evolutionary genetics of hybrid maize

Evolutionary Genetics of Hybrid Maize

Jeffrey Ross-Ibarra www.rilab.org @jrossibarra

http://www.rilab.org

Gra

in Y

ield

Year

Gra

in Y

ield

Year

How has breeding affected diversity across the maize genome?

Gra

in Y

ield

Year


How has the genome responded to selection for increasing hybrid yield?

Gra

in Y

ield

Year


How has the genome responded to selection for increasing hybrid yield?

What is the genetic basis of hybrid vigor?

van Heerwaarden et al. 2012 PNAS

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• increasingly small, homogeneous germplasm making up ancestry of modern lines



• changing ancestry not selection (sweeps) drives diversity across all heterotic groups



• changing ancestry not selection (sweeps) drives diversity across all heterotic groups

• no evidence that popular lines have more good alleles

Genetic change within a single program: BSSS/BSCB1

Gerke et al. 2015 Genetics

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Morell, Buckler, and Ross-Ibarra. Nat. Rev. Genetics. 2012

Box 1 | Genetic load

Genetic load refers to the reduction in fitness caused by suboptimal genotypes in a population121. Genetic load can arise in a number of ways, including directional selection, recombination or mutation. Mutational load — the presence of deleterious mutations segregating in a population — is of particular interest for crop genomics. Deleterious mutations are most readily detected in protein-coding genes and can take several forms, including premature stop codons, splice site variants or insertions and deletions (indels) that result in the loss or impairment of protein function. These types of mutations are frequently associated with Mendelian disorders in humans, providing direct evidence that loss-of-function changes tend to be deleterious, particularly when homozygous122. Although most nonsynonymous mutations in plants are strongly deleterious, a sizable proportion are only slightly so, and these mutations may segregate at appreciable frequencies123.

Unambiguously deleterious mutations are fairly common in crop genomes17,54,124. Statistical analysis of homologous sequence from multiple genomes can identify amino acid changes that are likely to be disadvantageous (for example, REF. 125), but these comparative analyses benefit from transcriptomic data, as transcript variation among individuals may render some putatively deleterious mutations inconsequential120. Part a of the figure shows a hypothetical alignment of coding sequence from multiple grass species. The conserved nature of the histidine amino acid across species suggests that the nonsynonymous change (indicated by the red ‘G’) observed in maize is likely to be deleterious. Synonymous changes are shown in black.

Selection against deleterious mutations is hindered by Hill–Robertson effects — because of linkage, selection can only act on the net effect of both beneficial and deleterious mutations. Deleterious mutations should thus be enriched in regions of the genome in which recombination is suppressed and around the targets of strong positive selection126,127. Although neither prediction has yet been explicitly demonstrated in crops, patterns of residual heterozygosity in the maize genome support the first prediction14, and evidence from humans128 bears out the second. Whereas inbreeding can act to purge deleterious mutations129,130, drift can increase the frequency of deleterious mutations in small populations131,132. Drift is a stochastic process, and unique sets of deleterious alleles would be expected to increase in frequency in different breeding populations (for example, REF. 124). This is illustrated in part b of the figure, in which two nonsynonymous mutations (indicated by the red ‘A’s) in the ancestral population increase in frequency in two derived populations. Because drift operates independently in isolated populations, different breeding programs are likely to have a number of distinct, high-frequency deleterious mutations. Given that most deleterious mutations are at least partially recessive, crosses between lines from different breeding populations should exhibit complementation at these loci, explaining, at least in part, the widespread observation of heterosis.

Nature Reviews | Genetics

. . . A A C G C C T T C . . .

. . . A A C G A C T T C . . .

. . . A A C G C C T T C . . .

. . . A A C G A C T T C . . .

. . . A A C G A C T T C . . .

. . . A A C G A C T T C . . .

. . . A G A G G A C T C . . .

. . . C G A G G A C T C . . .

. . . A G G G G A C T C . . .

. . . A G G G G A C T C . . .

. . . A G G G G A C T C . . .

. . . A G A G G A C T C . . .

