Why did evolution lead to another cell division ‘meiosis’ when mitosis was already existing?
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… if there is one event in the whole evolutionary sequence at which my own mind lets my awe still overcome my instinct to analyse, and where I might concede that there may be a difficulty in seeing a Darwinian gradualism hold sway throughout almost all, it is this event—the initiation of meiosis.
W. J. Hamilton (1999, p. 419)
THE origins of meiosis in early eukaryotic history have never been satisfactorily explained. Since the reduction-division process in meiosis is essential for sexual life cycles, discussion of the origins of meiosis has been closely tied to debates about the evolutionary value of sex itself and the selective pressures for its maintenance. Yet the cytological events involved in the origins of meiosis are as puzzling as the question of selective pressures. While meiosis almost certainly evolved from mitosis, it has not one but four novel steps: the pairing of homologous chromosomes, the occurrence of extensive recombination between non-sister chromatids during pairing, the suppression of sister-chromatid separation during the first meiotic division, and the absence of chromosome replication during the second meiotic division. This complexity presents a challenge to any Darwinian explanation of meiotic origins. While the simultaneous creation of these new features in one step seems impossible, their step-by-step acquisition via selection of separate mutations seems highly problematic, given that the entire sequence is required for reliable production of haploid chromosome sets. Both Maynard Smith (1978) and Hamilton (1999) regarded the origins of meiosis as one of the most difficult evolutionary problems.
In this Perspectives article, we present a hypothesis of the origins of meiosis that encompasses both the cytological novelties and the selective forces that might have favored them. We first present the reasons for thinking that the initial step involved a key innovation, that of extensive homolog pairing (synapsis), and then discuss how the other three distinctive properties can be accounted for. We next ask what selective pressures might have favored the acquisition of homolog synapsis. The conclusion is surprising: the initial function of chromosome pairing was to limit, not enhance, recombination. Finally, we review the evidence that much of the molecular machinery required for the initial forms of homolog pairing probably existed in proto-eukaryote unicellular forms prior to the evolution of meiosis and therefore could have been readily “recruited” for the new role. Some experimental tests of the hypothesis are proposed.