1932

Abstract

Immune defense and reproduction are physiologically and energetically demanding processes and have been observed to trade off in a diversity of female insects. Increased reproductive effort results in reduced immunity, and reciprocally, infection and activation of the immune system reduce reproductive output. This trade-off can manifest at the physiological level (within an individual) and at the evolutionary level (genetic distinction among individuals in a population). The resource allocation model posits that the trade-off arises because of competition for one or more limiting resources, and we hypothesize that pleiotropic signaling mechanisms regulate allocation of that resource between reproductive and immune processes. We examine the role of juvenile hormone, 20-hydroxyecdysone, and insulin/insulin-like growth factor-like signaling in regulating both oogenesis and immune system activity, and propose a signaling network that may mechanistically regulate the trade-off. Finally, we discuss implications of the trade-off in an ecological and evolutionary context.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-ento-010715-023924
2016-03-11
2024-06-16
Loading full text...

Full text loading...

/deliver/fulltext/ento/61/1/annurev-ento-010715-023924.html?itemId=/content/journals/10.1146/annurev-ento-010715-023924&mimeType=html&fmt=ahah

Literature Cited

  1. Abrisqueta M, Süren-Castillo S, Maestro JL. 1.  2014. Insulin receptor-mediated nutritional signalling regulates juvenile hormone biosynthesis and vitellogenin production in the German cockroach. Insect Biochem. Mol. Biol. 49:14–23 [Google Scholar]
  2. Abu-Hakima R, Davey KG. 2.  1977. Two actions of juvenile hormone on the follicle cells of Rhodnius prolixus: the importance of volume changes. J. Exp. Biol. 69:33–44 [Google Scholar]
  3. Adamo SA, Fidler TL, Forestell CA. 3.  2007. Illness-induced anorexia and its possible function in the caterpillar, Manduca sexta. Brain Behav. Immun. 21:292–300 [Google Scholar]
  4. Ahmed AM, Baggott SL, Maingon R, Hurd H. 4.  2002. The costs of mounting an immune response are reflected in the reproductive fitness of the mosquito Anopheles gambiae. Oikos 97:371–77 [Google Scholar]
  5. Ahmed AM, Hurd H. 5.  2006. Immune stimulation and malaria infection impose reproductive costs in Anopheles gambiae via follicular apoptosis. Microbes Infect. 8:308–15 [Google Scholar]
  6. Armitage SAO, Siva-Jothy MT. 6.  2005. Immune function responds to selection for cuticular colour in Tenebrio molitor. Heredity 94:660–66 [Google Scholar]
  7. Armitage SAO, Thompson JJW, Rolff J, Siva-Jothy MT. 7.  2003. Examining costs of induced and constitutive immune investment in Tenebrio molitor. J. Evol. Biol. 16:1038–44 [Google Scholar]
  8. Arrese EL, Soulages JL. 8.  2010. Insect fat body: energy, metabolism, and regulation. Annu. Rev. Entomol. 55:207–25 [Google Scholar]
  9. Attardo GM, Hansen IA, Raikhel AS. 9.  2005. Nutritional regulation of vitellogenesis in mosquitoes: implications for anautogeny. Insect Biochem. Mol. Bio. 35:661–75 [Google Scholar]
  10. Avila FW, Sirot LK, LaFlamme BA, Rubinstein CD, Wolfner MF. 10.  2011. Insect seminal fluid proteins: identification and function. Annu. Rev. Entomol. 56:21–40 [Google Scholar]
  11. Awmack CS, Leather SL. 11.  2002. Host plant quality and fecundity in herbivorous insects. Annu. Rev. Entomol. 47:817–44 [Google Scholar]
  12. Ayres JS, Schneider DS. 12.  2009. The role of anorexia in resistance and tolerance to infections in Drosophila. PLOS Biol. 7:e1000150 [Google Scholar]
