Are queen ants inhibited by their own pheromone? Regulation of productivity via negative feedback

Behavioral Ecology

Volumn 24, Issue 2, 2013, Pages 380-385

  Holman, Luke ^a,b   Leroy, Chloé ^c   Jørgensen, Charlotte ^b   Nielsen, John ^b   D'Ettorre, Patrizia ^b,c  

^a AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c UNIVERSITÉ PARIS 13   (France)

Author keywords

Cuticular hydrocarbons; Fertility signal; Larvae; Lasius niger; Social physiology

Indexed keywords

ANT; BEHAVIORAL RESPONSE; COLONY; CUTICLE; FECUNDITY; HYDROCARBON; INHIBITION; LARVA; PHEROMONE; PHYSIOLOGY; QUEEN; SIGNAL; SOCIAL INSECT; WORKER CASTE;

FORMICIDAE; HEXAPODA; LASIUS NIGER;

EID: 84876573099     PISSN: 10452249     EISSN: 14657279     Source Type: Journal    
DOI: 10.1093/beheco/ars174     Document Type: Article

References (43)

1. Adams ES, Balas MT. 1999. Worker discrimination among queens in newly founded colonies of the fire ant Solenopsis invicta. Behav Ecol Sociobiol. 45:330-338.
2. Blomquist GC, Bagnères AG, editors. 2010. Insect hydrocarbons: biology, biochemistry and chemical ecology. Cambridge (UK): Cambridge University Press.
3. Bonasio R, Zhang GJ, Ye CY, Mutti NS, Fang XD, Qin N, Donahue G, Yang PC, Li QY, Li C, et al. 2010. Genomic comparison of the ants Camponotus floridanus and Harpegnathos saltator. Science. 329:1068-1071.
4. Cheron B, Doums C, Federici P, Monnin T. 2009. Queen replacement in the monogynous ant Aphaenogaster senilis: supernumerary queens as life insurance. Anim Behav. 78:1317-1325.
5. Crespi BJ. 2001. The evolution of social behavior in microorganisms. Trends Ecol Evol. 16:178-183.
6. Cuvillier-Hot V, Lenoir A, Crewe R, Malosse C, Peeters C. 2004a. Fertility signalling and reproductive skew in queenless ants. Anim Behav. 68:1209-1219.
7. Cuvillier-Hot V, Lenoir A, Peeters C. 2004b. Reproductive monopoly enforced by sterile police workers in a queenless ant. Behav Ecol. 15:970-975.
8. Dietemann V, Peeters C, Liebig J, Thivet V, Hölldobler B. 2003. Cuticular hydrocarbons mediate discrimination of reproductives and nonreproductives in the ant Myrmecia gulosa. Proc Natl Acad Sci USA. 100:10341-10346.
9. Endler A, Liebig J, Schmitt T, Parker JE, Jones GR, Schreier P, Hölldobler B. 2004. Surface hydrocarbons of queen eggs regulate worker reproduction in a social insect. Proc Natl Acad Sci USA. 101:2945-2950.
10. Grozinger CM, Sharabash NM, Whitfield CW, Robinson GE. 2003. Pheromone-mediated gene expression in the honey bee brain. Proc Natl Acad Sci USA. 100:14519-14525.
11. Holman L. 2012. Costs and constraints conspire to produce honest signalling: insights from an ant queen pheromone. Evolution. 66:2094-2105.
12. Holman L, Dreier S, d'Ettorre P. 2010a. Selfish strategies and honest signalling: reproductive conflicts in ant queen associations. Proc R Soc B Biol Sci. 277:2007-2015.
13. Holman L, Jørgensen CG, Nielsen J, d'Ettorre P. 2010b. Identification of an ant queen pheromone regulating worker sterility. Proc Roy Soc B Biol Sci. 277:3793-3800.
14. Hoover SER, Keeling CI, Winston ML, Slessor KN. 2003. The effect of queen pheromones on worker honey bee ovary development. Naturwissenschaften. 90:477-480.
15. Johnson BR, Linksvayer TA. 2010. Deconstructing the superorganism: social physiology, groundplans, and sociogenomics. Q Rev Biol. 85:57-79.
16. Kaatz H-H, Hildebrandt H, Engels W. 1992. Primer effect of queen pheromone on juvenile hormone biosynthesis in adult worker honey bees. J Comp Physiol B Biochem Syst Environ Physiol. 162:588-592.
17. Keeling CI, Slessor KN, Higo HA, Winston ML. 2003. New components of the honey bee (Apis mellifera L. ) queen retinue pheromone. Proc Natl Acad Sci USA. 100:4486-4491.
18. Le Conte Y, Hefetz A. 2008. Primer pheromones in social hymenoptera. Annu Rev Entomol. 53:523-542.
