The evolution of recombination

The selective forces responsible for the evolution of genes mediating recombination are discussed. These genes originated because of their role indna repair. In eukaryotes, their role in repair is not sufficient to account for the evolution of meiosis and syngamy. Therefore, a “hitch-hiking” explanation is required, according to which a recombination gene gets a lift in frequency from the high-fitness genes to which it is linked. Such hitch-hiking models are reviewed: collectively they provide an adequate explanation for the maintenance of sex and recombination in eukaryotes. In prokaryotes, the main selective force favouring recombination isdna repair: the cross-overs caused by recombination may occasionally have important evolutionary effects, but they are the consequences, rather than the causes, of the evolution of recombination in prokaryotes. In both prokaryotes and eukaryotes, recombination genes also cause specific, repeatable and adaptive rearrangements of the genetic material.     

The evolution of sex and recombination

The evolution and maintenance of sexual reproduction, and the associated process of genetic recombination, are still controversial issues. Two recent books have provided overviews of the ideas and observations in this field. This article reviews some of the major ideas that have been proposed to account for sex and recombination, and comments on the results of attempts at empirical tests. While there is now an impressive body of well-formulated evolutionary models, it has proved hard to discriminate between them, either experimentally or by means of comparative data. It may well be that there is no unitary selective advantage to sex and recombination, but that a variety of forces are involved.     

The evolution of sex dimorphism in recombination

Sex dimorphism in recombination is widespread on both sex chromosomes and autosomes. Various hypotheses have been proposed to explain these dimorphisms. Yet no theoretical model has been explored to determine how heterochiasmy--the autosomal dimorphism--could evolve. The model presented here shows three circumstances in which heterochiasmy is likely to evolve: (i) a male-female difference in haploid epistasis, (ii) a male-female difference in cis-epistasis minus trans-epistasis in diploids, or (iii) a difference in epistasis between combinations of genes inherited maternally or paternally. These results hold even if sources of linkage disequilibria besides epistasis, such as migration or Hill-Robertson interference, are considered and shed light on previous verbal models of sex dimorphism in recombination rates. Intriguingly, these results may also explain why imprinted regions on the autosomes of humans or sheep are particularly heterochiasmate.     

The evolution of recombination in changing environments

Recombination generates under-represented genotypes by breaking down linkage disequilibrium between genes. Recent analyses have specified the conditions under which recombination is favored. These conditions are surprisingly sensitive to the form of selection and environmental change. This quantification makes it possible to use empirical measurements of critical parameters such as the form of epistasis, the rate of mutation, and the frequency of beneficial sweeps to assess different hypotheses for the evolution of recombination.     

Experimental evolution across different thermal regimes yields genetic divergence in recombination fraction but no divergence in temperature associated plastic recombination

Phenotypic plasticity is pervasive in nature. One mechanism underlying the evolution and maintenance of such plasticity is environmental heterogeneity. Indeed, theory indicates that both spatial and temporal variation in the environment should favor the evolution of phenotypic plasticity under a variety of conditions. Cyclical environmental conditions have also been shown to yield evolved increases in recombination frequency. Here, we use a panel of replicated experimental evolution populations of D. melanogaster to test whether variable environments favor enhanced plasticity in recombination rate and/or increased recombination rate in response to temperature. In contrast to expectation, we find no evidence for either enhanced plasticity in recombination or increased rates of recombination in the variable environment lines. Our data confirm a role of temperature in mediating recombination fraction in D. melanogaster, and indicate that recombination is genetically and plastically depressed under lower temperatures. Our data further suggest that the genetic architectures underlying plastic recombination and population‐level variation in recombination rate are likely to be distinct.     

