Evolutionary reasons for sex linkage

Evolutionary reasons for sex linkage

• Sexual conflict– Predicts initial X-linkage if genes that favor males but harm

females are recessive (Rice 1984)– Predicts initial Z-linkage when SA genes are dominant– Predict no bias once sex-limited

• Sexual selection: ornament-preference coevolution– Predicts faster evolution of female preference genes when there

are X-linked or autosomal ornaments and X-linked preferences (Kirkpatrick & Hall, 2004)

• Genomic conflict– Predicts faster evolution of female preference genes for X-linked

indicators of X-chromosome meiotic drive (Lande & Wilkinson, 1999)

Why does mode of inheritance matter?

Female Male

ZW ZZ

Female heterogamety

Male Female

XY XX

Male heterogamety

X-linked genes spend less time in males while Z-linked genesspend more time in males, compared to autosomal genes.

1. Sexual selection operates directly on males, indirectly on females.

Why does mode of inheritance matter?

Linkage disequilibrium arises due to joint inheritance of ornament and preference genes

Male Female

XY XX

X-linked

Male Female

XY XX

Autosomal

2. Linkage disequilibrium between trait and preference depends on mode

Preference-display inheritance

Pre

fere

nce

c ha n

g e

better

Thre

s ho l

d pr

efer

e nc e

better

Sexual selection and sex chromosomes(Kirkpatrick & Hall, 2004)

*

**

Do sexually selected traits exhibit sex-linkage?

• Are genes for sexually selected traits sex-linked?– YES – X

• Drosophila, mammals (Reinhold, 1998)• human reproductive traits (Saifa & Chandra

1999; Lercher et al. 2003)– YES – Z

• Butterflies (Prowell 1998; Iyengar 2002)• Birds (Saether et al. 2007; Wright 2005)

• Are genes with male-biased expression X-linked?– NO - under-represented

• Drosophila soma (Parisi et al., 2003)

– YES - over-represented• mosquitoes (Hahn & Lanzaro, 2005)• mouse spermatogonia (Wang et al. 2001; Yang

2006)

Outline• Stalk-eyed flies as a model for studying a sexually

selected trait• What regions (QTL) influence eyestalk

expression?• Which genes are expressed during eyestalk

development?• Does sex linkage influence the rate of evolution of

eyestalk genes?• Does sex linkage influence the expression of

eyestalk genes?

14 nuclear genesfull mtDNA genomes

Wiegmann et al. unpub.

Eyestalks have evolved in 8 families of Acalyptrate flies

Exaggerated eyestalks occur only in male flies

Achias rothschildiPlatystomatidae (New Guinea)

Diopsosoma primaPeriscelididae (Brazil)

Richardia telescopicaRichardiidae (Peru) Teleopsis whitei

Diopsidae (Malaysia)

Eye-Stalk Sexual Dimorphism has evolved repeatedly in DiopsidsTeloglabrus entabenensis

Dias. dubia

Dias. silvatica

Dias. obstans

Dias. fasciata

Dias. sp.F

Dias. sp.W

Dias. albifacies

Dias. sp.Q

Dias. meigeni

Dias. conjuncta

Dias. nebulosa

Dias. aethiopica

Dias. elongata

Dias. longipedunculata

Dias. hirsutu

Teleo. breviscopium

Teleo. rubicunda

Teleo. quadriguttata

Cyrto. dalmanni

Cyrto. whitei

Cyrto. quinqueguttata

Eurydiopsis subnottata

Diopsis apicalis

Diopsis fumipennis

Diopsis gnu

Sphyr. munroi

Sphyr. brevicornis

Sphyr. detrahens

Sphyr. beccarri

Monomorphic

EquivocalDimorphic

Most parsimonious reconstruction of sexual dimorphism in eyespan.

Body length

Eye

span

MalesFemales

Baker & Wilkinson 2001 Evolution

Sexual dimorphism evolves due to change in male eye span-body length allometry

Independent contrasts

Male slope Female slope

Sex

ual d

imor

phis

m

Teleopsis populations are genetically and reproductively isolated

NJ phylogram:

535 bp COII mtDNA535 bp 16s mtDNA655 bp wingless intron

Swallow et al. 2005 Mol. Ecol.

