Comparative Genomic Hybridization (CGH) Reveals a Neo-X Chromosome and Biased Gene Movement in Stalk-Eyed Flies (Genus )
Chromosomal location has a significant effect on the evolutionary dynamics of genes involved in sexual dimorphism, impacting both the pattern of sex-specific gene expression and the rate of duplication and protein evolution for these genes. For nearly all non-model organisms, however, knowledge of chromosomal gene content is minimal and difficult to obtain on a genomic scale. In this study, we utilized Comparative Genomic Hybridization (CGH), using probes designed from EST sequence, to identify genes located on the X chromosome of four species in the stalk-eyed fly genus Teleopsis. Analysis of log2 ratio values of female-to-male hybridization intensities from the CGH microarrays for over 3,400 genes reveals a strongly bimodal distribution that clearly differentiates autosomal from X-linked genes for all four species. Genotyping of 33 and linkage mapping of 28 of these genes in Teleopsis dalmanni indicate the CGH results correctly identified chromosomal location in all cases. Syntenic comparison with Drosophila indicates that 90% of the X-linked genes in Teleopsis are homologous to genes located on chromosome 2L in Drosophila melanogaster, suggesting the formation of a nearly complete neo-X chromosome from Muller element B in the dipteran lineage leading to Teleopsis. Analysis of gene movement both relative to Drosophila and within Teleopsis indicates that gene movement is significantly associated with 1) rates of protein evolution, 2) the pattern of gene duplication, and 3) the evolution of eyespan sexual dimorphism. Overall, this study reveals that diopsids are a critical group for understanding the evolution of sex chromosomes within Diptera. In addition, we demonstrate that CGH is a useful technique for identifying chromosomal sex-linkage and should be applicable to other organisms with EST or partial genomic information.
Vyšlo v časopise:
Comparative Genomic Hybridization (CGH) Reveals a Neo-X Chromosome and Biased Gene Movement in Stalk-Eyed Flies (Genus ). PLoS Genet 6(9): e32767. doi:10.1371/journal.pgen.1001121
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1001121
Souhrn
Chromosomal location has a significant effect on the evolutionary dynamics of genes involved in sexual dimorphism, impacting both the pattern of sex-specific gene expression and the rate of duplication and protein evolution for these genes. For nearly all non-model organisms, however, knowledge of chromosomal gene content is minimal and difficult to obtain on a genomic scale. In this study, we utilized Comparative Genomic Hybridization (CGH), using probes designed from EST sequence, to identify genes located on the X chromosome of four species in the stalk-eyed fly genus Teleopsis. Analysis of log2 ratio values of female-to-male hybridization intensities from the CGH microarrays for over 3,400 genes reveals a strongly bimodal distribution that clearly differentiates autosomal from X-linked genes for all four species. Genotyping of 33 and linkage mapping of 28 of these genes in Teleopsis dalmanni indicate the CGH results correctly identified chromosomal location in all cases. Syntenic comparison with Drosophila indicates that 90% of the X-linked genes in Teleopsis are homologous to genes located on chromosome 2L in Drosophila melanogaster, suggesting the formation of a nearly complete neo-X chromosome from Muller element B in the dipteran lineage leading to Teleopsis. Analysis of gene movement both relative to Drosophila and within Teleopsis indicates that gene movement is significantly associated with 1) rates of protein evolution, 2) the pattern of gene duplication, and 3) the evolution of eyespan sexual dimorphism. Overall, this study reveals that diopsids are a critical group for understanding the evolution of sex chromosomes within Diptera. In addition, we demonstrate that CGH is a useful technique for identifying chromosomal sex-linkage and should be applicable to other organisms with EST or partial genomic information.
