Population genetics of maize domestication, adaptation, and improvement
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The domestication of maize ~10,000 years ago resulted in dramatic differentiation from its wild ancestor teosinte. Subsequently, maize spread rapidly across the Americas, adapting to a number of new environments. Beginning in the 20th century, maize has also been subjected to intensive artificial selection by breeders. Each of these periods of adaptation have left their mark on patterns of genetic diversity. I will discuss some of our recent work using population genetics to learn about the history and process of adaptation in maize.
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Population genetics of maize domestication, adaptation, and improvement
- 1. Maize Evolution J. Ross-Ibarra Introduction Domestication Origins Diversity Population genetics of maize domestication, adaptation, and improvement Adaptation Parallel Introgression Improvement US germplasm Iowa RRS Deleterious Conclusions Je↵rey Ross-Ibarra www.rilab.org @jrossibarra rossibarra February 5, 2014
- 2. Maize Evolution Lead Authors J. Ross-Ibarra Introduction UC Davis Domestication Origins Diversity Adaptation Parallel Introgression Improvement Sofiane Mezmouk US germplasm Iowa RRS Deleterious Matthew Hu↵ord Conclusions Joost van Heerwaarden Shohei Takuno U Copenhagen U Missouri Justin Gerke Rute Fonseca
- 3. Maize Evolution Acknowledgements J. Ross-Ibarra Introduction Domestication Origins Diversity Adaptation Parallel Introgression Improvement US germplasm Iowa RRS Deleterious Conclusions People • Ed Buckler (USDA) • Jer-Ming Chia (CSHL) • John Doebley (Wisconsin) • Jode Edwards (USDA) • Tom Gilbert (Copenhagen) Funding • Mike McMullen (USDA) • Tanja Pyh¨j¨rvi aa • Lauren Sagara • Nathan Springer (Minnesota) • Doreen Ware (USDA)
- 4. Maize Evolution J. Ross-Ibarra Introduction Domestication Origins Diversity Adaptation Parallel Introgression Improvement US germplasm Iowa RRS Deleterious Conclusions Maize evolutionary genetics
- 5. Maize Evolution J. Ross-Ibarra Introduction Domestication Origins Diversity Adaptation Parallel Introgression Improvement US germplasm Iowa RRS Deleterious Conclusions Maize evolutionary genetics
- 6. Maize Evolution Maize evolutionary genetics J. Ross-Ibarra Introduction Domestication Origins Diversity Adaptation Parallel Introgression Improvement Conclusions Selective Sweep Diversity US germplasm Iowa RRS Deleterious Genome Sequence
- 7. Maize Evolution Outline J. Ross-Ibarra Introduction Domestication Origins Diversity Adaptation 1 Domestication Geographic origins of maize domestication Impacts of selection on genomic diversity Parallel Introgression Improvement US germplasm Iowa RRS Deleterious Conclusions 2 Adaptation Parallel adaptation to new environments Adaptive introgression from wild relatives 3 Improvement Historical genomics of US maize Drift and selection in the Iowa RRS The role of deleterious alleles in maize 4 Conclusions
- 8. Maize Evolution Maize origins: single domestication J. Ross-Ibarra Introduction Domestication Origins Diversity Adaptation Parallel Introgression Improvement US germplasm Iowa RRS Deleterious Conclusions Sawers & Sanchez Leon 2011 Front. Genet. • Single domestication from lowland ssp. parviglumis
- 9. Maize Evolution Maize origins: single domestication J. Ross-Ibarra Introduction Domestication Origins Diversity Adaptation Parallel Introgression Improvement US germplasm Iowa RRS Deleterious Conclusions Sawers & Sanchez Leon 2011 Front. Genet. Matsuoka et al. 2002 PNAS • Single domestication from lowland ssp. parviglumis • Microsatellite data suggested oldest maize from highlands
- 10. Maize Evolution differences between lowland and highland maize in terms of heterozygosity and differentiation from parviglumis (Fig. S3). Structure analysis (21) of all Mexican accessions lends support for this magnitude of introgression (Fig. 2). The three subspecies form clearly separated clusters, but evidence of admixture is the West Mexico group as the most ancestral population (Fig. 3B). To mitigate the impact of introgression, we used a slightly modified approach that excludes both parviglumis and mexicana and calculates genetic drift with respect to ancestral frequencies inferred from domesticated maize alone. Because the genetic Highland landraces genetically similar to teosinte J. Ross-Ibarra Introduction Domestication Origins Diversity Adaptation Parallel Introgression Improvement US germplasm Iowa RRS Deleterious Conclusions Fig. 1. (A) Map of sampled maize accessions colored by genetic group. (B) First three genetic PCs of all sampled accessions. | • 1K SNPs from 1200 landraces across Americas van Heerwaarden et al. PNAS January 18, 2011 | vol. 108 | no. 3 | 1089 • PCA identifies genetic clusters and confirms highland maize most similar to teosinte van Heerwaarden et al. 2011 PNAS
