Quantitative genetic analyses of complex behaviours in Drosophila

Nature Reviews Genetics

Volumn 5, Issue 11, 2004, Pages 838-849

  Anholt, Robert R H ^a   Mackay, Trudy F C ^a  

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALCOHOL; COCAINE; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP PHOSPHODIESTERASE; VOLTAGE GATED POTASSIUM CHANNEL;

AGGRESSION; ALCOHOL TOLERANCE; BEHAVIOR; CIRCADIAN RHYTHM; DROSOPHILA MELANOGASTER; FEMALE FERTILITY; GENE EXPRESSION REGULATION; GENE LINKAGE DISEQUILIBRIUM; GENE MAPPING; GENETIC ANALYSIS; GENETIC RECOMBINATION; GENETIC TRANSCRIPTION; GENETIC VARIABILITY; GENOME; GENOMICS; GENOTYPE; LEARNING; LIFESPAN; LOCOMOTION; MEMORY; NONHUMAN; PHENOTYPE; PLEIOTROPY; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; QUANTITATIVE GENETICS; QUANTITATIVE TRAIT LOCUS; REVIEW; SEX DIFFERENCE; SMELLING; TRANSGENE;

ANIMALS; DROSOPHILA MELANOGASTER; GENE EXPRESSION PROFILING; GENETICS, BEHAVIORAL; GENOTYPE; PHENOTYPE; SEX CHARACTERISTICS; TRANSCRIPTION, GENETIC;

DROSOPHILA MELANOGASTER; MELANOGASTER;

EID: 7644232462     PISSN: 14710056     EISSN: None     Source Type: Journal    
DOI: 10.1038/nrg1472     Document Type: Review

References (84)

