1932

Abstract

An enormous amount of work has been done on aging in , a classical genetic and molecular model system, but also in numerous other insects. However, these two extensive bodies of work remain poorly integrated to date. Studies in often explore genetic, developmental, physiological, and nutrition-related aspects of aging in the lab, while studies in other insects often explore ecological, social, and somatic aspects of aging in both lab and natural populations. Alongside exciting genomic and molecular research advances in aging in , many new studies have also been published on aging in various other insects, including studies on aging in natural populations of diverse species. However, no broad synthesis of these largely separate bodies of work has been attempted. In this review, we endeavor to synthesize these two semi-independent literatures to facilitate collaboration and foster the exchange of ideas and research tools. While lab studies of have illuminated many fundamental aspects of senescence, the stunning diversity of aging patterns among insects, especially in the context of their rich ecology, remains vastlyunderstudied. Coupled with field studies and novel, more easily applicable molecular methods, this represents a major opportunity for deepening our understanding of the biology of aging in insects and beyond.

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2022-01-07
2024-05-27
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Literature Cited

  1. 1. 
    Abrams PA. 1993. Does increased mortality favor the evolution of more rapid senescence?. Evolution 47:877–87
    [Google Scholar]
  2. 2. 
    Adler MI, Bonduriansky R. 2014. Why do the well-fed appear to die young? A new evolutionary hypothesis for the effect of dietary restriction on lifespan. Bioessays 36:439–50
    [Google Scholar]
  3. 3. 
    Alavi Y, Elgar MA, Jones TM. 2017. Sex versus parthenogenesis; immune function in a facultatively parthenogenetic phasmatid (Extatosoma tiaratum). J. Insect Physiol. 100:65–70
    [Google Scholar]
  4. 4. 
    Alpatov W, Pearl R 1929. Experimental studies on the duration of life. XII. Influence of temperature during the larval period and adult life on the duration of the life of the imago of Drosophila melanogaster. Am. Nat. 63:37–67
    [Google Scholar]
  5. 5. 
    Amdam GV, Simoes ZLP, Hagen A, Norberg K, Schroder K et al. 2004. Hormonal control of the yolk precursor vitellogenin regulates immune function and longevity in honeybees. Exp. Gerontol. 39:767–73
    [Google Scholar]
  6. 6. 
    Anholt BR. 1994. Cannibalism and early instar survival in a larval damselfly. Oecologia 99:60–65
    [Google Scholar]
  7. 7. 
    Archer CR, Hunt J. 2015. Understanding the link between sexual selection, sexual conflict and aging using crickets as a model. Exp. Gerontol. 71:4–13
    [Google Scholar]
  8. 8. 
    Austad SN. 1989. Life extension by dietary restriction in the bowl and doily spider, Frontinella pyramitela. Exp. Gerontol. 24:83–92
    [Google Scholar]
  9. 9. 
    Banks MJ, Thompson DJ. 1985. Emergence, longevity and breeding area fidelity in Coenagrion puella (L.) (Zygoptera: Coenagrionidae). Odonalologica 14:279–86
    [Google Scholar]
  10. 10. 
    Baumberger PJ. 1914. Studies in the longevity of insects. Ann. Entomol. Soc. Am. 7:323–53
    [Google Scholar]
  11. 11. 
    Beck J, Fiedler K. 2009. Adult life spans of butterflies (Lepidoptera: Papilionoidea + Hesperioidea): broadscale contingencies with adult and larval traits in multi-species comparisons. Biol. J. Linn. Soc. 96:166–84
    [Google Scholar]
  12. 12. 
    Behrends A, Scheiner R, Baker N, Amdam GV. 2007. Cognitive aging is linked to social role in honey bees (Apis mellifera). Exp. Gerontol. 42:1146–53
    [Google Scholar]
  13. 13. 
    Behrman EL, Watson SS, O'Brien KR, Heschel MS, Schmidt PS 2015. Seasonal variation in life history traits in two Drosophila species. J. Evol. Biol. 28:1691–704
    [Google Scholar]
  14. 14. 
    Beirne C, Delahay R, Young A. 2015. Sex differences in senescence: the role of intra-sexual competition in early adulthood. Proc. R. Soc. B 282:20151086
    [Google Scholar]
  15. 15. 
    Bell G, Koufopanou V 1985. The cost of reproduction. OSEB 3:83–131
    [Google Scholar]
  16. 16. 
    Bell G, Koufopanou V 1986. The Cost of Reproduction 3 Oxford, UK: Oxford Univ. Press
  17. 17. 
    Beramendi A, Peron S, Casanova G, Reggiani C, Cantera R 2007. Neuromuscular junction in abdominal muscles of Drosophila melanogaster during adulthood and aging. J. Comp. Neurol. 501:498–508
    [Google Scholar]
  18. 18. 
    Blanckenhorn WU, Fairbairn D. 1995. Life history adaptation along a latitudinal cline in the water strider Aquarius remigis (Heteroptera: Gerridae). J. Evol. Biol. 8:21–41
    [Google Scholar]
  19. 19. 
    Bonduriansky R, Brassil CE. 2002. Rapid and costly ageing in wild male flies. Nature 420:377
    [Google Scholar]
  20. 20. 
    Bonduriansky R, Brassil CE. 2005. Reproductive ageing and sexual selection on male body size in a wild population of antler flies (Protopiophila litigata). J. Evol. Biol. 18:1332–40
    [Google Scholar]
  21. 21. 
