Tsetse flies ( spp.), vectors of African trypanosomes, are distinguished by their specialized reproductive biology, defined by adenotrophic viviparity (maternal nourishment of progeny by glandular secretions followed by live birth). This trait has evolved infrequently among insects and requires unique reproductive mechanisms. A key event in reproduction involves the transition between periods of lactation and nonlactation (dry periods). Increased lipolysis, nutrient transfer to the milk gland, and milk-specific protein production characterize lactation, which terminates at the birth of the progeny and is followed by a period of involution. The dry stage coincides with embryogenesis of the progeny, during which lipid reserves accumulate in preparation for the next round of lactation. The obligate bacterial symbiont is critical to tsetse reproduction and likely provides B vitamins required for metabolic processes underlying lactation and/or progeny development. Here we describe findings that utilized transcriptomics, physiological assays, and RNA interference–based functional analysis to understand different components of adenotrophic viviparity in tsetse flies.


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Literature Cited

  1. Adams TS. 1.  1974. The role of juvenile hormone in housefly ovarian follicle morphogenesis. J. Insect Physiol. 20:263–76 [Google Scholar]
  2. Adams TS, Reinecke JP. 2.  1979. The reproductive physiology of the screwworm, Cochliomyia hominivorax (Diptera: Calliphoridae). I. Oogenesis. J. Med. Entomol. 15:472–83 [Google Scholar]
  3. Akman L, Yamashita A, Watanabe H, Oshima K, Shiba T. 3.  et al. 2002. Genome sequence of the endocellular obligate symbiont of tsetse flies, Wigglesworthia glossinidia. Nat. Genet. 32:402–7Provides the first genome sequence for Wigglesworthia. [Google Scholar]
  4. Attardo GM, Benoit JB, Michalkova V, Patrick KR, Krause TB, Aksoy S. 4.  2014. The homeodomain protein ladybird late regulates synthesis of milk proteins during pregnancy in the tsetse fly (Glossina morsitans). PLOS Negl. Trop. Dis. 10:e2645 [Google Scholar]
  5. Attardo GM, Benoit JB, Michalkova V, Yang G, Roller L. 5.  et al. 2012. Analysis of lipolysis underlying lactation in the tsetse fly, Glossina morsitans. Insect Biochem. Mol. Biol. 42:360–70 [Google Scholar]
  6. Attardo GM, Guz N, Strickler-Dinglasan P, Aksoy S. 6.  2006. Molecular aspects of viviparous reproductive biology of the tsetse fly (Glossina morsitans morsitans): regulation of yolk and milk gland protein synthesis. J. Insect Physiol. 52:1128–36Conducts the first in-depth molecular analyses of tsetse milk proteins. [Google Scholar]
  7. Attardo GM, Hansen IA, Raikhel AS. 7.  2005. Nutritional regulation of vitellogenesis in mosquitoes: implications for anautogeny. Insect Biochem. Mol. Biol. 35:661–75 [Google Scholar]
  8. Attardo GM, Lohs C, Heddi A, Alam UH, Yildirim S, Aksoy S. 8.  2008. Analysis of milk gland structure and function in Glossina morsitans: milk protein production, symbiont populations and fecundity. J. Insect Physiol. 54:1236–42 [Google Scholar]
  9. Balmand S, Lohs C, Aksoy S, Heddi A. 9.  2013. Tissue distribution and transmission routes for the tsetse fly endosymbionts. J. Invertebr. Pathol. 112:S116–22 [Google Scholar]
  10. Baumann A, Barry J, Wang S, Fujiwara Y, Wilson TG. 10.  2010. Paralogous genes involved in juvenile hormone action in Drosophila melanogaster. Genetics 185:1327–36 [Google Scholar]
  11. Baumann A, Benoit JB, Michalkova V, Mireji PO, Attardo GM. 11.  et al. 2012. Juvenile hormone and insulin signaling pathways regulate lipid levels during lactation and dry periods of tsetse fly pregnancy. Mol. Cell. Endocrinol. 372:30–41 [Google Scholar]
