Title: The phenotype of the last universal common ancestor and the evolution of complexity

Abstract: A fundamental concept in evolutionary theory is the last universal common ancestor (LUCA) from which all living organisms originated. While some authors have suggested a relatively complex LUCA it is still widely assumed that LUCA must have been a very simple cell and that life has subsequently increased in complexity through time. However, while current thought does tend towards a general increase in complexity through time in Eukaryotes, there is increasing evidence that bacteria and archaea have undergone considerable genome reduction during their evolution. This raises the surprising possibility that LUCA, as the ancestor of bacteria and archaea may have been a considerably complex cell. While hypotheses regarding the phenotype of LUCA do exist, all are founded on gene presence/absence. Yet, despite recent attempts to link genes and phenotypic traits in prokaryotes, it is still inherently difficult to predict phenotype based on the presence or absence of genes alone. In response to this, we used Bayesian phylogenetic comparative methods to predict ancestral traits. Testing for robustness to horizontal gene transfer (HGT) we inferred the phenotypic traits of LUCA using two robust published phylogenetic trees and a dataset of 3,128 bacterial and archaeal species.

Our results depict LUCA as a far more complex cell than has previously been proposed, challenging the evolutionary model of increased complexity through time in prokaryotes. Given current estimates for the emergence of LUCA we suggest that early life very rapidly evolved cellular complexity.