1. Selection and demography
in maize evolution
Jeffrey Ross-Ibarra
@jrossibarra • www.rilab.org
Dept. Plant Sciences • Center for Population Biology • Genome Center
University of California Davis
photo by lady_lbrty
19. Wang et al. 2005 Nature
1 2 3 4 5
6 7 8 9 10
Figure 1.
Phenotypes. a. Maize ear showing the cob (cb) exposed at top. b. Teosinte e
internode (in) and glume (gl) labeled. c. Teosinte ear from a plant with a m
introgressed into it. d. Close-up of a single teosinte fruitcase. e. Close-up o
teosinte plant with a maize allele of tga1 introgressed into it. f. Ear of maiz
(Tga1-maize allele) with the cob exposed showing the small white glumes a
of maize inbred W22:tga1 which carries the teosinte allele, showing enlarge
h. Ear of maize inbred W22 carrying the tga1-ems1 allele, showing enlarged g
NIH-PAAuthorManuscriptNIH-PAAuthorManuscriptNIH-P
tga1
Wang et al. 2015 Genetics
20. Wang et al. 2005 Nature
1 2 3 4 5
6 7 8 9 10
Figure 1.
Phenotypes. a. Maize ear showing the cob (cb) exposed at top. b. Teosinte e
internode (in) and glume (gl) labeled. c. Teosinte ear from a plant with a m
introgressed into it. d. Close-up of a single teosinte fruitcase. e. Close-up o
teosinte plant with a maize allele of tga1 introgressed into it. f. Ear of maiz
(Tga1-maize allele) with the cob exposed showing the small white glumes a
of maize inbred W22:tga1 which carries the teosinte allele, showing enlarge
h. Ear of maize inbred W22 carrying the tga1-ems1 allele, showing enlarged g
NIH-PAAuthorManuscriptNIH-PAAuthorManuscriptNIH-P
tga1
Wang et al. 2015 Genetics
24. 1 2 3 4 5
6 7 8 9 10
gt1 tga1
Wills et al. 2013 PLoS Genetics
5’ control region 3’ UTR
25. 1 2 3 4 5
6 7 8 9 10
tb1
Studer et al. 2011 Nat. Gen.; Vann et al. 2015 PeerJ
tga1gt1
26. 1 2 3 4 5
6 7 8 9 10
tb1
Studer et al. 2011 Nat. Gen.; Vann et al. 2015 PeerJ
tga1
GENETICS ADVANCE ONLINE PUBLICATION 3
nguish maize and teosinte. Both the maize and teosinte
s for the distal component repressed luciferase expression
luc
luc
luc
luc
luc
luc
Hopscotch
mpCaMV
M-dist
T-prox
M-prox
0 0.5 1.0 1.5 2.0
∆M-dist
∆M-prox
ProximalcontrolregionDistal
Constructs and corresponding normalized luciferase expression
nsient assays were performed in maize leaf protoplast. Each
is drawn to scale. The construct backbone consists of the
romoter from the cauliflower mosaic virus (mpCaMV, gray box),
ORF (luc, white box) and the nopaline synthase terminator
). Portions of the proximal and distal components of the
gion (hatched boxes) from maize and teosinte were cloned
ction sites upstream of the minimal promoter. “ ” denotes
on of either the Tourist or Hopscotch element from the maize
Horizontal green bars show the normalized mean with s.e.m.
onstruct.
relative expressionconstruct
gt1
27. 1 2 3 4 5
6 7 8 9 10
tb1
Figure 2 Map of parviglumis Populations and Hopscotch allele frequency. Map showing the frequency
of the Hopscotch allele in populations of parviglumis where we sampled more than 6 individuals. Size of
circles reflects number of individuals sampled. The Balsas River is shown, as the Balsas River Basin is
believed to be the center of domestication of maize.
as our independent trait for phenotyping analyses. SAS code used for analysis is available at
http://dx.doi.org/10.6084/m9.figshare.1166630.
RESULTS
Genotyping for the Hopscotch insertion
The genotype at the Hopscotch insertion was confirmed with two PCRs for 837 individuals
of the 1,100 screened (Table S1 and Table S2). Among the 247 maize landrace accessions
genotyped, all but eight were homozygous for the presence of the insertion Within
our parviglumis and mexicana samples we found the Hopscotch insertion segregating
in 37 (n = 86) and four (n = 17) populations, respectively, and at highest frequency
within populations in the states of Jalisco, Colima, and Michoac´an in central-western
Mexico (Fig. 2). Using our Hopscotch genotyping, we calculated diVerentiation between
populations (FST) and subspecies (FCT) for populations in which we sampled sixteen
or more chromosomes. We found that FCT = 0, and levels of FST among populations
within each subspecies (0.22) and among all populations (0.23) (Table 1) are similar to
genome-wide estimates from previous studies Pyh¨aj¨arvi, HuVord & Ross-Ibarra, 2013.
