Evidence for a Syncytial Origin of Eukaryotes from Ancestral State Reconstruction

Abstract

Modern accounts of eukaryogenesis entail an endosymbiotic encounter between an archaeal host and a proteobacterial endosymbiont, with subsequent evolution giving rise to aunicell possessing a singlenucleus and mitochondria. Themononucleate state of the last eukaryotic common ancestor (LECA) is seldom, if ever, questioned, even though cells harboringmultiple (syncytia, coenocytes, and polykaryons) are surprisingly common across eukaryotic supergroups. Here, we present a survey of multinucleated forms. Ancestral character state reconstruction for representatives of 106 eukaryotic taxa using 16 different possible roots and supergroup sister relationships, indicate that LECA, in addition to beingmitochondriate, sexual, andmeiotic,wasmultinucleate. LECA exhibited closedmitosis,whichis therule formodernsyncytial forms, sheddinglightonthemechanics of its chromosomesegregation.Asimple mathematical model shows that within LECA s multinucleate cytosol, relationships among mitochondria and nuclei were neither one-to-one, norone-to-many, butmany-to-many,placingmitonuclear interactionsandcytonuclear compatibility at the evolutionary base of eukaryotic cell origin. Within a syncytium, individual nuclei and individual mitochondria function as the initial lower-level evolutionary units of selection, as opposed to individual cells, during eukaryogenesis. Nuclei within a syncytium rescue each other s lethalmutations, thereby postponing selection for viable nuclei and cytonuclear compatibility to the generation of spores, buffering transitional bottlenecks at eukaryogenesis. The prokaryote-to-eukaryote transition is traditionally thought to have left no intermediates, yet if eukaryogenesis proceeded via a syncytial common ancestor, intermediate formshave persisted to the present throughout the eukaryotic tree as syncytia but have so far gone unrecognized.