19. Maisonnasse A, Lenoir J-C, Costagliola G, Beslay D, Choteau F, Crauser D, Becard J-M, Plettner E, Le Conte Y. 2009. A scientific note on E-?-ocimene, a new volatile primer pheromone that inhibits worker ovary development in honey bees. Apidologie. 40:562-564.
20. Martin SJ, Jones GR, Cháline N, Middleton H, Ratnieks FLW. 2002. Reassessing the role of the honeybee (Apis mellifera) Dufour's gland in egg marking. Naturwissenschaften. 89:528-532.
21. Robinson EJH, Jackson DE, Holcombe M, Ratnieks FLW. 2005. Insect communication: 'no entry' signal in ant foraging. Nature. 438:442.
22. Robinson GE, Vargo EL. 1997. Juvenile hormone in adult eusocial hymenoptera: gonadotropin and behavioral pacemaker. Arch Insect Biochem Physiol. 35:559-583.
23. Rolff J, Siva-Jothy MT. 2002. Copulation corrupts immunity: a mechanism for a cost of mating in insects. Proc Natl Acad Sci USA. 99:9916-9918.
24. Schroderus E, Jokinen I, Koivula M, Koskela E, Mappes T, Mills SC, Oksanen TA, Poikonen T. 2010. Intra-and intersexual trade-offs between testosterone and immune system: implications for sexual and sexually antagonistic selection. Am Nat. 176:E90-E97.
25. Seeley TD. 1995. The wisdom of the hive: the social physiology of honey bee colonies. Cambridge (MA): Harvard University Press.
26. Slessor KN, Winston ML, Le Conte Y. 2005. Pheromone communication in the honeybee (Apis mellifera L. ). J Chem Ecol. 31:2731-2745.
27. Smith AA, Hölldober B, Liebig J. 2009. Cuticular hydrocarbons reliably identify cheaters and allow enforcement of altruism in a social insect. Curr Biol. 19:78-81.
28. Sommer K, Hölldobler B. 1995. Colony founding by queen association and determinants of reduction in queen number in the ant Lasius niger. Anim Behav. 50:287-294.
29. Stearns SC. 1992. The evolution of life histories. Oxford: Oxford University Press.
30. Tillman JA, Seybold SJ, Jurenka RA, Blomquist GJ. 1999. Insect pheromones-an overview of biosynthesis and endocrine regulation. Insect Biochem Mol Biol. 29:481-514.
31. Tschinkel WR. 1988. Social control of egg-laying rate in queens of the fire ant, Solenopsis invicta. Physiol Entomol. 13:327-350.
32. Tschinkel WR. 1995. Stimulation of fire ant queen fecundity by a highly specific brood stage. Ann Entomol Soc Am. 88:876-882.
33. Urbani CB. 1991. Indiscriminate oophagy by ant larvae: an explanation for brood serial organization? Insectes Sociaux. 38:229-239.
34. van Wilgenburg E, Sulc R, Shea K, Tsutsui N. 2010. Deciphering the chemical basis of nestmate recognition. J Chem Ecol. 36:751-758.
35. van Zweden JS, Heinze J, Boomsma JJ, d'Ettorre P. 2009. Ant queen egg-marking signals: matching deceptive laboratory simplicity with natural complexity. PLoS ONE. 4:e4718.
36. Vargo EL. 1992. Mutual pheromonal inhibition among queens in polygyne colonies of the fire ant Solenopsis invicta. Behav Ecol Sociobiol. 31:205-210.
37. Vergoz V, Schreurs HA, Mercer AR. 2007. Queen pheromone blocks aversive learning in young worker bees. Science. 317:384-386.
38. Vinkler M, Albrecht T. 2010. Carotenoid maintenance handicap and the physiology of carotenoid-based signalisation of health. Naturwissenschaften. 97:19-28.
39. Wilson EO, Hölldobler B. 1988. Dense heterarchies and mass communication as the basis of organization in ant colonies. Trends Ecol Evol. 3:65-68.
40. Wurm Y, Wang J, Keller L. 2010. Changes in reproductive roles are associated with changes in gene expression in fire ant queens. Mol Ecol. 19:1200-1211.
41. Wyatt TD. 2003. Pheromones and animal behaviour. Cambridge (UK): Cambridge University Press.
42. Yamamoto Y, Matsuura K. 2011. Queen pheromone regulates egg production in a termite. Biol Lett. 7:727-729.
43. Yi HS, Heil M, Adame-Alvarez RM, Ballhorn DJ, Ryu CM. 2009. Airborne induction and priming of plant defenses against a bacterial pathogen. Plant Physiol. 151:2152-2161.