Queens stay, workers leave: caste-specific responses to fatal infections in an ant.

Julia Giehr, Jürgen Heinze
Author Information
  1. Julia Giehr: Department of Zoology/ Evolutionary Biology, University of Regensburg, 93053, Regensburg, Germany. Julia.Giehr@ur.de. ORCID
  2. Jürgen Heinze: Department of Zoology/ Evolutionary Biology, University of Regensburg, 93053, Regensburg, Germany.

Abstract

BACKGROUND: The intense interactions among closely related individuals in animal societies provide perfect conditions for the spread of pathogens. Social insects have therefore evolved counter-measures on the cellular, individual, and social level to reduce the infection risk. One striking example is altruistic self-removal, i.e., lethally infected workers leave the nest and die in isolation to prevent the spread of a contagious disease to their nestmates. Because reproductive queens and egg-laying workers behave less altruistically than non-laying workers, e.g., when it comes to colony defense, we wondered whether moribund egg-layers would show the same self-removal as non-reproductive workers. Furthermore, we investigated how a lethal infection affects reproduction and studied if queens and egg-laying workers intensify their reproductive efforts when their residual reproductive value decreases ("terminal investment").
RESULTS: We treated queens, egg-laying workers from queenless colonies, and non-laying workers from queenright colonies of the monogynous (single-queened) ant Temnothorax crassispinus either with a control solution or a solution containing spores of the entomopathogenic fungus Metarhizium brunneum. Lethally infected workers left the nest and died away from it, regardless of their reproductive status. In contrast, infected queens never left the nest and were removed by workers only after they had died. The reproductive investment of queens strongly decreased after the treatment with both, the control solution and the Metarhizium brunneum suspension. The egg laying rate in queenless colonies was initially reduced in infected colonies but not in control colonies. Egg number increased again with decreasing number of infected workers.
CONCLUSIONS: Queens and workers of the ant Temnothorax crassispinus differ in their reaction to an infection risk and a reduced life expectancy. Workers isolate themselves to prevent contagion inside the colony, whereas queens stay in the nest. We did not find terminal investment; instead it appeared that egg-layers completely shut down egg production in response to the lethal infection. Workers in queenless colonies resumed reproduction only after all infected individuals had died, probably again to minimize the risk of infecting the offspring.

Keywords

References

  1. Naturwissenschaften. 2016 Aug;103(7-8):70 [PMID: 27475810]
  2. Evolution. 2015 Nov;69(11):2979-84 [PMID: 26283006]
  3. J Evol Biol. 2012 Feb;25(2):342-51 [PMID: 22122288]
  4. Behav Ecol Sociobiol. 2017 Dec;71(12): [PMID: 30002566]
  5. Mol Ecol. 2016 May;25(9):1972-85 [PMID: 26880273]
  6. Science. 1981 Apr 3;212(4490):83-4 [PMID: 17747635]
  7. J Econ Entomol. 2012 Dec;105(6):1895-902 [PMID: 23356051]
  8. Curr Biol. 2013 Aug 19;23(16):1574-8 [PMID: 23910660]
  9. Insectes Soc. 2005 Aug;52(3):282-290 [PMID: 18521192]
  10. Proc Biol Sci. 2011 Nov 22;278(1723):3313-20 [PMID: 21920980]
  11. Sci Rep. 2016 Aug 31;6:31430 [PMID: 27578396]
  12. J Invertebr Pathol. 2004 Jan;85(1):46-53 [PMID: 14992860]
  13. Proc Biol Sci. 2001 Sep 22;268(1479):1959-64 [PMID: 11564355]
  14. J Insect Physiol. 2012 Dec;58(12):1589-96 [PMID: 23068993]
  15. Curr Biol. 2007 Aug 21;17(16):R693-702 [PMID: 17714663]
  16. Curr Biol. 2005 Feb 8;15(3):267-70 [PMID: 15694312]
  17. Elife. 2018 Jan 09;7: [PMID: 29310753]
  18. Biol Lett. 2010 Jun 23;6(3):329-32 [PMID: 20071394]
  19. J Evol Biol. 2010 Jul;23(7):1538-46 [PMID: 20500363]
  20. Annu Rev Entomol. 2009;54:405-23 [PMID: 18793100]
  21. Environ Microbiol. 2005 Sep;7(9):1361-8 [PMID: 16104859]
  22. Annu Rev Entomol. 2018 Jan 7;63:105-123 [PMID: 28945976]
  23. Mol Ecol. 2007 Feb;16(3):675-83 [PMID: 17257122]
  24. Proc Biol Sci. 2002 Sep 7;269(1502):1811-9 [PMID: 12350269]
  25. Proc Natl Acad Sci U S A. 2002 May 14;99(10):6838-42 [PMID: 12011442]
  26. Anim Behav. 1997 Oct;54(4):849-64 [PMID: 9344438]
  27. Annu Rev Entomol. 2016;61:297-316 [PMID: 26667274]
  28. Curr Biol. 2010 Feb 9;20(3):249-52 [PMID: 20116243]
  29. Proc Biol Sci. 2017 Mar 15;284(1850): [PMID: 28298341]
  30. Curr Biol. 2006 Jul 11;16(13):R482-3 [PMID: 16824903]
  31. J Invertebr Pathol. 2008 Jun;98(2):198-205 [PMID: 18280493]
  32. Zookeys. 2018 Apr 19;(751):1-40 [PMID: 29706783]
  33. R Soc Open Sci. 2017 Jul 5;4(7):170547 [PMID: 28791176]
  34. Naturwissenschaften. 2013 Dec;100(12):1125-36 [PMID: 24233126]
  35. J Invertebr Pathol. 2011 Mar;106(3):380-5 [PMID: 21156180]
  36. PLoS One. 2013 Nov 15;8(11):e81518 [PMID: 24260580]
  37. Toxicon. 2010 Dec 15;56(7):1267-74 [PMID: 20298710]

MeSH Term

Altruism
Animals
Ants
Behavior, Animal
Female
Fertility
Metarhizium
Oviposition
Reproduction
Social Behavior

Word Cloud

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