1932

Abstract

The () gene is a well-established example of a gene with major effects on behavior and natural variation. This gene is best known for underlying the behavioral strategies of rover and sitter foraging larvae, having been mapped and named for this phenotype. Nevertheless, in the last three decades an extensive array of studies describing ’s role as a modifier of behavior in a wide range of phenotypes, in both and other organisms, has emerged. Furthermore, recent work reveals new insights into the genetic and molecular underpinnings of how affects these phenotypes. In this article, we discuss the history of the gene and its role in natural variation in behavior, plasticity, and behavioral pleiotropy, with special attention to recent findings on the molecular structure and transcriptional regulation of this gene.

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2019-12-03
2024-06-22
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Literature Cited

  1. 1. 
    Allen AM, Anreiter I, Neville MC, Sokolowski MB 2017. Feeding-related traits are affected by dosage of the foraging gene in Drosophila melanogaster. Genetics 205:761–73
    [Google Scholar]
  2. 2. 
    Allen AM, Anreiter I, Vesterberg A, Douglas SJ, Sokolowski MB 2018. Pleiotropy of the Drosophila melanogaster foraging gene on larval feeding-related traits. J. Neurogenet. 32:256–66
    [Google Scholar]
  3. 3. 
    Anand A, Villella A, Ryner LC, Carlo T, Goodwin SF et al. 2001. Molecular genetic dissection of the sex-specific and vital functions of the Drosophila melanogaster sex determination gene fruitless. Genetics 158:1569–95
    [Google Scholar]
  4. 4. 
    Anreiter I, Biergans SD, Sokolowski MB 2019. Epigenetic regulation of behavior in Drosophila melanogaster. Curr. Opin. Behav. Sci 25:44–50
    [Google Scholar]
  5. 5. 
    Anreiter I, Kramer JM, Sokolowski MB 2017. Epigenetic mechanisms modulate differences in Drosophila foraging behavior. PNAS 114:12518–23
    [Google Scholar]
  6. 6. 
    Anreiter I, Sokolowski HM, Sokolowski MB 2017. Gene–environment interplay and individual differences in behavior. Mind Brain Educ 12:200–11
    [Google Scholar]
  7. 7. 
    Anreiter I, Sokolowski MB. 2018. Deciphering pleiotropy: how complex genes regulate behavior. Commun. Integr. Biol. 11:1–4
    [Google Scholar]
  8. 8. 
    Anreiter I, Vasquez OE, Allen AM, Sokolowski MB 2016. Foraging path-length protocol for Drosophila melanogaster larvae. J. Vis. Exp. 110:e53980
    [Google Scholar]
  9. 9. 
    Armstrong GAB, López-Guerrero JJ, Dawson-Scully K, Peña F, Robertson RM 2010. Inhibition of protein kinase G activity protects neonatal mouse respiratory network from hyperthermic and hypoxic stress. Brain Res 1311:64–72
    [Google Scholar]
  10. 10. 
    Armstrong GAB, Rodgers CI, Money TGA, Robertson RM 2009. Suppression of spreading depression-like events in locusts by inhibition of the NO/cGMP/PKG pathway. J. Neurosci. 29:8225–35
    [Google Scholar]
  11. 11. 
    Arya GH, Magwire MM, Huang W, Serrano-Negron YL, Mackay TFC, Anholt RRH 2015. The genetic basis for variation in olfactory behavior in Drosophila melanogaster. Chem. Senses 40:233–43
    [Google Scholar]
  12. 12. 
    Ashley-Koch AE, Garrett ME, Gibson J, Liu Y, Dennis MF et al. 2015. Genome-wide association study of posttraumatic stress disorder in a cohort of Iraq-Afghanistan era veterans. J. Affect. Disord. 184:225–34
    [Google Scholar]
  13. 13. 
    Baker BS, Taylor BJ, Hall JC 2001. Are complex behaviors specified by dedicated regulatory genes? Reasoning from Drosophila. Cell 105:13–24
    [Google Scholar]
  14. 14. 
    Ben-Shahar Y, Leung H-T, Pak WL, Sokolowski MB, Robinson GE 2003. cGMP-dependent changes in phototaxis: a possible role for the foraging gene in honey bee division of labor. J. Exp. Biol. 206:Part 142507–15
    [Google Scholar]
  15. 15. 