Zdroje
1. FisherRA
1931 The evolution of dominance. Biol Rev 6 345 368
2. MullerHJ
1932 Some genetic aspects of sex. Am Nat 66 118 138
3. BullJJ
1983 Evolution of Sex Determining Mechanisms. Menlo Park Benjamin Cummings
4. VicosoB
CharlesworthB
2006 Evolution on the X chromosome: unusual patterns and processes. Nat Rev Genet 7 645 653
5. WhiteMJD
1973 Animal Cytology and Evolution. Cambridge Cambridge University Press
6. BhutkarA
RussoSM
SmithTF
GelbartWM
2007 Genome-scale analysis of positionally relocated genes. Genome Res 17 1880 1887
7. KohnM
Kehrer-SawatzkiH
VogelW
GravesJAM
HameisterH
2004 Wide genome comparisons reveal the origins of the human X chromosome. Trends Genet 20 598 603
8. McLysaghtA
2008 Evolutionary steps of sex chromosomes are reflected in retrogenes. Trends Genet 24 478 481
9. MeiselRP
HanMV
HahnMW
2009 A complex suite of forces drives gene traffic from Drosophila X chromosomes. Genome Biol Evol 1 176 188
10. PotrzebowskiL
VinckenboschN
MarquesAC
ChalmelF
JegouB
2008 Chromosomal gene movements reflect the recent origin and biology of therian sex chromosomes. PLoS Biol 6 709 716 doi:10.1371/journal.pbio.0060080
11. SchaefferSW
BhutkarAU
McAllisterBF
MatsudaM
MatzkinLM
2008 Polytene chromosomal maps of 11 Drosophila species: The order of genomic scaffolds inferred from genetic and physical maps. Genetics 179 1601 1655
12. WaterhouseRM
WyderS
ZdobnovEM
2008 The Aedes aegypti genome: a comparative perspective. Insect Mol Biol 17 1 8
13. CharlesworthB
1978 Model for evolution of Y-chromosomes and dosage compensation. Proc Natl Acad Sci USA 75 5618 5622
14. CharlesworthB
1991 The evolution of sex chromosomes. Science 251 1030 1033
15. RiceWR
1984 Sex chromosomes and the evolution of sexual dimorphism. Evolution 38 735 742
16. RiceWR
1987 Genetic hitchhiking and the evolution of reduced genetic activity of the Y sex chromosome. Genetics 116 161 167
17. RiceWR
1996 Evolution of the Y sex chromosome in animals. Bioscience 46 331 343
18. ZhangY
OliverB
2007 Dosage compensation goes global. Curr Opin Genet Dev 17 113 120
19. StraubT
BeckerPB
2007 Dosage compensation: the beginning and end of generalization. Nat Rev Genet 8 47 57
20. CharlesworthB
CoyneJA
BartonNH
1987 The relative rates of evolution of sex chromosomes and autosomes. Am Nat 130 113 146
21. JinW
RileyRM
WolfingerRD
WhiteKP
Passador-GurgelG
2001 The contributions of sex, genotype and age to transcriptional variance in Drosophila melanogaster. Nat Genet 29 389 395
22. RanzJM
Castillo-DavisCI
MeiklejohnCD
HartlDL
2003 Sex-dependent gene expression and evolution of the Drosophila transcriptome. Science 300 1742 1745
23. EllegrenH
ParschJ
2007 The evolution of sex-biased genes and sex-biased gene expression. Nat Rev Genet 8 689 698
24. ParisiM
NuttallR
NaimanD
BouffardG
MalleyJ
2003 Paucity of genes on the Drosophila X chromosome showing male-biased expression. Science 299 697 700
25. SturgillD
ZhangY
ParisiM
OliverB
2007 Demasculinization of X chromosomes in the Drosophila genus. Nature 450 238 U233
26. LifschytzE
LindsleyDL
1972 The role of X-chromosome inactivation during spermatogenesis. Proc Natl Acad Sci USA 69 182 186
27. HenseW
BainesJF
ParschJ
2007 X chromosome inactivation during Drosophila spermatogenesis. PLoS Biol 5 2288 2295 doi:10.1371/journal.pbio.0050273
28. WuCI
XuEY
2003 Sexual antagonism and X inactivation - the SAXI hypothesis. Trends Genet 19 243 247
29. TurnerJM
2007 Meiotic sex chromosome inactivation. Development 134 1823 1831
30. BetranE
ThorntonK
LongM
2002 Retroposed new genes out of the X in Drosophila. Genome Res 12 1854 1859
31. VibranovskiMD
ZhangY
LongMY
2009 General gene movement off the X chromosome in the Drosophila genus. Genome Res 19 897 903
32. KhilPP
SmirnovaNA
RomanienkoPJ
Camerini-OteroRD
2004 The mouse X chromosome is enriched for sex-biased genes not subject to selection by meiotic sex chromosome inactivation. Nat Genet 36 642 646
