Negative frequency-dependent selection underlies overyielding through neighbor genotypic effects in Arabidopsis thaliana

Abstract

Negative frequency-dependent selection (FDS) can increase both genetic diversity and population-level mean fitness. While the dual consequence of negative FDS has long been theoretically recognized, its genomic basis remains unknown. To explore a genetic link between negative FDS and overyielding, I conducted a genome-wide association study (GWAS) of neighbor genotypic effects on the growth of 98 Arabidopsis thaliana genotypes. By incorporating neighbor genotypic similarity, my GWAS detected the most significant SNP on the fifth chromosome of A. thaliana, which was 6-kbp near a known locus responsible for indirect genetic effects. I found symmetric negative FDS on the most significant SNP, such that individual plants increased their biomass in the presence of neighbors with dissimilar alleles. I also observed overyielding in which a biallelic mixture of the most significant SNP showed a 3% increase in biomass compared to monoallelic conditions. Furthermore, I focused on the genomic region near the most significant SNP and found a signature of balancing selection near a negative regulator of ethylene responses SIRTUIN2. The present analysis uncovered a key locus linking balanced polymorphisms and overyielding in A. thaliana, showing a way to understand the maintenance of polymorphism and its positive impact on population productivity.