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The Genomic Signatures of Highland
Adaptation in Maize
Matthew Hufford
Iowa State University
Overview of Talk
1) Background on Landrace Adaptations
2) Highland Adaptation through Introgression
3) Parallel Adaptation to the Highlands
Overview of Talk
1) Background on Landrace Adaptations
2) Highland Adaptation through Introgression
3) Parallel Adaptation to the Highlands
Improved
Landraces
Teosinte
Vigouroux et al. 2008
Mark Miller
Highland Adaptation in Maize Landraces
Southwestern US Highlands
Adaptations to:
✦ Cooler
temperature
✦ Lower
partial pressure
of atmospheric gases
✦ Higher
Mexican Central Plateau
Guatemalan Highlands
Andes
UV radiation
6
Highland Phenotypes
mexicana
✦
Highland mexicana and
lowland parviglumis
distinguished by pigment
and macrohairs
✦
Both traits are thought to
be adaptations to highland
conditions
✦
Highland maize landraces
share these traits
parviglumis
Lauter et al. (2004) Genetics
Highland Maize
Lowland Maize
Are Highland Traits Adaptive?
Barthakur (1974) Int. J Biomet
Overview of Talk
1) Background on Landrace Adaptations
2) Highland Adaptation through Introgression
3) Parallel Adaptation to the Highlands
Local Adaptation through Introgression
mexicana
parviglumis
altitude (m)
*
altitude (m)
0 - 500
0 - 500
500 - 1,000
500 - 1,000
1,000
- 1,500
- 2,000
1,0001,500
- 1,500
2,000 - 2,500
1,5002,500
- 2,000
- 3,000
2,000 - 2,500
2,500 - 3,000
Hufford et al. (2013) PLoS Genetics
±
±
0
125 250
0
500 Kilometers
125 250
500 Kilometers
Background: Evidence for Hybridization
✦ mexicana
maize
✦
is sympatric to
hybrids are frequently
found
Maize
mexicana
Photo by Pesach Lubinsky
✦ 20%
admixture of highland
maize with mexicana
Wilkes (1977) Economic Botany
van Heerwaarden et al. (2011) PNAS
Photo by John Doebley
Ixtlan
Puruandiro
El Porvenir
Santa Clara
Opopeo
Tenango del Aire
Nabogame
Sample:
✦
✦
✦
✦
✦
9 sympatric population pairs
2 allopatric references
120 mexicana
95 maize
40,000 SNPs
Hufford et al. (2013) PLoS Genetics
Xochimilco
San Pedro
Amatlan
Genome-wide Introgression: HAPMIX
✦
Utilizes a Hidden Markov Model
(HMM)
✦
Admixed chromosomes modeled
as mosaics of ancestral
haplotypes
Price et al. (2009) PLoS Genetics
Genome-wide Introgression: STRUCTURE
✦
Site-by-site assignment
using the linkage model
Chromosome 4: maize
✦
Loci created from SNPs
separated by < 5kb
(~20,000 loci)
Chromosome 4: mexicana
✦
Considers all populations
Falush et al. (2003) Genetics
Hufford et al. (2013) PLoS Genetics
Mb
Identifying Introgressed Regions
Chromosome 4: maize (STRUCTURE)
Chromosome 4: maize (HapMix)
0
50
100
150
Mb
Characterized by:
Low FST
Many shared variants
Few fixed differences
Long shared haplotypes
Hufford et al. (2013) PLoS Genetics
200
250
Common Introgression: Chromosome 4
Hufford et al. (2013) PLoS Genetics
El Porvenir
El Porvenir
Opopeo
Opopeo
Santa Clara
Santa Clara
Nabogame
Nabogame
Puruandiro
Puruandiro
Xochimilco
Xochimilco
Tenango del Aire
Tenango del Aire
San Pedro
San Pedro
Ixtlan
Ixtlan
Allopatric
Allopatric
*
*
*
Common Introgression: Chromosome 9
El Porvenir
Opopeo
Santa Clara
Nabogame
*
Puruandiro
Xochimilco
Tenango del Aire
San Pedro
*
Ixtlan
*
Allopatric
Hufford et al. (2013) PLoS Genetics
*
*
Pairwise FST:
Populations with and without Introgression
Introgression
No
Introgression
Hufford et al. (2013) PLoS Genetics
Overlap with QTL in Teosinte
Lauter et al. (2004) Genetics
Barthakur (1974) Int. J. Biometeor.
Greenblatt (1968) Maize Genet. Coop.
✦
9 common mexicana
introgression regions into
maize
✦
6 overlap with 5 QTL for
pigment and macrohairs in
teosinte
✦
mhl1 locus on chromosome 9
fine-mapped
Moose et al. (2004) Genetics
Phenotypes under Highland Conditions
No Introgression
Introgression
Hufford et al. (2013) PLoS Genetics
Signature of Local Adaptation
Hufford et al. (2013) PLoS Genetics
Overview of Talk
1) Background on Landrace Adaptations
2) Highland Adaptation through Introgression
3) Parallel Adaptation to the Highlands
Two Independent Highland Adaptations in Maize
1. Adaptation to the
highlands of the Central
Plateau in Mexico
1
2
2. Adaptation to the
highlands of the Andes
in South America
Independent Highland Adaptation
24 Samples Each:
-Lowland Mexico
-Highland Mexico
-Lowland SA
-Highland SA
~40,000 SNPs, 55K chip
~90,000 SNPs, GBS
Takuno et al. (In Prep)
Fitting a Demographic Model
Without Introgression
With Introgression
Model IA
Model IB
Mode
tmex
NA
tD
tE
tF
NA
NB
NC
N1
N2
tD
tE
tF
Nmex
NB
NC
N1
N2
N2P
Lowland
NC
Highland
NA
tD
tE
tF
N1
tG
N2P
Mexico
Mexico
Lowland Highland
NC
NA
mexicana
Mexico
Lowlan
Takuno et al. (In Prep)
NC
Evidence for Parallel Adaptation?
✦
More adaptation in
parallel than expected by
chance
✦
Predominantly
independent adaptation
Takuno et al. (In Prep)
Parallel Highland Adaptation in Maize
✦
6 landraces per region
(n = 36)
✦
Illumina HiSeq to 30X
Depth
✦
High-density, genomewide analysis of parallel
adaptation
Acknowledgements
Jeffrey Ross-Ibarra
Shohei Takuno
Tanja Pyhäjärvi
Norm Ellstrand
Pesach Lubinski
Michael Devengenzo
Thanks!!
Questions?
email: [email protected]
Next Steps: Developing Near Isogenic Lines
Photos by Brian Gervais