Genetic basis of male sexual behavior

Journal of Neurobiology

Volumn 54, Issue 1, 2003, Pages 93-110

  Emmons, Scott W ^a   Lipton, Jonathan ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

Behavior; C. elegans; Copulation; Drosophila; Sex determination

Indexed keywords

ARGIPRESSIN; ESTROGEN RECEPTOR; GENE PRODUCT; MEMBRANE PROTEIN; NEUROPEPTIDE; TRANSCRIPTION FACTOR; TYROSINE 3 MONOOXYGENASE;

APOPTOSIS; BEHAVIOR GENETICS; CAENORHABDITIS ELEGANS; CELL DEATH; CELL LINEAGE; COPULATION; COURTSHIP; DROSOPHILA MELANOGASTER; GENE EXPRESSION; GENE IDENTIFICATION; GENE MUTATION; GENE SEQUENCE; GENETIC ANALYSIS; GENETIC CODE; GENETIC VARIABILITY; KNOCKOUT GENE; MOTIVATION; NERVOUS SYSTEM; NONHUMAN; PRIORITY JOURNAL; REGULATOR GENE; REVIEW; SEX DETERMINATION; SEX DIFFERENCE; SEXUAL BEHAVIOR; SEXUAL ORIENTATION; VERTEBRATE;

ANIMALS; CAENORHABDITIS ELEGANS; CENTRAL NERVOUS SYSTEM; COPULATION; DROSOPHILA MELANOGASTER; GENE EXPRESSION REGULATION; GENETICS, BEHAVIORAL; MALE; MUTATION; PHEROMONES; SEX DETERMINATION (GENETICS); SEXUAL BEHAVIOR, ANIMAL;

EID: 0037220104     PISSN: 00223034     EISSN: None     Source Type: Journal    
DOI: 10.1002/neu.10163     Document Type: Review

References (107)

