Eur. J. Entomol. 119: 170-182, 2022 | DOI: 10.14411/eje.2022.019

Diapause among the flesh flies (Diptera: Sarcophagidae)Ivo Hodek special issueReview

David L. DENLINGER
Departments of Entomology and Evolution, Ecology and Organismal Biology, Ohio State University, Columbus, OH 43210, USA; e-mail: denlinger.1@osu.edu

The rich diversity of information focusing on pupal diapause in the sarcophagids makes this fly family among the best-understood diapause models. This review summarizes the occurrence of pupal diapause in flesh flies from broad geographic regions of the world, as well as the apparent absence of diapause in select regions. The environmental cues used for programming diapause are discussed, as well as the requirements for breaking diapause. This taxon has been used for experiments ranging from the ecological to the molecular and offers a comprehensive overview of the diapause phenotype. A wide range of diapause attributes define the diapause phenotype of flesh flies, offering insights into such features as clock mechanisms, signaling pathways, maternal regulation, energy utilization, cell cycle regulation, metabolic depression, cyclic metabolic activity, cold tolerance, water balance, and other attributes, generating a diapause profile that offers an attractive comparison for diapause in other insect species as well as with other forms of animal dormancy.

Keywords: Pupal diapause, geographic responses, physiological attributes, molecular signaling

Received: April 1, 2022; Revised: April 28, 2022; Accepted: April 28, 2022; Published online: May 18, 2022  Show citation

ACS AIP APA ASA Harvard Chicago Chicago Notes IEEE ISO690 MLA NLM Turabian Vancouver
DENLINGER, D.L. (2022). Diapause among the flesh flies (Diptera: Sarcophagidae). EJE, 119, Article 170-182. https://doi.org/10.14411/eje.2022.019

This paper was contributed to a virtual special issue in memory of Ivo Hodek, a long-time editor of the European Journal of Entomo­logy, who died on June 11, 2021, shortly after his ninetieth birthday.

Share...
Download citation
  • BibTeX (.bib)
  • Bookends (.ris)
  • EasyBib (.ris)
  • EndNote (.enw)
  • EndNote 8 (.xml)
  • ISI WoS (.isi)
  • Medlars (.medlars)
  • Mendeley (.ris)
  • MODS (.xml)
  • Papers (.ris)
  • RefWorks (.txt)
  • RefManager (.ris)
  • RIS (.ris)
  • MS Word (.xml)
  • Zotero (.ris)
    • Open full article

    References

    1. Adedokun T.A. & Denlinger D.L. 1984: Cold-hardiness: a component of the syndrome in pupae of the flesh flies, Sarcophaga crassipalpis and S. bullata. - Physiol. Entomol. 9: 361-364. Go to original source...
    2. Adedokun T.A. & Denlinger D.L. 1985: Metabolic reserves associated with pupal diapause in the flesh fly, Sarcophaga crassipalpis. - J. Insect Physiol. 31: 229-233. Go to original source...
    3. Aldrich J.M. 1916: Sarcophaga and Allies. Thomas Say Foundation, Ent. Soc. Amer., West Lafayette, IN, 301 pp. Go to original source...
    4. Briers T. & De Loof A. 1980: The molting hormone activity in Sarcophaga bullata in relation to metamorphosis and reproduction. - Int. J. Invert. Reprod. 2: 363-372. Go to original source...
    5. Buenaventura E., Whitmore D. & Pape T. 2017: Molecular phylogeny of the hyperdiverse genus Sarcophaga (Diptera: Sarcophagidae), and the comparison between algorithms for identification of rogue taxa. - Cladistics 33: 109-133. Go to original source...
    6. Chen C., Mahar R., Merritt M.E., Denlinger D.L. & Hahn D.A. 2021: ROS and hypoxia signaling regulate arousal during insect dormancy to coordinate glucose, amino acid, and lipid metabolism. - Proc. Natl. Acad. Sci. USA 118: e2017603118, 10 pp. Go to original source...