The Hill-Robertson effect and the evolution of recombination

In finite populations, genetic drift generates interference between selected loci, causing advantageous alleles to be found more often on different chromosomes than on the same chromosome, which reduces the rate of adaptation. This "Hill-Robertson effect" generates indirect selection to increase recombination rates. We present a new method to quantify the strength of this selection. Our model represents a new beneficial allele (A) entering a population as a single copy, while another beneficial allele (B) is sweeping at another locus. A third locus affects the recombination rate between selected loci. Using a branching process model, we calculate the probability distribution of the number of copies of A on the different genetic backgrounds, after it is established but while it is still rare. Then, we use a deterministic model to express the change in frequency of the recombination modifier, due to hitchhiking, as A goes to fixation. We show that this method can give good estimates of selection for recombination. Moreover, it shows that recombination is selected through two different effects: it increases the fixation probability of new alleles, and it accelerates selective sweeps. The relative importance of these two effects depends on the relative times of occurrence of the beneficial alleles.     

The evolution of recombination in a heterogeneous environment

Most models describing the evolution of recombination have focused on the case of a single population, implicitly assuming that all individuals are equally likely to mate and that spatial heterogeneity in selection is absent. In these models, the evolution of recombination is driven by linkage disequilibria generated either by epistatic selection or drift. Models based on epistatic selection show that recombination can be favored if epistasis is negative and weak compared to directional selection and if the recombination modifier locus is tightly linked to the selected loci. In this article, we examine the joint effects of spatial heterogeneity in selection and epistasis on the evolution of recombination. In a model with two patches, each subject to different selection regimes, we consider the cases of mutation-selection and migration-selection balance as well as the spread of beneficial alleles. We find that including spatial heterogeneity extends the range of epistasis over which recombination can be favored. Indeed, recombination can be favored without epistasis, with negative and even with positive epistasis depending on environmental circumstances. The selection pressure acting on recombination-modifier loci is often much stronger with spatial heterogeneity, and even loosely linked modifiers and free linkage may evolve. In each case, predicting whether recombination is favored requires knowledge of both the type of environmental heterogeneity and epistasis, as none of these factors alone is sufficient to predict the outcome.     

The evolution of recombination in permanent translocation heterozygotes

The evolution of a selectively neutral locus that controls the degree to which alleles at a single selected locus are linked with a particular set of chromosomes in a permanent translocation heterozygote is studied. With complete selfing and fitness overdominance a new allele at the modifying locus will increase in frequency if it increases the linkage of all alleles at the selected locus to a particular set of chromosomes. With random mating a new allele at the modifying locus will increase when rare if it increases the linkage of alleles at the selected locus to a particular set of chromosomes. In addition, a parameter analogous to the coefficient of linkage disequilibrium in usual two-locus models with random mating must be nonzero if a new allele at the modifying locus is to increase in frequency at a geometric rate when rare. With mixed selfing and random mating a new allele at the modifying locus will apparently increase when rare only if it increases the linkage of alleles at the selected locus to a particular set of chromosomes.     

Genome evolution: recombination speeds up adaptive evolution

Mutual interference among linked genetic sites subject to selection may reduce the level of adaptation. A recent study detected this effect using data on protein sequence evolution and codon usage in Drosophila.     

Self-fertilization and the evolution of recombination

In this article, we study the effect of self-fertilization on the evolution of a modifier allele that alters the recombination rate between two selected loci. We consider two different life cycles: under gametophytic selfing, a given proportion of fertilizations involves gametes produced by the same haploid individual, while under sporophytic selfing, a proportion of fertilizations involves gametes produced by the same diploid individual. Under both life cycles, we derive approximations for the change in frequency of the recombination modifier when selection is weak relative to recombination, so that the population reaches a state of quasi-linkage equilibrium. We find that gametophytic selfing increases the range of epistasis under which increased recombination is favored; however, this effect is substantial only for high selfing rates. Moreover, gametophytic selfing affects the relative influence of different components of epistasis (additive x additive, additive x dominance, dominance x dominance) on the evolution of the modifier. Sporophytic selfing has much stronger effects: even a small selfing rate greatly increases the parameter range under which recombination is favored, when there is negative dominance x dominance epistasis. This effect is due to the fact that selfing generates a correlation in homozygosity at linked loci, which is reduced by recombination.     