    Ben-Shahar Y, Robichon A, Sokolowski MB, Robinson GE 2002. Influence of gene action across different time scales on behavior. Science 296:741–44
    [Google Scholar]
  16. 16. 
    Brown JB, Boley N, Eisman R, May GE, Stoiber MH et al. 2014. Diversity and dynamics of the Drosophila transcriptome. Nature 512:393–99
    [Google Scholar]
  17. 17. 
    Burns JG, Svetec N, Rowe L, Mery F, Dolan MJ et al. 2012. Gene-environment interplay in Drosophila melanogaster: Chronic food deprivation in early life affects adult exploratory and fitness traits. PNAS 109:17239–44
    [Google Scholar]
  18. 18. 
    Camiletti AL, Awde DN, Thompson GJ 2014. How flies respond to honey bee pheromone: the role of the foraging gene on reproductive response to queen mandibular pheromone. Naturwissenschaften 101:25–31
    [Google Scholar]
  19. 19. 
    Caplan SL, Milton SL, Dawson-Scully K 2013. A cGMP-dependent protein kinase (PKG) controls synaptic transmission tolerance to acute oxidative stress at the Drosophila larval neuromuscular junction. J. Neurophysiol. 109:649–58
    [Google Scholar]
  20. 20. 
    Dason JS, Allen AM, Vasquez OE, Sokolowski MB 2019. Distinct functions of a cGMP-dependent protein kinase in nerve terminal growth and synaptic vesicle cycling. J. Cell Sci. 132:jcs227165
    [Google Scholar]
  21. 21. 
    Dason JS, Cheung A, Anreiter I, Montemurri VA, Allen AM, Sokolowski MB 2019. Drosophila melanogaster foraging regulates a nociceptive-like escape behavior through a developmentally plastic sensory circuit. PNAS In press https://doi.org/10.1073/pnas.1820840116
    [Crossref] [Google Scholar]
  22. 22. 
    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
    [Google Scholar]
  23. 23. 
    Dawson-Scully K, Bukvic D, Chakaborty-Chatterjee M, Ferreira R, Milton SL, Sokolowski MB 2010. Controlling anoxic tolerance in adult Drosophila via the cGMP-PKG pathway. J. Exp. Biol. 213:2410–16
    [Google Scholar]
  24. 24. 
    de Belle JS, Hillikert AJ, Sokolowski MB 1989. Genetic localization of foraging (for): a major gene for larval behavior in Drosophila melanogaster. Genetics 123:157–63
    [Google Scholar]
  25. 25. 
    de Belle JS, Sokolowski MB 1987. Heredity of rover/sitter: alternative foraging strategies of Drosophila melanogaster larvae. Heredity 59:73–83
    [Google Scholar]
  26. 26. 
    Demyanenko GP, Halberstadt AI, Pryzwansky KB, Werner C, Hofmann F, Maness PF 2005. Abnormal neocortical development in mice lacking cGMP-dependent protein kinase I. Dev. Brain Res. 160:1–8
    [Google Scholar]
  27. 27. 
    Donlea J, Leahy A, Thimgan MS, Suzuki Y, Hughson BN et al. 2012. foraging alters resilience/vulnerability to sleep disruption and starvation in Drosophila. PNAS 109:2613–18
    [Google Scholar]
  28. 28. 
    Duraffourd C, Huckstepp RTR, Braren I, Fernandes C, Brock O et al. 2019. PKG1α oxidation negatively regulates food seeking behaviour and reward. Redox Biol 21:101077
    [Google Scholar]
  29. 29. 
    Eddison M, Belay AT, Sokolowski MB, Heberlein U 2012. A genetic screen for olfactory habituation mutations in Drosophila: analysis of novel foraging alleles and an underlying neural circuit. PLOS ONE 7:e51684
    [Google Scholar]
  30. 30. 
    Edelsparre AH, Shahid A, Fitzpatrick MJ 2018. Habitat connectivity is determined by the scale of habitat loss and dispersal strategy. Ecol. Evol. 8:5508–14
    [Google Scholar]
  31. 31. 
