CELL-CYCLES, DIPLOKARYOSIS AND THE ARCHEZOAN ORIGIN OF SEX

Sex (i.e. meiosis, syngamy and nuclear fusion) first evolved in primit ively amitochondrial eukaryotes of the kingdom Archezoa. It is argued that meiosis is monophyletic and that it evolved before either cell or nuclear fusion, as a means for ploidy reduction. Meiosis may have beg un so as to correct accidental endopolyploidy and been perfected to al low regular asexual ploidy cycles. These could have allowed early arch ezoa to have the advantages both of large multigenomic phagotrophic ce lls and of periodic reductions to a haploid stage to facilitate the se lective elimination of harmful mutations. I suggest that one-step meio ses, if they genuinely exist in protists, are all secondarily derived from conventional two-step meiosis and are not the ancestral condition . The origin of meiosis required changes in the coupling between DNA r eplication and nuclear division. Consideration of these cell cycle con trols suggests that two-step meiosis could have originated by a single mutation that delayed sister-centromere splitting and thereby simulta neously made it possible for meiosis II to occur in the absence of a p receding DNA replication. The proportionality between genome size and meiotic duration can be explained if meiotic chromosome-pairing is med iated primarily by DNA-DNA hybridization: special synaptonemal complex proteins were therefore not necessary for the origin of meiotic pairi ng. The diplokaryotic state, or diplokaryosis, which is widespread in the archezoan Microsporidia and Metamonada, may have played a key role in the evolution of these two phyla and has significant implications for early evolution of the eukaryotic cell cycle and recombination. Di plokaryosis is defined as the coexistence in the same cell of two hapl oid nuclei physically attached together and which divide equationally so that each daughter cell receives one daughter nucleus from each par ent. In principle nuclear fusion could have evolved in a diplokaryotic or in uninucleate archezoan after the origin of meiosis, and before t he origin of syngamy as part of an asexual ploidy cycle. Diplokaryosis itself may have directly favoured the origin of nucteocytoplasmic rea rrangements associated with encystation. Modification of the centriole /centrosome cycle was important in these and also in the origin of mei osis. If syngamy was the final step in the evolution of sex, not the i nitial one as commonly assumed, it could have rapidly spread through t he population of an asexual archezoan, with a ploidy cycle involving m eiosis and nuclear fusion, as the result of the evolution of a gene en coding a membrane-protein that promotes the fusion of the plasma membr ane with that of other related cells. Such a fusogenic gene might have spread faster by being closely linked to a highly beneficial novel ge ne than by virtue of a general effect on recombination, and faster sti ll if it were inserted into a transposon that could spread intragenomi cally.