33. WilkinsonGS
DodsonG
1997 Function and evolution of antlers and eye stalks in flies.
ChoeJ
CrespiB
The Evolution of Mating Systems in Insects and Arachnids Cambridge Cambridge University Press 310 328
34. BakerRH
WilkinsonGS
2001 Phylogenetic analysis of eye stalk allometry and sexual dimorphism in stalk-eyed flies (Diopsidae). Evolution 55 1373 1385
35. PanhuisTM
WilkinsonGS
1999 Exaggerated male eye span influences contest outcome in stalk-eyed flies. Behav Ecol Sociobiol 46 221 227
36. HingleA
FowlerK
PomiankowskiA
2001 Size-dependent mate preference in the stalk-eyed fly Cyrtodiopsis dalmanni. Anim Behav 61 589 595
37. WilkinsonGS
KahlerH
BakerRH
1998 Evolution of female mating preferences in stalk-eyed flies. Behav Ecol 9 525 533
38. WilkinsonGS
ReilloPR
1994 Female preference response to artificial selection on an exaggerated male trait in a stalk-eyed fly. Proc R Soc Lond B 255 1 6
39. WolfenbargerLL
WilkinsonGS
2001 Sex-linked expression of a sexually selected trait in the stalk-eyed fly, Cyrtodiopsis dalmanni. Evolution 55 103 110
40. JohnsPM
WolfenbargerLL
WilkinsonGS
2005 Genetic linkage between a sexually selected trait and X chromosome meiotic drive. Proc R Soc Lond B 272 2097 2103
41. JohnsPM
WilkinsonGS
2007 X chromosome influences sperm length in the stalk-eyed fly Cyrtodiopsis dalmanni. Heredity 99 56 61
42. WilkinsonGS
AmitinEG
JohnsPM
2005 Sex-linked correlated responses in female reproductive traits to selection on male eye span in stalk-eyed flies. Int Comp Biol 45 500 510
43. MeierR
BakerR
2002 A cladistic analysis of Diopsidae (Diptera) based on morphological and DNA sequence data. Insect Syst Evol 33 325 336
44. PresgravesDC
SeverenceE
WilkinsonGS
1997 Sex chromosome meiotic drive in stalk-eyed flies. Genetics 147 1169 1180
45. WilkinsonGS
SwallowJG
ChristiansonSJ
MaddenK
2003 Phylogeography of sex ratio and multiple mating in stalk-eyed flies from southeast Asia. Genetica 117 37 46
46. WilkinsonGS
PresgravesDC
CrymesL
1998 Male eye span in stalk-eyed flies indicates genetic quality by meiotic drive suppression. Nature 391 276 278
47. BarrettMT
SchefferA
Ben-DorA
SampasN
LipsonD
2004 Comparative genomic hybridization using oligonucleotide microarrays and total genomic DNA. Proc Natl Acad Sci USA 101 17765 17770
48. StankiewiczP
BeaudetAL
2007 Use of array CGH in the evaluation of dysmorphology, malformations, developmental delay, and idiopathic mental retardation. Curr Opin Genet Dev 17 182 192
49. ZhangF
GuW
HurlesME
LupskiJR
2009 Copy number variation in human health, disease, and evolution. Annu Rev Genomics Hum Genet 10 451 481
50. BakerRH
MorganJ
WangX
BooreJL
WilkinsonGS
2009 Genomic analysis of a sexually-selected character: EST sequencing and microarray analysis of eye-antennal imaginal discs in the stalk-eyed fly Teleopsis dalmanni (Diopsidae). BMC Genomics 10 1 20
51. BainesJF
SawyerSA
HartlDL
ParschJ
2008 Effects of X-linkage and sex-biased gene expression on the rate of adaptive protein evolution in Drosophila. Mol Biol Evol 25 1639 1650
52. BachtrogD