    Bonduriansky R, Maklakov A, Zajitschek F, Brooks R 2008. Sexual selection, sexual conflict and the evolution of ageing and life span. Funct. Ecol. 22:443–53
    [Google Scholar]
  22. 22. 
    Brenman-Suttner DB, Yost RT, Frame AK, Robinson JW, Moehring AJ, Simon AF. 2020. Social behavior and aging: a fly model. Genes Brain Behav 19:e12598
    [Google Scholar]
  23. 23. 
    Brent CS, Spurgeon DW. 2019. Egg production and longevity of Lygus hesperus (Hemiptera: Miridae) adult females under constant and variable temperatures. J. Entomol. Sci. 54:69–80
    [Google Scholar]
  24. 24. 
    Briceno R, Eberhard W. 1987. Genetic and environmental effects on wing polymorphisms in two tropical earwigs (Dermaptera: Labiidae). Oecologia 74:253–55
    [Google Scholar]
  25. 25. 
    Briga M, Verhulst S. 2015. What can long-lived mutants tell us about mechanisms causing aging and lifespan variation in natural environments?. Exp. Gerontol. 21:71–76
    [Google Scholar]
  26. 26. 
    Broughton SJ, Piper MDW, Ikeya T, Bass TM, Jacobson J et al. 2005. Longer lifespan, altered metabolism, and stress resistance in Drosophila from ablation of cells making insulin-like ligands. PNAS 102:3105–10
    [Google Scholar]
  27. 27. 
    Brown S, Strausfeld N. 2009. The effect of age on a visual learning task in the American cockroach. Learn. Mem. 16:210–23
    [Google Scholar]
  28. 28. 
    Buckley LB, Arakaki AJ, Cannistra AF, Kharouba HM, Kingsolver JG. 2017. Insect development, thermal plasticity and fitness implications in changing, seasonal environments. Integr. Comp. Biol. 57:988–98
    [Google Scholar]
  29. 29. 
    Burns JG, Mery F. 2010. Transgenerational memory effect of ageing in Drosophila. J. Evol. Biol. 23:678–86
    [Google Scholar]
  30. 30. 
    Burraco P, Orizaola G, Monaghan P, Metcalfe NB. 2020. Climate change and ageing in ectotherms. Glob. Change Biol. 26:5371–81
    [Google Scholar]
  31. 31. 
    Calabi P, Porter SD. 1989. Worker longevity in the fire ant Solenopsis invicta: ergonomic considerations of correlations between temperature, size and metabolic rates. J. Insect Physiol. 35:643–49
    [Google Scholar]
  32. 32. 
    Carbone MA, Yamamoto A, Huang W, Lyman RA, Meadors TB et al. 2016. Genetic architecture of natural variation in visual senescence in Drosophila. PNAS 113:E6620–29
    [Google Scholar]
  33. 33. 
    Carey JR. 2002. Longevity minimalists: life table studies of two species of northern Michigan adult mayflies. Exp. Gerontol. 37:567–70
    [Google Scholar]
  34. 34. 
    Charlesworth B. 1994. Evolution in Age-Structured Populations Cambridge, UK: Cambridge Univ. Press
  35. 35. 
    Chen HY, Maklakov AA. 2012. Longer life span evolves under high rates of condition-dependent mortality. Curr. Biol. 22:2140–43
    [Google Scholar]
  36. 36. 
    Churchill ER, Dytham C, Thom MDF. 2019. Differing effects of age and starvation on reproductive performance in Drosophila melanogaster. Sci. Rep. 9:2167
    [Google Scholar]
  37. 37. 
    Clancy DJ, Gems D, Harshman LG, Oldham S, Stocker H et al. 2001. Extension of life-span by loss of CHICO, a Drosophila insulin receptor substrate protein. Science 292:104–6
    [Google Scholar]
  38. 38. 
    Cohen AA 2017. Taxonomic diversity, complexity and the evolution of senescence. The Evolution of Senescence in the Tree of Life RP Sheferson, OR Jones, R Salguero-Gomez 83–102 Cambridge, UK: Cambridge Univ. Press
    [Google Scholar]
  39. 39. 
    Collier KJ, Smith BJ. 2000. Interactions of adult stoneflies (Plecoptera) with riparian zones. I. Effects of air temperature and humidity on longevity. Int. J. Freshwater Entomol. 22:275–84
    [Google Scholar]
  40. 40. 
    Contreras-Garduno J, Cordoba-Aguilar A, Lanz-Mendoza H, Rivera AC. 2009. Territorial behaviour and immunity are mediated by juvenile hormone: the physiological basis of honest signalling?. Funct. Ecol. 23:157–63
    [Google Scholar]
  41. 41. 
    Cook LG, Gullan PJ. 2001. Longevity and reproduction in Apiomorpha rubsaamen (Hemiptera: Sternorrhyncha: Coccoidea). Boll. Zool. Agr. Bachic. II 33:259–65
    [Google Scholar]
  42. 42. 
    Cooper TM, Mockett RJ, Sohal BH, Sohal RS, Orr WC. 2004. Effect of caloric restriction on life span of the housefly, Musca domestica. FASEB J 18:1591–93
    [Google Scholar]
  43. 43. 
    Corona M, Velarde RA, Remolina S, Moran-Lauter A, Wang Y et al. 2007. Vitellogenin, juvenile hormone, insulin signaling, and queen honey bee longevity. PNAS 104:7128–33
    [Google Scholar]
  44. 44. 
