Behavioral Ecology and Sociobiology

, Volume 68, Issue 12, pp 1901–1919 | Cite as

Worker senescence and the sociobiology of aging in ants

  • Ysabel Milton Giraldo
  • James F. A. Traniello


Senescence, the decline in physiological and behavioral function with increasing age, has been the focus of significant theoretical and empirical research in a broad array of animal taxa. Preeminent among invertebrate social models of aging are ants, a diverse and ecologically dominant clade of eusocial insects characterized by reproductive and sterile phenotypes. In this review, we critically examine selection for worker life span in ants and discuss the relationship between functional senescence, longevity, task performance, and colony fitness. We did not find strong or consistent support for the hypothesis that demographic senescence in ants is programmed, or its corollary prediction that workers that do not experience extrinsic mortality die at an age approximating their life span in nature. We present seven hypotheses concerning how selection could favor extended worker life span through its positive relationship to colony size and predict that large colony size, under some conditions, should confer multiple and significant fitness advantages. Fitness benefits derived from long worker life span could be mediated by increased resource acquisition, efficient division of labor, accuracy of collective decision-making, enhanced allomaternal care and colony defense, lower infection risk, and decreased energetic costs of workforce maintenance. We suggest future avenues of research to examine the evolution of worker life span and its relationship to colony fitness and conclude that an innovative fusion of sociobiology, senescence theory, and mechanistic studies of aging can improve our understanding of the adaptive nature of worker life span in ants.


Life history Social insect Division of labor Demography Caste evolution 



We thank Drs. Mario Muscedere, Wulfila Gronenberg, Kimberly McCall, and Karen Warkentin, as well as two anonymous reviewers and Dr. Olav Rueppell, for their critical reading of the manuscript. Andrew Hoadley, J. Frances Kamhi, Darcy G. Gordon, and Jake Uminski provided helpful discussions and suggestions. YMG was supported by the National Institute on Aging of the National Institutes of Health (grant F31AG041589) and the National Science Foundation (grant IOB 0725013; JFT sponsor for both awards). The work presented here is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.


  1. Adams ES (1990) Boundary disputes in the territorial ant Azteca trigona: effects of asymmetries in colony size. Anim Behav 39:321–328Google Scholar
  2. Adams ES (1998) Territory size and shape in fire ants: a model based on neighborhood interactions. Ecology 79:1125–1134Google Scholar
  3. Adams ES (2003) Experimental analysis of territory size in a population of the fire ant Solenopsis invicta. Behav Ecol 14:48–53Google Scholar
  4. Agarwal M, Giannoni Guzmán M, Morales-Matos C, Del Valle Díaz RA, Abramson CI, Giray T (2011) Dopamine and octopamine influence avoidance learning of honey bees in a place preference assay. PLoS ONE 6:e25371PubMedCentralPubMedGoogle Scholar
  5. Aiello LC, Wheeler P (1995) The expensive-tissue hypothesis: the brain and the digestive system in human and primate evolution. Curr Anthropol 36:199–221Google Scholar
  6. Al-Khafaji K, Tuljapurkar S, Carey JR, Page RE (2009) Hierarchical demography: a general approach with an application to honey bees. Ecology 90:556–566PubMedGoogle Scholar
  7. Amador-Vargas S (2012) Behavioral responses of acacia ants correlate with age and location on the host plant. Insect Soc 59:341–350Google Scholar
  8. Amdam GV (2011) Social context, stress, and plasticity of aging. Aging Cell 10:18–27PubMedGoogle Scholar
  9. Amdam GV, Page RE (2005) Intergenerational transfers may have decoupled physiological and chronological age in a eusocial insect. Ageing Res Rev 4:398–408PubMedCentralPubMedGoogle Scholar
  10. Amdam GV, Simões ZLP, Hagen A, Norberg K, Schrøder K, Mikkelsen Ø, Kirkwood TBL, Omholt SW (2004) Hormonal control of the yolk precursor vitellogenin regulates immune function and longevity in honeybees. Exp Gerontol 39:767–773PubMedGoogle Scholar
  11. Amdam GV, Aase ALTO, Seehuus S-C, Fondrk MK, Norberg K, Hartfelder K (2005) Social reversal of immunosenescence in honey bee workers. Exp Gerontol 40:939–947PubMedCentralPubMedGoogle Scholar
