Search for a 'Tree of Life' in the thicket of the phylogenetic forest

Pere Puigbò,Yuri I Wolf,Eugene V Koonin

doi:10.1186/jbiol159

Pere Puigbò, Yuri I Wolf + Show 1 more

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https://doi.org/10.1186/jbiol159

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Abstract

BackgroundComparative genomics has revealed extensive horizontal gene transfer among prokaryotes, a development that is often considered to undermine the 'tree of life' concept. However, the possibility remains that a statistical central trend still exists in the phylogenetic 'forest of life'.ResultsA comprehensive comparative analysis of a 'forest' of 6,901 phylogenetic trees for prokaryotic genes revealed a consistent phylogenetic signal, particularly among 102 nearly universal trees, despite high levels of topological inconsistency, probably due to horizontal gene transfer. Horizontal transfers seemed to be distributed randomly and did not obscure the central trend. The nearly universal trees were topologically similar to numerous other trees. Thus, the nearly universal trees might reflect a significant central tendency, although they cannot represent the forest completely. However, topological consistency was seen mostly at shallow tree depths and abruptly dropped at the level of the radiation of archaeal and bacterial phyla, suggesting that early phases of evolution could be non-tree-like (Biological Big Bang). Simulations of evolution under compressed cladogenesis or Biological Big Bang yielded a better fit to the observed dependence between tree inconsistency and phylogenetic depth for the compressed cladogenesis model.ConclusionsHorizontal gene transfer is pervasive among prokaryotes: very few gene trees are fully consistent, making the original tree of life concept obsolete. A central trend that most probably represents vertical inheritance is discernible throughout the evolution of archaea and bacteria, although compressed cladogenesis complicates unambiguous resolution of the relationships between the major archaeal and bacterial clades.

Highlights

Comparative genomics has revealed extensive horizontal gene transfer among prokaryotes, a development that is often considered to undermine the ‘tree of life’ concept
For most of the analyses described below, we analyzed the nearly universal trees (NUTs) in parallel with the complete set of trees in the forest of life or else traced the position of the NUTs in the results of the global analysis; this approach does not amount to using the NUTs as an a priori standard against which to compare the rest of the trees
We further introduced the inconsistency score (IS), a measure of how representative the topology of the given tree is of the entire forest of life

Summary

Introduction

Comparative genomics has revealed extensive horizontal gene transfer among prokaryotes, a development that is often considered to undermine the ‘tree of life’ concept. Advances in comparative genomics revealed that different genes very often had distinct tree topologies and, that HGT seemed to be extremely common among prokaryotes (bacteria and archaea) [8,9,10,11,12,13,14,15,16,17], and could have been important in the evolution of eukaryotes, especially as a consequence of endosymbiotic events [18,19,20,21]. The nearly universal realization that HGT among prokaryotes is common and extensive, rather than rare and inconsequential, led to the idea of ‘uprooting’ the tree of life, a development that is often viewed as a paradigm shift in evolutionary biology [11,22,23]

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