- 11. Maize Evolution Modern maize originated in lowlands J. Ross-Ibarra Introduction Domestication 2500 2000 m 1500 1000 500 0 Origins Diversity Adaptation Parallel Introgression Improvement US germplasm Iowa RRS Deleterious Conclusions mexicana parviglumis Meso-American Lowland West Mexico Mex. Highland Fig. 2. (Lower) Bar plot of assignment values for the sample of Mexican accessions: Mexicana (red), parviglumis (green), and mays (blue). (Upper) The solid black line indicates the altitude for each sample. The dotted line marks the minimum altitude at which mexicana occurs. similarity of some of our maize groups violates the assumption of independent drift, we infer ancestral frequencies by averaging over estimates obtained for pairs of diverged maize groups and calculate drift of individual populations with respect to these frequencies. In contrast to previous results, this comparison identifies the West Mexico group as being most similar to the common domesticated ancestor, followed by the Mexican Highland and Meso-American Lowland groups (Fig. 3C). Moreover, splitting the West Mexico group into highland (>2,000 m) and lowland (<1,500 m) components reveals that the lowland West Mexico group is most similar to the inferred ancestral maize. Direct comparison of genetic drift among the lowland West Mexico, Mexican Highland, and each of the remaining eight clusters shows further that the lowland West Mexico group is significantly closer than the Mexican Highland group to the inferred ancestor of each triplet (Fig. S4). These results strongly suggest that maize from the western lowlands of Mexico is genetically most similar to the common ancestor of maize and is more closely related to other extant populations than is maize from the highlands of central Mexico. The ancestral position of the lowland West Mexico group is confirmed in a spatially explicit analysis of current allele frequencies in modern landraces, in which we mapped the moment estimator of F with respect to inferred ancestral allele frequencies. Mapping against allele frequencies observed in parviglumis (Fig. 4A) recapitulates earlier genetic results identifying highland maize as most similar to its wild ancestor (5). Points in the lower 0.05 quantile of F cluster in the highlands, with a mean altitude of 1,745 m. In contrast, mapping F with respect to inferred ancestral allele frequencies (Fig. 4B) identifies the lowest 0.05 quantile of F values in the lowlands of western Mexico, including the Balsas region and the region south of the Mexican highlands, resulting in an average altitude of 1,268 m; this analysis also clearly estimates higher values of F for maize in the Mexican highlands, particularly in areas of high inferred introgression from mexicana (Fig S5). Discussion Resolving the origins and spread of domesticated crops is a fascinating and challenging endeavor that requires the integration of botanical, archeological, and genetic evidence (26, 27, 28). Maize provides an exceptional opportunity for studying the processes of domestication and subsequent diffusion because of the wealth of existing archaeobotanical data, germplasm accessions, and molecular markers. The contradiction between evidence supporting the earliest cultivation in the lowlands and the genetically ancestral position of Mexican Highland maize is therefore of particular interest. The disagreement is important, because the adaptive differences between highland and lowland maize are profound (14, 29). In other crops, uncertainty about • Identifying gene flow from ssp. mexicana van Heerwaarden et al. 2011 PNAS
- 12. Maize Evolution Modern maize originated in lowlands J. Ross-Ibarra Introduction Domestication 2500 2000 m 1500 1000 500 0 Origins Diversity Adaptation Parallel Introgression Improvement US germplasm Iowa RRS Deleterious Conclusions mexicana parviglumis Meso-American Lowland West Mexico Mex. Highland Fig. 2. (Lower) Bar plot of assignment values for the sample of Mexican accessions: Mexicana (red), parviglumis (green), and mays (blue). (Upper) The solid black line indicates the altitude for each sample. The dotted line marks the minimum altitude at which mexicana occurs. similarity of some of our maize groups violates the assumption of independent drift, we infer ancestral frequencies by averaging over estimates obtained for pairs of diverged maize groups and calculate drift of individual populations with respect to these frequencies. In contrast to previous results, this comparison identifies the West Mexico group as being most similar to the common domesticated ancestor, followed by the Mexican Highland and Meso-American Lowland groups (Fig. 3C). Moreover, splitting the West Mexico group into highland (>2,000 m) and lowland (<1,500 m) components reveals that the lowland West Mexico group is most similar to the inferred ancestral maize. Direct comparison of genetic drift among the lowland West Mexico, Mexican Highland, and each of the remaining eight clusters shows further that the lowland West Mexico group is significantly closer than the Mexican Highland group to the inferred ancestor of each triplet (Fig. S4). These results strongly suggest that maize from the western lowlands of Mexico is genetically most similar to the common ancestor of maize and is more closely related to other extant populations than is maize from the highlands of central Mexico. The ancestral position of the lowland West Mexico group is confirmed in a spatially explicit analysis of current allele frequencies in modern landraces, in which we mapped the moment estimator of F with respect to inferred ancestral allele frequencies. Mapping against allele frequencies observed in parviglumis (Fig. 4A) recapitulates earlier genetic results identifying highland maize as most similar to its wild ancestor (5). Points in the lower 0.05 quantile of F cluster in the highlands, with a mean altitude