Gene-environment interplay in Drosophila melanogaster: Chronic food deprivation in early life affects adult exploratory and fitness traits

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue SUPPL.2, 2012, Pages 17239-17244

  Burns, James Geoffrey ^a   Svetec, Nicolas ^a   Rowe, Locke ^a   Mery, Frederic ^b,c   Dolan, Michael J ^a   Boyce, W Thomas ^d   Sokolowski, Marla B ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b CNRS   (France)

^c UNIVERSITÉ PARIS SACLAY   (France)

^d UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Genotype environment interaction; Plasticity

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; EARLY LIFE STRESS; EXPLORATORY BEHAVIOR; FEMALE; FOOD DEPRIVATION; FORAGING BEHAVIOR; GENE EXPRESSION; GENETIC VARIABILITY; GENOTYPE ENVIRONMENT INTERACTION; NONHUMAN; NUTRITIONAL STATUS; PHENOTYPE; PRIORITY JOURNAL; REPRODUCTIVE FITNESS; ANIMAL; ANIMAL BEHAVIOR; FERTILITY; GENE; GENETICS; GROWTH, DEVELOPMENT AND AGING; MALE; PHYSIOLOGY;

BASIDIOMYCOTA; DROSOPHILA MELANOGASTER; EMMELICHTHYIDAE;

ANIMALS; BEHAVIOR, ANIMAL; DROSOPHILA MELANOGASTER; EXPLORATORY BEHAVIOR; FEMALE; FERTILITY; FOOD DEPRIVATION; GENE-ENVIRONMENT INTERACTION; GENES, INSECT; GENETIC FITNESS; MALE;

EID: 84872255872     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1121265109     Document Type: Article

References (73)

