Evolu&on of ma&ng systems
Frequency-‐dependent selec0on, dominance-‐recessivity
and self-‐incompa0bility in plants.
Vincent CASTRIC – CNRS & Université Lille Unité Evolu&on-‐Ecologie-‐Paléontologie
M2 Orsay-‐ oct 18th, 2016
B I G Q U E S T I O N 1
2
B I G Q U E S T I O N 1
3
Phenotype space
How do novel phenotypes arise ?
W H A T C O N S T R A I N S T H E D I V E R S I F I C A T I O N P R O C E S S ?
4
Phenotype space
How do novel phenotypes arise ?
W H A T C O N S T R A I N S T H E D I V E R S I F I C A T I O N P R O C E S S ?
5
Phenotype space Fitness
How do novel phenotypes arise ?
W H A T C O N S T R A I N S T H E D I V E R S I F I C A T I O N P R O C E S S ?
6
Challenge 1 :
Fitness
landscape
Genotype space Phenotype
space Fitness
How do novel phenotypes arise ?
Challenge 1 : Fitness landscape
Challenge 2 : Gene0c networks
W H A T C O N S T R A I N S T H E D I V E R S I F I C A T I O N P R O C E S S ?
7
• The bewildering diversity of plant ma0ng systems : so many ways of doing it !
• Several different types of mul0allelic self-‐incompa0bility systems
• How natural selec0on acts on self-‐incompa0bility
• What self-‐incompa0bility tells us about the molecular
bases and evolu0on of dominance/recessivity interac0ons
Outline
Régime de reproduction:
Autofécondation ó Allofécondation
Autogamie (selfing)
Allogamie (outcrossing)
Diversité des systèmes de reproduction chez les végétaux supérieurs
Prépondérance des allogames
Régime mixte
(mixed mating)
Mécanismes régulant le régime de reproduc0on
1) Séparation temporelle: DICHOGAMIE Protogynie
t
1t
22) Séparation spatiale : HERKOGAMIE
Herkogamie simple
Herkogamie réciproque:
Hétérostylie
3) Systèmes d’auto-incompatibilité:
sporophytique di-
allélique: S & s Ss [S]
ss
[s]
Varia0on du nombre de catégories de partenaires sexuels (types sexuels)
• 1 catégorie: hermaphrodisme et pas d’auto-incompatibilité
• 2 catégories: dioécie
Varia0on du nombre de catégories de partenaires sexuels
• n catégories: hermaphrodisme et auto-incompatibilité multi-allélique
S1S2 S3S4 S5S6 S7S8
• 2 catégories: hermaphrodisme et auto-incompatibilité diallélique
Ss [S]
ss [s]
distylie
Systèmes d'auto-‐incompa0bilité:
systèmes mul0alléliques
Auto-pollinisation d'une plante S
1S
2Allo-pollinisation d'une plante S
1S
2S
1S
2S
1ou S
2S
1S
2S
3ou S
4S
3S
4Rejet ac0f de l'auto-‐pollen
Les différents systèmes
d’auto-‐incompa&bilité mul&allélique
• Systèmes gamétophy&ques (GSI): phénotype du pollen dépend uniquement de son génotype
haploïde
• Systèmes sporophy&ques (SSI): phénotype du pollen dépend du génotype diploïde du parent
– rela0ons de dominance entre allèles possibles
• Ex. Génotype "S1 S2" et Phénotype [S2] si S2 dominant sur
S1 dans l'anthère
Combien d’allèles? études empiriques
Méthodes: croisements réciproques + observations (descendance, allongement des tubes polliniques);
et/ou typage moléculaire
• GSI: n
échant.= {10, 12, 13, 17, 20, 21, 22, 28, 30, 31, 34, 36}
• SSI: n
échant.= {6, 11, 13, 16, 17, 18, 22, 35}
(revue de Castric &Vekemans 2004, Mol. Ecol. 13: 2873)
ð beaucoup d’allèles (haplotypes) au locus d’auto-
