complex patterns of local adaptation in teosinte

complex patterns of local adaptation in teosinte

Photo: Ma6hew B. Hufford Tanja Pyhäjärvi UC Davis COMPLEX PATTERNS OF LOCAL ADAPTATION IN TEOSINTE Local adapta8on •  Selec8on varies in space •  Local genotypes have on average a higher rela8ve fitness in their local habitat than genotypes origina8ng from other habitats •  “Evolu8on in ac8on” Mimulus gu)atus (Savolainen et al. 2007) (Lowry & Willis 2010) Objec8ves Detect and describe the gene8c basis of local adapta8on in teosinte Inves8gate the distribu8on of adap8ve varia8on among subspecies, popula8ons and along the genome •  Teosintes, Zea mays ssp. parviglumis & mexicana •  A lot of gene8c, phenotypic and environmental varia8on among popula8ons •  Gene8c tools and resources of maize available •  Large, outcrossing popula8ons Two subspecies of Zea mays •  Zea mays ssp. mexicana –  high eleva8ons (1600-­‐2700 m) –  larger spikelets (7-­‐11 mm), less branching in tassels (1-­‐30) –  more common to hybridize with maize •  Zea mays ssp. parviglumis –  lower eleva8ons (400-­‐1900 m) –  small spikelets (5-­‐8 mm), more tassel branching (1-­‐65) –  Rare crossing with maize mexicana parviglumis Photo: Ma6hew B. Hufford Doebley & Il8s 1980, Fukunaga et al. 2005 Local adapta8on in teosinte Differences between mexicana and parviglumis •  Macrohair amount •  Anthocyanin content •  Adapta8ons to high eleva8ons? mexicana Lauter et al. 2004 parviglumis Sampled popula8ons Genotype Data •  11 parviglumis, 10 mexicana popula8ons × 10-­‐12 plants per popula8on, 250 genotyped individuals •  Maize 55 000 SNP chip (Illumina) –  Targeted in genic regions –  Average distance between SNPs: 40 kb •  SNPs ader quality check: 37 000 74 climate & soil variables -­‐> 6 principal components (PCs) www.worldclim.org Mean annual temperature Mean annual precipitaHon !"
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Tracy-­‐Widom: 20 significant PCs Clustering corresponds sampled popula8ons LD pagerns Inv9e Ting et al. (1964) Alltogether, four large inversions: Inv1n, Inv4m, Inv9e, Inv9d Three approaches to detect gene8c basis of local adapta8on 1.  FST outliers under hierarchical model 2.  Popula8on-­‐specific outliers, FFT to iden8fy SNPs that are differen8ated in a single popula8on 3.  BAYENV Fundamental differences among the methods Hierarchical island model FST FST FCT FCT FST (Excoffier et al. 2009) Popula8on specific differen8a8on, FFT FST 1% FFT 1% •  FFT : the propor8on of total variance due to differen8a8on between a focal popula8on and all the other popula8ons (Yang 1998) BAYENV, test for correla8on between environment and allele frequencies •  For each SNP, compare two models: –  M0: Allele freq. determined by drid and structure –  M1: Allele freq. determined by drid, structure AND environment •  Bayes Factor for each SNP × environmental PC combina8on Bayes factor (Coop et al. 2010) Overlap between FST and BAYENV Bayes Factors vs. FST p-­‐value correla8on max. rho: -­‐0.2 Red line: 1% Cutoff for FST outliers Black dots: SNPs correlated with PC2 (temperature range) 1% Func8onal characteriza8on of candidate SNPs •  Several sets of outliers •  No enrichment of genic or non-­‐syn. SNPs, contrary to A. thaliana (Hancock et al. 2011) –  FST outliers enriched for non-­‐genic SNPs •  Genes associated with precipita8on were more oden leaf expressed •  Not in specific metabolic pathways or gene ontology categories Effect of single popula8ons Signal for associa8on with temperature range 4
