1932

Abstract

Water is essential to life. Terrestrial insects lose water by evaporation from the body surface and respiratory surfaces, as well as in the excretory products, posing a challenge made more acute by their high surface-to-volume ratio. These losses must be kept to a minimum and be offset by water gained from other sources. By contrast, insects such as the blood-sucking bug consume up to 10 times their body weight in a single blood meal, necessitating rapid expulsion of excess water and ions. How do insects manage their ion and water budgets? A century of study has revealed a great deal about the organ systems that insects use to maintain their ion and water balance and their regulation. Traditionally, a taxonomically wide range of species were studied, whereas more recent research has focused on model organisms to leverage the power of the molecular genetic approach. Key advances in new technologies have become available for a wider range of species in the past decade. We document how these approaches have already begun to inform our understanding of the diversity and conservation of insect systemic osmoregulation. We advocate that these technologies be combined with traditional approaches to study a broader range of nonmodel species to gain a comprehensive overview of the mechanism underpinning systemic osmoregulation in the most species-rich group of animals on earth, the insects.

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2024-01-29
2024-04-21
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Literature Cited

  1. 1.
    Adams JR, Wilcox TA. 1973. Determination of osmolalities of insect hemolymph from several species. Ann. Entomol. Soc. Am. 66:575–77
    [Google Scholar]
  2. 2.
    Adams MD, Celniker SE, Holt RA, Evans CA, Gocayne JD et al. 2000. The genome sequence of Drosophila melanogaster. Science 287:2185–95
    [Google Scholar]
  3. 3.
    Al-Anzi B, Armand E, Nagamei P, Olszewski M, Sapin V et al. 2010. The leucokinin pathway and its neurons regulate meal size in Drosophila. Curr. Biol. 20:969–78
    [Google Scholar]
  4. 4.
    Andersen MK, Overgaard J. 2020. Maintenance of hindgut reabsorption during cold exposure is a key adaptation for Drosophila cold tolerance. J. Exp. Biol. 223:4jeb213934
    [Google Scholar]
  5. 5.
    Arab A, Caetano FH. 2002. Segmental specializations in the Malpighian tubules of the fire ant Solenopsis saevissima Forel 1904 (Myrmicinae): an electron microscopical study. Arthropod Struct. Dev. 30:281–92
    [Google Scholar]
  6. 6.
    Audsley N, Goldsworthy GJ, Coast GM. 1997. Circulating levels of Locusta diuretic hormone: the effect of feeding. Peptides 18:59–65
    [Google Scholar]
  7. 7.
    Baker DA, Nolan T, Fischer B, Pinder A, Crisanti A, Russell S. 2011. A comprehensive gene expression atlas of sex- and tissue-specificity in the malaria vector. Anopheles gambiae. BMC Genom. 12:296
    [Google Scholar]
  8. 8.
    Baldwin DC, Schegg KM, Furuya K, Lehmberg E, Schooley DA. 2001. Isolation and identification of a diuretic hormone from Zootermopsis nevadensis. Peptides 22:147–52
    [Google Scholar]
  9. 9.
    Barrett M, Orchard I. 1990. Serotonin-induced elevation of cAMP levels in the epidermis of the blood-sucking bug, Rhodnius prolixus. J. Insect Physiol. 36:625–33
    [Google Scholar]
  10. 10.
    Beament J, Noble-Nesbitt J, Watson J. 1964. The waterproofing mechanism of arthropods: III. Cuticular permeability in the firebrat, Thermobia domestica (Packard). J. Exp. Biol. 41:323–30
    [Google Scholar]
  11. 11.
    Benguettat O, Jneid R, Soltys J, Loudhaief R, Brun-Barale A et al. 2018. The DH31/CGRP enteroendocrine peptide triggers intestinal contractions favoring the elimination of opportunistic bacteria. PLOS Pathog. 14:e1007279
    [Google Scholar]
  12. 12.
    Berridge MJ, Gupta BL. 1967. Fine-structural changes in relation to ion and water transport in the rectal papillae of the blowfly. Calliphora. J. Cell Sci. 2:89–112
    [Google Scholar]
  13. 13.
    Beutel RG, Friedrich F, Aspöck U. 2010. The larval head of Nevrorthidae and the phylogeny of Neuroptera (Insecta). Zool. J. Linn. Soc. 158:533–62
    [Google Scholar]
  14. 14.
    Black K, Meredith J, Thomson B, Phillips J, Dietz T. 1987. Mechanisms and properties of sodium transport in locust rectum. Can. J. Zool. 65:3084–92
    [Google Scholar]
  15. 15.
    Blackburn MB, Kingan TG, Bodnar W, Shabanowitz J, Hunt DF et al. 1991. Isolation and identification of a new diuretic peptide from the tobacco hornworm, Manduca sexta. Biochem. Biophys. Res. Commun. 181:927–32
    [Google Scholar]
  16. 16.
    Blumenthal EM. 2003. Regulation of chloride permeability by endogenously produced tyramine in the Drosophila Malpighian tubule. Am. J. Physiol. Cell Physiol. 284:C718–28
    [Google Scholar]
  17. 17.
    Buxton PA. 1930. Evaporation from the meal-worm (Tenebrio: Coleoptera) and atmospheric humidity. Proc. R. Soc. Lond. B 106:560–77
    [Google Scholar]
  18. 18.
    Buxton PA, Haldane JS. 1930. Evaporation from the meal-worm Tenebrio (Coleoptera) and atmospheric humidity. Proc. R. Soc. Lond. B 106:560–77
    [Google Scholar]
  19. 19.
    Buxton PA, Lewis DJ, Marshall GAK. 1934. Climate and tsetse flies: laboratory studies upon Glossina submorsitans and tachinoides. Philos. Trans. R. Soc. Lond. B 224:175–240
    [Google Scholar]
  20. 20.