Belalong

Cameron/Langat

Bogor

Soraya

Bt Lawang

Gombak

Brastagi

Gombak

Chiang Mai

Bt Ringit

0.005 substitutions/site

100

T. dalmanni

T. whitei

T. quinquegutatta

100

100

100

100100

93

100

100

86

90

100

99

100

2.5 - 11 MYA

Male eyespan is under sexual selectionMales with longer eyespan roost and mate with more females (Wilkinson & Reillo 1994)

Eyespan is condition dependent, but relative eyespan has a genetic basis (Wilkinson & Taper 1999; David et al. 2000)

Male with longer relative eyespan are preferred by females (Wilkinson et al. 1998; Hingle et al. 2001)

Male with longer relative eyespan win contests (Panhuis et al. 1999)

Outline• Why use stalk-eyed flies as a model for studying

sexually selection traits?• Which genomic regions (QTL) influence eyestalk




eyestalk genes?

Selection on male eye span alters brood sex ratios

Wilkinson et al. 1998 Nature

Realized responsein eyespan

X drive can catalyze sexual selection

• If a male ornament indicates absence of the driving X chromosome

• then, choosy females, which avoid mating with SR males, will produce more grandchildren as long as there are more females than males in the population

• This process leads to rapid evolution of an autosomal female preference when genes for an ornament are linked to X drive

• Occasional recombination (or imprecise female choice) is necessary otherwise sexual selection should eliminate drive

Lande and Wilkinson 1999 Genet Res

QTL mapping of eye span

Gen 45 intercrossXDYL-XXH

738 flies (2 families)468 females270 males

Gen 30 intercrossXYH-XXL

490 flies (1 family)231 females259 males

Female-biased broods are due to X driveN

umbe

r of m

ales

test

ed

Chr 1 Chr 2

Chr XD

Chr X

Gen 30 F2 intercrossXY-XX

Gen 45 F2 intercrossXDY-XX

Drive X fails to recombine

QTL for relative eye span

Johns et al. 2005 Proc. R. Soc. Lond. B

Eye span indicates drive X

XD

Thus, females that choose long eye span mates produce more sons

Only dimorphic Teleopsis populations carry SR

10 changes

Wilkinson et al, 2003

C. dalm

anniC

. whitei

C. q.

= SR frequency

Sumatra

Sumatra

Pen Malaysia

Java

Pen Malaysia

Pen Malaysia

Thailand

Drive X evolves rapidly

70167125106

395

crc

71

312

21

6

18

2 X-linked regions autosomal gene

Number of segregating sites in 3 Kb sequence

Gom

bak

Driv

eN

= 1

1 m

ales

Gom

bak

Non

-driv

eN

= 1

4 m

ales

Sor

aya

N =

13

mal

es

25 29

14 13

0 13

Drive X evolves independently of autosomal genes

2 X regions 2 autosomal regions

Note that drive X lacks variation and is derived from nondrive X chromosomes

70167125106

395

crc

71

312

21

6

18

Drive X influences other traits

• Sperm length (drive sperm are shorter)• Sperm storage organ size in females• Sperm competition (drive sperm are less

competitive)• Male fertility (drive males are less fertile)• Mating rate (drive males mate less often)• Female fecundity (heterozygous females

produce more offspring)

• Consistent with a chromosomal region rather than a single pleiotropic gene


sexually selection?• What genomic regions (QTL) influence eyestalk




eyestalk genes?

EST Sequencing and Analysis• cDNA libraries were made from C. dalmanni eye-

antennal imaginal discs at 3 stages:– wandering larvae– 1-3 d pupae– 4-7 d pupae

• 24192 cDNAs were bidirectionally sequenced and annotated using the JGI EST pipeline and FlyBase

• EST assembly summary– Total # of high quality ESTs 33,229– # of clusters in assembly 7,066– # clusters w/ significant (e-9) Blast hits 4,422– # of unique protein genes 3,487– # ORFs > 300 bp w/out Blast hit 186– Average unique sequence per gene 1.65 Kb

