The origin of eukaryotes is linked to the rooting of the Tree of Life... but the phylogenetic jury is still out!

The origin of the eukaryotes remains one of the most contentious puzzles in evolution. In the late 1970s, C. Woese discovered Archaea and put an end to the dichotomous view of Life (eukaryote vs prokaryote). Since Woese’s revolution, the Tree of Life (ToL) has been divided into three domains (Bacteria, Archaea and Eukaryota), yet with unclear relationships. Rooting the ToL then became a problem. Indeed, the question of the origin of eukaryotes is directly related to the location of this root, which also affects the nature of the Last Universal Common Ancestor (LUCA). Several scenarios might explain the origin of the eukaryotic cell: (a) the three domains have an independent origin and directly stemmed from the primordial soup; (b) the three domains stemmed from a simple LUCA, and their evolution proceeded by increasing complexity in eukaryotes; (c) the three domains stemmed from a complex LUCA, and their evolution proceeded by simplification in prokaryotes; (d) eukaryotes originated from a fusion event between an archaeon and a bacterium, the latter being the mitochondrion and their other properties evolving after this event; (e) eukaryotes originated from a fusion event between an archaeon and a bacterium, the result being a proto-eukaryote not yet equipped with a mitochondrion.
During the last 15 years, technical advances in phylogenetic methods have relocated many simple organisms higher in the ToL, which means that they are actually secondary simplified. However, even the best evolutionary models are not yet able to address difficult phylogenetic issues, whether at shallow depth or at deep evolutionary times. This raises a fundamental question: does simple always mean ancestral? For the time being, the commonly accepted bacterial root for the ToL (in scenario (b)) is still unproven, so that the current consensus 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. Indeed, during early evolution, there might have been many independently arising lineages, both before and along LUCA, none of them having left extant descendants. The major bottlenecks that occurred as a result of catastrophic events in Earth’s history (e.g., meteorite impacts or snowball Earth periods) might explain why we only have three domains of Life nowadays. Furthermore, extant lineages coalesce to a LUCA that was not necessarily simple and located at the base of the ToL. Instead, it probably lived much later and was more complex than generally acknowledged.