    Cabrero P, Radford JC, Broderick KE, Costes L, Veenstra JA et al. 2002. The Dh gene of Drosophila melanogaster encodes a diuretic peptide that acts through cyclic AMP. J. Exp. Biol. 205:3799–807
    [Google Scholar]
  21. 21.
    Cabrero P, Richmond L, Nitabach M, Davies SA, Dow JAT. 2013. A biogenic amine and a neuropeptide act identically: tyramine signals through calcium in Drosophila tubule stellate cells. Proc. Biol. Sci. 280:20122943
    [Google Scholar]
  22. 22.
    Cabrero P, Terhzaz S, Dornan AJ, Ghimire S, Holmes HL et al. 2020. Specialized stellate cells offer a privileged route for rapid water flux in Drosophila renal tubule. PNAS 117:1779–87
    [Google Scholar]
  23. 23.
    Cabrero P, Terhzaz S, Romero MF, Davies SA, Blumenthal EM, Dow JAT. 2014. Chloride channels in stellate cells are essential for uniquely high secretion rates in neuropeptide-stimulated Drosophila diuresis. PNAS 111:14301–6
    [Google Scholar]
  24. 24.
    Cardoso JCR, Félix RC, Bergqvist CA, Larhammar D. 2014. New insights into the evolution of vertebrate CRH (corticotropin-releasing hormone) and invertebrate DH44 (diuretic hormone 44) receptors in metazoans. Gen. Comp. Endocrinol. 209:162–70
    [Google Scholar]
  25. 25.
    Chiang RG, Chiang JA, Davey KG. 1990. Structure of the abdominal receptor responsive to internally applied pressure in the blood-feeding insect, Rhodnius prolixus. Cell Tissue Res. 261:583–87
    [Google Scholar]
  26. 26.
    Chiang RG, Davey KG. 1988. A novel receptor capable of monitoring applied pressure in the abdomen of an insect. Science 241:1665–67
    [Google Scholar]
  27. 27.
    Chintapalli VR, Wang J, Dow JA. 2007. Using FlyAtlas to identify better Drosophila melanogaster models of human disease. Nat. Genet. 39:715–20
    [Google Scholar]
  28. 28.
    Coast GM, Hayes TK, Kay I, Chung J-S. 1992. Effect of Manduca sexta diuretic hormone and related peptides on isolated Malpighian tubules of the house cricket Acheta domesticus (L.). J. Exp. Biol. 162:331–38
    [Google Scholar]
  29. 29.
    Coast GM, Webster SG, Schegg KM, Tobe SS, Schooley DA. 2001. The Drosophila melanogaster homologue of an insect calcitonin-like diuretic peptide stimulates V-ATPase activity in fruit fly Malpighian tubules. J. Exp. Biol. 204:1795–804
    [Google Scholar]
  30. 30.
    Cognigni P, Bailey AP, Miguel-Aliaga I. 2011. Enteric neurons and systemic signals couple nutritional and reproductive status with intestinal homeostasis. Cell Metab. 13:92–104
    [Google Scholar]
  31. 31.
    Coutchié PA, Crowe JH. 1979. Transport of water vapor by Tenebrionid beetles. I. Kinetics. Physiol. Zool. 52:67–87
    [Google Scholar]
  32. 32.
    Coutchié PA, Machin J. 1984. Allometry of water vapor absorption in two species of tenebrionid beetle larvae. Am. J. Physiol. Regul. Integr. Comp. Physiol. 247:R230–36
    [Google Scholar]
  33. 33.
    Davies SA, Huesmann GR, Maddrell SH, O'Donnell MJ, Skaer NJ et al. 1995. CAP2b, a cardioacceleratory peptide, is present in Drosophila and stimulates tubule fluid secretion via cGMP. Am. J. Physiol. 269:R1321–26
    [Google Scholar]
  34. 34.
    Davies SA, Stewart EJ, Huesmann GR, Skaer NJ, Maddrell SH et al. 1997. Neuropeptide stimulation of the nitric oxide signaling pathway in Drosophila melanogaster Malpighian tubules. Am. J. Physiol. 273:R823–27
    [Google Scholar]
  35. 35.
    Day JP, Wan S, Allan AK, Kean L, Davies SA et al. 2008. Identification of two partners from the bacterial Kef exchanger family for the apical plasma membrane V-ATPase of Metazoa. J. Cell Sci. 121:2612–19
    [Google Scholar]
  36. 36.
    Denholm B, Hu H, Fauquier T, Caubit X, Fasano L, Skaer H. 2013. The tiptop/teashirt genes regulate cell differentiation and renal physiology in Drosophila. Development 140:1100–10
    [Google Scholar]
  37. 37.
    Dornan AJ, Halberg KA, Beuter L-K, Davies S-A, Dow JAT. 2023. Compromised junctional integrity phenocopies age-dependent renal dysfunction in Drosophila Snakeskin mutants. J. Cell Sci. 136jcs261118
  38. 38.
    Dow JAT, Halberg KA, Terhzaz S, Davies SA. 2018. Drosophila as a model for neuroendocrine control of renal homeostasis. Model Animals in Neuroendocrinology: From Worm to Mouse to Man M Ludwig, G Levkowitz 81–100. Hoboken, NJ: Wiley
    [Google Scholar]
  39. 39.
    Dow JAT, Maddrell SHP, Görtz A, Skaer NJV, Brogan S, Kaiser K. 1994. The Malpighian tubules of Drosophila melanogaster: a novel phenotype for studies of fluid secretion and its control. J. Exp. Biol. 197:421–28
    [Google Scholar]
  40. 40.
