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Adaptive (and not so adaptive)
introgression between maize and teosinte
Jeffrey Ross-Ibarra
@jrossibarra • www.rilab.org
Dept. Plant Sciences • Center for Population Biology • Genome Center
University of California Davis
photo by lady_lbrty
Servedio 2004 PloS Bio
Hopkins 2013 New Phyt.Servedio 2004 PloS Bio
Hopkins 2013 New Phyt.Servedio 2004 PloS Bio
with little population differentiation, even though trait frequencies
may differ greatly due to local adaptation. This creates relatively
greater mating opportunities for foreign, rare males in each pop-
ulation, directly countering the effects of local adaptation and re-
ducing population differentiation at a trait locus. Importantly,
stronger preferences exaggerate this effect. Fisherian sexual selec-
tion is thus a double-edged sword in the development of isolation
under these conditions, potentially driving differentiation in allop-
atry but removing it if there is contact. Ultimately its role in allo-
patric speciation is tenuous, failing even if contact is initiated after
substantive trait and preference divergence has occurred.
Model and Results
We consider a two-locus population genetic model with polygyny
(Methods). Locus T has alleles T1 and T2, which control two
sexually selected phenotypes in males. Locus P determines a fe-
male preference; P1 females are 1 + α1 times as likely to mate
with a T1 than a T2 male upon encounter, whereas P2 females
similarly prefer T2 males with preference strength 1 + α2. Our
basic model, in accordance with the Fisherian models of Lande
(4) and Kirkpatrick (13), does not include costs to preferences
(this assumption is varied below). Our models are haploid to
facilitate analyses, but the key factors that lead to our qualitative
results should be readily generalizable to diploids. We assume
that two allopatric populations have diverged such that individ-
uals in population 1 have primarily P1 and T1 alleles and those in
population 2 have primarily P2 and T2 alleles. Secondary contact
occurs between these populations by symmetric migration with
rate m. The onset of migration leads to variation in preferences
and traits within each population, and linkage disequilibrium
Fig. 1. Male trait and female preference frequencies show a decrease i
their differentiation between populations when sexual selection is strong
Servedio and Bürger 2014 PNAS
Beadle 1979 Field Museum of Natural History
parviglumis mays
ssp.	mexicana
ssp.	parviglumis
ssp.	mays
Matsuoka	et	al.	2002	PNAS
ssp.	mexicana
ssp.	parviglumis
ssp.	mays
Matsuoka	et	al.	2002	PNAS
ssp.	mexicana
ssp.	parviglumis
ssp.	mays
Matsuoka	et	al.	2002	PNAS
Piperno	et	al.	2009	PNAS
the presence of maize (Table 2; Fig. 1); for comparison, Fig.
S1A–C shows modern teosinte and maize starch grains. For
example, the grains isolated from the preceramic- and ceramic-
Fig. 1. Starch grains from maize recovered from early preceramic grinding
stones 318d (A and B) and 318e (C and D). The grains have irregular shapes and
surface contours, along with defined compression facets and transverse fis-
sures (A) or y-shaped and other fissures (B–D).
Table 2. Morphology of maize starch grains recovered from the Xihu
Provenience
Tool
Cat. no.
Shape
Round Oval Bell Irregular
Unit 1
Ceramic
Layer B 310a 0 17 0 83
312a 0 0 0 100
Layer C 314c 46 0 0 54
315c 11 0 0 89
Preceramic
Layer D 316c 0 0 0 100
316d 9 0 3 88
Layer E 318e 13 1 0 86
318d 5 0 0 90
319d 12 0 0 88
322c 9 0 0 91
Unit 2
Ceramic
ssp.	mexicana
ssp.	parviglumis
ssp.	mays
Matsuoka	et	al.	2002	PNAS
Piperno	et	al.	2009	PNAS
the presence of maize (Table 2; Fig. 1); for comparison, Fig.
S1A–C shows modern teosinte and maize starch grains. For
example, the grains isolated from the preceramic- and ceramic-
Fig. 1. Starch grains from maize recovered from early preceramic grinding
stones 318d (A and B) and 318e (C and D). The grains have irregular shapes and
surface contours, along with defined compression facets and transverse fis-
sures (A) or y-shaped and other fissures (B–D).
Table 2. Morphology of maize starch grains recovered from the Xihu
Provenience
Tool
Cat. no.
Shape
Round Oval Bell Irregular
Unit 1
Ceramic
Layer B 310a 0 17 0 83
312a 0 0 0 100
Layer C 314c 46 0 0 54
315c 11 0 0 89
Preceramic
Layer D 316c 0 0 0 100
316d 9 0 3 88
Layer E 318e 13 1 0 86
318d 5 0 0 90
319d 12 0 0 88
322c 9 0 0 91
Unit 2
Ceramic
mexicana parviglumis South/Caribbean West Highland
0
500
1000
1500
2000
2500
m
van	Heerwaarden	et	al.	2011	PNAS
clearly separated clusters, but evidence of admixture is inferred from domesticated maize alone. Because the genetic
Fig. 1. (A) Map of sampled maize accessions colored by genetic group. (B) First three genetic PCs of all sampled accessions.
