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.