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demography and linked selection in
maize and teosinte
Jeffrey Ross-Ibarra
@jrossibarra
UC Davis
photo by Jason Wallace
Photo: https://www.flickr.com/photos/croptrust/
Beadle 1979 Field Museum of Natural History Bulletin
maize ori
F1
teosinte
(Z. mays ssp. parviglumis)
maize
(Z. mays ssp. mays)
George Beadle
van Heerwaarden 2011 PNAS Matsuoka et al 2002 PNAS
Zea mays ssp.
parvgilumis
Zea mays ssp.
mexicana
Zea mays ssp.
mays
1250m
Title Text Title Text
Photos: Matt Hufford, Brandon Gaut, John Doebley
GGANAN AND D. Q. FULLER
mparison of evolutionary rate estimates. Box plots of the rates of evolution in (A) log (darwins) and (B) log (haldane
(DOM) as well as plants (PLAN) (from Bones and Farres 2001) and anthropogenic (AN) and natural (NAT) conditions for
s (Hendry et al. 2008). The asterisk indicates domestication rates under the assumption of the shortened 2000-year p
ecies. The vertical lines give the estimate ranges, whereas the boxes span the minimum and maximum quartile range
e within the box gives the median rate.
n/seed increase is 0.68 ± 0.15 × 10−3
haldanes.
(rate) estimates, we find that the evolutionary rates
Most of the studies that document rapid evolution in
plant species, however, represent cases of very strong sele
logDarwins(e/106yrs)
Purugganan and Fuller 2010 Evolution
Benz 2009 Hist. Maize
F1
F2
Beadle:
1/500
4-5 genes
Briggs et al. 2007 Genetics
Wang et al. 2005 Nature
1 2 3 4 5
6 7 8 9 10
tb1gt1
Figure 1.
Phenotypes. a. Maize ear showing the cob (cb) exposed at top. b. Teosinte ear with
internode (in) and glume (gl) labeled. c. Teosinte ear from a plant with a maize all
introgressed into it. d. Close-up of a single teosinte fruitcase. e. Close-up of a fruit
teosinte plant with a maize allele of tga1 introgressed into it. f. Ear of maize inbred
(Tga1-maize allele) with the cob exposed showing the small white glumes at the b
of maize inbred W22:tga1 which carries the teosinte allele, showing enlarged (whit
h. Ear of maize inbred W22 carrying the tga1-ems1 allele, showing enlarged glumes.
magnification copies of f–h see Supplementary Information.
Wang et al.
NIH-PAAuthorManuscriptNIH-PAAuthorManuscriptNIH-PAAuthorManus
tga1
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,
Studer et al. 2011 Nat. Gen.; Vann et al. PeerJ 2015
Wills et al. 2013 PLoS Gen
T/T
M/T
M/M
T/T
M/T
M/M
A B
T/T
M/T
M/M
T/T
M/T
M/M
3’ UTR
5’ control region
n=23 n=15
landraces teosinte
inbred lines, 3-5X coverage
Chia et al. 2012 Nat. Gen
Hufford et al. 2012 Nat. Gen.
strong selection (s~0.015) on ~1,100 genes
11M maize-teosinte shared SNPs
3,000 fixed SNPs
Tim Beissinger
teosintenucleotidediversity
maizenucleotidediversity
distance to nearest substitution (cM)
Tim Beissinger Wallace et al. 2014 PLoS Gen.
Hard sweeps?
distance to substitution (cM)
maizenucleotidediversity
Sattah et al. 2011 PLoS Gen.
nucleotidediversity
distance to nearest substitution (cM)
distance to nearest substitution (kb)
scaleddiversity
Ne ~ 150,000 Ne ~ 10,000
Ne ~ 2,000,000 Ne ~ 600,000
Sattah et al. 2011 PLoS Gen.
Williamson et al. 2014 PLoS Gen
Hernandez et al. 2011 Science
maize
Hufford et al. 2012 Nat. Gen.
teosinte
Tajima’s D
Tim Beissinger
relativenucleotidediversity
distance to gene (cM)
teosinte Ne~150,000
maize Ne~50,000
200-2000bp
Nordborg et al. 1996 Genetical Res.Tim Beissinger
het. selection (hs)deleterious mut. rate μ
recombination r
B ⇡ e
P
i
µiti
(ti+ri(1 ti))2
B=relativediversity
distance to gene (M)
observed
best fit
maize
teosinte
teosinte 2Ns=1
maize 2Ns=1
s (h=0.1)
Tim Beissinger
Fitness effects of new mutations
maize
3.6E-7
3.6E-9
teosinte
µ
t = hs 2.3E-7
6E-9
maize
Hufford et al. 2012 Nat. Gen.
teosinte
25% SNPs unique
36% SNPs unique
Tajima’s D
Wright et al. 2005 Science
Tenaillon et al. 2004 MBE
Eyre-Walker et al. 1996 PNAS
µ, r
teosinte
maize
DATAteosinte
maize
MODEL
Tim Beissinger
0.05Na
Na
Na 3Na
150,000 450,000
Nm~1.5
Kate Crosby Hearne et al. 2014 http://hdl.handle.net/11529/10034
4K samples
~1M SNPs
Ne ~106
time (years BP)
Li Wang
multiple sequential markovian coalescent
Ne~108
CIMMYT 1984
49M ha of open-pollinated maize
22,000 plants/ha.