  12. Amdam GV, Rueppell O, Fondrk MK, Page RE, Nelson CM (2009) The nurse’s load: early life exposure to brood-rearing affects behavior and lifespan in honey bees (Apis mellifera). Exp Gerontol 44:467–471PubMedCentralPubMedGoogle Scholar
  13. Anderson C, Ratnieks F (1999) Task partitioning in insect societies. I. Effect of colony size on queueing delay and colony ergonomic efficiency. Am Nat 154:521–535PubMedGoogle Scholar
  14. Asano E, Cassill DL (2011) Impact of worker longevity and other endogenous factors on colony size in the fire ant, Solenopsis invicta. Insect Soc 58:551–557Google Scholar
  15. Austad SN (2009) Is there a role for new invertebrate models for aging research? J Gerontol Biol Sci 64:192–194Google Scholar
  16. Batchelor TP, Briffa M (2011) Fight tactics in wood ants: individuals in smaller groups fight harder but die faster. Proc R Soc Lond B 278:3243–3250Google Scholar
  17. Baudisch A, Vaupel J (2010) Senescence vs. sustenance: evolutionary-demographic models of aging. Demogr Res 23:655–668Google Scholar
  18. Behrends A, Scheiner R (2010) Learning at old age: a study on winter bees. Front Behav Neurosci 4:15PubMedCentralPubMedGoogle Scholar
  19. Behrends A, Scheiner R, Baker N, Amdam GV (2007) Cognitive aging is linked to social role in honey bees (Apis mellifera). Exp Gerontol 42:1146–1153PubMedCentralPubMedGoogle Scholar
  20. Beshers SN, Fewell JH (2001) Models of division of labor in social insects. Annu Rev Entomol 46:413–440PubMedGoogle Scholar
  21. Bonasio R, Zhang G, Ye C, Mutti NS, Fang X et al (2010) Genomic comparison of the ants Camponotus floridanus and Harpegnathos saltator. Science 329:1068–1071PubMedCentralPubMedGoogle Scholar
  22. Bonner JT (1993) Dividing the labour in cells and societies. Curr Sci 64:459–466Google Scholar
  23. Boomsma JJ, Ratnieks FLW (1996) Paternity in eusocial hymenoptera. Phil Trans R Soc B 351:947–975Google Scholar
  24. Bourke AFG (1999) Colony size, social complexity and reproductive conflict in social insects. J Evol Biol 12:245–257Google Scholar
  25. Bourke AFG (2007) Kin selection and the evolutionary theory of aging. Ann Rev Ecol Evol Syst 38:103–128Google Scholar
  26. Brady SG, Schultz TR, Fisher BL, Ward PS (2006) Evaluating alternative hypotheses for the early evolution and diversification of ants. Proc Natl Acad Sci U S A 103:18172–18177PubMedCentralPubMedGoogle Scholar
  27. Bredesen DE (2004) The non-existent aging program: how does it work? Aging Cell 3:255–259Google Scholar
  28. Brown JJ, Traniello JFA (1998) Regulation of brood-care behavior in the dimorphic castes of the ant Pheidole morrisi (Hymenoptera: Formicidae): effects of caste ratio, colony size, and colony needs. J Insect Behav 11:209–219Google Scholar
  29. Buffenstein R (2008) Negligible senescence in the longest living rodent, the naked mole-rat: insights from a successfully aging species. J Comp Physiol B 178:439–445PubMedGoogle Scholar
  30. Burd M (1996) Foraging performance by Atta colombica, a leaf-cutting ant. Am Nat 148:597–612Google Scholar
  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 35:643–649Google Scholar
  32. Calabi P, Traniello JFA (1989a) Social organization in the ant Pheidole dentata: physical and temporal caste ratios lack ecological correlates. Behav Ecol Sociobiol 24:69–78Google Scholar
  33. Calabi P, Traniello JFA (1989b) Behavioral flexibility in age castes of the ant Pheidole dentata. J Insect Behav 2:663–677Google Scholar
  34. Calleri DV, McGrail Reid E, Rosengaus RB, Vargo EL, Traniello JFA (2006) Inbreeding and disease resistance in a social insect: effects of heterozygosity on immunocompetence in the termite Zootermopsis angusticollis. Proc R Soc Lond B 273:2633–2640Google Scholar
  35. Cao TT (2013) High social density increases foraging and scouting rates and induces polydomy in Temnothorax ants. Behav Ecol Sociobiol 67:1799–1807Google Scholar
  36. Cassill D (2002) Yoyo-bang: a risk-aversion investment strategy by a perennial insect society. Oecologia 132:150–158Google Scholar
  37. Cassill DL, Tschinkel WR (1995) Allocation of liquid food to larvae via trophallaxis in colonies of the fire ant, Solenopsis invicta. Anim Behav 50:801–813Google Scholar
  38. Cassill DL, Tschinkel WR (1999) Effects of colony-level attributes on larval feeding in the fire ant, Solenopsis invicta. Insect Soc 46:261–266Google Scholar
  39. Chapuisat M, Keller L (2002) Division of labour influences the rate of ageing in weaver ant workers. Proc R Soc Lond B 269:909–913Google Scholar
  40. Cole BJ (1983) Multiple mating and the evolution of social behavior in the Hymenoptera. Behav Ecol Sociobiol 12:191–201Google Scholar