incompatibilité
Les différents systèmes d’auto-‐incompa&bilité mul&allélique:distribu&on et origine
• Seraient présents chez 40% des espèces d'Angiospermes
• Origine indépendante des systèmes gamétophy0ques et sporophy0ques
• GSI: très large distribu0on (monocot/eudicot); gène cloné chez Solanaceae, Plantaginaceae, Rosaceae,
Papaveraceae; ≥ 2 origines indépendantes
• SSI: ≥ 7 familles dont Brassicaceae, Asteraceae,
Convolvulaceae, Caryophyllaceae
S1
pollen pis&l
Goubet et al. (2012), Castric et al. (2013)
Self-‐incompa&bility: molecular lock-‐and-‐key
O U R B I O L O G I C A L M O D E L
17
SCR
SRK
≈ 31-‐110 kb
S1 S2 S3 S4
5’
Flanking 3’
Flanking
S-‐locus
SCR SRK
pollen pis&l
• Large number of haplotypes
• Specific lock-‐and-‐key combina0ons
O U R B I O L O G I C A L M O D E L
Self-‐incompa&bility: molecular lock-‐and-‐key
18
Goubet et al. (2012), Castric et al. (2013)
≈ 31-‐110 kb
S1 S2 S3 S4
5’
Flanking 3’
Flanking
S-‐locus
pollen pis&l
Self
pollina&on Cross pollina&on
No molecular docking Molecular
docking
Inhibi0on of self-‐pollen germina0on
Cross-‐pollen germina0on O U R B I O L O G I C A L M O D E L
Self-‐incompa&bility: molecular lock-‐and-‐key
19
Goubet et al. (2012), Castric et al. (2013)
SCR
SRK
Sélec0on fréquence-‐dépendante néga0ve
• Wright (1939): sélec&on fréquence-‐dépendante néga0ve sur le succès reproducteur mâle
L' haplotype-S2
rare est favorisé
• Wright (1939): sélec0on fréquence-‐dépendante néga0ve sur le succès reproducteur mâle
L' haplotype-S1 commun est
défavorisé
Sélec0on fréquence-‐dépendante néga0ve
• Conséquence de la co-‐dominance dans un système
sporophy0que: augmente les risques de rejet du pollen
Le phénotype co-dominant
S2S3
est défavorisé
Sélec0on fréquence-‐dépendante néga0ve
Combien d’allèles? Etudes théoriques: distribu0on (spectre) des fréquences alléliques
Locus neutre: équilibre mutation ó dérive génétique
proport ion d’a ll èl es
0.00 0.05 0.10 0.15 0.20
0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9
Fréquence allélique (x)
N = 10
6u = 5 10
-8n
a= 1.6
≠ allèles rares
1 allèle commun
"U-shaped frequency spectrum"
Temps
Fréquences alléliques
0
fixa&on d'un alllèle mutant élimina&on d'un
alllèle mutant
1
Combien d’allèles? Etudes théoriques:
distribu0on des fréquences alléliques
locus-S: (Wright 1939) équilibre
mutation ó dérive génétique ó sélection
0.00 0.05 0.10
0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9
Fréquence allélique (x)
N = 100 u = 5 10
-8n
a= 6.0
proport ion d’a ll èl es
è Prédiction théorique:
allèles S en fréquences
similaires ≈ 1/n
aTable 2 Occurrence of known S-alleles in the adult and offspring populations of A. halleri.
Number of individuals with 0, 1, 2 or 3 S-alleles detected, and number of individuals carrying each S-allele
Number of individuals with 0
S-allele 1 S-allele
2 S-alleles
3 S-alleles
AhSRK01 AhSRK02 AhSRK04 AhSRK12 AhSRK15 AhSRK20 AhSRK22 AHSRK24
Adult sample (n=322)
27 129 166 5 124 38 55 97 36 95 23 8
Offspring sample (n=245)
6 71 168 0 94 27 75 72 35 75 15 13
8 different S alleles in this population
Allele frequencies are far from equal ! … ?
