Seminar on linked selection and demography in maize, U of Toronto, October 2015

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

2. Photos: Matt Hufford, Brandon Gaut, John Doebley

3. maizeteosinte

4. GeographicalBreadth
0
0.02
0.04
0.06
0.08
0.1
maize
potato
wheat
soybean
sorghum
barley
sunflower
rice
groundnut
rapeseed
cassava
millet
rye
sugarcane
oilpalm
sugarbeet
Hake & Ross-Ibarra 2015 eLife

5. Suketoshi Taba

6. hard sweep
Diversity

7. hard sweep
multiple
mutations
Diversity
standing
variation
“soft” sweeps

8. hard sweep
multiple
mutations polygenic adaptation
Diversity
standing
variation
“soft” sweeps

9. M T G P H R L
GGTCGAC ATG ACT GGT CCA CAT CGA CTG TAG

10. M T G P H R L
GGTCGAC ATG ACT GGT CCA CAT CGA CTG TAG
M T N P H R L
GGTCGAC ATG ACT GAT CCA CAT CGA CTG TAG

11. M T G P H R L
GGTAAAC ATG ACT GGT CCA CAT CGA CTG TAG
GG—-AC ATG ACT GGT CCA CAT CGA CTG TAG

12. maize origins
TripsacumF1
teosinte
(Z. mays ssp. parviglumis)
maize
(Z. mays ssp. mays)

13. F1
Beadle 1979 Field Museum of Nat. Hist. Bull.

14. F1
Beadle 1979 Field Museum of Nat. Hist. Bull.

15. F1
Beadle 1979 Field Museum of Nat. Hist. Bull.

16. F1
Beadle 1979 Field Museum of Nat. Hist. Bull.

17. Briggs et al. 2007 Genetics
1 2 3 4 5
6 7 8 9 10

18. 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

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. 1 2 3 4 5
6 7 8 9 10
gt1 tga1
Wills et al. 2013 PLoS Genetics

21. 1 2 3 4 5
6 7 8 9 10
gt1 tga1
Wills et al. 2013 PLoS Genetics
teosinte maize
Clint Whipple, BYU

22. 1 2 3 4 5
6 7 8 9 10
gt1 tga1
Wills et al. 2013 PLoS Genetics

23. 1 2 3 4 5
6 7 8 9 10
gt1 tga1
Wills et al. 2013 PLoS Genetics
5’ control region 3’ UTR

24. 1 2 3 4 5
6 7 8 9 10
tb1
Studer et al. 2011 Nat. Gen.; Vann et al. 2015 PeerJ
tga1gt1

25. 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

26. 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

27. hard sweep
M T N P H R L
GGTCGA ATG ACT GAT CCA CAT CGA CTG TAG
tga1

28. 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

29. Vann et al. 2015 PeerJ
polygenic adaptation
30%
phenotypic
variance
0%
phenotypic
variance

30. 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:

31. Hufford et al. 2012 Nat. Gen.
Chia et al. 2012 Nat. Gen
13 teosinte
23 maize
genomes:

32. Hufford et al. 2012 Nat. Gen.
Chia et al. 2012 Nat. Gen
13 teosinte
23 maize
genomes:

33. 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

34. Beissinger et al. In Prep
nucleotidediversity
distance to nearest substitution (cM)

35. Beissinger et al. In Prep
nucleotidediversity
distance to nearest substitution (cM)

36. Mexico lowland
9,000 BP
Matsuoka et al. 2002; Piperno 2006
Perry et al. 2006; Piperno et al. 2009

37. Mexico highland6,000 BP
Mexico lowland
9,000 BP
Matsuoka et al. 2002; Piperno 2006
Perry et al. 2006; Piperno et al. 2009