    Daly HV, Doyen JT, Ehrlich PR. 1978. Introduction to Insect Biology and Diversity New York: McGraw Hill
  45. 45. 
    Drewry MD, Williams JM, Hatle JD. 2011. Life-extending dietary restriction and ovariectomy result in similar feeding rates but different physiologic responses in grasshoppers. Exp. Gerontol. 46:781–86
    [Google Scholar]
  46. 46. 
    Ducatez S, Baguette M, Stevens V, Legrand D, Fréville H 2012. Complex interactions between paternal and maternal effects: parental experience and age at reproduction affect fecundity and offspring performance in a butterfly. Evolution 66:3558–69
    [Google Scholar]
  47. 47. 
    Elsner D, Meusemann K, Korb J. 2018. Longevity and transposon defense, the case of termite reproductives. PNAS 115:5504–9
    [Google Scholar]
  48. 48. 
    Encina F, De Los Ríos P, Vega R, Mardones A. 2020. Standard culture of Paratanytarsus grimmii Schneider, 1885 (Diptera: Chironomidae), for its use in toxicity bioassays. Braz. J. Biol. 80:735–40
    [Google Scholar]
  49. 49. 
    Fadamiro HY, Heimpel GE. 2001. Effects of partial sugar deprivation on lifespan and carbohydrate mobilization in the parasitoid Macrocentrus grandii (Hymenoptera: Braconidae). Ann. Entomol. Soc. Am. 94:909–16
    [Google Scholar]
  50. 50. 
    Farris SM, Robinson GE, Fahrbach SE 2001. Experience- and age-related outgrowth of intrinsic neurons in the mushroom bodies of the adult worker honeybee. J. Neurosci. 21:6395–404
    [Google Scholar]
  51. 51. 
    Ferkau C, Fischer K. 2006. Costs of reproduction in male Bicyclus anynana and Pieris napi butterflies: effects of mating history and food limitation. Ethology 112:1117–27
    [Google Scholar]
  52. 52. 
    Fielenbach N, Antebi A. 2008. C. elegans dauer formation and the molecular basis of plasticity. Genes Dev 22:2149–65
    [Google Scholar]
  53. 53. 
    Fisher DN, James A, Rodriguez-Munoz R, Tregenza T. 2015. Behaviour in captivity predicts some aspects of natural behaviour, but not others, in a wild cricket population. Proc. Biol. Sci. 282:20150708
    [Google Scholar]
  54. 54. 
    Flatt T. 2020. Life-history evolution and the genetics of fitness components in Drosophila melanogaster. Genetics 214:3–48
    [Google Scholar]
  55. 55. 
    Flatt T, Amdam GV, Kirkwood TBL, Omholt SW. 2013. Life-history evolution and the polyphenic regulation of somatic maintenance and survival. Q. Rev. Biol. 88:185–218
    [Google Scholar]
  56. 56. 
    Flatt T, Min KJ, D'Alterio C, Villa-Cuesta E, Cumbers J et al. 2008. Drosophila germ-line modulation of insulin signaling and lifespan. PNAS 105:6368–73
    [Google Scholar]
  57. 57. 
    Flatt T, Tu M-P, Tatar M. 2005. Hormonal pleiotropy and the juvenile hormone regulation of Drosophila development and life history. BioEssays 27:999–1010
    [Google Scholar]
  58. 58. 
    Formica VA, Augat ME, Barnard ME, Butterfield RE, Wood CW, Brodie ED. 2010. Using home range estimates to construct social networks for species with indirect behavioral interactions. Behav. Ecol. Sociobiol. 64:1199–208
    [Google Scholar]
  59. 59. 
    Fowler K, Partridge L 1989. A cost of mating in female fruitflies. Nature 338:760–61
    [Google Scholar]
  60. 60. 
    Fox CW, Bush ML, Roff DA, Wallin WG. 2004. Evolutionary genetics of lifespan and mortality rates in two populations of the seed beetle, Callosobruchus maculatus. Heredity 92:170–81
    [Google Scholar]
  61. 61. 
    Fox CW, Bush ML, Wallin WG. 2003. Maternal age affects offspring lifespan of the seed beetle, Callosobruchus maculatus. Funct. Ecol. 17:811–20
    [Google Scholar]
  62. 62. 
    Fraser MJ. 2011. Insect transgenesis: current applications and future prospects. Annu. Rev. Entomol. 57:267–89
    [Google Scholar]
  63. 63. 
    Giraldo YM, Kamhi JF, Fourcassié V, Moreau M, Robson SK et al. 2016. Lifespan behavioural and neural resilience in a social insect. Proc. Biol. Sci. 283:20152603
    [Google Scholar]
  64. 64. 
    Gompertz B. 1825. On the nature of the function expressive of the law of human mortality and on a new mode of determining life contingencies. Philos. Trans. R. Soc. Lond. 1825:513–85
    [Google Scholar]
  65. 65. 
    Greyvenstein B, Du Plessis H, Moulin N, Van den Berg J 2020. Distribution of Galepsus spp. in Southern Africa and Life History of Galepsus lenticularis (Mantodea: Tarachodidae). Insects 11:119
    [Google Scholar]
  66. 66. 
    Griffiths JT, Tauber OE. 1942. Fecundity, longevity, and parthenogenesis of the American Roach, Periplaneta americana L. Physiol. Zool. 15:196–209
    [Google Scholar]
  67. 67. 
