The Science of Nature

, 104:34 | Cite as

Intrinsic worker mortality depends on behavioral caste and the queens’ presence in a social insect

  • Philip Kohlmeier
  • Matteo Antoine Negroni
  • Marion Kever
  • Stefanie Emmling
  • Heike Stypa
  • Barbara Feldmeyer
  • Susanne Foitzik
Original Paper

Abstract

According to the classic life history theory, selection for longevity depends on age-dependant extrinsic mortality and fecundity. In social insects, the common life history trade-off between fecundity and longevity appears to be reversed, as the most fecund individual, the queen, often exceeds workers in lifespan several fold. But does fecundity directly affect intrinsic mortality also in social insect workers? And what is the effect of task on worker mortality? Here, we studied how social environment and behavioral caste affect intrinsic mortality of ant workers. We compared worker survival between queenless and queenright Temnothorax longispinosus nests and demonstrate that workers survive longer under the queens’ absence. Temnothorax ant workers fight over reproduction when the queen is absent and dominant workers lay eggs. Worker fertility might therefore increase lifespan, possibly due to a positive physiological link between fecundity and longevity, or better care for fertile workers. In social insects, division of labor among workers is age-dependant with young workers caring for the brood and old ones going out to forage. We therefore expected nurses to survive longer than foragers, which is what we found. Surprisingly, inactive inside workers showed a lower survival than nurses but comparable to that of foragers. The reduced longevity of inactive workers could be due to them being older than the nurses, or due to a positive effect of activity on lifespan. Overall, our study points to behavioral caste-dependent intrinsic mortality rates and a positive association between fertility and longevity not only in queens but also in ant workers.

Keywords

Division of labor Intrinsic mortality Life history Trade-offs Fecundity Survival Social insects 