  12. Benoit JB, Attardo GM, Michalkova V, Bohova J, Zhang Q. 12.  et al. 2014. A novel highly divergent protein family from a viviparous insect identified by RNA-seq analysis: a potential target for tsetse fly-specific abortifacients. PLOS Genet. 10:e1003874Performs a comprehensive transcriptome analysis to compare dry and lactating periods during tsetse pregnancy. [Google Scholar]
  13. Benoit JB, Attardo GM, Michalkova V, Takac P, Bohova J, Aksoy S. 13.  2012. Sphingomyelinase activity in mother's milk is essential for juvenile development: a case from lactating tsetse flies. Biol. Reprod. 87:1–10 [Google Scholar]
  14. Benoit JB, Hansen IA, Attardo GM, Michalkova V, Mireji PO. 14.  et al. 2014. Aquaporins are critical for provision of water for lactation and progeny hydration to maintain tsetse fly reproductive success. PLOS Negl. Trop. Dis. 8:e2517 [Google Scholar]
  15. Benoit JB, Yang G, Krause TB, Patrick KR, Aksoy S, Attardo GM. 15.  2011. Lipophorin acts as a shuttle of lipids to the milk gland during tsetse fly pregnancy. J. Insect Physiol. 57:1553–61 [Google Scholar]
  16. Bermingham J, Wilkinson TL. 16.  2009. Embryo nutrition in parthenogenetic viviparous aphids. Physiol. Entomol. 34:103–9 [Google Scholar]
  17. Blackburn DG. 17.  1999. Viviparity and oviparity: evolution and reproductive strategies. Encyclopedia of Reproduction TE Knobil 4994–1003 London: Academic [Google Scholar]
  18. Borovsky D, Song Q, Ma MC, Carlson DA. 18.  1994. Biosynthesis, secretion, and immunocytochemistry of trypsin modulating oostatic factor of Aedes aegypti. Arch. Insect Biochem. Physiol. 27:27–38 [Google Scholar]
  19. Bownes M. 19.  1979. Three genes for three yolk proteins in Drosophila melanogaster. FEBS Lett. 100:95–98 [Google Scholar]
  20. Briers T, Huybrechts R. 20.  1984. Control of vitellogenin synthesis by ecdysteroids in Sarcophaga bullata. Insect Biochem. 14:121–26 [Google Scholar]
  21. Brown MR, Clark KD, Gulia M, Zhao Z, Garczynski SF. 21.  et al. 2008. An insulin-like peptide regulates egg maturation and metabolism in the mosquito Aedes aegypti. Proc. Natl. Acad. Sci. USA 105:5716–21 [Google Scholar]
  22. Brun R, Schumacher R, Schmid C, Kunz C, Burri C. 22.  2001. The phenomenon of treatment failures in human African trypanosomiasis. Trop. Med. Int. Health 6:906–14 [Google Scholar]
  23. Budd LT. 23.  1999. DFID-Funded Tsetse and Trypanosome Research and Development Since 1980 2 Economic Analysis London: Dep. Int. Dev. [Google Scholar]
  24. Bursell E. 24.  1977. Synthesis of proline by the fat body of the tsetse fly (Glossina morsitans). Metabolic pathways. Insect Biochem. 7:427–34 [Google Scholar]
  25. Bursell E. 25.  1981. The role of proline in energy metabolism. Energy Metabolism in Insects RGH Downer 135–54 New York: Springer [Google Scholar]
  26. Buxton P. 26.  1955. The Natural History of Tsetse Flies London: H.K. Lewis & Co. [Google Scholar]
  27. Chaudhury MF, Dhadialla TS. 27.  1976. Evidence of hormonal control of ovulation in tsetse flies. Nature 260:243–44 [Google Scholar]
  28. Chaudhury MFB, Dhadialla TS, Kunyiha RW. 28.  1981. Evidence of neuroendocrine relationships between mating and ovulation in the tsetse fly, Glossina morsitans morsitans. Insect Sci. Appl. 1:161–66 [Google Scholar]
  29. Chen AC, Kim HR, Mayer RT, Norman JO. 29.  1987. Vitellogenesis in the stable fly, Stomoxys calcitrans. Comp. Biochem. Physiol. B 88:897–903 [Google Scholar]
  30. Chen X, Li S, Aksoy S. 30.  1999. Concordant evolution of a symbiont with its host insect species: molecular phylogeny of genus Glossina and its bacteriome-associated endosymbiont, Wigglesworthia glossinidia. J. Mol. Evol. 48:49–58 [Google Scholar]
