Function and evolution of sex determination mechanisms, genes and pathways in insects

BioEssays

Volumn 33, Issue 1, 2011, Pages 52-60

  Gempe, Tanja ^a   Beye, Martin ^a  

^a HEINRICH HEINE UNIVERSITY   (Germany)

Author keywords

Evolution; Evolutionary forces; Gene duplication; Sex determination; Sexual differentiation and selection

Indexed keywords

BIODIVERSITY; DROSOPHILA; FEMALE; GENE DUPLICATION; GENETIC VARIABILITY; INSECT; MALE; MOLECULAR EVOLUTION; NONHUMAN; REGULATORY MECHANISM; REVIEW; SEX DETERMINATION; SEXUAL DEVELOPMENT;

ANIMALS; BIOLOGICAL EVOLUTION; FEMALE; GENES; GENETIC VARIATION; INSECTS; MALE; MODELS, ANIMAL; MUTATION; SEX CHARACTERISTICS; SEX DETERMINATION PROCESSES; SEX DIFFERENTIATION; SPECIES SPECIFICITY;

ANIMALIA; HEXAPODA;

EID: 78650023664     PISSN: 02659247     EISSN: 15211878     Source Type: Journal    
DOI: 10.1002/bies.201000043     Document Type: Review

References (100)

1. Cline TW, Meyer BJ. 1996. Vive la difference: males vs. females in flies vs. worms. Annu Rev Genet 30: 637-702.
2. Zarkower D. 2006. Somatic sex determination. WormBook 1-12.
3. Lovell-Badge R, Canning C, Sekido R. 2002. Sex-determining genes in mice: building pathways. Novartis Found Symp 244: 4-18.
4. Sekido R, Lovell-Badge R. 2008. Sex determination involves synergistic action of SRY and SF1 on a specific Sox9 enhancer. Nature 453: 930-4.
5. Marshall Graves JA. 2008. Weird animal genomes and the evolution of vertebrate sex and sex chromosomes. Annu Rev Genet 42: 565-86.
6. Graves JA. 2006. Sex chromosome specialization and degeneration in mammals. Cell 124: 901-14.
7. Bull JJ. 1983. Evolution of Sex Determining Mechanisms. Menlo Park, California: Benjamin/Cummings Publishing Company.
8. Franco MG, Rubini PG, Vecchi M. 1982. Sex-determinants and their distribution in various populations of Musca domestica L. of Western Europe. Genet Res 40: 279-93.
9. Thompson PE, Bowen JS. 1972. Interactions of differentiated primary sex factors in Chironomus tentans. Genetics 70: 491-3.
10. Traut W. 1994. Sex determination in the fly Megaselia scalaris, a model system for primary steps of sex chromosome evolution. Genetics 136: 1097-1104.
11. Matsuda M. 2005. Sex determination in the teleost medaka, Oryzias latipes. Annu Rev Genet 39: 293-307.
12. Hasselmann M, Gempe T, Schiott M, Nunes-Silva CG, et al. 2008. Evidence for the evolutionary nascence of a novel sex determination pathway in honeybees. Nature 454: 519-22.
13. Pane A, Salvemini M, Bovi PD, Polito C, et al. 2002. The transformer gene in Ceratitis capitata provides a genetic basis for selecting and remembering the sexual fate. Development 129: 3715-25.
14. Gempe T, Hasselmann M, Schiott M, Hause G, et al. 2009. Sex determination in honeybees: two separate mechanisms induce and maintain the female pathway. PLoS Biol 7: e1000222.
15. Hediger M, Henggeler C, Meier N, Perez R, et al. 2010. Molecular characterization of the key switch F provides a basis for understanding the rapid divergence of the sex-determining pathway in the housefly. Genetics 184: 155-70.
16. Hediger M, Burghardt G, Siegenthaler C, Buser N, et al. 2004. Sex determination in Drosophila melanogaster and Musca domestica converges at the level of the terminal regulator doublesex. Dev Genes Evol 214: 29-42.