1. Arnold AP. 1997. Sexual differentiation of the zebra finch song system: Positive evidence, negative evidence, null hypotheses, and a paradigm shift. J Neurobiol 33:572-584.
2. Arthur BI, Jallon JM, Caflisch B, Choffat Y, Nothinger R. 1998. Sexual behaviour in Drosophila is irreversibly programmed during a critical period. Curr Biol 8:1187-1190.
3. Ayasse M, Paxton RJ, Tengö J. 2001. Mating behavior and chemical communication in the order Hymenoptera. Ann Rev Entomol 46:31-78.
4. Bagemihl B. 1999. Biological Exuberance. Animal Homosexuality and Natural Diversity. New York: St. Martin's Press. 751 p.
5. Baker BS, Taylor BJ, Hall JC. 2001. Are complex behaviors specified by dedicated regulatory genes? Reasoning from Drosophila. Cell 105:13-24.
6. Barr MM, DeModena J, Braun D, Nguyen CQ, Hall DH, Sternberg PW. 2001. The Caenorhabditis elegans autosomal dominant polycystic kidney disease gene homologs lov-1 and pkd-2 act in the same pathway. Curr Biol 11:1341-1346.
7. Barr MM, Sternberg PW. 1999. A polycystic kidney-disease gene homologue required for male mating behaviour in C. elegans. Nature 401:386-389.
8. Belote JM, Baker BS. 1987. Sexual behavior: Its genetic control during development and adulthood in Drosophila melanogaster. PNAS 84:8026-8030.
9. Brenowitz EA. 1997. Comparative approaches to the avian song system. J Neurobiol 33:517-531.
10. Cline TW, Meyer BJ. 1996. Vive la difference: Males vs females in flies vs worms. Annu Rev Genet 30:637-702.
11. Conradt B, Horvitz HR. 1999. The TRA-1A sex determination protein of C. elegans regulates sexually dimorphic cell deaths by repressing the egl-1 cell death activator gene. Cell 98:317-327.
12. Costa M, Weir M, Coulson A, Sulston J, Kenyon C. 1988. Posterior pattern formation in C. elegans involves position-specific expression of a gene containing a homeobox. Cell 55:747-756.
13. Coyne JA. 1996a. Genetics of differences in pheromonal hydrocarbons between Drosophila melanogaster and D. simulans. Genetics 143:353-364.
14. Coyne JA. 1996b. Genetics of a difference in male cuticular hydrocarbons between two sibling species, Drosophila simulans and D. sechellia. Genetics 143:1689-1698.
15. Coyne JA, Crittenden AP, Mah K. 1994. Genetics of a pheromonal difference contributing to reproductive isolation in Drosophila. Science 265:1461-1464.
16. Crawley JN, Belknap JK, Collins A, Crabbe JC, Frankel W, Henderson N, Hitzemann RJ, Maxson SC, Miner LL, Silva AJ, Wehner JM, Wynshaw-Boris A, Paylor R. 1997. Behavioral phenotypes of inbred mouse strains: Implications and recommendations for molecular studies. Psychopharmacology 132:107-124.
17. Dulac C, Axel R. 1995. A novel family of genes encoding putative pheromone receptors in mammals. Cell 83: 195-206.
18. Emmons SW, Somlo S. 1999. Mating, channels, and kidney cysts (News and Views). Nature 401:339-340.
19. Emmons SW, Sternberg PW. 1997. Male development and mating behavior. In: Riddle DL, Blumenthal T, Meyer BJ, Priess JR, editors. C. Elegans II. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press. p 295-334.
20. Ferveur J. 1997. The pheromonal role of cuticular hydrocarbons in Drosophila melanogaster. BioEssays 19:353-358.
21. Ferveur J-F. 1991. Genetic control of pheromones in Drosophila simulans. I. Ngbo, a locus on the second chromosome. Genetics 128:293-301.
22. Ferveur J-F, Cobb M, Boukella H, Jallon J-M. 1996. Worldwide variation in Drosophila melanogaster sex pheromone: Behavioral effects, genetic bases and evolutionary consequences. Genetica 97:73-80.
23. Ferveur JF, Jallon JM. 1996. Genetic control of male cuticular hydrocarbons in Drosophila melanogaster. Genet Res 67:211-218.
24. Finley KD, Edeen PT, Foss M, Gross E, Ghbeish N, Palmer RH, Taylor BJ, McKeown M. 1998. Dissatisfaction encodes a tailless-like nuclear receptor expressed in a subset of CNS neurons controlling Drosophila sexual behavior. Neuron 21:1363-1374.
25. Finley KD, Taylor BJ, Milstein M, McKeown M. 1997. Dissatisfaction, a gene involved in sex-specific behavior and neural development of Drosophila melanogaster. Proc Natl Acad Sci USA 94:913-918.
26. th Drosophila Res. Conf. Atlanta, p. 89.