1. Mackay, T. F. C. Quantitative trait loci in Drosophila. Nature Rev. Genet. 2, 11-20 (2001).
2. Mackay, T. F. C. The generic architecture of quantitative traits. Annu. Rev. Genet. 35, 303-339 (2001).
3. Adams, M. D. et al. The genome sequence of Drosophila melanogaster. Science 287, 2185-2195 (2000).
4. Dudai, Y., Jan, Y. N., Byers, D., Quinn, W. G. & Benzer, S. dunce, a mutant of Drosophila deficient in learning. Proc. Natl Acad. Sci. USA 73, 1684-1688 (1976).
5. Quinn, W. G., Harris, W. A. & Benzer, S. Conditioned behavior in Drosophila melanogaster. Proc. Natl Acad. Sci. USA 71, 708-712 (1974).
6. Konopka, R. J. & Benzer, S. Clock mutants of Drosophila melanogaster. Proc. Natl Acad. Sci. USA 68, 2112-2116 (1971).
7. Greenspan, R. J. & Ferveur, J.-F. Courtship in Drosophila. Annu. Rev. Genet. 34, 205-232 (2000).
8. Moehring, A. J. & Mackay, T. F. C. The quantitative genetic basis of male mating behavior in Drosophila melanogaster. Genetics 167, 1249-1263 (2004).
9. Osborne, K. A. et al. Natural behavior polymorphism due to a cGMP-dependent protein kinase of Drosophila. Science 277, 834-836 (1997). A classic paper, reporting the behavioural effects of naturally occurring polymorphisms in the foraging gene, which encodes a cGMP-dependent protein kinase. The authors show that subtle alterations in enzyme activity profoundly alter larval foraging behaviour in D. melanogaster.
10. Anhoit, R. R. H., Lyman, R. F. & Mackay, T. F. C. Effects of single P-element insertions on olfactory behavior in Drosophila melanogaster. Genetics 143, 293-301 (1996).
11. Chen, S., Lee, A. Y., Bowens, N. M., Huber, R. & Kravitz, E. A. Fighting fruit flies: a model system for the study of aggression. Proc. Natl Acad. Sci. USA 99, 5664-5668 (2002).
12. Benzer, S. Behavioral mutants of Drosophila isolated by countercurrent distribution. Proc. Natl Acad. Sci. USA 58, 1112-1119 (1967).
13. Hirsch, J. & Edenmeyer-Kimling, L. Sign of taxis as a property of the genotype. Science 143, 835-835 (1961). Reports one of the earliest experiments in fly behavioural genetics. The authors demonstrate that artificial selection can be used to generate flies that prefer to migrate either upwards or downwards in a geotactic maze. The selection lines reported in this paper were used 40 years later in the transcriptional profiling studies described in reference 62.
14. Quinn, W. G., Sziber, P. P. & Booker, R. The Drosophila memory mutant amnesiac. Nature 277, 212-214 (1979).
15. Weber, K. E. An apparatus for measurement of resistance to gas-phase reagents. Drosoph. Inf. Serv. 67, 91-93 (1988).
16. Moore, M. S. et al. Ethanol intoxication in Drosophila: genetic and pharmacological evidence for regulation by the cAMP signaling pathway. Cell 93, 997-1007 (1998).
17. Rothenfluh, A. & Hebedein, U. Drugs, flies, and videotape: the effects of ethanol and cocaine on Drosophila locomotion. Curr. Opin. Neurobiol. 12, 639-645 (2002).
18. Hall, J. C. The mating of a fly. Science 264, 1702-1714 (1994).
19. Dubnau, J. & Tully, T. Gene discovery in Drosophila: new insights for learning and memory. Annu. Rev. Neurosci. 21, 407-444 (1998).
20. Waddell, S. & Quinn, W. G. Flies, genes and learning. Annu. Rev. Neurosci. 24, 1283-1309 (2001).
21. McKenna, M., Monte, P., Helfand, S. L., Woodard, C. & Carlson, J. A simple chemosensory response in Drosophila and the isolation of acj mutants in which it is affected. Proc. Natl Acad. Sci. USA 86, 8118-8122 (1989).
22. Anholt, R. R. H. et al. The genetic architecture of odor-guided behavior in Drosophila: epistasis and the transcriptome. Nature Genet. 35, 180-184 (2003). Quantifies the extent of transcriptional co-regulation among a set of co-isogenic mutant lines with single P-element insertions that affect olfactory avoidance behaviour and illustrates how transcriptional profiling together with quantitative complementation tests for epistasis can be used for gene discovery.
23. Brand, A. H. & Perrimon, N. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118, 401-415 (1993).
24. Falconer, D. S. & Mackay, T. F. C. Introduction to Quantitative Genetics (Longman, Essex, 1996).
25. McGuire, S. E., Le, P. T. & Davis, R. L. The role of Drosophila mushroom body signaling in olfactory memory. Science 293, 1330-1333 (2001).
26. Allada, R., Emery, P., Takahashi, J. S. & Rosbash, M. Stopping time: the genetics of fly and mouse circadian clocks. Annu. Rev. Neurosci. 24, 1091-1119 (2001).
27. Ben-Shlomo, R. & Kyriacou, C. P. Circadian rhythm entrainment in flies and mammals. Cell. Biochem. Biophys. 37, 141-156 (2002).
28. Ashmore, L. J. & Sehgal, A. A fly's eye view of circadian entrainment. J. Biol. Rhythms 18, 206-216 (2003).
29. Cirelli, C. Searching for sleep mutants of Drosophila melanogaster. Bioessays 25, 940-949 (2003).
30. McDonald, M. J. & Rosbash, M. Microarray analysis and organization of circadian gene expression in Drosophila. Cell 107, 567-578 (2001). This paper, together with reference 31, presents the first expression microarray analyses of a behavioural trait in D. melanogaster. Although the observed transcriptional profiles differ between these papers, they both demonstrate that circadian time affects not only expression of genes that are directly implicated in the biological clock, but has far reaching implications for the transcription of many genes, including those implicated in several behaviours.