    Edelsparre AH, Vesterberg A, Lim JH, Anwari M, Fitzpatrick MJ 2014. Alleles underlying larval foraging behaviour influence adult dispersal in nature. Ecol. Lett. 17:333–39
    [Google Scholar]
  32. 32. 
    Engel JE, Xie XJ, Sokolowski MB, Wu CF 2000. A cGMP-dependent protein kinase gene, foraging, modifies habituation-like response decrement of the giant fiber escape circuit in Drosophila. Learn. Mem 7:341–52
    [Google Scholar]
  33. 33. 
    Falconer DS, Mackay TF. 1996. Introduction to Quantitative Genetics Harlow, UK: Addison Wesley Longman. , 4th ed..
    [Google Scholar]
  34. 34. 
    Feil R, Hartmann J, Luo C, Wolfsgruber W, Schilling K et al. 2003. Impairment of LTD and cerebellar learning by Purkinje cell–specific ablation of cGMP-dependent protein kinase I. J. Cell Biol. 163:295–302
    [Google Scholar]
  35. 35. 
    Feil R, Hölter SM, Weindl K, Wurst W, Langmesser S et al. 2009. cGMP-dependent protein kinase I, the circadian clock, sleep and learning. Commun. Integr. Biol. 2:298–301
    [Google Scholar]
  36. 36. 
    Fitzpatrick MJ, Ben-Shahar Y, Smid HM, Vet LEM, Robinson GE, Sokolowski MB 2005. Candidate genes for behavioural ecology. Trends Ecol. Evol. 20:96–104
    [Google Scholar]
  37. 37. 
    Fitzpatrick MJ, Feder E, Rowe L, Sokolowski MB 2007. Maintaining a behaviour polymorphism by frequency-dependent selection on a single gene. Nature 447:210–12
    [Google Scholar]
  38. 38. 
    Foucaud J, Philippe A-S, Moreno C, Mery F 2013. A genetic polymorphism affecting reliance on personal versus public information in a spatial learning task in Drosophila melanogaster. Proc. R. Soc. B 280:20130588
    [Google Scholar]
  39. 39. 
    Freedman B. 2015. Ecological Effects of Environmental Stressors, Vol. 1 Oxford, UK: Oxford Univ. Press
    [Google Scholar]
  40. 40. 
    Fujiwara M, Sengupta P, McIntire SL 2002. Regulation of body size and behavioral state of C. elegans by sensory perception and the EGL-4 cGMP-dependent protein kinase. Neuron 36:1091–102
    [Google Scholar]
  41. 41. 
    Graf SA, Sokolowski MB. 1989. Rover/sitter Drosophila melanogaster larval foraging polymorphism as a function of larval development, food-patch quality, and starvation. J. Insect Behav. 2:301–13
    [Google Scholar]
  42. 42. 
    Graveley BR, Brooks AN, Carlson JW, Duff MO, Landolin JM et al. 2011. The developmental transcriptome of Drosophila melanogaster. Nature 471:473–79
    [Google Scholar]
  43. 43. 
    Haas B, Mayer P, Jennissen K, Scholz D, Berriel Diaz M et al. 2009. Protein kinase G controls brown fat cell differentiation and mitochondrial biogenesis. Sci. Signal. 2:ra78
    [Google Scholar]
  44. 44. 
    Harbison ST, Serrano Negron YL, Hansen NF, Lobell AS 2017. Selection for long and short sleep duration in Drosophila melanogaster reveals the complex genetic network underlying natural variation in sleep. PLOS Genet 13:e1007098
    [Google Scholar]
  45. 45. 
    Hawn SE, Sheerin CM, Webb BT, Peterson RE, Do EK et al. 2018. Replication of the interaction of PRKG1 and trauma exposure on alcohol misuse in an independent African American sample. J. Trauma. Stress 31:927–32
    [Google Scholar]
  46. 46. 
    Heylen K, Gobin B, Billen J, Hu T-T, Arckens L, Huybrechts R 2008. Amfor expression in the honeybee brain: a trigger mechanism for nurse–forager transition. J. Insect Physiol. 54:1400–3
    [Google Scholar]
  47. 47. 
