Epistatic interactions among herbicide resistances in Arabidopsis thaliana: the fitness cost of multiresistance

The type of interactions among deleterious mutations is considered to be crucial in numerous areas of evolutionary biology, including the evolution of sex and recombination, the evolution of ploidy, the evolution of selfing, and the conservation of small populations. Because the herbicide resistance genes could be viewed as slightly deleterious mutations in the absence of the pesticide selection pressure, the epistatic interactions among three herbicide resistance genes (acetolactate synthase CSR, cellulose synthase IXR1, and auxin-induced AXR1 target genes) were estimated in both the homozygous and the heterozygous states, giving 27 genotype combinations in the model plant Arabidopsis thaliana. By analyzing eight quantitative traits in a segregating population for the three herbicide resistances in the absence of herbicide, we found that most interactions in both the homozygous and the heterozygous states were best explained by multiplicative effects (each additional resistance gene causes a comparable reduction in fitness) rather than by synergistic effects (each additional resistance gene causes a disproportionate fitness reduction). Dominance coefficients of the herbicide resistance cost ranged from partial dominance to underdominance, with a mean dominance coefficient of 0.07. It was suggested that the csr1-1, ixr1-2, and axr1-3 resistance alleles are nearly fully recessive for the fitness cost. More interestingly, the dominance of a specific resistance gene in the absence of herbicide varied according to, first, the presence of the other resistance genes and, second, the quantitative trait analyzed. These results and their implications for multiresistance evolution are discussed in relation to the maintenance of polymorphism at resistance loci in a heterogeneous environment.