EVOLUTION
altitude	
mexicana parviglumis mays
mexicana parviglumis
Lauter et al. (2004) Genetics
Pyhäjärvi	et	al.	GBE	2013
Lauter et al. 2004 Genetics
0
10
20
30
40
60 80 100 120
days to pollen
count
subpsecies
parviglumis
mexicana
Rodriguez et al. (2006) Maydica
Environmental Association for temperature/altitude
																					
mexicana parviglumis
Lauter et al. (2004) Genetics
Pyhäjärvi	et	al.	GBE	2013
Lauter et al. 2004 Genetics
Days to Flowering
highlandlowland
daystoflowering
HiLo field trials 2014,2016 (unpublished)
Lowland Highland
Photos: Ruairidh Sawers, LANGEBIO
Lowland Field Highland Field
Days to Flowering
highlandlowland
daystoflowering
HiLo field trials 2014,2016 (unpublished)
Lowland Highland
Photos: Ruairidh Sawers, LANGEBIO
Lowland Field Highland Field
Days to Flowering
highlandlowland
daystoflowering
HiLo field trials 2014,2016 (unpublished)
Lowland Highland
Photos: Ruairidh Sawers, LANGEBIO
Lowland Field Highland Field
mexicanamaize
Photo	by	Pesach	Lubinsky
Photo	by	Anna	O’Brien
K = 2
K = 5
K = 4
K = 3
mexicana maize references
K = 7
K = 8
K = 9
K = 10
Hufford	et	al.	2013	PLoS	GeneGcs
Hufford	et	al.	2013	PLoS	GeneGcs
low
elevation
maize
mexicana
allele
El Porvenir
Opopeo
Xochimilco
Puruandiro
Tenango del Aire
Ixtlan
Nabogame
Santa Clara
San Pedro
Allopatric
Hufford	et	al.	2013	PLoS	GeneGcs
low
elevation
maize
mexicana
allele
El Porvenir
Opopeo
Xochimilco
Puruandiro
Tenango del Aire
Ixtlan
Nabogame
Santa Clara
San Pedro
Allopatric
Hufford	et	al.	2013	PLoS	GeneGcs
low
elevation
maize
mexicana
allele
El Porvenir
Opopeo
Xochimilco
Puruandiro
Tenango del Aire
Ixtlan
Nabogame
Santa Clara
San Pedro
Allopatric
Hufford	et	al.	2013	PLoS	GeneGcs
low
elevation
maize
mexicana
allele
El Porvenir
Opopeo
Xochimilco
Puruandiro
Tenango del Aire
Ixtlan
Nabogame
Santa Clara
San Pedro
Allopatric
Hufford	et	al.	2013	PLoS	GeneGcs
low
elevation
maize
mexicana
allele0 1000 2000 3000 4000 5000
-447000
generations
com
0 1000 2000 3000 4000 5000
-452000-450000
Santa Clara Likelihoods
generations
comp.loglikelihood
0 1000 2000 3000 4000 5000
-40650
generations
com
0 1000 2000 3000 4000 5000
-420000-418500
Puruandiro Likelihoods
generations
comp.loglikelihood
0 1000 2000 3000
-418000
generations
com
0 1000 2000 3000
-418000-416500
Opopeo Likelihoo
generations
comp.loglikelihood
55500-254000
San Pedro Likelihoods
comp.loglikelihood
0000-288000
El Porvenir Likelihoods
comp.loglikelihood
-311500-310000
Ixtlan Likelihood
comp.loglikelihood
B
0 1000 2000 3000 4000 5000
-292
generations
com
0 1000 2000 3000 4000 5000
-293000-291500-290000
Santa Clara Likelihoods
generations
comp.loglikelihood
0 1000 2000 300
-296500
generations
com
0 1000 2000 300
-286000-284000
Puruandiro Like
generations
comp.loglikelihood
maize into mexicana mexicana into maize
generations since admixture
Photo	by	Anna	O’Brien
Hufford	et	al.	2013	PLoS	GeneGcs
0 50 100 150 200 250 300
0.00.6
Chromosome 1
bp
proportionofpopulations
0 50 100 150 200
0.00.6
Chromosome 2
bp
proportionofpopulations
0 50 100 1
0.00.6
Chromosome 6
bp
proportionofpopulations
0 50 100 150
0.00.6
Chromosome 7
bp
proportionofpopulations
Mb Mb
MbMb
B
gt1 tb1bif2
zfl2 pbf1
zag1
ra1
Chr1: mexicana to maize
1-admixture
Photo	by	Anna	O’Brien
Hufford	et	al.	2013	PLoS	GeneGcs
0 50 100 150 200
0.00.6 Chromosome 3
bp
proportionofpopulations
0 50 100 150 200 250
0.00.6
Chromosome 4
bp
proportionofpopulations
0 50 100 15
0.00.6
Chromosome 8
bp
proportionofpopulations
0 50 100
0.00.6
Chromosome 9
bp
proportionofpopulations
Mb
Mb
Mb
Mb
zag2 ba1
su1
tga1 bt2ga1
tcb1
Mb
Chr4: maize to mexicana
0 50 100 150 200 250 300
0.00.6
Chromosome 1
bp
proportionofpopulations
0 50 100 150 200
0.00.6
Chromosome 2
bp
proportionofpopulations
0 50 100 1
0.00.6
Chromosome 6
bp
proportionofpopulations
0 50 100 150
0.00.6
Chromosome 7
bp
proportionofpopulations
Mb Mb
MbMb
B
gt1 tb1bif2
zfl2 pbf1
zag1
ra1
Chr1: mexicana to maize
1-admixture
Photo	by	Anna	O’Brien
Hufford	et	al.	2013	PLoS	GeneGcs
Photo: U. Nebraska-Lincoln
♀silk
Photo: Tarek Siala
♂tassel
Photo: Henry Mühlpfordt
																							Pollen				
Pistil
M	 m	
F- ✓ ✗
ff ✓ ✓
F/f M/m
tcb1
Photo: U. Nebraska-Lincoln
♀silk
Photo: Tarek Siala
♂tassel
Photo: Henry Mühlpfordt
																							Pollen				
Pistil
M	 m	
F- ✓ ✗
ff ✓ ✓
F/f M/m
tcb1
Photo: U. Nebraska-Lincoln
♀silk
Photo: Tarek Siala
♂tassel
Photo: Henry Mühlpfordt
																							Pollen				
Pistil
M	 m	
F- ✓ ✗
ff ✓ ✓
F/f M/m
tcb1
Meyerowitz 1994 Current Biology
Duvick et al. 1999 US 6639132 B1
maize origins
Tripsacum extinct maizeF1F1
maize orig
TF1
allopatric
maize
ff;mm
allopatric
mexicana
ff;M-
M m
F- ✓ ✗
ff ✓ ✓
Meyerowitz 1994 Current Biology
Duvick et al. 1999 US 6639132 B1
maize origins
Tripsacum extinct maizeF1F1
maize orig
TF1
allopatric
maize
ff;mm
allopatric
mexicana
ff;M-
M m
F- ✓ ✗
ff ✓ ✓