    Hoke KL, Adkins-Regan E, Bass AH, McCune AR, Wolfner MF 2019. Co-opting evo-devo concepts for new insights into mechanisms of behavioural diversity. J. Exp. Biol. 222:jeb190058
    [Google Scholar]
  48. 48. 
    Hughson BN, Anreiter I, Jackson Chornenki NL, Murphy KR, Ja WW et al. 2017. The adult foraging assay (AFA) detects strain and food-deprivation effects in feeding-related traits of Drosophila melanogaster. J. Insect Physiol 106:20–29
    [Google Scholar]
  49. 49. 
    Ingram KK, Oefner P, Gordon DM 2005. Task-specific expression of the foraging gene in harvester ants. Mol. Ecol. 14:813–18
    [Google Scholar]
  50. 50. 
    Kaun KR, Hendel T, Gerber B, Sokolowski MB 2007. Natural variation in Drosophila larval reward learning and memory due to a cGMP-dependent protein kinase. Learn. Mem. 14:342–49
    [Google Scholar]
  51. 51. 
    Kaun KR, Riedl CAL, Chakaborty-Chatterjee M, Belay AT, Douglas SJ et al. 2007. Natural variation in food acquisition mediated via a Drosophila cGMP-dependent protein kinase. J. Exp. Biol. 210:3547–58
    [Google Scholar]
  52. 52. 
    Kaye JA, Rose NC, Goldsworthy B, Goga A, L'Etoile ND 2009. A 3′UTR Pumilio-binding element directs translational activation in olfactory sensory neurons. Neuron 61:57–70
    [Google Scholar]
  53. 53. 
    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
    [Google Scholar]
  54. 54. 
    Klengel T, Mehta D, Anacker C, Rex-Haffner M, Pruessner JC et al. 2013. Allele-specific FKBP5 DNA demethylation mediates gene–childhood trauma interactions. Nat. Neurosci. 16:33–41
    [Google Scholar]
  55. 55. 
    Kleppisch T, Pfeifer A, Klatt P, Ruth P, Montkowski A et al. 1999. Long-term potentiation in the hippocampal CA1 region of mice lacking cGMP-dependent kinases is normal and susceptible to inhibition of nitric oxide synthase. J. Neurosci. 19:48–55
    [Google Scholar]
  56. 56. 
    Kleppisch T, Wolfsgruber W, Feil S, Allmann R, Wotjak CT et al. 2003. Hippocampal cGMP-dependent protein kinase I supports an age- and protein synthesis-dependent component of long-term potentiation but is not essential for spatial reference and contextual memory. J. Neurosci. 23:6005–12
    [Google Scholar]
  57. 57. 
    Kodaira Y, Ohtsuki H, Yokoyama J, Kawata M 2009. Size-dependent foraging gene expression and behavioral caste differentiation in Bombus ignitus. BMC Res. Notes 2:184
    [Google Scholar]
  58. 58. 
    Kohn NR, Reaume CJ, Moreno C, Burns JG, Sokolowski MB 2013. Social environment influences performance in a cognitive task in natural variants of the foraging gene. PLOS ONE 8:e81272
    [Google Scholar]
  59. 59. 
    Kroetz SM, Srinivasan J, Yaghoobian J, Sternberg PW, Hong RL 2012. The cGMP signaling pathway affects feeding behavior in the necromenic nematode Pristionchus pacificus. PLOS ONE 7:e34464
    [Google Scholar]
  60. 60. 
    Kuntz S, Poeck B, Sokolowski MB, Strauss R 2012. The visual orientation memory of Drosophila requires foraging (PKG) upstream of ignorant (RSK2) in ring neurons of the central complex. Learn. Mem. 19:337–40
    [Google Scholar]
  61. 61. 
    L'Etoile ND, Coburn CM, Eastham J, Kistler A, Gallegos G, Bargmann CI 2002. The cyclic GMP-dependent protein kinase EGL-4 regulates olfactory adaptation in C. elegans. Neuron 36:1079–89
    [Google Scholar]
  62. 62. 
    Lucas C, Kornfein R, Chakaborty-Chatterjee M, Schonfeld J, Geva N et al. 2010. The locust foraging gene. Arch. Insect Biochem. Physiol. 74:52–66
    [Google Scholar]
  63. 63. 