Llaurens et al. (2009)
Maternal plants
GENOTYPES
S01S01 S01S02 S01S04 S01S12 S01S15 S01S20 S01S22 S02S02 S02S04 S02S12 S02S15 S04S12 S04S20 S12S15 S12S20 S20S24
Inferred paternal phenotype
S01S01 0.07
(0.05) 1.00 1.00 1.00 1.00 1.00 1.00 S1
S01S02 0.83 0.0
(0.0) 1.00 0.00 0.10 0.20 1.00 S2
S01S04 1.00 0.0
(0.0) 1.00 0.20 0.00 0.32 1.00 S4
S01S12 1.00 1.00 0.0
(-) 0.67 1.00 0.00 0.00 0.00 0.20 1.00 S12
S01S15 1.00 0.0
(0.17) 0.00 0.00 S15
S01S20 0.90 0.0
(-) 1.00 0.06 0.20 0.20 S20
S01S22 1.00 0.0
(-) S22
S02S02 0.00 1.00 0.0
(0.0) 0.00 1.00 S2
S02S04 1.00 0.10 0.0
(0.0) S4
S02S12 1.00 0.00 1.00 0.0
(-) 0.00 S12
S02S15 1.00 0.00 0.17
(0.0) 0.00 S15
S04S12 0.80 0.12 0.25 0.0
(-) S12
S04S20 0.97 0.00 0
(0.21) S20
S12S15 1.00 0.00 0.80 0.00 0.0
(0.13) S15
S12S20 1.00 0.10 0.2
(-) S20
S20S24 0.00 1.00 0.1
(-)
S20 or S20-S24 Inferred
maternal phenotype
S 1 S 2 S 4 S 1 2 S 1 5 S 2 0 S 2 2 S 2 S2-S4 S2-S12 S 1 5 S4-S12 S 2 0 S12-S15 S12-S20 S20 or
S20-S24
1
Controlled crosses between 16 A. halleri
Llaurens et al.Evolution 2009
à Dominance relationships between alleles
?
Most dominant
01
02 04
12 15 20
Pistil phenotype Most
recessive
01
02
04
12
20
Pollen phenotype
Observed dominance network
à Not strictly hierarchical
à Different b/w pollen and pistil
15
Dominance and intensity of selection
Billiard et al. 2007
Asymetrical intensity of selection:
stronger for dominant alleles weaker for recessive alleles
à “hiding” effect allows recessive
alleles to increase in frequency
0 0,1 0,2 0,3 0,4 0,5 0,6
AhSRK01 AhSRKS02AhSRK04 AhSRK12 AhSRK15 AhSRK20 AhSRK22 AhSRK24 Observed
Wright model - Pattern 1
Fecundity selection model - Pattern 1
S-alleles
Observedand expectedfrequencies
0 0,1 0,2 0,3 0,4 0,5 0,6
AhSRK01 AhSRKS02AhSRK04 AhSRK12 AhSRK15 AhSRK20 AhSRK22 AhSRK24 Observed
Wright model - Pattern 1
Fecundity selection model - Pattern 1
S-alleles
Observedand expectedfrequencies
à Asymetry of allele frequencies is well explained by position in the dominance network
Allele frequencies
Allele frequency varia0on
Offspring from 22 maternal plants, N=245
Llaurens et al. 2008
Tab l e 5 O b ser v ed a n d e x pec t ed f reque n c i es o f each S - a ll e l e i n t h e o ff spr i n g p o pu l a t i o n sa m p l e . S im ul a t i o n s ( N = 8 00, µ =10 - 6 ) wer e per f o r m e d
u n der W r i g h t ﾕs m o de l o f N F D S w i t h d o mi n a n ce i n t erac ti o ns acc o rd i n g to d o mi n an ce pa tte r n 1 ( see Fi g. 4 ) .
S - a ll e l e Obse r ved fr equency Ex pected 95 %
bounda ries
Ah S R K 0 1 0.263 0.25 - 0.32
Ah S R K 0 2 0. 065 0.05 - 0.09
Ah S R K 0 4 0.18 4* 0.08 - 0.13
AhSR K 12 0.156* 0.16 - 0.22
Ah S R K 15 0. 071 0.06 - 0.1
Ah S R K 20 0. 148 0.14 - 0.2
Ah S R K 22 0. 030* 0.04 - 0.08
Ah S R K 24 0.0 28 0 - 0.03
à Again, the observed variation of allele frequencies is compatible with a model of negative frequency-dependent selection
implementing the dominance network (but…)
Allele frequency varia0on
This effet is strong
It is only correctly understood when taking into account : - the complex dominance network
- the particular mode of selection (on male vs. male + female fitness)
Modifies the distribu0on of allelic frequencies and its evolu0on between successive genera0ons
Balancing selec0on
at the self-‐incompa0bility locus
• The bewildering diversity of plant ma0ng systems : so many ways of doing it !