  41. Cole BJ (2009) The ecological setting of social evolution: the demography of ant populations. In: Fewell JH, Gadau J (eds) New frontiers for behavioral ecology: from gene to society. Harvard University Press, pp 74–104Google Scholar
  42. Conradt L, Roper TJ (2005) Consensus decision making in animals. Trends Ecol Evol 20:449–456PubMedGoogle Scholar
  43. Constant N, Santorelli LA, Lopes JFS, Hughes WOH (2012) The effects of genotype, caste, and age on foraging performance in leaf-cutting ants. Behav Ecol 23:1284–1288Google Scholar
  44. Couzin ID (2009) Collective cognition in animal groups. Trends Cogn Sci 13:36–43PubMedGoogle Scholar
  45. Couzin ID, Krause J, Franks NR, Levin SA (2005) Effective leadership and decision-making in animal groups on the move. Nature 433:513–516PubMedGoogle Scholar
  46. Cremer S, Armitage SAO, Schmid-Hempel P (2007) Social immunity. Curr Biol 17:R693–R702PubMedGoogle Scholar
  47. Crozier RH, Page RE (1985) On being the right size: male contributions and multiple mating in social Hymenoptera. Behav Ecol Sociobiol 18:105–115Google Scholar
  48. Crozier RH, Newey PS, Schlüns EA, Robson SKA (2010) A masterpiece of evolution—Oecophylla weaver ants (Hymenoptera: Formicidae). Myrmecol News 13:57–71Google Scholar
  49. den Boer SPA, Baer B, Dreier S, Aron S, Nash DR, Boomsma JJ (2009) Prudent sperm use by leaf-cutter ant queens. Proc R Soc Lond B 276:3945–3953Google Scholar
  50. Donaldson-Matasci MC, DeGrandi-Hoffman G, Dornhaus A (2013) Bigger is better: honeybee colonies as distributed information-gathering systems. Anim Behav 85:585–592Google Scholar
  51. Dornhaus A, Holley J-A, Pook VG, Worswick G, Franks NR (2008) Why do not all workers work? Colony size and workload during emigrations in the ant Temnothorax albipennis. Behav Ecol Sociobiol 63:43–51Google Scholar
  52. Dornhaus A, Holley J-A, Franks NR (2009) Larger colonies do not have more specialized workers in the ant Temnothorax albipennis. Behav Ecol 20:922–929Google Scholar
  53. Dornhaus A, Powell S, Bengston S (2012) Group size and its effects on collective organization. Annu Rev Entomol 57:123–141PubMedGoogle Scholar
  54. Duarte A, Weissing FJ, Pen I, Keller L (2011) An evolutionary perspective on self-organized division of labor in social insects. Ann Rev Ecol Evol Syst 42:91–110Google Scholar
  55. Dukas R, Dukas L (2011) Coping with nonrepairable body damage: effects of wing damage on foraging performance in bees. Anim Behav 81:635–638Google Scholar
  56. Eelen D, Børgesen L, Billen J (2006) Functional morphology of the postpharyngeal gland of queens and workers of the ant Monomorium pharaonis (L.). Acta Zool 87:101–111Google Scholar
  57. Fefferman NH, Traniello JFA, Rosengaus RB, Calleri DV (2007) Disease prevention and resistance in social insects: modeling the survival consequences of immunity, hygienic behavior, and colony organization. Behav Ecol Sociobiol 61:565–577Google Scholar
  58. Fernández-Marín H, Zimmerman JK, Nash DR, Boomsma JJ, Wcislo WT (2009) Reduced biological control and enhanced chemical pest management in the evolution of fungus farming in ants. Proc R Soc Lond B 276:2263–2269Google Scholar
  59. Ferrari R, Gonzalez-Rivero M, Mumby P (2012) Size matters in competition between corals and macroalgae. Mar Ecol Prog Ser 467:77–88Google Scholar
  60. Finch CE (1990) Longevity, senescence, and the genome. University of Chicago Press, ChicagoGoogle Scholar
  61. Finch CE (1998) Variations in senescence and longevity include the possibility of negligible senescence. J Gerontol 53A:B235–B239Google Scholar
  62. Finch CE (2009) Update on slow aging and negligible senescence—a mini-review. Gerontology 55:307–313PubMedGoogle Scholar
  63. Fjerdingstad EJ, Crozier RH (2006) The evolution of worker caste diversity in social insects. Am Nat 167:390–400PubMedGoogle Scholar
  64. Flanagan TP, Letendre K, Burnside WR, Fricke GM, Moses ME (2012) Quantifying the effect of colony size and food distribution on harvester ant foraging. PLoS ONE 7:e39427PubMedCentralPubMedGoogle Scholar
  65. Forsyth A (1978) Studies on the behavioral ecology of polygynous social wasps. Dissertation, Harvard UniversityGoogle Scholar
  66. Franks NR, Dornhaus A, Fitzsimmons JP, Stevens M (2003) Speed versus accuracy in collective decision making. Proc R Soc Lond B 270:2457–2463Google Scholar
  67. Franks NR, Dornhaus A, Best CS, Jones EL (2006) Decision making by small and large house-hunting ant colonies: one size fits all. Anim Behav 72:611–616Google Scholar
