I recently attended two talks by Professor Ford Doolittle of Dalhousie University. Doolittle’s argument is about the validity of phylogenetic trees. For prokaryotes specifically, his claim is that trees do not map onto natural kinds. Or more starkly the idea that there is a tree of life is a hypothesis which has now shown to be incorrect for the majority of life on earth.
In his first talk, he began by discussing classification as a common and useful practice and mentioned a paper by Jared Diamond (this one I think) showing that zoological classification by tribal peoples can correspond with scientific classifications. This inter-subjectivity seems to confirm the existence of real phenotypic gaps, but these days we are wont to think of our modified Linnean hierarchical system as reflecting something else: descent with modification (to use Darwin’s term). Creatures assigned to one taxon cannot also be assigned to another and higher level taxa are inclusive of lower level taxa.
Doolittle’s core point is that the prevalence of horizontal gene transfer (HGT) means that descent with modification needn’t produce a branching structure so much as a reticulate one. Perhaps the best known example of HGT is one Doolittle has been pivotal in establishing as a biological fact: the invasion of early eukaryotes by alpha-proteobacteria giving rise to mitochondria, but many more examples are now well known and these are mediated in bacteria by the processes of transformation, transduction and conjugation (loosely these are the uptake of naked DNA, viral DNA transfer and plasmid exchange, respectively). The key point is that the larger the segment of time considered, the smaller the proportion of a bacterial genome that has not been subject to HGT. He provided data in support of this.
In his second talk Doolittle gave details of his own research in the field of metagenomics where the concept of a metagenome is significant. Gene-level phylogenies frequently contrast with organismal phylogenies demonstrating HGT and in his study systems he provided evidence in support of exchange between halophylic archaea and eubacteria (organisms in different domains of life) with the former transferring salt-tolerant genes to the latter and metabolic genes flowing the other way. He gave some reasons for thinking that HGT can be recurrent in structured environments and that significant rearrangement of functional units can take place over periods of decades: i.e., that bacterial macroevolution is reticulate.
Doolittle’s principle philosophical claim flowing from this, and made with Eric Baptiste in this paper, is that while evolutionary biology now admits of multiple evolutionary processes besides natural selection, it needs to adopt a similarly pluralistic stance about the patterns produced by these. He calls those who accept (even implicitly) the tree of life idea, pattern monists. And he cited S. J. Gould’s criticism of process monists: those who attribute all of life’s complexity to natural selection alone.
This made me think of (and ask) a question. In this blog I have previously defended a kind of monism by emphasising that I am monist with respect to adaptation not the origin of species or diversity in general. I think most evolutionists would accept that selection (natural or sexual) is the only process able to generate adaptive change (though the details of any particular adaptive walk may involve drift or recombination as a key component). In brief I have defended this notion by pointing to the need for some sort of discrimination (something not provided in Lamarck’s alternative evolutionary theory for example). So I asked if monism/pluralism disputes about pattern might similarly be resolved by an analogous change of focus. Is the tree concept valid for some lower level unit? Let’s call it an atom. He suggested I might be able to wriggle in that direction but that he was betting against monism at any level of organisation (at least in prokaryotes; one questioner raised the interesting point that sex in eukaryotes might be a way of regulating HGT to largely within-group transfers).
Now an obvious candidate for the atom of analysis mentioned is the gene, particularly when you consider that HGT is often demonstrated using discordance between organismal and gene-level phylogenetic trees. But the trees used here are still arguably only instrumental and homologous recombination between similar genomes (which might also be counted a form of HGT) may be seen to occur across functional genes. This forces our atom definition into a unit of zero recombination or more generally and accurately anything that selection or linkage maintains in linkage disequilibrium. Ultimately we are referring to the selfish genetic element concept a la Dawkins and Trivers and much of this seems unsurprising from a neo-Darwinian perspective (contra Doolittle’s claim that his thesis represents a radical departure and, even more provocatively, one required to create a creationism-resistant evolutionary biology – I take issue with this as there is already evidence enough for evolution and for the processes posited to explain it).
I think that the timescale matters and that during microevolution it is reasonable to describe a tree of selfish genes, which include hyper-motile elements such as integrons. At the organismal level these trees may move in and out of phase with each other as the coalitions we call organisms shift about, but we can still validly describe a tree of life at lower levels. At the macroevolutionary level beyond the population dynamics and lifetime of particular selfish genetic elements, I am not so sure and there may be parts of the genome that are evolutionarily modular at a different scale from others (how this relates to function is interesting). The problem is that the birth and death of these elements seems to invalidate any claim to a universal tree of life. Fine, but remember this has the possible and interesting connotation that there is no last universal common ancestor (LUCA; which is not a statement about a unitary origin of life – this is about backward coalescence and all chemistries not extant are excluded).
Where I think I depart from Doolittle (if I represent his claim fairly) is in his saying, in answer to a question, that even the genetic code has no last common ancestor (LCA). There is basically one genetic code so far known with a few minor variants and given the combinatorial architecture of the transcription and translation machinery this amounts to a vanishingly small segment of the possible code space. It therefore seems likely that common descent explains code identity across the natural world. There are two objections to this: 1. the code may be the only optimal code and we have it thanks to selection and 2. it may itself be modular and hence derived from multiple lineages. With respect to point 1 it is well known that the code is highly optimised but it is not perfect and a better code is known to exist in a distant point of code space. With respect to point 2, it is reasonable to suppose gradual recruitment of tRNAs and competition between alternatives, but it is hard to imagine the de novo assembly of these sets of tRNAs into independent but identical codes in separate lineages. Once derived that would seem to be it.
In summary each of the major transitions in evolution may have fashioned a new set of replicators and the tree of life familiar to us in the eukaryote world is approximately correct but we must acknowledge its roots among the prokaryotes are highly reticulate.