Larval brain + eye disc

Eye-antennal imaginal disc

EST representation in GO categories essential to eye-stalk development

0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9

regulation of body size

cell growth

regulation of cell size

morphogenesis of an epithelium

actin cytoskeleton organization and biogenesis

Wnt/N/smo/fz/TGFb/InR signaling pathways

axonogenesis

growth

eye development

regulation of cell shape

eye-antennal disc morphogenesis

metamorphosis

cell motility

% of D.m. genes in EST database

Pre-pupalPupal 1-3Pupal 4-6

GO categories that exhibit over-representation with respect to developmental stage

0.0000

0.1000

0.2000

0.3000

0.4000

0.5000

0.6000

0.7000

0.8000

0.9000

All Gen

es

meiosis

embryo

nic morphogen

esis

anato

mical s

tructu

re form

ation

cell p

rolife

ration

transc

riptio

n

smoothen

ed si

gnaling path

way

axonogen

esis

protein fo

lding

carb

ohydrat

e meta

bolism

transm

ission of n

erve i

mpulse

structu

ral co

nstituen

t of c

uticle

Cuticular protein 30BCuticular protein 30FCuticular protein 49AaCuticular protein 49AcCuticular protein 49AeCuticular protein 56FCuticular protein 57ACuticular protein 62BbCuticular protein 62BcCuticular protein 64AcCuticular protein 65EcCuticular protein 66CaCuticular protein 66CbCuticular protein 66DCuticular protein 67Fa1Cuticular protein 76BdCuticular protein 92FCuticular protein 97EaCuticular protein 97EbCuticular protein 100A

Developmental Time






eyestalk genes?

Identifying sex-linked genes by CGH

• Designed custom 44K oligoarray– 60 bp oligo probes– 6-10 nonoverlapping probes/gene– 3,400 genes from EST library– ~200 ORFs

• Hybridize male and female genomic DNA– 4 replicates/sex/species– 4 Teleopsis species

• Expect X-linked genes in females to have 2-fold intensity of males

CGH chromosome inference:T. dalmanni

Freq

uenc

y

Median log2(F/M intensity)

Autosomal X

-7.5

Y

Freq

uenc

y

Median log2(F/M intensity)

Autosomal X

-7.5

Y

CGH chromosome inference:T. dalmanni

A X Y

A 27 0 0

X 0 7 0

Y 0 0 1

Chr Prediction

Chr

con

firm

atio

n

35/35 correct = 100%

PCR confirmation

Teleopsis has a neo-X = Dm 2L

Left neo-X

Moved onto neo-X

Schaeffer et al. 2008 Genetics

Note 1: Muller element A is the ancestral X

Note 2: X drive is common in obscura group flies, which have a fused X and also have a new Y chromosome which contains genes not on XR (Carvalho et al 2009)

Muller elements in Drosophila

Y replacement

Drosophila-Anopheles

synteny

53% of X-linked genes in A. gambiae are X-linked in D. melanogaster

Zdobnov et al. 2002 Science

Drosophila-Anopheles shared a common ancestor ~ 260 MYA

T. dalmanni - D. melanogaster synteny

Td chromosomeMuller element A+D C+E B

Gene movement ->

CGH chromosome inference:T. quinqueguttata

Freq

uenc

y

Median log2(M/F intensity)

Autosomal XY

-5.0

Median log2(CD M/F intensity)

Med

ian

log 2

(CQ

M/F

inte

nsity

)

Autosome

A X YA 3105 17 1X 12 560 0Y 2 0 0

Cd chr

Cqchr

2 = 2392P < 0.0001

X

XA

utosome

Recent gene movement

Gene movement to X is associated with increased dimorphism in Teleopsis

Genes may leave X chromosome to avoid X chromosome inactivation during meiosis

Sequence divergence using relative branch lengths

To identify genes that evolve faster in stalk-eyed flies than in Drosophila, we used relative branch lengths

All conseqs translated and aligned to transcript/gene alignments for 3 Drosophila species and Anopheles. Alignments for conseqs from same gene were concatenated prior to BL estimate. Trees constrained to ‘known’ topology generated with PhyML.

Distance measure: T.d. branch length / tree length

A. g.

D. m.

C. d.

D. p.

D. v.

A. g.

D. m.

C. d.

D. p.

D. v.scramb1:

CG10561:

Transposed genes show faster divergence

Teleopsis chromosomal location

Tel

eops

is b

ranc

h pr

op.

