Field studies have shown that plant phenological and architectural traits often explain substantial variation in herbivory. Although plant genes involved in physical and chemical defense are well studied, less is known about the genetic basis underlying effects of plant growth traits on herbivory. Here, we conducted a genome-wide association study (GWAS) of aphid abundance in a field population ofArabidopsis thaliana. This field GWAS detected a significant peak on the third chromosome ofA. thaliana. Out of candidate genes near this significant genomic region, a mutant of a ribosomal gene (AT3G13882) exhibited slower growth and later flowering than a wild type under laboratory conditions. A no-choice assay with the turnip aphid,Lipaphis erysimi, found that aphids were unable to successfully establish on the mutant. These findings suggest the potential role of growth-related genes in altering herbivore abundance.

Frequency-dependent selection (FDS) is an evolutionary regime that can maintain or reduce polymorphisms. Despite the increasing availability of polymorphism data, few effective methods are available for estimating the gradient of FDS from the observed fitness components. We modeled the effects of genotype similarity on individual fitness to develop a selection gradient analysis of FDS. This modeling enabled us to estimate FDS by regressing fitness components on the genotype similarity among individuals. We detected known negative FDS on the visible polymorphism in a wild Arabidopsis and damselfly by applying this analysis to single-locus data. Further, we simulated genome-wide polymorphisms and fitness components to modify the single-locus analysis as a genome-wide association study (GWAS). The simulation showed that negative or positive FDS could be distinguished through the estimated effects of genotype similarity on simulated fitness. Moreover, we conducted the GWAS of the reproductive branch number in Arabidopsis thaliana and found that negative FDS was enriched among the top-associated polymorphisms of FDS. These results showed the potential applicability of the proposed method for FDS on both visible polymorphism and genome-wide polymorphisms. Overall, our study provides an effective method for selection gradient analysis to understand the maintenance or loss of polymorphism.

Frequency-dependent selection (FDS) drives an evolutionary regime that maintains or disrupts polymorphisms. Despite the increasing feasibility of genetic association studies on fitness components, there are a few methods to uncover the loci underlying FDS. Based on a simplified model of pairwise genotype-genotype interactions, we propose a linear regression that can infer FDS from observed fitness. The key idea behind our method is the inclusion of genotype similarity as a pseudo-trait in selection gradient analysis. Single-locus analysis of Arabidopsis and damselfly data could detect known negative FDS on visible polymorphism that followed Mendelian inheritance with complete dominance. By extending the single-locus analysis to genome-wide association study (GWAS), our simulations showed that the regression coefficient of genotype similarity can distinguish negative or positive FDS without confounding other forms of balancing selection. Field GWAS of the branch number further revealed that negative FDS, rather than positive FDS, was enriched among the top-scoring single nucleotide polymorphisms (SNPs) in Arabidopsis thaliana. These results showed the wide applicability of our method for FDS on both visible polymorphism and genome-wide SNPs. Our study provides an effective method for selection gradient analysis to understand the maintenance or loss of polymorphism.