Meyerowitz 1994 Current Biology
Duvick et al. 1999 US 6639132 B1
maize origins
Tripsacum extinct maizeF1F1
maize orig
TF1
allopatric
maize
ff;mm
allopatric
mexicana
ff;M-
Meyerowitz 1994 Current Biology
Duvick et al. 1999 US 6639132 B1
maize origins
Tripsacum extinct maizeF1F1
mexicana
ff;M-
Meyerowitz 1994 Current Biology
Duvick et al. 1999 US 6639132 B1
maize origins
Tripsacum extinct maizeF1F1
maize
ff;MM
sympatry
ff;mm
M m
F- ✓ ✗
ff ✓ ✓
Meyerowitz 1994 Current Biology
Duvick et al. 1999 US 6639132 B1
maize origins
Tripsacum extinct maizeF1F1
maize orig
TF1
allopatric
maize
ff;mm
allopatric
mexicana
ff;M-
Meyerowitz 1994 Current Biology
Duvick et al. 1999 US 6639132 B1
maize origins
Tripsacum extinct maizeF1F1
mexicana
ff;M-
Meyerowitz 1994 Current Biology
Duvick et al. 1999 US 6639132 B1
maize origins
Tripsacum extinct maizeF1F1
maize
ff;MM
sympatry
FM haplotype arises & increases in
frequency in sympatry due to reinforcement
ff;mm FF;MM
M m
F- ✓ ✗
ff ✓ ✓
Meyerowitz 1994 Current Biology
Duvick et al. 1999 US 6639132 B1
maize origins
Tripsacum extinct maizeF1F1
maize orig
TF1
allopatric
maize
ff;mm
allopatric
mexicana
ff;M-
Meyerowitz 1994 Current Biology
Duvick et al. 1999 US 6639132 B1
maize origins
Tripsacum extinct maizeF1F1
mexicana
ff;M-
Meyerowitz 1994 Current Biology
Duvick et al. 1999 US 6639132 B1
maize origins
Tripsacum extinct maizeF1F1
maize
ff;MM
sympatry
fM increases in sympatric maize due to
extra pollination afforded by M
FF;MM
M m
F- ✓ ✗
ff ✓ ✓
A a
Genotype Fitness
A A 1
A a 1	–	0.5s
a a 1	–	s	
Genotype Fitness
A A 1	–	s	
A a 1	–	0.5	s
a a 1	
F1
Meyerowitz 1994 Current Biology
Duvick et al. 1999 US 6639132 B1
Tripsacum extinct maizeF1
Alison Wardlaw
mexicana (A) maize (a)
Yaniv Brandvain
r
F	M							
m
A
0 200 400 600 800 1000
0.0
0.2
0.4
0.6
0.8
1.0
Genotype	Frequency
Generation
Meyerowitz 1994 Current Biology
maize origins
Tripsacum extinct maizeF1F1
Meyerowitz 1994 Current Biology
Duvick et al. 1999 US 6639132 B1
Tripsacum extinct maizeF1F1
0 200 400 600 800 1000
0.0
0.2
0.4
0.6
0.8
1.0
mexicana (A)
maize (a)
m = 0.1
s = 1
r = 0.01
fMA
FMA
FmA
fmA
FMa
fMa
Fma
fma
0 200 400 600 800 1000
0.0
0.2
0.4
0.6
0.8
1.0
Genotype	Frequency
Generation
Meyerowitz 1994 Current Biology
maize origins
Tripsacum extinct maizeF1F1
Meyerowitz 1994 Current Biology
Duvick et al. 1999 US 6639132 B1
Tripsacum extinct maizeF1F1
0 200 400 600 800 1000
0.0
0.2
0.4
0.6
0.8
1.0
FML
fML
FmL
fmL
FMl
fMl
Fml
fml
M at high frequency in mexicana
F at low frequency
f,m at high frequency in maize
fMA
FMA
fma
fMa
mexicana (A)
maize (a)
m = 0.1
s = 1
r = 0.01
fMA
FMA
FmA
fmA
FMa
fMa
Fma
fma
0 200 400 600 800 1000
0.0
0.2
0.4
0.6
0.8
1.0
Genotype	Frequency
Generation
Meyerowitz 1994 Current Biology
maize origins
Tripsacum extinct maizeF1F1
Meyerowitz 1994 Current Biology
Duvick et al. 1999 US 6639132 B1
Tripsacum extinct maizeF1F1
0 200 400 600 800 1000
0.0
0.2
0.4
0.6
0.8
1.0
FML
fML
FmL
fmL
FMl
fMl
Fml
fml
fMA
FMA
fma
fMa
mexicana (A)
maize (a)
m = 0.1
s = 1
r = 0.01
fMA
FMA
FmA
fmA
FMa
fMa
Fma
fma
F increases in mexicana
due to selection against
maize pollen
0 200 400 600 800 1000
0.0
0.2
0.4
0.6
0.8
1.0
Genotype	Frequency
Generation
Meyerowitz 1994 Current Biology
maize origins
Tripsacum extinct maizeF1F1
Meyerowitz 1994 Current Biology
Duvick et al. 1999 US 6639132 B1
Tripsacum extinct maizeF1F1
0 200 400 600 800 1000
0.0
0.2
0.4
0.6
0.8
1.0
FML
fML
FmL
fmL
FMl
fMl
Fml
fml
fMA
FMA
fma
fMa
mexicana (A)
maize (a)
m = 0.1
s = 1
r = 0.01
fMA
FMA
FmA
fmA
FMa
fMa
Fma
fma
F increases in mexicana
due to selection against
maize pollen
M increases in maize due
to sexual selection for
increased pollination
0 200 400 600 800 1000
0.0
0.2
0.4
0.6
0.8
1.0
Genotype	Frequency
Generation
Meyerowitz 1994 Current Biology
maize origins
Tripsacum extinct maizeF1F1
Meyerowitz 1994 Current Biology
Duvick et al. 1999 US 6639132 B1
Tripsacum extinct maizeF1F1
0 200 400 600 800 1000
0.0
0.2
0.4
0.6
0.8
1.0
FML
fML
FmL
fmL
FMl
fMl
Fml
fml
fMA
FMA
fma
fMa
mexicana (A)
maize (a)
m = 0.1
s = 1
r = 0.01
fMA
FMA
FmA
fmA
FMa
fMa
Fma
fma
M in maize overcomes
rep. isolation; allele
frequencies equilibrate
Reinforcement
Generation
0 200 400 600 800 1000
0.2
0.4
0.6
0.8
1.0
Lu	et	al.	2014	Plant	Repro.
of the tested tubes had clustered callose plugs (Fig. 6).
Incompatible pollen tube growth in Ga2-s was distinct
from both Tcb1-s and Ga1-s. Like Tcb1-s and Ga1-s, the
Ga2-s barrier caused clustered callose plugs (18 % of
Ga2-s
8 HAP
(55)
9)
(60)
nts after
Ga1-s Ga2-stcb1
Phenotype )94(27)05(69)05(001 98 (50)
Tcb1-s
*
Silks
Pollen tcb1 ga1 ga2
d
n
r
e
e
of the silk length in Ga1-s and 8 % of the silk length in
Ga2-s (Fig. 3b). All three barriers are pre-zygotic and
caused by arrest of pollen tube growth. However, these
crossing barriers have different strengths in blocking
incompatible pollen.
