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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

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Evolutionary reasons for sex linkage

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  1. 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)

  2. Male heterogamety Female heterogamety Male Female Female Male X-linked genes spend less time in males while Z-linked genes spend more time in males, compared to autosomal genes. XY XX ZW ZZ Why does mode of inheritance matter? 1. Sexual selection operates directly on males, indirectly on females.

  3. X-linked Autosomal Male Female Male Female XY XX XY XX Why does mode of inheritance matter? 2. Linkage disequilibrium between trait and preference depends on mode Linkage disequilibrium arises due to joint inheritance of ornament and preference genes

  4. Threshold preference better Preference change better Sexual selection and sex chromosomes(Kirkpatrick & Hall, 2004) * * Preference-display inheritance *

  5. 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)

  6. 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?

  7. Eyestalks have evolved in 8 families ofAcalyptrate flies 14 nuclear genes full mtDNA genomes Wiegmann et al. unpub.

  8. Richardiatelescopica Richardiidae (Peru) Achias rothschildi Platystomatidae (New Guinea) Diopsosoma prima Periscelididae (Brazil) Exaggerated eyestalks occur only in male flies Teleopsiswhitei Diopsidae (Malaysia)

  9. Males Teloglabrus entabenensis Females Dias. dubia Monomorphic Dias. silvatica Dias. obstans Dimorphic Dias. fasciata Equivocal 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 Eye-Stalk Sexual Dimorphism has evolved repeatedly in Diopsids Eyespan Body length Most parsimonious reconstruction of sexual dimorphism in eyespan.

  10. Sexual dimorphism evolves due to change in male eye span-body length allometry Independent contrasts Sexual dimorphism Male slope Female slope Baker & Wilkinson 2001 Evolution

  11. Teleopsis populations are genetically and reproductively isolated 100 Belalong 100 100 Cameron/Langat 100 Bogor T. dalmanni Soraya 100 93 Bt Lawang 100 99 Gombak 100 100 100 Brastagi NJ phylogram: 535 bp COII mtDNA 535 bp 16s mtDNA 655 bp wingless intron 86 Gombak T. whitei 100 Chiang Mai 90 2.5 - 11 MYA T. quinquegutatta Bt Ringit Swallow et al. 2005 Mol. Ecol. 0.005 substitutions/site

  12. Male eyespan is under sexual selection Males with longer eyespan roost and mate with more females (Wilkinson & Reillo 1994) Male with longer relative eyespan win contests (Panhuis et al. 1999) Male with longer relative eyespan are preferred by females (Wilkinson et al. 1998; Hingle et al. 2001) Eyespan is condition dependent, but relative eyespan has a genetic basis (Wilkinson & Taper 1999; David et al. 2000)

  13. Outline • Why use stalk-eyed flies as a model for studying sexually selection traits? • Which genomic 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. Realized response in eyespan Selection on male eye span alters brood sex ratios Wilkinson et al. 1998 Nature

  15. 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

  16. Gen 45 intercross XDYL-XXH 738 flies (2 families) 468 females 270 males Gen 30 intercross XYH-XXL 490 flies (1 family) 231 females 259 males QTL mapping of eye span

  17. Female-biased broods are due to X drive Number of males tested

  18. Chr X Chr XD Gen 30 F2 intercross XY-XX Drive X fails to recombine Chr 1 Chr 2 Gen 45 F2 intercross XDY-XX

  19. QTL for relative eye span Johns et al. 2005 Proc. R. Soc. Lond. B

  20. QTL for relative eye span Johns et al. 2005 Proc. R. Soc. Lond. B

  21. Eye span indicates drive X Thus, females that choose long eye span mates produce more sons XD

  22. 10 changes = SR frequency Only dimorphic Teleopsispopulations carry SR Sumatra Sumatra C. dalmanni Pen Malaysia Java Pen Malaysia C. whitei Thailand C. q. Pen Malaysia Wilkinson et al, 2003

  23. 70 3 167 1 125 2 106 21 395 6 crc 18 71 Drive X evolves rapidly Number of segregating sites in 3 Kb sequence 2 X-linked regions autosomal gene 25 29 Soraya N = 13 males 14 13 Gombak Non-drive N = 14 males 0 13 Gombak Drive N = 11 males

  24. 70 3 167 1 125 2 106 21 395 6 crc 18 71 Drive X evolves independently of autosomal genes 2 autosomal regions 2 X regions Note that drive X lacks variation and is derived from nondrive X chromosomes

  25. 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

  26. Outline • Why use stalk-eyed flies as a model for studying sexually selection? • What genomic 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?