31. Claridge-Chang, A. et al. Circadian regulation of gene expression systems in the Drosophila head. Neuron 32, 657-671 (2001).
32. Norga, K. K. et al. Quantitative analysis of bristle number in Drosophila mutants identifies genes involved in neural development. Curr. Biol. 13, 1388-1396 (2003).
33. Crabbe, J. C., Wahlsten, D. & Dudek, B. C. Genetics of mouse behavior: interactions with laboratory environment. Science 284, 1670-1672 (1999).
34. Mackay, T. F. C., Hackett, J. B., Lyman, R. F., Wayne, M. L. & Anholt, R. R. H. Quantitative genetic variation of odor-guided behavior in a natural population of Drosophila melanogaster. Genetics 144, 727-735 (1996).
35. Devaud, J. M. Experimental studies of adult Drosophila chemosensory behaviour. Behav. Processes 64, 177-196 (2003).
36. Belgacem, Y. H. & Martin, J. R. Neuroendocrine control of a sexually dimorphic behavior by a few neurons of the pars intercerebralis in Drosophila, Proc. Natl Acad. Sci. USA 99, 15154-15158 (2002).
37. Helfrich-Forster C. Differential control of morning and evening components in the activity rhythm of Drosophila melanogaster - sex-specific differences suggest a different quality of activity. J. Biol. Rhythms 15, 135-154 (2000).
38. Jin, W. et al. The contributions of sex, genotype and age to transcriptional variance in Drosophila melanogaster. Nature Genet. 29, 389-395 (2001).
39. Ranz, J. M., Castillo-Davis, C. I., Meklejohn, C. D. & Hartl, D. L. Sex-dependent gene expression and evolution of the Drosophila transcriptome. Science 300, 1742-1745 (2003).
40. Parisi, M. et al. Paucity of genes on the Drosophila X chromosome showing male-biased expression. Science 299, 697-700 (2003).
41. Fujii, S. & Amren, H. Genes expressed in the Drosophila head reveal a role for fat cells in sex-specific physiology. EMBO J. 21, 5353-5363 (2002).
42. Rice, W. R. Sexually antagonistic genes: experimental evidence. Science 256, 1436-1439 (1992).
43. Levene. H. Genetic equilibrium when more than one ecological niche is available. Am. Nat. 87, 331-333 (1953).
44. Greenspan, R. J. A kinder, gentler genetic analysis of behavior: dissection gives way to modulation. Curr. Opin. Neurobiol. 7, 805-811 (1997).
45. Ganguly, L. Mackay, T. F. C. & Anholt, R. R. H. Scribble is essential for olfactory behavior in Drosophila. Genetics 164, 1447-1457 (2003).
46. Kulkarni, N. H., Yamamoto, A. H., Robinson, K. O., Mackay, T. F. C. & Anholt, R. R. H. The DSC1 channel, encoded by the smi60E locus, contributes to odor-guided behavior in Drosophila melanogaster. Genetics 161, 1507-1516 (2002).
47. Thibault, S. T. et al. A complementary transposon tool kit for Drosophila melanogaster using P and piggyBac. Nature Genet. 36, 283-287 (2004).
48. Fanara, J. J., Robinson, K. O., Rollmann, S. M., Anholt, R. R. H. & Mackay, T. F. C. Vanaso is a candidate quantitative trait gene for olfactory behavior in Drosophila melanogaster. Genetics 162, 1321-1328 (2002).
49. Gleason, J. M., Nuzhdin, S. V. & Ritchie, M. G. Quantitative trait loci affecting a courtship signal in Drosophila melanogaster. Heredity 89, 1-6 (2002).
50. Zeng, Z. B. Precision mapping of quantitative trait loci. Genetics 136, 1457-1468 (1994).
51. Doerge, R. W. & Churchill, G. A. Permutation tests for multiple loci affecting a quantitative character. Genetics 142, 285-294 (1996).
52. Hill, W. G. Predictions of response to artificial selection from new mutations. Genet. Res. 40, 255-278 (1982).
53. Mackay, T. F., Fry, J. D., Lyman, R. F. & Nuzhdin, S. V. Polygenic mutation in Drosophila melanogaster: estimates from response to selection of inbred strains. Genetics 136, 937-951 (1994).
54. Rodriguez-Ramilo, S. T., Perez-Figueroa, A., Fernandez, B., Fernandez, J. & Caballero, A. Mutation-selection balance accounting for genetic variation for viability in Drosophila melanogaster as deduced from an inbreeding and artificial selection experiment. J. Evol. Biol. 17, 528-541 (2004).
55. Berger, J. et al. Genetic mapping with SNP markers in Drosophila. Nature Genet. 29, 475-481 (2001).
56. Pasyukova, E. G., Vieira, C. & Mackay, T. F. C. Deficiency mapping of quantitative trait loci affecting longevity in Drosophila melanogaster. Genetics 156, 1129-1146 (2000). Introduces the method of quantitative complementation mapping using deficiencies, and demonstrates how this method can be used to narrow QTL regions to a small number of candidate genes that affect variation in lifespan in D. melanogaster.
57. Parks, A. L., et al. Systematic generation of high-resolution deletion coverage of the Drosophila melanogaster genome. Nature Genet. 36, 288-292 (2004).
58. DeLuca, M. et al. Do decarboxylase (Ddc) affects variation in Drosophila longevity. Nature Genet. 34, 429-433 (2003). Demonstrates how LD mapping can be used as a powerful method to identify not only a candidate gene, but also polymorphisms (QTNs) and haplotypes within such genes that contribute to natural variation in a complex trait, in this case lifespan.