  68. Gao Q, Bidochka MJ, Thompson GJ (2012) Effect of group size and caste ratio on individual survivorship and social immunity in a subterranean termite. Acta Ethol 15:55–63Google Scholar
  69. Garcia MB, Dahlgren JP, Ehrlén J (2011) No evidence of senescence in a 300-year-old mountain herb. J Ecol 99:1424–1430Google Scholar
  70. Gordon DM (1989) Dynamics of task switching in harvester ants. Anim Behav 38:194–204Google Scholar
  71. Gordon DM, Mehdiabadi NJ (1999) Encounter rate and task allocation in harvester ants. Behav Ecol Sociobiol 45:370–377Google Scholar
  72. Gordon DM, Chu J, Lillie A, Tissot M, Pinter N (2005) Variation in the transition from inside to outside work in the red harvester ant Pogonomyrmex barbatus. Insect Soc 52:212–217Google Scholar
  73. Hara K (2003) Queen discrimination ability of ant workers (Camponotus japonicus) coincides with brain maturation. Brain Behav Evol 62:56–64PubMedGoogle Scholar
  74. Hartmann A, Heinze J (2003) Lay eggs, live longer: division of labor and life span in a clonal ant species. Evolution 57:2424–2429PubMedGoogle Scholar
  75. Heinze J, Schrempf A (2008) Aging and reproduction in social insects—a mini-review. Gerontology 54:160–167PubMedGoogle Scholar
  76. Heinze J, Walter B (2010) Moribund ants leave their nests to die in social isolation. Curr Biol 20:249–252PubMedGoogle Scholar
  77. Herbers JM (1986) Nest site limitation and facultative polygyny in the ant Leptothorax longispinosus. Behav Ecol Sociobiol 19:115–122Google Scholar
  78. Holbrook CT, Barden PM, Fewell JH (2011) Division of labor increases with colony size in the harvester ant Pogonomyrmex californicus. Behav Ecol 22:960–966Google Scholar
  79. Holbrook CT, Eriksson TH, Overson RP, Gadau J, Fewell JH (2013) Colony-size effects on task organization in the harvester ant Pogonomyrmex californicus. Insect Soc 60:191–201Google Scholar
  80. Hölldobler B, Wilson EO (1978) The multiple recruitment systems of the African weaver ant Oecophylla longinoda (Latreille) (Hymenoptera: Formicidae). Behav Ecol Sociobiol 3:19–60Google Scholar
  81. Hölldobler B, Wilson EO (1990) The ants. Belknap Press of Harvard University Press, CambridgeGoogle Scholar
  82. Hughes WOH, Boomsma JJ (2004) Genetic diversity and disease resistance in leaf-cutting ant societies. Evolution 58:1251–1260PubMedGoogle Scholar
  83. Hughes WOH, Eilenberg J, Boomsma JJ (2002) Trade-offs in group living: transmission and disease resistance in leaf-cutting ants. Proc R Soc Lond B 269:1811–1819Google Scholar
  84. Jeanson R, Fewell JH, Gorelick R, Bertram SM (2007) Emergence of increased division of labor as a function of group size. Behav Ecol Sociobiol 62:289–298Google Scholar
  85. Jemielity S, Chapuisat M, Parker JD, Keller L (2005) Long live the queen: studying aging in social insects. Age 27:241–248PubMedCentralPubMedGoogle Scholar
  86. Kamhi JF, Traniello JFA (2013) Biogenic amines and collective organization in a superorganism: neuromodulation of social behavior in ants. Brain Behav Evol 82:220–236PubMedGoogle Scholar
  87. Kaptein N, Billen J, Gobin B (2005) Larval begging for food enhances reproductive options in the ponerine ant Gnamptogenys striatula. Anim Behav 69:293–299Google Scholar
  88. Kaspari M (1993) Removal of seeds from neotropical frugivore droppings: ant responses to seed number. Oecologia 95:81–88Google Scholar
  89. Kaspari M, Vargo E (1995) Colony size as a buffer against seasonality: Bergmann’s rule in social insects. Am Nat 145:610–632Google Scholar
  90. Keeler KH (1993) Fifteen years of colony dynamics in Pogonomyrmex occidentalis, the western harvester ant, in western Nebraska. Southwest Nat 38:286–289Google Scholar
  91. Keller L (1998) Queen lifespan and colony characteristics in ants and termites. Insect Soc 45:235–246Google Scholar
  92. Keller L, Genoud M (1997) Extraordinary lifespans in ants: a test of evolutionary theories of ageing. Nature 389:3–6Google Scholar
  93. Kern MJ (1985) Metabolic rate of the insect brain in relation to body size and phylogeny. Comp Biochem Physiol A 81A:501–506Google Scholar
  94. Kern M, Wegener G (1984) Age affects the metabolic rate of insect brain. Mech Ageing Dev 28:237–242PubMedGoogle Scholar
  95. Kirkwood TBL (1977) Evolution of ageing. Nature 270:301–304PubMedGoogle Scholar
  96. Kirkwood TBL, Melov S (2011) On the programmed/non-programmed nature of ageing within the life history. Curr Biol 21:R701–R707Google Scholar
  97. Kramer BH, Schaible R (2013) Colony size explains the lifespan differences between queens and workers in eusocial Hymenoptera. Biol J Linn Soc 109:710–724Google Scholar
