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

Authors: SAMAYOA, LUIS FERNANDO - North Carolina State University; OLUKOLU, B - University Of Tennessee; YANG, C - University Of Wisconsin; CHEN, Q - University Of Wisconsin; STETTER, MARKUS - University Of Cologne; YORK, ALESSANDRA - University Of Wisconsin; SANCHEZ-GONZALEZ, JOSE DE JESUS - University Of Guadalajara; GLAUBITZ, JEFFREY - Cornell University; Bradbury, Peter; CINTA ROMAY, MARIA - Cornell University; SUN, QI - Cornell University; YANG, JINLIANG - University Of Nebraska; ROSS-IBARRA, JEFFREY - University Of California, Davis; Buckler, Edward - Ed; DOEBLEY, J - University Of Wisconsin; Holland, Jim - Jim

Submitted to: PLoS Genetics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/3/2021
Publication Date: 12/20/2021
Citation: Samayoa, L., Olukolu, B.A., Yang, C.J., Chen, Q., Stetter, M.G., York, A.M., Sanchez-Gonzalez, J., Glaubitz, J.C., Bradbury, P., Cinta Romay, M., Sun, Q., Yang, J., Ross-Ibarra, J., Buckler IV, E.S., Doebley, J.F., Holland, J.B. 2021. Domestication reshaped the genetic basis of inbreeding depression in a maize landrace compared to its wild relative, teosinte. PLoS Genetics. 2:1009797. https://doi.org/10.6084/m9.figshare.14750790.
DOI: https://doi.org/10.6084/m9.figshare.14750790

Interpretive Summary: 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.

Technical Abstract: 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 rare large-effect variation versus potentially more common 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 predicted from sequence data in the maize population. For many traits - and more commonly in maize - genetic variation among self-fertilized families was less than expected based on additive and dominance variance estimated in outcrossed families, suggesting that a negative covariance between additive and homozygous dominance effects limits the variation available to selection under partial inbreeding. We identified 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 recessive variation underlying inbreeding depression, with an additional contribution from rare larger-effect variants that was more important in teosinte but depleted in maize following to the domestication bottleneck. Purging associated with the maize domestication bottleneck may have selected against large effect variants, but polygenic load is harder to purge and segregating mutational burden increased in maize compared to teosinte.