Review: The Selfish Genius

People love a good argument with Richard Dawkins. So many people are so desperately seeking reassurance that he is wrong, and book shop shelves groan under the output of writers who are happy to provide that reassurance, in big words and glossy covers, with referenciness aplenty and a friendly review from an Oxbridge theologian. Dawkins calls them his fleas: the hastily bashed out "Dawkins Delusions" and "God Solutions" that claim to refute Dawkins' writings on God, while presenting the same old pitiful arguments for His existence. Parasites on his name, contributing nothing, and not even worth the effort to crush.

Into this environment steps The Selfish Genius, in which Fern Elsdon-Baker sets out to explain why Richard Dawkins is wrong on almost everything he has ever written about. Elsdon-Baker is not a conservative preacher or obscure amateur theologian trying to convince us of God's greatness, though. She's a historian of science who, though she can't keep herself from commenting on Dawkins' religious work, is interesting for spending three quarters of her book arguing that Dawkins has his history of science wrong, his philosophy of science wrong, and, uniquely for the current plague of anti-Dawkins books, his science wrong.

Elsdon-Baker was the guest at the Royal Institution's October Cafe Scientifique, and I and some other curious biology nerds went along -- without having read the book -- to find out whether this flea had a bite. The jaws moved. The jaws moved a lot. But the teeth are missing. To convey the full humiliating extent of this book's failure to break flesh is going to take a little bit of history of evolutionary biology, and some fascinating and exciting contemporary molecular biology. Biology nerds can skip the history, but should be amused by the science.

 

A brief history of evolution

For the purpose of brevity this will to some extent be what Elsdon-Baker scoffs at as the "Whiggish" version of the history of evolutionary biology -- the victor's skewed tale. This is because I just can't get over that inexplicable bias that we science types have towards those scientific claims that turned out to actually reflect the way the world works. Specifically, what we are interested in here is the history of the proposed mechanisms of evolution.

Briefly: Darwin (and Wallace) proposed in 1858 that evolution could occur by a process of natural selection: in populations, some hereditary traits vary, that variation affects individuals' survival and reproduction rates, and therefore variations will be "selected" for or against according their effect on those rates. Darwin was, however, ignorant of the mechanisms of heredity. Some proposed mechanisms of heredity at the time, including those championed by Lamarck and Darwin, allowed for the "inheritance of acquired characteristics": events during an individual's lifetime could affect the hereditary material and thus the characteristics of future generations also. In 1868, Darwin developed his Pangenesis hypothesis for the mechanism of heredity, in which information about all of the characteristics of the body flows to the reproductive organs to be incorporated into the heredity material. People usually neglect to mention Pangenesis when discussing Darwin's greatness. Not because it wasn't a very clever idea. Simply, it was wrong. Bad luck on that one, Chaz.

Inheritance of acquired characteristics was never demonstrated, and it suffered a series of blows, eventually fatal, first from the rediscovery of Mendel's of laws of inheritance, and then from 20th century advances in physiology and molecular biology. Mendel had discovered the basics of the actual mechanisms of heredity: genetics. He observed that inheritance had a particulate nature, and followed a mathematical pattern that ruled out the inheritance of acquired characteristics. Later, the heredity material was determined to be DNA, and it was shown that, in complex multicellular organisms, the reproductive organs guard a small population of special cells -- the germ cells -- which remain isolated from the rest of the body, unable to receive any information about the current state of the body's characteristics with which to feed back into DNA. Inheritance of aquired characteristics was left for dead, and evolutionary biology united with genetics and molecular biology to focus on natural selection acting on random mutation, in the "neo-Darwinian modern synthesis".

In his first popularisation of science, in 1976's The Selfish Gene, Dawkins explained some of the mid-20th century's developments in evolutionary biology -- the "gene-centric" picture of evolution, which focuses on the gene as the unit of inheritance on which evolutionary processes act, and which defines evolution as "a change in allele (variants of a gene) frequencies in a gene pool over time." Dawkins' particular spin on the gene-centric view has received some legitimate criticism -- for dismissing the importance of the process of genetic drift, for example. But the gene-centric view itself -- the "change in allele frequencies" definition -- remains standing as a standard definition of evolution.