    Haddadi M, Jahromi SR, Chandrasekhar Sagar BK, Patil RK, Shivanandappa T, Ramesh SR 2014. Brain aging, memory impairment and oxidative stress: a study in Drosophila melanogaster. Behav. Brain Res. 259:60–69
    [Google Scholar]
  68. 68. 
    Han CS, Jablonski PG. 2010. Male water striders attract predators to intimidate females into copulation. Nat. Commun. 1:52
    [Google Scholar]
  69. 69. 
    Harshman L, Zera A. 2007. The cost of reproduction: the devil in the details. Trends Ecol. Evol. 22:80–86
    [Google Scholar]
  70. 70. 
    Harvanek ZM, Lyu Y, Gendron CM, Johnson JC, Kondo S et al. 2017. Perceptive costs of reproduction drive ageing and physiology in male Drosophila. Nat. Ecol. Evol. 1:152
    [Google Scholar]
  71. 71. 
    Hatle JD, Wells SM, Fuller LE, Allen IC, Gordy LJ et al. 2006. Calorie restriction and late-onset calorie restriction extend lifespan but do not alter protein storage in female grasshoppers. Mech. Ageing Dev. 127:883–91
    [Google Scholar]
  72. 72. 
    Heatwole H, Heatwole A. 1968. Movements, host-fungus preferences, and longevity of Bolitotherus cornutus (Coleoptera: Tenebrionidae). Ann. Entomol. Soc. Am. 61:18–23
    [Google Scholar]
  73. 73. 
    Hercus MJ, Hoffmann AA. 2000. Maternal and grandmaternal age influence offspring fitness in Drosophila. Proc. R. Soc. Lond. B 267:2105–10
    [Google Scholar]
  74. 74. 
    Hercus MJ, Loeschcke V, Rattan SI 2003. Lifespan extension of Drosophila melanogaster through hormesis by repeated mild heat stress. Biogerontology 4:149–56
    [Google Scholar]
  75. 75. 
    Hodkova M. 2008. Tissue signaling pathways in the regulation of life-span and reproduction in females of the linden bug, Pyrrhocoris apterus. J. Insect Physiol. 54:508–17
    [Google Scholar]
  76. 76. 
    Hoffman JM, Soltow QA, Li S, Sidik A, Jones DP, Promislow DEL. 2014. Effects of age, sex, and genotype on high-sensitivity metabolomic profiles in the fruit fly, Drosophila melanogaster. Aging Cell 13:596–604
    [Google Scholar]
  77. 77. 
    Hoffmann AA, Sgro CM. 2011. Climate change and evolutionary adaptation. Nature 470:479–85
    [Google Scholar]
  78. 78. 
    Hollingsworth MJ, Maynard Smith J. 1955. The effects of inbreeding on rate of development and on fertility in Drosophila subobscura. J. Genet. 53:295–314
    [Google Scholar]
  79. 79. 
    Hooper AK, Spagopoulou F, Wylde Z, Maklakov AA, Bonduriansky R. 2017. Ontogenetic timing as a condition-dependent life history trait: High-condition males develop quickly, peak early, and age fast. Evolution 71:671–85
    [Google Scholar]
  80. 80. 
    How Y-F, Lee C-Y. 2014. Effects of temperature and humidity on the survival and water loss of Cimex hemipterus (Hemiptera: Cimicidae). J. Med. Entomol. 47:987–95
    [Google Scholar]
  81. 81. 
    Ibanez S, Gallet C, Després L. 2012. Plant insecticidal toxins in ecological networks. Toxins 4:228–43
    [Google Scholar]
  82. 82. 
    Ihle EK, Mutti SN, Kaftanoglu O, Amdam VG 2019. Insulin receptor substrate gene knockdown accelerates behavioural maturation and shortens lifespan in honeybee workers. Insects 10:390
    [Google Scholar]
  83. 83. 
    Ivimey-Cook E, Moorad J. 2018. Disentangling pre- and postnatal maternal age effects on offspring performance in an insect with elaborate maternal care. Am. Nat. 192:564–76
    [Google Scholar]
  84. 84. 
    Jin K, Wilson KA, Beck JN, Nelson CS, Brownridge GW 3rd et al. 2020. Genetic and metabolomic architecture of variation in diet restriction-mediated lifespan extension in Drosophila. PLOS Genet 16:e1008835
    [Google Scholar]
  85. 85. 
    Jones MA, Grotewiel M. 2011. Drosophila as a model for age-related impairment in locomotion and other behaviours. Exp. Gerontol. 46:320–25
    [Google Scholar]
  86. 86. 
    Jones OR, Scheuerlein A, Salguero-Gomez R, Camarda CG, Schaible R et al. 2014. Diversity of ageing across the tree of life. Nature 505:169–73
    [Google Scholar]
  87. 87. 
    Kaitala A. 1991. Phenotypic plasticity in reproductive behaviour of waterstriders: trade-offs between reproduction and longevity during food stress. Funct. Ecol. 5:12–18
    [Google Scholar]
  88. 88. 
    Kapahi P, Zid BM, Harper T, Koslover D, Sapin V, Benzer S. 2004. Regulation of lifespan in Drosophila by modulation of genes in the TOR signaling pathway. Curr. Biol. 14:885–90
    [Google Scholar]
  89. 89. 
    Kawasaki N, Brassil CE, Brooks RC, Bonduriansky R. 2008. Environmental effects on the expression of life span and aging: an extreme contrast between wild and captive cohorts of Telostylinus angusticollis (Diptera: Neriidae). Am. Nat. 172:346–57
    [Google Scholar]
  90. 90. 
