Natural selection and the advantage of recombination

Cordero

et al. 2020

Preprint

Self Cite

Exchanging genetic material with another individual seems risky from an evolutionary standpoint, and yet living things across all scales and phyla do so quite regularly. The pervasiveness of such genetic exchange, or recombination, in nature has defied explanation since the time of Darwin1–4. Conditions that favor recombination, however, are well-understood: recombination is advantageous when the genomes of individuals in a population contain more selectively mismatched combinations of alleles than can be explained by chance alone. Recombination remedies this imbalance by shuffling alleles across individuals. The great difficulty in explaining the ubiquity of recombination in nature lies in identifying a source of this imbalance that is comparably ubiquitous. Intuitively, it would seem that natural selection should reduce the imbalance by favoring selectively matched combinations of high-fitness alleles. We show, however, that this widely-held intuition is wrong; to the contrary, we find that natural selection has an encompassing tendency to assemble selectively mismatched combinations of alleles, thereby increasing the imbalance and promoting the evolution of recombination across demes in a structured population. We further show that, on average, selection-driven changes in allele frequencies over time within a single evolving population generate a net imbalance that promotes recombination, and additive fitness effects drive this imbalance. Our findings provide a novel theoretical point of departure from which the enormous body of established work on the evolution of sex and recombination may be viewed anew. They further suggest that recombination evolved and is maintained more as a byproduct of natural selection than as a catalyst.

Natural selection and the advantage of recombination

Cordero

et al. 2020

Preprint

Self Cite

Natural selection promotes the evolution of recombination 1: between the products of natural selection*

Sniegowski

et al. 2021

Preprint

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Shuffling one's genetic material with another individual seems a risky endeavor more likely to decrease than to increase offspring fitness. This intuitive argument is commonly employed to explain why the ubiquity of sex and recombination in nature is enigmatic. It is predicated on the notion that natural selection assembles selectively well-matched combinations of genes that recombination would break up resulting in low-fitness offspring -- a notion so intuitive that it is often stated in the literature as a self-evident premise. We show, however, that this common premise is only self evident on the surface and that, upon closer examination, it is fundamentally flawed: we find that natural selection in fact has an encompassing tendency to assemble selectively mismatched combinations of alleles; recombination breaks up these selectively mismatched combinations (on average), assembles selectively matched combinations, and should thus be favored. The new perspective our findings offer suggests that sex and recombination are not so enigmatic but are instead natural and unavoidable byproducts of natural selection.

Natural selection promotes the evolution of recombination 2: during the process of natural selection*

Cordero

et al. 2021

Preprint

Self Cite

The ubiquity of genetic mixing in nature has eluded unified explanation since the time of Darwin. Conditions that promote the evolution of genetic mixing (recombination) are fairly well understood: it is favored when genomes tend to contain more selectively mismatched combinations of alleles than can be explained by chance alone. Yet, while a variety of theoretical approaches have been put forth to explain why such conditions would have an overarching tendency to prevail in natural populations, each has turned out to be of limited scope and applicability. In our two-part study, we show that, simply and surprisingly, the action of natural selection acting on standing heritable variation creates conditions favoring the evolution of recombination. In this paper, we focus on the mean selective advantage created by recombination between individuals from the same population. We find that the mean selective advantages of recombinants and recombination are non-negative, in expectation, independently of how genic fitnesses in the standing variation are distributed. We further find that the expected asymptotic frequency of a recombination-competent modifier is effectively equal to the probability that the fittest possible genotype is a virtual recombinant; remarkably, expected asymptotic modifier frequency is independent of the strength of selection. Taken together, our findings indicate that the evolution of recombination should be promoted in expectation wherever natural selection is operating.