    Lucas C, Sokolowski MB. 2009. Molecular basis for changes in behavioral state in ant social behaviors. PNAS 106:6351–56
    [Google Scholar]
  64. 64. 
    Mackay TFC, Stone EA, Ayroles JF 2009. The genetics of quantitative traits: challenges and prospects. Nat. Rev. Genet. 10:565–77
    [Google Scholar]
  65. 65. 
    MacPherson MR, Broderick KE, Graham S, Day JP, Houslay MD et al. 2004. The dg2 (for) gene confers a renal phenotype in Drosophila by modulation of cGMP-specific phosphodiesterase. J. Exp. Biol. 207:2769–76
    [Google Scholar]
  66. 66. 
    MacPherson MR, Lohmann SM, Davies S-A 2004. Analysis of Drosophila cGMP-dependent protein kinases and assessment of their in vivo roles by targeted expression in a renal transporting epithelium. J. Biol. Chem. 279:40026–34
    [Google Scholar]
  67. 67. 
    Malé P-JG, Turner KM, Doha M, Anreiter I, Allen AM et al. 2017. An ant–plant mutualism through the lens of cGMP-dependent kinase genes. Proc. R. Soc. B 284:20170896
    [Google Scholar]
  68. 68. 
    Mery F, Belay AT, So AK-C, Sokolowski MB, Kawecki TJ 2007. Natural polymorphism affecting learning and memory in Drosophila. PNAS 104:13051–55
    [Google Scholar]
  69. 69. 
    Miyashita K, Itoh H, Tsujimoto H, Tamura N, Fukunaga Y et al. 2009. Natriuretic peptides/cGMP/cGMP-dependent protein kinase cascades promote muscle mitochondrial biogenesis and prevent obesity. Diabetes 58:2880–92
    [Google Scholar]
  70. 70. 
    Neale BM, Medland S, Ripke S, Anney RJL, Asherson P et al. 2010. Case-control genome-wide association study of attention-deficit/hyperactivity disorder. J. Am. Acad. Child Adolesc. Psychiatry 49:906–20
    [Google Scholar]
  71. 71. 
    Nègre N, Brown CD, Ma L, Bristow CA, Miller SW et al. 2011. A cis-regulatory map of the Drosophila genome. Nature 471:527–31
    [Google Scholar]
  72. 72. 
    Oettler J, Nachtigal A-L, Schrader L 2015. Expression of the foraging gene is associated with age polyethism, not task preference, in the ant Cardiocondyla obscurior. PLOS ONE 10:e0144699
    [Google Scholar]
  73. 73. 
    Okhovat M, Berrio A, Wallace G, Ophir AG, Phelps SM 2015. Sexual fidelity trade-offs promote regulatory variation in the prairie vole brain. Science 350:1371–74
    [Google Scholar]
  74. 74. 
    Osborne KA, Robichon A, Burgess E, Butland S, Shaw RA et al. 1997. Natural behavior polymorphism due to a cGMP-dependent protein kinase of Drosophila. Science 277:834–36
    [Google Scholar]
  75. 75. 
    Ott SR, Verlinden H, Rogers SM, Brighton CH, Quah PS et al. 2012. Critical role for protein kinase A in the acquisition of gregarious behavior in the desert locust. PNAS 109:E381–87
    [Google Scholar]
  76. 76. 
    Paul C, Schöberl F, Weinmeister P, Micale V, Wotjak CT 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. 28:14202–12
    [Google Scholar]
  77. 77. 
    Paul C, Stratil C, Hofmann F, Kleppisch T 2010. cGMP-dependent protein kinase type I promotes CREB/CRE-mediated gene expression in neurons of the lateral amygdala. Neurosci. Lett. 473:82–86
    [Google Scholar]
  78. 78. 
    Peng Q, Wang Y, Li M, Yuan D, Xu M et al. 2016. cGMP-dependent protein kinase encoded by foraging regulates motor axon guidance in Drosophila by suppressing Lola function. J. Neurosci. 36:4635–46
    [Google Scholar]
  79. 79. 