. . . A A C G A C T T C . . .

. . . A A C G C C T T C . . .

. . . A G A G G A C T C . . .

. . . C G A G G C C T C . . .

. . . A G G G G A C T C . . .

. . . A G A G G A C T C . . .

. . . A A C G C C T T C . . .

. . . A A C G C C T T C . . .

. . . A A C G C C T T T . . .

. . . A A C G C C T T T . . .

. . . A A C G C C T T T . . .

. . . A G A A G A C T C . . .

. . . A G A A G A C T C . . .

. . . A G A A G A C T A . . .

. . . A G A A G A C T C . . .

. . . A G A G G A C T C . . .

. . . A G A A G A C T C . . .

Derived population 1 Derived population 2

. . . A A T G C C T T C . . .

. . . A A C G C C T T T . . .

. . . A A C G C C T T T . . .

. . . A G G G G A C T C . . .

. . . A G A A G A C T C . . .

Gene 1

a

Gene 2

Gene 2 Gene 1 Gene 2

. . . A A C G A T C T C . . .

HisAsn Leu

AspAsn Leu

. . . A A T C A T C T C . . .

. . . A A C C A C C T C . . .

. . . A A C C A C C T T . . .

. . . A A T G C G T T C . . .

. . . A A C G C G T T C . . .

Ancestral populationb

Rice

Brachypodium

Sorghum

Maize

Gene 1

REVIEWS

NATURE REVIEWS | GENETICS ADVANCE ONLINE PUBLICATION | 5

© 2012 Macmillan Publishers Limited. All rights reserved







. . . A A C G C C T T C . . .

. . . A A C G A C T T C . . .

. . . A A C G C C T T C . . .

. . . A A C G A C T T C . . .

. . . A A C G A C T T C . . .

. . . A A C G A C T T C . . .

. . . A G A G G A C T C . . .

. . . C G A G G A C T C . . .

. . . A G G G G A C T C . . .

. . . A G G G G A C T C . . .

. . . A G G G G A C T C . . .

. . . A G A G G A C T C . . .

. . . A A C G A C T T C . . .

. . . A A C G C C T T C . . .

. . . A G A G G A C T C . . .

. . . C G A G G C C T C . . .

. . . A G G G G A C T C . . .

. . . A G A G G A C T C . . .

. . . A A C G C C T T C . . .

. . . A A C G C C T T C . . .

. . . A A C G C C T T T . . .

. . . A A C G C C T T T . . .

. . . A A C G C C T T T . . .

. . . A G A A G A C T C . . .

. . . A G A A G A C T C . . .

. . . A G A A G A C T A . . .

. . . A G A A G A C T C . . .

. . . A G A G G A C T C . . .

. . . A G A A G A C T C . . .


. . . A A T G C C T T C . . .

. . . A A C G C C T T T . . .

. . . A A C G C C T T T . . .

. . . A G G G G A C T C . . .

. . . A G A A G A C T C . . .

Gene 1

a

Gene 2


. . . A A C G A T C T C . . .

HisAsn Leu

AspAsn Leu

. . . A A T C A T C T C . . .

. . . A A C C A C C T C . . .

. . . A A C C A C C T T . . .

. . . A A T G C G T T C . . .

. . . A A C G C G T T C . . .


Rice

Brachypodium

Sorghum

Maize

Gene 1

REVIEWS








. . . A A C G C C T T C . . .

. . . A A C G A C T T C . . .

. . . A A C G C C T T C . . .

. . . A A C G A C T T C . . .

. . . A A C G A C T T C . . .

. . . A A C G A C T T C . . .

. . . A G A G G A C T C . . .

. . . C G A G G A C T C . . .

. . . A G G G G A C T C . . .

. . . A G G G G A C T C . . .

. . . A G G G G A C T C . . .

. . . A G A G G A C T C . . .

. . . A A C G A C T T C . . .

. . . A A C G C C T T C . . .

. . . A G A G G A C T C . . .

. . . C G A G G C C T C . . .

. . . A G G G G A C T C . . .

. . . A G A G G A C T C . . .