• Several different types of mul0allelic self-‐incompa0bility systems
• How natural selec0on acts on self-‐incompa0bility
• What self-‐incompa0bility tells us about the molecular
bases and evolu0on of dominance/recessivity interac0ons
Outline
Raphael
MEHEUST Eléonore
DURAND Jonathan
KITT Pauline
GOUBET
L’équipe “Ecologie et évolu&on de l’auto-‐incompa&bilité”
Dominance/recessivity
Phenotypic effect of an allele (recessive) masqued
by that of another allele at the same locus (dominant).
Dominance/recessivity
wt/wt -‐/wt -‐/-‐
1
1-‐s trait
Dominance/recessivity
wt/wt -‐/wt -‐/-‐
?
1
1-‐s 1-‐hs
trait
Dominance/recessivity
wt/wt -‐/wt -‐/-‐
?
1
1-‐s 1-‐hs
trait
wt/wt -‐/wt -‐/-‐
h<0.5 recessive
Dominance/recessivity
wt/wt -‐/wt -‐/-‐
wt/wt -‐/wt -‐/-‐
?
h=0.5co-‐dominant
h<0.5 1
1-‐s 1-‐hs
trait
recessive
Dominance/recessivity
wt/wt -‐/wt -‐/-‐
?
1
1-‐s 1-‐hs
trait
wt/wt -‐/wt -‐/-‐
h=0.5
co-‐dominant
h<0.5 h>0.5
recessive dominant
copy (hence have higher than average heterozygous effect).
In the second case, because holes are independent of trait effects, heterozygous effects of strongly and mildly deleteri- ous mutations should be drawn from the same distribution and thus have the same mean value. The data on lethal mutations in Drosophila (Simmons and Crow 1977) and yeast (Szafraniec et al. 2003) clearly support the second possibility. The data on the fitness effect of gene deletion in yeast (Steinmetz et al. 2002) also show that strongly deleterious deletion (around 20% of the deletions) have independent heterozygous and homozygous effect as indi- cated by the analysis of Agrawal and Whitlock (2011). Using their “model7” (providing the best fit to the data), muta- tions with s = 0.05 have hs = 0.013 while mutations with s = 0.5 (a 10-times increase) have hs = 0.014 (a 1.06 times increase). In other words, mean heterozygote fitness is constant for a wide variation ofsvalues within the minority of deletion of large effect. Such a flat relationship is exactly
what is predicted if the ruggedness on homozygotes takes the form of holes as we intuitively present it (Figure 10B).
These observations show first that a smooth landscape model is not sufficient to account for the distribution of mutations of large effects. Second they show that incorpo- rating ruggedness in the form of holes (rather than thresh- olds) may account for the distribution of effect of this class of mutations. This is not so surprising; genetic incompati- bilities are commonplace as revealed by recent progress on the genetics of speciation (Orr and Presgraves 2000) or the observation that species can often have very similar pheno- types and yet cannot interbreed. Of course, this does not exclude the possibility that extreme trait values could be lethal or that environmental variation can cause some form of lethal fitness threshold too (Figure 10a), but it does sug- gest that incompatibilities are the main source of strongly deleterious mutation in the laboratory experiments men- tioned above. New data would be valuable to further study
Figure 9 Survey of empirical estimates of average dominance. We confronted our prediction (hRwithin [0.25–0.5] and closer to 0.25, shaded region) with different empirical estimates ofhR(with their confidence interval), across species and different traits.D. melanogaster: (A) viability (Chavarriaset al.
2001), (B) viability (Fry and Nuzhdin 2003), (C) female early fecundity, female late fecundity, male longevity, female longevity, male mating ability, weighted mean (not used to calculate our composite estimate of average dominance) (Houleet al. 1997), (D) viability, recalculated hR from different Mukai’s experiments (Simmons and Crow 1977).C. elegans: (E) productivity, survival to maturity, longevity, intrinsic rate of increase, convergence rate, generation rate (Vassilievaet al. 2000), (F) relative fitness (Peters et al. 2003). Saccharomyces cerevisiae, (G) growth rate (Szafraniec et al. 2003). (H) Composite weighted estimate ofhR across studies 0.27 [CI 0.18–0.36].