0
20
40
60
80
100
tcb1 Tcb1-s Ga1-s Ga2-s
tcb1pollentubelength
(%ofthesilk)
(b)
Silk genotype
(40)
(50)
(62) (55)
Ga1-F Ga2-F
FF
ff
m
Allopatry Sympatry
Locus mex maize mex maize
tcb1 fM fm FM fm
ga1 fM fm FM fM
ga2 fM fm FM fM
Lu	et	al.	2014	Plant	Repro.
of the tested tubes had clustered callose plugs (Fig. 6).
Incompatible pollen tube growth in Ga2-s was distinct
from both Tcb1-s and Ga1-s. Like Tcb1-s and Ga1-s, the
Ga2-s barrier caused clustered callose plugs (18 % of
Ga2-s
8 HAP
(55)
9)
(60)
nts after
Ga1-s Ga2-stcb1
Phenotype )94(27)05(69)05(001 98 (50)
Tcb1-s
*
Silks
Pollen tcb1 ga1 ga2
d
n
r
e
e
of the silk length in Ga1-s and 8 % of the silk length in
Ga2-s (Fig. 3b). All three barriers are pre-zygotic and
caused by arrest of pollen tube growth. However, these
crossing barriers have different strengths in blocking
incompatible pollen.
0
20
40
60
80
100
tcb1 Tcb1-s Ga1-s Ga2-s
tcb1pollentubelength
(%ofthesilk)
(b)
Silk genotype
(40)
(50)
(62) (55)
Ga1-F Ga2-F
FF
ff
m
Allopatry Sympatry
Locus mex maize mex maize
tcb1 fM fm FM fm
ga1 fM fm FM fM
ga2 fM fm FM fM
Lu	et	al.	2014	Plant	Repro.
of the tested tubes had clustered callose plugs (Fig. 6).
Incompatible pollen tube growth in Ga2-s was distinct
from both Tcb1-s and Ga1-s. Like Tcb1-s and Ga1-s, the
Ga2-s barrier caused clustered callose plugs (18 % of
Ga2-s
8 HAP
(55)
9)
(60)
nts after
Ga1-s Ga2-stcb1
Phenotype )94(27)05(69)05(001 98 (50)
Tcb1-s
*
Silks
Pollen tcb1 ga1 ga2
d
n
r
e
e
of the silk length in Ga1-s and 8 % of the silk length in
Ga2-s (Fig. 3b). All three barriers are pre-zygotic and
caused by arrest of pollen tube growth. However, these
crossing barriers have different strengths in blocking
incompatible pollen.
0
20
40
60
80
100
tcb1 Tcb1-s Ga1-s Ga2-s
tcb1pollentubelength
(%ofthesilk)
(b)
Silk genotype
(40)
(50)
(62) (55)
Ga1-F Ga2-F
FF
ff
m
Allopatry Sympatry
Locus mex maize mex maize
tcb1 fM fm FM fm
ga1 fM fm FM fM
ga2 fM fm FM fM
Lu	et	al.	2014	Plant	Repro.
of the tested tubes had clustered callose plugs (Fig. 6).
Incompatible pollen tube growth in Ga2-s was distinct
from both Tcb1-s and Ga1-s. Like Tcb1-s and Ga1-s, the
Ga2-s barrier caused clustered callose plugs (18 % of
Ga2-s
8 HAP
(55)
9)
(60)
nts after
Ga1-s Ga2-stcb1
Phenotype )94(27)05(69)05(001 98 (50)
Tcb1-s
*
Silks
Pollen tcb1 ga1 ga2
d
n
r
e
e
of the silk length in Ga1-s and 8 % of the silk length in
Ga2-s (Fig. 3b). All three barriers are pre-zygotic and
caused by arrest of pollen tube growth. However, these
crossing barriers have different strengths in blocking
incompatible pollen.
0
20
40
60
80
100
tcb1 Tcb1-s Ga1-s Ga2-s
tcb1pollentubelength
(%ofthesilk)
(b)
Silk genotype
(40)
(50)
(62) (55)
Ga1-F Ga2-F
FF
ff
m
Nabogame
Ixtlan
Santa	Clara
Puruandiro
Opopeo
El	Porvenir
Tenango	del	Aire
Xochimilco
San	Pedro
Amatlan
✦ 16	sympatric	pairs	
✦ 2	allopatric	mexicana
Fstmex-maizeadmxiturediversity
Mb
Fstmex-maizeadmxiturediversity
Mb
Fstmex-maizeadmxiturediversity
Mb Mb Mb
maize
mexicana
B73:g/g
sample:?/?
x
19 F1 g/?
GBS, identify
both alleles
♀
♂
♂
x
B73:s/s
♀
?
x ?
♂
x
B73:g/g
♀
?
x ?
A
B
unknown	
sample
tester:	
ff;mm
19	F1
genotype	to	
find	both	
alleles
maize
mexicana
B73:g/g
sample:?/?
x
19 F1 g/?
GBS, identify
both alleles
♀
♂
♂
x
B73:s/s
♀
?
x ?
♂
x
B73:g/g
♀
?
x ?
A
B
tester:	ff;mmtester:	FF;MM
• how	different	are	dynamics	of	funcXonal	haplotypes		
among	populaXons?	
• inbreeding	depression,	local	selecXon,	migraXon	
differences	
• how	does	evoluXon	of	reinforcement	change	with	3	
interrelated	loci?	
• pollen	compeXXon,	epistasis,	mutaXon	change	stability?	
• how	do	alleles	at	these	loci	evolve?	
• M	in	maize	should	originate	from	local	mexicana	
• M	in	allopatric	mexicana	arises	de	novo?	
