Tal Dagan and William Martin
Institute of Botany, University of Düsseldorf, D-40225 Düsseldorf, Germany
author email corresponding author email
Genome Biology 2006, 7:118doi:10.1186/gb-2006-7-10-118
Subject areas: Evolution, Microbiology and parasitology, Genome studies
The electronic version of this article is the complete one and can be found online at: http://genomebiology.com/2006/7/10/118
Published: 1 November 2006
© 2006 BioMed Central Ltd
Genome Biology 2006, 7:118doi:10.1186/gb-2006-7-10-118
Subject areas: Evolution, Microbiology and parasitology, Genome studies
The electronic version of this article is the complete one and can be found online at: http://genomebiology.com/2006/7/10/118
Published: 1 November 2006
© 2006 BioMed Central Ltd
Abstract
Two significant evolutionary processes are fundamentally not tree-like in nature - lateral gene transfer among prokaryotes and endosymbiotic gene transfer (from organelles) among eukaryotes. To incorporate such processes into the bigger picture of early evolution, biologists need to depart from the preconceived notion that all genomes are related by a single bifurcating tree.
Opinion
Evolutionary biologists like to think in terms of trees. Since Darwin, biologists have envisaged phylogeny as a tree-like process of lineage splittings. But Darwin was not concerned with the evolution of microbes, where lateral gene transfer (LGT; a distinctly non-treelike process) is an important mechanism of natural variation, as prokaryotic genome sequences attest [1-4]. Evolutionary biologists are not debating whether LGT exists. But they are debating - and heatedly so - how much LGT actually goes on in evolution. Recent estimates of the proportion of prokaryotic genes that have been affected by LGT differ 30-fold, ranging from 2% [5] to 60% [6]. Biologists are also hotly debating how LGT should influence our approach to understanding genome evolution on the one hand, and our approach to the natural classification of all living things on the other. These debates erupt most acutely over the concept of a tree of life. Here we consider how LGT and endosymbiosis bear on contemporary views of microbial evolution, most of which stem from the days before genome sequences were available.
A tree of life?
When it comes to the concept of a tree of life, there are currently two main camps. One camp, which we shall call the positivists, says that there is a tree of life, that microbial genomes are, in the main, related by a series of bifurcations, and that when we have sifted out a presumably small amount of annoying chaff (LGT), the wheat (the tree) will be there and will still our hunger for a grand and natural system [7-10]. The other camp, which we will call the microbialists, says that LGT is just as natural among prokaryotes as is point mutation, and that furthermore, it has occurred throughout microbial history. This means that even were we to agree on a grand natural classification, the process of microbial evolution underlying it would be fundamentally undepictable as a single bifurcating tree, because a substantial component of the evolutionary process - LGT - is not tree-like to begin with [1,11,12].
A recent paper by Ciccarelli et al. [9] brings these two views head-to-head. It purports to weigh in heavily for the positivists, but in doing so it inadvertently provides some of the strongest support for the microbialist camp that has been published so far. A closer look reveals why. Ciccarelli et al. [9] report an automated procedure for identifying protein families that are universally distributed among all genomes, with pipeline alignment and tree building. Their routine looked for possible cases of LGT (detected as unusual tree topologies), excluded such proteins, and reiterated the procedure until the universe of proteins had been examined. This left them with 31 presumably orthologous protein sequences present in 191 genomes each, the alignments of which were concatenated to produce a data matrix with 8,089 sites (of which only 1,212 would have remained had gapped sites been excluded). A maximum likelihood tree was inferred from this matrix, motivating a brief discussion of some important events in life's history as inferred from that tree.
Fair enough, one might say, what is there to debate? Lots. Bearing in mind that an average prokaryotic proteome represents about 3,000 protein-coding genes, the 31-protein tree of life represents only about 1% of an average prokaryotic proteome and only 0.1% of a large eukaryotic proteome. Thus, the positivists can say that there is a tree of life after all: a bit skimpier than expected, but a tree nonetheless. But the microbialists, glaring at the same data, can say that the glass is only 1% full at best, and more than 99% empty! There might be a tree there, but it is not the tree of life, it is the 'tree of one percent of life'.
Looking at the issue openly, the finding that, on average, only 0.1% to 1% of each genome fits the metaphor of a tree of life overwhelmingly supports the central pillar of the microbialist argument that a single bifurcating tree is an insufficient model to describe the microbial evolutionary process. If throwing out all non-universally distributed genes and all suspected cases of LGT in our search for the tree of life leaves us with a tree of one percent, then we should probably abandon the tree as a working hypothesis. When chemists or physicists find that a given null hypothesis can account for only 1% of their data, they immediately start searching for a better hypothesis. Not so with microbial evolution, it seems, which is rather worrying. Could it be that many biologists have their heart set on finding a tree of life, regardless of what the data actually say?
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Gente, Árvore da Vida de 1%? Darwin, todo mundo pensou que você tinha ilustrado sua Árvore da Vida com todo o cuidado de um pesquisador meticuloso como você que levou uns 20 anos para publicar sua teoria para não chocar os pruridos da Igreja Anglicana, e agora ela não rende mais do que míseros 1% de evidência?
E a Nomenklatura científica tem a cara de pau de dizer que o fato, Fato, FATO da evolução é um fato científico tão comprovado como a lei da gravidade. A lei da gravidade é um fenômeno científico 100% comprovado, mas o que dizer de uma árvore da vida com apenas 1% de evidência? Eu, se ainda fosse darwinista, não usaria mais esta retórica ufanista e em descompasso com a verdade das evidências.
Fui, nem sei por que, pensando no pesadelo que a Nomenklatura científica vem tendo desde 1859: as hipóteses transformistas de Darwin (um Australopithecus afarensis se transformar em Antropólogo amazonense) não são corroboradas em um contexto de justificação teórica.
O fato, Fato, FATO da evolução é uma verdade científica aceita a priori: um mero axioma.