Figure 10 Alternative models for mutations of large ef- fect and lethals. (A) The fitness function is truncated for extreme trait values: any mutation with effect larger than some fitness threshold has a much stronger deleterious effect than with a smooth landscape model. As a conse- quence, the average heterozygous effect of mutations of weak homozygous effect (pink) is necessarily smaller than that of mutations of large homozygous (blue). (B) Muta- tions of large effects and lethals result from genetic in- compatibilities unrelated to the trait values. For the sake of illustration, these incompatibilities are illustrated as small random holes on thefitness surface, but these holes are not necessarily a fixed feature of the fitness surface, they may differ across genetic background or environ- ments. In this case the average heterozygous effect of mild and strongly deleterious mutations (including lethal) is equal on average.
932 F. Manna, G. Martin, and T. Lenormand
Dominance/recessivity
à Most major-‐effect muta0ons are recessive;
i.e., the wild-‐type allele is almost always the dominant allele
Manna et al. 2012
What makes dominant alleles dominant and recessive alleles recessive ?
à A major scien0fic controversy of the XXth century
Fisher (1928):
Existence of dominance modifiers
Wright (1929, 1934)
MIR5629
Dominance/recessivity
« …there is a tendency always at work in nature which modifies the response of the organism to each mutant gene in such a way that the wild type tends to become dominant. » Fisher (Am. Nat. 1928)
à The dominance of wt alleles would have evolved to decrease the impact of muta0ons
à Fisher postulates the existence of genes M/m modifiers of dominance between alleles of other genes A/a
Dominance/recessivity
Wright (Am Nat. 1929)
Equilibrium frequency of allele a : µ /hs
à Selec0ve advantage exists but is very small !
Dominance/recessivity
Wright’s physiological model (1934)
Kaczer & Burns 1981 à Dominance = a simple physiological consequence
of the structure of metabolic networks
Dominance/recessivity
Le coup de grâce ?
Even in Chlamydomonas (mostly haploid), muta0ons tend to be recessive.
« This result falsifies Fisher's theory of dominance and provides strong support for the alterna0ve physiological theory. »
Orr, Nature 1991
Dominance/recessivity
What makes dominant alleles dominant and recessive alleles recessive ?
à A major scien0fic controversy of the XXth century
Fisher (1928):
Existence of dominance modifiers
Wright (1929, 1934):
Dominance modifiers very unlikely rather : physiological theory
(Kaczer & Burns 1981).
MIR5629
Dominance/recessivity
What makes dominant alleles dominant and recessive alleles recessive ?
à A major scien0fic controversy of the XXth century
Fisher (1928):
Existence of dominance modifiers
Wright (1929, 1934):
Dominance modifiers very unlikely rather : physiological theory
(Kaczer & Burns 1981).
MIR5629
0-‐1 ✔
✗
Dominance/recessivity
… an old and resolved issue ?
Main argument : low heterozygote frequency
… but what about gene0c systems in which heterozygote frequency is high ?
-‐ selec0on in heterogeneous environnement -‐ during spread of a favorable allele
-‐ heterozygote avantage
-‐ nega0ve frequency-‐dependant selec0on
O}o & Bourget (Am. Nat 1999)
Dominance/recessivity
Self-‐incompa&bility in the flowering plants
Self-‐incompa&bility in the flowering plants
✔
S1
SCR SRK
pollen pis&l
Goubet et al. (2012), Castric et al. (2013)
Brassicaceae self-‐incompa&bility at a glance
≈ 31-‐110 kb
S1 S2 S3 S4
5’
Flanking 3’
Flanking
S-‐locus
SCR SRK
pollen pis&l
Goubet et al. (2012), Castric et al. (2013)
Brassicaceae self-‐incompa&bility at a glance
• Large number of haplotypes
• Specific lock-‐and-‐key combina0ons
≈ 31-‐110 kb
S1 S2 S3 S4
5’
Flanking 3’
Flanking
S-‐locus
SCR SRK
pollen pis&l
Self
pollina&on Cross pollina&on
No molecular docking Molecular
docking
Inhibi0on of self-‐pollen germina0on
Cross-‐pollen germina0on
Goubet et al. (2012), Castric et al. (2013)
Brassicaceae self-‐incompa&bility at a glance
mécanisme moléculaire
Hi sco ck e t a l., T RP S SCR1
SCR2 SRK1
SRK3
Pollen S1/ S2
Pis0l S1/ S3
molecular recognition
signalling pathway
Self-‐incompa&bility in the Brassicaceae
(from Schierup &
Vekemans 2008 Curr.