  13. Badisco L, Van Wielendaele P, Vanden Broeck J. 13.  2013. Eat to reproduce: a key role for the insulin signaling pathway in adult insects. Front. Physiol. 4:1–16 [Google Scholar]
  14. Baer B, Armitage SAO, Boomsma JJ. 14.  2006. Sperm storage induces an immunity cost in ants. Nature 441:872–75 [Google Scholar]
  15. Bajgar A, Kucerova K, Jonatova L, Tomcala A, Schneedorferova I. 15.  et al. 2015. Extracellular adenosine mediates a systemic metabolic switch during immune response. PLOS Biol. doi: 10.1371/journal.pbio.1002135 [Google Scholar]
  16. Barnes AI, Wigby S, Boone JM, Partridge L, Chapman T. 16.  2008. Feeding, fecundity and lifespan in female Drosophila melanogaster. Proc. Biol. Sci. 275:1675–83 [Google Scholar]
  17. Bascuñán-García AP, Lara C, Córdoba-Aguilar A. 17.  2010. Immune investment impairs growth, female reproduction and survival in the house cricket, Acheta domesticus. J. Insect Physiol. 56:204–11 [Google Scholar]
  18. Bashir-Tanoli S, Tinsley MC. 18.  2014. Immune response costs are associated with changes in resource acquisition and not resource reallocation. Funct. Ecol. 28:1011–19 [Google Scholar]
  19. Becker T, Loch G, Beyer M, Zinke I, Aschenbrenner AC. 19.  et al. 2010. FOXO-dependent regulation of innate immune homeostasis. Nature 463:369–73 [Google Scholar]
  20. Boots M, Begon M. 20.  1993. Trade-offs with resistance to a granulosis virus in the Indian meal moth, examined by a laboratory evolution experiment. Funct. Ecol. 7:528–34 [Google Scholar]
  21. Brookes VJ. 21.  1969. The induction of yolk protein synthesis in the fat body of an insect, Leucophaea maderae, by an analog of the juvenile hormone. Dev. Biol. 20:459–71 [Google Scholar]
  22. Büning J. 22.  1994. The Insect Ovary: Ultrastructure, Previtellogenic Growth, and Evolution London: Chapman and Hall [Google Scholar]
  23. Carvalho GB, Kapahi P, Anderson DJ, Benzer S. 23.  2006. Allocrine modulation of feeding behavior by the sex peptide of Drosophila. Curr. Biol. 16:692–96 [Google Scholar]
  24. Castella G, Christe P, Chapuisat M. 24.  2009. Mating triggers dynamic immune regulations in wood ant queens. J. Evol. Biol. 22:564–70 [Google Scholar]
  25. Castillo JC, Reynolds SE, Eleftherianos I. 25.  2011. Insect immune responses to nematode parasites. Trends Parasitol. 27:537–47 [Google Scholar]
  26. Catalán TP, Barceló M, Niemeyer HM, Kalergis AM, Bozinovic F. 26.  2011. Pathogen- and diet-dependent foraging, nutritional and immune ecology in mealworms. Evol. Ecol. Res. 13:711–23 [Google Scholar]
  27. Cavaliere V, Bernardi F, Romani P, Duchi S, Gargiulo G. 27.  2008. Building up the Drosophila eggshell: First of all the eggshell genes must be transcribed. Dev. Dyn. 237:2061–72 [Google Scholar]
  28. Chen S-L, Lin C-P, Lu K-H. 28.  2012. cDNA isolation, expression, and hormonal regulation of yolk protein genes in the oriental fruit fly, Bactrocera dorsalis (Hendel) (Diptera: Tephritidae). J. Insect Physiol. 58:763–70 [Google Scholar]
  29. Chinzei Y, Wyatt GR. 29.  1985. Vitellogenin titre in haemolymph of Locusta migratoria in normal adults, after ovariectomy, and in response to methoprene. J. Insect Physiol. 31:441–45 [Google Scholar]
  30. Clifton M, Correa S. 30.  2014. Male Aedes aegypti mosquitoes use JHIII transferred during copulation to influence previtellogenic ovary physiology and affect the reproductive output of female mosquitoes. J. Insect Physiol. 64:40–47 [Google Scholar]
  31. Clifton ME, Noriega FG. 31.  2011. Nutrient limitation results in juvenile hormone-mediated resorption of previtellogenic ovarian follicles in mosquitoes. J. Insect Physiol. 57:1274–81 [Google Scholar]
