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

Abstract

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 and the advantage of recombination

“…The net effect, it is argued, should be that alleles across loci will on average be selectively mismatched within a population. On one hand, our findings (ev1 [30]) diverge slightly from this Otto & Barton effect: we find that even genotypes that are ultimately fixed carry selectively mismatched alleles on average. On the other hand, however (ev2 [31]), our findings are entirely consistent with this effect; indeed, our proof that ∞ 0 ⟨σ XY (u)⟩du ≤ 0, unconditionally (Prop 3 in ev2 [31]), may be interpreted as a proof of the universality of the Otto & Barton effect.…”

“…Our analyses further show that the expected asymptotic frequency of the rec + allele is effectively equal to the probability that the fittest possible genotype is a virtual (or potential) recombinant. When covariance between X and Y in the initial variation is non-positive, as would be the case for example if the initial variants are themselves products of previous selection (ev1 [30]), this finding implies that the expected asymptotic modifier frequency is 1) , where m is the number of loci and n the number of alleles per locus. From this expression it is apparent that expected asymptotic modifier frequency can be very close to one under reasonable conditions.…”

“…On the surface, the Bulmer effect appears similar to the phenomena we describe. On closer examination, however, it differs in several critical ways that are listed and discussed in ev1 [30] and the SM. In the context of the evolution of recombination, the most consequential difference is depicted in Fig 4 . The Bulmer effect is only non-negligible under strong selection in small populations and assumes the initial distribution of fitness components is multivariate normal.…”

“…The second term is not transient and we are interested in its temporal limit as an indication of whether recombination is promoted or suppressed on average between different products of natural selection coming from different local populations. Math-ematically, the two prongs of our study thus focus on the quantities ( ev 2 [31]) and lim t →∞ σ 〈X〉〈Y〉 ( ev 1 [30]).…”

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

“…To preface our developments therefore, we cover some essential background and make reference to some reviews [3][4][5][6][7][8][9] that give a much more complete overview of the remarkable wealth of previous and current work in this area. Also, we refer to our companion publications ev0 [1] and ev1 [2] for additional introductory material.…”