27. Garcia LR, Mehta P, Sternberg PW. 2001. Regulation of distinct muscle behaviors controls the C. elegans male's copulatory spicules during mating. Cell 107:777-788.
28. Gems D, Riddle DL. 2000. Genetic, behavioral and environmental determinants of male longevity in Caenorhabditis elegans. Genetics 154:1597-1610.
29. Glover TJ, Campbell MG, Robbins PS, Roelofs WL. 1990. Sex-linked control of sex pheromone behavioral responses in European corn borer moths (Ostrinia Nubilalis) confirmed with TPI marker gene. Arch Insect Biochem Physiol 15:67-77.
30. Goodwin SF, Taylor BJ, Villella A, Foss M, Ryner LC, Baker BS, Hall JC. 2000. Aberrant splicing and altered spatial expression patterns in fruitless mutants of Drosophila melanogaster. Genetics 154:725-745.
31. th Edition. New York: McGraw-Hill. p 1131-1148.
32. Götz KG. 1994. Exploratory strategies in Drosophila. In: Schildberger K, Elsner N, editors. Neural Basis of Behavioural Adaptations Progress in Zoology 39:47-59. Stuttgart: G. Fischer.
33. Greenspan RJ. 1995a. Understanding the genetic construction of behavior. Sci Am 271:72-78.
34. Greenspan RJ. 1995b. Flies, genes, learning and memory. Neuron 15:747-750.
35. Greenspan RJ, Ferveur J. 2000. Courtship in Drosophila. Ann Rev Genet 34:205-232.
36. Hall JC. 1994. The mating of a fly. Science 264:1702-1714.
37. Hamer DH, Hu S, Magnuson VL, Hu N, Pattatucci AML. 1993. A linkage between DNA markers on the X chromosome and male sexual orientation. Science 261:321-327.
38. Hardie RC. 1986. The photoreceptor array of the dipteran retina. Trends Neurosci 9:419-423.
39. Herrada G, Dulac C. 1997. A novel family of putative pheromone receptors in mammals with a topographically organized and sexually dimorphic distribution. Cell 90:763-773.
40. Hodgkin J. 1983. Male phenotypes and mating efficiency in Caenorhabditis elegans. Genetics 103:43-64.
41. Hodgkin J. 1992. Genetic sex determination mechanisms and evolution. BioEssays 14:253-261.
42. Hodgkin J, Doniach T. 1997. Natural variation and copulatory plug formation in Caenorhabditis elegans. Genetics 146:149-164.
43. Hu S, Pattatucci AML, Patterson C, Li L, Fulker DW, Cherny SS, Kruglyak L, Hamer DH. 1995. Linkage between sexual orientation and chromosome Xq28 in males but not in females. Nat Genet 11:248-256.
44. Hull EM, Lorrain DS, Du J, Matuszewich L, Lumley LA, Putnam SK, Moses J. 1999. Hormone-neurotransmitter interactions in the control of sexual behavior. Behav Brain Res 105:105-116.
45. Hull EM, Meisel RL, Sachs BD. 2002. Male sexual behavior. In: Pfaff DW, Arnold AP, Fahrbach SE, Etgen AM, Rubin RT, editors. Hormones, Brain and Behavior. Academic Press. p 3-137.
46. Ito H, Fujitani K, Usui K, Shimizu-Nishikawa K, Tanaka S, Yamamoto D. 1996. Sexual orientation of Drosophila is altered by the satori mutation in the sex-determination gene fruitless that encodes a zinc finger protein with a BTB domain. PNAS 93:9687-9692.
47. 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 1:215-225.
48. Keisman TC, Baker BS. 2001. The Drosophila sex determination hierarchy modulates wingless and decapentaplegic signaling to deploy dachshund sex-specifically in the genital imaginal disc. Development 128:1643-1656.
49. Kelley DB. 1988. Sexually dimorphic behaviors. Ann Rev Neurosci 11:225-251.
50. Kopp A, Duncan I, Carroll SB. 2000. Genetic control and evolution of sexually dimorphic characters in Drosophila. Nature 408:553-559.
51. Kupfermann I, Kandel ER, Iversen S. 2000. Motivational and addictive states. In: Kandel ER, Schwartz JH, Jessell TM, editors. Principles of Neural Science. New York: McGraw-Hill. p 998-1013.
52. Leinders-Zufall T, Lan A, Puche A, Ma W, Novotny M, Shipley M, Zufall F. 2000. Ultrasensitive pheromone detection by mammalian vomeronasal neurons. Nature 405:792-796.
53. Lints R, Emmons SW. 2002. Regulation of sex-specific differentiation and mating behavior in C. elegans by a new member of the DM domain transcription factor family. Genes Dev 16:2390-2402.
54. Liu KS, Sternberg PW. 1995. Sensory regulation of male mating behavior in Caenorhabditis elegans. Neuron 14: 1-20.
55. Loer CM, Kenyon CJ. 1993. Serotonin-deficient mutants and male mating behavior in the nematode Caenorhabditis elegans. J Neurosci 13:5407-5417.