Op. Pl. Biol. 11: 116)
A textbook example of balancing (nega0ve frequency-‐dependent) selec&on
è mul0allelism (Wright 1939)
è long-‐term maintenance of S-‐alleles (Vekemans & Slatkin 1994) è high heterozygosity
Self-‐incompa&bility in the Brassicaceae
[S
2] [S
1] S
2,S
1S 2 >S 1
Dominance/recessivity
at the self-‐incompa&bility locus
Dominance/recessivity
at the self-‐incompa&bility locus
7
Le réseau de dominance chez Arabidopsis
Arabidopsis lyrata Arabidopsis halleri
Castric et al., 2008
Ah01 Ah03 Ah28 Ah29Ah10 Ah04 Ah12 Ah13 Ah20 Ah15
=>>>>>>>
?
Dr Éléonore Durand
> 50 haplotypes
→ > 1225 combinaisons hétérozygotes possibles !
→ 26/45 combinaisons testées
→ 1 seul cas de codominance
→ Hiérarchie de dominance linéaire
Eléonore DURAND
Ah01 Ah03 Ah04 Ah12 Ah13 Ah20
Ah01
" " " " "
Ah03 1.00(5)0.00(9)11 " " "
"
Ah04 1.00(10)0.00(22)22 1.00(10)1
0.07(15)1 " "
"
Ah12 1.00(12)0.00(19)22 0.83(6)1
0.00(5)1 0.90(20)1 & 2
0.09(23) 1 & 2 "
"
Ah13 1.00(5)0.00(4)11 0.83(12)1
0.00(10)1 1.00(11)1
0.08(13)1 1.00(10)1
0.00(11)1
Ah20 0.90(10)0.00(16)22 1.00(5)0.00(5)11 0.97(32)0.00(15)22 1.00(11)0.10(10)2 2 0.00(11)0.00(11)11
Dominance is prevalent:
almost no co-‐dominance.
Dominance/recessivity
at the self-‐incompa&bility locus
7
Le réseau de dominance chez Arabidopsis
Arabidopsis lyrata Arabidopsis halleri
Castric et al., 2008
Ah01 Ah03 Ah28 Ah29Ah10 Ah04 Ah12 Ah13 Ah20 Ah15
=>>>>>>>
?
Dr Éléonore Durand
> 50 haplotypes
→ > 1225 combinaisons hétérozygotes possibles !
→ 26/45 combinaisons testées
→ 1 seul cas de codominance
→ Hiérarchie de dominance linéaire
Eléonore DURAND
Ah01 Ah03 Ah04 Ah12 Ah13 Ah20
Ah01
" " " " "
Ah03 1.00(5)0.00(9)11 " " "
"
Ah04 1.00(10)0.00(22)22 1.00(10)1
0.07(15)1 " "
"
Ah12 1.00(12)0.00(19)22 0.83(6)1
0.00(5)1 0.90(20)1 & 2
0.09(23) 1 & 2 "
"
Ah13 1.00(5)0.00(4)11 0.83(12)1
0.00(10)1 1.00(11)1
0.08(13)1 1.00(10)1
0.00(11)1
Ah20 0.90(10)0.00(16)22 1.00(5)0.00(5)11 0.97(32)0.00(15)22 1.00(11)0.10(10)2 2 0.00(11)0.00(11)11
Ah01 Ah03 Ah04 Ah12
Ah13
=
Ah20> > > >
Dominance is prevalent:
almost no co-‐dominance.
Dominance/recessivity
at the self-‐incompa&bility locus
7
Le réseau de dominance chez Arabidopsis
Arabidopsis lyrata Arabidopsis halleri
Castric et al., 2008
Ah01 Ah03 Ah28 Ah29Ah10 Ah04 Ah12 Ah13 Ah20 Ah15
=>>>>>>>
?
Dr Éléonore Durand
> 50 haplotypes
→ > 1225 combinaisons hétérozygotes possibles !