    Keil G, Cummings E, de Magalhaes JP. 2015. Being cool: how body temperature influences ageing and longevity. Biogerontology 16:383–97
    [Google Scholar]
  91. 91. 
    Kenyon C. 2011. The first long-lived mutants: discovery of the insulin/IGF-1 pathway for ageing. Philos. Trans. R. Soc. B 366:9–16
    [Google Scholar]
  92. 92. 
    Khazaeli AA, Tatar M, Pletcher SD, Curtsinger JW. 1997. Heat-induced longevity extension in Drosophila. I. Heat treatment, mortality, and thermotolerance. J. Gerontol. A 52:B48–52
    [Google Scholar]
  93. 93. 
    Kiritani K. 2013. Different effects of climate change on the population dynamics of insects. Appl. Entomol. Zool. 48:97–104
    [Google Scholar]
  94. 94. 
    Kirkwood TBL. 1977. Evolution and ageing. Nature 270:301–4
    [Google Scholar]
  95. 95. 
    Kirkwood TBL, Shanley DP. 2005. Food restriction, evolution and ageing. Mech. Ageing Dev. 126:1011–16
    [Google Scholar]
  96. 96. 
    Kowalczyk A, Partha R, Clark NL, Chikina M 2020. Pan-mammalian analysis of molecular constraints underlying extended lifespan. eLife 9:e51089
    [Google Scholar]
  97. 97. 
    Lane SJ, Frankino WA, Elekonich MM, Roberts SP. 2014. The effects of age and lifetime flight behavior on flight capacity in Drosophila melanogaster. J. Exp. Biol. 217:1437–43
    [Google Scholar]
  98. 98. 
    Lansing AI. 1947. A transmissible, cumulative, and reversible factor in aging. J. Gerontol. 2:228–39
    [Google Scholar]
  99. 99. 
    Lee ET. 1992. Statistical Methods for Survival Data Analysis New York: Wiley
  100. 100. 
    Lee KP, Simpson SJ, Clissold FJ, Brooks R, Ballard JWO et al. 2008. Lifespan and reproduction in Drosophila: new insights from nutritional geometry. PNAS 105:2498–503
    [Google Scholar]
  101. 101. 
    Liao S, Broughton S, Nässel DR. 2017. Behavioral senescence and aging-related changes in motor neurons and brain neuromodulator levels are ameliorated by lifespan-extending reproductive dormancy in Drosophila. Front. Cell Neurosci. 11:111
    [Google Scholar]
  102. 102. 
    Libert S, Zwiener J, Chu X, Vanvoorhies W, Roman G, Pletcher SD 2007. Regulation of Drosophila life span by olfaction and food-derived odors. Science 315:1133–37
    [Google Scholar]
  103. 103. 
    Lin Y-J, Seroude L, Benzer S 1998. Extended life-span and stress resistance in the Drosophila mutant methuselah. Science 282:943–46
    [Google Scholar]
  104. 104. 
    Lindsay E. 1940. The biology of the silverfish, Ctenolepisma longicaudata Esch. with particular reference to its feeding habits. Proc. R. Soc. Victoria 52:35–83
    [Google Scholar]
  105. 105. 
    Liu P-C, Wei J-R, Tian S, Hao D-J 2017. Male-male lethal combat in the quasi-gregarious parasitoid Anastatus disparis (Hymenoptera: Eupelmidae). Sci. Rep. 7:11875
    [Google Scholar]
  106. 106. 
    Loeb J, Northrop J. 1917. On the influence of food and temperature upon the duration of life. J. Biol. Chem. 32:103–21
    [Google Scholar]
  107. 107. 
    Maklakov AA, Simpson SJ, Zajitschek F, Hall MD, Dessmann J et al. 2008. Sex-specific fitness effects of nutrient intake on reproduction and lifespan. Curr. Biol. 18:1062–66
    [Google Scholar]
  108. 108. 
    Mallard F, Farina M, Tully T 2015. Within-species variation in long-term trajectories of growth, fecundity and mortality in the Collembola Folsomia candida. J. Evol. Biol. 28:2275–84
    [Google Scholar]
  109. 109. 
    Mathur V, Schmidt PS. 2017. Adaptive patterns of phenotypic plasticity in laboratory and field environments in Drosophila melanogaster. Evolution 71:465–74
    [Google Scholar]
  110. 110. 
    Mautz B, Rode N, Bonduriansky R, Rundle H. 2019. Comparing ageing and the effects of diet supplementation in wild versus captive antler flies, Protopiophila litigata. J. Anim. Ecol. 88:1913–24
    [Google Scholar]
  111. 111. 
    Maynard Smith J 1958. The effects of temperature and of egg-laying on the longevity of Drosophila subobscura. J. Exp. Biol. 35:832–42
    [Google Scholar]
  112. 112. 
    Maynard Smith J 1958. Prolongation of the life of Drosophila subobscura by brief exposure of adults to a high temperature. Nature 181:496–97
    [Google Scholar]
  113. 113. 
    Mery F. 2007. Aging and its differential effects on consolidated memory forms in Drosophila. Exp. Gerontol. 42:99–101
    [Google Scholar]
  114. 114. 
    Mery F, Kawecki T. 2005. A cost of long-term memory in Drosophila. Science 308:1148
    [Google Scholar]
  115. 115. 
