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

Abstract

Background: Comparative 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'.

Results: A 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.

Conclusions: Horizontal 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.