  32. Cotter SC, Kruuk LEB, Wilson K. 32.  2004. Costs of resistance: genetic correlations and potential trade-offs in an insect immune system. J. Evol. Biol. 17:421–29 [Google Scholar]
  33. Cotter SC, Simpson SJ, Raubenheimer D, Wilson K. 33.  2011. Macronutrient balance mediates trade-offs between immune function and life history traits. Funct. Ecol. 25:186–98 [Google Scholar]
  34. Cressler CE, Nelson WA, Day T, McCauley E. 34.  2013. Disentangling the interaction among host resources, the immune system and pathogens. Ecol. Lett. 17:284–93 [Google Scholar]
  35. DiAngelo JR, Bland ML, Bambina S, Cherry S, Birnbaum MJ. 35.  2009. The immune response attenuates growth and nutrient storage in Drosophila by reducing insulin signaling. PNAS 106:20853–58 [Google Scholar]
  36. Dimarcq JL, Imler JL, Lanot R, Ezekowitz RAB, Hoffmann JA. 36.  et al. 1997. Treatment of l(2)mbn Drosophila tumorous blood cells with the steroid hormone ecdysone amplifies the inducibility of antimicrobial peptide gene expression. Insect Biochem. Mol. Biol. 27:877–86 [Google Scholar]
  37. Dionne MS, Pham LN, Shirasu-Hiza M, Schneider DS. 37.  2006. Akt and foxo dysregulation contribute to infection-induced wasting in Drosophila. Curr. Biol. 16:1977–85 [Google Scholar]
  38. Dixon A. 38.  1963. Reproductive activity of the sycamore aphid, Drepanosiphum platanoides (Schr.) (Hemiptera, Aphididae). J. Anim. Ecol. 32:33–48 [Google Scholar]
  39. Domanitskaya EV, Liu H, Chen S, Kubli E. 39.  2007. The hydroxyproline motif of male sex peptide elicits the innate immune response in Drosophila females. FEBS J. 274:5659–68 [Google Scholar]
  40. Drummond-Barbosa D, Spradling AC. 40.  2001. Stem cells and their progeny respond to nutritional changes during Drosophila oogenesis. Dev. Biol. 231:265–78 [Google Scholar]
  41. Du Plessis H, Byrne MJ, Van den Berg J. 41.  2012. The effect of different host plants on the reproduction and longevity of Nysius natalensis. Entomol. Exp. Appl. 145:209–14 [Google Scholar]
  42. Duneau D, Ebert D. 41a.  2012. Host sexual dimorphism and parasite adaptation. PLOS Biol 10:2e1001271 doi: 10.1371/journal.pbio.1001271 [Google Scholar]
  43. Fan Y, Rafaeli A, Moshitzky P, Kubli E, Choffat Y, Applebaum SW. 42.  2000. Common functional elements of Drosophila melanogaster seminal peptides involved in reproduction of Drosophila melanogaster and Helicoverpa armigera females. Insect Biochem. Mol. Biol. 30:805–12 [Google Scholar]
  44. Fedorka KM, Linder JE, Winterhalter W, Promislow D. 43.  2007. Post-mating disparity between potential and realized immune response in Drosophila melanogaster. Proc. Biol. Sci. 274:1211–17 [Google Scholar]
  45. Fedorka KM, Zuk M, Mousseau T. 44.  2004. Immune suppression and the cost of reproduction in the ground cricket, Allonemobius socius. Evolution 58:2478–85 [Google Scholar]
  46. Fellowes MDE, Kraaijeveld AR, Godfray HCJ. 45.  1999. The relative fitness of Drosophila melanogaster (Diptera, Drosophilidae) that have successfully defended themselves against the parasitoid Asobara tabida (Hymenoptera, Braconidae). J. Evol. Biol. 12:123–28 [Google Scholar]
  47. Ferdig MT, Beerntsen BT, Spray FJ, Li J, Christensen BM. 46.  1993. Reproductive costs associated with resistance in a mosquito-filarial worm system. Am. J. Trop. Med. Hyg. 49:756–62 [Google Scholar]
  48. Finch CE, Rose MR. 47.  1995. Hormones and the physiological architecture of life history evolution. Q. Rev. Biol. 70:1–52 [Google Scholar]