Where did Dawkins get it all wrong?

Elsdon-Baker cites a number of impressive sounding bits of research -- usually with a reference to "an article in New Scientist" -- which she believes, or has been told, prove problematic for Dawkins and the "selfish gene". (Interestingly, she doesn't cite the likes of genetic drift amongst them.) The challenges to Dawkins are:

• Horizontal gene transfer
• Inheritance of immune response
• Epigenetics
• Evo-devo

Oh my. According to Elsdon-Baker, these cutting edge fields of research are the downfall not just of the gene-centric view, but of neo-Darwinism in general. They are the four horsemen of the neo-Lamarckian revolution. Horizontal gene transfer (HGT), she says, undermines the concept of the "immortal replicater" that is so vital for the "selfish gene". (No, please, stop laughing now. Yes, it is so very obvious that HGT is not a problem for the gene-centric view of evolution that I don't intend to discuss it. If you think it needs explaining, I will happily give a patronisingly basic account.) Inheritance of immune response... well, Dawkins had already responded to this by the time of The Extended Phenotype in the 1980s. The last two horsemen though -- they look like impressive new discoveries that might revolutionise evolution, right?

Elsdon-Baker certainly thinks epigenetics is a "threat to the citadel": "...epigenetics may be showing how DNA may be bypassed altogether, enabling traits to be passed on 'epi-genetically' -- that is, outside the genes. If this is the case, then the gene-centric view might start to look rather outdated." (p.119) "Mays" and "mights" and "ifs" and "coulds": what is epigenetics, and how might it be a threat to the gene-centric view?

What is "epigenetics"?

The word "epigenetics" has been used to mean several things over the years. Its definitions have been so uselessly broad as to cover the entirety of developmental biology and great swathes of molecular biology. Elsdon-Baker defines it on p.119 as, "how genes are 'expressed' -- that is, just what effect the genes have on the organism." This is just the first of many absurd sentences that occur on this and the following pages. Observant readers will already have noticed that "how genes are expressed" and "what effect genes have on an organism" are not statements that can be concatenated with a casual "that is". The two statements do not even come close to meaning the same things. You'd have thought that the "how" and the "what" might have given that one away a bit.

Biologists, meanwhile, will have spotted that we already have perfectly good terminology for both things ("gene expression" and "developmental biology"), and will hopefully also have noticed that even those uselessly broad definitions of "epigenetics" that are actually genuinely used do not include, "what effect genes have on the organism." The word has never been defined that way. It is not what "epigenetics" means. Adrian Bird has made several attempts at defining epigenetics, including, "a useful word if you don't know what's going on."^[1] It seems that "epigenetics" is a useful word if you don't know any biology, but want to sound impressively up-to-date to the lay reader.

Before fully reading the book, I tried to challenge Elsdon-Baker on exactly what she meant by "epigenetics", and why it was a problem for neo-Darwinism. She was unable to tell me, but (despite my not having told her my own preferred definition), she did manage to accuse me of having "a very narrow definition of the word." (her emphasis)

In 2007 both Cell and Nature set out to pin down exactly what "epigenetics" means in modern science. To give it some clarity and precision, if you like. To take a uselessly broad term and make it "narrow", if you prefer. Adrian Bird looked at past and present definitions in Nature:^[2]

• There is Conrad Waddington's 1957 definition: "how genotypes give rise to phenotypes during development." We already have a good and universally used term for that field though: "developmental biology." This definition of "epigenetics" simply isn't used by biologists.
• There is a very widely used modern definition: "the study of mitotically [accross generations of cells within the individual] and/or meiotically [from parent to child] heritable changes in gene function that cannot be explained by changes in DNA sequence."
• And Bird's own refinement of the above: "the structural adaptation of chromosomal regions so as to register, signal or perpetuate altered activity states." That is, a mechanism for preserving gene expression patterns over multiple cellular generations (usually known by the more specific term "chromatin remodelling", but also increasingly what is meant when people use the term "epigenetics".)