    7. Danneels E.L., Formesyn E.M., Hahn D.A., Denlinger D.L., Cardoen D., Verleyen P., Wenseleers T., Schoofs L. & De Graaf D.C. 2013: Early changes in the pupal transcriptome of the flesh fly, Sarcophaga crassipalpis to paratization by the ectoparasitic wasp, Nasonia vitripennis. - Insect Biochem. Mol. Biol. 43: 1189-1200. Go to original source...
    8. Denlinger D.L. 1971: Embryonic determination of pupal diapause induction in the flesh fly Sarcophaga crassipalpis Macquart. - J. Insect Physiol. 17: 1815-1822. Go to original source...
    9. Denlinger D.L. 1972a: Induction and termination of pupal diapause in Sarcophaga (Diptera: Sarcophagidae). - Biol. Bull. 142: 11-24. Go to original source...
    10. Denlinger D.L. 1972b: Seasonal phenology of diapause in the flesh fly Sarcophaga bullata. - Ann. Entomol. Soc. Am. 65: 410-414. Go to original source...
    11. Denlinger D.L. 1974: Diapause potential in tropical flesh flies. - Nature 252: 223-224. Go to original source...
    12. Denlinger D.L. 1976: Preventing insect diapause with hormones and cholera toxin. - Life Sci. 19: 1485-1490. Go to original source...
    13. Denlinger D.L. 1979: Pupal diapause in tropical flesh flies: environmental and endocrine regulation, metabolic rate and genetic selection. - Biol. Bull. 156: 31-46. Go to original source...
    14. Denlinger D.L. 1981: Basis for a skewed sex ratio in diapause-destined flesh flies. - Evolution 35: 1247-1248. Go to original source...
    15. Denlinger D.L. 1991: Relationship between cold-hardiness and diapause. In Lee R.E. Jr. & Denlinger D.L. (eds): Insects at Low Temperature. Chapman and Hall, New York, pp. 174-198. Go to original source...
    16. Denlinger D.L. 2022: Insect Diapause. Cambridge University Press, Cambridge, 464 pp. Go to original source...
    17. Denlinger D.L. & Shukla M. 1984: Increased length and variability of the life cycle in tropical flesh flies (Diptera: Sarcophagidae) that lack diapause. - Ann. Entomol. Soc. Amer. 77: 46-49. Go to original source...
    18. Denlinger D.L. & Tanaka S. 1989: Cycles of juvenile hormone esterase activity during the juvenile hormone-driven cycles of oxygen consumption in pupal diapause of flesh flies. - Experientia 45: 474-476. Go to original source...
    19. Denlinger D.L. & Wingard P. 1978: Cyclic GMP breaks pupal diapause in the flesh fly Sarcophga crassipalpis. - J. Insect Physiol. 24: 715-719. Go to original source...
    20. Denlinger D.L. & ®ïárek J. 1994: Metamorphosis behavior of flies. - Annu. Rev. Entomol. 39: 243-266. Go to original source...
    21. Denlinger D.L., Willis J.H. & Fraenkel G. 1972: Rates and cycles of metabolism in diapausing Sarcophaga pupae. - J. Insect Physiol. 18: 871-882. Go to original source...
    22. Denlinger D.L., Campbell J.J. & Bradfield J.Y. 1980: Stimulatory effect of organic solvents on initiating development in diapausing pupae of the flesh fly Sarcophaga crassipalpis and the tobacco hornworm Manduca sexta. - Physiol. Entomol. 5: 7-15. Go to original source...
    23. Denlinger D.L., Shukla M. & Faustini D.L. 1984: Juvenile hormone involvement in pupal diapause in the flesh fly Sarcophaga crassipalpis: regulation of infradian cycles of O2 consumption. - J. Exp. Biol. 109: 191-199. Go to original source...
    24. Denlinger D.L., Giebultowicz J. & Adedokun T. 1988: Insect diapause: dynamics of hormone sensitivity and vulnerability to environmental stress. In Sehnal F., Zabza A. & Denlinger D.L. (eds): Endocrinological Frontiers in Physiological Insect Ecology. Wroclaw Technical University Press, Wroclaw, pp. 309-324.