  27. Larval brain + eye disc Eye-antennal imaginal disc 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 bpw/out Blast hit 186 • Average unique sequence per gene 1.65 Kb

  28. cell motility metamorphosis eye-antennal disc morphogenesis regulation of cell shape eye development growth axonogenesis Wnt/N/smo/fz/TGFb/InR signaling pathways actin cytoskeleton organization and biogenesis morphogenesis of an epithelium regulation of cell size cell growth regulation of body size 0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 % of D.m. genes in EST database EST representation in GO categories essential to eye-stalk development

  29. 0.9000 Cuticular protein 30B Cuticular protein 30F Cuticular protein 49Aa Cuticular protein 49Ac Cuticular protein 49Ae Cuticular protein 56F Cuticular protein 57A Cuticular protein 62Bb Cuticular protein 62Bc Cuticular protein 64Ac Cuticular protein 65Ec Cuticular protein 66Ca Cuticular protein 66Cb Cuticular protein 66D Cuticular protein 67Fa1 Cuticular protein 76Bd Cuticular protein 92F Cuticular protein 97Ea Cuticular protein 97Eb Cuticular protein 100A 0.8000 0.7000 Pre-pupal Pupal 1-3 0.6000 Pupal 4-6 0.5000 0.4000 0.3000 0.2000 0.1000 0.0000 meiosis All Genes transcription axonogenesis protein folding cell proliferation carbohydrate metabolism embryonic morphogenesis transmission of nerve impulse smoothened signaling pathway structural constituent of cuticle anatomical structure formation GO categories that exhibit over-representation with respect to developmental stage Developmental Time

  30. Outline • Why use stalk-eyed flies as a model for studying sexually selection? • What genomic 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?

  31. Identifying sex-linked genes by CGH • Designed custom 44K oligoarray • 60 bpoligo 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 Teleopsisspecies • Expect X-linked genes in females to have 2-fold intensity of males

  32. CGH chromosome inference:T. dalmanni Y Autosomal X Frequency -7.5 Median log2(F/M intensity)

  33. CGH chromosome inference:T. dalmanni Y Autosomal X PCR confirmation Chr Prediction Frequency Chr confirmation 35/35 correct = 100% -7.5 Median log2(F/M intensity)

  34. Teleopsishas a neo-X = Dm 2L Left neo-X Moved onto neo-X

  35. Muller elements in Drosophila Y replacement 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) Schaeffer et al. 2008 Genetics

  36. Drosophila-Anopheles synteny 53% of X-linked genes in A. gambiae are X-linked in D. melanogaster Drosophila-Anopheles shared a common ancestor ~ 260 MYA Zdobnov et al. 2002 Science

  37. T. dalmanni - D. melanogastersynteny Gene movement -> Td chromosome Muller element A+D C+E B

  38. CGH chromosome inference:T. quinqueguttata Y Autosomal X Frequency -5.0 Median log2(M/F intensity)

  39. Recent gene movement Autosome X X Median log2(CQ M/F intensity) Cd chr Autosome Cq chr 2 = 2392 P < 0.0001 Median log2(CD M/F intensity)

  40. Gene movement to X is associated with increased dimorphism in Teleopsis Genes may leave X chromosome to avoid X chromosome inactivation during meiosis

  41. 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. D. m. CG10561: D. p. D. v. C. d. A. g. scramb1: D. v. D. m. D. p. C. d. A. g. Distance measure: T.d. branch length / tree length

  42. Transposed genes show faster divergence Teleopsisbranch prop. Teleopsis chromosomal location

  43. Sequence divergence by CGH 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 “Recent” gene divergence (Cd(m+f) - Cq(m+f))/(Cd(m+f) + Cq(m+f)) R2 = 0.23, P < 0.0001 Dm-Cd divergence (1-BlastX)

  44. CGH divergence and ancestral X movement CD-CQ divergence is highest forDm genes which move on or off the X in Cd Note: excludes unique Cd genes (unknown location in Dm)

  45. CGH divergence by Dm chromosome arm * Divergence of eyespan genes is greatest forgenes which are unique to C dalmanni

  46. .67 Cd B.Law crolA .44 .17 1.18 Cd Gombak crolA 1.15 2.38 Cd Soraya crolA zinc finger protein - 10 domains 1.21 Cd B.Law crolB Cd Gom crol .40 1.57 Cd Gom crolA Cd Gombak crol .16 .56 .34 Cd B.Law crol .50 .31 Cd Soraya crol • Example: crooked legs, 3 copies confirmed by phylogenetic analysis of ~ 1700 bp of crol genes for 7 populations of C. dalmanni + C. whitei .46 Cd Brunei crol .55 .50 .27 Cd Bogor crol xxxxxxxxxxx 1.01 Cd Langat crol .38 Cw crol dN/dS .77 Cd Bras crol Gene Duplication in EST Database • Possible duplicates: 234 cases in which two or more clusters had the top Blast hit to overlapping regions of the same D.m. gene • Tentatively assigned clusters as paralogs if >10% amino acid divergence for aligned regions and all clusters are monophyletic relative to D. mel and D. pseudohomologs • Found 20 gene duplicates. Over-represented for genes involved in spermatogenesis and mRNA binding

  47. Sex-linkage and gene duplication • Gene duplications (21) preferentially involve neo-X • 11 homologs on neo-X (Dm 2L) and 10 on ancestral A • c2 = 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%) • c2 = 31.0, P < 0.0001 • Duplicate copies preferentially move off neo-X • 7 X -> A; 2 A -> X; 1 A -> Y

  48. One autosome -> X duplication/translocation: -> 2R -> 2 -> 3R -> X (Cd-Cq div: 0.48) -> auto (Cd-Cq div: 0.79) Sex-linkage and gene duplication evolution Six autosome duplications: Mean CGH divergence change = 0.15 ± 0.04

  49. Outline • Why use stalk-eyed flies as a model for studying sexually selection? • What genomic 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?

  50. Sex-bias by species gene expression & • Comparison • Male vs female T. dalmanniand 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

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