  31. Cmelik SHW, Bursell E, Slack E. 31.  1969. Composition of the gut contents of third-instar tsetse larvae (Glossina morsitans Westwood). Comp. Biochem. Physiol. 29:447–53 [Google Scholar]
  32. Davis S, Aksoy S, Galvani A. 32.  2011. A global sensitivity analysis for African sleeping sickness. Parasitology 138:516–26 [Google Scholar]
  33. De Loof A, Bylemans D, Schoofs L, Janssen I, Spittaels K. 33.  et al. 1995. Folliculostatins, gonadotropins and a model for control of growth in the grey fleshfly, Neobellieria (Sarcophaga) bullata. Insect Biochem. Mol. Biol. 25:661–67 [Google Scholar]
  34. Denlinger DL. 34.  1975. Insect hormones as tsetse abortifacients. Nature 253:347–48 [Google Scholar]
  35. Denlinger DL. 35.  1983. Who controls the rhythm of tsetse parturition: mother or larva?. Bull. Entomol. Res. 8:25–28 [Google Scholar]
  36. Denlinger DL, Chaudhury MF, Dhadialla TS. 36.  1978. Cyclic AMP is a likely mediator of ovulation in the tsetse fly. Experientia 34:1296–97 [Google Scholar]
  37. Denlinger DL, Ma W-C. 37.  1974. Dynamics of the pregnancy cycle in the tsetse Glossina morsitans. J. Insect Physiol. 20:1015–19, 1021–26Describes the changes in the larval size and milk gland size during the course of pregnancy. [Google Scholar]
  38. Denlinger DL, Saini RK, Chaudhury MFB. 38.  1983. Parturition in the tsetse fly Glossina morsitans: pattern of activity, sound production and evidence for control by the mother's brain. J. Insect Physiol. 29:715–21 [Google Scholar]
  39. Denlinger DL, Ždárek J. 39.  1996. A hormone from the uterus of the tsetse fly, Glossina morsitans, stimulates parturition and abortion. J. Insect Physiol. 43:135–42 [Google Scholar]
  40. Dubrovsky EB, Dubrovskaya VA, Bernardo T, Otte V, DiFilippo R, Bryan H. 40.  2011. The Drosophila FTZ-F1 nuclear receptor mediates juvenile hormone activation of E75A gene expression through an intracellular pathway. J. Biol. Chem. 286:33689–700 [Google Scholar]
  41. Ejezie GC, Davey KG. 41.  1974. Changes in the neurosecretory cells, corpus cardiacum and corpus allatum during pregnancy in Glossina austeni Newst. (Diptera, Glossinidae). Bull. Entomol. Res. 64:247–56 [Google Scholar]
  42. Ejezie GC, Davey KG. 42.  1976. Some effects of allatectomy in female tsetse, Glossina austeni. J. Insect Physiol. 22:1743–49 [Google Scholar]
  43. Fallon AM, Hagedorn HH, Wyatt GR, Laufer H. 43.  1974. Activation of vitellogenin synthesis in the mosquito Aedes aegypti by ecdysone. J. Insect Physiol. 20:1815–23 [Google Scholar]
  44. Farris SM, Rio RV. 44.  2012. Brain development in an insect with extensive maternal care, the tsetse fly Glossina morsitans (Diptera: Glossinidae). Front. Behav. Neurosci. Conf. Abstr.: Tenth Int. Congr. Neuroethol. doi: 10.3389/conf.fnbeh.2012.27.00397 [Google Scholar]
  45. Foster WA. 45.  1974. Surgical inhibition of ovulation and gestation in the tsetse fly Glossina austeni Newst. (Dipt., Glossinidae). Bull. Entomol. Res. 63:483–93 [Google Scholar]
  46. Fourney RM, Pratt GF, Harnish DG, Wyatt GR, White BN. 46.  1982. Structure and synthesis of vitellogenin and vitellin from Calliphora erythrocephala. Insect Biochem. 12:311–21 [Google Scholar]
  47. French A, Hoopingarner R. 47.  1965. Gametogenesis in the house fly, Musca domestica. Ann. Entomol. Soc. Am. 58:650–57 [Google Scholar]
  48. Garabedian MJ, Hung MC, Wensink PC. 48.  1985. Independent control elements that determine yolk protein gene expression in alternative Drosophila tissues. Proc. Natl. Acad. Sci. USA 82:1396–400 [Google Scholar]
  49. Guimaraes JH. 49.  1977. A systematic revision of the Mesembrinellidae, stat. nov. (Diptera, Cyclorrhapha). Arq. Zool. 29:1–109 [Google Scholar]
