On the origin of meiosis in eukaryotic evolution: Coevolution of meiosis and mitosis from feeble beginnings

Abstract

The processes making up meiosis are complex and, arguably, may be the most complicated cellular process in eukaryotes. Its origin has been discussed at length for over 100 years, without any consensus. Although earlier investigators favored it as being very ancient, there has been a tendency over recent decades to consider it as a feature that arose relatively late in the evolution of eukaryotes. However, the study of the genomes of early-diverging eukaryotes makes it appear that many proteins that are specific and/or required for meiosis occur widely throughout eukaryotes, implying that meiosis must have evolved at least before their last common ancestor. Indeed, the advantages of genetic recombination would have applied to much earlier forms of life, right back to the hypothesized RNA world. In agreement with a very early origin, many of the proteins involved in meiosis, especially those involved in recombination and/or in repair of double-stranded DNA breaks (DSBs), have homologs in prokaryotes. The simplest hypothesis at present is that some form of recombination would have occurred extremely early in life (possibly even before the origin of protein synthesis) and it is likely that there was always some form of genetic recombination since that time. At some point in early evolution, a more specialized regimen of abundant recombination was uncoupled from the repair of accidental damage to serve a once-per-lifecycle event of genomic reconstitution. This happened before the last common eukaryotic ancestor, when the mitotic system in the modern sense had not yet been fully consolidated. We call this the Coevolution Hypothesis for the origin of meiosis - that both mitotic segregation mechanisms and meiotic recombination and chromosome reshuffling occurred very early and kept improving with increasing complexity during the evolution of eukaryotes. © 2007 Springer-Verlag Berlin Heidelberg.