. . . A A C G C C T T C . . .

. . . A A C G C C T T C . . .

. . . A A C G C C T T T . . .

. . . A A C G C C T T T . . .

. . . A A C G C C T T T . . .

. . . A G A A G A C T C . . .

. . . A G A A G A C T C . . .

. . . A G A A G A C T A . . .

. . . A G A A G A C T C . . .

. . . A G A G G A C T C . . .

. . . A G A A G A C T C . . .


. . . A A T G C C T T C . . .

. . . A A C G C C T T T . . .

. . . A A C G C C T T T . . .

. . . A G G G G A C T C . . .

. . . A G A A G A C T C . . .

Gene 1

a

Gene 2


. . . A A C G A T C T C . . .

HisAsn Leu

AspAsn Leu

. . . A A T C A T C T C . . .

. . . A A C C A C C T C . . .

. . . A A C C A C C T T . . .

. . . A A T G C G T T C . . .

. . . A A C G C G T T C . . .


Rice

Brachypodium

Sorghum

Maize

Gene 1

REVIEWS









. . . A A C G C C T T C . . .

. . . A A C G A C T T C . . .

. . . A A C G C C T T C . . .

. . . A A C G A C T T C . . .

. . . A A C G A C T T C . . .

. . . A A C G A C T T C . . .

. . . A G A G G A C T C . . .

. . . C G A G G A C T C . . .

. . . A G G G G A C T C . . .

. . . A G G G G A C T C . . .

. . . A G G G G A C T C . . .

. . . A G A G G A C T C . . .

. . . A A C G A C T T C . . .

. . . A A C G C C T T C . . .

. . . A G A G G A C T C . . .

. . . C G A G G C C T C . . .

. . . A G G G G A C T C . . .

. . . A G A G G A C T C . . .

. . . A A C G C C T T C . . .

. . . A A C G C C T T C . . .

. . . A A C G C C T T T . . .

. . . A A C G C C T T T . . .

. . . A A C G C C T T T . . .

. . . A G A A G A C T C . . .

. . . A G A A G A C T C . . .

. . . A G A A G A C T A . . .

. . . A G A A G A C T C . . .

. . . A G A G G A C T C . . .

. . . A G A A G A C T C . . .


. . . A A T G C C T T C . . .

. . . A A C G C C T T T . . .

. . . A A C G C C T T T . . .

. . . A G G G G A C T C . . .

. . . A G A A G A C T C . . .

Gene 1

a

Gene 2


. . . A A C G A T C T C . . .

HisAsn Leu

AspAsn Leu

. . . A A T C A T C T C . . .

. . . A A C C A C C T C . . .

. . . A A C C A C C T T . . .

. . . A A T G C G T T C . . .

. . . A A C G C G T T C . . .


Rice

Brachypodium

Sorghum

Maize

Gene 1

REVIEWS








. . . A A C G C C T T C . . .

. . . A A C G A C T T C . . .

. . . A A C G C C T T C . . .

. . . A A C G A C T T C . . .

. . . A A C G A C T T C . . .

. . . A A C G A C T T C . . .

. . . A G A G G A C T C . . .

. . . C G A G G A C T C . . .

. . . A G G G G A C T C . . .

. . . A G G G G A C T C . . .

. . . A G G G G A C T C . . .

. . . A G A G G A C T C . . .

. . . A A C G A C T T C . . .

. . . A A C G C C T T C . . .

. . . A G A G G A C T C . . .

. . . C G A G G C C T C . . .

. . . A G G G G A C T C . . .

. . . A G A G G A C T C . . .

. . . A A C G C C T T C . . .

. . . A A C G C C T T C . . .

. . . A A C G C C T T T . . .

. . . A A C G C C T T T . . .

. . . A A C G C C T T T . . .

. . . A G A A G A C T C . . .

. . . A G A A G A C T C . . .

. . . A G A A G A C T A . . .

. . . A G A A G A C T C . . .

. . . A G A G G A C T C . . .

. . . A G A A G A C T C . . .


. . . A A T G C C T T C . . .