  50. Gulia-Nuss M, Robertson AE, Brown MR, Strand MR. 50.  2011. Insulin-like peptides and the target of rapamycin pathway coordinately regulate blood digestion and egg maturation in the mosquito Aedes aegypti. PLOS ONE 6:e20401 [Google Scholar]
  51. Guz N, Attardo GM, Wu Y, Aksoy S. 51.  2007. Molecular aspects of transferrin expression in the tsetse fly (Glossina morsitans morsitans). J. Insect Physiol. 53:715–23 [Google Scholar]
  52. Hagan HR. 52.  1951. Embryology of Viviparous Insects New York: Ronald Press [Google Scholar]
  53. Hagedorn HH, O'Connor JD, Fuchs MS, Sage B, Schlaeger DA, Bohm MK. 53.  1975. The ovary as a source of alpha-ecdysone in an adult mosquito. Proc. Natl. Acad. Sci. USA 72:3255–59 [Google Scholar]
  54. Hagedorn HH, Shapiro JP, Hanaoka K. 54.  1979. Ovarian ecdysone secretion is controlled by a brain hormone in an adult mosquito. Nature 282:92–94 [Google Scholar]
  55. Hansen IA, Attardo GM, Park JH, Peng Q, Raikhel AS. 55.  2004. Target of rapamycin-mediated amino acid signaling in mosquito anautogeny. Proc. Natl. Acad. Sci. USA 101:10626–31 [Google Scholar]
  56. Hecker H, Moloo SK. 56.  1983. Quantitative morphological changes of the uterine gland cells in relation to physiological events during a pregnancy cycle in Glossina morsitans morsitans. J. Insect Physiol. 29:651–58 [Google Scholar]
  57. Hens K, Lemey P, Macours N, Francis C, Huybrechts R. 57.  2004. Cyclorraphan yolk proteins and lepidopteran minor yolk proteins originate from two unrelated lipase families. Insect Mol. Biol. 13:615–23 [Google Scholar]
  58. Hens K, Macours N, Claeys I, Francis C, Huybrechts R. 58.  2004. Cloning and expression of the yolk protein of the tsetse fly Glossina morsitans morsitans. Insect Biochem. Mol. Biol. 34:1281–87 [Google Scholar]
  59. Horn D, McCulloch R. 59.  2010. Molecular mechanisms underlying the control of antigenic variation in African trypanosomes. Curr. Opin. Microbiol. 13:700–5 [Google Scholar]
  60. Houseman JG, Morrison PE. 60.  1986. Absence of female-specific protein in the hemolymph of stable fly Stomoxys calcitrans (L.) (Diptera: Muscidae). Arch. Insect Biochem. Physiol. 3:205–13 [Google Scholar]
  61. Hu CY, Rio RVM, Medlock J, Haines LR, Nayduch D. 61.  et al. 2008. Infections with immunogenic trypanosomes reduce tsetse reproductive fitness: potential impact of different parasite strains on vector population structure. PLOS Negl. Trop. Dis. 2:e192 [Google Scholar]
  62. Huebner E, Tobe SS, Davey KG. 62.  1975. Structural and functional dynamics of oogenesis in Glossina austeni: general features, previtellogenesis and nurse cells. Tissue Cell 7:297–317 [Google Scholar]
  63. 63. International Glossina Genome Initiative 2014. Genome sequence of the tsetse fly (Glossina morsitans): vector of African trypanosomiasis. Science 344:380–86Provides the genome sequence for Glossina morsitans. [Google Scholar]
  64. Isaac PG, Bownes M. 64.  1982. Ovarian and fat-body vitellogenin synthesis in Drosophila melanogaster. Eur. J. Biochem. 123:527–34 [Google Scholar]
  65. Jackson AP, Berry A, Aslett M, Allison HC, Burton P. 65.  et al. 2012. Antigenic diversity is generated by distinct evolutionary mechanisms in African trypanosome species. Proc. Natl. Acad. Sci. USA 109:3416–21 [Google Scholar]
  66. Jannin J, Cattand P. 66.  2004. Treatment and control of human African trypanosomiasis. Curr. Opin. Infect. Dis. 17:565–71 [Google Scholar]
  67. Jensen PV, Hansen BL, Hansen GN, Thomsen E. 67.  1981. Vitellogenin and vitellin from the blowfly Calliphora vicina: occurrence, purification and antigenic characterization. Insect Biochem. 11:129–35 [Google Scholar]