    Dus M, Lai JS, Gunapala KM, Min S, Tayler TD et al. 2015. Nutrient sensor in the brain directs the action of the brain-gut axis in Drosophila. Neuron 87:139–51
    [Google Scholar]
  41. 41.
    Edney EB. 1967. Water balance in desert arthropods. Despite their small size, arthropods may be highly adapted for life in xeric conditions. Science 156:1059–66
    [Google Scholar]
  42. 42.
    Esquivel CJ, Cassone BJ, Piermarini PM. 2016. A de novo transcriptome of the Malpighian tubules in non-blood-fed and blood-fed Asian tiger mosquitoes Aedes albopictus: insights into diuresis, detoxification, and blood meal processing. PeerJ 4:e1784
    [Google Scholar]
  43. 43.
    Evans JM, Allan AK, Davies SA, Dow JA. 2005. Sulphonylurea sensitivity and enriched expression implicate inward rectifier K+ channels in Drosophila melanogaster renal function. J. Exp. Biol. 208:3771–83
    [Google Scholar]
  44. 44.
    Farmer J, Maddrell S, Spring J. 1981. Absorption of fluid by the midgut of Rhodnius. J Exp. Biol. 94:301–16
    [Google Scholar]
  45. 45.
    Feingold D, Knogler L, Starc T, Drapeau P, O'Donnell MJ et al. 2019. secCl is a cys-loop ion channel necessary for the chloride conductance that mediates hormone-induced fluid secretion in Drosophila. Sci. Rep. 9:7464
    [Google Scholar]
  46. 46.
    Flanagan TR, Berlind A. 1984. Serotonin modulation of the release of sequestered [3H]serotonin from nerve terminals in an insect neurohemal organ in vitro. Brain Res 306:243–50
    [Google Scholar]
  47. 47.
    Fraenkel G, Blewett M. 1944. The utilisation of metabolic water in insects. Bull. Entomol. Res. 35:127–39
    [Google Scholar]
  48. 48.
    Furuya K, Harper MA, Schegg KM, Schooley DA. 2000. Isolation and characterization of CRF-related diuretic hormones from the whitelined sphinx moth Hyles lineata. Insect Biochem. Mol. Biol. 30:127–33
    [Google Scholar]
  49. 49.
    Furuya K, Milchak RJ, Schegg KM, Zhang J, Tobe SS et al. 2000. Cockroach diuretic hormones: characterization of a calcitonin-like peptide in insects. PNAS 97:6469–74
    [Google Scholar]
  50. 50.
    Furuya K, Schegg KM, Schooley DA. 1998. Isolation and identification of a second diuretic hormone from Tenebrio molitor. Peptides 19:619–26
    [Google Scholar]
  51. 51.
    Furuya K, Schegg KM, Wang H, King DS, Schooley DA. 1995. Isolation and identification of a diuretic hormone from the mealworm Tenebrio molitor. PNAS 92:12323–27
    [Google Scholar]
  52. 52.
    Gáliková M, Dircksen H, Nässel DR. 2018. The thirsty fly: Ion transport peptide (ITP) is a novel endocrine regulator of water homeostasis in Drosophila. PLOS Genet. 14:e1007618
    [Google Scholar]
  53. 53.
    Gáliková M, Klepsatel P. 2022. Ion transport peptide regulates energy intake, expenditure, and metabolic homeostasis in Drosophila. Genetics 222:iyac150
    [Google Scholar]
  54. 54.
    Gee JD. 1975. The control of diuresis in the tsetse fly Glossina austeni: a preliminary investigation of the diuretic hormone. J. Exp. Biol. 63:391–401
    [Google Scholar]
  55. 55.
    Gee JD. 1975. Diuresis in the tsetse fly Glossina austeni. J. Exp. Biol. 63:381–90
    [Google Scholar]
  56. 56.
    Gerencser GA, Zhang J. 2003. Existence and nature of the chloride pump. Biochim. Biophys. Acta Biomembr. 1618:133–39
    [Google Scholar]
  57. 57.
    Green LF. 1980. Cryptonephric Malpighian tubule system in a dipteran larva, the New Zealand glow-worm, Arachnocampa luminosa (Diptera: Mycetophilidae): a structural study. Tissue Cell 12:141–51
    [Google Scholar]
  58. 58.
    Grimstone AV, Mullinger AM, Ramsay JA. 1968. Further studies on the rectal complex of the mealworm, Tenebrio molitor L. (Coleoptera: Teneebrionidae). Philos. Trans. R. Soc. Lond. B 253:343–82
    [Google Scholar]
  59. 59.
    Guo X, Yin C, Yang F, Zhang Y, Huang H et al. 2019. The cellular diversity and transcription factor code of Drosophila enteroendocrine cells. Cell Rep. 29:4172–85.e5
    [Google Scholar]
  60. 60.
    Gupta BL, Berridge MJ. 1966. Fine structural organization of the rectum in the blowfly, Calliphora erythrocephala (Meig.) with special reference to connective tissue, tracheae and neurosecretory innervation in the rectal papillae. J. Morphol. 120:23–81
    [Google Scholar]
  61. 61.
    Halberg KA, Terhzaz S, Cabrero P, Davies SA, Dow JA. 2015. Tracing the evolutionary origins of insect renal function. Nat. Commun. 6:6800
    [Google Scholar]
  62. 62.
    Hanrahan JW, Phillips JE. 1983. Cellular mechanisms and control of KCl absorption in insect hindgut. J. Exp. Biol. 106:71–89
    [Google Scholar]
  63. 63.
    Harshini S, Nachman RJ, Sreekumar S. 2002. Inhibition of digestive enzyme release by neuropeptides in larvae of Opisina arenosella (Lepidoptera: Cryptophasidae). Comp. Biochem. Physiol. B 132:353–58
    [Google Scholar]
  64. 64.