Sequence divergence by CGH

“Rec

ent”

gene

div

erge

nce

(Cd(

m+f

) - C

q(m

+f))

/(Cd(

m+f

) + C

q(m

+f))

Dm-Cd divergence (1-BlastX)

R2 = 0.23, P < 0.0001

To identify genes that have evolved rapidly between the dimorphic and monomorphic stalk-eyed flies, we used the relative difference in total signal intensity from the CGH microarray

CGH divergence and ancestral X movement

source F PCd-Cq div 9.4 < 0.0001

Note: excludes unique Cd genes (unknown location in Dm)

CD-CQ divergence is highest for Dm genes which move on or off the X in Cd

CGH divergence by Dm chromosome arm

*

source F PDm arm 32.4 < 0.0001

Divergence of eyespan genes is greatest for genes which are unique to C dalmanni

Gene Duplication in EST Database

• Tentatively assigned clusters as paralogs if >10% amino acid divergence for aligned regions and all clusters are monophyletic relative to D. mel and D. pseudo homologs

• Found 20 gene duplicates. Over-represented for genes involved in spermatogenesis and mRNA binding

• Possible duplicates: 234 cases in which two or more clusters had the top Blast hit to overlapping regions of the same D.m. gene

Cd B.Law crolA

Cd Gombak crolA

Cd Soraya crolA

Cd B.Law crolB

Cd Gombak crol

Cd B.Law crol

Cd Soraya crol

Cd Brunei crol

Cd Bogor crol

Cd Langat crol

Cw crol

Cd Bras crol

.40

.44

.67

.46

.50

1.15

1.18

.55

1.01

2.38

1.21

1.57

.16

.34.56

.50

.27

.77

.31

.38

.17

dN/dS

• Example: crooked legs, 3 copies confirmed by phylogenetic analysis of ~ 1700 bp of crol genes for 7 populations of C. dalmanni + C. whitei

xxxxxxxxxxx

zinc finger protein - 10 domainsCd Gom crol

Cd Gom crolA

Sex-linkage and gene duplication

• Gene duplications (21) preferentially involve neo-X– 11 homologs on neo-X (Dm 2L) and 10 on ancestral A– 2 = 14.1, P = 0.0002

• Genes involved in duplications are more likely to move chromosomes– 10 genes in 21 sets moved chromosomes (exp 2.8%)– 2 = 31.0, P < 0.0001

• Duplicate copies preferentially move off neo-X– 7 X -> A; 2 A -> X; 1 A -> Y

Sex-linkage and gene duplication evolution

-> X (Cd-Cq div: 0.48)-> auto (Cd-Cq div: 0.79)

-> 3R

-> 2R-> 2

One autosome -> X duplication/translocation:

Six autosome duplications: Mean CGH divergence change = 0.15 ± 0.04






eyestalk genes?

Sex-bias by species gene expression

• Comparison– Male vs female T. dalmanni and T. quinqueguttata– Using probes with least divergence in CGH

• Method– Sample: eye-antennal imaginal discs from 25

wandering larvae– Sex: genotyped larvae using X & Y-linked

microsat markers, then pooled discs by sex– Replicates: 8 samples/sex/spp with dye swap– Hybridized to 44k custom oligoarrays

• 5 nonoverlapping probes/gene• each probe printed in duplicate• 3320 unique genes• Used normalized (intensity – background) intensity

– Averaged log2(M/F intensity) over probes/gene

&

Sex-bias x species gene expression

SAM ANOVA569/1922 genes FDR < 0.1%

Sex-biased expression, sexual dimorphism and sex linkage

Ave

rage

log 2

(M/F

) exp

ress

ion

Ave

rage

log 2

(M/F

) exp

ress

ion

Sex-biased expression, sexual dimorphism and gene movement

Gene name Dm Td Tqcapulet 2L A XRNA polymerase II 215kD subunit X A YORF-65 X Aextradenticle X X Aaubergine 2L X ADeoxyribonuclease II 3R X AORF-25 X ASpindly 2L X ACG9246 2L X ALa autoantigen-like 2L X ARan GTPase activating protein 2L X Amitochondrial ribosomal protein L28 2L X APendulin 2L X Amsb1l 2L X ACG3305 2L X ACG14341 2L X ACG7870 2L X A

Sex-biased gene expression and gene movement among Teleopsis

Conclusions

• Exaggerated eyestalks are influenced by X-linked genes– X chromosome drive likely has influenced sexual selection and

may have facilitated evolutionary change due to restricted recombination.