of 1,745 m. In contrast, mapping F with respect to inferred ancestral allele frequencies (Fig. 4B) identifies the lowest 0.05 quantile of F values in the lowlands of western Mexico, including the Balsas region and the region south of the Mexican highlands, resulting in an average altitude of 1,268 m; this analysis also clearly estimates higher values of F for maize in the Mexican highlands, particularly in areas of high inferred introgression from mexicana (Fig S5). Discussion Resolving the origins and spread of domesticated crops is a fascinating and challenging endeavor that requires the integration of botanical, archeological, and genetic evidence (26, 27, 28). Maize provides an exceptional opportunity for studying the processes of domestication and subsequent diffusion because of the wealth of existing archaeobotanical data, germplasm accessions, and molecular markers. The contradiction between evidence supporting the earliest cultivation in the lowlands and the genetically ancestral position of Mexican Highland maize is therefore of particular interest. The disagreement is important, because the adaptive differences between highland and lowland maize are profound (14, 29). In other crops, uncertainty about • Identifying gene flow from ssp. mexicana • Ancestral reconstruction identifies lowland origin van Heerwaarden et al. 2011 PNAS
- 13. Maize Evolution Allele frequencies reveal bottleneck, growth J. Ross-Ibarra Introduction Domestication Origins Diversity Adaptation Parallel Introgression Improvement US germplasm Iowa RRS Deleterious Conclusions • 30X landrace genome estimates population size Vince Bu↵alo, In Prep
- 14. Maize Evolution Allele frequencies reveal bottleneck, growth J. Ross-Ibarra Introduction Domestication Origins Diversity Adaptation Parallel Introgression Improvement US germplasm Iowa RRS Deleterious Conclusions Rare (= =) Common • 30X landrace genome estimates population size • Genic regions reflect bottleneck loss of rare alleles • Nongenic regions of maize show new mutations (⇡ 40% unique) due to exponential growth Vince Bu↵alo, In Prep
- 15. Maize Evolution Genome sequencing identifies changes in diversity J. Ross-Ibarra Introduction Domestication Origins Diversity Adaptation Parallel Introgression Improvement US germplasm Iowa RRS Deleterious Conclusions • Full genome sequencing to ⇡ 5x of > 100 temperate and tropical inbreds, landraces, and teosinte • Maize retained most diversity through both domestication (⇡ 80%) and improvement (> 95%) Hu↵ord et al. 2012 Nature Genetics; Chia et al. 2012 Nature Genetics
- 16. Maize Evolution Genome sequencing identifies changes in diversity J. Ross-Ibarra Introduction Domestication Origins Diversity Adaptation Parallel Introgression Improvement US germplasm Iowa RRS Deleterious Conclusions • Full genome sequencing to ⇡ 5x of > 100 temperate and tropical inbreds, landraces, and teosinte • Maize retained most diversity through both domestication (⇡ 80%) and improvement (> 95%) Hu↵ord et al. 2012 Nature Genetics; Chia et al. 2012 Nature Genetics
- 17. Maize Evolution Strong selection, including regulatory regions J. Ross-Ibarra Introduction Domestication Origins Diversity Adaptation Parallel Introgression Improvement US germplasm Iowa RRS Deleterious Conclusions • Selection stronger during domestication (s ⇡ 1.5%) • ⇡ 18% domestication genes show continued selection Hu↵ord et al. 2012 Nature Genetics; Swanson-Wagner et al. 2012 PNAS
- 18. Maize Evolution Strong selection, including regulatory regions J. Ross-Ibarra GRMZM2G136072 Introduction Domestication Origins Diversity Adaptation Parallel Introgression Improvement US germplasm Iowa RRS Deleterious Conclusions • Selection stronger during domestication (s ⇡ 1.5%) • ⇡ 18% domestication genes show continued selection • 6 10% of selected regions contain no genes • Expression suggests selection on regulatory sequence Hu↵ord et al. 2012 Nature Genetics; Swanson-Wagner et al. 2012 PNAS
- 19. Domestication candidate genes J. Ross-Ibarra Domestication Origins Diversity Adaptation US germplasm Iowa RRS Deleterious • 484 selected regions identified • Majority of show stronger selection than tb1 or tga1 Hu↵ord et al. 2012 Nature Genetics Conclusions Parallel Introgression Improvement Introduction Maize Evolution
- 20. Maize Evolution Outline J. Ross-Ibarra Introduction Domestication Origins Diversity Adaptation 1 Domestication Geographic origins of maize domestication Impacts of selection on genomic diversity Parallel Introgression Improvement US germplasm Iowa RRS Deleterious Conclusions 2 Adaptation Parallel adaptation to new environments Adaptive introgression from wild relatives 3 Improvement Historical genomics of US maize Drift and selection in the Iowa RRS The role of deleterious alleles in maize 4 Conclusions
- 21. Maize Evolution Repeated adaptation to highlands J. Ross-Ibarra Introduction Highland SW US 4,000BP Domestication Origins Diversity Adaptation Parallel Introgression Highland Mexico 6,000BP Improvement US germplasm Iowa RRS Deleterious Lowland S. America 6,000BP Conclusions Domestication 9,000BP Highland S. America 4,000BP Fonseca et al. in prep.
- 22. Maize Evolution Parallel phenotypes in S. America and Mexico J. Ross-Ibarra Introduction Domestication Origins Diversity Adaptation Parallel Introgression Improvement US germplasm Iowa RRS Deleterious Conclusions Barthakur 1974 Int. J. Biometeor.