    Harvey WR, Wieczorek H. 1997. Animal plasma membrane energization by chemiosmotic H+ V-ATPases. J. Exp. Biol. 200:203–16
    [Google Scholar]
  65. 65.
    Hauser F, Neupert S, Williamson M, Predel R, Tanaka Y, Grimmelikhuijzen CJ. 2010. Genomics and peptidomics of neuropeptides and protein hormones present in the parasitic wasp Nasonia vitripennis. J. Proteome Res. 9:5296–310
    [Google Scholar]
  66. 66.
    Hayes TK, Pannabecker TL, Hinckley DJ, Holman GM, Nachman RJ et al. 1989. Leucokinins, a new family of ion transport stimulators and inhibitors in insect Malpighian tubules. Life Sci. 44:1259–66
    [Google Scholar]
  67. 67.
    Hector CE, Bretz CA, Zhao Y, Johnson EC. 2009. Functional differences between two CRF-related diuretic hormone receptors in Drosophila. J. Exp. Biol. 212:3142–47
    [Google Scholar]
  68. 68.
    Herman AM, Blumenthal EM. 2006. Identification of the tyramine receptor in the Drosophila Malpighian tubule. FASEB J. 20:A345–46
    [Google Scholar]
  69. 69.
    Irvine HB. 1966. In vitro rectal transport and rectal ultrastructure in the desert locust Schistocerca gregaria. M.Sc. Thesis, Univ. B. C. Vancouver, Can:.
  70. 70.
    Irvine HB. 1969. Sodium and potassium secretion by isolated insect Malpighian tubules. Am. J. Physiol. 217:1520–27
    [Google Scholar]
  71. 71.
    Iversen A, Cazzamali G, Williamson M, Hauser F, Grimmelikhuijzen CJ. 2002. Molecular cloning and functional expression of a Drosophila receptor for the neuropeptides capa-1 and -2. Biochem. Biophys. Res. Commun. 299:628–33
    [Google Scholar]
  72. 72.
    Jarial MS. 1992. Fine structure of the rectal pads in the desert locust Schistocerca gregaria with reference to the mechanism of water uptake. Tissue Cell 24:139–55
    [Google Scholar]
  73. 73.
    Johnson EC, Shafer OT, Trigg JS, Park J, Schooley DA et al. 2005. A novel diuretic hormone receptor in Drosophila: evidence for conservation of CGRP signaling. J. Exp. Biol. 208:1239–46
    [Google Scholar]
  74. 74.
    Kataoka H, Troetschler RG, Li JP, Kramer SJ, Carney RL, Schooley DA. 1989. Isolation and identification of a diuretic hormone from the tobacco hornworm, Manduca sexta. PNAS 86:2976–80
    [Google Scholar]
  75. 75.
    Keeley LL, Chung JS, Hayes TK. 1992. Diuretic and antifeedant actions by Manduca sexta diuretic hormone in lepidopteran larvae. Experientia 48:1145–48
    [Google Scholar]
  76. 76.
    Kim SK, Rulifson EJ. 2004. Conserved mechanisms of glucose sensing and regulation by Drosophila corpora cardiaca cells. Nature 431:316–20
    [Google Scholar]
  77. 77.
    King B, Denholm B. 2014. Malpighian tubule development in the red flour beetle (Tribolium castaneum). Arthropod Struct. Dev. 43:605–13
    [Google Scholar]
  78. 78.
    Kolosov D, O'Donnell MJ. 2019. The Malpighian tubules and cryptonephric complex in lepidopteran larvae. Adv. Insect Physiol. 56:165–202
    [Google Scholar]
  79. 79.
    Koyama T, Naseem MT, Kolosov D, Vo CT, Mahon D et al. 2021. A unique Malpighian tubule architecture in Tribolium castaneum informs the evolutionary origins of systemic osmoregulation in beetles. PNAS 118:e2023314118
    [Google Scholar]
  80. 80.
    Koyama T, Rana DW, Halberg KV. 2023. Managing fuels and fluids: network integration of osmoregulatory and metabolic hormonal circuits in the polymodal control of homeostasis in insects. BioEssays 45(9):2300011
    [Google Scholar]
  81. 81.
    Koyama T, Terhzaz S, Naseem MT, Nagy S, Rewitz K et al. 2021. A nutrient-responsive hormonal circuit mediates an inter-tissue program regulating metabolic homeostasis in adult Drosophila. Nat. Commun. 12:5178
    [Google Scholar]
  82. 82.
    Kunst M, Hughes ME, Raccuglia D, Felix M, Li M et al. 2014. Calcitonin gene-related peptide neurons mediate sleep-specific circadian output in Drosophila. Curr. Biol. 24:2652–64
    [Google Scholar]
  83. 83.
    Lange AB, Orchard I, Barrett FM. 1989. Changes in haemolymph serotonin levels associated with feeding in the blood-sucking bug, Rhodnius prolixus. J. Insect Physiol. 35:393–99
    [Google Scholar]
  84. 84.
    Leader DP, Krause SA, Pandit A, Davies SA, Dow JA T. 2017. FlyAtlas 2: a new version of the Drosophila melanogaster expression atlas with RNA-Seq, miRNA-Seq and sex-specific data. Nucleic Acids Res. 46:D809–15
    [Google Scholar]
  85. 85.
    Lehmberg E, Ota RB, Furuya K, King DS, Applebaum SW et al. 1991. Identification of a diuretic hormone of Locusta migratoria. Biochem. Biophys. Res. Commun. 179:1036–41
    [Google Scholar]
  86. 86.
    Li B, Predel R, Neupert S, Hauser F, Tanaka Y et al. 2008. Genomics, transcriptomics, and peptidomics of neuropeptides and protein hormones in the red flour beetle Tribolium castaneum. Genome Res. 18:113–22
    [Google Scholar]
  87. 87.