  98. Kramer BH, Scharf I, Foitzik S (2014) The role of per-capita productivity in the evolution of small colony sizes in ants. Behav Ecol Sociobiol 68:41–53Google Scholar
  99. Kronauer DJC, Johnson RA, Boomsma JJ (2007) The evolution of multiple mating in army ants. Evolution 61:413–422PubMedGoogle Scholar
  100. Kwapich CL, Tschinkel WR (2013) Demography, demand, death, and the seasonal allocation of labor in the Florida harvester ant (Pogonomyrmex badius). Behav Ecol Sociobiol 67:2011–2027Google Scholar
  101. Lacey EA, Sherman PW (1991) Social organization of naked mole-rat colonies: evidence for division of labor. In: Sherman PW, Jarvis JUM, Alexander R (eds) The biology of the naked mole-rat. Princeton University Press, Princeton, pp 275–336Google Scholar
  102. Lee RD (2003) Rethinking the evolutionary theory of aging: transfers, not births, shape senescence in social species. Proc Natl Acad Sci U S A 100:9637–9642PubMedCentralPubMedGoogle Scholar
  103. Lenoir A (1979) Le comportement alimentaire et la division du travail chez la fourmi Lasius niger (L.). Bull Biol Fr Belg 113:79–314Google Scholar
  104. Lewis KN, Mele J, Hornsby PJ, Buffenstein R (2012) Stress resistance in the naked mole-rat: the bare essentials—a mini-review. Gerontology 58:453–462PubMedGoogle Scholar
  105. Libbrecht R, Oxley PR, Kronauer DJ, Keller L (2013) Ant genomics sheds light on the molecular regulation of social organization. Genome Biol 14:212PubMedCentralPubMedGoogle Scholar
  106. London KB, Jeanne RL (2003) Effects of colony size and stage of development on defense response by the swarm-founding wasp Polybia occidentalis. Behav Ecol Sociobiol 54:539–546Google Scholar
  107. Lopes JFS, Hughes WOH, Camargo RS, Forti LC (2005) Larval isolation and brood care in Acromyrmex leaf-cutting ants. Insect Soc 52:333–338Google Scholar
  108. Lucas E, Keller L (2014) Ageing and somatic maintenance in social insects. Curr Op Insect Sci. (published online, doi: 10.1016/j.cois.2014.09.009)
  109. Medawar PB (1952) An unsolved problem of biology. H. K. Lewis, LondonGoogle Scholar
  110. Mersch DP, Crespi A, Keller L (2013) Tracking individuals shows spatial fidelity is a key regulator of ant social organization. Science 340:1090–1093PubMedGoogle Scholar
  111. Morand-Ferron J, Quinn JL (2011) Larger groups of passerines are more efficient problem solvers in the wild. Proc Natl Acad Sci U S A 108:15898–15903PubMedCentralPubMedGoogle Scholar
  112. Moreau CS, Bell CD, Vila R, Archibald SB, Pierce NE (2006) Phylogeny of the ants: diversification in the age of angiosperms. Science 312:101–104PubMedGoogle Scholar
  113. Moroń D, Lenda M, Skórka P, Woyciechowski M (2012) Short-lived ants take greater risks during food collection. Am Nat 180:744–750PubMedGoogle Scholar
  114. Münch D, Amdam GV (2010) The curious case of aging plasticity in honey bees. FEBS Lett 584:2496–2503PubMedGoogle Scholar
  115. 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 22:407–421PubMedCentralPubMedGoogle Scholar
  116. Muscedere ML, Willey TA, Traniello JFA (2009) Age and task efficiency in the ant Pheidole dentata: young minor workers are not specialist nurses. Anim Behav 77:911–918Google Scholar
  117. Muscedere ML, Traniello JFA, Gronenberg W (2011) Coming of age in an ant colony: cephalic muscle maturation accompanies behavioral development in Pheidole dentata. Naturwissenschaften 98:783–793PubMedGoogle Scholar
  118. Muscedere ML, Johnson N, Gillis BC, Kamhi JF, Traniello JFA (2012) Serotonin modulates worker responsiveness to trail pheromone in the ant Pheidole dentata. J Comp Physiol A 198:219–227Google Scholar
  119. Muscedere ML, Djermoun A, Traniello JFA (2013) Brood-care experience, nursing performance, and neural development in the ant Pheidole dentata. Behav Ecol Sociobiol 67:775–784Google Scholar
  120. Nussey DH, Froy H, Lemaitre J-F, Gaillard J-M, Austad SN (2013) Senescence in natural populations of animals: widespread evidence and its implications for bio-gerontology. Ageing Res Rev 12:214–225PubMedGoogle Scholar
  121. O’Donnell S, Bulova SJ (2007) Worker connectivity: a simulation model of variation in worker communication and its effects on task performance. Insect Soc 54:211–218Google Scholar
  122. Oster GF, Wilson EO (1978) Caste and ecology in the social insects. Princeton University Press, PrincetonGoogle Scholar
  123. Parker JD (2010) What are social insects telling us about aging? Myrmecol News 13:103–110Google Scholar