1. Gordon E, Cooper N, Rennie C, Hermens D, Williams LM (2005) Integrative neuroscience: The role of a standardized database. Clin EEG Neurosci 36:64-75. (Pubitemid 41175288)
2. Committee on a Framework for Developing a New Taxonomy of Disease; National Research Council (2011) Toward Precision Medicine: Building a Knowledge Network for Biomedical Research and a New Taxonomy of Disease (National Academy Press, Washington, DC).
3. Gluckman PD, Hanson MA (2004) The developmental origins of the metabolic syndrome. Trends Endocrinol Metab 15:183-187. (Pubitemid 38510499)
4. Hales CN, Barker DJP (2001) The thrifty phenotype hypothesis. Br Med Bull 60:5-20. (Pubitemid 34123501)
5. Ogden CL, Lamb MM, Carroll MD, Flegal KM (2010) Obesity and Socioeconomic Status in Children and Adolescents: United States, 2005-2008 (US Department of Health and Human Services Centers for Disease Control and Prevention, National Center for Health Statistics, Hyattsville, MD).
6. Wauben IPM, Wainwright PE (1999) The influence of neonatal nutrition on behavioral development: A critical appraisal. Nutr Rev 57:35-44. (Pubitemid 29116761)
7. Scrimshaw NS (1998) Malnutrition, brain development, learning, and behavior. Nutr Res 18:351-379.
8. Kaun KR, Chakaborty-Chatterjee M, Sokolowski MB (2008) Natural variation in plasticity of glucose homeostasis and food intake. J Exp Biol 211:3160-3166.
9. Stöger R (2008) The thrifty epigenotype: An acquired and heritable predisposition for obesity and diabetes? Bioessays 30:156-166.
10. Walley AJ, Asher JE, Froguel P (2009) The genetic contribution to non-syndromic human obesity. Nat Rev Genet 10:431-442.
11. Turelli M, Barton NH (2004) Polygenic variation maintained by balancing selection: Pleiotropy, sex-dependent allelic effects and G x E interactions. Genetics 166:1053-1079. (Pubitemid 38391761)
12. Via S, Lande R (1985) Genotype-environment interaction and the evolution of phenotypic plasticity. Evolution 39:505-522. (Pubitemid 17245190)
13. Gillespie JH, Turelli M (1989) Genotype-environment interactions and the maintenance of polygenic variation. Genetics 121:129-138. (Pubitemid 19026326)
14. Hedrick PW (1986) Genetic polymorphism in heterogeneous environments: A decade later. Annu Rev Ecol Syst 17:535-566.
15. Gluckman PD, Hanson MA, Spencer HG (2005) Predictive adaptive responses and human evolution. Trends Ecol Evol 20:527-533. (Pubitemid 41323708)
16. Meaney MJ, Szyf M, Seckl JR (2007) Epigenetic mechanisms of perinatal programming of hypothalamic-pituitary-adrenal function and health. Trends Mol Med 13:269-277. (Pubitemid 47017003)
17. Dewitt TJ, Sih A, Wilson DS (1998) Costs and limits of phenotypic plasticity. Trends Ecol Evol 13:77-81. (Pubitemid 28081011)
18. Kent CF, Daskalchuk T, Cook L, Sokolowski MB, Greenspan RJ (2009) The Drosophila foraging gene mediates adult plasticity and gene-environment interactions in behaviour, metabolites, and gene expression in response to food deprivation. PLoS Genet 5:e1000609.
19. Kaun KR, et al. (2007) Natural variation in food acquisition mediated via a Drosophila cGMP-dependent protein kinase. J Exp Biol 210:3547-3558. (Pubitemid 350144352)
20. Sokolowski MB (2010) Social interactions in "simple" model systems. Neuron 65:780-794.
21. Donlea J, et al. (2012) Foraging alters resilience/vulnerability to sleep disruption and starvation in Drosophila. Proc Natl Acad Sci USA 109:2613-2618.
22. Mery F, Belay AT, So AKC, Sokolowski MB, Kawecki TJ (2007) Natural polymorphism affecting learning and memory in Drosophila. Proc Natl Acad Sci USA 104:13051-13055. (Pubitemid 351737591)
23. Paul C, et al. (2008) Signaling through cGMP-dependent protein kinase I in the amygdala is critical for auditory-cued fear memory and long-term potentiation. J Neurosci 28:14202-14212.
24. Hartell NA (1994) cGMP acts within cerebellar Purkinje cells to produce long term depression via mechanisms involving PKC and PKG. Neuroreport 5:833-836.
25. Pereira HS, Sokolowski MB (1993) Mutations in the larval foraging gene affect adult locomotory behavior after feeding in Drosophila melanogaster. Proc Natl Acad Sci USA 90:5044-5046. (Pubitemid 23182972)
26. Sokolowski MB (1980) Foraging strategies of Drosophila melanogaster: A chromosomal analysis. Behav Genet 10:291-302.
27. Osborne KA, et al. (1997) Natural behavior polymorphism due to a cGMP-dependent protein kinase of Drosophila. Science 277:834-836. (Pubitemid 27366738)
28. Sokolowski MB, Pereira HS, Hughes K (1997) Evolution of foraging behavior in Drosophila by density-dependent selection. Proc Natl Acad Sci USA 94:7373-7377. (Pubitemid 27345322)
29. Fitzpatrick MJ, Feder E, Rowe L, Sokolowski MB (2007) Maintaining a behaviour polymorphism by frequency-dependent selection on a single gene. Nature 447:210-212. (Pubitemid 46763079)
30. Crusio WE (2001) Genetic dissection of mouse exploratory behaviour. Behav Brain Res 125:127-132.
31. Fraser DF, Gilliam JF, Daley MJ, Le AN, Skalski GT (2001) Explaining leptokurtic movement distributions: Intrapopulation variation in boldness and exploration. Am Nat 158:124-135. (Pubitemid 32682539)
32. Dingemanse NJ, Both C, van Noordwijk AJ, Rutten AL, Drent PJ (2003) Natal dispersal and personalities in great tits (Parus major). Proc Biol Sci 270:741-747. (Pubitemid 36433927)
33. Both C, Dingemanse NJ, Drent PJ, Tinbergen JM (2005) Pairs of extreme avian personalities have highest reproductive success. J Anim Ecol 74:667-674. (Pubitemid 41576934)
34. Wilson RC, Vacek T, Lanier DL, Dewsbury DA (1976) Open-field behavior in muroid rodents. Behav Biol 17:495-506.
35. Carducci JP, Jakob EM (2000) Rearing environment affects behaviour of jumping spiders. Anim Behav 59:39-46. (Pubitemid 30106792)
