Antagonistic selection and pleiotropy constrain the evolution of plant chemical defenses.

ABSTRACT

When pleiotropy is present, genetic correlations may constrain the evolution of ecologically important traits. We used a quantitative genetics approach to investigate constraints on the evolution of secondary metabolites in a wild mustard, Boechera stricta. Much of the genetic variation in chemical composition of glucosinolates in B. stricta is controlled by a single locus, BCMA1/3. In a large-scale common garden experiment under natural conditions, we quantified fitness and glucosinolate profile in two leaf types and in fruits. We estimated genetic variances and covariances (the G-matrix) and selection on chemical profile in each tissue. Chemical composition of defenses was strongly genetically correlated between tissues. We found antagonistic selection between defense composition in leaves and fruits compounds that were favored in leaves were disadvantageous in fruits. The positive genetic correlations and antagonistic selection led to strong constraints on the evolution of defenses in leaves and fruits. In a hypothetical population with no genetic variation at BCMA1/3, we found no evidence for genetic constraints, indicating that pleiotropy affecting chemical profile in multiple tissues drives constraints on the evolution of secondary metabolites.