- 23. Maize Evolution Genetic data confirm independent origin J. Ross-Ibarra Introduction Domestication Origins Diversity Adaptation Parallel Introgression Improvement US germplasm Iowa RRS Deleterious Conclusions • GBS data from Mexico and S. America landraces • Independent origins, little admixture between highlands Takuno et al. in prep
- 24. Maize Evolution Distinct genetic architecture of highland adaptation J. Ross-Ibarra Introduction Domestication Origins Diversity Adaptation Parallel Introgression Improvement US germplasm Iowa RRS Deleterious Conclusions • FST identifies many candidate SNPs, < 5% shared • Most (> 80%) found segregating in lowland samples Takuno et al. in prep
- 25. Maize Evolution Distinct genetic architecture of highland adaptation J. Ross-Ibarra Introduction Domestication Origins Diversity Adaptation Parallel Introgression Improvement US germplasm Iowa RRS Deleterious Conclusions Yi et al. 2010 Science • FST identifies many candidate SNPs, < 5% shared • Most (> 80%) found segregating in lowland samples • Contrast to highland adaptation in humans Takuno et al. in prep
- 26. Maize Evolution Repeated adaptation in maize and teosinte J. Ross-Ibarra Introduction maize mexicana Domestication Origins Diversity Adaptation Parallel Introgression Improvement US germplasm Iowa RRS Deleterious Conclusions Photo: Pesach Lubinsky • Colonization of highland Mexico brought maize into sympatry with highland ssp. mexicana Ross-Ibarra et al. 2009 Genetics
- 27. Maize Evolution Repeated adaptation in maize and teosinte J. Ross-Ibarra Introduction maize mexicana mexicana parviglumis Domestication Origins Diversity Adaptation Parallel Introgression Improvement US germplasm Iowa RRS Deleterious Conclusions Photo: Pesach Lubinsky Latuer et al. 2004 Genetics • Colonization of highland Mexico brought maize into sympatry with highland ssp. mexicana • mexicana and parviglumis diverged ⇡ 60, 000BP Ross-Ibarra et al. 2009 Genetics
- 28. San Pedro Maize Evolution Widespread introgression from mexicana Ixtlan J. Ross-Ibarra Introduction El Porvenir Domestication Opopeo Origins Diversity Santa Clara Adaptation Nabogame Parallel Introgression Puruandiro Improvement Xochimilco US germplasm Iowa RRS Deleterious Tenango del Aire San Pedro Ixtlan Conclusions Allopatric Chromosome 4: Maize • SNP genotyping 8 landraces sympatric with mexicana El Porvenir Opopeo Santa Clara Nabogame Puruandiro Xochimilco Tenango del Aire San Pedro Ixtlan • 6 genomic regions with mexicana haplotypes introgressed HAPMIX in multiple landraces at high frequencies STRUCTURE • No consistent introgression from maize into mexicana Hu↵ord et al. 2013 PLoS Genetics
- 29. Maize Evolution Introgressed regions overlap with teosinte QTL J. Ross-Ibarra Introduction Domestication Origins Diversity Adaptation Parallel Introgression Improvement US germplasm Iowa RRS Deleterious Conclusions Hu↵ord et al. 2013 PLoS Genetics
- 30. Maize Evolution Adaptive introgression from mexicana J. Ross-Ibarra Introduction Domestication Origins Diversity Adaptation Parallel Introgression Improvement US germplasm Iowa RRS Deleterious Conclusions • Landraces with introgression show mexicana-like phenotype and superior growth in cold temperatures Hu↵ord et al. 2013 PLoS Genetics
- 31. Maize Evolution Adaptive introgression from mexicana J. Ross-Ibarra Introduction Domestication Origins Diversity Adaptation Parallel Introgression Improvement US germplasm Iowa RRS Deleterious Conclusions • Landraces with introgression show mexicana-like phenotype and superior growth in cold temperatures • Maize adapted to highland environments in Mexico via gene flow from mexicana Hu↵ord et al. 2013 PLoS Genetics
- 32. Maize Evolution Outline J. Ross-Ibarra Introduction Domestication Origins Diversity Adaptation 1 Domestication Geographic origins of maize domestication Impacts of selection on genomic diversity Parallel Introgression Improvement US germplasm Iowa RRS Deleterious Conclusions 2 Adaptation Parallel adaptation to new environments Adaptive introgression from wild relatives 3 Improvement Historical genomics of US maize Drift and selection in the Iowa RRS The role of deleterious alleles in maize 4 Conclusions
- 33. Maize Evolution Historical genomics of US maize J. Ross-Ibarra Introduction Domestication Origins Diversity Adaptation Parallel Introgression Improvement US germplasm Iowa RRS Deleterious Conclusions • SNP genotyping of 400 historical landraces and inbreds • Track allele frequencies • Estimate genome-wide ancestry using identity by state
- 34. Maize Evolution Genetic structure and diversity of US maize J. Ross-Ibarra Introduction Domestication Origins Diversity Adaptation Parallel Introgression Improvement US germplasm Iowa RRS Deleterious Conclusions • Increasing structure over time mirrors development of heterotic groups • Number and diversity of ancestors decreases over time van Heerwaarden et al. 2012 PNAS
