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.
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
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
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.
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