Nc ~1012
min. 10 plants/ha to reseed Ne ~5 x 108
Tim Beissinger
0.05Na
Na
Na 3Na
nucleotidediversity
distance to gene (cM)
singletondiversity
distance to gene (cM)
Tim Beissinger
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
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Presentation at SMBEBA

  • 1. demography and linked selection in maize and teosinte Jeffrey Ross-Ibarra @jrossibarra UC Davis photo by Jason Wallace
  • 3. Beadle 1979 Field Museum of Natural History Bulletin maize ori F1 teosinte (Z. mays ssp. parviglumis) maize (Z. mays ssp. mays) George Beadle
  • 4. van Heerwaarden 2011 PNAS Matsuoka et al 2002 PNAS Zea mays ssp. parvgilumis Zea mays ssp. mexicana Zea mays ssp. mays 1250m
  • 5. Title Text Title Text Photos: Matt Hufford, Brandon Gaut, John Doebley
  • 6.
  • 7. GGANAN AND D. Q. FULLER mparison of evolutionary rate estimates. Box plots of the rates of evolution in (A) log (darwins) and (B) log (haldane (DOM) as well as plants (PLAN) (from Bones and Farres 2001) and anthropogenic (AN) and natural (NAT) conditions for s (Hendry et al. 2008). The asterisk indicates domestication rates under the assumption of the shortened 2000-year p ecies. The vertical lines give the estimate ranges, whereas the boxes span the minimum and maximum quartile range e within the box gives the median rate. n/seed increase is 0.68 ± 0.15 × 10−3 haldanes. (rate) estimates, we find that the evolutionary rates Most of the studies that document rapid evolution in plant species, however, represent cases of very strong sele logDarwins(e/106yrs) Purugganan and Fuller 2010 Evolution Benz 2009 Hist. Maize
  • 9. Briggs et al. 2007 Genetics Wang et al. 2005 Nature 1 2 3 4 5 6 7 8 9 10 tb1gt1 Figure 1. Phenotypes. a. Maize ear showing the cob (cb) exposed at top. b. Teosinte ear with internode (in) and glume (gl) labeled. c. Teosinte ear from a plant with a maize all introgressed into it. d. Close-up of a single teosinte fruitcase. e. Close-up of a fruit teosinte plant with a maize allele of tga1 introgressed into it. f. Ear of maize inbred (Tga1-maize allele) with the cob exposed showing the small white glumes at the b of maize inbred W22:tga1 which carries the teosinte allele, showing enlarged (whit h. Ear of maize inbred W22 carrying the tga1-ems1 allele, showing enlarged glumes. magnification copies of f–h see Supplementary Information. Wang et al. NIH-PAAuthorManuscriptNIH-PAAuthorManuscriptNIH-PAAuthorManus tga1 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, Studer et al. 2011 Nat. Gen.; Vann et al. PeerJ 2015 Wills et al. 2013 PLoS Gen T/T M/T M/M T/T M/T M/M A B T/T M/T M/M T/T M/T M/M 3’ UTR 5’ control region
  • 10. n=23 n=15 landraces teosinte inbred lines, 3-5X coverage Chia et al. 2012 Nat. Gen
  • 11. Hufford et al. 2012 Nat. Gen. strong selection (s~0.015) on ~1,100 genes 11M maize-teosinte shared SNPs 3,000 fixed SNPs
  • 13. Tim Beissinger Wallace et al. 2014 PLoS Gen. Hard sweeps? distance to substitution (cM) maizenucleotidediversity
  • 14. Sattah et al. 2011 PLoS Gen. nucleotidediversity distance to nearest substitution (cM) distance to nearest substitution (kb) scaleddiversity Ne ~ 150,000 Ne ~ 10,000 Ne ~ 2,000,000 Ne ~ 600,000 Sattah et al. 2011 PLoS Gen. Williamson et al. 2014 PLoS Gen Hernandez et al. 2011 Science
  • 15. maize Hufford et al. 2012 Nat. Gen. teosinte Tajima’s D
  • 16. Tim Beissinger relativenucleotidediversity distance to gene (cM) teosinte Ne~150,000 maize Ne~50,000 200-2000bp
  • 17. Nordborg et al. 1996 Genetical Res.Tim Beissinger het. selection (hs)deleterious mut. rate μ recombination r B ⇡ e P i µiti (ti+ri(1 ti))2 B=relativediversity distance to gene (M) observed best fit maize teosinte
  • 18. teosinte 2Ns=1 maize 2Ns=1 s (h=0.1) Tim Beissinger Fitness effects of new mutations maize 3.6E-7 3.6E-9 teosinte µ t = hs 2.3E-7 6E-9
  • 19. maize Hufford et al. 2012 Nat. Gen. teosinte 25% SNPs unique 36% SNPs unique Tajima’s D
  • 20. Wright et al. 2005 Science Tenaillon et al. 2004 MBE Eyre-Walker et al. 1996 PNAS µ, r
  • 22. Kate Crosby Hearne et al. 2014 http://hdl.handle.net/11529/10034 4K samples ~1M SNPs Ne ~106
  • 23. time (years BP) Li Wang multiple sequential markovian coalescent Ne~108
  • 24. CIMMYT 1984 49M ha of open-pollinated maize 22,000 plants/ha. Nc ~1012 min. 10 plants/ha to reseed Ne ~5 x 108
  • 25. Tim Beissinger 0.05Na Na Na 3Na nucleotidediversity distance to gene (cM) singletondiversity distance to gene (cM)
  • 27. 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