  68. Joja LL, Okoli UA. 68.  2001. Trapping the vector: community action to curb sleeping sickness in southern Sudan. Am. J. Public Health 91:1583–85 [Google Scholar]
  69. Jordan AM. 69.  1986. Trypanosomiasis Control and African Rural Development London: Longman [Google Scholar]
  70. Kabayo JP. 70.  2002. Aiming to eliminate tsetse from Africa. Trends Parasitol. 18:473–75 [Google Scholar]
  71. Kgori PM, Modo S, Torr SJ. 71.  2006. The use of aerial spraying to eliminate tsetse from the Okavango Delta of Botswana. Acta Trop. 99:184–99 [Google Scholar]
  72. King RC. 72.  1970. Ovarian Development in Drosophila melanogaster New York: Academic [Google Scholar]
  73. King RC, Aggarwal SK, Aggarwal U. 73.  1968. The development of the female Drosophila reproductive system. J. Morphol. 124:143–66 [Google Scholar]
  74. Krafsur ES. 74.  2009. Tsetse flies: genetics, evolution, and role as vectors. Infect. Genet. Evol. 9:124–41 [Google Scholar]
  75. Langley PA, Bursell E. 75.  1980. Role of fat body and uterine gland in milk synthesis by adult female Glossina morsitans. Insect Biochem. 10:11–17 [Google Scholar]
  76. Langley PA, Bursell E, Kabayo J, Pimley RW, Trewen MA, Marshall J. 76.  1981. Hemolymph lipid transport from fat body to uterine gland in pregnant females of Glossina morsitans. Insect Biochem. 11:225–31Conducts critical research on nutrient metabolism during tsetse fly lactation (see also References 78–83). [Google Scholar]
  77. Langley PA, Clutton-Brock TH. 77.  1998. Does reproductive investment change with age in tsetse flies, Glossina morsitans morsitans (Diptera: Glossinidae)?. Funct. Ecol. 12:866–70 [Google Scholar]
  78. Langley PA, Felton T, Oouchi H. 78.  1988. Juvenile hormone mimics as effective sterilants for the tsetse fly Glossina morsitans morsitans. Med. Vet. Entomol. 2:29–35 [Google Scholar]
  79. Langley PA, Pimley RW. 79.  1974. Utilization of U-14C amino acids or U-14C protein by adult Glossina morsitans during in utero development of larva. J. Insect Physiol. 20:2157–70 [Google Scholar]
  80. Langley PA, Pimley RW. 80.  1975. Quantitative aspects of reproduction and larval nutrition in Glossina morsitans morsitans Westw. (Diptera: Glossinidae) fed in vitro. Bull. Entomol. Res. 65:129–42 [Google Scholar]
  81. Langley PA, Pimley RW. 81.  1979. Influence of diet on synthesis and utilization of lipids for reproduction by the tsetse fly Glossina morsitans. J. Insect Physiol. 25:79–86 [Google Scholar]
  82. Langley PA, Pimley RW. 82.  1979. Storage and mobilisation of nutriment for uterine milk synthesis by Glossina morsitans. J. Insect Physiol. 25:193–97 [Google Scholar]
  83. Langley PA, Pimley RW. 83.  1986. A role of juvenile hormone and the effects of so-called anti-juvenile hormones in Glossina morsitans. J. Insect Physiol. 32:727–31 [Google Scholar]
  84. Lea AO. 84.  1963. Some relationships between environment, corpora allata, and egg maturation in aedine mosquitoes. J. Insect Physiol. 9:793–809 [Google Scholar]
  85. Lenoble BJ, Denlinger DL. 85.  1982. The milk gland of the sheep ked, Melophagus ovinus: a comparison with Glossina. J. Insect Physiol. 28:165–72 [Google Scholar]
  86. Ma WC, Denlinger DL, Jarlfors U, Smith DS. 86.  1975. Structural modulations in the tsetse fly milk gland during a pregnancy cycle. Tissue Cell 7:319–30 [Google Scholar]
  87. Martinez A, Bownes M. 87.  1994. The sequence and expression pattern of the Calliphora erythrocephala yolk protein A and B genes. J. Mol. Evol. 38:336–51 [Google Scholar]
  88. McCabe CT, Bursell E. 88.  1975. Interrelationships between amino acid and lipid metabolism in the tsetse fly, Glossina morsitans. Insect Biochem. 5:781–89 [Google Scholar]