38. 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

39. 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

40. Mexico
photobyMonthonWachirasettakul
Andes
photobyMattHufford

41. 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

42. 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
cluding mexicana, in which Mexican Highland maize is tied wit
the West Mexico group as the most ancestral population (Fig. 3B
To mitigate the impact of introgression, we used a slight
modified approach that excludes both parviglumis and mexican
and calculates genetic drift with respect to ancestral frequencie
inferred from domesticated maize alone. Because the genet
Fig. 1. (A) Map of sampled maize accessions colored by genetic group. (B) First three genetic PCs of all sampled accessions.
van Heerwaarden et al. PNAS | January 18, 2011 | vol. 108 | no. 3 | 108
van Heerwaarden et al. 2011 PNAS

43. 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
cluding mexicana, in which Mexican Highland maize is tied wit
the West Mexico group as the most ancestral population (Fig. 3B
To mitigate the impact of introgression, we used a slight
modified approach that excludes both parviglumis and mexican
and calculates genetic drift with respect to ancestral frequencie
inferred from domesticated maize alone. Because the genet
Fig. 1. (A) Map of sampled maize accessions colored by genetic group. (B) First three genetic PCs of all sampled accessions.
van Heerwaarden et al. PNAS | January 18, 2011 | vol. 108 | no. 3 | 108
van Heerwaarden et al. 2011 PNAS

44. 95 landraces
~100K SNPs
Takuno et al. 2015 Genetics

45. -Logp-valueFstS.America
-Log p-value Fst Mexico
shared SNPs
unique S.America
unique Mexico
95 landraces
~100K SNPs
Takuno et al. 2015 Genetics

46. -Logp-valueFstS.America
-Log p-value Fst Mexico
shared SNPs
unique S.America
unique Mexico
39%
61%
Intergenic
Genic
19%
81%
Standing Variation
New mutation
Takuno et al. 2015 Genetics

47. Beissinger et al. In Prep (b) Berg & Coop 2014 PLoS Genetics

48. Beissinger et al. In Prep (b) Berg & Coop 2014 PLoS Genetics
Z =
LX
i=1
↵ipi
allele freq.population
breeding value
effect size

49. 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

50. Beissinger et al. In Prep (b) Berg & Coop 2014 PLoS Genetics
Warm

51. Cold
Beissinger et al. In Prep (b) Berg & Coop 2014 PLoS Genetics
Warm

52. Cold
Beissinger et al. In Prep (b) Berg & Coop 2014 PLoS Genetics
Warm

53. Wallace et al. 2014 PLoS Genetics

54. masl
Pyhäjärvi et al. GBE 2013

55. Pyhäjärvi et al. GBE 2013

56. Pyhäjärvi et al. GBE 2013

57. Pyhäjärvi et al. GBE 2013

58. Beissinger et al. In Prep

59. how to adapt: Zea mays
soft sweeps
M T G P H R L
GGTAAA ATG ACT GGT CCA CAT CGA CTG TAG
polygenic adaptation
regulatory variation

60. Sattah et al. 2011 PLoS Gen.
Williamson et al. 2014 PLoS Gen
Hernandez et al. 2011 Science

61. Sattah et al. 2011 PLoS Gen.
Williamson et al. 2014 PLoS Gen
Hernandez et al. 2011 Science

62. Sattah et al. 2011 PLoS Gen.
Williamson et al. 2014 PLoS Gen
Hernandez et al. 2011 Science
diversity

63. Ne diploids
s selection coefficient
selection is effective if 2Nes > 1

64. Ne diploids
s selection coefficient
selection is effective if 2Nes > 1
Ne ~ 150,000 Ne ~ 10,000
Ne ~ 2,000,000 Ne ~ 600,000

65. 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

66. Beissinger et al. In Prep
Hufford et al. 2012
teosinte maize

67. teosinte
maize
DATA
teosinte
maize
MODEL
Beissinger et al. In Prep
Hufford et al. 2012
teosinte maize

68. teosinte
maize
DATA
teosinte
maize
MODEL
0.05Na
Na
Na 3Na
Beissinger et al. In Prep
Hufford et al. 2012
teosinte maize

69. Sara Hearne, Li Wang
1M SNPs
4K samples
SeeD