    25. Denlinger D.L., Yocum G.D. & Rinehart J.P. 2012: Hormonal control of diapause. In Gilbert L.I. (ed.): Insect Endocrinology. Academic Press, San Diego, pp. 430-463. Go to original source...
    26. Fraenkel G. & Hsiao C. 1968a: Manifestation of a pupal diapause in two species of flies, Sarcophaga argyrotoma and S. bullata. - J. Insect Physiol. 14: 689-705. Go to original source...
    27. Fraenkel G. & Hsiao C. 1968b: Morphological and endocrino­logical aspects of pupal diapause in a flesh fly, Sarcophaga argyrostoma (Robineau-Desvoidy). - J. Insect Physiol. 14: 707-718. Go to original source...
    28. Giebultowicz J.M. & Denlinger D.L. 1986: Role of the brain and ring gland in regulation of pupal diapause in the flesh fly, Sarcophaga crassipalpis. - J. Insect Physiol. 32: 161-166. Go to original source...
    29. Giroux M. & Wheeler T.A. 2009: Systematics and phylogeny of the subgenus Sarcophaga (Neobellieria) (Diptera: Sarcophagidae). - Ann. Entomol. Soc. Amer. 102: 567-587. Go to original source...
    30. Gnagey A.L. & Denlinger D.L. 1984: Photoperiodic induction of pupal diapause in the flesh fly, Sarcophaga crassipalpis: embryonic sensitivity. - J. Comp. Physiol. (B) 154: 91-96. Go to original source...
    31. Goto S.G. 2009: Genetic analysis of diapause capacity and association between larval and pupal photoperiodic responses in the flesh fly Sarcophaga similis. - Physiol. Entomol. 34: 46-51. Go to original source...
    32. Goto S.G. & Denlinger D.L. 2002: Short-day and long-day expression patterns of genes involved in the flesh fly clock mechanism: period, timeless, cycle and cryptochrome. - J. Insect Physiol. 48: 803-816. Go to original source...
    33. Goto S.G., Han B. & Denlinger D.L. 2006: A nondiapausing variant of the flesh fly, Sarcophaga bullata, that shows arrhythmic adult eclosion and elevated expression of two circadian clock genes, period and timeless. - J. Insect Physiol. 52: 1213-1218. Go to original source...
    34. Hahn D.A., Ragland G.J., Shoemaker D.D. & Denlinger D.L. 2009: Gene discovery using massively parallel pyrosequencing to develop ESTs for the flesh fly Sarcophaga crassipalpis. - BMC Genomics 10: 234, 9 pp. Go to original source...
    35. Han B. & Denlinger D.L. 2009a: Length variation in a specific region of the period gene correlates with differences in pupal diapause incidence in the flesh fly, Sarcophaga bullata. - J. Insect Physiol. 55: 415-418. Go to original source...
    36. Han B. & Denlinger D.L. 2009b: Mendelian inheritance of pupal diapause in the flesh fly, Sarcophaga bullata. - J. Hered. 100: 251-255. Go to original source...
    37. Hanski I. 1987: Carrion fly community dynamics: patchiness, seasonality and coexistence. - Ecol. Entomol. 12: 257-266. Go to original source...
    38. Henrich V.C. & Denlinger D.L. 1982a: A maternal effect that eliminates pupal diapause in progeny of the flesh fly, Sarcophaga bullata. - J. Insect Physiol. 28: 881-884. Go to original source...
    39. Henrich V.C. & Denlinger D.L. 1982b: Selection for late pupariation affects diapause incidence and duration in the flesh fly, Sarcophaga bullata. - Physiol. Entomol. 7: 407-411. Go to original source...
    40. Henrich V.C. & Denlinger D.L. 1983: Genetic differences in pupal diapause incidence between two selected strains of the flesh fly. - J. Hered. 74: 371-374. Go to original source...
    41. House H.L. 1967: The decreasing occurrence of diapause in the fly Pseudosarcophaga affinis through laboratory-reared gene­rations. - Can. J. Zool. 45: 149-153. Go to original source...
    42. Joplin K.H. & Denlinger D.L. 1989: Cycles of protein synthesis during pupal diapause in the flesh fly, Sarcophaga crassipalpis. - Arch. Insect Biochem. Physiol. 12: 111-122. Go to original source...