JensenJD
ZhangZ
2009 Accelerated adaptive evolution on a newly formed X chromosome. PLoS Biol 7 e1000082 doi:10.1371/journal.pbio.1000082
53. BachtrogD
2008 The temporal dynamics of processes underlying Y chromosome degeneration. Genetics 179 1513 1525
54. BachtrogD
HomE
WongKM
MasideX
de JongP
2008 Genomic degradation of a young Y chromosome in Drosophila miranda. Genome Biol 9 R30
55. CarvalhoAB
ClarkAG
2005 Y chromosome of D. pseudoobscura is not homologous to the ancestral Drosophila Y. Science 307 108 110
56. CarvalhoAB
KoerichLB
ClarkAG
2009 Origin and evolution of Y chromosomes: Drosophila tales. Trends Genet 25 270 277
57. KoerichLB
WangXY
ClarkAG
CarvalhoAB
2008 Low conservation of gene content in the Drosophila Y chromosome. Nature 456 949 951
58. MikhaylovaLM
NguyenK
NurminskyDI
2008 Analysis of the Drosophila melanogaster testes transcriptome reveals coordinate regulation of paralogous genes. Genetics 179 305 315
59. SchuttC
NothigerR
2000 Structure, function and evolution of sex-determining systems in dipteran insects. Development 127 667 677
60. AlvarezM
RuizMF
SánchezL
2009 Effect of the gene doublesex of Anastrepha on the somatic sexual development of Drosophila. PLoS ONE 4 e5141 doi:10.1371/journal.pone.0005141
61. HedigerM
BurghardtG
SiegenthalerC
BuserN
Hilfiker-KleinerD
2004 Sex determination in Drosophila melanogaster and Musca domestica converges at the level of the terminal regulator doublesex. Dev Genes Evol 214 29 42
62. KuhnS
SievertV
TrautW
2002 The sex-determining gene doublesex in the fly Megaselia scalaris: conserved structure and sex-specific splicing. Genome 43 1011 1020
63. PaneA
De SimoneA
SacconeG
PolitoC
2005 Evolutionary conservation of Ceratitis capitata transformer gene function. Genetics 171 615 624
64. SacconeG
PaneA
PolitoLC
2002 Sex Determination in Flies, Fruitflies and Butterflies. Genetica 116 15 23
65. MarinI
BakerBS
1998 The evolutionary dynamics of sex determination. Science 281 1990 1994
66. ShearmanDCA
2002 The evolution of sex determination systems in dipteran insects other than Drosophila. Genetica 116 25 43
67. DaviesN
RoderickGK
2005 Dipteran sex chromsomes in evolutionary developmental biology.
YeatesDK
WeigmannBM
The Evolutionary Biology of Flies New York Columbia University Press 196 213
68. HedigerM
MinetAD
NiessenM
SchmidtR
Hilfiker-KleinerD
1998 The male-determining activity on the Y chromosome of the housefly (Musca domestica L.) consists of separable elements. Genetics 150 651 661
69. InoueH
FukimoriY
HiroyoshiT
1986 Mapping of autosomal male-determining factors of the housefly, Musca domestica L., by means of sex-reversal. Jpn J Genet 58 451 461
70. ZdobnovEM
von MeringC
LetunicI
TorrentsD
SuyamaM
2002 Comparative genome and proteome analysis of Anopheles gambiae and Drosophila melanogaster. Science 298 149 159
71. SeversonDW
deBruynB
LovinDD
BrownSE
KnudsonDL
2004 Comparative genome analysis of the yellow fever mosquito Aedes aegypti with Drosophila melanogaster and the malaria vector mosquito Anopheles gambiae. J Hered 95 103 113