References

  1. Alloway TM, Buschinger A, Talbot M, Stuart R, Thomas C (1982) Polygyny and polydomy in three North American species of the ant genus Leptothorax Mayr (Hymenoptera: Formicidae). Psyche 89:249–274CrossRefGoogle Scholar
  2. Amdam GV, Nilsen KA, Norberg K, Fondrk MK, Hartfelder K (2007) Variation in endocrine signaling underlies variation in social life history. Am Nat 170:37–46CrossRefPubMedPubMedCentralGoogle Scholar
  3. Bernadou A, Busch J, Heinze J (2015) Diversity in identity: behavioral flexibility, dominance, and age polyethism in a clonal ant. Behav Ecol Sociobiol 69:1365–1375CrossRefGoogle Scholar
  4. Bocher A, Tirard C, Doums C (2007) Phenotypic plasticity of immune defence linked with foraging activity in the ant Cataglyphis velox. J Evol Biol 20:2228–2234CrossRefPubMedGoogle Scholar
  5. Bourke AFG (1988) Worker reproduction in the higher eusocial Hymenoptera. Q Rev Biol 63:291–311CrossRefGoogle Scholar
  6. Bourke AF, Franks NR (1995) Social evolution in ants. Princeton University Press, PrincetonGoogle Scholar
  7. 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 35:643–649CrossRefGoogle Scholar
  8. Chapuisat M, Keller L (2002) Division of labour influences the rate of ageing in weaver ant workers. P Roy Soc B 269:909–913CrossRefGoogle Scholar
  9. Charbonneau D, Dornhaus A (2015) Workers ‘specialized’ on inactivity: behavioral consistency of inactive workers and their role in task allocation. Behav Ecol Sociobiol 69:1459–1472CrossRefGoogle Scholar
  10. Charbonneau D, Hillis N, Dornhaus A (2015) ‘Lazy’ in nature: ant colony time budgets show high ‘inactivity’ in the field as well as in the lab. Insect Soc 62:31–35CrossRefGoogle Scholar
  11. Choe JC (1988) Worker reproduction and social evolution in ants (Hymenoptera: Formicidae). In: Trager JC (ed) Advances in myrmecology. Brill, New York, pp 163–187Google Scholar
  12. Cole BJ (1986) The social behavior of Leptothorax allardycei (Hymenoptera, Formicidae): time budgets and the evolution of worker reproduction. Behav Ecol Sociobiol 18:165–173CrossRefGoogle Scholar
  13. Colgan TJ, Carolan JC, Bridgett SJ et al (2011) Polyphenism in social insects: insights from a transcriptome-wide analysis of gene expression in the life stages of the key pollinator, Bombus terrestris. BMC Genomics 12:623CrossRefPubMedPubMedCentralGoogle Scholar
  14. Corbara B, Lachaud JP, Fresneau D (1989) Individual variability, social structure and division of labour in the ponerine ant Ectatomma ruidum Roger (Hymenoptera, Formicidae). Ethology 82:89–100CrossRefGoogle Scholar
  15. Corona M, Velarde RA, Remolina S et al (2007) Vitellogenin, juvenile hormone, insulin signaling, and queen honey bee longevity. P Natl Acad Sci USA 104:7128–7133CrossRefGoogle Scholar
  16. Cuvillier-Hot V, Lenoir A, Crewe R, Malosse C, Peeters C (2004) Fertility signalling and reproductive skew in queenless ants. Anim Behav 68:1209–1219CrossRefGoogle Scholar
  17. D'Ettorre P, Heinze J, Schulz C, Francke W, Ayasse M (2004) Does she smell like a queen? Chemoreception of a cuticular hydrocarbon signal in the ant Pachycondyla inversa. J Exp Biol 207:1085–1091CrossRefPubMedGoogle Scholar
  18. Dixon L, Kuster R, Rueppell O (2014) Reproduction, social behavior, and aging trajectories in honeybee workers. Age 36:89–101CrossRefPubMedGoogle Scholar
  19. Dussutour A, Poissonnier LA, Buhl J, Simpson SJ (2016) Resistance to nutritional stress in ants: when being fat is advantageous. J Exp Biol 219:824–833CrossRefPubMedGoogle Scholar
  20. Feldmeyer B, Elsner D, Foitzik S (2014) Gene expression patterns associated with caste and reproductive status in ants: worker-specific genes are more derived than queen-specific ones. Mol Ecol 23:151–161CrossRefPubMedGoogle Scholar
  21. Ferreira PG, Patalano S, Chauhan R, Ffrench-Constant R, Gabaldón T, Guigó R, Sumner S (2013) Transcriptome analyses of primitively eusocial wasps reveal novel insights into the evolution of sociality and the origin of alternative phenotypes. Genome Biol 14:R20CrossRefPubMedPubMedCentralGoogle Scholar