• M,F	should	show	selecXon	in	maize,	mexicana
• gene	flow	plays	key	role	in	maize	landraces	and	teosinte
• gene	flow	plays	key	role	in	maize	landraces	and	teosinte
• adapXve	introgression	associated	with	maize	colonizaXon	of	highlands
• gene	flow	plays	key	role	in	maize	landraces	and	teosinte
• adapXve	introgression	associated	with	maize	colonizaXon	of	highlands
• likely	selecXon	against	hybrids	and	for	reinforcement	in	teosinte
• gene	flow	plays	key	role	in	maize	landraces	and	teosinte
• adapXve	introgression	associated	with	maize	colonizaXon	of	highlands
• likely	selecXon	against	hybrids	and	for	reinforcement	in	teosinte
• sexual	selecXon	seems	to	prevent	stable	reinforcement
• gene	flow	plays	key	role	in	maize	landraces	and	teosinte
• adapXve	introgression	associated	with	maize	colonizaXon	of	highlands
• likely	selecXon	against	hybrids	and	for	reinforcement	in	teosinte
• sexual	selecXon	seems	to	prevent	stable	reinforcement
• great	system	to	study	dynamics	of	post-maXng	prezygoXc	isolaXon	
• geneXc	tools	(mulXple	references,	mapping	populaXons)	
• natural	populaXons	
• experimental	inbreds	with	all	combinaXons	of	alleles	at	all	loci
Acknowledgments
HiLo Group
Graham Coop
Sherry Flint-Garcia
Matt Hufford
Ruben Rellan
Dan Runcie
Ruairidh Sawers
Lab Alumni
Matt Hufford (Iowa State)
Tanja Pyhäjärvi (Oulu)
Joost van Heerwaarden (Wageningen)
PanZea
Ed Buckler
John Doebley
Mike McMullen
UMN
Yaniv Brandvain
Alison Wardlaw
UCR
Norm Ellstrand
Pesach Lubinsky Carnegie Institution
Matt Evans
Introgression
No	Introgression
K = 2
K = 7
K = 6
K = 5
K = 4
K = 3
K = 8
K = 9
K = 10
mexicana maize references
Kermicle	2006	GeneXcs	
Ellstrand	et	al.	2007	J.	Heredity
sympatric	
F-;M-
seed	set	of	
fm	gamete	
(rel.	to	self)
allopatric	
ff;M-
●
●
0.10
0.12
0.14
introgression nonintrogression
percentageofdeleteriousalleles(%)
group
introgression
nonintrogression
Photos: Matt Hufford, Brandon Gaut, Anna O’Brien

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Gene flow and cross-incompatibility in maize and teosinte

  • 1. Adaptive (and not so adaptive) introgression between maize and teosinte Jeffrey Ross-Ibarra @jrossibarra • www.rilab.org Dept. Plant Sciences • Center for Population Biology • Genome Center University of California Davis photo by lady_lbrty
  • 3. Hopkins 2013 New Phyt.Servedio 2004 PloS Bio
  • 4. Hopkins 2013 New Phyt.Servedio 2004 PloS Bio with little population differentiation, even though trait frequencies may differ greatly due to local adaptation. This creates relatively greater mating opportunities for foreign, rare males in each pop- ulation, directly countering the effects of local adaptation and re- ducing population differentiation at a trait locus. Importantly, stronger preferences exaggerate this effect. Fisherian sexual selec- tion is thus a double-edged sword in the development of isolation under these conditions, potentially driving differentiation in allop- atry but removing it if there is contact. Ultimately its role in allo- patric speciation is tenuous, failing even if contact is initiated after substantive trait and preference divergence has occurred. Model and Results We consider a two-locus population genetic model with polygyny (Methods). Locus T has alleles T1 and T2, which control two sexually selected phenotypes in males. Locus P determines a fe- male preference; P1 females are 1 + α1 times as likely to mate with a T1 than a T2 male upon encounter, whereas P2 females similarly prefer T2 males with preference strength 1 + α2. Our basic model, in accordance with the Fisherian models of Lande (4) and Kirkpatrick (13), does not include costs to preferences (this assumption is varied below). Our models are haploid to facilitate analyses, but the key factors that lead to our qualitative results should be readily generalizable to diploids. We assume that two allopatric populations have diverged such that individ- uals in population 1 have primarily P1 and T1 alleles and those in population 2 have primarily P2 and T2 alleles. Secondary contact occurs between these populations by symmetric migration with rate m. The onset of migration leads to variation in preferences and traits within each population, and linkage disequilibrium Fig. 1. Male trait and female preference frequencies show a decrease i their differentiation between populations when sexual selection is strong Servedio and Bürger 2014 PNAS
  • 5.
  • 6. Beadle 1979 Field Museum of Natural History parviglumis mays
  • 9. ssp. mexicana ssp. parviglumis ssp. mays Matsuoka et al. 2002 PNAS Piperno et al. 2009 PNAS the presence of maize (Table 2; Fig. 1); for comparison, Fig. S1A–C shows modern teosinte and maize starch grains. For example, the grains isolated from the preceramic- and ceramic- Fig. 1. Starch grains from maize recovered from early preceramic grinding stones 318d (A and B) and 318e (C and D). The grains have irregular shapes and surface contours, along with defined compression facets and transverse fis- sures (A) or y-shaped and other fissures (B–D). Table 2. Morphology of maize starch grains recovered from the Xihu Provenience Tool Cat. no. Shape Round Oval Bell Irregular Unit 1 Ceramic Layer B 310a 0 17 0 83 312a 0 0 0 100 Layer C 314c 46 0 0 54 315c 11 0 0 89 Preceramic Layer D 316c 0 0 0 100 316d 9 0 3 88 Layer E 318e 13 1 0 86 318d 5 0 0 90 319d 12 0 0 88 322c 9 0 0 91 Unit 2 Ceramic