56. Marín I, Baker BS. 1998. The evolutionary dynamics of sex determination. Science 281:1990-1994.
57. Matsuda M, Nagahama Y, Shinomiya A, Sato T, Matsuda C, Kobayashi T, Morrey CE, Shibata N, Saskawa S, Shimizu N, Hori H, Hamaguchi S, Sakaizumi M. 2002. DMY is a Y-specific DM-domain gene required for male development in the medaka fish. Nature 417:559-563.
58. Matsunami H, Buck L. 1997. A multigene family encoding a diverse array of putative pheromone receptors in mammals. Cell 90:775-784.
59. Meisel RL, Sachs BD. 1994. The physiology of male sexual behavior. In: Knobil E, Neill JD, editors. The Physiology of Reproduction, Vol 2. New York: Raven.
60. Mendelson SD, Pfaus JG. 1989. Level searching: A new assay of sexual motivation in the male rat. Physiol Behav 45:337-341.
61. Montejo AL, Llorca G, Izquierdo JA, Rico-Villademoros F. 2001. Incidence of sexual dysfunction associated wth antidepressant agents: A prospective multicenter study of 1022 outpatients. J Clin Psychiatry 62:10-20.
62. Nealen PM, Perkel DJ. 2000. Sexual dimorphism in the song system of the Carolina Wren Thryothorus ludovicianus. J Comp Neurol 418:346-360.
63. Nef S, Parada LF. 2000. Hormones in male sexual development. Genes Dev 14:3075-3086.
64. Ogawa S, Chester AE, Hewitt SC, Walker VR, Gustafsson J-A, Smithies O, Korach KS, Pfaff DW. 2000. Abolition of male sexual behaviors in mice lacking estrogen receptors α and β (αβERKO). PNAS 97:14737-14741.
65. Orgad S, Rosenfeld G, Greenspan RJ, Segal D. 2000. Courtless, the Drosophila UBC7 homolog, is involved in male courtship behavior and spermatogenesis. Genetics 155: 1267-1280.
66. Ottolenghi C, Fellous M, Barbieri M, McElreavey K. 2002. Novel paralogy relations among human chromosomes support a link between the phylogeny of doublesex-related genes and the evolution of sex determination. Genomics 79:333-343.
67. Pantages E, Dulac C. 2000. A novel family of candidate pheromone receptors in mammals. Neuron 28:835-845.
68. Pfaus JG. 1999. Neurobiology of sexual behavior. Curr Opin Neurobiol 9:751-758.
69. Portman DS, Emmons SW. 2000. The basic helix-loop-helix transcription factors LIN-32 and HLH-2 function together in multiple steps of a C. elegans neuronal sublineage. Development 127:5415-5426.
70. Possidente DR, Murphey RK. 1989. Genetic control of sexually dimorphic axon morphology in Drosophila sensory neurons. Dev Biol 132:448-457.
71. Raymond CS, Murphy MW, O'Sullivan MG, Bardwell VG, Zarkower D. 2000. Dmrt1, a gene related to worm and fly sexual regulators, is required for mammalian testis differentiation. Genes Dev 14:2587-2595.
72. Raymond CS, Shamu CE, Shen MM, Seifert KJ, Hirsch B, Hodgkin J, Zarkower D. 1998. Evidence for evolutionary conservation of sex-determining genes. Nature 391:691-695.
73. Rice G, Anderson C, Risch N, Ebers G. 1999. Male homosexuality: Absence of linkage to microsatellite markers at Xq28. Science 284:665-667.
74. Roelofs WL. 1995. Chemistry of sex attraction. PNAS 92:44-49.
75. Roelofs WL, Glover TJ, Tang SH, Sreng I, Robbins P, Eckenrode CJ, Lofstedt C, Hansson BS, Bengtsson BO. 1987. Sex pheromone production and perception in European corn borer moths is determined by both autosomal and sex-linked genes. PNAS 84:7585-7589.
76. Ryba NJ, Tirindelli R. 1997. A new multigene family of putative pheromone receptors. Neuron 19:371-379.
77. Ryner LC, Goodwin SF, Castrillon DH, Anand A, Villella A, Baker BS, Hall JC, Taylor BJ, Wasserman SA. 1996. Control of male sexual behavior and sexual orientation in Drosophila by the fruitless gene. Cell 87:1079-1089.
78. 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 128:1033-1043.
79. Schlinger BA. 1998. Sexual differentiation of avian brain and behavior: Current views on gonadal hormone-dependent and independent mechanisms. Annu Rev Physiol 60:407-429.
80. Shen MM, Hodgkin J. 1988. mab-3, a gene required for sex-specific yolk protein expression and a male-specific lineage in C. elegans. Cell 54:1019-1031.
81. Simon JM, Sternberg PW. 2002. Evidence of a mate-finding cue in the hermaphrodite nematode Caenorhabditis elegans. PNAS 99:1598-1603.
82. Sokolowski MB. 2001. Drosophila: Genetics meets behaviour. Nat Rev Genet 2:879-890.