    Pereira HS, Sokolowski MB. 1993. Mutations in the larval foraging gene affect adult locomotory behavior after feeding in Drosophila melanogaster. PNAS 90:5044–46
    [Google Scholar]
  80. 80. 
    Pfeifer A, Klatt P, Massberg S, Ny L, Sausbier M et al. 1998. Defective smooth muscle regulation in cGMP kinase I-deficient mice. EMBO J 17:3045–51
    [Google Scholar]
  81. 81. 
    Philippe A-S, Jeanson R, Pasquaretta C, Rebaudo F, Sueur C, Mery F 2016. Genetic variation in aggregation behaviour and interacting phenotypes in Drosophila. Proc. R. Soc. B 283:20152967
    [Google Scholar]
  82. 82. 
    Polimanti R, Kaufman J, Zhao H, Kranzler HR, Ursano RJ et al. 2018. A genome-wide gene-by-trauma interaction study of alcohol misuse in two independent cohorts identifies PRKG1 as a risk locus. Mol. Psychiatry 23:154–60
    [Google Scholar]
  83. 83. 
    Raizen DM, Zimmerman JE, Maycock MH, Ta UD, You Y et al. 2008. Lethargus is a Caenorhabditis elegans sleep-like state. Nature 451:569–72
    [Google Scholar]
  84. 84. 
    Reaume CJ, Sokolowski MB, Mery F 2011. A natural genetic polymorphism affects retroactive interference in Drosophila melanogaster. Proc. R. Soc. B 278:91–98
    [Google Scholar]
  85. 85. 
    Renger JJ, Yao WD, Sokolowski MB, Wu CF 1999. Neuronal polymorphism among natural alleles of a cGMP-dependent kinase gene, foraging, in Drosophila. J. Neurosci 19:RC28
    [Google Scholar]
  86. 86. 
    Robertson RM, Sillar KT. 2009. The nitric oxide/cGMP pathway tunes the thermosensitivity of swimming motor patterns in Xenopus laevis tadpoles. J. Neurosci. 29:13945–51
    [Google Scholar]
  87. 87. 
    Robinson GE. 1992. Regulation of division of labor in insect societies. Annu. Rev. Entomol. 37:637–65
    [Google Scholar]
  88. 88. 
    Sanyal A, Naumann J, Hoffmann LS, Chabowska-Kita A, Ehrlund A et al. 2017. Interplay between obesity-induced inflammation and cGMP signaling in white adipose tissue. Cell Rep 18:225–36
    [Google Scholar]
  89. 89. 
    Scheiner R, Sokolowski MB, Erber J 2004. Activity of cGMP-dependent protein kinase (PKG) affects sucrose responsiveness and habituation in Drosophila melanogaster. Learn. Mem 11:303–11
    [Google Scholar]
  90. 90. 
    Schmidt H, Werner M, Heppenstall PA, Henning M, Moré MI et al. 2002. cGMP-mediated signaling via cGKIα is required for the guidance and connectivity of sensory axons. J. Cell Biol. 159:489–98
    [Google Scholar]
  91. 91. 
    Shaver SA, Varnam CJ, Hilliker AJ, Sokolowski MB 1998. The foraging gene affects adult but not larval olfactory-related behavior in Drosophila melanogaster. Behav. Brain Res 95:23–29
    [Google Scholar]
  92. 92. 
    Sokolowski HM, Vasquez OE, Unternaehrer E, Sokolowski DJ, Biergans SD et al. 2017. The Drosophila foraging gene human orthologue PRKG1 predicts individual differences in the effects of early adversity on maternal sensitivity. Cogn. Dev. 42:62–73
    [Google Scholar]
  93. 93. 
    Sokolowski MB. 1980. Foraging strategies of Drosophila melanogaster: a chromosomal analysis. Behav. Genet. 10:291–302
    [Google Scholar]
  94. 94. 
    Sokolowski MB, Hansell RIC. 1983. Elucidating the behavioral phenotype of Drosophila melanogaster larvae: correlations between larval foraging strategies and pupation height. Behav. Genet. 13:267–80
    [Google Scholar]
  95. 95. 
    Sokolowski MB, Pereira HS, Hughes K, Mery F, Dolan MJ et al. 1997. Evolution of foraging behavior in Drosophila by density-dependent selection. PNAS 94:7373–77
    [Google Scholar]
  96. 96. 