    43. Joplin K.H., Yocum G.D. & Denlinger D.L. 1990: Diapause specific proteins expressed by the brain during pupal diapause of the flesh fly, Sarcophaga crassipalpis. - J. Insect Physiol. 36: 775-783. Go to original source...
    44. Ko¹»ál V., Závodská R. & Denlinger D.L. 2009: Clock genes period and timeless are rhythmically expressed in brains of newly-hatched, photosensitive larvae of the fly, Sarcophaga crassipalpis. - J. Insect Physiol. 55: 408-414. Go to original source...
    45. Kukal O., Denlinger D.L. & Lee R.E. Jr. 1991: Developmental and metabolic changes induced by anoxia in diapausing and nondiapausing flesh fly pupae. - J. Comp. Physiol. (B) 160: 683-389. Go to original source...
    46. Kurahashi H. & Ohtaki T. 1977: Crossing between nondiapausing and diapausing races of Sarcophaga peregrina. - Experientia 33: 186-187. Go to original source...
    47. Kurahashi H. & Ohtaki T. 1979: Induction of pupal diapause and photoperiodic sensitivity during early development of Sarcophaga peregrina larvae. - Jpn. J. Med. Sci. Biol. 32: 77-82. Go to original source...
    48. Kurahashi H. & Ohtaki T. 1989: Geographic variation in the incidence of pupal diapause in Asian and Oceanic species of the flesh fly Boettcherisca (Diptera: Sarcophagidae). - Physiol. Entomol. 14: 291-298. Go to original source...
    49. Lee R.E. Jr. & Denlinger D.L. 1985: Cold tolerance in diapausing and non-diapausing stages of the flesh fly, Sarcophaga crassipalpis. - Physiol. Entomol. 10: 309-315. Go to original source...
    50. Lee R.E. Jr, Chen C.-P., Meacham M.H. & Denlinger D.L. 1987: Ontogenetic patterns of cold-hardiness and glycerol production in Sarcophaga crassipalpis. - J. Insect Physiol. 33: 587-592. Go to original source...
    51. Li A., Rinehart J.P. & Denlinger D.L. 2009a: Neuropeptide-like precursor 4 is uniquely expressed during pupal diapause in the flesh fly. - Peptides 30: 518-521. Go to original source...
    52. Li A., Michaud M.R. & Denlinger D.L. 2009b: Rapid elevation of Inos and decreases in abundance of other proteins at pupal diapause termination in the flesh fly Sarcophaga crassipalpis. - Biochim. Biophys. Acta - Proteins and Proteomics 1794: 663-668. Go to original source...
    53. Martinson E.O, Peyton J., Yogeshwar D.K., Jennings E.C., Benoit J.B., Werren J.H. & Denlinger D.L. 2019: Genome and ontogenetic-based transcriptomic analysis of the flesh fly, Sarcophaga bullata. - G3 9: 1313-1320. Go to original source...
    54. Michaud M.R. & Denlinger D.L. 2007: Shifts in the carbohydrate, polyol, and amino acid pools during rapid cold-hardening and diapause-associated cold-hardening in flesh flies (Sarcophaga crassipalpis): a metabolomic comparison. - J. Comp. Physiol. (B) 177: 753-763. Go to original source...
    55. Miura M., Hayasaka S., Yamada T., Hayasaki Y. & Kamimura K. 2005: Ophthalmomyiasis caused by larvae of Boettcherisca peregrina. - Jpn. J. Ophthalmol. 49: 177-179. Go to original source...
    56. Moribayashi A., Kurahashi H. & Ohtaki T. 1988: Different profiles of ecdysone secretion and its metabolism between diapause- and nondiapause-destined culture of the fleshfly, Boettcherisca peregrina. - Comp. Biochem. Physiol. (A) 91: 157-164. Go to original source...
    57. Moribayashi A., Kurahashi H. & Ohtaki T. 1992: Physiological differentiation of the ring glands in mature larvae of the flesh fly, Boettcherisca peregrina, programmed for diapause or non-diapause. - J. Insect Physiol. 38: 177-183. Go to original source...