  49. Fisher RA. 48.  1930. The Genetical Theory of Natural Selection Oxford, UK: Oxford Univ. Press [Google Scholar]
  50. Flatt T, Heyland A, Rus F, Porpiglia E, Sherlock C. 49.  et al. 2008. Hormonal regulation of the humoral innate immune response in Drosophila melanogaster. J. Exp. Biol. 211:2712–24 [Google Scholar]
  51. Flatt T, Kawecki T. 50.  2007. Juvenile hormone as a regulator of the trade-off between reproduction and life span in Drosophila melanogaster. Evolution 61:1980–91 [Google Scholar]
  52. Flatt T, Tu M-P, Tatar M. 51.  2005. Hormonal pleiotropy and the juvenile hormone regulation of Drosophila development and life history. BioEssays 27:999–1010 [Google Scholar]
  53. Fleig R. 52.  1995. Role of the follicle cells for yolk uptake in ovarian follicles of the honey bee Apis mellifera (Hymenoptera: Apidae). Int. J. Insect Morphol. Embryol. 24:427–33 [Google Scholar]
  54. Foley K, Fazio G, Jensen AB, Hughes WOH. 53.  2012. Nutritional limitation and resistance to opportunistic Aspergillus parasites in honey bee larvae. J. Invertebr. Pathol. 111:68–73 [Google Scholar]
  55. Gabrieli P, Kakani EG, Mitchell SN, Mameli E, Want EJ. 54.  et al. 2014. Sexual transfer of the steroid hormone 20E induces the postmating switch in Anopheles gambiae. PNAS 111:16353–58 [Google Scholar]
  56. Gadgil M, Bossert WH. 55.  1970. Life historical consequences of natural selection. Am. Nat. 104:1–24 [Google Scholar]
  57. González-Santoyo I, Córdoba-Aguilar A. 56.  2012. Phenoloxidase: a key component of the insect immune system. Entomol. Exp. Appl. 142:1–16 [Google Scholar]
  58. Gruntenko NE, Rauschenbach IY. 57.  2008. Interplay of JH, 20E and biogenic amines under normal and stress conditions and its effect on reproduction. J. Insect Physiol. 54:902–8 [Google Scholar]
  59. Gupta V, Ali ZS, Prasad NG. 58.  2013. Sexual activity increases resistance against Pseudomonas entomophila in male Drosophila melanogaster. BMC Evol. Biol 13:185 [Google Scholar]
  60. Gwynn DM, Callaghan A, Gorham J, Walters KFA, Fellowes MDE. 59.  2005. Resistance is costly: trade-offs between immunity, fecundity, and survival in the pea aphid. Proc. R. Soc. B 272:1803–8 [Google Scholar]
  61. Hansen IA, Attardo GM, Rodriguez SD, Drake LL. 60.  2014. Four-way regulation of mosquito yolk protein precursor genes by juvenile hormone-, ecdysone-, nutrient-, and insulin-like peptide signaling pathways. Front. Physiol. 5:1–8 [Google Scholar]
  62. Harshman LG, Zera AJ. 61.  2007. The cost of reproduction: the devil in the details. Trends Ecol. Evol. 22:80–86 [Google Scholar]
  63. Hepat R, Kim Y. 62.  2014. JH modulates a cellular immunity of Tribolium castaneum in a Met-independent manner. J. Insect Physiol. 63:40–47 [Google Scholar]
  64. Hoffmann JA. 63.  2003. The immune response of Drosophila. Nature 426:33–38 [Google Scholar]
  65. Hogg JC, Hurd H. 64.  1995. Plasmodium yoelii nigeriensis: the effect of high and low intensity of infection upon the egg production and bloodmeal size of Anopheles stephensi during three gonotrophic cycles. Parasitology 111:555–62 [Google Scholar]
  66. Hosken DJ. 65.  2001. Sex and death: microevolutionary trade-offs between reproductive and immune investment in dung flies. Curr. Biol. 11:R379 [Google Scholar]
  67. Hosken DJ, Garner TWJ, Ward PI. 66.  2001. Sexual conflict selects for male and female reproductive characters. Curr. Biol. 11:489–93 [Google Scholar]
  68. Hossain MS, Liu Y, Zhou S, Li K, Tian L, Li S. 67.  2013. 20-hydroxyecdysone-induced transcriptional activity of FoxO upregulates brummer and acid lipase-1 and promotes lipolysis in Bombyx fat body. Insect Biochem. Mol. Biol. 43:829–38 [Google Scholar]