17. Salvemini M, Robertson M, Aronson B, Atkinson P, et al. 2009. Ceratitis capitata transformer-2 gene is required to establish and maintain the autoregulation of Cctra, the master gene of female sex determination. Int J Dev Biol 53: 109-20.
18. Alvarez M, Ruiz MF, Sanchez L. 2009. Effect of the gene doublesex of Anastrepha on the somatic sexual development of Drosophila. PLoS One 4: e5141.
19. Lagos D, Ruiz MF, Sanchez L, Komitopoulou K. 2005. Isolation and characterization of the Bactrocera oleae genes orthologous to the sex determining Sex-lethal and doublesex genes of Drosophila melanogaster. Gene 348: 111-21.
20. Concha C, Scott MJ. 2009. Sexual development in Lucilia cuprina (Diptera, Calliphoridae) is controlled by the transformer gene. Genetics 182: 785-98.
21. Lagos D, Koukidou M, Savakis C, Komitopoulou K. 2007. The transformer gene in Bactrocera oleae: the genetic switch that determines its sex fate. Insect Mol Biol 16: 221-30.
22. Verhulst EC, Beukeboom LW, van de Zande L. 2010. Maternal control of haplodiploid sex determination in the wasp Nasonia. Science 328: 620-3.
23. Dzierzon J. 1845. Gutachten über die von Herrn Direktor Stöhr im ersten und zweiten Kapitel des General-Gutachtens aufgestellten Fragen. Eichstädter Bienenzeitung 1: 109-113, 119-121.
24. McClung CE. 1902. The accessory chromosome - sex determinant? Biol Bull 3: 43-84.
25. Wilson EB. 1905. The chromosomes in relation to determination of sex in insects. Science 22: 500-2.
26. Sanchez L. 2008. Sex-determining mechanisms in insects. Int J Dev Biol 52: 837-56.
27. Schutt C, Nöthiger R. 2000. Structure, function and evolution of sex-determining systems in Dipteran insects. Development 127: 667-77.
28. Erickson JW, Quintero JJ. 2007. Indirect effects of ploidy suggest X chromosome dose, not the X:A ratio, signals sex in Drosophila. PLoS Biol 5: e332.
29. Dubendorfer A, Hediger M, Burghardt G, Bopp D. 2002. Musca domestica, a window on the evolution of sex-determining mechanisms in insects. Int J Dev Biol 46: 75-9.
30. Marin I, Baker BS. 1998. The evolutionary dynamics of sex determination. Science 281: 1990-4.
31. Kraemer C, Schmidt ER. 1993. The sex determining region of Chironomus thummi is associated with highly repetitive DNA and transposable elements. Chromosoma 102: 553-62.
32. Cook JM. 1993. Sex determination in the hymenoptera: a review of models and evidence. Heredity 71: 421-35.
33. Beye M. 2004. The dice of fate: the csd gene and how its allelic composition regulates sexual development in the honey bee, Apis mellifera. BioEssays 26: 1131-9.
34. Beye M, Hasselmann M, Fondrk MK, Page RE, et al. 2003. The gene csd is the primary signal for sexual development in the honeybee and encodes an SR-type protein. Cell 114: 419-29.
35. Inoue H, Fukumori Y, Hiroyoshi T. 1983. Mapping of autosomal male-determining factors of the housefly, Musca domestica L., by means of sex-reversal. Jpn J Genet 58: 451-61.
36. McDonald IC, Evenson P, Nickel CA, Johnson OA. 1978. Housefly genetics: isolation of a female determining factor on chromosome 4. Ann Entomol Soc Am 71: 692-4.
37. Willhoeft U, Franz G. 1996. Identification of the sex-determining region of the Ceratitis capitata Y chromosome by deletion mapping. Genetics 144: 737-45.
38. McKeown M, Belote JM, Baker BS. 1987. A molecular analysis of transformer, a gene in Drosophila melanogaster that controls female sexual differentiation. Cell 48: 489-99.