    Song H, Foquet B, Mariño-Pérez R, Woller DA 2017. Phylogeny of locusts and grasshoppers reveals complex evolution of density-dependent phenotypic plasticity. Sci. Rep. 7:6606
    [Google Scholar]
  97. 97. 
    Spong KE, Rodríguez EC, Robertson XRM 2016. Spreading depolarization in the brain of Drosophila is induced by inhibition of the Na+/K+-ATPase and mitigated by a decrease in activity of protein kinase G. J. Neurophysiol. 116:1152–60
    [Google Scholar]
  98. 98. 
    Stamatakis A. 2014. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–13
    [Google Scholar]
  99. 99. 
    Steiner JA, Carneiro AMD, Wright J, Matthies HJG, Prasad HC et al. 2009. cGMP-dependent protein kinase Iα associates with the antidepressant-sensitive serotonin transporter and dictates rapid modulation of serotonin uptake. Mol. Brain 2:26
    [Google Scholar]
  100. 100. 
    Struk AA, Mugon J, Huston A, Scholer AA, Stadler G et al. 2019. Self-regulation and the foraging gene (PRKG1) in humans. PNAS 116:4434–39
    [Google Scholar]
  101. 101. 
    Takahashi Y, Tanaka R, Yamamoto D, Noriyuki S, Kawata M 2018. Balanced genetic diversity improves population fitness. Proc. R. Soc. B 285:20172045
    [Google Scholar]
  102. 102. 
    Tegeder I, Del Turco D, Schmidtko A, Sausbier M, Feil R et al. 2004. Reduced inflammatory hyperalgesia with preservation of acute thermal nociception in mice lacking cGMP-dependent protein kinase I. PNAS 101:3253–57
    [Google Scholar]
  103. 103. 
    Thamm M, Scheiner R. 2014. PKG in honey bees: spatial expression, Amfor gene expression, sucrose responsiveness, and division of labor. J. Comp. Neurol. 522:1786–99
    [Google Scholar]
  104. 104. 
    Thoday JM, Thompson JN. 1976. The number of segregating genes implied by continuous variation. Genetica 46:335–44
    [Google Scholar]
  105. 105. 
    Thompson JN. 1975. Quantitative variation and gene number. Nature 258:665–68
    [Google Scholar]
  106. 106. 
    Tobback J, Mommaerts V, Vandersmissen HP, Smagghe G, Huybrechts R 2011. Age- and task-dependent foraging gene expression in the bumblebee Bombus terrestris. . Arch. Insect Biochem. Physiol 76:30–42
    [Google Scholar]
  107. 107. 
    Wang S, Sokolowski MB. 2017. Aggressive behaviours, food deprivation and the foraging gene. R. Soc. Open Sci. 4:170042
    [Google Scholar]
  108. 108. 
    Wang Z, Pan Y, Li W, Jiang H, Chatzimanolis L et al. 2008. Visual pattern memory requires foraging function in the central complex of Drosophila. Learn. Mem 15:133–42
    [Google Scholar]
  109. 109. 
    Wenseleers T, Billen J, Arckens L, Tobback J, Huybrechts R et al. 2008. Cloning and expression of PKG, a candidate foraging regulating gene in Vespula vulgaris. Anim. Biol 58:341–51
    [Google Scholar]
  110. 110. 
    Zayed A, Robinson GE. 2012. Understanding the relationship between brain gene expression and social behavior: lessons from the honey bee. Annu. Rev. Genet. 46:591–615
    [Google Scholar]
  111. 111. 
    Zhang Y-W, Rudnick G. 2011. Myristoylation of cGMP-dependent protein kinase dictates isoform specificity for serotonin transporter regulation. J. Biol. Chem. 286:2461–68
    [Google Scholar]
  112. 112. 
    Zhao Z, Webb BT, Jia P, Bigdeli TB, Maher BS et al. 2013. Association study of 167 candidate genes for schizophrenia selected by a multi-domain evidence-based prioritization algorithm and neurodevelopmental hypothesis. PLOS ONE 8:e67776
    [Google Scholar]
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