Resource allocation trade-offs and the loss of chemical defences during apple domestication.

Abstract

Most crops have been dramatically altered from their wild ancestors with the primary goal of increasing harvestable yield. A long-held hypothesis is that increased allocation to yield has reduced plant investment in defence and resulted in crops that are highly susceptible to pests. However, clear demonstrations of these trade-offs have been elusive due to the many selective pressures that occur concurrently during crop domestication. To provide a robust test of whether increased allocation to yield can alter plant investment in defence, this study examined fruit chemical defence traits and herbivore resistance across 52 wild and 56 domesticated genotypes of apples that vary >26-fold in fruit size. Ninety-six phenolic metabolites were quantified in apple skin, pulp and seeds, and resistance to the codling moth was assessed with a series of bioassays. The results show that wild apples have higher total phenolic concentrations and a higher diversity of metabolites than domesticated apples in skin, pulp and seeds. A negative phenotypic relationship between fruit size and phenolics indicates that this pattern is driven in part by allocation-based trade-offs between yield and defence. There were no clear differences in codling moth performance between wild and domesticated apples and no overall effects of total phenolic concentration on codling moth performance, but the results did show that codling moth resistance was increased in apples with higher phenolic diversity. The concentrations of a few individual compounds (primarily flavan-3-ols) also correlated with increased resistance, primarily driven by a reduction in pupal mass of female moths. The negative phenotypic relationship between fruit size and phenolic content, observed across a large number of wild and domesticated genotypes, supports the hypothesis of yield-defence trade-offs in crops. However, the limited effects of phenolics on codling moth highlight the complexity of consequences that domestication has for plant-herbivore interactions. Continued studies of crop domestication can further our understanding of the multiple trade-offs involved in plant defence, while simultaneously leading to novel discoveries that can improve the sustainability of crop production.