    Messina FJ, Fry J. 2003. Environment-dependent reversal of a life history trade-off in the seed beetle Callosobruchus maculatus. J. Evol. Biol. 16:501–9
    [Google Scholar]
  116. 116. 
    Michelutti KB, Soares ERP, Sguarizi-Antonio D, Piva RC, Súarez YR et al. 2018. Influence of temperature on survival and cuticular chemical profile of social wasps. J. Therm. Biol. 71:221–31
    [Google Scholar]
  117. 117. 
    Michiels NK, Dhondt AA. 1989. Effects of emergence characteristics on longevity and maturation in the dragonfly Sympetrum danae (Anisoptera: Libellulidae). Hydrobiologia 171:149–58
    [Google Scholar]
  118. 118. 
    Molleman F, Ding J, Boggs CL, Carey JR, Arlet ME 2009. Does dietary restriction reduce life span in male fruit-feeding butterflies?. Exp. Gerontol. 44:601–6
    [Google Scholar]
  119. 119. 
    Molleman F, Zwaan BJ, Brakefield PM, Carey JR. 2007. Extraordinary long life spans in fruit-feeding butterflies can provide window on evolution of life span and aging. Exp. Gerontol. 42:472–82
    [Google Scholar]
  120. 120. 
    Moorad J, Promislow D, Silvertown J 2019. Evolutionary ecology of senescence and a reassessment of Williams' “extrinsic mortality” hypothesis. Trends Ecol. Evol. 34:519–30
    [Google Scholar]
  121. 121. 
    Moorad JA, Nussey DH. 2016. Evolution of maternal effect senescence. PNAS 113:362–67
    [Google Scholar]
  122. 122. 
    Moorad JA, Promislow DE. 2011. Evolutionary demography and quantitative genetics: age-specific survival as a threshold trait. Proc. Biol. Sci. 278:144–51
    [Google Scholar]
  123. 123. 
    Mossman JA, Mabeza RMS, Blake E, Mehta N, Rand DM 2019. Age of both parents influences reproduction and egg dumping behavior in Drosophila melanogaster. J. Hered. 110:300–9
    [Google Scholar]
  124. 124. 
    Müller HG, Wang JL, Carey JR, Caswell-Chen EP, Chen C et al. 2004. Demographic window to aging in the wild: constructing life tables and estimating survival functions from marked individuals of unknown age. Aging Cell 3:125–31
    [Google Scholar]
  125. 125. 
    Münch D, Amdam GV, Wolschin F. 2008. Ageing in a eusocial insect: molecular and physiological characteristics of life span plasticity in the honey bee. Funct. Ecol. 22:407–21
    [Google Scholar]
  126. 126. 
    Münch D, Kreibich CD, Amdam GV. 2013. Aging and its modulation in a long-lived worker caste of the honey bee. J. Exp Biol. 216:1638–49
    [Google Scholar]
  127. 127. 
    Myers JH, Rothman LE. 1995. Virulence and transmission of infectious diseases in humans and insects: evolutionary and demographic patterns. Trends Ecol. Evol. 10:194–98
    [Google Scholar]
  128. 128. 
    Nelson CM, Ihle KE, Fondrk MK, Page RE Jr., Amdam GV. 2007. The Gene vitellogenin has multiple coordinating effects on social organization. PLOS Biol 5:e62
    [Google Scholar]
  129. 129. 
    Neumann FG. 1976. Egg production, adult longevity and mortality of the stick insect Didymuria violescens (Leach) (Phasmatodea: Plasmatidae) inhabiting mountain ash forest in Victoria. J. Aust. Ent. Soc. 15:183–90
    [Google Scholar]
  130. 130. 
    Neuvonen S, Virtanen T 2015. Abiotic factors, climatic variability and forest insect pests. Climate Change and Insect Pests C Björkman, P Niemelä 154–72 Wallingford, UK: CABI
    [Google Scholar]
  131. 131. 
    Paital B, Panda SK, Hati AK, Mohanty B, Mohapatra MK et al. 2016. Longevity of animals under reactive oxygen species stress and disease susceptibility due to global warming. World J. Biol. Chem. 7:110–27
    [Google Scholar]
  132. 132. 
    Paukku S, Kotiaho JS. 2005. Cost of reproduction in Callosobruchus maculatus: effects of mating on male longevity and the effect of male mating status on female longevity. J. Insect Physiol. 51:1220–26
    [Google Scholar]
  133. 133. 
    Piper MD, Partridge L. 2007. Dietary restriction in Drosophila: delayed aging or experimental artefact?. PLOS Genet 3:e57
    [Google Scholar]
  134. 134. 
    Piper MDW, Partridge L. 2018. Drosophila as a model for ageing. Biochim. Biophys. Acta Mol. Basis Dis. 1864:2707–17
    [Google Scholar]
  135. 135. 
    Promislow DEL. 1991. Senescence in natural populations of mammals: a comparative study. Evolution 45:1869–87
    [Google Scholar]
  136. 136. 
    Promislow DEL. 2003. Mate choice, sexual conflict, and evolution of senescence. Behav. Genet. 33:191–201
    [Google Scholar]
  137. 137. 
    Raut G, Gaikwad S. 2016. Observations on the life cycle mating and cannibalism of Mantis religiosa Linnaeus, 1758 (Insecta: Mantodea: Mantidae). J. Entomol. Zool. Stud. 4:478–82
    [Google Scholar]
  138. 138. 