    Li Y, Piermarini PM, Esquivel CJ, Drumm HE, Schilkey FD, Hansen IA. 2017. RNA-seq comparison of larval and adult Malpighian tubules of the yellow fever mosquito Aedes aegypti reveals life stage-specific changes in renal function. Front. Physiol. 8:283
    [Google Scholar]
  88. 88.
    Lison L. 1937. Sur la structure de la region cryptosoleniee chez les Coleopteres Tenebrio molitor L. et Dermestes lardarius L. Bull. R. Acad. Belg. 23:317–27
    [Google Scholar]
  89. 89.
    Ludwig D, Wugmeister M. 1953. Effects of starvation on the blood of Japanese beetle (Popillia japonica Newman) larvae. Physiol. Zool. 26:254–59
    [Google Scholar]
  90. 90.
    Machin J. 1975. Water balance in Tenebrio molitor, L. larvae; the effect of atmospheric water absorption. J. Comp. Physiol. A 101:121–32
    [Google Scholar]
  91. 91.
    Machin J, O'Donnell MJ. 1991. Rectal complex ion activities and electrochemical gradients in larvae of the desert beetle, Onymacris: comparisons with Tenebrio. J. Insect Physiol. 37:829–38
    [Google Scholar]
  92. 92.
    MacMillan HA, Nazal B, Wali S, Yerushalmi GY, Misyura L et al. 2018. Anti-diuretic activity of a CAPA neuropeptide can compromise Drosophila chill tolerance. J. Exp. Biol. 221:jeb185884
    [Google Scholar]
  93. 93.
    Maddrell SH. 1964. Excretion in the blood-sucking bug, Rhodnius prolixus Stål. 3. The control of the release of the diuretic hormone. J. Exp. Biol. 41:459–72
    [Google Scholar]
  94. 94.
    Maddrell SH. 1964. Excretion in the blood-sucking bug, Rhodnius prolixus Stål. II. The normal course of diuresis and the effect of temperature. J. Exp. Biol. 41:163–76
    [Google Scholar]
  95. 95.
    Maddrell SH, Pilcher DE, Gardiner BO. 1969. Stimulatory effect of 5-hydroxytryptamine (serotonin) on secretion by Malpighian tubules of insects. Nature 222:784–85
    [Google Scholar]
  96. 96.
    Maddrell SH, Pilcher DE, Gardiner BO. 1971. Pharmacology of the Malpighian tubules of Rhodnius and Carausius: the structure-activity relationship of tryptamine analogues and the role of cyclic AMP. J. Exp. Biol. 54:779–804
    [Google Scholar]
  97. 97.
    Maddrell SHP. 1963. Excretion in the blood-sucking bug, Rhodnius prolixus Stål. I. The control of diuresis. J. Exp. Biol. 40:247–56
    [Google Scholar]
  98. 98.
    Maddrell SHP. 1969. Secretion by the Malpighian tubules of Rhodnius. The movements of ions and water. J. Exp. Biol. 51:71–97
    [Google Scholar]
  99. 99.
    Maddrell SHP. 1978. Physiological discontinuity in an epithelium with an apparently uniform structure. J. Exp. Biol. 75:133–45
    [Google Scholar]
  100. 100.
    Maddrell SHP. 1991. The fastest fluid-secreting cell known: the upper Malpighian tubule cell of Rhodnius. Bioessays 13:357–62
    [Google Scholar]
  101. 101.
    Maddrell SHP. 2015. Functional design of the neurosecretory system controlling diuresis in Rhodnius prolixus. Am. Zool. 16:131–39
    [Google Scholar]
  102. 102.
    Maddrell SHP, Herman WS, Farndale RW, Riegel JA. 1993. Synergism of hormones controlling epithelial fluid transport in an insect. J. Exp. Biol. 174:65–80
    [Google Scholar]
  103. 103.
    Maddrell SHP, Herman WS, Mooney RL, Overton JA. 1991. 5-Hydroxytryptamine: a second diuretic hormone in Rhodnius prolixus. J. Exp. Biol. 156:557–66
    [Google Scholar]
  104. 104.
    Maddrell SHP, Overton J. 1990. Methods for the study of fluid and solute transport and their control in insect Malpighian tubules. Methods Enzymol. 192:617–32
    [Google Scholar]
  105. 105.
    Maddrell SHP, Phillips JE. 1975. Secretion of hypo-osmotic fluid by the lower Malpighian tubules of Rhodnius prolixus. J. Exp. Biol. 62:671–83
    [Google Scholar]
  106. 106.
    Maxwell DE. 1955. The comparative internal larval anatomy of sawflies (Hymenoptera: Symphyta). Mem. Entomol. Soc. Can. 87:5–132
    [Google Scholar]
  107. 107.
    Mellanby K. 1932. The effect of atmospheric humidity on the metabolism of the fasting mealworm (Tenebrio molitor L., Coleoptera). Proc. R. Soc. Lond. B 111:376–90
    [Google Scholar]
  108. 108.
    Mirabeau O, Joly JS. 2013. Molecular evolution of peptidergic signaling systems in bilaterians. PNAS 110:E2028–37
    [Google Scholar]
  109. 109.
    Montoreano R, Triana F, Abate T, Rangel-Aldao R. 1990. Cyclic AMP in the Malpighian tubule fluid and in the urine of Rhodnius prolixus. Gen. Comp. Endocrinol. 77:136–42
    [Google Scholar]
  110. 110.
    Naseem MT, Beaven R, Koyama T, Naz S, Su S-Y et al. 2023. NHA1 is a cation/proton antiporter essential for the water-conserving functions of the rectal complex in Tribolium castaneum. PNAS 120:e2217084120
    [Google Scholar]
  111. 111.