. . . A A C G C C T T T . . .

. . . A A C G C C T T T . . .

. . . A G G G G A C T C . . .

. . . A G A A G A C T C . . .

Gene 1

a

Gene 2


. . . A A C G A T C T C . . .

HisAsn Leu

AspAsn Leu

. . . A A T C A T C T C . . .

. . . A A C C A C C T C . . .

. . . A A C C A C C T T . . .

. . . A A T G C G T T C . . .

. . . A A C G C G T T C . . .


Rice

Brachypodium

Sorghum

Maize

Gene 1

REVIEWS








. . . A A C G C C T T C . . .

. . . A A C G A C T T C . . .

. . . A A C G C C T T C . . .

. . . A A C G A C T T C . . .

. . . A A C G A C T T C . . .

. . . A A C G A C T T C . . .

. . . A G A G G A C T C . . .

. . . C G A G G A C T C . . .

. . . A G G G G A C T C . . .

. . . A G G G G A C T C . . .

. . . A G G G G A C T C . . .

. . . A G A G G A C T C . . .

. . . A A C G A C T T C . . .

. . . A A C G C C T T C . . .

. . . A G A G G A C T C . . .

. . . C G A G G C C T C . . .

. . . A G G G G A C T C . . .

. . . A G A G G A C T C . . .

. . . A A C G C C T T C . . .

. . . A A C G C C T T C . . .

. . . A A C G C C T T T . . .

. . . A A C G C C T T T . . .

. . . A A C G C C T T T . . .

. . . A G A A G A C T C . . .

. . . A G A A G A C T C . . .

. . . A G A A G A C T A . . .

. . . A G A A G A C T C . . .

. . . A G A G G A C T C . . .

. . . A G A A G A C T C . . .


. . . A A T G C C T T C . . .

. . . A A C G C C T T T . . .

. . . A A C G C C T T T . . .

. . . A G G G G A C T C . . .

. . . A G A A G A C T C . . .

Gene 1

a

Gene 2


. . . A A C G A T C T C . . .

HisAsn Leu

AspAsn Leu

. . . A A T C A T C T C . . .

. . . A A C C A C C T C . . .

. . . A A C C A C C T T . . .

. . . A A T G C G T T C . . .

. . . A A C G C G T T C . . .


Rice

Brachypodium

Sorghum

Maize

Gene 1

REVIEWS



Complementation & Hybrid Vigor


• genetic drift explains most change in diversity



• little overlap in selected regions



• little overlap in selected regions

• complementation of deleterious alleles rather than overdominance likely basis of heterosis

How important are deleterious variants?

Mezmouk & Ross-Ibarra G3 2014

similar AAlikely neutral

similar AAlikely neutral

different AAlikely deleterious

nss

ts

0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 1

00.1

0.2

0.3

0.4

0.5

0.6

0.7

0.8

0.9

1

NSS

TRO

PICA

LDeleterious allele frequency

nss

ts

0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 1

00.1

0.2

0.3

0.4

0.5

0.6

0.7

0.8

0.9

1

NSS

TRO

PICA

L

nss

ts0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 1

00.1

0.2

0.3

0.4

0.5

0.6

0.7

0.8

0.9

1

ss

nss

0

0.1

0.2

0.3

0.4

0.5

0.6

0.7

0.8

0.9

1

0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 1SS

NSS

Deleterious allele frequency

23

45

67

89

chr10

−log10(p)

20 40 60 80 100 120 140

●

●●● ●

●

●

●●

●

●

●

Chromosome 1

Prop

ortio

n no

nsyn

omyo

us

0.0

0.4

0.8

7 42 77 119 168 217 266

Gore et al. 2009 ScienceLarièpe et al. 2012 Genetics


• deleterious alleles common, usually at low frequency in at least one group



• all traits show enrichment of genes with deleterious alleles



• all traits show enrichment of genes with deleterious alleles

• complementation of deleterious alleles in low recombination regions likely important for heterosis