83. Sternberg PW, Horvitz HR. 1982. Postembryonic nongonadal cell lineages of the nematode Panagrellus redivivus: Description and comparison with those of Caenorhabditis elegans. Dev Biol 93:181-205.
84. Stowers L, Holy TE, Meister M, Dulac C, Koentges G. 2002. Loss of sex discrimination and male-male aggression in mice deficient for trp2. Science 295:1493-1500.
85. Sulston JE, Albertson DG, Thomson JN. 1980. The Caenorhabditis elegans male: Postembryonic development of nongonadal structures. Dev Biol 78:542-576.
86. Sulston JE, Horvitz HR. 1977. Post-embryonic cell lineages of the nematode Caenorhabditis elegans. Dev Biol 56: 111-156.
87. Sulston JE, Schierenberg E, White JG, Thomson JN. 1983. The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev Biol 100:64-119.
88. Swaab DF, Hofman MA. 1995. Sexual differentiation of the human hypothalamus in relation to gender and sexual orientation. TINS 18:264-270.
89. Taylor BJ. 1989a. Sexually dimorphic neurons in the terminalia of Drosophila melanogaster: I. Sex-specific axonal arborizations in the central nervous system. J Neurogenet 5:193-213.
90. Taylor BJ. 1989b. Sexually dimorphic neurons in the terminalia of Drosophila melanogaster: II. Development of sensory neurons in the genital disc during metamorphosis. J Neurogenet 5:173-192.
91. Taylor BJ, Villella A, Ryner LC, Baker BS, Hall JC. 1994. Behavioral and neurobiological implications of sex-determining factors in Drosophila. Dev Genet 15:275-296.
92. Technau GM. 1984. Fiber number in the mushroom bodies of adult Drosophila melanogaster depends on age, sex and experience. J Neurogenet 1:113-126.
93. Toivonen JM, O'Dell KM, Petit N, Irvine SC, Knight GK, Lehtonen M, Longmuir M, Luoto K, Touraille S, Wang Z, Alziari S, Shah ZH, Jacobs HT. 2001. Technical knockout, a Drosophila model of mitochondrial deafness. Genetics 159:241-254.
94. Troemel ER, Chou JH, Dwyer ND, Colbert HA, Bargmann CI. 1995. Divergent seven transmembrane receptors are candidate chemosensory receptors in C. elegans. Cell 83:207-218.
95. Usui-Aoki K, Ito H, Ui-Tei K, Takahashi K, Lukacsovich T, Awano W, Nakata H, Piao ZF, Nilsson EE, Tomida J, Yamamoto D. 2000. Formation of the male-specific muscle in female Drosophila by ectopic fruitless expression. Nat Cell Biol 2:500-506.
96. Uy JAC, Patricelli GL, Borgia G. 2000. Dynamic matesearching tactic allows female satin bowerbirds Ptilonorhynchus violaceus to reduce searching. Proc R Soc Lond B 267:251-256.
97. Villella A, Hall JC. 1996. Courtship anomalies caused by doublesex mutations in Drosophila melanogaster. Genetics 143:331-344.
98. Wheeler DA, Kyriacuo CP, Greenacre ML, Yu Q, Rutila JE, Rosbash M, Hall JC. 1991. Molecular transfer of a species-specific behavior from Drosophila simulans to Drosophila melanogaster. Science 251:1082-1085.
99. White JG, Southgate E, Thomson JN, Brenner S. 1986. The structure of the nervous system of Caenorhabditis elegans. Philos Trans R Soc Lond B Biol Sci 314:1-340.
100. Wilkins AS. 1995. Moving up the hierarchy: A hypothesis on the evolution of a genetic sex-determination pathway. BioEssays 17:71-77.
101. Woollard A, Hodgkin J. 2000. The Caenorhabditis elegans fate-determining gene mab-9 encodes a T-box protein required to pattern the posterior hindgut. Genes Dev 14:596-603.
102. Yamomoto D, Jallon JM, Komatsu A. 1997. Genetic dissection of sexual behavior in Drosophila melanogaster. Ann Rev Entomol 42:551-585.
103. Yi W, Ross JM, Zarkower D. 2000. mab-3 is a direct tra- I target gene regulating diverse aspects of C. elegans male sexual development and behavior. Development 127:4469-4480.
104. Yi W, Zarkower D. 1999. Similarity of DNA binding and transcriptional regulation by Caenorhabditis elegans MAB-3 and Drosophila melanogaster DSX suggests conservation of sex determining mechanisms. Development 126:873-881.
105. Young LJ, Nilsen R, Waymire KG, MacGregor GR, Insel TR. 1999. Increased affiliative response to vasopressin in mice expressing the Vla receptor from a monogamous vole. Nature 400:766-768.
106. Zarkower D. 2001. Establishing sexual dimorphism: Conservation amidst diversity? Nat Rev Genet 2:175-185.
107. Zhao C, Emmons SW. 1995. A transcription factor controlling development of peripheral sense organs in C. elegans. Nature 373:74-78.