• X chromosome history influences divergence rates– Gene movement on or off the X results in faster divergence.– Unique stalk-eyed fly genes evolve faster between sexually

monomorphic and dimorphic species– Gene duplications preferentially involve neo-X

• X linkage and history influence gene expression– Sexual dimorphism is associated with female bias among X-linked

genes– Genes that moved off the X show male-biased expression while

those that joined the X show female-biased expression in the dimorphic species, consistent with sexual conflict

AcknowledgementsCollaborator:

Rick Baker (AMNH)

Postdocs:Philip Johns (Bard College)Xianhui WangLeanna Birge (UCL)

Technicians:Marie PittsSarah Josway

Graduate students:Sarah ChristiansonJackie Metheny

Undergraduates: Cara Brand

and many others!

Gene expression between lines

• Comparison– High vs low lines after 50 generations

of selection on relative eye span• Method:

– Sample: eye-antennal imaginal discs from 25 wandering larvae

– Replicates: 8 samples per line, with dye swap

– Hybridized to 44k custom oligoarrays• three nonoverlapping oligos/gene• each oligo printed in triplicate• 3320 unique genes

– Average log2(H/L intensity) over probes/gene

Biased gene expression between lines

SAM (FDR = < 1%)176 biased clusters; 111 genes

19 sig genes unique to Cd

Gene expression and ancestral X transposition

source F PCd-Dm chr 1.6 0.19

N = 2969; excludes Cd genes with unknown location in Dm

Gene expression and recent sex chromosome transposition

source F PCq-Cd chr 1.06 0.38

N = 3053; includes Cd genes with unknown location in Dm

Gene expression by chromosome arm

Biased expression is greatest for

• 154 Cd genes which are not detected in Dm

• No effect of Cd X chromosome

*

source F PDm arm 9.0 < 0.0001

Cd chr 1.0 0.322

Where do drive chromosomes come from?

Hypothesis: drive chromosomes arise when new sex chromosomes evolve

because suppressors are initially absent

Biased sex ratios in medfliescaused by B chromosomes

Basso et al. 2009 PLoS One

Percent malesY+B X+B

Where do drive chromosomes come from?

Hypothesis: drive chromosomes arise when new sex chromosomes appear,

which in flies may be initiated by fusions of B chromosomes or other

elements

Candidate genes for expression regulation

Single amino-acid repeat polymorphisms (SARPs)– Common in coding sequences of transcription factors– Repeat expansions/contractions occur more often than point mutations– Can enhance or suppress transcription in a length dependent manner

Fondon & Gardner 2004

0

0.1

0.2

0.3

0.4

0.5

0.6

Q L F N S T A C D E G I Y P K V R H M W

AA repeat > 8 bp (N = 129)

AA abundance (N = 1651205)

Single amino-acid repeats in C. dalmanni EST database

Amino acid code

Pro

porti

on

Q repeat genes are most commonTranscription factors are over-representedGene divergence is less than for other genes

For homologous genes, Q repeats are longer in Cd than Dm

X AQ rep 9 54

all genes 542 2894

Chromosome location does not influence repeat length or purity

No. Cd - Dm Q repeats per gene

Q repeats vary in length between populations

Cd_CRC-A: 6 VLTQLTPPHSPPQTAASSAFPNASIETSTNVNDAPF-QVSSTPPLASPVQI--------- 55Dm_CRC-A: 148 ILQQLTPPQSPPQ------F------------DA-YKQAGDAQP--KPVLVKAEQKVQCY 186

Cd_CRC-A: 56 ---VTNDKFGSSAVQPTFLNFNNWQQQQQQQQQQQQEQQQQQNQHSTVGALNNEFNVDIA 112Dm_CRC-A: 187 TPDVTH---AASAT-P-F-NFTNW-----------------------VGG--SE----IA 211