- 35. Maize Evolution Selection on quantitative traits J. Ross-Ibarra Introduction Domestication Origins Diversity Adaptation Parallel Introgression Improvement AGRICULTURAL SCIENCES US germplasm Iowa RRS Deleterious Conclusions Fig. 3. Evidence for directional selection (Top), basal ancestry distortion (Middle), and ancestral haplotype diversity (Bottom) across the genome. Colors indicate the separate chromosomes with red vertical lines marking the centromeres. Green dashed horizontal line marks the 99th percentile of Bayes factors; purple dashed horizontal lines indicate median values of ancestry distortion and effective number of basal ancestors. Black vertical ticks mark selected features. Gray dots mark candidate SNPs. Black circles mark candidates that coincide with sites of low ancestral diversity. • Time GWA reveals SNPs selected across breeding pools • Frequency, diversity suggest Compared with the dramatic shifts in ancestry, directional selection on common alleles of Discussion The genomics of breeding history is of great importance to understanding the genetic basis of crop improvement and is instrumental to the identification of molecular targets of artificial selection. The current state of marker technology has granted us an unprecedented look across eight decades of breeding and selection, providing insight into historical developments in di- selection has had limited effect on the genome, with only 5% of SNPs showing some evidence of consistent selection. Candidate sites, apart from a slight reduction in ancestral diversity, do not deviate meaningfully from genome-wide patterns of haplotype length and ancestry. A potential caveat regarding this observation is that our selection scan is most sensitive to cumulative small e↵ect at quantitative traits van Heerwaarden et al. 2012 PNAS
- 36. Maize Evolution Ancestry, not selection, drives diversity J. Ross-Ibarra Introduction Domestication Origins Diversity Adaptation Parallel Introgression Improvement AGRICULTURAL SCIENCES US germplasm Iowa RRS Deleterious Conclusions Fig. 3. Evidence for directional selection (Top), basal ancestry distortion (Middle), and ancestral haplotype diversity (Bottom) across the genome. Colors indicate the separate chromosomes with red vertical lines marking the centromeres. Green dashed horizontal line marks the 99th percentile of Bayes factors; purple dashed horizontal lines indicate median values of ancestry distortion and effective number of basal ancestors. Black vertical ticks mark selected features. Gray dots mark candidate SNPs. Black circles mark candidates that coincide with sites of low ancestral diversity. • No deviation from genome-wide ancestry at selected sites Compared diversity in ancestral Discussion • Unusual breeding history is of great importance to un- selection has had limiteddramaticonshiftsin ancestry, only 5% of lines ancestry instead reflects with the effect the genome, with directional The genomics of derstanding the genetic basis of crop improvement and is instrumental to the identification of molecular targets of artificial selection. The current state of marker technology has granted us an unprecedented look across eight decades of breeding and selection, providing insight into historical developments in di- van Heerwaarden et al. 2012 PNAS SNPs showing some evidence of consistent selection. Candidate sites, apart from a slight reduction in ancestral diversity, do not deviate meaningfully from genome-wide patterns of haplotype length and ancestry. A potential caveat regarding this observation is that our selection scan is most sensitive to cumulative
- 37. Popular lines do not show superior genotypes J. Ross-Ibarra Origins Diversity Adaptation Parallel Introgression Improvement US germplasm Iowa RRS Deleterious Conclusions log10(ancestry at favorable alleles) Domestication WF9 MO1W -4.0 -3.5 -3.0 -2.5 -2.0 -1.5 -1.0 Introduction relation between enrichment for favorable alleles in individual era 1 lines and genome-wide ancestry ancestral overrepresentation of individual era 1 lines at favorable alleles enrichment for favorable alleles 0 5 10 Maize Evolution -3.5 -3.0 -2.5 -2.0 -1.5 -1.0 log10(genome-wide ancestry) H49 W182B W22 OH43 I205 B37 CI187-2 C103 B14 -5 -4 -3 -2 -1 0 log10(genome-wide ancestry) Fig. 4. Analysis of disproportionate ancestral contributions of individual era 1 lines to favorable alleles in era 3. Left: Overrepresentation of individual era 1 lines in the ancestry of favorable alleles, estimated by plotting the average ancestry proportion at favorable alleles against the genome-wide proportion. Right: Enrichment (as defined by the log probability ratio (LPR) with respect to noncandidate SNP) of favorable alleles in era 1 lines as a function of their average ancestral contribution to era 3. Black dotted lines represent the 1:1 diagonal and 0 horizontal, respectively. Gray dotted lines are regression lines (slope/r2: 1.15/0.85 and −0.1/0.00). Line names on the Right are shown for lines with LPR values higher than 4 or ancestry proportion above 0.03. Labels in boldface mark breeding lines of known historic popularity. • No over-representation of early inbreds at selected sites The genomic signature of selection is informative of the genetic architecture of breeding progress. Two issues of obvious interest are the selective importance of rare alleles of large effect and the contribution of dominant ancestors with superior multilocus genotypes. The infrequent occurrence of rare ancestral contributors and absence of extended haplotypes at candidate loci favor a model of selection on common variants rather than one of strong selective sweeps (26, 27), and we find no evidence of the long-term success of specific lines being determined by their multilocus genotype. This being said, the exceptionally favorable genotypes observed for some era 1 inbreds suggests that selection of outstanding lines may have occurred, albeit with limited effect on future genomic composition. In all, our results suggest that genetic gain achieved by plant breeding has been a complex process, involving a steady accumulation of changes