    Nijhout HF, Carrow GM. 1978. Diuresis after a bloodmeal in female Anopheles freeborni. J. Insect Physiol. 24:293–98
    [Google Scholar]
  112. 112.
    Noble-Nesbitt J. 1969. Water balance in the firebrat, Thermobia domestica (Packard). Exchanges of water with the atmosphere. J. Exp. Biol. 50:745–69
    [Google Scholar]
  113. 113.
    Noble-Nesbitt J. 1970. Water uptake from subsaturated atmospheres: its site in insects. Nature 225:753–54
    [Google Scholar]
  114. 114.
    Noirot C, Noirot-Timothée C. 1977. Fine structure of the rectum in termites (Isoptera): a comparative study. Tissue Cell 9:693–710
    [Google Scholar]
  115. 115.
    O'Donnell MJ, Dow JA, Huesmann GR, Tublitz NJ, Maddrell SH. 1996. Separate control of anion and cation transport in Malpighian tubules of Drosophila melanogaster. J. Exp. Biol. 199:1163–75
    [Google Scholar]
  116. 116.
    O'Donnell MJ, Machin J. 1991. Ion activities and electrochemical gradients in the mealworm rectal complex. J. Exp. Biol. 155:375–402
    [Google Scholar]
  117. 117.
    O'Donnell MJ, Maddrell SH. 1995. Fluid reabsorption and ion transport by the lower Malpighian tubules of adult female Drosophila. J. Exp. Biol. 198:Pt 81647–53
    [Google Scholar]
  118. 118.
    Orchard I. 1989. Serotonergic neurohaemal tissue in Rhodnius prolixus: synthesis, release and uptake of serotonin. J. Insect Physiol. 35:943–47
    [Google Scholar]
  119. 119.
    Orchard I, Lange AB, Barrett FM. 1988. Serotonergic supply to the epidermis of Rhodnius prolixus: evidence for serotonin as the plasticising factor. J. Insect Physiol. 34:873–79
    [Google Scholar]
  120. 120.
    Orchard I, Leyria J, Al-Dailami A, Lange AB. 2021. Fluid secretion by Malpighian tubules of Rhodnius prolixus: neuroendocrine control with new insights from a transcriptome analysis. Front. Endocrinol. 12:722487
    [Google Scholar]
  121. 121.
    Orchard I, Paluzzi JP. 2009. Diuretic and antidiuretic hormones in the blood-gorging bug Rhodnius prolixus. Ann. N. Y. Acad. Sci. 1163:501–3
    [Google Scholar]
  122. 122.
    Overend G, Cabrero P, Halberg KA, Ranford-Cartwright LC, Woods DJ et al. 2015. A comprehensive transcriptomic view of renal function in the malaria vector, Anopheles gambiae. Insect Biochem. Mol. Biol. 67:47–58
    [Google Scholar]
  123. 123.
    Phillips J. 1981. Comparative physiology of insect renal function. Am. J. Physiol. Regul. Integr. Comp. Physiol. 241:R241–57
    [Google Scholar]
  124. 124.
    Phillips J, Hanrahan J, Chamberlin M, Thomson B. 1987. Mechanisms and control of reabsorption in insect hindgut. Adv. Insect Physiol. 19:329–422
    [Google Scholar]
  125. 125.
    Phillips J, Wiens C, Audsley N, Jeffs L, Bilgen T, Meredith J. 1996. Nature and control of chloride transport in insect absorptive epithelia. J. Exp. Zool. 275:292–99
    [Google Scholar]
  126. 126.
    Phillips JE. 1961. Studies on the rectal reabsorption of water and salts in the locust Scitistocerca gregaria and the blowfly Calliphora erythrocephala PhD Thesis Univ. Cambridge Cambridge, UK:
    [Google Scholar]
  127. 127.
    Phillips JE. 1964. Rectal absorption in the desert locust, Schistocerca gregaria Forskål. I. Water. J. Exp. Biol. 41:15–38
    [Google Scholar]
  128. 128.
    Phillips JE. 1964. Rectal absorption in the desert locust, Schistocerca gregaria Forskål. II. Sodium, potassium and chloride. J. Exp. Biol. 41:39–67
    [Google Scholar]
  129. 129.
    Phillips JE. 1964. Rectal absorption in the desert locust, Schistocerca gregaria Forskål. III. The nature of the excretory process. J. Exp. Biol. 41:69–80
    [Google Scholar]
  130. 130.
    Piermarini P. 2016. Renal excretory processes in mosquitoes. Adv. Insect Physiol. 51:393–433
    [Google Scholar]
  131. 131.
    Piermarini PM, Esquivel CJ, Denton JS. 2017. Malpighian tubules as novel targets for mosquito control. Int. J. Environ. Res. Public Health 14:111
    [Google Scholar]
  132. 132.
    Predel R, Wegener C, Russell WK, Tichy SE, Russell DH, Nachman RJ. 2004. Peptidomics of CNS-associated neurohemal systems of adult Drosophila melanogaster: a mass spectrometric survey of peptides from individual flies. J. Comp. Neurol. 474:379–92
    [Google Scholar]
  133. 133.
    Quinlan MC, Tublitz NJ, O'Donnell MJ. 1997. Anti-diuresis in the blood-feeding insect Rhodnius prolixus Stål: the peptide CAP2b and cyclic GMP inhibit Malpighian tubule fluid secretion. J. Exp. Biol. 200:2363–67
    [Google Scholar]
  134. 134.
    Radford JC, Davies SA, Dow JAT. 2002. Systematic G-protein-coupled receptor analysis in Drosophila melanogaster identifies a leucokinin receptor with novel roles. J. Biol. Chem. 277:38810–17
    [Google Scholar]
  135. 135.