39. Butler B, Pirrotta V, Irminger-Finger I, Nöthiger R. 1986. The sex-determining gene tra of Drosophila: molecular cloning and transformation studies. EMBO J 5: 3607-13.
40. Savard J, Tautz D, Richards S, Weinstock GM, et al. 2006. Phylogenomic analysis reveals bees and wasps (Hymenoptera) at the base of the radiation of Holometabolous insects. Genome Res 16: 1334-8.
41. Marsh JL, Wieschaus E. 1978. Is sex determination in germ line and soma controlled by separate genetic mechanisms? Nature 272: 249-51.
42. Bell LR, Horabin JI, Schedl P, Cline TW. 1991. Positive autoregulation of Sex-lethal by alternative splicing maintains the female determined state in Drosophila. Cell 65: 229-39.
43. Shearman DC, Frommer M. 1998. The Bactrocera tryoni homologue of the Drosophila melanogaster sex-determination gene doublesex. Insect Mol Biol 7: 355-66.
44. Sievert V, Kuhn S, Traut W. 1997. Expression of the sex determining cascade genes Sex-lethal and doublesex in the phorid fly Megaselia scalaris. Genome 40: 211-4.
45. Kuhn S, Sievert V, Traut W. 2000. The sex-determining gene doublesex in the fly Megaselia scalaris: conserved structure and sex-specific splicing. Genome 43: 1011-20.
46. Ohbayashi F, Suzuki MG, Mita K, Okano K, et al. 2001. A homologue of the Drosophila doublesex gene is transcribed into sex-specific mRNA isoforms in the silkworm, Bombyx mori. Mol Genet Metab 128: 145-58.
47. Ruiz MF, Eirin-Lopez JM, Stefani RN, Perondini AL, et al. 2007. The gene doublesex of Anastrepha fruit flies (Diptera, Tephritidae) and its evolution in insects. Dev Genes Evol 217: 725-31.
48. Ruiz MF, Stefani RN, Mascarenhas RO, Perondini AL, et al. 2005. The gene doublesex of the fruit fly Anastrepha obliqua (Diptera, Tephritidae). Genetics 171: 849-54.
49. Cho S, Huang ZY, Zhang J. 2007. Sex-specific splicing of the honeybee doublesex gene reveals 300 million years of evolution at the bottom of the insect sex-determination pathway. Genetics 177: 1733-41.
50. Dearden PK, Wilson MJ, Sablan L, Osborne PW, et al. 2006. Patterns of conservation and change in honey bee developmental genes. Genome Res 16: 1376-84.
51. Cristino AS, Nascimento AM, Costa LF, Simoes ZL. 2006. A comparative analysis of highly conserved sex-determining genes between Apis mellifera and Drosophila melanogaster. Genet Mol Res 5: 154-68.
52. Williams TM, Carroll SB. 2009. Genetic and molecular insights into the development and evolution of sexual dimorphism. Nat Rev Genet 10: 797-804.
53. Burtis KC, Baker BS. 1989. Drosophila doublesex gene controls somatic sexual differentiation by producing alternatively spliced mRNAs encoding related sex-specific polypeptides. Cell 56: 997-1010.
54. Coschigano KT, Wensink PC. 1993. Sex-specific transcriptional regulation by the male and female doublesex proteins of Drosophila. Genes Dev 7: 42-54.
55. Suzuki MG, Funaguma S, Kanda T, Tamura T, et al. 2003. Analysis of the biological functions of a doublesex homologue in Bombyx mori. Dev Genes Evol 213: 345-54.
56. Vincent S, Perkins LA, Perrimon N. 2001. Doublesex surprises. Cell 106: 399-402.
57. Kopp A, Duncan I, Godt D, Carroll SB. 2000. Genetic control and evolution of sexually dimorphic characters in Drosophila. Nature 408: 553-9.