at multiple loci (28), combined with heterosis due to differentiation of breeding pools (29). We thereby support the notion that selected traits of agronomic importance are predominantly quantitative in nature (30), with relatively few dominant contributions from individual alleles or lines. It will therefore be interesting to see whether our candidates prove van Heerwaarden et al. 2012 PNAS For each accession, DNA was extracted by a standard cetyltrimethyl ammonium bromide (CTAB) protocol (31) for genotyping on the Illumina MaizeSNP50 Genotyping BeadChip platform using the clustering algorithm of the GenomeStudio Genotyping Module v1.0 (Illumina). Of the total of 56,110 markers contained on the chip, 45,997 polymorphic SNPs were genotyped successfully with less than 10% missing data for use in subsequent analysis. SNPs were of diverse origins and discovery schemes. We evaluated the effects of ascertainment by comparing results for 33,575 SNPs derived from more diverse discovery panels to 12,422 SNPs that were discovered between the advanced public lines B73 and Mo17. Effects on differentiation and selection inference were found to be statistically significant but modest (SI Text). Diversity, Linkage, and Ancestry Analysis. Diversity analyses followed (32, 33). Briefly, PCA was performed on normalized genotype matrices and the number of significant eigenvalues determined by comparison with a Tracy– Widom (TW) distribution (18). Genotypes were assigned to k groups by Ward clustering on the Euclidean distance calculated from the k −1 significant PCs. PCA-based clustering into groups was done separately for each era. To improve clustering within era 0, Corn Belt Dents were analyzed separately from Northern Flints and a divergent group containing a popcorn and a Cherokee
- 38. Popular lines do not show superior genotypes J. Ross-Ibarra Improvement US germplasm Iowa RRS Deleterious Conclusions -3.5 -3.0 -2.5 -3.5 -2.0 -3.0 -1.5 -2.5 -1.0 -2.0 -1.5 -1.0 -5 log10(genome-wide ancestry) log10(genome-wide ancestry) enrichment for favorable alleles 0 5 10 Parallel Introgression WF9 MO1W MO1W enrichment for favorable alleles 0 5 10 Adaptation log10(ancestry at favorable alleles) Origins Diversity log10(ancestry at favorable alleles) Domestication -4.0 -3.5 -3.0 -2.5 -2.0 -1.5 -1.0 Introduction relation between enrichment for ancestral overrepresentation of individual era 1 of individual era 1 relation between enrichment for favorable alleles favorable alleles ancestral overrepresentation lines lines in individual era 1 lines and genome-wide and genome-wide ancestry in individual era 1 lines ancestry at favorable alleles favorable alleles at -4.0 -3.5 -3.0 -2.5 -2.0 -1.5 -1.0 Maize Evolution -4 H49 W182B W22 WF9 H49 W182B OH43W22 I205 OH43 I205 B37 -3 -5 -2 -4 B37 CI187-2 C103 B14 CI187-2 C103 B14 -1 -3 0 -2 -1 0 log10(genome-wide ancestry) log10(genome-wide ancestry) Fig. 4. Analysis of disproportionate ancestral contributions of individual era 1 lines to favorable alleles in erafavorable alleles in era 3. Left: Overrepresentation of individual era 1 Fig. 4. Analysis of disproportionate ancestral contributions of individual era 1 lines to 3. Left: Overrepresentation of individual era 1 lines in the ancestry of favorable alleles, estimated by plotting estimated by ancestry proportion atancestry proportion at favorable alleles against the genome-wide proportion. lines in the ancestry of favorable alleles, the average plotting the average favorable alleles against the genome-wide proportion. Right: Enrichment (as defined by the log(as defined by the log probability ratio noncandidate SNP) to noncandidate SNP) of favorable alleles in era 1 their as a function of their Right: Enrichment probability ratio (LPR) with respect to (LPR) with respect of favorable alleles in era 1 lines as a function of lines average ancestral contribution ancestral contribution to erarepresentdotted lines represent 0 horizontal, respectively. Gray dotted lines are regression lines are regression lines average to era 3. Black dotted lines 3. Black the 1:1 diagonal and the 1:1 diagonal and 0 horizontal, respectively. Gray dotted lines 2 (slope/r : 1.15/0.85 and −0.1/0.00). Line names−0.1/0.00). Line names onfor lines with LPR values higher than 4 or ancestry proportionor ancestry proportion above 0.03. Labels in (slope/r2: 1.15/0.85 and on the Right are shown the Right are shown for lines with LPR values higher than 4 above 0.03. Labels in boldface mark breeding lines of known historic popularity. boldface mark breeding lines of known historic popularity. • No over-representation of early inbreds at selected sites • Early inbreds contributing most to ancestry are not enriched for beneficial alleles For each accession, DNA was extracted byDNA was extracted by a standard cetyltrimethyl amFor each accession, a standard cetyltrimethyl amThe genomic signature genomic signature of selectionthe informative of the geThe of selection is informative of is gemonium bromide monium bromide for genotyping (31) for genotyping on the Illumina netic architecture of breeding progress. breeding progress. Two issues of obvious (CTAB) protocol (31) (CTAB) protocol on the Illumina netic architecture of Two issues of obvious MaizeSNP50 Genotyping BeadChip Genotyping BeadChip platform using the clustering algorithm MaizeSNP50 platform using the clustering algorithm interest are the selective importance of rare importance of rare alleles of large effect interest are the selective alleles of large effect