    Ramsay JA. 1950. Osmotic regulation in mosquito larvae. J. Exp. Biol. 27:145–57
    [Google Scholar]
  136. 136.
    Ramsay JA. 1952. The excretion of sodium and potassium by the Malpighian tubules of Rhodnius. J. Exp. Biol. 29:110–26
    [Google Scholar]
  137. 137.
    Ramsay JA. 1953. Active transport of potassium by the Malpighian tubules of insects. J. Exp. Biol. 30:358–69
    [Google Scholar]
  138. 138.
    Ramsay JA. 1953. Exchanges of sodium and potassium in mosquito larvae. J. Exp. Biol. 30:79–89
    [Google Scholar]
  139. 139.
    Ramsay JA. 1954. Active transport of water by the Malpighian tubules of the stick insect, Dixippus morosus (Orthoptera, Phasmidae). J. Exp. Biol. 31:104–13
    [Google Scholar]
  140. 140.
    Ramsay JA. 1955. The excretory system of the stick insect, Dixippus morosus (Orthoptera, Phasmidae). J. Exp. Biol. 32:183–99
    [Google Scholar]
  141. 141.
    Ramsay JA. 1964. The rectal complex of the mealworm Tenebrio molitor, L. (Coleoptera, Tenebrionidae). Philos. Trans. R. Soc. B 248:279–314
    [Google Scholar]
  142. 142.
    Ramsay JA, Keynes RD. 1971. Insect rectum. Philos. Trans. R. Soc. Lond. B 262:251–60
    [Google Scholar]
  143. 143.
    Rheault MR, O'Donnell MJ. 2001. Analysis of epithelial K+ transport in Malpighian tubules of Drosophila melanogaster: evidence for spatial and temporal heterogeneity. J. Exp. Biol. 204:2289–99
    [Google Scholar]
  144. 144.
    Rosay P, Davies SA, Yu Y, Sözen MA, Kaiser K, Dow JA. 1997. Cell-type specific calcium signalling in a Drosophila epithelium. J. Cell Sci. 110:Pt 151683–92
    [Google Scholar]
  145. 145.
    Ruiz-Sanchez E, O'Donnell MJ. 2015. The insect excretory system as a target for novel pest control strategies. Curr. Opin. Insect Sci. 11:14–20
    [Google Scholar]
  146. 146.
    Saini RS. 1964. Histology and physiology of the cryptonephridial system of insects. Philos. Trans. R. Soc. Lond. B 274:203–26
    [Google Scholar]
  147. 147.
    Santos JG, Pollák E, Rexer KH, Molnár L, Wegener C. 2006. Morphology and metamorphosis of the peptidergic Va neurons and the median nerve system of the fruit fly, Drosophila melanogaster. Cell Tissue Res. 326:187–99
    [Google Scholar]
  148. 148.
    Senapati B, Tsao C-H, Juan Y-A, Chiu T-H, Wu C-L et al. 2019. A neural mechanism for deprivation state-specific expression of relevant memories in Drosophila. Nat. Neurosci. 22:2029–39
    [Google Scholar]
  149. 149.
    Sozen MA, Armstrong JD, Yang M, Kaiser K, Dow JA. 1997. Functional domains are specified to single-cell resolution in a Drosophila epithelium. PNAS 94:5207–12
    [Google Scholar]
  150. 150.
    Stork NE. 2018. How many species of insects and other terrestrial arthropods are there on Earth?. Annu. Rev. Entomol. 63:31–45
    [Google Scholar]
  151. 151.
    Sutcliffe DW. 1960. Osmotic regulation in the larvae of some euryhaline Diptera. Nature 187:331–32
    [Google Scholar]
  152. 152.
    Te Brugge VA, Miksys SM, Coast GM, Schooley DA, Orchard I. 1999. The distribution of a CRF-like diuretic peptide in the blood-feeding bug Rhodnius prolixus. J. Exp. Biol. 202:2017–27
    [Google Scholar]
  153. 153.
    Terhzaz S, Cabrero P, Robben JH, Radford JC, Hudson BD et al. 2012. Mechanism and function of Drosophila capa GPCR: a desiccation stress-responsive receptor with functional homology to human neuromedinU receptor. PLOS ONE 7:e29897
    [Google Scholar]
  154. 154.
    Terhzaz S, O'Connell FC, Pollock VP, Kean L, Davies SA et al. 1999. Isolation and characterization of a leucokinin-like peptide of Drosophila melanogaster. J. Exp. Biol. 202:3667–76
    [Google Scholar]
  155. 155.
    Terhzaz S, Teets NM, Cabrero P, Henderson L, Ritchie MG et al. 2015. Insect capa neuropeptides impact desiccation and cold tolerance. PNAS 112:2882–87
    [Google Scholar]
  156. 156.
    Thomsen E. 1952. Functional significance of the neurosecretory brain cells and the corpus cardiacum in the female blow-fly, Calliphora erythrocephala Meig. J. Exp. Biol. 29:137–72
    [Google Scholar]
  157. 157.
    Torrie LS, Radford JC, Southall TD, Kean L, Dinsmore AJ et al. 2004. Resolution of the insect ouabain paradox. PNAS 101:13689–93
    [Google Scholar]
  158. 158.
    Tublitz NJ, Allen AT, Cheung CC, Edwards KK, Kimble DP et al. 1992. Insect cardioactive peptides—regulation of hindgut activity by cardioacceleratory peptide-2 (CAP2) during wandering behavior in Manduca sexta larvae. J. Exp. Biol. 165:241–64
    [Google Scholar]
  159. 159.