Experimental test of deleterious complementation

Yang et al. bioRxiv 2017

B73 Mo17 PHZ51

B73

Mo17

PHZ51

B73 Mo17 PHZ51

B73

Mo17

PHZ51

Flowering Time

Height

Yield

GERP = Neutral rate - Estimated rate

High GERP (high function)

Low GERP (low function)

●

●●●

●●●

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TW DTP

DTS AS

I

PHT

EHT

GY

0

50

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200

BPH

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−10 −5 0 5

0.0

0.2

0.4

0.6

GERP Score

Del

eter

ious

Alle

le F

requ

ency

●

●

LR MZ LR MZ LR MZ

0.08

0.12

0.16

0.20

Del

eter

ious

Loa

d pe

r bp

0.6

0.8

1.0

1.2

Quantiles of cM/Mb

GER

P Sc

ore

25 50 75 100

a b

c d

All Sites

Fixed Segregating

aj, additive effect of the jth GERP-SNP; Xij, 0-1-2 coding of jth GERP-SNP on ith hybrid;

dj, dominance effect of the jth GERP-SNP; Wij, 0-1-0 coding of jth GERP-SNP on ith hybrid.

Heterosis increasing

Height YieldFlowering Time



Heterosis increasing

Height YieldFlowering Time



k > 1 Overdominance

k = 1 Dominance

k = -1 Recessive

k < -1 Underdominance

k = 0 Additive

0.00

0.01

0.02

0.03

0.0 0.5 1.0 1.5 2.0GERP Score

Add

itive

Effe

ct

0.00

0.01

0.02

0.03

0.0 0.5 1.0 1.5 2.0GERP Score

Dom

inan

t Effe

ct

0.0

0.1

0.2

0.3

0.4

0.0 0.5 1.0 1.5 2.0GERP Score

Deg

ree

of D

omia

nce

(k)

TW DTP DTS ASI PHT EHT GY

−1

0

1

2

Deg

ree

of D

omin

ance

(k)

TraitsTWDTPDTSASIPHTEHTGY3.

5e−0

64.

0e−0

64.

5e−0

65.

0e−0

6

0.1 0.2 0.3 0.4 0.5

Allele Frequency

Varia

nce

Expl

aine

d

ba

c d e

0.00

0.01

0.02

0.03

0.0 0.5 1.0 1.5 2.0GERP Score

Add

itive

Effe

ct

0.00

0.01

0.02

0.03

0.0 0.5 1.0 1.5 2.0GERP Score

Dom

inan

t Effe

ct

0.0

0.1

0.2

0.3

0.4

0.0 0.5 1.0 1.5 2.0GERP Score

Deg

ree

of D

omia

nce

(k)

TW DTP DTS ASI PHT EHT GY

−1

0

1

2

Deg

ree

of D

omin

ance

(k)

TraitsTWDTPDTSASIPHTEHTGY3.

5e−0

64.

0e−0

64.

5e−0

65.

0e−0

6

0.1 0.2 0.3 0.4 0.5

Allele Frequency

Varia

nce

Expl

aine

d

ba

c d e

GenotypeGERP Scores

*

* * *

YieldFlowering Height

GERP

YieldFlowering Height

random

Experimental test of deleterious complementation

• yield shows more dominance than other traits

• how deleterious an allele is matters for yield

• deleterious alleles are recessive (for yield)

• modeling complementation improves prediction of hybrid yield and heterosis 5-10%

Heterosis yield

Duvick 2005 Maydica

Hybrid yield

Inbred yield

Unasked for opinions on heterotic groups from a guy who knows nothing

about breeding

• The Good:

• intellectual & genetic control of germplasm

• hybrid vigor (it’s not all dominance)

• The Bad:

• diversity loss

• inefficient selection

Unasked for opinions on heterotic groups from a guy who knows nothing

about breeding

• Option 1:

• heterotic groups, but large Ne and genotype to enrich for recombination

• Option 2:

• mass (genomic) selection on randomly mated populations

Joost van Heerwaarden

Justin Gerke

Sofiane Mezmouk

Jinliang Yang

Wageningen University

Dupont Pioneer KWS U. Nebraska Lincoln