  89. McCabe CT, Bursell E. 89.  1975. The metabolism of digestive products in the tsetse fly, Glossina morsitans. Insect Biochem. 5:769–79 [Google Scholar]
  90. Meier R, Kotrba M, Ferrar P. 90.  1999. Ovoviviparity and viviparity in the Diptera. Biol. Rev. Camb. Philos. Soc. 74:199–258Reviews fly reproductive mechanisms. [Google Scholar]
  91. Michalkova V, Benoit JB, Attardo GM, Medlock J, Aksoy S. 91.  2014. Amelioration of reproduction-associated oxidative stress in a viviparous insect is critical to prevent reproductive senescence. PLOS ONE 9:e87554 [Google Scholar]
  92. Michalkova V, Benoit JB, Weiss BL, Attardo GM, Aksoy S. 92.  2014. Obligate symbiont-generated vitamin B6 is critical to maintain proline homeostasis and fecundity in tsetse flies. Appl. Environ. Microbiol. 80:5844–53 [Google Scholar]
  93. Minakuchi C, Zhou X, Riddiford LM. 93.  2008. Krüppel homolog 1 (Kr-h1) mediates juvenile hormone action during metamorphosis of Drosophila melanogaster. Mech. Dev. 125:91–105 [Google Scholar]
  94. Moloo SK. 94.  1971. Oocyte differentiation and vitellogenesis in Glossina morsitans Westw. Acta Trop. 28:334–40 [Google Scholar]
  95. Moloo SK. 95.  1976. Aspects of the nutrition of adult female Glossina morsitans during pregnancy. J. Insect Physiol. 22:563–67 [Google Scholar]
  96. Moloo SK. 96.  1976. Storage of nutriments by adult female Glossina morsitans and their transfer to the intra-uterine larva. J. Insect Physiol. 22:111–15 [Google Scholar]
  97. Nogge G. 97.  1976. Sterility in tsetse flies (Glossina morsitans Westwood) caused by loss of symbionts. Experientia 32:995–96 [Google Scholar]
  98. Nogge G. 98.  1981. Significance of symbionts for the maintenance of an optimal nutritional state for successful reproduction in hematophagous arthropods. Parasitology 82:101–4 [Google Scholar]
  99. Nok AJ. 99.  2003. Arsenicals (melarsoprol), pentamidine and suramin in the treatment of human African trypanosomiasis. Parasitol. Res. 90:71–79 [Google Scholar]
  100. Nyberg L, Farooqi A, Blackberg L, Duan RD, Nilsson A, Hernell O. 100.  1998. Digestion of ceramide by human milk bile salt-stimulated lipase. J. Pediatr. Gastroenterol. Nutr. 27:560–67 [Google Scholar]
  101. Ochanda JO, Osir EO, Nguu EK, Olembo NK. 101.  1991. Lipophorin from the tsetse fly, Glossina morsitans morsitans. Comp. Biochem. Physiol. B 99:811–14 [Google Scholar]
  102. Osir EO, Kotengo M, Chaudhury MFB, Otieno LH. 102.  1991. Structural studies on the major milk gland protein of the tsetse fly, Glossina morsitans morsitans. Comp. Biochem. Physiol. B 99:803–9Discovers the partial amino acid sequence for the first identified tsetse milk protein. [Google Scholar]
  103. Pais R, Lohs C, Wu Y, Wang J, Aksoy S. 103.  2008. The obligate mutualist Wigglesworthia glossinidia influences reproduction, digestion, and immunity processes of its host, the tsetse fly. Appl. Environ. Microbiol. 74:5965–74 [Google Scholar]
  104. Pellegrini A, Bigliardi E, Bechi N, Paulesu L, Lehane MJ, Avanzati AM. 104.  2011. Fine structure of the female reproductive system in a viviparous insect, Glossina morsitans morsitans (Diptera, Glossinidae). Tissue Cell 43:1–7 [Google Scholar]
  105. Pimley RW, Langley PA. 105.  1981. Hormonal control of lipid synthesis in the fat body of the adult female tsetse fly, Glossina morsitans. J. Insect Physiol. 27:839–47 [Google Scholar]
  106. Pimley RW, Langley PA. 106.  1982. Hormone stimulated lipolysis and proline synthesis in the fat body of the adult tsetse fly, Glossina morsitans. J. Insect Physiol. 28:781–89 [Google Scholar]
