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

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

^aDepartment of Crop and Soil Sciences, North Carolina State University, Raleigh, NC 27695 USA
^bDepartment of Crop and Soil Sciences, North Carolina State University, Raleigh, North Carolina, United States of America
^cDepartment of Entomology and Plant Pathology, University of Tennessee, Knoxville, Tennessee 37996 USA
^dDepartment of Entomology and Plant Pathology, University of Tennessee, Knoxville, Tennessee, United States of America
^eLaboratory of Genetics, University of Wisconsin – Madison, Madison, WI 53706 USA
^fLaboratory of Genetics, University of Wisconsin–Madison, Madison, Wisconsin, United States of America
^gInstitute for Plant Sciences and Center of Excellence on Plant Sciences, University of Cologne, Cologne 50674 Germany
^hInstitute for Plant Sciences and Center of Excellence on Plant Sciences, University of Cologne, Cologne, Germany
ⁱCentro Universitario de Ciencias Biológicas y Agropecuarias, Universidad de Guadalajara, Zapopan, Jalisco CP45110, Mexico
^jCentro Universitario de Ciencias Biológicas y Agropecuarias, Universidad de Guadalajara, Zapopan, Jalisco, México
^kInstitute of Biotechnology, Cornell University, Ithaca, NY 14853 USA
^lInstitute of Biotechnology, Cornell University, Ithaca, New York, United States of America
^mUS Department of Agriculture–Agricultural Research Service, Cornell University, Ithaca, NY 14853 USA
ⁿUS Department of Agriculture–Agricultural Research Service, Cornell University, Ithaca, New York, United States of America
^oDepartment of Agronomy and Horticulture, University of Nebraska-Lincoln, Lincoln, NE 68583 USA
^pDepartment of Agronomy and Horticulture, University of Nebraska-Lincoln, Lincoln, Nebraska, United States of America
^qDepartment of Evolution and Ecology, Center for Population Biology, and Genome Center, University of California, Davis, CA 95616 USA
^rDepartment of Evolution and Ecology, Center for Population Biology, and Genome Center, University of California, Davis, California, United States of America
^sUnited States Department of Agriculture – Agriculture Research Service, Raleigh, NC 27695 USA
^tUnited States Department of Agriculture–Agriculture Research Service, Raleigh, North Carolina, United States of America
✉Corresponding author

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 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.

TL;DRThis work 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, and identified quantitative trait loci representing large-effect rare variants carried by only a single parent, which were more important in teOSinte than maize. (Semantic Scholar)

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

Abstract

Plain-language summary

Discussion