Cd_CRC-A: 113 REMQIVDEIVNKRVKEL-FDSN----NDDCESMSSYSAPSQIES-ST-----------DE 155Dm_CRC-A: 212 RENQLVDDIVNMRAKELELSTNWQQLNEDCESQAS----SSLDSRSTGSGVCSSIADADE 267

Cd_CRC-A: 156 EWMP---CSSYSSAGSSPVHNGCEESSLKATATNGS--KKRTRPYGRGIEDRKLRKKEQN 210Dm_CRC-A: 268 DWVPELISSS-----SSPAPTTIEQSA--------SQPKKRTRTYGRGVEDRKIRKKEQN 314

Cd_CRC-A: 211 KNAATRYRQKKKLEMENVLSEEQQLTQRNDELKRILSDR 249Dm_CRC-A: 315 KNAATRYRQKKKLEMENVLGEEHVLSKENEQLRRTLQER 353

No Q repeats for D. melanogaster homologue in 4 of 63 genes, e.g.crc (cryptocephal): Ecdysone-regulated transcription factor

X-linked Q repeat genes tend to be more polymorphic

F = 4.31P = 0.051

Q repeat gene association study

275...298.

299.

300.

20

20

20

20

20

20

20

20

Sires(n = 300)

Dams(n = 300)

Offspring(n = 2000)

Breeding values/family

20

20

20

20

20

20

20

20

X =

=

=

=

=

=

=

=

1.

2.

3....25.

X

X

X

X

X

X

X

HQQQQQQQQQQL........................................................................................................................

Progeny breeding values

(n = 50 fams)

ParentalGenotypes

HQQQQ---QQQQQQL.....QQQ............QQQ............QQQ............QQQ............QQQ............QQQ............QQQ............QQQ............QQQ............QQQ.......

A. Screen variable loci (n=32)

A. Autosomal loci screen Female LS-ES Male LS-ES 1 2 3 Locus F P F P N 4 5 6 Bar1 0.45 0.77 0.62 0.65 92 7 Bifocal 1.46 0.20 1.89 0.09 91 8 CG4409 1.43 0.24 1.38 0.26 92 9 CG10082 1.57 0.18 1.77 0.13 88 10 CG10321 0.8 0.49 1.82 0.13 88 11 CG10435 0.04 0.85 0.04 0.84 89 12 CG11848 6.01 0.0002 4.72 0.0016 98 13 CG12104 3.19 0.046 2.09 0.13 89 14 CG31064 0.35 0.93 0.69 0.68 98 15 CG31224 1.11 0.37 1.76 0.10 73 16 CG32133 1.25 0.28 2.84 0.0079 88 17 CG33692 2.98 0.011 3.16 0.0074 98 18 CG34347 0.66 0.78 1.01 0.45 89 19 Cap-n-collar 0.55 0.58 0.57 0.57 89 20 Corto 2.25 0.022 2.59 0.0087 96 21 Domino 1.58 0.11 2.04 0.029 85 22 E5 0.85 0.43 0.90 0.41 84 23 Ecdysone-induced protein 75B 2.71 0.07 6.13 0.0032 91 24 Grainy head 1.09 0.38 1.38 0.22 86 25 M-spondin 0.37 0.83 0.75 0.56 87 26 Mastermind 1.52 0.21 2.19 0.08 88 27 SRPK 1.95 0.06 2.54 0.015 99 28 Tenascin major 0.56 0.57 1.91 0.15 90 29 Toutatis 1.07 0.40 1.23 0.28 89 30 Trachealess 0.82 0.44 3.00 0.055 92 31 32

A. X-linked loci screen Female LS-ES Male LS-ES 1 2 3 Locus Parent F P F P N 4 5 6 Bunched Male 0.22 0.80 0.42 0.66 45 7 Female 0.71 0.62 0.88 0.50 45 8

9 CG8668 Male 0.65 0.69 0.60 0.73 48 10 Female 0.64 0.77 1.18 0.34 46 11

12 CG10107 Male 4.18 0.011 3.03 0.039 48 13 Female 0.99 0.46 0.97 0.47 49 14

15 CG31738 Male 2.04 0.12 1.87 0.15 49 16 Female 0.81 0.55 1.83 0.13 50 17

18 Cryptocephal Male 0.82 0.54 1.28 0.29 50 19 Female 0.33 0.92 0.71 0.65 49 20 21

Q repeat gene association study

275...298.