  107. Raikhel AS, Kokoza VA, Zhu J, Martin D, Wang SF. 107.  et al. 2002. Molecular biology of mosquito vitellogenesis: from basic studies to genetic engineering of antipathogen immunity. Insect Biochem. Mol. Biol. 32:1275–86 [Google Scholar]
  108. Retnakaran A, Percy J. 108.  1985. Fertilization and special modes of reproduction. Comprehensive Insect Physiology, Biochemistry and Pharmacology GA Kerkut, LI Gilbert 1231–94 Oxford, UK: Pergamon [Google Scholar]
  109. Richard DS, Rybczynski R, Wilson TG, Wang Y, Wayne ML. 109.  et al. 2005. Insulin signaling is necessary for vitellogenesis in Drosophila melanogaster independent of the roles of juvenile hormone and ecdy-steroids: Female sterility of the chico1 insulin signaling mutation is autonomous to the ovary. J. Insect Physiol. 51:455–64 [Google Scholar]
  110. Riddiford LM. 110.  2012. How does juvenile hormone control insect metamorphosis and reproduction?. Gen. Comp. Endocrinol. 179:477–84 [Google Scholar]
  111. Riddiford LM, Dhadialla TS. 111.  1990. Protein synthesis by the milk gland and fat body of the tsetse fly, Glossina pallidipes. Insect Biochem. 20:493–500 [Google Scholar]
  112. Rio RV, Symula RE, Wang J, Lohs C, Wu YN. 112.  et al. 2012. Insight into the transmission biology and species-specific functional capabilities of tsetse (Diptera: Glossinidae) obligate symbiont Wigglesworthia. mBio 3:e00240 [Google Scholar]
  113. Robert A, Grillot JP, Guilleminot J, Raabe M. 113.  1984. Experimental and ultrastructural study of the control of ovulation and parturition in the tsetse fly Glossina fuscipes (Diptera). J. Insect Physiol. 30:671–79 [Google Scholar]
  114. Robert A, Strambi A, Strambi C. 114.  1985. Haemolymph ecdysteroid levels in female tsetse fly Glossina fuscipes (Diptera) during the first reproductive cycle: a comparison between virgin and mated females. J. Insect Physiol. 32:665–71 [Google Scholar]
  115. Roberts MJ. 115.  1972. The role of the choriothete in tsetse flies. Parasitology 64:23–36 [Google Scholar]
  116. Rogers D, Robinson T. 116.  2004. Tsetse distribution. The Trypanosomiases I Maudlin, P Holmes, M Miles 139–79 Oxford, UK: CABI [Google Scholar]
  117. Sappington TW. 117.  2002. The major yolk proteins of higher Diptera are homologs of a class of minor yolk proteins in Lepidoptera. J. Mol. Evol. 55:470–75 [Google Scholar]
  118. Saunders DS. 118.  1960. Ovaries of Glossina morsitans. Nature 185:121–22 [Google Scholar]
  119. Saunders DS. 119.  1961. Studies on ovarian development in tsetse flies (Glossina, Diptera). Parasitology 51:545–64 [Google Scholar]
  120. Saunders DS, Dodd CWH. 120.  1972. Mating, insemination, and ovulation in the tsetse fly, Glossina morsitans. J. Insect Physiol. 18:187–98 [Google Scholar]
  121. Schwenk RW, Holloway GP, Luiken JJ, Bonen A, Glatz JF. 121.  2010. Fatty acid transport across the cell membrane: regulation by fatty acid transporters. Prostaglandins Leukot. Essent. Fatty Acids 82:149–54 [Google Scholar]
  122. Søndergaard L, Mauchline D, Egetoft P, White N, Wulff P, Bownes M. 122.  1995. Nutritional response in a Drosophila yolk protein gene promoter. Mol. Gen. Genet. 248:25–32 [Google Scholar]
  123. Stay B, Coop AC. 123.  1974. ‘Milk’ secretion for embryogenesis in a viviparous cockroach. Tissue Cell 6:669–93 [Google Scholar]
  124. Steelman CD. 124.  1976. Effects of external and internal arthropod parasites on domestic livestock production. Annu. Rev. Entomol. 21:155–78 [Google Scholar]
  125. Strickler-Dinglasan PM, Guz N, Attardo G, Aksoy S. 125.  2006. Molecular characterization of iron binding proteins from Glossina morsitans morsitans (Diptera: Glossinidae). Insect Biochem. Mol. Biol. 36:921–33 [Google Scholar]