58. Keisman EL, Baker BS. 2001. The Drosophila sex determination hierarchy modulates wingless and decapentaplegic signalling to deploy dachshund sex-specifically in the genital imaginal disc. Development 128: 1643-56.
59. Christiansen AE, Keisman EL, Ahmad SM, Baker BS. 2002. Sex comes in from the cold: the integration of sex and pattern. Trends Genet 18: 510-6.
60. Keisman EL, Christiansen AE, Baker BS. 2001. The sex determination gene doublesex regulates the A/P organizer to direct sex-specific patterns of growth in the Drosophila genital imaginal disc. Dev Cell 1: 215-25.
61. Sanchez L, Guerrero I. 2001. The development of the Drosophila genital disc. BioEssays 23: 698-707.
62. Sanchez L, Gorfinkiel N, Guerrero I. 2001. Sex determination genes control the development of the Drosophila genital disc, modulating the response to Hedgehog, Wingless and Decapentaplegic signals. Development 128: 1033-43.
63. Williams TM, Selegue JE, Werner T, Gompel N, et al. 2008. The regulation and evolution of a genetic switch controlling sexually dimorphic traits in Drosophila. Cell 134: 610-23.
64. Ryner LC, Goodwin SF, Castrillon DH, Anand A, et al. 1996. Control of male sexual behavior and sexual orientation in Drosophila by the fruitless gene. Cell 87: 1079-89.
65. Demir E, Dickson BJ. 2005. Fruitless splicing specifies male courtship behavior in Drosophila. Cell 121: 785-94.
66. Rideout EJ, Dornan AJ, Neville MC, Eadie S, et al. 2010. Control of sexual differentiation and behavior by the doublesex gene in Drosophila melanogaster. Nat Neurosci 13: 458-66.
67. Gailey DA, Billeter JC, Liu JH, Bauzon F, et al. 2006. Functional conservation of the fruitless male sex-determination gene across 250 Myr of insect evolution. Mol Biol Evol 23: 633-43.
68. Bertossa RC, van de Zande L, Beukeboom LW. 2009. The fruitless gene in Nasonia displays complex sex-specific splicing and contains new zinc finger domains. Mol Biol Evol 26: 1557-69.
69. Traut W, Niimi T, Ikeo K, Sahara K. 2006. Phylogeny of the sex-determining gene Sex-lethal in insects. Genome 49: 254-62.
70. Hasselmann M, Vekemans X, Pflugfelder J, Koeniger N, et al. 2008. Evidence for convergent nucleotide evolution and high allelic turnover rates at the complementary sex determiner gene of Western and Asian honeybees. Mol Biol Evol 25: 696-708.
71. Hasselmann M, Beye M. 2004. Signatures of selection among sex-determining alleles of the honey bee. Proc Natl Acad Sci USA 101: 4888-93.
72. Heimpel GE, de Boer JG. 2008. Sex determination in the hymenoptera. Annu Rev Entomol 53: 209-30.
73. Hamilton WD. 1967. Extraordinary sex ratios. A sex-ratio theory for sex linkage and inbreeding has new implications in cytogenetics and entomology. Science 156: 477-88.
74. Trivers RL, Willard DE. 1973. Natural selection of parental ability to vary the sex ratio of offspring. Science 179: 90-2.
75. Rice WR. 1986. On the instability of polygenic sex determination: the effect of sex-specific selection. Evolution 40: 633-9.
76. Van Doorn GS, Kirkpatrick M. 2007. Turnover of sex chromosomes induced by sexual conflict. Nature 449: 909-12.
77. Sandler L, Novitski E. 1957. Meiotic drive as an evolutionary force. Am Nat 41: 105-10.
78. Temin RG. 1991. The independent distorting ability of the Enhancer of Segregation Distortion, E(SD), in Drosophila melanogaster. Genetics 128: 339-56.
79. Pomiankowski A, Nothiger R, Wilkins A. 2004. The evolution of the Drosophila sex-determination pathway. Genetics 166: 1761-73.