  124. Partridge L, Gems D (2006) Beyond the evolutionary theory of ageing, from functional genomics to evo-gero. Trends Ecol Evol 21:334–340PubMedGoogle Scholar
  125. Passera L, Roncin E, Kaufmann B, Keller L (1996) Increased soldier production in ant colonies exposed to intraspecific competition. Nature 379:630–631Google Scholar
  126. Pie MR, Rosengaus RB, Traniello JFA (2004) Nest architecture, activity pattern, worker density and the dynamics of disease transmission in social insects. J Theor Biol 226:45–51PubMedGoogle Scholar
  127. Porter SD, Jorgensen CD (1981) Foragers of the harvester ant, Pogonomyrmex owyheei: a disposable caste? Behav Ecol Sociobiol 9:247–256Google Scholar
  128. Porter SD, Tschinkel WR (1985) Fire ant polymorphism: the ergonomics of brood production. Behav Ecol Sociobiol 16:323–336Google Scholar
  129. Porter SD, Tschinkel WR (1986) Adaptive value of nanitic workers in newly founded red imported fire ant colonies (Hymenoptera: Formicidae). Ann Entomol Soc Am 79:723–726Google Scholar
  130. Poulsen M, Bot ANM, Nielsen MG, Boomsma JJ (2002) Experimental evidence for the costs and hygienic significance of the antibiotic metapleural ants gland secretion in leaf-cutting ants. Behav Ecol Sociobiol 52:151–157Google Scholar
  131. Powell S (2011) How much do army ants eat? On the prey intake of a neotropical top-predator. Insect Soc 58:317–324Google Scholar
  132. Pratt S, Mallon E, Sumpter D, Franks N (2002) Quorum sensing, recruitment, and collective decision-making during colony emigration by the ant Leptothorax albipennis. Behav Ecol Sociobiol 52:117–127Google Scholar
  133. Purcell J, Brütsch T, Chapuisat M (2011) Effects of the social environment on the survival and fungal resistance of ant brood. Behav Ecol Sociobiol 66:467–474Google Scholar
  134. Rauser CL, Mueller LD, Rose MR (2006) The evolution of late life. Ageing Res Rev 5:14–32PubMedGoogle Scholar
  135. Remolina SC, Hafez DM, Robinson GE, Hughes KA (2007) Senescence in the worker honey bee Apis mellifera. J Insect Physiol 53:1027–1033PubMedCentralPubMedGoogle Scholar
  136. Ricklefs RE (1998) Evolutionary theories of aging: confirmation of a fundamental prediction, with implications for the genetic basis and evolution of life span. Am Nat 152:24–44PubMedGoogle Scholar
  137. Ridley M (1993) Clutch size and mating frequency in parasitic Hymenoptera. Am Nat 142:893–910Google Scholar
  138. Robinson GE (1992) Regulation of division of labor in insect societies. Annu Rev Entomol 37:637–665PubMedGoogle Scholar
  139. Robinson GE, Page R Jr, Huang Z (1994) Temporal polyethism in social insects is a developmental process. Anim Behav 48:467–469Google Scholar
  140. Robinson EJH, Feinerman O, Franks NR (2009) Flexible task allocation and the organization of work in ants. Proc R Soc Lond B 276:4373–4380Google Scholar
  141. Robinson EJH, Feinerman O, Franks NR (2012) Experience, corpulence and decision making in ant foraging. J Exp Biol 215:2653–2659PubMedGoogle Scholar
  142. Robson SK, Beshers SN (1997) Division of labour and “foraging for work”: simulating reality versus the reality of simulations. Anim Behav 53:214–218Google Scholar
  143. Rosengaus RB, Traniello JFA (2001) Disease susceptibility and the adaptive nature of colony demography in the dampwood termite Zootermopsis angusticollis. Behav Ecol Sociobiol 50:546–556Google Scholar
  144. Rosengaus RB, Maxmen AB, Coates LE, Traniello JFA (1998) Disease resistance: a benefit of sociality in the dampwood termite Zootermopsis angusticollis (Isoptera: Termopsidae). Behav Ecol Sociobiol 44:125–134Google Scholar
  145. Rueppell O (2009) Aging of social insects. In: Gadeau J, Fewell J, Wilson EO (eds) Organization of insect societies: from genome to sociocomplexity. Harvard University Press, Cambridge, pp 51–73Google Scholar
  146. Rueppell O, Bachelier C, Fondrk MK, Page RE (2007a) Regulation of life history determines lifespan of worker honey bees (Apis mellifera L.). Exp Gerontol 42:1020–1032PubMedCentralPubMedGoogle Scholar
  147. Rueppell O, Christine S, Mulcrone C, Groves L (2007b) Aging without functional senescence in honey bee workers. Curr Biol 17:R274–R275PubMedCentralPubMedGoogle Scholar
  148. Rueppell O, Kaftanouglu O, Page RE (2009) Honey bee (Apis mellifera) workers live longer in small than large colonies. Exp Gerontol 44:447–452PubMedCentralPubMedGoogle Scholar
  149. Rueppell O, Hayworth MK, Ross NP (2010) Altruistic self-removal of health-compromised honey bee workers from their hive. J Evol Biol 23:1538–1546PubMedGoogle Scholar