  69. Howick VM, Lazzaro BP. 68.  2014. Genotype and diet shape resistance and tolerance across distinct phases of bacterial infection. BMC Evol. Biol. 14:56 [Google Scholar]
  70. Hsu H-J, Drummond-Barbosa D. 69.  2009. Insulin levels control female germline stem cell maintenance via the niche in Drosophila. PNAS 106:1117–21 [Google Scholar]
  71. Hurd H. 70.  2001. Host fecundity reduction: a strategy for damage limitation?. Trends Parasitol. 17:363–68 [Google Scholar]
  72. Innocenti P, Morrow EH. 71.  2009. Immunogenic males: a genome-wide analysis of reproduction and the cost of mating in Drosophila melanogaster females. J. Evol. Biol. 22:964–73 [Google Scholar]
  73. Isaac PG, Bownes M. 72.  1982. Ovarian and fat-body vitellogenin synthesis in Drosophila melanogaster. Eur. J. Biochem. 123:527–34 [Google Scholar]
  74. Kelly CD. 73.  2011. Reproductive and physiological costs of repeated immune challenges in female Wellington tree weta (Orthoptera: Anostostomatidae). Biol. J. Linn. Soc. 104:38–46 [Google Scholar]
  75. Kim Y, Jung S, Madanagopal N. 74.  2008. Antagonistic effect of juvenile hormone on hemocyte-spreading behavior of Spodoptera exigua in response to an insect cytokine and its putative membrane action. J. Insect Physiol. 54:909–15 [Google Scholar]
  76. Klemola N, Klemola T, Rantala MJ, Ruuhola T. 75.  2007. Natural host-plant quality affects immune defence of an insect herbivore. Entomol. Exp. Appl. 23:167–76 [Google Scholar]
  77. Knell RJ, Webberley KM. 76.  2004. Sexually transmitted diseases of insects: distribution, evolution, ecology and host behaviour. Biol. Rev. Camb. Philos. Soc. 79:557–81 [Google Scholar]
  78. Kokoza VA, Martin D, Mienaltowski MJ, Ahmed A, Morton CM, Raikhel AS. 77.  2001. Transcriptional regulation of the mosquito vitellogenin gene via a blood meal-triggered cascade. Gene 274:47–65 [Google Scholar]
  79. Kraaijeveld AR, Elrayes NP, Schuppe H, Newland PL. 78.  2011. l-arginine enhances immunity to parasitoids in Drosophila melanogaster and increases NO production in lamellocytes. Dev. Comp. Immunol. 35:857–64 [Google Scholar]
  80. Kraaijeveld AR, Ferrari J, Godfray HCJ. 79.  2002. Costs of resistance in insect-parasite and insect-parasitoid interactions. Parasitology 125:S71–82 [Google Scholar]
  81. LaFever L, Drummond-Barbosa D. 80.  2005. Direct control of germline stem cell division and cyst growth by neural insulin in Drosophila. Science 309:1071–73 [Google Scholar]
  82. Law R. 81.  1979. Optimal life histories under age-specific predation. Am. Nat. 114:399–417 [Google Scholar]
  83. Lawniczak MKN, Barnes AI, Linklater JR, Boone JM, Wigby S, Chapman T. 82.  2007. Mating and immunity in invertebrates. Trends Ecol. Evol. 22:48–55 [Google Scholar]
  84. Lawniczak MKN, Begun DJ. 83.  2004. A genome-wide analysis of courting and mating responses in Drosophila melanogaster females. Genome 47:900–10 [Google Scholar]
  85. Lazzaro BP, Flores HA, Lorigan JG, Yourth CP. 84.  2008. Genotype-by-environment interactions and adaptation to local temperature affect immunity and fecundity in Drosophila melanogaster. PLOS Pathog. 4:e100025 [Google Scholar]
  86. Lazzaro BP, Little TJ. 85.  2009. Immunity in a variable world. Philos. Trans. R. Soc. B. 364:15–26 [Google Scholar]
  87. Lee KP, Simpson SJ, Wilson K. 86.  2008. Dietary protein-quality influences melanization and immune function in an insect. Funct. Ecol. 22:1052–61 [Google Scholar]
