The genomic impacts of drift and selection for hybrid performance in maize

TL;DR

This study investigates the genomic effects of long-term breeding selection in maize, revealing decreased genetic diversity, haplotype fixation, and complex selection signatures influenced by genetic drift.

Contribution

It provides the first detailed haplotype-level view of a historic maize breeding experiment, highlighting the impact of drift and selection on genome structure.

Findings

Genetic diversity within populations steadily decreases.

Extensive haplotype fixation occurs in pericentromeric regions.

Selection signatures are obscured by strong genetic drift.

Abstract

Modern maize breeding relies upon selection in inbreeding populations to improve the performance of cross-population hybrids. The United States Department of Agriculture - Agricultural Research Service reciprocal recurrent selection experiment between the Iowa Stiff Stalk Synthetic (BSSS) and the Iowa Corn Borer Synthetic No. 1 (BSCB1) populations represents one of the longest standing models of selection for hybrid performance. To investigate the genomic impact of this selection program, we used the Illumina MaizeSNP50 high-density SNP array to determine genotypes of progenitor lines and over 600 individuals across multiple cycles of selection. Consistent with previous research (Messmer et al., 1991; Labate et al., 1997; Hagdorn et al., 2003; Hinze et al., 2005), we found that genetic diversity within each population steadily decreases, with a corresponding increase in population structure. High marker density also enabled the first view of haplotype ancestry, fixation and recombination within this historic maize experiment. Extensive regions of haplotype fixation within each population are visible in the pericentromeric regions, where large blocks trace back to single founder inbreds. Simulation attributes most of the observed reduction in genetic diversity to genetic drift. Signatures of selection were difficult to observe in the background of this strong genetic drift, but heterozygosity in each population has fallen more than expected. Regions of haplotype fixation represent the most likely targets of selection, but as observed in other germplasm selected for hybrid performance (Feng et al., 2006), there is no overlap between the most likely targets of selection in the two populations. We discuss how this pattern is likely to occur during selection for hybrid performance, and how it poses challenges for dissecting the impacts of modern breeding and selection on the maize genome.