72. YeatesDK
WiegmannBM
2005 Phylogeny and evolution of Diptera: Recent insights and new perspectives.
YeatesDK
WiegmannBM
The Evolutionary Biology of Flies New York Columbia University Press 14 44
73. WilkinsAS
1995 Moving up the hierarchy: A hypothesis on the evolution of a genetic sex determination pathway. Bioessays 17 71 77
74. SteinemannS
SteinemannM
2007 Evolution of sex chromosomes: dosage compensation of the Lcp1-4 gene cluster on the evolving neo-X chromosome in Drosophila miranda. Insect Mol Biol 16 167 174
75. BachtrogD
2004 Evidence that positive selection drives Y-chromosome degeneration in Drosophila miranda. Nat Genet 36 518 522
76. BachtrogD
2006 A dynamic view of sex chromosome evolution. Curr Opin Genet Dev 16 578 585
77. EvansAL
MenaPA
McAllisterBF
2007 Positive selection near an inversion breakpoint on the neo-X chromosome of Drosophila americana. Genetics 177 1303 1319
78. RichardsS
LiuY
BettencourtBR
HradeckyP
LetovskyS
2005 Comparative genome sequencing of Drosophila pseudoobscura: Chromosomal, gene, and cis-element evolution. Genome Res 15 1 18
79. GelbartME
KurodaMI
2009 Drosophila dosage compensation: a complex voyage to the X chromosome. Development 136 1399 1410
80. RuizMF
EstebanMR
DonoroC
GodayC
SanchezL
2000 Evolution of dosage compensation in Diptera: The gene maleless implements dosage compensation in Drosophila (Brachycera suborder) but Its homolog in Sciara (Nematocera suborder) appears to play no role in dosage compensation. Genetics 156 1853 1865
81. EmersonJJ
KaessmannH
BetranE
LongMY
2004 Extensive gene traffic on the mammalian X chromosome. Science 303 537 540
82. VinckenboschN
DupanloupI
KaessmannH
2006 Evolutionary fate of retroposed gene copies in the human genome. Proc Natl Acad Sci USA 103 3220 3225
83. HahnMW
LanzaroG
2005 Female-biased gene expression in the malaria mosquito Anopheles gambiae. Curr Biol 15 192 193
84. BegunDJ
HollowayAK
StevensK
HillierLW
PohY-P
2007 Population Genomics: Whole-Genome Analysis of Polymorphism and Divergence in Drosophila simulans. PLoS Biol 5 e310 doi:10.1371/journal.pbio.0050310
85. SinghND
LarracuenteAM
ClarkAG
2008 Contrasting the efficacy of selection on the X and autosomes in Drosophila. Mol Biol Evol 25 454 467
86. BetancourtAJ
PresgravesDC
SwansonWJ
2002 A test for faster X evolution in Drosophila. Mol Biol Evol 19 1816 1819
87. ConnallonT
2007 Adaptive protein evolution of X-linked and autosomal genes in Drosophila: Implications for faster-X hypotheses. Mol Biol Evol 24 2566 2572
88. ThorntonK
BachtrogD
AndolfattoP
2006 X chromosomes and autosomes evolve at similar rates in Drosophila: No evidence for faster-X protein evolution. Genome Res 16 498 504
89. GiladY
RifkinSA
BertoneP
GersteinM
WhiteKP
2005 Multi-species microarrays reveal the effect of sequence divergence on gene expression profiles. Genome Res 15 674 680
90. ChristiansonSJ
SwallowJG
WilkinsonGS
2005 Rapid evolution of postzygotic reproductive isolation in stalk-eyed flies. Evolution 59 849 857
91. BakerRH
WilkinsonGS
DeSalleR
2001 The phylogenetic utility of different types of molecular data used to infer evolutionary relationships among stalk-eyed flies (Diopsidae). Syst Biol 50 87 105
92. FoldvariM
PomiankowskiA
CottonS
CarrM
2007 A morphological and molecular description of a new Teleopsis species (Diptera: Diopsidae) from Thailand. Zootaxa 1620 37 51
93. ChristiansonSJ
2008 Reproductive isolation and X chromosome meiotic drive in Cyrtodiopsis stalk-eyed flies [Dissertation]. College Park University of Maryland 135
94. HartiganJA
WongMA
1979 A K-Means Clustering Algorithm. Appl Stat 28 100 108
95. SaeedA
SharovV
WhiteJ
LiJ
LiangW
2003 TM4: a free, open-source system for microarray data management and analysis. Biotechniques 34 374 378
96. Castillo-DavisCI
HartlDL
2003 GeneMerge—post-genomic analysis, data mining, and hypothesis testing. Bioinformatics 19 891 892
97. SAS Institute 2003 JMP. Cary, N.C. SAS Institute, Inc 5.0.1.2 ed.
98. WrightTF
JohnsPM
WaltersJR
LernerAP
SwallowJG
2004 Microsatellite variation among divergent populations of stalk-eyed flies, genus Cyrtodiopsis. Genet Res 84 27 40
99. BirgeL
PittsM
BakerR
WilkinsonG
2010 Length polymorphism and head shape association among genes with polyglutamine repeats in the stalk-eyed fly, Teleopsis dalmanni. BMC Evol Biol 10 227
100. Van OoijenJW
2006 JoinMap ® 4, Software for the calculation of genetic linkage maps in experimental populations. Wageningen, Netherlands Kyazma B.V
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