Crop populations derived from experimental crosses enable the genetic dissection of complex traits and support modern plant breeding. Among these, multi-parent populations now play a central role. By mixing and recombining the genomes of multiple founders, multi-parent populations combine many commonly sought beneficial properties of genetic mapping populations. For example, they have high power and resolution for mapping quantitative trait loci, high genetic diversity and minimal population structure. Many multi-parent populations have been constructed in crop species, and their inbred germplasm and associated phenotypic and genotypic data serve as enduring resources. Their utility has grown from being a tool for mapping quantitative trait loci to a means of providing germplasm for breeding programmes. Genomics approaches, including de novo genome assemblies and gene annotations for the population founders, have allowed the imputation of rich sequence information into the descendent population, expanding the breadth of research and breeding applications of multi-parent populations. Here, we report recent successes from crop multi-parent populations in crops. We also propose an ideal genotypic, phenotypic and germplasm ‘package’ that multi-parent populations should feature to optimise their use as powerful community resources for crop research, development and breeding.

Background: Selection has dramatically shaped genetic and phenotypic variation in bread wheat. We can assess the genomic basis of historical phenotypic changes, and the potential for future improvement, using experimental populations that attempt to undo selection through the randomizing effects of recombination. Results: We bred the NIAB Diverse MAGIC multi-parent population comprising over 500 recombinant inbred lines, descended from sixteen historical UK bread wheat varieties released between 1935 and 2004. We sequence the founders’ genes and promoters by capture, and the MAGIC population by low-coverage whole-genome sequencing. We impute 1.1 M high-quality SNPs that are over 99% concordant with array genotypes. Imputation accuracy only marginally improves when including the founders’ genomes as a haplotype reference panel. Despite capturing 73% of global wheat genetic polymorphism, 83% of genes cluster into no more than three haplotypes. We phenotype 47 agronomic traits over 2 years and map 136 genome-wide significant associations, concentrated at 42 genetic loci with large and often pleiotropic effects. Around half of these overlap known quantitative trait loci. Most traits exhibit extensive polygenicity, as revealed by multi-locus shrinkage modelling. Conclusions: Our results are consistent with a gene pool of low haplotypic diversity, containing few novel loci of large effect. Most past, and projected future, phenotypic changes arising from existing variation involve fine-scale shuffling of a few haplotypes to recombine dozens of polygenic alleles of small effect. Moreover, extensive pleiotropy means selection on one trait will have unintended consequences, exemplified by the negative trade-off between yield and protein content, unless selection and recombination can break unfavorable trait-trait associations.

Significance: Predominantly diploid organisms shape the extent to which their haploid gametes and gametophytes experience selection. Although animals are thought to experience only mild selection in the haploid stage, plants often experience strong haploid selection. When should parents limit exposure of gametes to haploid selection and when should they strengthen this selection? We develop mathematical models that consider the “selective arena” within which male gametes or gametophytes (sperm or pollen) compete for fertilization, examining how the intensity of this selective arena evolves when controlled by the mother or the father. These models predict substantial variation in the outcome, depending on whether mothers or fathers exert more control over the selective arena, with mothers often favoring stronger haploid selection than fathers.

Sex determination is remarkably dynamic; many taxa display shifts in the location of sex-determining loci or the evolution of entirely new sex-determining systems. Predominant theories for why we observe such transitions generally conclude that novel sex-determining systems are favoured by selection if they equalise the sex ratio or increase linkage with a locus that experiences different selection in males versus females. We use population genetic models to extend these theories in two ways: (1) We consider the dynamics of loci very tightly linked to the ancestral sex-determining loci, e.g., within the nonrecombining region of the ancestral sex chromosomes. Variation at such loci can favour the spread of new sex-determining systems in which the heterogametic sex changes (XY to ZW or ZW to XY) and the new sex-determining region is less closely linked (or even unlinked) to the locus under selection. (2) We consider selection upon haploid genotypes either during gametic competition (e.g., pollen competition) or meiosis (i.e., nonmendelian segregation), which can cause the zygotic sex ratio to become biased. Haploid selection can drive transitions between sex-determining systems without requiring selection to act differently in diploid males versus females. With haploid selection, we find that transitions between male and female heterogamety can evolve so that linkage with the sex-determining locus is either strengthened or weakened. Furthermore, we find that sex ratio biases may increase or decrease with the spread of new sex chromosomes, which implies that transitions between sex-determining systems cannot be simply predicted by selection to equalise the sex ratio. In fact, under many conditions, we find that transitions in sex determination are favoured equally strongly in cases in which the sex ratio bias increases or decreases. Overall, our models predict that sex determination systems should be highly dynamic, particularly when haploid selection is present, consistent with the evolutionary lability of this trait in many taxa. Systems of sex determination are strikingly diverse and labile in many clades. This poses the question: what drives transitions between sex-determining systems? Here, we use models to derive conditions under which new sex-determining systems spread. Prevailing views suggest that new sex-determining systems are favoured when they equalise the sex ratio and/or when they are more closely linked to genes that experience differential selection in males and females. Our models include selection upon haploid genotypes (meiotic drive or gametic competition), which biases the sex ratio and occurs differently in male and female gametes. Surprisingly, we find the two forces (selection to equalise the sex ratio and the benefits of hitchhiking alongside driven alleles that distort the sex ratio) will often be equally strong, and thus neither is sufficient to explain the spread of new sex-determining systems in every case. We also find that new sex-determining alleles can spread despite being less closely linked to selected loci, as long as initial linkage is tight or haploid selection is present. Our models therefore predict that loci in previously unexpected genomic locations and/or experiencing various types of selection (including haploid selection) can now be implicated as drivers of transitions between sex-determining systems.