Natural selection and the advantage of recombination

Abstract

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

“…If the heritable variation upon which natural selection acts is itself a product of previous selection, our companion papers [1,2] show that the genic fitness correlation between loci will be negative. For this case, asymptotic modifier frequency is even higher:…”

“…Muller surmised that in order for separately arising beneficial mutations to fix in the same genotype, in an asexual population they must arise in the same lineage sequentially, while in a recombining population, they may arise contemporaneously and be subsequently reshu✏ed into the same background. Fisher argued that a single beneficial mutation, because it arises in a single individual, has a ⇤ This article is published in concert with [1] and [2] † pgerrish@unm.edu significant probability of arising on a non-optimal genetic background. In an asexual population, the beneficial mutation is stuck with this non-optimal background, while in a recombining population, the background can be swapped out for a fitter one.…”

“…In companion papers [1] and [2], we show that natural selection acting on standing variation has an encompassing tendency to fix selectively mismatched combinations of alleles, thereby promoting the evolution of recombination across selected genotypes. In the present study, we assess how the selective value of recombinants and recombination are a↵ected during the process of natural selection within a population.…”

“…In companion papers prl [1] and pre1 [2] , we show that natural selection acting on standing variation has an encompassing tendency to amplify selectively mismatched combinations of alleles, thereby promoting the evolution of recombination across the products of selection, defined as genotypes that have become locally prevalent in their respective populations, subpopulations, demes, or clones through the local action of natural selection. In the present study, we assess how the selective value of recombinants and recombination are affected during the process of natural selection within an unstructured population.…”

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

“…We employ this definition of ϕ extensively in the main text and in our analyses, both because of its simplicity and because of its connection to classical population genetics and notions of additive fitness. On the left-hand side, the genomes are not sorted in any order; on the right-hand side, the same genomes are sorted (ranked) by their total fitness, Z , such that Z [1] is the genome of lowest fitness and Z [ n ] is the genome of highest fitness. In an infinite population (deterministic selection), the fittest genome ( Z [ n ] , highlighted by a frame) always eventually displace all other genomes.…”