    58. Moribayashi A., Kurahashi H. & Taylor D. 2021: Emergence at lower temperatures facilitates movement of the flesh flies Parasarcophaga similis and Boettcherisca peregrina (Diptera: Sarcophagidae) into temperate and subarctic regions. - Med. Entomol. Zool. 72: 213-220. Go to original source...
    59. Monzu N. 1979: Flystrike in sheep: secondary and tertiary flies striking sheep in Western Australia. - J. Dept. Agric., Western Australia 20: 48-51.
    60. Muirhead K.A. & Perry K.D. 2021: Biocontrol of invasive conical snails by the parasitoid fly Sarcophaga villeneuveana in South Australia 20 years after release. - Insects 12: 865. Go to original source...
    61. Mukai A., Yamaguchi K. & Goto S.G. 2021: Urban warming and artificial light alter dormancy in the flesh fly. - Roy. Soc. Open Sci. 8: 210866. Go to original source...
    62. Pape T. 1996: Catalogue of the Sarcophagidae of the world (Insecta: Diptera). - Mem. Entomol. Int. 8: 1-558.
    63. Pavlides S.C., Pavlides S.A. & Tammariello S.P. 2011: Proteomic and phosphoproteomic profiling during diapause entrance in the flesh fly, Sarcophaga crassipalpis. - J. Insect Physiol. 57: 635-644. Go to original source...
    64. Pengelley E.T. & Fisher K.C. 1961: Rhythmical arousal from hibernation in the golden-manteled ground squirrel, Citellus lateralis tescorum. - Can. J. Zool. 39: 105-120. Go to original source...
    65. Ragland G.J., Denlinger D.L. & Hahn D.A. 2010: Mechanisms of suspended animation are revealed by transcript profiling of diapause in the flesh fly. - Proc. Nat'l. Acad. Sci., USA 107: 14909-14914. Go to original source...
    66. Reynolds J.A. 2017: Epigenetic influences on diapause. - Adv. Insect Physiol. 53: 115-144. Go to original source...
    67. Reynolds J.A., Clark J., Diakoff S.J. & Denlinger D.L. 2013: Transcriptional evidence for small RNA regulation of pupal diapause in the flesh fly, Sarcophaga bullata. - Insect Biochem. Mol. Biol. 43: 982-989. Go to original source...
    68. Reynolds J.A., Bautista-Jimenez R. & Denlinger D.L. 2016: Changes in histone acetylation as potential mediators of pupal diapause in the flesh fly, Sarcophaga bullata. - Insect Biochem. Mol. Biol. 76: 29-37. Go to original source...
    69. Reynolds J.A., Peyton J.T. & Denlinger D.L. 2017: Changes in microRNA abundance may regulate diapause in the flesh fly, Sarcophaga bullata. - Insect Biochem. Mol. Biol. 84: 1-14. Go to original source...
    70. Richards D.S. & Saunders D.S. 1987: Prothoracic gland function in diapause and non-diapause Sarcophaga argyrostoma and Calliphora vicina. - J. Insect Physiol. 33: 385-392. Go to original source...
    71. Rinehart J.P., Diakoff S.J. & Denlinger D.L. 2003: Sarcotoxin II from the flesh fly Sarcophaga crassipalpis: a comparison of transcript expression in diapausing and nondiapausing pupae. - Eur. J. Entomol. 100: 251-254. Go to original source...
    72. Rinehart J.P., Li A., Yocum G.D., Robich R.M., Hayward S.A.L. & Denlinger D.L. 2007: Up-regulation of heat shock proteins is essential for cold survival during insect diapause. - Proc. Natl. Acad. Sci. USA 104: 11130-11137. Go to original source...
    73. Rinehart J.P., Robich R.M. & Denlinger D.L. 2010: Isolation of diapause-regulated genes from the flesh fly, Sarcophaga crassipalpis by suppressive subtractive hybridization. - J. Insect Physiol. 56: 603-609. Go to original source...
