The primary divisions of life: a phylogenomic approach employing composition-heterogeneous methods

Abstract

The three-domains tree, which depicts eukaryotes and archaebacteria as monophyletic sister groups, is the dominant model for early eukaryotic evolution. By contrast, the 'eocyte hypothesis', where eukaryotes are proposed to have originated from within the archaebacteria as sister to the Crenarchaeota (also called the eocytes), has been largely neglected in the literature. We have investigated support for these two competing hypotheses from molecular sequence data using methods that attempt to accommodate the across-site compositional heterogeneity and across-tree compositional and rate matrix heterogeneity that are manifest features of these data. When ribosomal RNA genes were analysed using standard methods that do not adequately model these kinds of heterogeneity, the three-domains tree was supported. However, this support was eroded or lost when composition-heterogeneous models were used, with concomitant increase in support for the eocyte tree for eukaryotic origins. Analysis of combined amino acid sequences from 41 protein-coding genes supported the eocyte tree, whether or not composition-heterogeneous models were used. The possible effects of substitutional saturation of our data were examined using simulation; these results suggested that saturation is delayed by among-site rate variation in the sequences, and that phylogenetic signal for ancient relationships is plausibly present in these data.

An archaeal origin of eukaryotes supports only two primary domains of life

“…The earliest fossils identified as eukaryotic appeared by about 1.8 billion years ago 20 ; over this enormous span of time, the accumulation of multiple substitutions in DNA and protein sequences might have erased any signal that would allow the relationship between archaeal and eukaryotic core genes to be established 21 . However, more recent simulations and empirical studies suggest that there are reasons to be cautiously optimistic that this is not the case: functional constraints vary across real DNA and protein sequences so that sites evolve at different rates [22][23][24][25] . Fast-evolving sites are indeed…”

“…The earliest fossils identified as eukaryotic appeared by about 1.8 billion years ago 20 ; over this enormous span of time, the accumulation of multiple substitutions in DNA and protein sequences might have erased any signal that would allow the relationship between archaeal and eukaryotic core genes to be established 21 . However, more recent simulations and empirical studies suggest that there are reasons to be cautiously optimistic that this is not the case: functional constraints vary across real DNA and protein sequences so that sites evolve at different rates [22][23][24][25] a, The rooted three-domains tree 14 depicts cellular life divided into three major monophyletic groups or domains: the Bacteria, Archaea and Eukaryota-the latter representing the host lineage, sometimes also called the nuclear or nucleo-cytoplasmic lineage 5 , that acquired the mitochondrial endosymbiont. In this tree the Archaea and Eukaryota are most closely related to each other because they share a common ancestor that is not shared with Bacteria.…”

“…b, The rooted eocyte tree recovers the host-cell lineage nested within the quickly saturated but the slowest sites can still retain useful phylogenetic information, explaining why we are able to align some genes over the entire tree of life. Analyses of molecular sequences might therefore be able to distinguish between the alternative hypotheses for eukaryotic core gene origins, but the phylogenetic methods used and the types of data analysed are likely to be of critical importance in attempts to recover any historical signal [22][23][24][25][26] . The problems associated with phylogenetic reconstruction come into particularly sharp focus when comparing support for the three-domains and eocyte trees.…”

“…These models seem to fit molecular sequence data much better than simpler models and this may make them less susceptible to LBA and other artefacts of model mis-specification 25 . Although relatively few analyses of the core gene set have used these models so far, all of them have recovered the eocyte tree, rather than the three-domains tree 12,22,[47][48][49] .…”

Evolutionary origin of a streamlined marine bacterioplankton lineage

“…This recoding scheme has been used to improve topological estimation in the presence of compositional heterogeneity in a number of phylogenomic studies (Cox et al, 2008;Foster et al, 2009;Nesnidal et al, 2010), including a recent study of the evolutionary placement of the SAR11 clade (Rodríguez-Ezpeleta and Embley, 2012). The Dayhoff-recoded concatenated datasets of the 52 protein sequences (the 28 homogeneous and the 24 heterogeneous ribosomal proteins) were analyzed using multiple configurations of the NDCH (node-discrete composition heterogeneity) and NDRH (node-discrete rate matrix heterogeneity) models, general time reversible (GTR) substitution matrix plus four Gamma-distributed rate categories, and employing the polytomy prior (Lewis et al, 2005).…”