2
Tenango del Aire
San Pedro
Xochimilco
Opopeo
Santa Clara
El Porvenir
Nabogame
Puruandiro
Puerta Encantada
Ixtlan
0
All
log(BayesFactor)
6
Spa8ally restricted environmental varia8on & restricted geographical distribu8on of rare alleles -­‐> false posi8ves? (Mathieson & McVean 2012) All
Tenango del Aire
San Pedro
Xochimilco
Opopeo
Santa Clara
El Porvenir
Nabogame
Puruandiro
Puerta Encantada
Ixtlan
Ahuacatitlan
EjutlaA
La Mesa
El Sauz
EjutlaB
San Lorenzo
Los Guajes
El Rodeo
Amatlan de Casas
La Cadena
Crucero Lagunitas
0.0
0.2
0.4
0.6
p-value FST
0.8
1.0
Effect of single popula8ons FST p-­‐value Differen8a8on along genome 6 x enrichment of FST outliers (p: <0.001) 12 x enrichment of FCT outliers (p: <0.001) Correla8on with al8tude and temperature within mexicana 33 x enrichment of SNPs associated with temperature range (p: <0.001) 8 x enrichment of SNPs associated topsoil type (p: <0.001) Candidates for local adap8on are enriched within inversions •  All four inversions are enriched for outlier SNPs Analysis
Both
parviglumis
mexicana
F
F
CT
!
ST
Variable
PC1
PC2
PC3
p-value
Inv1n
<0.001 (4.5)
0.032 (1.7)
<0.001 (5.7)
Inv4m
0.003 (3.7)
0.824
1.000
Inv9d
<0.001 (7.6)
<0.001 (3.9)
0.819
Inv9e
0.027 (2.2)
0.331
0.186
PC4
PC5
0.002 (2.7)
0.440
0.574
1.000
0.001 (3.1)
1.000
<0.001 (4.0)
0.938
PC6
PC1
PC2
0.672
0.450
0.616
1.000
1.000
0.016 (3.2)
0.859
0.290
0.045 (2.3)
0.687
1.000
0.728
PC3
PC4
PC1
0.261
0.271
0.001 (3.8)
1.000
1.000
1.000
1.000
1.000
<0.001 (33.0)
0.812
0.474
0.095
PC2
PC3
PC4
0.748
0.136
0.002 (3.9)
0.694
1.000
1.000
<0.001 (4.3)
1.000
1.000
0.027 (2.0)
1.000
<0.001 (8.2)
<0.001 (2.9)
<0.001 (2.7)
<0.001 (11.7)
<0.001 (6.3)
0.049 (1.6)
<0.001 (1.8)
0.705
0.866
Inv1n Fang et al. (2012) Conclusions •  Single popula8ons can have excess effect on signal of local adapta8on •  Methods have strong effect on what loci are iden8fied as underlying local adapta8on •  Some important factors, especially bio8c (e.g. herbivores, compe88on) are not reflected in our environmental PCs Corn learopper (Medina et al. 2012) Conclusions •  Large polymorphic inversions play role in teosinte local adapta8on •  Inversions suppress recombina8on and may be adap8ve because: –  Dobzhansky: they contain sets of co-­‐adapted alleles –  Kirkpatrick and Barton (2006): They capture locally adapted alleles • 
Dobzhansky 1948 Role in specia8on: once established, can accumulate incompa8bility genes Acknowledgements •  Coauthors: Maghew B. Hufford Jeffrey Ross-­‐Ibarra •  Sta8s8cal advice: Joost van Heerwaarden, Andrew Eckert •  Samples: Pesach Lubinsky & Norm Ellstrand, UC Riverside •  Lab: Lauren Sagara •  Funding: Correla8ons between al8tude, environment and taxonomy 30.0 1800 ssp. parviglumis ssp. parviglumis
Mean annual precipita8on Mean annual temperature 1600 25.0 ssp. mexicana
1400 ssp. mexicana 20.0 1200 1000 15.0 10.0 5.0 0.0 0 500 1000 1500 2000 Al8tude 2500 3000 800 600 400 200 0 0 500 1000 1500 2000 Al8tude 2500 3000