And Goldberg et al did the same in Cell:^[3]

• "Historically, the word epigenetics was used to describe events that could not be explained by genetic principles." Events being inheritance events (at the scale of generations of cells).
• "The branch of biology which studies the causal interactions between genes and their products, which bring the phenotype into being." That is, developmental biology.
• The authors go on to explain chromatin remodelling as a major example of what we mean by "epigenetics" these days.

So "epigenetics" has in the past been concerned with developmental biology and with inheritance, and in modern times its definition has begun to be reigned in to specifically refer to the molecular mechanisms of perpetuating gene expression over multiple cellular generations. This latter version of "epigenetics" is of course of great relevance to both developmental biology and inheritance. But it is only a small detail of those wider fields. Elsdon-Baker seems to have overlooked this subtlety.

So Elsdon-Baker is obviously somewhat confused about the definition of "epigenetics", but, despite the constant mixing of definitions, it becomes clear to the reader (even if not to the author) that it is the latter more modern definitions that she thinks vindicates Lamarck (and Darwin) on the inheritance of acquired characteristics. This "epigenetics" is a collection of phenomena relating to the stable inheritance of gene expression states ("on", "off", and a few subtleties between) when cells proliferate during development. It is often thought of as a "memory", allowing cells to remember where in the body they are, and what function it is they are supposed to perform. This "epigenetics" is not a mysterious or revolutionary new force: its molecular mechanisms -- the processes of chromatin remodelling -- are well documented, and thoroughly reconciled with the orthodoxy.

Where's the revolution?

Chromatin remodelling and the inheritance of gene expression states are best known to us from developmental biology, where the phenomena are exciting but orthodox details (and where it comes as little surprise to anybody that cells have a mechanism for remembering where they are in the body and what it is they are supposed to be doing). But one discovery that has excited people in recent years is that some of these processes can also occur in the germ-line, meaning that some gene expression states could potentially be set in the parent and maintained in the child (the "meiotic" inheritance mentioned above). And some fascinating studies appear to have observed just this: causative correlations between environmental conditions in one generation, and the characteristics of their descendants. The most oft example is an apparent correlation between grandparental malnutrition during the war and a grandchild's predisposition to diabetes. Elsdon-Baker believes that this is neo-Lamarckian "inheritance of acquired characteristics" that just doesn't fit into the gene-centric neo-Darwinian paradigm.

She is wrong. Let me explain the basics of how chromatin remodelling works -- how "structural adaptation of chromosomal regions" leads to "altered gene activity states". Chromosomes are, of course, the structures which our DNA is packaged into. The long, fragile, and vulnerable DNA molecules in our cells are arranged into these structures by chromatin proteins. The DNA is wound around strings of these proteins, both for protection and as a scaffold to aid the regulation of gene expression. In cells, messages are constantly flowing, bringing status updates on the cell's environment and relaying signals from outside the cell (such as those produced by hormones, pathogens, drugs, and so on). These messages usually take the form of specific proteins, and they work by binding to the cell's DNA and initiating processes that alter the structure of chromosomal regions and the patterns of gene expression. The chromatin, the signals, and all of the regulators and mechanisms of gene expression are enzymes -- proteins -- products of genes, refined by natural selection.

During cell division, either within the body, or in the production of sex cells, the DNA must be stripped of chromatin so that the machinery of DNA replication may access it. However, little chemical tags on the DNA keep note of its intended structure ("DNA methylation"), and that structure is then reproduced in the daughter cells, and thus enabling "heritable changes in gene expression patterns". These tags, you might have guessed, are put there by enzymes: products of genes, refined by natural selection.

