Origins of the machinery of recombination and sex

Abstract

Mutation plays the primary role in evolution that Weismann mistakenly attributed to sex. Homologous recombination, as in sex, is important for population genetics -shuffling of minor variants, but relatively insignificant for large-scale evolution. Major evolutionary innovations depend much more on illegitimate recombination, which makes novel genes by gene duplication and by gene chimaerisationessentially mutational forces. The machinery of recombination and sex evolved in two distinct bouts of quantum evolution separated by nearly 3 Gy of stasis; I discuss their nature and causes. The dominant selective force in the evolution of recombination and sex has been selection for replicational fidelity and viability; without the recombination machinery, accurate reproduction, stasis, resistance to radical deleterious evolutionary change and preservation of evolutionary innovations would be impossible. Recombination proteins betray in their phylogeny and domain structure a key role for gene duplication and chimaerisation in their own origin. They arose about 3.8 Gy ago to enable faithful replication and segregation of the first circular DNA genomes in precellular ancestors of Gram-negative eubacteria. Then they were recruited and modified by selfish genetic parasites (viruses; transposons) to help them spread from host to host. Bacteria differ fundamentally from eukaryotes in that gene transfer between cells, whether incidental to their absorptive feeding on DNA and virus infection or directly by plasmids, involves only genomic fragments. This was radically changed by the neomuran revolution about 850 million years ago when a posibacterium evolved

A microscopic model of evolution of recombination

“…Meiosis and recombination then evolved as a mechanism to restore the ploidity characteristic of the species during excystment; haploid cells then reproduced through mitosis [13,14]. It should be noted that the evolution of meiosis was a comparatively simple evolutionary step as many recombination enzymes already existed being involved in other processes like replication, transcription and repair [15]. Even if syngamy originally evolved for trophic reasons, on the long run, sex fixed in populations due to the several advantages of gene mixing.…”

Seaweed reproductive biology: environmental and genetic controls

“…We refer to several excellent reviews for an in-depth discussion on the origin and maintenance of sexual reproduction (e.g. Maynard-Smith 1978, Bernstein et al 1981, Michod 1993, Barton and Charlesworth 1998, Cavalier-Smith 2002. In the context of this review, the empirical observation that starvation is known to induce sexual reproduction in many protists is important.…”

“…The carposporophyte releases diploid spores, carpospores, which grow into diploid tetrasporophytes (West and Hommersand 1981). Regardless of this large variation in life cycles, the core processes of life cycles, meiosis and syngamy, are conserved among virtually all eukaryotes (Cavalier-Smith 2002), leading to questions about the levels at which the ecological and molecular processes controlling these processes and their relative timing are conserved.…”

“…An alternation of haploid and diploid life stages mediated by meiosis and syngamy evolved at the base of the eukaryotic tree of life (Cavalier-Smith 2002, Speijer et al 2015. A number of non-mutually exclusive theories, e.g.…”

Evolutionary mysteries in meiosis

“…The first is that diploidy accidentally occurred by replication of the nuclear genome without subsequent cell division (endoreplication) [8][9][10][11][12], and that returning to haploidy was selected for to correct this. Because either haploidy or higher ploidy levels may be favoured in different ecological situations [13,14], a variant of this scenario is that a proto-meiosis-endoreplication cycle evolved to switch between ploidy levels [5]. The resulting life cycle may have resembled modern 'parasexual' fungi in which diploid cells lose chromosomes in subsequent mitotic divisions, leading to haploidy via aneuploid intermediates [15].…”