  22. Finch CE (1990) Longevity senescence and the genome. Chicago University Press, Chicago and LondonGoogle Scholar
  23. Foitzik S, Heinze J (1998) Nest site limitation and colony takeover in the ant Leptothorax nylanderi. Behav Ecol 9:367–375Google Scholar
  24. Fresneau D (1984) Développement ovarien et statut social chez une fourmi primitive Neoponera obscuricornis Emery (Hym. Formicidae, Ponerinae). Insect Soc 31:387–402CrossRefGoogle Scholar
  25. Giraldo YM, Traniello JFA (2014) Worker senescence and the sociobiology of aging in ants. Behav Evol Sociobiol 68:1901–1919CrossRefGoogle Scholar
  26. Giraldo YM, Kamhi JF, Fourcassié V et al (2016) Lifespan behavioural and neural resilience in a social insect. Proc Roy Soc B 283:2015–2603CrossRefGoogle Scholar
  27. Graeff J, Jemielity S, Parker JD, Parker KM, Keller L (2007) Differential gene expression between adult queens and workers in the ant Lasius niger. Mol Ecol 16:675–683CrossRefGoogle Scholar
  28. Harrison MC, Hammond RL, Mallon EB (2015) Reproductive workers show queenlike gene expression in an intermediately eusocial insect, the bufftailed bumble bee Bombus terrestris. Mol Ecol 24:3043–3063CrossRefPubMedGoogle Scholar
  29. Hartmann A, Heinze J (2003) Lay eggs, live longer: division of labor and life span in a clonal ant species. Evolution 57:2424–2429CrossRefPubMedGoogle Scholar
  30. Heinze J, Schrempf A (2008) Aging and reproduction in social insects—a mini-review. Gerontology 54:160–167CrossRefPubMedGoogle Scholar
  31. Heinze J, Schrempf A (2012) Terminal investment: individual reproduction of ant queens increases with age. PLoS One 7:e35201CrossRefPubMedPubMedCentralGoogle Scholar
  32. Heinze J, Puchinger W, Hölldobler B (1997) Worker reproduction and social hierarchies in Leptothorax ants. Anim Behav 54:849–864CrossRefPubMedGoogle Scholar
  33. Heinze J, Stengl B, Sledge MF (2002) Worker rank, reproductive status and cuticular hydrocarbon signature in the ant, Pachycondyla cf. inversa. Behav Evol Sociobiol 52:59–65CrossRefGoogle Scholar
  34. Heinze J, Frohschammer S, Bernadou A (2013) Queen life-span and total reproductive success are positively associated in the ant Cardiocondyla cf. kagutsuchi. Behav Ecol Sociobiol 67:1555–1562CrossRefGoogle Scholar
  35. Helft F, Tirard C, Doums C (2012) Effects of division of labour on immunity in workers of the ant Cataglyphis cursor. Insect Soc 59:333–340CrossRefGoogle Scholar
  36. Higashi S, Ito F, Sugiura N, Ohkawara K (1994) Worker's age regulates the linear dominance hierarchy in the queenless ponerine ant, Pachycondyla sublaevis (Hymenoptera: Formicidae). Anim Behav 47:179–184CrossRefGoogle Scholar
  37. Hölldobler B, Wilson EO (1990) The ants. Belknap Press of Harvard Univ. Press, CambridgeCrossRefGoogle Scholar
  38. Holliday R (2006) Aging is no longer an unsolved problem in biology. Annals New York Academy of Sciences 1067:1–9CrossRefGoogle Scholar
  39. Jaisson P, Fresneau D, Lachaud JP (1988) Individual traits of social behavior in ants. In: Jeanne RL (ed) Interindividual behavioral variability in social insects. Boulder Westview Press, Boulder, pp 1–51Google Scholar
  40. Jandt JM, Dornhaus A (2011) Competition and cooperation: bumblebee spatial organization and division of labor may affect worker reproduction late in life. Behav Ecol Sociobiol 65:2341–2349CrossRefGoogle Scholar
  41. Jeanne RL (1986) The evolution of the organization of work in social insects. Ital J Zool 20:119–133Google Scholar
  42. Jemielity S, Chapuisat M, Parker JD, Keller L (2005) Long live the queen: studying aging in social insects. Age 27:241–248CrossRefPubMedPubMedCentralGoogle Scholar
  43. Johnson BR (2008) Global information sampling in the honey bee. Naturwissenschaften 95:523–530CrossRefPubMedGoogle Scholar
  44. Keller L (1998) Queen lifespan and colony characteristics in ants and termites. Insect Soc 45:235–246CrossRefGoogle Scholar