299.

300.

20

20

20

20

20

20

20

20

Sires(n = 300)

Dams(n = 300)

Offspring(n = 2000)

20

20

20

20

20

20

20

20

X =

=

=

=

=

=

=

=

1.

2.

3....25.

X

X

X

X

X

X

X

HQQQQQQQQQQL........................................................................................................................

Progeny breeding values

(n = 50 fams)

ParentalGenotypes


A. Screen variable loci (n=32)

B. Confirm associations

HQQQQQQQQQQL........................................................................................................................

Progeny phenotypes

(n > 300)

ProgenyGenotypes


B. Progeny genotype-phenotype associations Females Males 1 2 So urce of variat ion df Va r Comp% F P df Var Comp% F P 3 4 5 CG33 692 (1) 6 Famil y 5 37. 3 13. 2 < 0.00 01 5 38. 6 18. 2 < 0.0001 7 Ge notype 7 5.6 2.7 0.01 1 7 6.8 3.5 0.0013 8 Erro r 168 200 9 10 Ecdysone -induced protein 75b (1) 11 Famil y 4 32. 9 14. 3 < 0.000 1 4 43. 3 19. 2 < 0.0001 12 Ge notype 2 5.4 4.6 0.01 2 2 1.2 1.8 0.18 13 Erro r 134 119 14 15 CG11 848 (2) 16 Famil y 5 36.9 14. 5 < 0.000 1 5 53. 6 31. 7 < 0.0001 17 Ge notype 4 2.0 1.7 0.1 6 4 1.1 1.6 0.17 18 Erro r 177 202 19 20 Corto (2) 21 Famil y 5 33. 7 10. 5 < 0.000 1 5 46. 1 18. 4 < 0.00 01 22 Ge notype 9 4.9 2.1 0.03 5 9 1.1 1.3 0.23 23 Erro r 175 200 24 25 CG10 107 (X) 26 Famil y 4 47. 7 16. 2 < 0.0 001 4 50. 6 22. 6 < 0.0001 27 Ge notype 5 -1.0 0.7 0.5 9 5 6.5 4.5 0.0049 28 Erro r 143 144 29 30

Genotype-phenotype associations

B. Progeny phenotypes by progeny genotypes

A. Progeny breeding values by parent genotypesCG33692 Dm X -> Cd A

CG10107 Dm A -> Cd X

Cq A -> Cd X

Multiple SR haplotypes occur in a populationM

icro

sate

llite

hap

loty

pe

(ms1

25, 2

44, 3

95 b

ps)

Screen of 89 Gombak males at 3 X-linked microsatellite loci

Wilkinson et al, 2006

If there is an arms race between a drive X and suppressors in

each population, then matings between populations should

reveal cryptic drive

Reproductive isolation increases with genetic distance

(reciprocal matings among 8 populations)

Each data point represents average values from 16 cages containing 1 male and 3 females

Christianson et al. (2005) Evolution

Matings/h Progeny/2 wks

Cross-population matings produce sterile male, fertile female progeny

(Haldane’s Rule)

Pro

porti

on h

ybrid

s fe

rtile

Gombak (Malaysia) x Soraya (Sumatra)

Christianson & Wilkinson 2005 Evol

between parental populations

Mapping cryptic drive

GBX(n = 438)

SBX(n = 261)

Determine brood sex ratios for all fertile BX progenyGenotype all progeny at 30 microsatellite loci

Intact X is required for fertility70167125106

395

crc

71

312

21

6

18

GBX SBX

# S alleles

Fertile Sterile

0 159 123

> 1 6 152

# G alleles

Fertile Sterile

0 121 108

> 1 0 21

70167125106

395

crc

71

312

21

6

18

Proportion male progeny

GSRX chromosome is lost presumably because it causes hybrid inviability.

Chr 1

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One region on chr 1 is associated with female-bias

SBX reveals female-biasing modifiers

GSRX chromosome is present, but unrelated to male-biased sex ratios

Proportion male progeny

Chr 1 Chr 2

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***

****

***

*****

Parts of chr 1 and 2 are associated with male-bias

GBX reveals male biasing modifiers

Evolutionary reasons for sex linkage

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