36. Martin JR (2004) A portrait of locomotor behaviour in Drosophila determined by a video-tracking paradigm. Behav Processes 67:207-219.
37. Lebreton S, Martin JR (2009) Mutations affecting the cAMP transduction pathway disrupt the centrophobism behavior. J Neurogenet 23:225-234.
38. Liu LZ, Davis RL, Roman G (2007) Exploratory activity in Drosophila requires the kurtz nonvisual arrestin. Genetics 175:1197-1212. (Pubitemid 46798224)
39. Götz KG, Biesinger R (1985) Centrophobism in Drosophila melanogaster 1. Behavioral modification induced by ether. J Comp Physiol A 156:319-327.
40. Reaume CJ, Sokolowski MB (2006) The nature of Drosophila melanogaster. Curr Biol 16:R623-R628. (Pubitemid 44233286)
41. Stamps J, Buechner M, Alexander K, Davis J, Zuniga N (2005) Genotypic differences in space use and movement patterns in Drosophila melanogaster. Anim Behav 70:609-618. (Pubitemid 43293141)
42. Carere C, Drent PJ, Koolhaas JM, Groothuis TGG (2005) Epigenetic effects on personality traits: Early food provisioning and sibling competition. Behaviour 142:1329-1355. (Pubitemid 44430963)
43. Werner EE, Anholt BR (1993) Ecological consequences of the trade-off between growth and mortality rates mediated by foraging activity. Am Nat 142:242-272. (Pubitemid 24408296)
44. Csanyi V, Gerlai R (1988) Open-field behavior and the behavior-genetic analysis of the paradise fish (Macropodus opercularis). J Comp Psychol 102:326-336.
45. Walsh RN, Cummins RA (1976) The Open-Field Test: A critical review. Psychol Bull 83:482-504.
46. Templeton CN, Shriner WM (2004) Multiple selection pressures influence Trinidadian guppy (Poecilia reticulata) antipredator behavior. Behav Ecol 15:673-678. (Pubitemid 38871367)
47. Godin JGJ (1997) Evading predators. Behavioural Ecology of Teleost Fishes, ed Godin JGJ (Oxford Univ Press, Oxford), pp 191-236.
48. Rilling S, Mittelstaedt H, Roeder KD (1959) Prey recognition in the praying mantis. Behaviour 14:164-184.
49. Treit D, Fundytus M (1988) Thigmotaxis as a test for anxiolytic activity in rats. Pharmacol Biochem Behav 31:959-962. (Pubitemid 19274312)
50. Belay AT, et al. (2007) The foraging gene of Drosophila melanogaster: Spatial-expression analysis and sucrose responsiveness. J Comp Neurol 504:570-582. (Pubitemid 47572979)
51. Busto GU, Cervantes-Sandoval I, Davis RL (2010) Olfactory learning in Drosophila. Physiology (Bethesda) 25:338-346.
52. Heisenberg M (2003) Mushroom body memoir: from maps to models. Nat Rev Neurosci 4:266-275.
53. Besson M, Martin JR (2005) Centrophobism/thigmotaxis, a new role for the mushroom bodies in Drosophila. J Neurobiol 62:386-396.
54. Martin JR, Ernst R, Heisenberg M (1998) Mushroom bodies suppress locomotor activity in Drosophila melanogaster. Learn Mem 5:179-191. (Pubitemid 29108280)
55. Aso Y, et al. (2009) The mushroom body of adult Drosophila characterized by GAL4 drivers. J Neurogenet 23:156-172.
56. Brand AH, Perrimon N (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118:401-415. (Pubitemid 23214028)
57. Gorgens T, Meng X, Vaithianathan R (2012) Stunting and selection effects of famine: A case study of the Great Chinese Famine. J Dev Econ 97:99-111.
58. Painter RC, et al. (2008) Transgenerational effects of prenatal exposure to the Dutch famine on neonatal adiposity and health in later life. BJOG 115:1243-1249.
59. Ellis BJ, Boyce WT (2008) Biological sensitivity to context. Curr Dir Psychol Sci 17:183-187.
60. Belsky J, Pluess M (2009) Beyond diathesis stress: Differential susceptibility to environmental influences. Psychol Bull 135:885-908.
61. Boyce WT, Ellis BJ (2005) Biological sensitivity to context: I. An evolutionary-developmental theory of the origins and functions of stress reactivity. Dev Psychopathol 17:271-301. (Pubitemid 41388314)
62. Caspi A, et al. (2002) Role of genotype in the cycle of violence in maltreated children. Science 297:851-854. (Pubitemid 34839638)
63. Obradović J, Bush NR, Stamperdahl J, Adler NE, Boyce WT (2010) Biological sensitivity to context: The interactive effects of stress reactivity and family adversity on socioemotional behavior and school readiness. Child Dev 81:270-289.
64. Evans GW, Kim P (2007) Childhood poverty and health: Cumulative risk exposure and stress dysregulation. Psychol Sci 18:953-957.
65. Lupien SJ, King S, Meaney MJ, McEwen BS (2000) Child's stress hormone levels correlate with mother's socioeconomic status and depressive state. Biol Psychiatry 48:976-980.
66. Rutter M, Moffitt TE, Caspi A (2006) Gene-environment interplay and psychopathology: Multiple varieties but real effects. J Child Psychol Psychiatry 47:226-261. (Pubitemid 43356058)
67. Dukas R, Mooers AO (2003) Environmental enrichment improves mating success in fruit flies. Anim Behav 66:741-749. (Pubitemid 37284123)
68. Heisenberg M, Heusipp M, Wanke C (1995) Structural plasticity in the Drosophila brain. J Neurosci 15:1951-1960.
69. Dawson-Scully K, et al. (2010) Controlling anoxic tolerance in adult Drosophila via the cGMP-PKG pathway. J Exp Biol 213:2410-2416.
70. Dawson-Scully K, Armstrong GAB, Kent C, Robertson RM, Sokolowski MB (2007) Natural variation in the thermotolerance of neural function and behavior due to a cGMP-dependent protein kinase. PLoS ONE 2:e773.
71. Chen A, et al. (2011) The influence of natural variation at the foraging gene on thermotolerance in adult Drosophila in a narrow temperature range. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 197:1113-1118.
72. Kahsai L, Martin JR, Winther AME (2010) Neuropeptides in the Drosophila central complex in modulation of locomotor behavior. J Exp Biol 213:2256-2265.
73. Kafkafi N, et al. (2003) Darting behavior: A quantitative movement pattern designed for discrimination and replicability in mouse locomotor behavior. Behav Brain Res 142:193-205. (Pubitemid 36681559)