  • 10. ssp. mexicana ssp. parviglumis ssp. mays Matsuoka et al. 2002 PNAS Piperno et al. 2009 PNAS the presence of maize (Table 2; Fig. 1); for comparison, Fig. S1A–C shows modern teosinte and maize starch grains. For example, the grains isolated from the preceramic- and ceramic- Fig. 1. Starch grains from maize recovered from early preceramic grinding stones 318d (A and B) and 318e (C and D). The grains have irregular shapes and surface contours, along with defined compression facets and transverse fis- sures (A) or y-shaped and other fissures (B–D). Table 2. Morphology of maize starch grains recovered from the Xihu Provenience Tool Cat. no. Shape Round Oval Bell Irregular Unit 1 Ceramic Layer B 310a 0 17 0 83 312a 0 0 0 100 Layer C 314c 46 0 0 54 315c 11 0 0 89 Preceramic Layer D 316c 0 0 0 100 316d 9 0 3 88 Layer E 318e 13 1 0 86 318d 5 0 0 90 319d 12 0 0 88 322c 9 0 0 91 Unit 2 Ceramic
  • 11. mexicana parviglumis South/Caribbean West Highland 0 500 1000 1500 2000 2500 m van Heerwaarden et al. 2011 PNAS clearly separated clusters, but evidence of admixture is inferred from domesticated maize alone. Because the genetic Fig. 1. (A) Map of sampled maize accessions colored by genetic group. (B) First three genetic PCs of all sampled accessions. EVOLUTION altitude mexicana parviglumis mays
  • 12. mexicana parviglumis Lauter et al. (2004) Genetics Pyhäjärvi et al. GBE 2013 Lauter et al. 2004 Genetics 0 10 20 30 40 60 80 100 120 days to pollen count subpsecies parviglumis mexicana Rodriguez et al. (2006) Maydica
  • 13. Environmental Association for temperature/altitude mexicana parviglumis Lauter et al. (2004) Genetics Pyhäjärvi et al. GBE 2013 Lauter et al. 2004 Genetics
  • 14. Days to Flowering highlandlowland daystoflowering HiLo field trials 2014,2016 (unpublished) Lowland Highland Photos: Ruairidh Sawers, LANGEBIO Lowland Field Highland Field
  • 15. Days to Flowering highlandlowland daystoflowering HiLo field trials 2014,2016 (unpublished) Lowland Highland Photos: Ruairidh Sawers, LANGEBIO Lowland Field Highland Field
  • 16. Days to Flowering highlandlowland daystoflowering HiLo field trials 2014,2016 (unpublished) Lowland Highland Photos: Ruairidh Sawers, LANGEBIO Lowland Field Highland Field
  • 18. K = 2 K = 5 K = 4 K = 3 mexicana maize references K = 7 K = 8 K = 9 K = 10 Hufford et al. 2013 PLoS GeneGcs
  • 20. El Porvenir Opopeo Xochimilco Puruandiro Tenango del Aire Ixtlan Nabogame Santa Clara San Pedro Allopatric Hufford et al. 2013 PLoS GeneGcs low elevation maize mexicana allele
  • 21. El Porvenir Opopeo Xochimilco Puruandiro Tenango del Aire Ixtlan Nabogame Santa Clara San Pedro Allopatric Hufford et al. 2013 PLoS GeneGcs low elevation maize mexicana allele
  • 22. El Porvenir Opopeo Xochimilco Puruandiro Tenango del Aire Ixtlan Nabogame Santa Clara San Pedro Allopatric Hufford et al. 2013 PLoS GeneGcs low elevation maize mexicana allele
  • 23. El Porvenir Opopeo Xochimilco Puruandiro Tenango del Aire Ixtlan Nabogame Santa Clara San Pedro Allopatric Hufford et al. 2013 PLoS GeneGcs low elevation maize mexicana allele0 1000 2000 3000 4000 5000 -447000 generations com 0 1000 2000 3000 4000 5000 -452000-450000 Santa Clara Likelihoods generations comp.loglikelihood 0 1000 2000 3000 4000 5000 -40650 generations com 0 1000 2000 3000 4000 5000 -420000-418500 Puruandiro Likelihoods generations comp.loglikelihood 0 1000 2000 3000 -418000 generations com 0 1000 2000 3000 -418000-416500 Opopeo Likelihoo generations comp.loglikelihood 55500-254000 San Pedro Likelihoods comp.loglikelihood 0000-288000 El Porvenir Likelihoods comp.loglikelihood -311500-310000 Ixtlan Likelihood comp.loglikelihood B 0 1000 2000 3000 4000 5000 -292 generations com 0 1000 2000 3000 4000 5000 -293000-291500-290000 Santa Clara Likelihoods generations comp.loglikelihood 0 1000 2000 300 -296500 generations com 0 1000 2000 300 -286000-284000 Puruandiro Like generations comp.loglikelihood maize into mexicana mexicana into maize generations since admixture
  • 25. 0 50 100 150 200 250 300 0.00.6 Chromosome 1 bp proportionofpopulations 0 50 100 150 200 0.00.6 Chromosome 2 bp proportionofpopulations 0 50 100 1 0.00.6 Chromosome 6 bp proportionofpopulations 0 50 100 150 0.00.6 Chromosome 7 bp proportionofpopulations Mb Mb MbMb B gt1 tb1bif2 zfl2 pbf1 zag1 ra1 Chr1: mexicana to maize 1-admixture Photo by Anna O’Brien Hufford et al. 2013 PLoS GeneGcs
  • 26. 0 50 100 150 200 0.00.6 Chromosome 3 bp proportionofpopulations 0 50 100 150 200 250 0.00.6 Chromosome 4 bp proportionofpopulations 0 50 100 15 0.00.6 Chromosome 8 bp proportionofpopulations 0 50 100 0.00.6 Chromosome 9 bp proportionofpopulations Mb Mb Mb Mb zag2 ba1 su1 tga1 bt2ga1 tcb1 Mb Chr4: maize to mexicana 0 50 100 150 200 250 300 0.00.6 Chromosome 1 bp proportionofpopulations 0 50 100 150 200 0.00.6 Chromosome 2 bp proportionofpopulations 0 50 100 1 0.00.6 Chromosome 6 bp proportionofpopulations 0 50 100 150 0.00.6 Chromosome 7 bp proportionofpopulations Mb Mb MbMb B gt1 tb1bif2 zfl2 pbf1 zag1 ra1 Chr1: mexicana to maize 1-admixture Photo by Anna O’Brien Hufford et al. 2013 PLoS GeneGcs
