Domestication reshaped the genetic basis of inbreeding depression in a maize landrace compared to its wild relative, teosinte

Inbreeding depression is the reduction in fitness and vigor resulting from mating of close relatives observed in many plant and animal species. The extent to which the genetic load of mutations contributing to inbreeding depression is due to large-effect mutations versus variants with very small individual effects is unknown and may be affected by population history. We compared the effects of outcrossing and self-fertilization on 18 traits in a landrace population of maize, which underwent a population bottleneck during domestication, and a neighboring population of its wild relative teosinte. Inbreeding depression was greater in maize than teosinte for 15 of 18 traits, congruent with the greater segregating genetic load in the maize population that we predicted from sequence data. Parental breeding values were highly consistent between outcross and selfed offspring, indicating that additive effects determine most of the genetic value even in the presence of strong inbreeding depression. We developed a novel linkage scan to identify quantitative trait loci (QTL) representing large-effect rare variants carried by only a single parent, which were more important in teosinte than maize. Teosinte also carried more putative juvenile-acting lethal variants identified by segregation distortion. These results suggest a mixture of mostly polygenic, small-effect partially recessive effects in linkage disequilibrium underlying inbreeding depression, with an additional contribution from rare larger-effect variants that was more important in teosinte but depleted in maize following the domestication bottleneck. Purging associated with the maize domestication bottleneck may have selected against some large effect variants, but polygenic load is harder to purge and overall segregating mutational burden increased in maize compared to teosinte.
Author summary Inbreeding depression is the reduction in fitness and vigor resulting from mating of close relatives observed in many plant and animal species. Mating of close relatives increases the probability that an individual inherits two non-functioning mutations at the same gene, resulting in lower fitness of such matings. We do not know the extent to which inbreeding depression is due to mutations with large-effects versus small-effect polygenic variants. We compared the effects of outcrossing and self-fertilization on 18 traits in a landrace population of maize, which underwent a population bottleneck during domestication, and a neighboring population of its wild relative teosinte. Inbreeding depression was greater in maize than teosinte for 15 of 18 traits and we found that this was consistent with higher predicted ‘genetic load’ in maize based solely on the evolutionary conservation of the sequence variants observed in the population. We also mapped genome positions associated with inbreeding depression, identifying more and larger-effect genetic variants in teosinte than maize. These results suggest that during domestication, some of the rare large-effect variants in teosinte were bred out, but many genetic variants of small effects on inbreeding depression increased in frequency maize.