Antagonistic pleiotropic effects reduce the potential adaptive value of the FRIGIDA locus

Abstract

Although the occurrence of epistasis and pleiotropy is widely accepted at the molecular level, its effect on the adaptive value of fitness-related genes is rarely investigated in plants. Knowledge of these features of a gene is critical to understand the molecular basis of adaptive evolution. Here we investigate the importance of pleiotropy and epistasis in determining the adaptive value of a candidate gene using the gene FRI (FRIGIDA), which is thought to be the major gene controlling flowering time variation in Arabidopsis thaliana. The effect of FRI on flowering time was analyzed in an outbred population created by randomly mating 19 natural accessions of A. thaliana. This unique population allows the estimation of FRI effects independent of any linkage association with other loci due to demographic processes or to coadapted genes. It also allows for the estimation of pleiotropic effects of FRI on fitness and inflorescence architecture. We found that FRI explains less variation in flowering time than previously observed among natural accessions, and interacts epistatically with the FLC locus. Although early flowering plants produce more fruits under spring conditions, and nonfunctional alleles of FRI were associated with early flowering, variation at FRI was not associated with fitness. We show that nonfunctional FRI alleles have negative pleiotropic effects on fitness by reducing the numbers of nodes and branches on the inflorescence. We propose that these antagonistic pleiotropic effects reduce the adaptive value of FRI, and helps explain the maintenance of alternative life history strategies across natural populations of A. thaliana.

Fig. 1.

Distribution of flowering time in the F₅ population (white bars) and among the 19 parental accessions (black bars) under spring and fall treatments.

Fig. 2.

Effect of FRI and the FLC genotypes on flowering time under spring treatments. Letters (a and b), numbers (1 and 2), or symbols (+ and ‡) indicate groups that are significantly different based on Tukey's post hoc tests. Error bars represent the 95% confidence interval.

Fig. 3.

Path coefficients (standardized partial regression coefficients) from FRI and FLC to flowering time, inflorescence traits, and fruit production. Dashed lines represent nonsignificant paths. The overall significance of the model is indicated below each diagram and was calculated including only significant paths.