In the case of the wartime-malnutrition effect, then, the likely mechanism involves genes for detecting, conveying and responding to environmental conditions, genes for chromatin remodelling, and genes for DNA methylation, leaving heritable notes attached to genes relating to diabetes risk (e.g. the blood sugar monitoring system).

Chromatin remodelling is a fascinating, albeit not entirely unforeseen (after all, it is obvious enough for decades that expression of genes must be controlled and regulated somehow) detail of molecular biology. But it is itself entirely the product of genes, and of orthodox gene-centric neo-Darwinian evolution. If it says anything at all about the ideas of The Selfish Gene and The Extended Phenotype, it is that they were right: that it makes more sense to think of evolution in terms of the gene than of the individual, and that to ensure their survival, genes refined by natural selection reach beyond the vehicle that they happen to find themselves in.

The epigenetics that Elsdon-Baker cites as a revolution is not Lamarckian or "neo-Lamarckian". As a set of processes, chromatin remodelling is fascinating and complex, but no different to the countless other fascinating and complex molecular processes that make up the biological cell. As a phenomenon, epigenetics is fascinating not because it shows evolution without genes, but because it shows how how far genes reach, and how evolution evolves.

A science communication disaster

At the Cafe Scientifique, before I had read the book, I was already far from satisfied with Elsdon-Baker's claim that epigenetics is a problem for the gene-centric view of evolution. I asked her to elaborate on that question, how might it be a threat?

There was a little backtracking and some evasive handwaving; an admission that she didn't really know much about the science of epigenetics. She explained that epigenetics is just one example, a demonstration of Dawkins's ignorance of the subtleties and ambiguities of biology as revealed since The Selfish Gene. "If we don't communicate the subtleties of epigenetic inheritance," she said, "we risk a science communication disaster." This is the ultimate thesis of The Selfish Genius: that Dawkins's fame and the corresponding intransigence of the gene-centric view as the reigning paradigm in evolutionary biology are holding the field back and keeping the public in the dark about revolutionary advances that Dawkins just does not understand; that this "constrains thought and the communication of key ideas." She wants to show that you don't have to be a creationist to reject Dawkins's scientific writings.

Elsdon-Baker explains Dawkins's ignorance of the subtleties of biology on page 226, in The sword of rhetoric: "Evolutionary biology encompasses a very large number of research avenues. Dawkins is obviously slightly biased towards his previous field -- ethology -- and it is understandable that he should be on shakier ground with microbiology." This sentence stood out to me because, on p.121, she had said, "Microbiologists are now tentatively embarking on a Human Epigenome Project." Oh. Wow. Dawkins might be on shaky ground when it comes to microbiology, but at least he knows what microbiology is. (Hint: microbiologists study microbes; humans are not microbes.)

This is not an unfortunate but isolated typographical error. The book is littered with the most basic factual mistakes, from a confusion of gene mapping and genome sequencing in the introduction, to the bizarre claim that horizontal gene transfer is "neo-Lamarckian" in the conclusion. If Dawkins is on shaky ground when he comments on "microbiology", Elsdon-Baker is lost at sea. Never mind the subtleties and ambiguities, Elsdon-Baker is fundamentally, thoroughly, and humiliatingly wrong about almost every bit of science that she cites as evidence for her thesis. She fails to understand the science that she criticises and she fails to understand the science that she cites in her favour, making embarrassing mistakes along the way, and at every step failing to pick up on the genuine subtleties of the mechanisms of evolution. By her own criteria, this is one great big science communication disaster. A trainwreck.

Is The Selfish Genius just another flea -- a cheap, lazily researched and hastily bashed out book cashing in on its subject's fame? That conclusion would certainly reflect better on its author than that she really believes it to be cogent and serious scholarship.

References

1. ^  "Language: Disputed definitions", Nature 455, 1023-1028
2. ^  Nature 447, 396-398 (24 May 2007) doi link
3. ^  Cell 128, 635-638 (23 February 2007) doi link