  88. Libert S, Chao Y, Zwiener J, Pletcher SD. 87.  2008. Realized immune response is enhanced in long-lived puc and chico mutants but is unaffected by dietary restriction. Mol. Immunol. 45:810–17 [Google Scholar]
  89. Luong LT, Polak M. 88.  2007. Costs of resistance in the Drosophila-Macrocheles system: a negative genetic correlation between ectoparasite resistance and reproduction. Evolution 61:1391–402 [Google Scholar]
  90. Mack PD, Kapelnikov A, Heifetz Y, Bender M. 89.  2006. Mating-responsive genes in reproductive tissues of female Drosophila melanogaster. PNAS 103:10358–63 [Google Scholar]
  91. McGraw LA, Gibson G, Clark A, Wolfner MF. 90.  2004. Genes regulated by mating, sperm, or seminal proteins in mated female Drosophila melanogaster. Curr. Biol. 14:1509–14 [Google Scholar]
  92. McKean KA, Lazzaro BP. 91.  2010. The costs of immunity and the evolution of immunological defense mechanisms. Mechanisms of Life History Evolution T Flatt, A Heyland 299–310 Oxford, UK: Oxford Univ. Press [Google Scholar]
  93. McKean KA, Nunney L. 92.  2001. Increased sexual activity reduces male immune function in Drosophila melanogaster. PNAS 98:7904–9 [Google Scholar]
  94. McKean KA, Nunney L. 93.  2005. Bateman's principle and immunity: Phenotypically plastic reproductive strategies predict changes in immunological sex differences. Evolution 59:1510–17 [Google Scholar]
  95. McKean KA, Yourth CP, Lazzaro BP, Clark AG. 94.  2008. The evolutionary costs of immunological maintenance and deployment. BMC Evol. Biol. 8:76–95 [Google Scholar]
  96. McNamara KB, Van Lieshout E, Simmons LW. 95.  2013. Females suffer a reduction in the viability of stored sperm following an immune challenge. J. Evol. Biol. 27:133–40 [Google Scholar]
  97. Meister M, Lagueux M. 96.  2003. Drosophila blood cells. Cell. Microbiol. 5:9573–80 [Google Scholar]
  98. Miest TS, Bloch-Qazi MC. 97.  2008. Sick of mating: sexual transfer of a pathological bacterium in Drosophila melanogaster. Fly 2:215–19 [Google Scholar]
  99. Mirth CK, Tang HY, Makohon-Moore SC, Salhadar S, Gokhale RH. 98.  et al. 2014. Juvenile hormone regulates body size and perturbs insulin signaling in Drosophila. PNAS 111:7018–23 [Google Scholar]
  100. Moret Y, Schmid-Hempel P. 99.  2000. Survival for immunity: the price of immune system activation for bumblebee workers. Science 290:1166–68 [Google Scholar]
  101. Nijhout HF. 100.  1994. Insect Hormones Princeton, NJ: Princeton Univ. Press [Google Scholar]
  102. Nystrand M, Dowling DK. 101.  2014. Dose-dependent effects of an immune challenge at both ultimate and proximate levels in Drosophila melanogaster. J. Evol. Biol. 27:876–88 [Google Scholar]
  103. Parthasarathy R, Palli SR. 102.  2011. Molecular analysis of nutritional and hormonal regulation of female reproduction in the red flour beetle, Tribolium castaneum. Insect Biochem. Mol. Biol. 41:294–305 [Google Scholar]
  104. Peng J, Zipperlen P, Kubli E. 103.  2005. Drosophila Sex-peptide stimulates female innate immune system after mating via the Toll and Imd pathways. Curr. Biol. 15:1690–94 [Google Scholar]
  105. Polak M. 104.  1996. Ectoparasite effects on host survival and reproduction: the Drosophila-Macrocheles association. Ecology 77:1379–89 [Google Scholar]
  106. Povey S, Cotter SC, Simpson SJ, Wilson K. 105.  2013. Dynamics of macronutrient self-medication and illness-induced anorexia in virally infected insects. J. Anim. Ecol. 83:245–55 [Google Scholar]
  107. Reaney LT, Knell RJ. 106.  2010. Immune activation but not male quality affects female current reproductive investment in a dung beetle. Behav. Ecol. 21:1367–72 [Google Scholar]