→ 26/45 combinaisons testées
→ 1 seul cas de codominance
→ Hiérarchie de dominance linéaire
Eléonore DURAND
Linear hierarchy
Ah01 Ah03 Ah04 Ah12 Ah13 Ah20
Ah01
" " " " "
Ah03 1.00(5)0.00(9)11 " " "
"
Ah04 1.00(10)0.00(22)22 1.00(10)1
0.07(15)1 " "
"
Ah12 1.00(12)0.00(19)22 0.83(6)1
0.00(5)1 0.90(20)1 & 2
0.09(23) 1 & 2 "
"
Ah13 1.00(5)0.00(4)11 0.83(12)1
0.00(10)1 1.00(11)1
0.08(13)1 1.00(10)1
0.00(11)1
Ah20 0.90(10)0.00(16)22 1.00(5)0.00(5)11 0.97(32)0.00(15)22 1.00(11)0.10(10)2 2 0.00(11)0.00(11)11
Dominance/recessivity
at the self-‐incompa&bility locus
Allele frequencies
in natural popula0ons Pa}erns of molecular evolu0on
V. LLAURENS ET AL.
Figure 3.Frequencies of S-haplotypes observed in the adult population and predicted from finite population simulations according to dominance pattern 1 assuming three dominance classes in pistils and strictly hierarchical relationships in pollen (see Fig. 4). Black bars:
observed frequencies in adult population; white bars: expected frequencies under Wright’s model; gray bars: expected frequencies under the fecundity selection model; error bars represent the 95% confidence intervals obtained across 10,000 simulation runs.
AhS22 was dominant over AhS01. Overall, these results demon- strate for six S-haplotypes (all but AhS22 and AhS24) that they are expressed and functional inA. halleri.
COMPARING OBSERVED AND EXPECTED HAPLOTYPE FREQUENCIES IN THE ADULT POPULATION
When computing S-allele frequencies in the adult population sample, we assumed that when each of the most recessive S- haplotypes AhS01, AhS02, and AhS04 were found alone in an individual, this individual was a homozygote. The results showed that AhS01, the most recessive S-haplotype, had by far the highest observed frequency, as expected from theory (Fig. 3). In contrast, for the other haplotypes, we found no clear relationship between frequencies and dominance levels.
To simulate the evolution of haplotype frequencies at the S- locus, we used the dominance interactions inferred from the exper- imental pollinations, and for the unresolved cases (see above) we tested three alternative dominance patterns (Fig. 4). Under both frequency-dependent selection models (Wright’s and fecundity selection models), pattern 1 provided the best fit to the empirical data, followed closely by pattern 2, whereas the worst fit was ob- tained when assuming strict codominance among all S-haplotypes (Table 3). This analysis demonstrates that the pattern of domi- nance interactions among S-haplotypes has a paramount influence on haplotype frequencies in natural populations. Wright’s model under patterns of dominance 1 and 2 significantly outperformed
(!AIC>25) the fecundity selection model (Table 3, Fig. 3).
The rank orders of likelihoods of the different models and dom- inance patterns were consistent under various mutation ratesµ and population sizesN(results not shown).
HAPLOTYPE DIVERSITY AT THE S-LOCUS
To determine whether haplotype diversity at the S-locus in this population was compatible with a model of mutation/drift/NFDS, we recorded the proportion of simulation runs in which any of the eight S-haplotypes was lost (Table 4). Both models of selection showed similar overall proportions of haplotype loss, with only 21% and 24% of simulations losing at least one S-haplotype, under Wright’s model and the fecundity selection model, respectively.
However, the distributions of allele losses were strikingly different between models. In Wright’s model, only recessive S-haplotypes (AhS01, AhS02, or AhS04) were likely to be lost, whereas domi- nant S-haplotypes (AhS22 and AhS24) were more susceptible to drift in the fecundity selection model. This suggests either that the population is young and will probably lose S-haplotypes in the future, or that low but recurrent levels of gene flow into the population are maintaining the observed haplotype diversity.
As we found 33 individuals with no S-haplotype identified in a total of 567 individuals (5.8%), we are certainly missing one or a few additional S-haplotypes. Because the number of gene copies observed for S-haplotypes ranged from 21 (AhS24) to 218 (AhS01), with a median around 100, it is likely that we did not miss 2 5 5 2 EVOLUTIONOCTOBER 2008
Llaurens et al. Evolu0on 2008 Goubet et al. PLoS Gene0cs 2012