Although we found large variation in Hopscotch allele frequency among our populations,
BayEnv analysis did not indicate a correlation between the Hopscotch insertion and
environmental variables (all Bayes Factors < 1).
Studer et al. 2011 Nat. Gen.; Vann et al. 2015 PeerJ
tga1
GENETICS ADVANCE ONLINE PUBLICATION 3
nguish maize and teosinte. Both the maize and teosinte
s for the distal component repressed luciferase expression
luc
luc
luc
luc
luc
luc
Hopscotch
mpCaMV
M-dist
T-prox
M-prox
0 0.5 1.0 1.5 2.0
∆M-dist
∆M-prox
ProximalcontrolregionDistal
Constructs and corresponding normalized luciferase expression
nsient assays were performed in maize leaf protoplast. Each
is drawn to scale. The construct backbone consists of the
romoter from the cauliflower mosaic virus (mpCaMV, gray box),
ORF (luc, white box) and the nopaline synthase terminator
). Portions of the proximal and distal components of the
gion (hatched boxes) from maize and teosinte were cloned
ction sites upstream of the minimal promoter. “ ” denotes
on of either the Tourist or Hopscotch element from the maize
Horizontal green bars show the normalized mean with s.e.m.
onstruct.
relative expressionconstruct
gt1
28. hard sweep
M T N P H R L
GGTCGA ATG ACT GAT CCA CAT CGA CTG TAG
tga1
29. hard sweep
M T N P H R L
GGTCGA ATG ACT GAT CCA CAT CGA CTG TAG
tga1
gt1
tb1
Multiple
Mutations
Standing
Variation
M T G P H R L
GGTAAA ATG ACT GGT CCA CAT CGA CTG TAG
30. Vann et al. 2015 PeerJ
polygenic adaptation
30%
phenotypic
variance
0%
phenotypic
variance
31. Hufford et al. 2012 Nat. Gen.
Chia et al. 2012 Nat. Gen
13 teosinte
23 maize
~500 genes (2%)
11M shared SNPs
3,000 fixed
genomes:
32. Hufford et al. 2012 Nat. Gen.
Chia et al. 2012 Nat. Gen
13 teosinte
23 maize
genomes:
33. Hufford et al. 2012 Nat. Gen.
Chia et al. 2012 Nat. Gen
13 teosinte
23 maize
genomes:
34. Swanson-Wagner et al. 2012 PNAS
E
ze network edges
6
7
2
Mb
or conservation and targets of selection during improvement and/or domestication. (A) Venn diagram
es, and the genes that occur in genomic regions that have evidence for selective sweeps during maize
s). (B) Teosinte coexpression networks for three genes (GRMZM2G068436, GRMZM2G137947, and
ned in maize coexpression networks are shown. Although the differentially expressed gene (red node) is
tions are lost in maize. However, some parts of the teosinte network are still conserved in maize. (C) Cross-
ExpressionGenealogy
teosinte
maize
38. Mexico highland6,000 BP
Mexico lowland
9,000 BP
Matsuoka et al. 2002; Piperno 2006
Perry et al. 2006; Piperno et al. 2009
39. Mexico highland6,000 BP
S. America
lowland
6,000 BP
Mexico lowland
9,000 BP
Matsuoka et al. 2002; Piperno 2006
Perry et al. 2006; Piperno et al. 2009
40. Mexico highland6,000 BP
S. America
lowland
6,000 BP
S. America
Highland
4,000 BP
Mexico lowland
9,000 BP
Matsuoka et al. 2002; Piperno 2006
Perry et al. 2006; Piperno et al. 2009
42. SA MEX SA MEX
SA MEX SA MEX SA MEX SA MEX
Ear Height Plant Height
Tassel Br. Number
TW
Days to Anthesis
SA MEX SA MEX
SA MEX SA MEX
LowlandHighland
47. Beissinger et al. In Prep (b) Berg & Coop 2014 PLoS Genetics
Z =
LX
i=1
↵ipi
allele freq.
population
breeding value
effect size
48. Beissinger et al. In Prep (b) Berg & Coop 2014 PLoS Genetics
Z =
LX
i=1
↵ipi
allele freq.
population
breeding value
effect size
relatednessdispersion
add. genetic var.
