Wednesday, 24 August 2011

From Selfish Genes to Public Goods

Most people have heard of "The Selfish Gene" and many will know what it's about. For those that don't... in essence, it is about "genes" as the primary driving force of evolution. A "gene" in this context is a piece of DNA within some form of entity that replicates that DNA. The rules are simple: if that piece of DNA does anything to increase the chance of its future replication and persistence, it will spread. Usually, we perceive this as a "gene" having some positive beneficial effect on the organism to which it "belongs" (or, perhaps more accurately, within which it is carried and replicated). Life, as usual, is more complicated than that, however, and examples exist of "genes" that spread at the cost of their replicator host - viruses and transposable elements being two such examples.

The point is, though, the genes are "in it for themselves". Yes, they often form complex cooperatives - genomes - that build intricate organisms but only because the members of those cooperatives replicate more successfully in this fashion than going it alone. Natural Selection is not about the good of the species, or even the good of the individual, it is the good of The Selfish Gene.

As you can tell, I am a big fan of this gene's-eye view of evolution. It begs the question, though, if the units of evolution are genes, where does this leave organisms? Species? Even genomes? How does this marry with the standard "Tree of Life" (TOL) model of evolution, in which all species are gradually splitting and diverging over time, carrying their genes with them?

In their recent Biology Direct paper, The public goods hypothesis for the evolution of life on Earth, James McInerney et al. summarise the issue quite nicely. "Horizontal Gene Transfer" (HGT) - essentially the passing of genetic material from one organism to another, other than to offspring (and often a different species) - is widespread, especially in bacteria. So widespread, in fact, that the TOL hypothesis just does not hold up. Instead, we should take a economist-style view of genes as "public goods", with the evolution of Life on Earth as the product of sampling (and retention) of different genes over time, rather than a TOL pattern of bifurcation and divergence.

Of course, the story is a lot richer than that and builds on a body of other ideas. It is also not without criticism. I strongly encourage you to read the paper and the interesting discussion with reviewers that can be found at the end of the manuscript. Time will tell whether the Public Goods hypothesis really offers something more than TOL+HGT but it's definitely something worth considering.

So what does this mean for evolution? Does questioning the TOL put evolution in peril? Well, no. It is important to point out that the genes themselves are still evolving in a tree-like fashion. Molecular evolution and molecular phylogenetics is not substantially altered by this idea. What is altered is the way we interpret this molecular data in terms of trying to determine the relationship of "species", especially bacteria. This is nothing new - the "species" concept for bacteria has been dead for a long time, to be honest - but it potentially gives us some new tools and ideas with which to probe the Natural History of prokaryotic life with more clarity and insight than ever before.

And what about all the claims us evolutionary biologists make about the molecular evidence for evolution, and how we get remarkably consistent trees when looking at different genes from a set of animals? Was that all lies? Well, no. It is also important to point out that the problems with the TOL are largely restricted to bacteria, viruses and the like. For eukaryotes - e.g. plants, animals, fungi - the tree picture is still pretty solid. The authors themselves make a nice analogy with mechanics. Quantum Mechanics did not stop previous observations about Newtonian Mechanics being right, it just extended our understanding into realms where our old Newtonian understanding began to break down. I am not sure whether this idea represents such a game-changer but I do know that it's a exciting, if slightly head-wrecking, time to be a microbial geneticist.


  1. This sharing of genes may be telling us something important about the origin of life. Maybe life began everywhere with a single Giain like ecosystem level open metabolism. Bacteria might be the remnants of that primordial single mother earth original life form. From there chance segregation of groups of genes and selfish competition could have led to the TOL distribution of gene sets we see today.

  2. @jpacoeur: Yes, that's one of the things that appeals to me about the idea. Under the "Public Goods Hypothesis", there is a clear continuum between cellular and pre-cellular life. There is no need to invoke something special en route to the Last Universal Common Ancestor (LUCA) that suddenly switched life into a different mode of evolution by putting genes in bags. I think all these ideas about pre-membrane early life have been around for ages and it would not change the ideas about their origins and evolution (or the origin of the Universal Genetic Code etc.) but the extra continuity is pleasing. (As an aside, I am not sure what the "life form" is in the primordial ecosystem - I would probably go for the gene unit itself. The alternative wanders too close to "Gaia" nonsense for my tastes.)

  3. I am suggesting Gaia in geneless semi-living world. Imagine the thin layer of atmosphere and water around the earth taking energy from the sun and geothermal sources to drive oscillating carbon based chemical reactions involving basic metabolism (Gaia in a very physical sense). This could have become divided in puddles or some other units which could be variable. The first of these units that could convert it's neighbour to work like itself would then multiply by converting the other units. This might have involved DNA based genes as the physical seeding entities. The rest would be history. And yes this does beg the question of what exactly life is. Anyway,that's my best guess at what happened.

  4. @jparcoeur: "Gaia" in the sense of the Earth as a single, connected complex system: yes. "Gaia" in the sense of a single "self-regulating" life form: that makes me squirm. I suspect a lot of it largely comes down to semantics and "what is life"? (I don't think re-defining life to include a large complex system like the planet is useful. Phage, viruses and even transposable elements, yes. Planets, no.) But, yes, whether Gaia or not, the kind of process you describe seems to be the most likely way for life (as we currently understand it) and replicators to originate.


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