    Reed DH, Bryant EH. 2000. The evolution of senescence under curtailed life span in laboratory populations of Musca domestica (the housefly). Heredity 85:115–21
    [Google Scholar]
  139. 139. 
    Reinhardt K, Anthes N, Lange R. 2015. Copulatory wounding and traumatic insemination. Cold Spring Harb. Perspect. Biol. 7:a017582
    [Google Scholar]
  140. 140. 
    Reyes TM, Gabriel BP. 1975. The life history and consumption habits of Cyrtorhinus lividipennis Reuter (Hemiptera: Miridae). Philipp. Ent. 3:79–88
    [Google Scholar]
  141. 141. 
    Reznick DN, Bryant MJ, Roff D, Ghalambor CK, Ghalambor DE. 2004. Effect of extrinsic mortality on the evolution of senescence in guppies. Nature 431:1095–99
    [Google Scholar]
  142. 142. 
    Rodríguez-Muñoz R, Boonekamp JJ, Liu XP, Skicko I, Fisher DN et al. 2019. Testing the effect of early-life reproductive effort on age-related decline in a wild insect. Evolution 73:317–28
    [Google Scholar]
  143. 143. 
    Rodríguez-Muñoz R, Hopwooda P, Fisher D, Skicko I, Tucker R et al. 2019. Older males attract more females but get fewer matings in a wild field cricket. Anim. Behav. 153:1–14
    [Google Scholar]
  144. 144. 
    Rogina B, Reenan RA, Nilsen SP, Helfand SL. 2000. Extended life-span conferred by cotransporter gene mutations in Drosophila. Science 290:2137–40
    [Google Scholar]
  145. 145. 
    Rose MR. 1991. Evolutionary Biology of Aging Oxford, UK: Oxford Univ. Press
  146. 146. 
    Rosewell J, Shorrocks B. 1987. The implication of survival rates in natural populations of Drosophila: capture-recapture experiments on domestic species. Biol. J. Linn. Soc. 32:373–84
    [Google Scholar]
  147. 147. 
    Rueppell O, Christine S, Mulcrone C, Groves L 2007. Aging without functional senescence in honey bee workers. Curr. Biol. 17:R274–75
    [Google Scholar]
  148. 148. 
    Scannapieco AC, Sørensen JG, Loeschcke V, Norry FM 2007. Heat-induced hormesis in longevity of two sibling Drosophila species. Biogerontology 8:315–25
    [Google Scholar]
  149. 149. 
    Schaffner AK, Anholt BR. 1998. Influence of predator presence and prey density on behavior and growth of damselfly larvae (Ischnura elegans) (Odonata: Zygoptera). J. Insect Behav. 11:793–809
    [Google Scholar]
  150. 150. 
    Seid MA, Harris KM, Traniello JF. 2005. Age-related changes in the number and structure of synapses in the lip region of the mushroom bodies in the ant Pheidole dentata. J. Comp. Neurol. 488:269–77
    [Google Scholar]
  151. 151. 
    Sgro CM, Partridge L. 2000. Evolutionary responses of the life history of wild-caught Drosophila melanogaster to two standard methods of laboratory culture. Am. Nat. 156:341–53
    [Google Scholar]
  152. 152. 
    Shepard M, Waddill V, Kloft W. 1973. Biology of the predaceous earwig Labidura riparia (Dermaptera: Labiduridae). Ann. Entomol. Soc. Am. 66:837–41
    [Google Scholar]
  153. 153. 
    Simpson GB. 1993. Effects of temperature on the development, longevity and fecundity of Nala lividipes (Dufour) (Dermaptera: Labiduridae). Aust. J. Entomol. 32:265–72
    [Google Scholar]
  154. 154. 
    Singh K, Omkar 2009. Effect of parental ageing on offspring developmental and survival attributes in an aphidophagous ladybird, Cheilomenes sexmaculata. J. Appl. Entomol. 133:500–4
    [Google Scholar]
  155. 155. 
    Stearns SC. 1992. The Evolution of Life Histories Oxford, UK: Oxford Univ. Press
  156. 156. 
    Stearns SC, Ackermann M, Doebeli M, Kaiser M 2000. Experimental evolution of aging, growth, and reproduction in fruitflies. PNAS 97:3309–13
    [Google Scholar]
  157. 157. 
    Steigenga MJ, Hoffmann KH, Fischer K. 2006. Effects of the juvenile hormone mimic pyriproxyfen on female reproduction and longevity in the butterfly Bicyclus anynana. Entomol. Sci. 9:269–79
    [Google Scholar]
  158. 158. 
    Sun D, Guo Z, Liu Y, Zhang Y. 2017. Progress and prospects of CRISPR/Cas systems in insects and other arthropods. Front. Physiol. 8:608
    [Google Scholar]
  159. 159. 
    Sweeny BW, Vannote R. 1987. Population synchrony in mayflies: a predator satiation hypothesis. Evolution 36:810–21
    [Google Scholar]
  160. 160. 
    Takemon Y. 1993. Water intake by the adult mayfly Epeorus ikanonis (Ephemeroptera: Heptageniidae) and its effect on their longevity. Ecol. Res. 8:185–92
    [Google Scholar]
  161. 161. 
    Tamura T, Chiang A-S, Ito N, Liu H-P, Horiuchi J et al. 2003. Aging specifically impairs amnesiac-dependent memory in Drosophila. Neuron 40:1003–11
    [Google Scholar]
  162. 162. 