  126. Terashima J, Bownes M. 126.  2004. Translating available food into the number of eggs laid by Drosophila melanogaster. Genetics 167:1711–19 [Google Scholar]
  127. Thomson TC, Johnson J. 127.  2010. Inducible somatic oocyte destruction in response to rapamycin requires wild-type regulation of follicle cell epithelial polarity. Cell Death Differ. 17:1717–27 [Google Scholar]
  128. Tobe SS, Davey KG. 128.  1971. The choriothete of Glossina austeni Newst. Bull. Entomol. Res. 61:363–68 [Google Scholar]
  129. Tobe SS, Davey KG. 129.  1974. Autoradiographic study of protein synthesis in abdominal tissues of Glossina austeni. Tissue Cell 6:255–68 [Google Scholar]
  130. Tobe SS, Davey KG, Huebner E. 130.  1973. Nutrient transfer during the reproductive cycle in Glossina austeni Newst.: histology and histochemistry of the milk gland, fat body, and oenocytes. Tissue Cell 5:633–50 [Google Scholar]
  131. Tobe SS, Langley PA. 131.  1978. Reproductive physiology of Glossina. Annu. Rev. Entomol. 23:283–307Reviews tsetse reproductive physiology. [Google Scholar]
  132. Tworzydlo W, Kisiel E, Bilinski SM. 132.  2013. Embryos of the viviparous dermapteran, Arixenia esau develop sequentially in two compartments: terminal ovarian follicles and the uterus. PLOS ONE 8:e64087 [Google Scholar]
  133. Van der Horst DJ, Ryan RO. 133.  2012. Lipid transport. Insect Molecular Biology and Biochemistry LI Gilbert 317–45 Amsterdam: Elsevier [Google Scholar]
  134. Vreysen MJ, Saleh KM, Ali MY, Abdulla AM, Zhu ZR. 134.  et al. 2000. Glossina austeni (Diptera: Glossinidae) eradicated on the island of Unguja, Zanzibar, using the sterile insect technique. J. Econ. Entomol. 93:123–35 [Google Scholar]
  135. Wang J, Aksoy S. 135.  2012. PGRP-LB is a maternally transmitted immune milk protein that influences symbiosis and parasitism in tsetse's offspring. Proc. Natl. Acad. Sci. USA 109:10552–57 [Google Scholar]
  136. Wang J, Weiss BL, Aksoy S. 136.  2013. Tsetse fly microbiota: form and function. Front. Cell. Infect. Microbiol. 3:69 [Google Scholar]
  137. Wang SL, Baumann A, Wilson TG. 137.  2007. Drosophila melanogaster Methoprene-tolerant (Met) gene homologs from three mosquito species: members of PAS transcriptional factor family. J. Insect Physiol. 53:246–53 [Google Scholar]
  138. Weiss BL, Maltz M, Aksoy S. 138.  2012. Obligate symbionts activate immune system development in the tsetse fly. J. Immunol. 188:3395–403Studies the role of symbionts for immune development (see also References 139 and 140). [Google Scholar]
  139. Weiss BL, Wang J, Aksoy S. 139.  2011. Tsetse immune system maturation requires the presence of obligate symbionts in larvae. PLOS Biol. 9:e1000619 [Google Scholar]
  140. Weiss BL, Wang J, Maltz MA, Wu Y, Aksoy S. 140.  2013. Trypanosome infection establishment in the tsetse fly gut is influenced by microbiome-regulated host immune barriers. PLOS Pathog. 9:e1003318 [Google Scholar]
  141. Welburn SC, Fèvre EM, Coleman PG, Odiit M, Maudlin I. 141.  2001. Sleeping sickness: a tale of two diseases. Trends Parasitol. 17:19–24 [Google Scholar]
  142. White NM, Bownes M. 142.  1997. Cloning and characterization of three Musca domestica yolk protein genes. Insect Mol. Biol. 6:329–41 [Google Scholar]
  143. Williford A, Stay B, Bhattacharya D. 143.  2004. Evolution of a novel function: nutritive milk in the viviparous cockroach, Diploptera punctata. Evol. Dev. 6:67–77 [Google Scholar]
  144. Yang G, Attardo GM, Lohs C, Aksoy S. 144.  2010. Molecular characterization of two novel milk proteins in the tsetse fly (Glossina morsitans morsitans). Insect Mol. Biol. 19:253–62 [Google Scholar]

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