  45. Keller L, Genoud M (1997) Extraordinary lifespans in ants: a test of evolutionary theories of ageing. Nature 389:958–960CrossRefGoogle Scholar
  46. Kirkwood TBL, Rose MR (1991) Evolution of senescence: late survival sacrificed for reproduction. Philos T R Soc B 332:15–24CrossRefGoogle Scholar
  47. Klein BA, Olzsowy KM, Klein A, Saunders KM, Seeley TD (2008) Caste-dependent sleep of worker honey bees. J Exp Biol 211:3028–3040CrossRefPubMedGoogle Scholar
  48. Konrad M, Pamminger T, Foitzik S (2012) Two pathways ensuring social harmony. Naturwissenschaften 99:627–636CrossRefPubMedGoogle Scholar
  49. Kramer BH, Schaible R (2013) Life span evolution in eusocial workers—a theoretical approach to understanding the effects of extrinsic mortality in a hierarchical system. PLoS One 8:e61813CrossRefPubMedPubMedCentralGoogle Scholar
  50. Kramer BH, Scharf I, Foitzik S (2014) The role of per-capita productivity in the evolution of small colony sizes in ants. Behav Evol Sociobiol 68:41–53CrossRefGoogle Scholar
  51. Kramer BH, Schrempf A, Scheuerlein A, Heinze J (2015) Ant colonies do not trade-off reproduction against maintenance. PLoS One 10:e0137969CrossRefPubMedPubMedCentralGoogle Scholar
  52. Libbrecht R, Oxley PR, Kronauer DJC, Keller L (2013) Ant genomics sheds light on the molecular regulation of social organization. Genome Biol 14:212CrossRefPubMedPubMedCentralGoogle Scholar
  53. Lighton JR, Bartholomew GA, Feener DH (1987) Energetics of locomotion and load carriage and a model of the energy cost of foraging in the leaf-cutting ant Atta colombica Guer. Physiol Zool 60:524–537CrossRefGoogle Scholar
  54. Medawar P (1952) An unsolved problem in biology. HK Lewis and company, LondonGoogle Scholar
  55. Mersch DP, Crespi A, Keller L (2013) Tracking individuals shows spatial fidelity is a key regulator of ant social organization. Science 340:1090–1093CrossRefPubMedGoogle Scholar
  56. Negroni M, Jongepier E, Feldmeyer B, Kramer BH, Foitzik S (2016) Life history evolution in social insects: a female perspective. Curr Opin Insect Sci 16:51–57CrossRefPubMedGoogle Scholar
  57. O'Donnell S, Jeanne RL (1992) Lifelong patterns of forager behavior in a tropical swarm-founding wasp: effects of specialization and activity level on longevity. Anim Behav 44:1021–1027CrossRefGoogle Scholar
  58. Oettler J, Schrempf A (2016) Fitness and aging in Cardiocondyla obscurior ant queens. Curr Opin Insect Sci 16:58–63CrossRefPubMedGoogle Scholar
  59. Pamminger T, Foitzik S, Kaufmann K, Menzel F (2014) Worker personality and its association with spatially structured division of labor. PLoS One 9:e79616CrossRefPubMedPubMedCentralGoogle Scholar
  60. Plateaux L (1986) Comparison des cycles saisonniers, des durees des societes et des production des trois especes de fourmis Leptothorax (Myrafant) du groupe nylanderi. Actes Coll Ins Soc 3:221–234Google Scholar
  61. Promislow DE, Harvey PH (1990) Living fast and dying young: a comparative analysis of life-history variation among mammals. J Zool 220:417–437CrossRefGoogle Scholar
  62. Prothero J, Jürgens KD (1987) Scaling of maximal lifespan in mammals: a review. In: Woodhead AD, Thompson KH (eds) Evolution of longevity in animals. Plenum Press, New York, pp 49–74CrossRefGoogle Scholar
  63. Retana J, Cerdá X (1990) Social Organization of Cataglyphis cursor ant colonies (Hymenoptera, Formicidae): inter- and intraspecific comparisons. Ethology 84:105–122CrossRefGoogle Scholar
  64. Roff DA (1992) The evolution of life histories: theory and analysis. Chapman and Hall, LondonGoogle Scholar
  65. Rüppell O, Christine S, Mulcrone C, Groves L (2007) Aging without functional senescence in honey bee workers. Curr Biol 17:R274CrossRefGoogle Scholar
  66. Rüppell O, Königseder F, Heinze J, Schrempf A (2015) Intrinsic survival advantage of social insect queens depends on reproductive activation. J Evol Biol 28:2349–2354CrossRefGoogle Scholar