    Tatar M. 1999. Transgenes in the analysis of life span and fitness. Am. Nat. 154:S67–81
    [Google Scholar]
  163. 163. 
    Tatar M. 2011. The plate half-full: status of research on the mechanisms of dietary restriction in Drosophila melanogaster. Exp. Gerontol 46:363–68
    [Google Scholar]
  164. 164. 
    Tatar M, Bartke A, Antebi A. 2003. The endocrine regulation of aging by insulin-like signals. Science 299:1346–51
    [Google Scholar]
  165. 165. 
    Tatar M, Carey JR. 1995. Nutrition mediates reproductive trade-offs with age-specific mortality in the beetle Callosobruchus maculatus. Ecology 76:2066–73
    [Google Scholar]
  166. 166. 
    Tatar M, Chien SA, Priest NK. 2001. Negligible senescence during reproductive dormancy in Drosophila melanogaster. Am. Nat. 158:248–58
    [Google Scholar]
  167. 167. 
    Tatar M, Kopelman A, Epstein D, Tu MP, Yin CM, Garofalo RS. 2001. A mutant Drosophila insulin receptor homolog that extends life-span and impairs neuroendocrine function. Science 292:107–10
    [Google Scholar]
  168. 168. 
    Tatar M, Yin CM. 2001. Slow aging during insect reproductive diapause: why butterflies, grasshoppers and flies are like worms. Exp. Gerontol. 36:723–38
    [Google Scholar]
  169. 169. 
    Taylor BW, Anderson CR, Peckarsky BL 1998. Effects of size at metamorphosis on stonefly fecundity, longevity, and reproductive success. Oecologia 114:494–502
    [Google Scholar]
  170. 170. 
    Technau G. 1984. Fiber number in the mushroom bodies of adult Drosophila melanogaster depends on age, sex and experience. J. Neurogenet. 1:113–26
    [Google Scholar]
  171. 171. 
    Tetlak A, Burnett J, Hahn D, Hatle J. 2015. Vitellogenin-RNAi and ovariectomy each increase life-span, increase protein storage, and decrease feeding, but are not additive in grasshoppers. Biogerontology 16:761–74
    [Google Scholar]
  172. 172. 
    Visscher SN, Lund R, Whitmore W. 1979. Host plant growth temperatures and insect rearing temperatures influence reproduction and longevity in the grasshopper, Aulocara elliotti (Orthoptera: Acrididae). Environ. Entomol. 8:253–58
    [Google Scholar]
  173. 173. 
    Williams GC. 1957. Pleiotropy, natural selection, and the evolution of senescence. Evolution 11:398–411
    [Google Scholar]
  174. 174. 
    Williams PD, Day T. 2003. Antagonistic pleiotropy, mortality source interactions, and the evolutionary theory of senescence. Evolution 57:1478–88
    [Google Scholar]
  175. 175. 
    Wipfler B, Letsch H, Frandsen P, Kapli P, Mayer C et al. 2019. Evolutionary history of Polyneoptera and its implications for our understanding of early winged insects. PNAS 116:3024–29
    [Google Scholar]
  176. 176. 
    Wylde Z, Spagopoulou F, Hooper AK, Maklakov AA, Bonduriansky R. 2019. Parental breeding age effects on descendants’ longevity interact over 2 generations in matrilines and patrilines. PLOS Biol 17:e3000556
    [Google Scholar]
  177. 177. 
    Yamamoto R, Bai H, Dolezal A, Amdam G, Tatar M 2013. Juvenile hormone regulation of Drosophila aging. BMC Biol 11:85
    [Google Scholar]
  178. 178. 
    Yoon JS, Pausic Gagen K, Zhu DL 1990. Longevity of 68 species of Drosophila. Ohio J. Sci. 90:16–32
    [Google Scholar]
  179. 179. 
    Zajitschek F, Bonduriansky R, Zajitschek SRK, Brooks R. 2009. Sexual dimorphism in life history: age, survival and reproduction in male and female field crickets Teleogryllus commodus under seminatural conditions. Am. Nat. 173:792–802
    [Google Scholar]
  180. 180. 
    Zajitschek F, Zajitschek S, Bonduriansky R 2020. Senescence in wild insects: key questions and challenges. Funct. Ecol. 34:26–37
    [Google Scholar]
  181. 181. 
    Zhan M, Yamaza H, Sun Y, Sinclair J, Li H, Zou S 2007. Temporal and spatial transcriptional profiles of aging in Drosophila melanogaster. Genome Res 17:1236–43
    [Google Scholar]
  182. 182. 
    Zhao Y, Huang G, Zhang W. 2019. Mutations in NlInR1 affect normal growth and lifespan in the brown planthopper Nilaparvata lugens. Insect Biochem. Mol. Biol. 115:103246
    [Google Scholar]
  183. 183. 
    Zhong B, Lv C, Qin W. 2016. Preliminary study on biology and feeding capacity of Chelisoches morio (Fabricius) (Dermaptera: Chelisochidae) on Tirathaba rufivena (Walker). SpringerPlus 5:1944
    [Google Scholar]
  184. 184. 
    Zhou Z-S, Guo J-Y, Chen H-S, Wan F-H. 2010. Effects of temperature on survival, development, longevity, and fecundity of Ophraella communa (Coleoptera: Chrysomelidae), a potential biological control agent against Ambrosia artemisiifolia (Asterales: Asteraceae). Environ. Entomol. 39:1021–27
    [Google Scholar]
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