  • 27. Photo: U. Nebraska-Lincoln ♀silk Photo: Tarek Siala ♂tassel Photo: Henry Mühlpfordt Pollen Pistil M m F- ✓ ✗ ff ✓ ✓ F/f M/m tcb1
  • 28. Photo: U. Nebraska-Lincoln ♀silk Photo: Tarek Siala ♂tassel Photo: Henry Mühlpfordt Pollen Pistil M m F- ✓ ✗ ff ✓ ✓ F/f M/m tcb1
  • 29. Photo: U. Nebraska-Lincoln ♀silk Photo: Tarek Siala ♂tassel Photo: Henry Mühlpfordt Pollen Pistil M m F- ✓ ✗ ff ✓ ✓ F/f M/m tcb1
  • 30. Meyerowitz 1994 Current Biology Duvick et al. 1999 US 6639132 B1 maize origins Tripsacum extinct maizeF1F1 maize orig TF1 allopatric maize ff;mm allopatric mexicana ff;M- M m F- ✓ ✗ ff ✓ ✓
  • 31. Meyerowitz 1994 Current Biology Duvick et al. 1999 US 6639132 B1 maize origins Tripsacum extinct maizeF1F1 maize orig TF1 allopatric maize ff;mm allopatric mexicana ff;M- M m F- ✓ ✗ ff ✓ ✓
  • 32. Meyerowitz 1994 Current Biology Duvick et al. 1999 US 6639132 B1 maize origins Tripsacum extinct maizeF1F1 maize orig TF1 allopatric maize ff;mm allopatric mexicana ff;M- Meyerowitz 1994 Current Biology Duvick et al. 1999 US 6639132 B1 maize origins Tripsacum extinct maizeF1F1 mexicana ff;M- Meyerowitz 1994 Current Biology Duvick et al. 1999 US 6639132 B1 maize origins Tripsacum extinct maizeF1F1 maize ff;MM sympatry ff;mm M m F- ✓ ✗ ff ✓ ✓
  • 33. Meyerowitz 1994 Current Biology Duvick et al. 1999 US 6639132 B1 maize origins Tripsacum extinct maizeF1F1 maize orig TF1 allopatric maize ff;mm allopatric mexicana ff;M- Meyerowitz 1994 Current Biology Duvick et al. 1999 US 6639132 B1 maize origins Tripsacum extinct maizeF1F1 mexicana ff;M- Meyerowitz 1994 Current Biology Duvick et al. 1999 US 6639132 B1 maize origins Tripsacum extinct maizeF1F1 maize ff;MM sympatry FM haplotype arises & increases in frequency in sympatry due to reinforcement ff;mm FF;MM M m F- ✓ ✗ ff ✓ ✓
  • 34. Meyerowitz 1994 Current Biology Duvick et al. 1999 US 6639132 B1 maize origins Tripsacum extinct maizeF1F1 maize orig TF1 allopatric maize ff;mm allopatric mexicana ff;M- Meyerowitz 1994 Current Biology Duvick et al. 1999 US 6639132 B1 maize origins Tripsacum extinct maizeF1F1 mexicana ff;M- Meyerowitz 1994 Current Biology Duvick et al. 1999 US 6639132 B1 maize origins Tripsacum extinct maizeF1F1 maize ff;MM sympatry fM increases in sympatric maize due to extra pollination afforded by M FF;MM M m F- ✓ ✗ ff ✓ ✓
  • 35. A a Genotype Fitness A A 1 A a 1 – 0.5s a a 1 – s Genotype Fitness A A 1 – s A a 1 – 0.5 s a a 1 F1 Meyerowitz 1994 Current Biology Duvick et al. 1999 US 6639132 B1 Tripsacum extinct maizeF1 Alison Wardlaw mexicana (A) maize (a) Yaniv Brandvain r F M m A
  • 36. 0 200 400 600 800 1000 0.0 0.2 0.4 0.6 0.8 1.0 Genotype Frequency Generation Meyerowitz 1994 Current Biology maize origins Tripsacum extinct maizeF1F1 Meyerowitz 1994 Current Biology Duvick et al. 1999 US 6639132 B1 Tripsacum extinct maizeF1F1 0 200 400 600 800 1000 0.0 0.2 0.4 0.6 0.8 1.0 mexicana (A) maize (a) m = 0.1 s = 1 r = 0.01 fMA FMA FmA fmA FMa fMa Fma fma
  • 37. 0 200 400 600 800 1000 0.0 0.2 0.4 0.6 0.8 1.0 Genotype Frequency Generation Meyerowitz 1994 Current Biology maize origins Tripsacum extinct maizeF1F1 Meyerowitz 1994 Current Biology Duvick et al. 1999 US 6639132 B1 Tripsacum extinct maizeF1F1 0 200 400 600 800 1000 0.0 0.2 0.4 0.6 0.8 1.0 FML fML FmL fmL FMl fMl Fml fml M at high frequency in mexicana F at low frequency f,m at high frequency in maize fMA FMA fma fMa mexicana (A) maize (a) m = 0.1 s = 1 r = 0.01 fMA FMA FmA fmA FMa fMa Fma fma
  • 38. 0 200 400 600 800 1000 0.0 0.2 0.4 0.6 0.8 1.0 Genotype Frequency Generation Meyerowitz 1994 Current Biology maize origins Tripsacum extinct maizeF1F1 Meyerowitz 1994 Current Biology Duvick et al. 1999 US 6639132 B1 Tripsacum extinct maizeF1F1 0 200 400 600 800 1000 0.0 0.2 0.4 0.6 0.8 1.0 FML fML FmL fmL FMl fMl Fml fml fMA FMA fma fMa mexicana (A) maize (a) m = 0.1 s = 1 r = 0.01 fMA FMA FmA fmA FMa fMa Fma fma F increases in mexicana due to selection against maize pollen
  • 39. 0 200 400 600 800 1000 0.0 0.2 0.4 0.6 0.8 1.0 Genotype Frequency Generation Meyerowitz 1994 Current Biology maize origins Tripsacum extinct maizeF1F1 Meyerowitz 1994 Current Biology Duvick et al. 1999 US 6639132 B1 Tripsacum extinct maizeF1F1 0 200 400 600 800 1000 0.0 0.2 0.4 0.6 0.8 1.0 FML fML FmL fmL FMl fMl Fml fml fMA FMA fma fMa mexicana (A) maize (a) m = 0.1 s = 1 r = 0.01 fMA FMA FmA fmA FMa fMa Fma fma F increases in mexicana due to selection against maize pollen M increases in maize due to sexual selection for increased pollination
  • 40. 0 200 400 600 800 1000 0.0 0.2 0.4 0.6 0.8 1.0 Genotype Frequency Generation Meyerowitz 1994 Current Biology maize origins Tripsacum extinct maizeF1F1 Meyerowitz 1994 Current Biology Duvick et al. 1999 US 6639132 B1 Tripsacum extinct maizeF1F1 0 200 400 600 800 1000 0.0 0.2 0.4 0.6 0.8 1.0 FML fML FmL fmL FMl fMl Fml fml fMA FMA fma fMa mexicana (A) maize (a) m = 0.1 s = 1 r = 0.01 fMA FMA FmA fmA FMa fMa Fma fma M in maize overcomes rep. isolation; allele frequencies equilibrate
  • 41. Reinforcement Generation 0 200 400 600 800 1000 0.2 0.4 0.6 0.8 1.0