80. Singh RS, Artieri CG. 2010. Male sex drive and the maintenance of sex: evidence from Drosophila. J Hered 101 (Suppl 1): S100-6.
81. Singh RS, Kulathinal RJ. 2005. Male sex drive and the masculinization of the genome. BioEssays 27: 518-25.
82. Charlesworth B, Charlesworth D. 1978. A model for the evolution of dioecy and gynodioecy. Am Nat 112: 975-97.
83. Charlesworth D, Charlesworth B, Marais G. 2005. Steps in the evolution of heteromorphic sex chromosomes. Heredity 95: 118-28.
84. Charlesworth D, Charlesworth B. 2005. Sex chromosomes: evolution of the weird and wonderful. Curr Biol 15: R129-31.
85. Denholm I, Franco MG, Rubini PG, Vecchi M. 1983. Identification of a male determinant on the X chromosome of housefly (Musca domestica L.) populations in south east England. Genet Res 42: 311-22.
86. Hamm RL, Gao JR, Lin GG, Scott JG. 2009. Selective advantage for IIIM males over YM males in cage competition, mating competition, and pupal emergence in Musca domestica L. (Diptera: Muscidae). Environ Entomol 38: 499-504.
87. Lynch M. 2007. The evolution of genetic networks by non-adaptive processes. Nat Rev Genet 8: 803-13.
88. Hasselmann M, Beye M. 2006. Pronounced differences of recombination activity at the sex determination locus (SDL) of the honey bee, a locus under strong balancing selection. Genetics 174: 1469-80.
89. Gadau J, Gerloff CU, Kruger N, Chan H, et al. 2001. A linkage analysis of sex determination in Bombus terrestris (L.) (Hymenoptera: Apidae). Heredity 87: 234-42.
90. Excoffier L, Heckel G. 2006. Computer programs for population genetics data analysis: a survival guide. Nat Rev Genet 7: 745-58.
91. Kato Y, Kobayashi K, Oda S, Tatarazako N, et al. 2010. Sequence divergence and expression of a transformer gene in the branchiopod crustacean, Daphnia magna. Genomics 95: 160-5.
92. Kulathinal RJ, Skwarek L, Morton RA, Singh RS. 2003. Rapid evolution of the sex-determining gene, transformer: structural diversity and rate heterogeneity among sibling species of Drosophila. Mol Biol Evol 20: 441-52.
93. McAllister BF, McVean GA. 2000. Neutral evolution of the sex-determining gene transformer in Drosophila. Genetics 154: 1711-20.
94. Mita K, Kasahara M, Sasaki S, Nagayasu Y, et al. 2004. The genome sequence of silkworm, Bombyx mori. DNA Res 11: 27-35.
95. Xia Q, Zhou Z, Lu C, Cheng D, et al. 2004. A draft sequence for the genome of the domesticated silkworm (Bombyx mori). Science 306: 1937-40.
96. Suzuki MG, Funaguma S, Kanda T, Tamura T, et al. 2005. Role of the male BmDSX protein in the sexual differentiation of Bombyx mori. Evol Dev 7: 58-68.
97. Shirangi TR, Dufour HD, Williams TM, Carroll SB. 2009. Rapid evolution of sex pheromone-producing enzyme expression in Drosophila. PLoS Biol 7: e1000168.
98. Siera SG, Cline TW. 2008. Sexual backtalk with evolutionary implications: stimulation of the Drosophila sex-determination gene Sex-lethal by its target transformer. Genetics 180: 1963-81.
99. Yeates DK, Wiegmann BM, Courtney GW, Meier M, et al. 2007. Phylogeny and systematics of Diptera: two decades of progress and prospects. Zootaxa 1668: 565-90.
100. Hasselmann M, Lechner S, Schulte C, Beye M. 2010. Origin of a function by tandem gene duplication limits the evolutionary capability of its sister copy. Proc Natl Acad Sci USA 107: 13378-83.