxy, but not with recent research. Dawkins (2007) stakes his critique of a book by “intelligent design” creationist Michael Behe entirely on his faith in the gene pool theory. Behe claims, in effect, that there was not sufficient time for all the mutations needed to account for evolution. Dawkins responds by attacking the premise that evolutionary rates depend on mutation rates:

“If correct, Behe’s calculations would at a stroke confound generations of mathematical geneticists, who have repeatedly shown that evolutionary rates are not limited by mutation. Single-handedly, Behe is taking on Ronald Fisher, Sewall Wright, J.B.S. Haldane, Theodosius Dobzhansky, Richard Lewontin, John Maynard Smith and hundreds of their talented co-workers and intellectual descendants. Notwithstanding the inconvenient existence of dogs, cabbages and pouter pigeons, the entire corpus of mathematical genetics, from 1930 to today, is flat wrong. Michael Behe, the disowned biochemist of Lehigh University, is the only one who has done his sums right. You think? The best way to find out is for Behe to submit a mathematical paper to The Journal of Theoretical Biology, say, or The American Naturalist, whose editors would send it to qualified referees.”

With his signature over-the-top rhetoric, Dawkins insists that “mathematical genetics” has proven that evolutionary rates are not limited by mutation. Allowing for some exaggeration, this is an accurate representation of MS orthodoxy ca. 1959, the approximate vintage of Dawkins’s views. If Mayr had been alive, he might have said the same thing.

Meanwhile, no one who has been active in evolutionary genetics research in the past 15 years would represent the current state of knowledge in this way. If you want to know what a contemporary researcher would say, take a look at the most recent issue of Evolution in which the article by Douglas Futuyma (famous for his evolution textbook) gives many examples of how evolutionists (including himself) repeated the doctrine that mutation does not “limit” evolution, but argues that we are no longer making this dubious assumption. Another example would be the piece by Ronny Woodruff and James Thompson (1998) that introduces their symposium volume on Mutation and Evolution.

Also, Nei published a graduate-student level book, now available from Amazon -

The purpose of this book is to present a new mechanistic theory of mutation- driven evolution based on recent advances in genomics and evolutionary developmental biology. The theory asserts, perhaps somewhat controversially, that the driving force behind evolution is mutation, with natural selection being of only secondary importance. The word ‘mutation’ is used to describe any kind of change in DNA such as nucleotide substitution, gene duplication/deletion, chromosomal change, and genome duplication. A brief history of the principal evolutionary theories (Darwinism, mutationism, neo- Darwinism, and neo-mutationism) that preceded the theory of mutation-driven evolution is also presented in the context of the last 150 years of research. However, the core of the book is concerned with recent studies of genomics and the molecular basis of phenotypic evolution, and their relevance to mutation- driven evolution. In contrast to neo-Darwinism, mutation-driven evolution is capable of explaining real examples of evolution such as the evolution of olfactory receptors, sex-determination in animals, and the general scheme of hybrid sterility. In this sense the theory proposed is more realistic than its predecessors, and gives a more logical explanation of various evolutionary events.

Mutation-Driven Evolution is suitable for graduate level students as well as professional researchers (both empiricists and theoreticians) in the fields of molecular evolution and population genetics. It assumes that the readers are acquainted with basic knowledge of genetics and molecular biology.

Here are technical-oriented papers to back the claims -

http://people.ibest.uidaho.edu/~celesteb/Phagerefs/Holly/ng1535.pdf

http://eebweb.arizona.edu/courses/ecol451_551/readings/coyne_orr_1989.pdf

http://www.joelvelasco.net/teaching/2890/coyneorr04-speciationch1.pdf