ofsuperior multhe GenomeStudio of the GenomeStudiov1.0 (Illumina). Of thev1.0 (Illumina). Of the total of Genotyping Module Genotyping Module total of and the contribution ofthe contribution of dominant ancestors with and dominant ancestors with superior mul56,110 the chip, 45,997 polymorphic SNPs were gentilocus genotypes. tilocus genotypes. The infrequent occurrence of56,110 markers contained on markers contained on the chip, 45,997 polymorphic SNPs were genThe infrequent occurrence of rare ancestral rare ancestral otyped successfully otyped successfully with data for use missing data contributors and absence of extended haplotypes at candidate contributors and absence of extended haplotypes at candidate with less than 10% missingless than 10%in subsequent for use in subsequent analysis. SNPs were diverse SNPs were discovery origins and evaluated loci favor a model lociselection model of selection onrather than of favor a on common variants common variants rather than of analysis.origins and of diverse schemes. Wediscovery schemes. We evaluated the effects of ascertainment by 33,575 SNPs derived one of strong selective sweeps (26, 27), and we find no evidence find no evidence one of strong selective sweeps (26, 27), and we the effects of ascertainment by comparing results for comparing results for 33,575 SNPs derived from more diverse discovery that to 12,422 SNPs of the long-term success long-term success of specific lines by of the of specific lines being determined being from more diverse discovery panels to 12,422 SNPspanels were discovered that were discovered determined by between the advanced public lines B73 and Mo17. Effects B73differentiation between the advanced public lines on and Mo17. Effects on differentiation their multilocus genotype. This being said, the exceptionally fa- exceptionally fatheir multilocus genotype. This being said, the and selection inference were found to be statistically significant statistically significant but modest and selection inference were found to be but modest vorable genotypes observed for some observed for some era that vorable genotypes era 1 inbreds suggests 1 inbreds Text). suggests that (SI (SI Text). selection of outstanding lines may have occurred, albeit with selection of outstanding lines may have occurred, albeit with limited effect on future genomic on future genomic composition. Diversity, Linkage, and Diversity, Analysis. Diversity analyses followed (32, analyses followed (32, 33). limited effect composition. Ancestry Linkage, and Ancestry Analysis. Diversity 33). In all, our results suggest our results suggestachieved by plant achieved PCAplant performed PCAnormalized genotype normalized genotype matrices and the In all, that genetic gain that genetic gain Briefly, by was Briefly, on was performed on matrices and the breeding has been breeding has been a involving a steady involving number of significant number of significant eigenvalues determined by comparison with a Tracy– a complex process, complex process, accua steady accueigenvalues determined by comparison with a Tracy– mulation of changes at multiple loci (28), combined with hetermulation of changes at multiple loci (28), combined with heterWidom (TW) distribution (18). Genotypes were assigned to k groups by Ward to k groups by Ward Widom (TW) distribution (18). Genotypes were assigned osis due to differentiation of breeding pools of breeding pools (29). We thereby osis due to differentiation (29). We thereby clustering on the Euclidean distance the Euclidean distance−1 significant PCs. k −1 significant PCs. clustering on calculated from the k calculated from the support the notion support the notion that selected traits of agronomic importance into groups clustering into groupsfor each era. To im- for each era. To imthat selected traits of agronomic importance PCA-based clustering PCA-based was done separately was done separately are predominantly quantitative in nature (30), within nature (30), with relatively few are predominantly quantitative relatively few prove clustering within era 0,clustering within were analyzed separately from prove Corn Belt Dents era 0, Corn Belt Dents were analyzed separately from dominant contributions fromcontributions from or lines. It alleles or lines.Flints and a divergent groupand a divergent group and a Cherokee dominant individual alleles individual will It will Northern Northern Flints containing a popcorn containing a popcorn and a Cherokee therefore be interesting to see interesting to candidates prove candidates prove therefore be whether our see whether our van Heerwaarden et al. 2012 PNAS
- 39. Maize Evolution Selection in the Iowa RRS J. Ross-Ibarra Introduction Domestication Origins Diversity Adaptation Parallel Introgression Improvement US germplasm Iowa RRS Deleterious Conclusions • BSSS, BSCB1 selected for hybrid yield and agronomics
- 40. Maize Evolution Selection in the Iowa RRS J. Ross-Ibarra Introduction Domestication Origins Diversity Adaptation Parallel Introgression Improvement US germplasm Iowa RRS Deleterious Conclusions • BSSS, BSCB1 selected for hybrid yield and agronomics • SNP genotyping of founders and plants from 5 cycles • Allele frequency divergence mostly due to genetic drift Gerke et al. In Review
- 41. Maize Evolution No overlap in selection suggests complementation J. Ross-Ibarra Introduction Domestication Origins Diversity Adaptation Parallel Introgression Improvement US germplasm Iowa RRS Deleterious Conclusions Gerke et al. In Review