    74. Rivers D.B. & Denlinger D.L.1995: Fecundity and development of the ectoparasitic wasp Nasonia vitripennis are dependent on host quality. - Entomol. Exp. Appl. 76: 15-24. Go to original source...
    75. Roberts B. & Warren M.A. 1975: Diapause in the Australian flesh fly Tricholioproctia impatiens (Diptera: Sarcophagidae). - Aust. J. Zool. 23: 563-567. Go to original source...
    76. Rockey S.J. & Denlinger D.L. 1983: Deuterium oxide alters pupal diapause response in the flesh fly, Sarcophaga crassipalpis. - Physiol. Entomol. 8: 445-449. Go to original source...
    77. Rockey S.J. & Denlinger D.L. 1986: Influence of maternal age on incidence of pupal diapause in the flesh fly, Sarcophaga bullata. - Physiol. Entomol. 11: 199-203. Go to original source...
    78. Rockey S.J., Miller B.B. & Denlinger D.L. 1989: A diapause maternal effect in the flesh fly, Sarcophaga bullata: transfer of information from mother to progeny. - J. Insect Physiol. 35: 553-558. Go to original source...
    79. Rockey S.J., Yoder J.A. & Denlinger D.L. 1991: Reproductive and developmental consequences of a diapause maternal effect in the flesh fly, Sarcophaga bullata. - Physiol. Entomol. 16: 477-483. Go to original source...
    80. Roubaud E. 1922: Etudes sur le sommeil d'hiver pré-imaginal des muscides. - Biol. Bull. Fr. Belg. 56: 455-544.
    81. Saunders D.S. 1971: The temperature-compensated photoperio­dic clock 'programming' development and pupal diapause in the flesh fly, Sarcophaga argyrostoma. - J. Insect Physiol. 17: 801-812. Go to original source...
    82. Saunders D.S. 2002: Insect Clocks, 3rd ed. Elsevier, Amsterdam, 576 pp.
    83. Saunders D.S. 2020: Dormancy, diapause and the role of the circadian system in insect photoperiodism. - Annu. Rev. Entomol. 65: 373-389. Go to original source...
    84. Schneiderman H.A. & Horwitz J. 1958: The induction and termination of facultative diapause in the chalcid wasps Mormoniella vitripennis (Walker) and Tritneptis klugii (Ratzenburg). - J. Exp. Biol. 35: 520-551. Go to original source...
    85. Schneiderman H.A. & Williams C.M. 1953: The physiology of insect diapause. VII. The respiratory metabolism of the cecropia silkworm during diapause and development. - Biol. Bull. 105: 320-334. Go to original source...
    86. Short C.A., Meuti M.E., Zhang Q. & Denlinger D.L. 2016: Entrainment of eclosion and preliminary ontogeny of circadian clock gene expression in the flesh fly, Sarcophaga crassipalpis. - J. Insect Physiol. 93-94: 28-35. Go to original source...
    87. Sláma K. & Denlinger D.L. 1992: Infradian cycles of oxygen consumption in diapausing pupae of the flesh fly, Sarcophaga crassipalpis, monitored by a scanning microrespirographic method. - Arch. Insect Biochem. Physiol. 20: 135-143. Go to original source...
    88. Sláma K. & Denlinger D.L. 2013: Transitions in the heartbeat pattern during pupal diapause and adult development in the flesh fly, Sarcophaga crassipalpis. - J. Insect Physiol. 59: 767-780. Go to original source...
    89. Solar Cruz M.D., Vega Robles M.C. & Thomas G. 1996: In vivo rearing and development of Wohlfahrtia magnifica (Diptera: Sarcophagidae). - J. Med. Entomol. 33: 586-591. Go to original source...
    90. Szpila K., Madra A., Jarmusz M. & Matuszewski S. 2015: Flesh flies (Diptera: Sarcophagidae) colonizing large carcasses in Central Europe. - Parasitol. Res. 114: 2341-2348. Go to original source...
    91. Tammariello S.P. & Denlinger D.L. 1998: G0/G1 cell cycle arrest in the brain of Sarcophaga crassipalpis during pupal diapause and the expression of the cell cycle regulator proliferating cell nuclear antigen. - Insect Biochem. Mol. Biol. 28: 83-89. Go to original source...