  150. Scharf I, Modlmeier AP, Beros S, Foitzik S (2012) Ant societies buffer individual-level effects of parasite infections. Am Nat 180:671–683PubMedGoogle Scholar
  151. Schmid-Hempel P (1983) Foraging ecology and colony structure of two sympatric species of desert ants Cataglyphis bicolor and Cataglyphis albicans. Dissertation, Universität ZürichGoogle Scholar
  152. Schmid-Hempel P (1992) Worker castes and adaptive demography. J Evol Biol 5:1–12Google Scholar
  153. Schmid-Hempel P (1998) Parasites in social insects. Princeton University Press, PrincetonGoogle Scholar
  154. Schmid-Hempel P, Schmid-Hempel R (1984) Life duration and turnover of foragers in the ant Cataglyphis bicolor (Hymenoptera, Formicidae). Insect Soc 31:345–360Google Scholar
  155. Schmid-Hempel P, Kacelnik A, Houston AI (1985) Honeybees maximize efficiency by not filling their crop. Behav Ecol Sociobiol 17:61–66Google Scholar
  156. Schofield RMS, Emmett KD, Niedbala JC, Nesson MH (2011) Leaf-cutter ants with worn mandibles cut half as fast, spend twice the energy, and tend to carry instead of cut. Behav Ecol Sociobiol 65:969–982Google Scholar
  157. Schrempf A, Cremer S, Heinze J (2011) Social influence on age and reproduction: reduced lifespan and fecundity in multi-queen ant colonies. J Evol Biol 24:1455–1461PubMedGoogle Scholar
  158. Schulz DJ, Robinson GE (2001) Octopamine influences division of labor in honey bee colonies. J Comp Physiol A 187:53–61PubMedGoogle Scholar
  159. Sebens KP (1987) The ecology of indeterminant growth in animals. Annu Rev Ecol Syst 18:371–407Google Scholar
  160. Seid MA, Traniello JFA (2005) Age-related changes in biogenic amines in individual brains of the ant Pheidole dentata. Naturwissenschaften 92:198–201PubMedGoogle Scholar
  161. Seid MA, Traniello JFA (2006) Age-related repertoire expansion and division of labor in Pheidole dentata (Hymenoptera: Formicidae): a new perspective on temporal polyethism and behavioral plasticity in ants. Behav Ecol Sociobiol 60:631–644Google Scholar
  162. Sendova-Franks A, Franks NR (1993) Task allocation in ant colonies within variable environments (a study of temporal polyethism: experimental). Bull Math Biol 55:75–96Google Scholar
  163. Sendova-Franks AB, Franks NR (1995) Spatial relationships within nests of the ant Leptothorax unifasciatus (Latr.) and their implications for division of labor. Anim Behav 50:121–136Google Scholar
  164. Shahrestani P, Mueller LD, Rose MD (2009) Does aging stop? Curr Aging Sci 2:3–11PubMedGoogle Scholar
  165. Shik JZ (2008) Ant colony size and the scaling of reproductive effort. Funct Ecol 22:674–681Google Scholar
  166. Shik JZ (2010) The metabolic costs of building ant colonies from variably sized subunits. Behav Ecol Sociobiol 64:1981–1990Google Scholar
  167. Shik JZ, Hou C, Kay A, Kaspari M, Gillooly JF (2012) Towards a general life-history model of the superorganism: predicting the survival, growth and reproduction of ant societies. Biol Lett 8:1059–1062PubMedCentralPubMedGoogle Scholar
  168. Simons AM (2004) Many wrongs: the advantage of group navigation. Trends Ecol Evol 19:453–455PubMedGoogle Scholar
  169. Smith AR, Muscedere ML, Seid MA, Traniello JFA, Hughes WOH (2013) Biogenic amines are associated with worker task but not patriline in the leaf-cutting ant Acromyrmex echinatior. J Comp Physiol A 199:1117–1127Google Scholar
  170. Tanner CJ (2006) Numerical assessment affects aggression and competitive ability: a team-fighting strategy for the ant Formica xerophila. Proc R Soc Lond B 273:2737–2742Google Scholar
  171. Tarpy DR (2003) Genetic diversity within honeybee colonies prevents severe infections and promotes colony growth. Proc R Soc Lond B 270:99–103Google Scholar
  172. Thomas ML, Elgar MA (2003) Colony size affects division of labour in the ponerine ant Rhytidoponera metallica. Naturwissenschaften 90:88–92PubMedGoogle Scholar
  173. Tofilski A (2000) Senescence and learning in honeybee (Apis mellifera) workers. Acta Neurobiol Exp 60:35–39Google Scholar
  174. Tofts C, Franks NR (1992) Doing the right thing: ants, honeybees and naked mole-rats. Trends Ecol Evol 7:346–349PubMedGoogle Scholar
  175. Toth AL, Robinson GE (2007) Evo-devo and the evolution of social behavior. Trends Genet 23:334–341PubMedGoogle Scholar
  176. Traniello JFA, Rosengaus RB (1997) Ecology, evolution and division of labour in social insects. Anim Behav 53:209–213Google Scholar
  177. Traniello IM, Sîrbulescu RF, Ilieş I, Zupanc GKH (2013) Age-related changes in stem cell dynamics, neurogenesis, apoptosis, and gliosis in the adult brain: a novel teleost fish model of negligible senescence. Dev Neurobiol 74:514–530PubMedGoogle Scholar