- 42. Maize Evolution No overlap in selection suggests complementation J. Ross-Ibarra Introduction Domestication Origins Diversity Adaptation Parallel Introgression Improvement US germplasm Iowa RRS Deleterious Conclusions Gerke et al. In Review
- 43. Maize Evolution Many new mutations, most deleterious J. Ross-Ibarra Introduction Domestication Origins Diversity Adaptation Parallel Introgression Improvement US germplasm Iowa RRS Deleterious Conclusions Jones 1924 Genetics Lohmueller 2013 arXiv • ⇡90 mutations per meiosis, > 80% deleterious • Population growth increases rare deleterious variants and these explain a larger proportion of VA • GWAS has low power to detect rare deleterious variants
- 44. Maize Evolution Computational prediction of deleterious alleles J. Ross-Ibarra Introduction Domestication Origins Diversity Adaptation Parallel Introgression Improvement US germplasm Iowa RRS Deleterious Conclusions • Published GBS, heterosis data of maize 282 population • A priori identify putatively deleterious alleles from conservation and physicochemical properties • Deleterious nonsynonymous at lower frequencies than nondeleterious Mezmouk & Ross-Ibarra 2014 G3
- 45. Maize Evolution Constraint; no evidence of positive selection J. Ross-Ibarra Introduction 0.5 Domestication Origins Diversity 0.4 Adaptation Improvement US germplasm Iowa RRS Deleterious del 0.3 KN KS Parallel Introgression Deleterious None 0.2 0.1 Conclusions NotC C 0.0 • Few of high-frequency deleterious alleles show significant signals of selection • Genes with del. SNPs show lower constraint (higher KN ) KS Mezmouk & Ross-Ibarra 2014 G3; Hu↵ord et al. 2012 Nature Genetics
- 46. Maize Evolution Deleterious allele frequencies consistent with BPH J. Ross-Ibarra Introduction Domestication Origins Diversity Adaptation Parallel Introgression Improvement US germplasm Iowa RRS Deleterious Conclusions • BPH increases with distance from B73 tester • Significant BPH even among sti↵-stalk lines Mezmouk & Ross-Ibarra 2014 G3
- 47. Maize Evolution Deleterious allele frequencies consistent with BPH J. Ross-Ibarra Introduction Domestication Origins Diversity Adaptation Parallel Introgression Improvement US germplasm Iowa RRS Deleterious Conclusions • BPH increases with distance from B73 tester • Significant BPH even among sti↵-stalk lines Mezmouk & Ross-Ibarra 2014 G3
- 48. Maize Evolution Heterosis GWA genes enriched for deleterious alleles J. Ross-Ibarra Introduction Domestication Origins Diversity Adaptation Parallel Introgression Improvement US germplasm Iowa RRS Deleterious Conclusions • No enrichment for individual deleterious SNPs (low power) • Genes associated with heterosis (for all traits) are enriched in deleterious alleles Mezmouk & Ross-Ibarra 2014 G3
- 49. Maize Evolution Conclusions J. Ross-Ibarra Introduction Domestication Origins Diversity Adaptation Parallel Introgression Improvement US germplasm Iowa RRS Deleterious Conclusions • Population genetic analyses are allowing clarification of maize origins and e↵ects of selection on maize genome. • Maize adaptation to new environments has taken multiple distinct routes, including utilizing genes from wild relatives. • Genetic drift and selection on common variants appears to have dominated US maize germplasm. • Patterns of complementation and frequencies of deleterious alleles support a simple dominance model of heterosis.
- 50. Maize Evolution Improvement candidate genes J. Ross-Ibarra • 695 selected regions identified Hu↵ord et al. 2012 Nature Genetics
- 51. Maize Evolution Selection on gene expression J. Ross-Ibarra Expression changes Directional change Tissue Specificity Dominance in crosses Domestication yes no no Improvement no yes yes • Expression at > 18, 000 genes in both maize and teosinte • Domestication directly acted on candidate gene expression • Improvement worked with highly expressed genes • Modern breeding selected for dominance in expression Hu↵ord et al. 2012 Nature Genetics; Swanson-Wagner et al. 2012 PNAS
- 52. Maize Evolution Repeated evolution at grassy tillers J. Ross-Ibarra • Cloned gt1 as gene underlying QTL for prolificacy • Selection on di↵erent parts of gene: A) Temperate zones: selection on 5’ enhancer region B) Tropical zones: selection on 3’ UTR Wills et al. 2013 PLoS Genetics
- 53. Maize Evolution Consistent with QTL for heterosis J. Ross-Ibarra • QTL for heterosis enriched in centromeric regions1 1 Lari`pe et al. 2012 Genetics e
- 54. Maize Evolution Consistent with change in inbred and hybrid yield? GENETIC PROGRESS IN YIELD OF U.S. MAIZE 199 J. Ross-Ibarra 68 alleles from 98 SSR loci distributed or the historical series of widely grown d on patterns of change in allele fredes. Number of alleles per group is om DUVICK et al. (2004a). Copyright © ns, Inc. This material is used by permis, Inc. FIGURE 7 - Yields of single crosses (SX) and their inbred parent • Selectionmeans high recombination regions improve inbreds? in (MP), and heterosis as SX – MP. Single-cross pedigrees are based on heterotic inbred combinations in the Era hybrids during the blocks 1930s through 1980s, 12 inbreds and six single • Haplotype six decades, in low recombination maintain crosses per decade. Means of trials grown in three locations in heterosis?2 and two locations in 1993 at three densities (30, 54, and 79 1992 2 thousand plants/ha) with one replication per density. From DUVICK et al. (2004b). Copyright © 2004 by John Wiley & Sons, Inc. This material is used by permission of John Wiley & Sons, Inc. Duvick 205 Advances in Agronomy