  108. Regan JC, Brandão AS, Leitão AB, Mantas Dias AR, Sucena E. 107.  et al. 2013. Steroid hormone signaling is essential to regulate innate immune cells and fight bacterial infection in Drosophila. PLOS Pathog. 9:e1003720 [Google Scholar]
  109. Ribeiro C, Dickson BJ. 108.  2010. Sex Peptide receptor and neuronal TOR/S6K signaling modulate nutrient balancing in Drosophila. Curr. Biol. 20:1000–5 [Google Scholar]
  110. 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 ecdysteroids: Female sterility of the chico1 insulin signaling mutation is autonomous to the ovary. J. Insect Physiol. 51:455–64 [Google Scholar]
  111. Roff DA. 110.  1992. Evolution of Life Histories: Theory and Analysis London: Chapman and Hall [Google Scholar]
  112. Rolff J. 111.  2002. Bateman's principle and immunity. Proc. R. Soc. B 269:867–72 [Google Scholar]
  113. Rolff J, Siva-Jothy MT. 112.  2002. Copulation corrupts immunity: a mechanism for a cost of mating in insects. PNAS 99:9916–18 [Google Scholar]
  114. Rose MR, Bradley TJ. 113.  1998. Evolutionary physiology of the cost of reproduction. Oikos 83:443–51 [Google Scholar]
  115. Rus F, Flatt T, Tong M, Aggarwal K, Okuda K. 114.  et al. 2013. Ecdysone triggered PGRP-LC expression controls Drosophila innate immunity. EMBO J. 32:1626–38 [Google Scholar]
  116. Sander JD, Joung JK. 115.  2014. CRISPR-Cas systems for editing, regulating, and targeting genomes. Nat. Biotechnol. 32:347–55 [Google Scholar]
  117. Schilder RJ, Marden JH. 116.  2006. Metabolic syndrome and obesity in an insect. PNAS 103:18805–9 [Google Scholar]
  118. Schmid-Hempel P. 117.  2005. Evolutionary ecology of insect immune defenses. Annu. Rev. Entomol. 50:529–51 [Google Scholar]
  119. Sheng Z, Xu J, Bai H, Zhu F, Palli SR. 118.  2011. Juvenile hormone regulates vitellogenin gene expression through insulin-like peptide signaling pathway in the red flour beetle, Tribolium castaneum. J. Biol. Chem. 286:41924–36 [Google Scholar]
  120. Shoemaker KL, Parsons NM, Adamo SA. 119.  2006. Mating enhances parasite resistance in the cricket Gryllus texensis. Anim. Behav. 71:371–80 [Google Scholar]
  121. Short SM, Lazzaro BP. 120.  2010. Female and male genetic contributions to post-mating immune defence in female Drosophila melanogaster. Proc. Biol. Sci. 277:3649–57 [Google Scholar]
  122. Short SM, Wolfner MF, Lazzaro BP. 121.  2012. Female Drosophila melanogaster suffer reduced defense against infection due to seminal fluid components. J. Insect Physiol. 58:1192–201 [Google Scholar]
  123. Simmons LW. 122.  2011. Resource allocation trade-off between sperm quality and immunity in the field cricket, Teleogryllus oceanicus. Behav. Ecol. 23:168–73 [Google Scholar]
  124. Siva-Jothy MT, Yoshitaka T, Hooper R. 123.  1998. Decreased immune response as a proximate cost of copulation and oviposition in a damselfly. Physiol. Entomol. 23:274–77 [Google Scholar]
  125. Soller M, Bownes M, Kubli E. 124.  1999. Control of oocyte maturation in sexually mature Drosophila females. Dev. Biol. 208:337–51 [Google Scholar]
  126. Sorrentino RP, Carton Y, Govind S. 125.  2002. Cellular immune response to parasite infection in the Drosophila lymph gland is developmentally regulated. Dev. Biol. 243:65–80 [Google Scholar]
  127. Stahlschmidt ZR, Rollinson N, Acker M, Adamo SA. 126.  2013. Are all eggs created equal? Food availability and the fitness trade-off between reproduction and immunity. Funct. Ecol. 27:800–6 [Google Scholar]
  128. Stearns SC. 127.  1992. Evolution of Life Histories Oxford, UK: Oxford Univ. Press [Google Scholar]