  67. Schmid-Hempel P, Schmid-Hempel R (1984) Life duration and turnover of foragers in the ant Cataglyphis bicolor (Hymenoptera, Formicidae). Insect Soc 31:345–360CrossRefGoogle Scholar
  68. Schmid-Hempel P, Wolf T (1988) Foraging effort and life span of workers in a social insect. J Anim Ecol 57:500–521CrossRefGoogle Scholar
  69. Schrempf A, Heinze J, Cremer S (2005) Sexual cooperation: mating increases longevity in ant queens. Curr Biol 15:267–270PubMedGoogle Scholar
  70. Shattuck MR, Williams SA (2010) Arboreality has allowed for the evolution of increased longevity in mammals. PNAS 107:4635–4639CrossRefPubMedPubMedCentralGoogle Scholar
  71. Sohal RS (1986) The rate of living theory: a contemporary interpretation. In: Collatz KG, Sohal RS (eds) Insect aging. Springer, Berlin, pp 23–44CrossRefGoogle Scholar
  72. Solis CR, Strassmann JE (1990) Presence of brood affects caste differentiation in the social wasp, Polistes exclamans Viereck (Hymenoptera: Vespidae). Funct Ecol 4:531–541CrossRefGoogle Scholar
  73. Sparkman AM, Arnold SJ, Bronikowski AM (2007) An empirical test of evolutionary theories for reproductive senescence and reproductive effort in the garter snake Thamnophis elegans. Proc Roy Soc B 274:943–950CrossRefGoogle Scholar
  74. Stearns SC (1992) The evolution of life histories. Oxford Univ. Press, OxfordGoogle Scholar
  75. Trout WE, Kaplan WD (1970) A relation between longevity, metabolic rate, and activity in shaker mutants of Drosophila melanogaster. Exp Gerontol 5:83–92CrossRefPubMedGoogle Scholar
  76. Tsuji K (1990) Reproductive division of labour related to age in the Japanese queenless ant, Pristomyrmex pungens. Anim Behav 39:843–849CrossRefGoogle Scholar
  77. Tsuji K, Nakata K, Heinze J (1996) Ants, age and reproduction. Naturwissenschaften 83:577–578CrossRefGoogle Scholar
  78. Van Doorn A, Heringa J (1986) The ontogeny of a dominance hierarchy in colonies of the bumblebee Bombus terrestris (Hymenoptera, Apidae). Insect Soc 33:3–25CrossRefGoogle Scholar
  79. Von Wyschetzki K, Rüppell O, Oettler J, Heinze J (2015) Transcriptomic signatures mirror the lack of the fecundity/longevity trade-off in ant queens. Mol Biol Evol 32:3173–3185PubMedPubMedCentralGoogle Scholar
  80. Wachter KW, Finch CE (1997) Between Zeus and the Salmon. The Biodemography of longevity. National Academy Press, WashingtonGoogle Scholar
  81. Wakano JY, Nakata K, Yamamura N (1998) Dynamic model of optimal age polyethism in social insects under stable and fluctuating environments. J Theor Biol 193:153–165CrossRefGoogle Scholar
  82. Wheeler DE (1986) Developmental and physiological determinants of caste in social Hymenoptera: evolutionary implications. Am Nat 128:13–34CrossRefGoogle Scholar
  83. Williams GC (1957) Pleiotropy, natural selection and the evolution of senescence. Evolution 11:398–411CrossRefGoogle Scholar
  84. Wilson EO (1971) The insect societies. Harvard University Press, CambridgeGoogle Scholar
  85. Wolf TJ, Schmid-Hempel P (1989) Extra loads and foraging life span in honeybee workers. J Anim Ecol 58:943–954CrossRefGoogle Scholar
  86. Woyciechowski M, Moroń D (2009) Life expectancy and onset of foraging in the honeybee (Apis mellifera). Insect Soc 56:193–201CrossRefGoogle Scholar
  87. Wurm Y, Wang J, Keller L (2010) Changes in reproductive roles are associated with changes in gene expression in fire ant queens. Mol Ecol 19:1200–1211CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  • Philip Kohlmeier
    • 1
  • Matteo Antoine Negroni
    • 1
  • Marion Kever
    • 1
  • Stefanie Emmling
    • 1
  • Heike Stypa
    • 1
  • Barbara Feldmeyer
    • 2
  • Susanne Foitzik
    • 1
  1. 1.Institute of Organismic and Molecular EvolutionJohannes Gutenberg University MainzMainzGermany
  2. 2.Senckenberg Biodiversity and Climate Research Centre, Senckenberg Gesellschaft für NaturforschungFrankfurt am MainGermany

Personalised recommendations