Effect of Varying Epistasis on the Evolution of Recombination

Whether recombination decelerates or accelerates a population's response to selection depends, at least in part, on how fitness-determining loci interact. Realistically, all genomes likely contain fitness interactions both with positive and with negative epistasis. Therefore, it is crucial to determine the conditions under which the potential beneficial effects of recombination with negative epistasis prevail over the detrimental effects of recombination with positive epistasis. Here, we examine the simultaneous effects of diverse epistatic interactions with different strengths and signs in a simplified model system with independent pairs of interacting loci and selection acting only on the haploid phase. We find that the average form of epistasis does not predict the average amount of linkage disequilibrium generated or the impact on a recombination modifier when compared to results using the entire distribution of epistatic effects and associated single-mutant effects. Moreover, we show that epistatic interactions of a given strength can produce very different effects, having the greatest impact when selection is weak. In summary, we observe that the evolution of recombination at mutation–selection balance might be driven by a small number of interactions with weak selection rather than by the average epistasis of all interactions. We illustrate this effect with an analysis of published data of Saccharomyces cerevisiae. Thus to draw conclusions on the evolution of recombination from experimental data, it is necessary to consider the distribution of epistatic interactions together with the associated selection coefficients.

[1]  J. D. de Visser,et al.  An experimental test for synergistic epistasis and its application in Chlamydomonas. , 1997, Genetics.

[2]  M. Feldman,et al.  On the evolutionary effect of recombination. , 1970, Theoretical population biology.

[3]  Santiago F. Elena,et al.  Little Evidence for Synergism Among Deleterious Mutations in a Nonsegmented RNA Virus , 1999, Journal of Molecular Evolution.

[4]  S. Otto,et al.  Evolution of sex: Resolving the paradox of sex and recombination , 2002, Nature Reviews Genetics.

[5]  R. Korona,et al.  Epistatic interactions of spontaneous mutations in haploid strains of the yeast Saccharomyces cerevisiae , 2001 .

[6]  S. Elena,et al.  EFFECT OF DELETERIOUS MUTATION-ACCUMULATION ON THE FITNESS OF RNA BACTERIOPHAGE MS2 , 2000 .

[7]  A. D. Peters,et al.  A test for epistasis among induced mutations in Caenorhabditis elegans. , 2000, Genetics.

[8]  T MUKAI,et al.  THE GENETIC STRUCTURE OF NATURAL POPULATIONS OF DROSOPHILA MELANOGASTER. I. SPONTANEOUS MUTATION RATE OF POLYGENES CONTROLLING VIABILITY. , 1964, Genetics.

[9]  C. Petropoulos,et al.  Evidence for Positive Epistasis in HIV-1 , 2004, Science.

[10]  Andres Moya,et al.  EFFECT OF DELETERIOUS MUTATION‐ACCUMULATION ON THE FITNESS OF RNA BACTERIOPHAGE MS2 , 2000, Evolution; international journal of organic evolution.

[11]  R. Korona,et al.  Small fitness effects and weak genetic interactions between deleterious mutations in heterozygous loci of the yeast Saccharomyces cerevisiae. , 2003, Genetical research.

[12]  R. Lenski,et al.  Test of synergistic interactions among deleterious mutations in bacteria , 1997, Nature.

[13]  N. Barton,et al.  A general model for the evolution of recombination. , 1995, Genetical research.

[14]  M W Feldman,et al.  Deleterious mutations, variable epistatic interactions, and the evolution of recombination. , 1997, Theoretical population biology.

[15]  A. D. Peters,et al.  Testing for epistasis between deleterious mutations. , 1998, Genetics.

[16]  O. Kitagawa Interaction in fitness between lethal genes in heterozygous condition in Drosophila melanogaster. , 1967, Genetics.