QX =
~Z0
T
F 1 ~Z0
2VA
62. Ne diploids
s selection coefficient
selection is effective if 2Nes > 1
Ne ~ 150,000 Ne ~ 10,000
Ne ~ 2,000,000 Ne ~ 600,000
63. Ne diploids
s selection coefficient
selection is effective if 2Nes > 1
Ne ~ 150,000 Ne ~ 10,000
Ne ~ 2,000,000 Ne ~ 600,000
20% nonsyn. subs 10% nonsyn. subs
50% nonsyn. subs 40% nonsyn. subs
67. 0.05Na
Na
Na 3Na
Ne ~ 450,000
Beissinger et al. In Prep: http://biorxiv.org/content/early/
68. 0.05Na
Na
Na 3Na
Ne ~ 450,000
Ne ~ 1,000,000
Beissinger et al. In Prep: http://biorxiv.org/content/early/
69. 0.05Na
Na
Na 3Na
Ne ~ 450,000
Ne ~ 1,000,000
1e+05
1e+07
1e+09
1e+03 1e+042e+04 1e+05
years(u=3e−8, generation=1)
effectivepopulationsize
pop
BKN_4Hap
BKN_6Hap
TIL_4Hap_Jalisco
TIL_6Hap
Ne ~ 1,000,000,000
Beissinger et al. In Prep: http://biorxiv.org/content/early/
70. 0.05Na
Na
Na 3Na
Ne ~ 450,000
Ne ~ 1,000,000
1e+05
1e+07
1e+09
1e+03 1e+042e+04 1e+05
years(u=3e−8, generation=1)
effectivepopulationsize
pop
BKN_4Hap
BKN_6Hap
TIL_4Hap_Jalisco
TIL_6Hap
Ne ~ 1,000,000,000
Ne ~ 5,000,000,000
Beissinger et al. In Prep: http://biorxiv.org/content/early/
74. Sattah et al. 2011 PLoS Gen.
Williamson et al. 2014 PLoS Gen
Hernandez et al. 2011 Science
diversity
Ne >> 1,000,000 Ne ~ 10,000*
Ne ~ 2,000,000 Ne ~ 600,000
84. Makarevitch et al. 2014 PLoS Genetics
single TE family, many genes
new insertions activate expression
Makarevitch et al. 2014 bioRxiv
Lines with the
TE insertion
Lines without the
TE insertion
GRMZM2G071206
Log2(stress/control)
-2
0
2
4
6
8
10
12
Lines with the
TE insertion
Lines without the
TE insertion
-2
0
2
4
6
8
10
12
Log2(stress/control)
GRMZM2G400718
C
1.0
1.5
2.0
D
GRMZM2G102447
-2
0
2
4
6
8
10
12
14
Lines with the
TE insertion
Lines without the
TE insertion
GRMZM2G108149
A
B
Log2(stress/control)s/control)
http://biDownloaded from
-0.5
0.0
0.5
1.0
1.5
2.0
2.5
3.0
3.5
1 2 3 4 5 6 7 8 9 10
Oh43
B73
Mo17
- - + - - + - + - - ++ - - + - - + - - + - - + - - + - - +
Gene
Log2(stress/control)
TE
presence
0%
20%
40%
60%
80%
100%
alaw
dagaf
etug
flip
gyma
ipiki
jeli
joemon
naiba
nihep
odoj
pebi
raider
riiryl
ubel
uwum
Zm00346
Zm02117
Zm03238
Zm05382
Salt
UV
Heat
Cold
B
A
Percentofconserved
genes
*
**
***
*
*
** *
single gene,
many individuals
85. Hancock et al 2011 Science
Hernandez et al. 2011 Science
Fraser et al. 2013 Gen. Research
enrichment
intergenic<———>coding
Pyhäjärvi et al. GBE 2013
enrichment
intergenic<———>coding
86. Ne diploids
µ beneficial mutation rate per trait
selection from standing variation when 2Neµ > 1
87. Ne diploids
µ beneficial mutation rate per trait
selection from standing variation when 2Neµ > 1
Garud et al. 2015 PLoS Gen.
Jensen 2014 Nat. Comm.
Pritchard et al. 2010 Curr. Bio.
Enard et al. 2014 Gen. Res.
Beissinger et al. In Prep
µ ∝ 2,500 Mbp µ ∝ 3,100 Mbp
µ ∝ 130 Mbp
88. Ne diploids
µ beneficial mutation rate per trait
selection from standing variation when 2Neµ > 1
Garud et al. 2015 PLoS Gen.
Jensen 2014 Nat. Comm.
Pritchard et al. 2010 Curr. Bio.
Enard et al. 2014 Gen. Res.
Beissinger et al. In Prep
µ ∝ 2,500 Mbp µ ∝ 3,100 Mbp
µ ∝ 130 Mbp µ ∝ 220 Mbp
µ ∝ 130 Mbp
Williamson et al. 2014 PLoS Gen
90. • “Soft sweeps” and polygenic selection predominate
in maize and teosinte
• Most selection appears in noncoding sequence
• Both effective population size & mutational target
contribute
• Large, complex genomes may mean more targets &
more soft sweeps & less linked effects of selection
Concluding Thoughts
91. Acknowledgments
Maize Diversity Group
Peter Bradbury
Ed Buckler
John Doebley
Theresa Fulton
Sherry Flint-Garcia
Jim Holland
Sharon Mitchell
Qi Sun
Doreen Ware
Collaborators
Graham Coop
Nathan Springer
Ruairidh Sawers
Lab Alumni
Tim Beissinger (USDA-ARS, Mizzou)
Kate Crosby (Monsanto)
Matt Hufford (Iowa State)
Tanja Pyhäjärvi (Oulu)
Shohei Takuno (Sokendai)
Joost van Heerwaarden (Wageningen)