  • 42. Lu et al. 2014 Plant Repro. of the tested tubes had clustered callose plugs (Fig. 6). Incompatible pollen tube growth in Ga2-s was distinct from both Tcb1-s and Ga1-s. Like Tcb1-s and Ga1-s, the Ga2-s barrier caused clustered callose plugs (18 % of Ga2-s 8 HAP (55) 9) (60) nts after Ga1-s Ga2-stcb1 Phenotype )94(27)05(69)05(001 98 (50) Tcb1-s * Silks Pollen tcb1 ga1 ga2 d n r e e of the silk length in Ga1-s and 8 % of the silk length in Ga2-s (Fig. 3b). All three barriers are pre-zygotic and caused by arrest of pollen tube growth. However, these crossing barriers have different strengths in blocking incompatible pollen. 0 20 40 60 80 100 tcb1 Tcb1-s Ga1-s Ga2-s tcb1pollentubelength (%ofthesilk) (b) Silk genotype (40) (50) (62) (55) Ga1-F Ga2-F FF ff m
  • 43. Allopatry Sympatry Locus mex maize mex maize tcb1 fM fm FM fm ga1 fM fm FM fM ga2 fM fm FM fM Lu et al. 2014 Plant Repro. of the tested tubes had clustered callose plugs (Fig. 6). Incompatible pollen tube growth in Ga2-s was distinct from both Tcb1-s and Ga1-s. Like Tcb1-s and Ga1-s, the Ga2-s barrier caused clustered callose plugs (18 % of Ga2-s 8 HAP (55) 9) (60) nts after Ga1-s Ga2-stcb1 Phenotype )94(27)05(69)05(001 98 (50) Tcb1-s * Silks Pollen tcb1 ga1 ga2 d n r e e of the silk length in Ga1-s and 8 % of the silk length in Ga2-s (Fig. 3b). All three barriers are pre-zygotic and caused by arrest of pollen tube growth. However, these crossing barriers have different strengths in blocking incompatible pollen. 0 20 40 60 80 100 tcb1 Tcb1-s Ga1-s Ga2-s tcb1pollentubelength (%ofthesilk) (b) Silk genotype (40) (50) (62) (55) Ga1-F Ga2-F FF ff m
  • 44. Allopatry Sympatry Locus mex maize mex maize tcb1 fM fm FM fm ga1 fM fm FM fM ga2 fM fm FM fM Lu et al. 2014 Plant Repro. of the tested tubes had clustered callose plugs (Fig. 6). Incompatible pollen tube growth in Ga2-s was distinct from both Tcb1-s and Ga1-s. Like Tcb1-s and Ga1-s, the Ga2-s barrier caused clustered callose plugs (18 % of Ga2-s 8 HAP (55) 9) (60) nts after Ga1-s Ga2-stcb1 Phenotype )94(27)05(69)05(001 98 (50) Tcb1-s * Silks Pollen tcb1 ga1 ga2 d n r e e of the silk length in Ga1-s and 8 % of the silk length in Ga2-s (Fig. 3b). All three barriers are pre-zygotic and caused by arrest of pollen tube growth. However, these crossing barriers have different strengths in blocking incompatible pollen. 0 20 40 60 80 100 tcb1 Tcb1-s Ga1-s Ga2-s tcb1pollentubelength (%ofthesilk) (b) Silk genotype (40) (50) (62) (55) Ga1-F Ga2-F FF ff m
  • 45. Allopatry Sympatry Locus mex maize mex maize tcb1 fM fm FM fm ga1 fM fm FM fM ga2 fM fm FM fM Lu et al. 2014 Plant Repro. of the tested tubes had clustered callose plugs (Fig. 6). Incompatible pollen tube growth in Ga2-s was distinct from both Tcb1-s and Ga1-s. Like Tcb1-s and Ga1-s, the Ga2-s barrier caused clustered callose plugs (18 % of Ga2-s 8 HAP (55) 9) (60) nts after Ga1-s Ga2-stcb1 Phenotype )94(27)05(69)05(001 98 (50) Tcb1-s * Silks Pollen tcb1 ga1 ga2 d n r e e of the silk length in Ga1-s and 8 % of the silk length in Ga2-s (Fig. 3b). All three barriers are pre-zygotic and caused by arrest of pollen tube growth. However, these crossing barriers have different strengths in blocking incompatible pollen. 0 20 40 60 80 100 tcb1 Tcb1-s Ga1-s Ga2-s tcb1pollentubelength (%ofthesilk) (b) Silk genotype (40) (50) (62) (55) Ga1-F Ga2-F FF ff m
  • 50. maize mexicana B73:g/g sample:?/? x 19 F1 g/? GBS, identify both alleles ♀ ♂ ♂ x B73:s/s ♀ ? x ? ♂ x B73:g/g ♀ ? x ? A B unknown sample tester: ff;mm 19 F1 genotype to find both alleles maize mexicana B73:g/g sample:?/? x 19 F1 g/? GBS, identify both alleles ♀ ♂ ♂ x B73:s/s ♀ ? x ? ♂ x B73:g/g ♀ ? x ? A B tester: ff;mmtester: FF;MM • how different are dynamics of funcXonal haplotypes among populaXons? • inbreeding depression, local selecXon, migraXon differences • how does evoluXon of reinforcement change with 3 interrelated loci? • pollen compeXXon, epistasis, mutaXon change stability? • how do alleles at these loci evolve? • M in maize should originate from local mexicana • M in allopatric mexicana arises de novo? • M,F should show selecXon in maize, mexicana
  • 51.
  • 55. • gene flow plays key role in maize landraces and teosinte • adapXve introgression associated with maize colonizaXon of highlands • likely selecXon against hybrids and for reinforcement in teosinte • sexual selecXon seems to prevent stable reinforcement
  • 56. • gene flow plays key role in maize landraces and teosinte • adapXve introgression associated with maize colonizaXon of highlands • likely selecXon against hybrids and for reinforcement in teosinte • sexual selecXon seems to prevent stable reinforcement • great system to study dynamics of post-maXng prezygoXc isolaXon • geneXc tools (mulXple references, mapping populaXons) • natural populaXons • experimental inbreds with all combinaXons of alleles at all loci
  • 57. Acknowledgments HiLo Group Graham Coop Sherry Flint-Garcia Matt Hufford Ruben Rellan Dan Runcie Ruairidh Sawers Lab Alumni Matt Hufford (Iowa State) Tanja Pyhäjärvi (Oulu) Joost van Heerwaarden (Wageningen) PanZea Ed Buckler John Doebley Mike McMullen UMN Yaniv Brandvain Alison Wardlaw UCR Norm Ellstrand Pesach Lubinsky Carnegie Institution Matt Evans
  • 58.
  • 60. K = 2 K = 7 K = 6 K = 5 K = 4 K = 3 K = 8 K = 9 K = 10 mexicana maize references
  • 62.
  • 64. Photos: Matt Hufford, Brandon Gaut, Anna O’Brien