The effect of recombination on the neutral evolution of genetic robustness

Conventional population genetics considers the evolution of a limited number of genotypes corresponding to phenotypes with different fitness. As model phenotypes, in particular RNA secondary structure, have become computationally tractable, however, it has become apparent that the context dependent effect of mutations and the many-to-one nature inherent in these genotype-phenotype maps can have fundamental evolutionary consequences. It has previously been demonstrated that populations of genotypes evolving on the neutral networks corresponding to all genotypes with the same secondary structure only through neutral mutations can evolve mutational robustness [E. van Nimwegen, J.P. Crutchfield, M. Huynen, Neutral evolution of mutational robustness, Proc. Natl. Acad. Sci. USA 96(17), 9716-9720 (1999)], by concentrating the population on regions of high neutrality. Introducing recombination we demonstrate, through numerically calculating the stationary distribution of an infinite population on ensembles of random neutral networks that mutational robustness is significantly enhanced and further that the magnitude of this enhancement is sensitive to details of the neutral network topology. Through the simulation of finite populations of genotypes evolving on random neutral networks and a scaled down microRNA neutral network, we show that even in finite populations recombination will still act to focus the population on regions of locally high neutrality.     

The evolution of the midface lift in aesthetic plastic surgery

The midface lift has recently gained significant popularity with many surgeons. It allows the surgeon an opportunity to achieve greater facial harmony with facial rejuvenation procedures by correcting midfacial atrophy, addressing the tear trough deformity, and correcting the perceived malposition of the malar fat pad. This article examines the history of midfacial procedures. Surgical attempts at improving the aging face have evolved from minimal excisions and skin closure to aggressive dissections at multiple planes. The midface target area is peripheral to classic approaches, and its correction has required further anterior dissection from a distance or direct access centrally. Ultimately, conquering the stigmata of midface aging is entirely related to vectors and volume.     

The evolution of the brow lift in aesthetic plastic surgery

For nearly 100 years, aesthetic improvement of the aging face has included surgical elevation of the brow. Early attempts to correct brow ptosis were largely unsuccessful. Recognizing the need to modify the frown muscles heralded the achievement of results previously unobtainable. Within the past decade, the minimal incision approach to brow lifting afforded with the endoscope radically changed surgical options in forehead rejuvenation. Further advances have added to these options and have provided a palette of alternatives in aesthetic correction of the upper one-third of the aging face.     

The role of epistasis on the evolution of recombination in host-parasite coevolution

Antagonistic coevolution between hosts and parasites is known to affect selection on recombination in hosts. The Red Queen Hypothesis (RQH) posits that genetic shuffling is beneficial for hosts because it quickly creates resistant genotypes. Indeed, a large body of theoretical studies have shown that for many models of the genetic interaction between host and parasite, the coevolutionary dynamics of hosts and parasites generate selection for recombination or sexual reproduction. Here we investigate models in which the effect of the host on the parasite (and vice versa) depend approximately multiplicatively on the number of matched alleles. Contrary to expectation, these models generate a dynamical behavior that strongly selects against recombination/sex. We investigate this atypical behavior analytically and numerically. Specifically we show that two complementary equilibria are responsible for generating strong linkage disequilibria of opposite sign, which in turn causes strong selection against sex. The biological relevance of this finding stems from the fact that these phenomena can also be observed if hosts are attacked by two parasites that affect host fitness independently. Hence the role of the Red Queen Hypothesis in natural host parasite systems where infection by multiple parasites is the rule rather than the exception needs to be reevaluated.     

The evolution of recombination under domestication: a test of two hypotheses

The successful domestication of wild plants has been one of the most important human accomplishments of the last 10,000 yr. Though our empirical knowledge of the genetic mechanisms of plant domestication is still relatively limited, there exists a large body of theory that offers a host of hypotheses on the genetics of domestication. Two of these that have not been addressed concern the role of recombination in the process of domestication. The first predicts an increase in recombination rate through domestication, while the second argues that recombination rate should serve as a preadaptation to domestication. This study makes use of data on chiasma frequencies available from almost a century of plant cytogenetical literature to test these two hypotheses. The results support the hypothesis that domestication selects for an increase in recombination, and in rejecting the preadaptation hypothesis, they suggest directions for future research into the possibility of preadaptation to domestication.