59. Long, A. D., Lyman, R. F., Langley, C. H. & Mackay, T. F. C. Two sites in the Delta gene region contribute to naturally occurring variation in bristle number in Drosophila melanogaster. Genetics 149, 999-1017 (1998).
60. Lyman, R. F. & Mackay, T. F. C. Candidate quantitative trait loci and naturally occurring phenotypic variation for bristle number in Drosophila melanogaster: the Delta-Hairless gene region. Genetics 149, 953-998 (1998).
61. Robin, C., Lyman, R. F., Long, A. D., Langley, C. H. & Mackay, T. F. C. hairy: a quantitative trait locus for Drosophila sensory bristle number. Genetics 162, 155-164 (2002).
62. Toma, D. P., White, K. P., Hirsch, J. & Greenspan, R. J. Identification of genes involved in Drosophila melanogaster geotaxis, a complex behavioral trait. Nature Genet. 31, 349-353 (2002).
63. Kerr, M. K. & Churchill, G. A. Experimental design for gene expression microarrays. Biostatistics 2, 183-201 (2001). Contains excellent advice on the design and analysis of expression microarrays.
64. Storey, J. D. & Tibshirani, R. Statistical significance for genome-wide studies. Proc. Natl Acad. Sci. USA 100, 9440-9445 (2003). Introduces assessment of the false discovery rate to estimate false positives in transcriptional profiling experiments. The statistical method described will probably become the standard procedure for microarray analysis.
65. Borrás, T. et al. Transcription profiling in Drosophila eyes that overexpress the human glaucoma-associated trabecular meshwork-inducible glucocorticoid response protein/myocilin (TIGR/MYOC). Genetics 163, 637-645 (2003).
66. Fedorowicz, G. M., Fry, J. D., Anholt, R. R. H. & Mackay, T. F. C. Epistatic interactions between smell-impaired loci in Drosophila melanogaster. Genetics 148, 1885-1891 (1998). Describes the first application of the half-diallel cross design for the analysis of epistasis among behavioural genes, and reports an unexpectedly large extent of epistasis among 12 independently isolated co-isagenic P-element insertion lines that affect olfactory avoidance behaviour. This paper formed the basis for the subsequent transcriptional profiling study described in reference 22.
67. Sprague, G. F. & Tatum, L. A. General vs. specific combining ability in single crosses of corn. J. Amer. Soc. Agron. 34, 923-932 (1942).
68. Griffing, B. Concept of general and specific combining ability in relation to diallel crossing systems. Aust. J. Biol. Sci. 9, 463-493 (1956).
69. Cockerham, C. C. An extension of the concept of partitioning hereditary variance for analysis of covariances among relatives when epistasis is present. Genetics 39, 859-882 (1954).
70. Clark, A. G. & Wang, L. Epistasis in measured genotypes: Drosophila P-element insertions. Genetics 147, 157-163 (1997).
71. Ebed, D. F., Duyk, G. M. & Perrimon, N. A genetic screen for mutations that disrupt an auditory response in Drosophila melanogaster. Proc. Natl Acad. Sci. USA 94, 14837-14842 (1997).
72. Ejima, A., Nakayama, S. & Aigaki, T. Phenotypic association of spontaneous ovulation and sexual receptivity in virgin females of Drosophila melanogaster mutants. Behav. Genet. 31, 437-444 (2001).
73. Baker, B. S., Taylor, B. J. & Hall, J. C. Are complex behaviors specified by dedicated regulatory genes? Reasoning from Drosophila. Cell 105, 13-24 (2001).
74. Williams, J. A. & Sehgal, A. Molecular components of the circadian system in Drosophila. Annu. Rev. Physiol. 63, 729-755 (2001).
75. Park, S. K., Sedore, S. A., Cronmiller, C. & Hirsh, J. Type II cAMP-dependent protein kinase-deficient Drosophila are viable but show developmental, circadian, and drug response phenotypes. J. Biol. Chem. 275, 20588-20596 (2000).
76. Kauvar, L. M. Defective cyclic adenosine 3′:5′-monophosphate phosphodiesterase in the Drosophila memory mutant dunce. J. Neurosci. 2, 1347-1358 (1982).
77. Levine, J. D., Casey, C. I., Kalderon, D. D. & Jackson, F. R. Altered circadian pacemaker functions and cyclic AMP rhythms in the Drosophila learning mutant dunce. Neuron 13, 967-974 (1994).
78. Martin, F., Charro, M. J. & Alcorta, E. Mutations affecting the cAMP transduction pathway modify olfaction in Drosophila. J. Comp. Physiol. A 187, 359-370 (2001).
79. Tinette, S., Zhang, L. & Robichon, A. Cooperation between Drosophila flies in searching behavior. Genes Brain Behav. 3, 39-50 (2004).
80. Ueyama, M. & Fuyama, Y. Enhanced cost of mating in female sterile mutants of Drosophila melanogaster. Genes Genet. Syst. 78, 29-36 (2003).
81. Dauwalder, B. & Davis, R. L. Conditional rescue of the dunce learning/memory and female fertility defects with Drosophila or rat transgenes. J. Neurosci. 15, 3490-3499 (1995).
82. Sokal, R. R. & Rohlf, F. J. Biometry 2nd edn (W. H. Freeman and Company, New York, 1981).
83. Lai, C., Lyman, R. F., Long, A. D., Langley, C. H. & Mackay, T. F. C. Naturally occurring variation in bristle number and DNA polymorphisms at the scabrous locus of Drosophila melanogaster. Science 266, 1697-1702 (1994).
84. Sokolowski, M. B. Drosophila: genetics meets behaviour. Nature Rev. Genet. 2, 879-890 (2001).