  129. Stearns SC. 128.  2000. Life history evolution: successes, limitations, and prospects. Naturwissenschaften 87:476–86 [Google Scholar]
  130. Strand M. 129.  2008. Insect hemocytes and their role in immunity. Insect Immunology NE Beckage 25–47 San Diego, CA: Elsevier [Google Scholar]
  131. Süren-Castillo S, Abrisqueta M, Maestro JL. 130.  2012. FoxO inhibits juvenile hormone biosynthesis and vitellogenin production in the German cockroach. Insect Biochem. Mol. Biol. 42:491–98 [Google Scholar]
  132. Tan KL, Vlisidou I, Wood W. 131.  2014. Ecdysone mediates the development of immunity in the Drosophila embryo. Curr. Biol. 24:1–8 [Google Scholar]
  133. Terashima J, Bownes M. 132.  2004. Translating available food into the number of eggs laid by Drosophila melanogaster. Genetics 167:1711–19 [Google Scholar]
  134. Toivonen JM, Partridge L. 133.  2009. Endocrine regulation of aging and reproduction in Drosophila. Mol. Cell. Endocrinol. 299:39–50 [Google Scholar]
  135. Tsukamoto Y, Kataoka H, Nagasawa H, Nagata S. 134.  2014. Mating changes the female dietary preference in the two-spotted cricket, Gryllus bimaculatus. Front. Physiol. 5:95 [Google Scholar]
  136. Tu M-P, Yin C-M, Tatar M. 135.  2005. Mutations in insulin signaling pathway alter juvenile hormone synthesis in Drosophila melanogaster. Gen. Comp. Endocrinol. 142:347–56 [Google Scholar]
  137. Valtonen TM, Viitaniemi H, Rantala MJ. 136.  2010. Copulation enhances resistance against an entomopathogenic fungus in the mealworm beetle Tenebrio molitor. Parasitology 137:985–89 [Google Scholar]
  138. Wang MC, Bohmann D, Jasper H. 137.  2005. JNK extends life span and limits growth by antagonizing cellular and organism-wide responses to insulin signaling. Cell 121:115–25 [Google Scholar]
  139. Wheeler D. 138.  1996. The role of nourishment in oogenesis. Annu. Rev. Entomol. 41:407–31 [Google Scholar]
  140. Wigglesworth VB. 139.  1960. Nutrition and reproduction in insects. Proc. Nutr. Soc. 19:18–23 [Google Scholar]
  141. Williams G. 140.  1966. Natural selection, the costs of reproduction, and a refinement of Lack's principle. Am. Nat. 100:687–90 [Google Scholar]
  142. Wu Q, Brown MR. 141.  2006. Signaling and function of insulin-like peptides in insects. Annu. Rev. Entomol. 51:1–24 [Google Scholar]
  143. Yan G, Severson DW, Christensen BM. 142.  1997. Costs and benefits of mosquito refractoriness to malaria parasites: implications for genetic variability of mosquitoes and genetic control of malaria. Evolution 51:441–50 [Google Scholar]
  144. Ye YH, Chenoweth SF, McGraw EA. 143.  2009. Effective but costly, evolved mechanisms of defense against a virulent opportunistic pathogen in Drosophila melanogaster. PLOS Pathog. 5:e1000385 [Google Scholar]
  145. Zera AJ, Harshman LG, Williams TD. 144.  2007. Evolutionary endocrinology: the developing synthesis between endocrinology and evolutionary genetics. Annu. Rev. Ecol. Evol. Syst. 38:793–817 [Google Scholar]
  146. Zerofsky M, Harel E, Silverman N, Tatar M. 145.  2005. Aging of the innate immune response in Drosophila melanogaster. Aging Cell 4:103–8 [Google Scholar]
  147. Zhang Z, Palli SR. 146.  2009. Identification of a cis-regulatory element required for 20-hydroxyecdysone enhancement of antimicrobial peptide gene expression in Drosophila melanogaster. Insect Mol. Biol. 18:595–605 [Google Scholar]
/content/journals/10.1146/annurev-ento-010715-023924
Loading
/content/journals/10.1146/annurev-ento-010715-023924
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error