Rooting the tree of life: the phylogenetic jury is still out

Abstract

One contribution of 17 to a theme issue 'Eukaryotic origins: progress and challenges'. This article aims to shed light on difficulties in rooting the tree of life (ToL) and to explore the (sociological) reasons underlying the limited interest in accurately addressing this fundamental issue. First, we briefly review the difficulties plaguing phylogenetic inference and the ways to improve the modelling of the substitution process, which is highly heterogeneous, both across sites and over time. We further observe that enriched taxon samplings, better gene samplings and clever data removal strategies have led to numerous revisions of the ToL, and that these improved shallow phylogenies nearly always relocate simple organisms higher in the ToL provided that longbranch attraction artefacts are kept at bay. Then, we note that, despite the flood of genomic data available since 2000, there has been a surprisingly low interest in inferring the root of the ToL. Furthermore, the rare studies dealing with this question were almost always based on methods dating from the 1990s that have been shown to be inaccurate for much more shallow issues! This leads us to argue that the current consensus about a bacterial root for the ToL can be traced back to the prejudice of Aristotle's Great Chain of Beings, in which simple organisms are ancestors of more complex life forms. Finally, we demonstrate that even the best models cannot yet handle the complexity of the evolutionary process encountered both at shallow depth, when the outgroup is too distant, and at the level of the inter-domain relationships. Altogether, we conclude that the commonly accepted bacterial root is still unproven and that the root of the ToL should be revisited using phylogenomic supermatrices to ensure that new evidence for eukaryogenesis, such as the recently described Lokiarcheota, is interpreted in a sound phylogenetic framework.

Changing ideas about eukaryotic origins

“…Gouy et al [80] tackle the question of what came first from a methodological perspective, questioning whether alternatives to the bacterial root depicted in universal trees (figure 1) can really be rejected, given the limitations of the models used to recover it [69][70][71]. They suggest that the use of better models and more careful attention to the properties of data are needed to re-evaluate the root position, and we firmly agree that this is urgently needed.…”

Arguments Reinforcing the Three-Domain View of Diversified Cellular Life

“…Instead, Bacteria-like eukaryotic genes can alternatively be explained by a combination of (i) endosymbiosis in a protoeukaryotic ancestor (i.e., not an archaeon), (ii) recent HGTs between bacterial and eukaryotic species, and/or (iii) Bacteria-Eukarya sisterhood in an alternative topology of the 3D ToL [28, 67, 68], without the need to invoke the AAS. It is important to note that, despite several concerns and the use of methods that do not root ToLs (reviewed in [29]), the early origin of Bacteria is taken by default or as a fact under AAS and corresponding phylogenetic trees are rooted using bacterial outgroup sequences. This rooting is ad hoc and could be problematic because it ignores a large body of work challenging the “traditional” bacterial rooting of the ToL [28, 30].…”

“…However, the presence of distant outgroups (e.g., bacterial ribosomal proteins that are quite divergent from archaeal-eukaryotic counterparts but are used to root the ToLs) and fast-evolving species (e.g., Nanoarchaeota [32] and Methanopyrus kandleri [33]) in datasets can make even these sophisticated methods prone to LBA, as shown by recent simulations [29] (see also [34]). Moreover, a concatenated (i.e., supermatrix) approach to phylogenetics, as applied by Spang et al [1] to support AAS, could be problematic especially when member genes have independent evolutionary histories.…”

Genomic data do not support comb jellies as the sister group to all other animals

“…Outgroup selection (the species used to root the tree) can also strongly affect phylogenetic results (13,25,26). In particular, the inclusion of outgroups very distant from the ingroup can cause reconstruction artifacts by attracting fast-evolving (long-branched) ingroup species toward the root (25,(27)(28)(29)(30)(31).…”