Genomic evidence of genetic variation with pleiotropic effects on caterpillar fitness and plant traits in a model legume

Abstract

Plant-insect interactions are ubiquitous, and have been studied intensely because of their relevance to damage and pollination in agricultural plants, and to the ecology and evolution of biodiversity. Variation within species can affect the outcome of these interactions, such as whether an insect successfully develops on a plant species. Whereas specific genes and chemicals that mediate these interactions have been identified, studies of genome-or metabolome-wide intraspecific variation might be necessary to better explain patterns of host-plant use and adaptation often observed in the wild. Here, we present such a study. Specifically, we assess the consequences of genome-wide genetic variation in the model plant Medicago truncatula for Lycaeides melissa caterpillar growth and survival (i.e., larval performance). Using a rearing experiment and a whole-genome SNP data set (>5 million SNPs), we show that polygenic variation in M. truncatula explains 9-41% of the observed variation in caterpillar growth and survival. We detect genetic correlations among caterpillar performance and other plant traits, such as structural defenses and some anonymous chemical features; these genetic correlations demonstrate that multiple M. truncatula alleles have pleiotropic effects on plant traits and caterpillar growth or survival (or that there is substantial linkage disequilibrium among loci affecting these traits). We further show that a moderate proportion of the genetic effect of M. truncatula alleles on L. melissa performance can be explained by the effect of these alleles on the plant traits we measured, especially leaf toughness. Taken together, our results show that intraspecific genetic variation in M. truncatula has a substantial effect on the successful development of L. melissa caterpillars (i.e., on a plant-insect interaction), and further point toward traits mediating this genetic effect.