    92. Tanaka S., Wolda H. & Denlinger D.L. 1987: Seasonality and its physiological regulation in three neotropical insect taxa from Barro Colorado Island, Panama. - Insect Sci. Appl. 8: 507-514. Go to original source...
    93. Ternovoy V.I. 1978: A study of diapause in Wohlfahrtia magnifica Schin. (Diptera: Sarcophagidae). - Rev. Entomol. USSR 57: 481-487.
    94. Verleyen P., Huybrechts J., Sas F., Clynen E., Baggerman G., De Loof A. & Schoofs L. 2004: Neuropeptidomics of the grey flesh fly, Neobellieria bullata. - Biochem. Biophys. Res. Com. 316: 763-770. Go to original source...
    95. Vinogradova E.B. 1976: Embryonic photoperiodic sensitivity in two species of fleshflies, Parasarcophaga similis and Boett­cherisca septentrionalis. - J. Insect Physiol. 22: 819-822. Go to original source...
    96. Walker G.P. & Denlinger D.L. 1980: Juvenile hormone and moulting hormone titers in diapause and nondiapause destined flesh flies. - J. Insect Physiol. 26: 661-664. Go to original source...
    97. Wasserman S.L. & Itagaki H. 2003: The olfactory responses of the antenna and maxillary palp of the fleshfly, Neobellieria bullata (Diptera: Sarcophagidae), and their sensitivity to blockage of nitric oxide synthase. - J. Insect Physiol. 49: 271-280. Go to original source...
    98. Webb M.-L.Z. & Denlinger D.L.1997: Deuterium oxide prevents expression of a diapause maternal effect in the flesh fly, Sarcophaga bullata, and alters development and fecundity. - Eur. J. Entomol. 94: 177-182.
    99. Webb M.-L.Z. & Denlinger D.L. 1998: GABA and picrotoxin alter expression of a maternal effect that influences pupal diapause in the flesh fly, Sarcophga bullata. - Physiol. Entomol. 23: 184-191. Go to original source...
    100. Werren J.H., Richards S., Desjardins C.A., Niehuis O., Gadau J., Colbourne J.K. et al. 2010: Functional and evolutionary insights from the genomes of three parasitoid Nasonia species. - Science 327: 343-348. Go to original source...
    101. Whitten J.M. 1969: Coordinated development in the foot pad of the fly Sarcophaga bullata during metamorphosis: changing puffing patterns of the giant cell chromosomes. - Chromosoma 26: 215-244. Go to original source...
    102. Yamaguchi K. & Goto S.G. 2019: Distinct physiological mechanisms induce latitudinal and sexual differences in the photoperiodic induction of diapause in a fly. - J. Biol. Rhyth. 34: 293-306. Go to original source...
    103. Yoder J.A. & Denlinger D.L. 1991: Water balance in flesh fly pupae and water vapor absorption associated with diapause. - J. Exp. Biol. 157: 273-286. Go to original source...
    104. Yoder J.A., Denlinger D.L. Dennis M.W. & Kolattukudy P.E. 1992: Enhancement of diapausing flesh fly puparia with additional hydrocarbons and evidence for alkane biosynthesis by a decarbonylation mechanism. - Insect Biochem. Mol. Biol. 22: 237-243. Go to original source...
    105. ®ïárek J. 1985: Regulation of pupariation in flies. In Kerkut G.A. & Gilbert L.I. (eds): Comprehensive Insect Physiology Biochemistry and Pharmacology, Vol. 8. Pergamon Press, Oxford, pp. 301-333. Go to original source...
    106. ®ïárek J. & Denlinger D.L. 1975: Action of ecdysoids, juvenoids, and non-hormonal agents on termination of pupal diapause in the flesh fly. - J. Insect Physiol. 21: 1193-1202. Go to original source...

    This is an open access article distributed under the terms of the Creative Commons Attribution 4.0 International License (CC BY 4.0), which permits use, distribution, and reproduction in any medium, provided the original publication is properly cited. No use, distribution or reproduction is permitted which does not comply with these terms.


    Return to the content