The deep(er) roots of Eukaryotes and Akaryotes

Abstract

Background: Locating the root node of the “tree of life” (ToL) is one of the hardest problems in phylogenetics. The root-node or the universal common ancestor (UCA) divides descendants into organismal domains. Two notable variants of the two-domains ToL (2D-ToL) have gained support recently. One 2D-ToL posits that eukaryotes (organisms with nuclei) and akaryotes (organisms without nuclei) are sister clades that diverged from the UCA and that Asgard archaea are sister to other archaea, whereas the other proposes that eukaryotes emerged within archaea and places Asgard archaea sister to eukaryotes. Williams et al. (Nature Ecol. Evol. 4: 138–147; 2020) re-evaluated the data and methods that support the competing two-domains proposals and concluded that eukaryotes are the closest relatives of Asgard archaea. Critique: We argue that important aspects of estimating evolutionary relatedness and assessing phylogenetic signal in empirical data were overlooked. We focus on phylogenetic character reconstructions necessary to describe the UCA or its closest descendants in the absence of reliable fossils. It is well known that different character types present different perspectives on evolutionary history that relate to different phylogenetic depths. Which 2D-ToL is better supported depends on which kind of molecular features – protein-domains or their component amino acids – are better for resolving common ancestors at the roots of clades. In practice, this involves reconstructing character compositions of the ancestral nodes all the way back to the UCA. We believe the criticisms of 2D-ToL focus on superficial aspects of the data and reflects common misunderstandings of phylogenetic reconstructions using protein domains (folds).   Clarifications: Models of protein domain evolution support more reliable phylogenetic reconstructions. In contrast, even the best available amino acid substitution models fail to resolve the archaeal radiation, despite employing thousands of genes. Therefore, the primary domains Eukaryotes and Akaryotes are better supported in a 2D-ToL.