  178. Tschinkel WR (1987) Fire ant queen longevity and age: estimation by sperm depletion. Ann Entomol Soc Am 80:263–266Google Scholar
  179. Tschinkel WR (1988) Social control of egg-laying rate in queens of the fire ant, Solenopsis invicta. Physiol Entomol 13:327–350Google Scholar
  180. Tschinkel WR (1993) Sociometry and sociogenesis of colonies of the fire ant Solenopsis invicta during one annual cycle. Ecol Monogr 63:425–457Google Scholar
  181. Tsuji K, Nakata K, Heinze J (1996) Lifespan and reproduction in a queenless ant. Naturwissenschaften 83:577–578Google Scholar
  182. Turon X, Becerro MA (1992) Growth and survival of several ascidian species from the northwest Mediterranean. Mar Ecol Prog Ser 82:235–247Google Scholar
  183. Ugelvig LV, Kronauer DJC, Schrempf A, Heinze J, Cremer S (2010) Rapid anti-pathogen response in ant societies relies on high genetic diversity. Proc R Soc Lond B 277:2821–2828Google Scholar
  184. Vance JT, Williams JB, Elekonich MM, Roberts SP (2009) The effects of age and behavioral development on honey bee (Apis mellifera) flight performance. J Exp Biol 212:2604–2611PubMedCentralPubMedGoogle Scholar
  185. Vaquero A, Reinberg D (2009) Calorie restriction and the exercise of chromatin. Genes Dev 23:1849–1869PubMedCentralPubMedGoogle Scholar
  186. Vargo EL (1988) Effect of pleometrosis and colony size on the production of sexuals in monogyne colonies of the fire ant Solenopsis invicta. In: Trager JC (ed) Advances in myrmecology. E. J. Brill, New York, pp 217–225Google Scholar
  187. Walker J, Stamps J (1986) A test of optimal caste ratio theory using the ant Camponotus (Colobopsis) impressus. Ecology 67:1052–1062Google Scholar
  188. Wehner R, Meier C, Zollikofer C (2004) The ontogeny of foraging behaviour in desert ants, Cataglyphis bicolor. Ecol Entomol 29:240–250Google Scholar
  189. Weier J, Feener D (1995) Foraging in the seed-harvester ant genus Pogonomyrmex: are energy costs important? Behav Ecol Sociobiol 36:291–300Google Scholar
  190. Williams GC (1957) Pleiotropy, natural selection, and the evolution of senescence. Evolution 11:398–411Google Scholar
  191. Williams GC (1999) The Tithonus error in modern gerontology. Q Rev Biol 74:405–415PubMedGoogle Scholar
  192. Williams JB, Roberts SP, Elekonich MM (2008) Age and natural metabolically-intensive behavior affect oxidative stress and antioxidant mechanisms. Exp Gerontol 43:538–549PubMedGoogle Scholar
  193. Wilson EO (1959) Some ecological characteristics of ants in New Guinea rain forests. Ecology 40:437–447Google Scholar
  194. Wilson EO (1971) The insect societies. Oxford University Press, LondonGoogle Scholar
  195. Wilson EO (1976a) Behavioral discretization and the number of castes in an ant species. Behav Ecol Sociobiol 154:141–154Google Scholar
  196. Wilson EO (1976b) The organization of colony defense in the ant Pheidole dentata Mayr (Hymenoptera: Formicidae). Behav Ecol Sociobiol 1:63–81Google Scholar
  197. Wilson EO (1983a) Caste and division of labor in leaf-cutter ants (Hymenoptera: Formicidae: Atta): IV. Colony ontogeny of A. cephalotes. Behav Ecol Sociobiol 14:55–60Google Scholar
  198. Wilson EO (1983b) Caste and division of labor in leaf-cutter ants (Hymenoptera: Formicidae: Atta): III. Ergonomic resiliency in foraging by A. cephalotes. Behav Ecol Sociobiol 14:47–54Google Scholar
  199. Wilson EO (1985) The sociogenesis of insect colonies. Science 228:1489–1495PubMedGoogle Scholar
  200. Wilson-Rich N, Spivak M, Fefferman NH, Starks PT (2009) Genetic, individual, and group facilitation of disease resistance in insect societies. Annu Rev Entomol 54:405–423PubMedGoogle Scholar
  201. Wolf H (2008) Desert ants adjust their approach to a foraging site according to experience. Behav Ecol Sociobiol 62:415–425Google Scholar
  202. Yang AS (2006) Seasonality, division of labor, and dynamics of colony-level nutrient storage in the ant Pheidole morrisi. Insect Soc 53:456–462Google Scholar
  203. Yang AS, Martin CH, Nijhout HF (2004) Geographic variation of caste structure among ant populations. Curr Biol 14:514–519PubMedGoogle Scholar
  204. Yek SH, Mueller UG (2011) The metapleural gland of ants. Biol Rev Camb Philos Soc 86:774–791PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Ysabel Milton Giraldo
    • 1
    • 2
  • James F. A. Traniello
    • 1
  1. 1.Department of BiologyBoston UniversityBostonUSA
  2. 2.Department of NeurobiologyHarvard Medical SchoolBostonUSA

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