    Wall B, Oschman J. 1970. Water and solute uptake by rectal pads of Periplaneta americana. Am. J. Physiol. 218:1208–15
    [Google Scholar]
  160. 160.
    Wang J, Kean L, Yang J, Allan AK, Davies SA et al. 2004. Function-informed transcriptome analysis of Drosophila renal tubule. Genome Biol 5:R69
    [Google Scholar]
  161. 161.
    Waterson MJ, Chung BY, Harvanek ZM, Ostojic I, Alcedo J, Pletcher SD. 2014. Water sensor ppk28 modulates Drosophila lifespan and physiology through AKH signaling. PNAS 111:8137–42
    [Google Scholar]
  162. 162.
    Wayland MT, Defaye A, Rocha J, Jayaram SA, Royet J et al. 2014. Spotting the differences: probing host/microbiota interactions with a dedicated software tool for the analysis of faecal outputs in Drosophila. J. Insect Physiol. 69:126–35
    [Google Scholar]
  163. 163.
    Wegener C, Reinl T, Jansch L, Predel R. 2006. Direct mass spectrometric peptide profiling and fragmentation of larval peptide hormone release sites in Drosophila melanogaster reveals tagma-specific peptide expression and differential processing. J. Neurochem. 96:1362–74
    [Google Scholar]
  164. 164.
    Wharton DR, Wharton ML, Lola J. 1965. Blood volume and water content of the male american cockroach, Periplanata americana L.—methods and influence of age and starvation. J. Insect Physiol. 11:391–404
    [Google Scholar]
  165. 165.
    Wieczorek H, Putzenlechner M, Zeiske W, Klein U. 1991. A vacuolar-type proton pump energizes K+/H+ antiport in an animal plasma membrane. J. Biol. Chem. 266:15340–47
    [Google Scholar]
  166. 166.
    Wiehart UI, Nicolson SW, Eigenheer RA, Schooley DA. 2002. Antagonistic control of fluid secretion by the Malpighian tubules of Tenebrio molitor: effects of diuretic and antidiuretic peptides and their second messengers. J. Exp. Biol. 205:493–501
    [Google Scholar]
  167. 167.
    Wigglesworth VB. 1931. The physiology of excretion in a blood-sucking insect, Rhodnius prolixus (Hemiptera, Reduviidae): I. Composition of the urine. J. Exp. Biol. 8:411–27
    [Google Scholar]
  168. 168.
    Wigglesworth VB. 1931. The physiology of excretion in a blood-sucking insect, Rhodnius prolixus (Hemiptera, Reduviidae): II. Anatomy and histology of the excretory system. J. Exp. Biol. 8:428–41
    [Google Scholar]
  169. 169.
    Wigglesworth VB. 1931. The physiology of excretion in a blood-sucking insect, Rhodnius prolixus (Hemiptera, Reduviidae): III. The mechanism of uric acid excretion. J. Exp. Biol. 8:443–51
    [Google Scholar]
  170. 170.
    Wigglesworth VB. 1932. On the function of the so-called “rectal glands” of insects. J. Cell Sci.s2–75: 131–50
    [Google Scholar]
  171. 171.
    Wigglesworth VB. 1934. Insect Physiology London: Methuen
  172. 172.
    Wigglesworth VB. 1939. The Principles of Insect Physiology London: Methuen
  173. 173.
    Wu Y, Baum M, Huang C-L, Rodan AR. 2015. Two inwardly rectifying potassium channels, Irk1 and Irk2, play redundant roles in Drosophila renal tubule function. Am. J. Physiol. Regul. Integr. Comp. Physiol. 309:R747–56
    [Google Scholar]
  174. 174.
    Wu Y, Schellinger JN, Huang C-L, Rodan AR. 2014. Hypotonicity stimulates potassium flux through the WNK-SPAK/OSR1 kinase cascade and the Ncc69 sodium-potassium-2-chloride cotransporter in the Drosophila renal tubule. J. Biol. Chem. 289:26131–42
    [Google Scholar]
  175. 175.
    Xu J, Liu Y, Li H, Tarashansky AJ, Kalicki CH et al. 2022. Transcriptional and functional motifs defining renal function revealed by single-nucleus RNA sequencing. PNAS 119:e2203179119
    [Google Scholar]
  176. 176.
    Yang Z, Huang R, Fu X, Wang G, Qi W et al. 2018. A post-ingestive amino acid sensor promotes food consumption in Drosophila. Cell Res 28:1013–25
    [Google Scholar]
  177. 177.
    Yeoh JGC, Pandit AA, Zandawala M, Nässel DR, Davies S-A, Dow JAT. 2017. DINeR: Database for Insect Neuropeptide Research. Insect Biochem. Mol. Biol. 86:9–19
    [Google Scholar]
  178. 178.
    Yuan F, Wei C. 2022. Gene expression profiles in Malpighian tubules of the vector leafhopper Psammotettix striatus (L.) revealed regional functional diversity and heterogeneity. BMC Genom. 23:67
    [Google Scholar]
  179. 179.
    Zandawala M, Marley R, Davies SA, Nässel DR. 2018. Characterization of a set of abdominal neuroendocrine cells that regulate stress physiology using colocalized diuretic peptides in Drosophila. Cell Mol. Life Sci. 75:1099–115
    [Google Scholar]
  180. 180.
    Zandawala M, Nguyen T, Balanyà Segura M, Johard HAD, Amcoff M et al. 2021. A neuroendocrine pathway modulating osmotic stress in Drosophila. PLOS Genet. 17:e1009425
    [Google Scholar]
  181. 181.
    Zandawala M, Yurgel ME, Texada MJ, Liao S, Rewitz KF et al. 2018. Modulation of Drosophila post-feeding physiology and behavior by the neuropeptide leucokinin. PLOS Genet. 14:e1007767
    [Google Scholar]
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