Advertisement

Journal of Chemical Ecology

, Volume 44, Issue 9, pp 805–817 | Cite as

Queen Control or Queen Signal in Ants: What Remains of the Controversy 25 Years After Keller and Nonacs’ Seminal Paper?

  • Irene Villalta
  • Silvia Abril
  • Xim Cerdá
  • Raphael Boulay
Review Article

Abstract

Ant queen pheromones (QPs) have long been known to affect colony functioning. In many species, QPs affect important reproductive functions such as diploid larvae sexualization and egg-laying by workers, unmated queens (gynes), or other queens. Until the 1990s, these effects were generally viewed to be the result of queen manipulation through the use of coercive or dishonest signals. However, in their seminal 1993 paper, Keller and Nonacs challenged this idea, suggesting that QPs had evolved as honest signals that informed workers and other colony members of the queen’s presence and reproductive state. This paper has greatly influenced the study of ant QPs and inspired numerous attempts to identify fertility-related compounds and test their physiological and behavioral effects. In the present article, we review the literature on ant QPs in various contexts and pay special attention to the role of cuticular hydrocarbons (CHCs). Although the controversy generated by Keller and Nonacs’ (Anim Behav 45:787–794, 1993) paper is currently less intensively debated, there is still no clear evidence which allows the rejection of the queen control hypothesis in favor of the queen signal hypothesis. We argue that important questions remain regarding the mode of action of QPs, and their targets which may help understanding their evolution.

Keywords

Cuticular hydrocarbons Fertility signal Signal honesty Signal perception Social insects Sociobiology 

Notes

Acknowledgments

We thank Lindsay Higgins for her help with English editing. This study was funded by the Spanish Ministry of Economy, Industry and Competitiveness and FEDER (project CGL2015-65807-P). We thank Laurent Keller and two anonymous reviewers for very interesting comments on this manuscript.

References

  1. Abril S, Diaz M, Lenoir A, Ivon Paris C, Boulay R, Gómez C (2018) Cuticular hydrocarbons correlate with queen reproductive status in native and invasive Argentine ants (Linepithema humile, Mayr). PLoS One 13:e0193115PubMedPubMedCentralGoogle Scholar
  2. Amor F, Ortega P, Jowers MJ, Cerdá X, Billen J, Lenoir A, Boulay RR (2011) The evolution of worker-queen polymorphism in Cataglyphis ants: interplay between individual-and colony-level selections. Behav Ecol Sociobiol 65:1473–1482.  https://doi.org/10.1007/s00265-011-1157-7 Google Scholar
  3. Amor F, Villalta I, Doums C et al (2016) Nutritional versus genetic correlates of caste differentiation in a desert ant. Ecol Entomol 41:660–667.  https://doi.org/10.1111/een.12337 Google Scholar
  4. Barker JF (1978) Neuroendocrine regulation of oocyte maturation in the imported fire ant Solenopsis invicta. Gen Comp Endocrinol 35:234–237.  https://doi.org/10.1016/0016-6480(78)90067-9 PubMedGoogle Scholar
  5. Berndt KP (1975) Physiology and reproduction in the pharaoh’s ant (Monomorium pharaonis L.). 1. pheromone mediated cyclic production of sexuals. Wiad Parazytol 23:163–166Google Scholar
  6. Bier K (1954) Über den Einfluss der Königin auf die arbeiterinnen Fertilität im Ameisenstaat. Insect Soc 1:7–19Google Scholar
  7. Blomquist GJ, Bagnères A-G (2010) Insect hydrocarbons Biology, Biochemistry, and Chemical Ecology. Cambridge University Press, CambridgeGoogle Scholar
  8. Boonen S, Billen J (2017) Caste regulation in the ant Monomorium pharaonis (L.) with emphasis on the role of queens. Insect Soc 64:113–121.  https://doi.org/10.1007/s00040-016-0521-z Google Scholar
  9. Boulay R, Hooper-Bui LM, Woodring J (2001) Oviposition and oogenesis in virgin fire ant females Solenopsis invicta are associated with a high level of dopamine in the brain. Physiol Entomol 26:294–299.  https://doi.org/10.1046/j.0307-6962.2001.00250.x Google Scholar
  10. Boulay R, Hefetz A, Cerdá X, Devers S, Francke W, Twele R, Lenoir A (2007) Production of sexuals in a fission-performing ant: dual effects of queen pheromones and colony size. Behav Ecol Sociobiol 61:1531–1541.  https://doi.org/10.1007/s00265-007-0385-3 Google Scholar
  11. Boulay R, Cerdá X, Fertin A et al (2009) Brood development into sexual females depends on the presence of a queen but not on temperature in an ant dispersing by colony fission, Aphaenogaster senilis. Ecol Entomol 34:595–602.  https://doi.org/10.1111/j.1365-2311.2009.01108.x Google Scholar
  12. Bourke AFG (1993) Lack of experimental evidence for pheromonal inhibition of reproduction among queens in the ant Leptothorax acervorum. Anim Behav 45:501–509.  https://doi.org/10.1006/anbe.1993.1061 Google Scholar
  13. Bourke AFG, Ratnieks FLW (1999) Kin conflict over caste determination in social Hymenoptera. Behav Ecol Sociobiol 46:287–297.  https://doi.org/10.1007/s002650050622 Google Scholar
  14. Brand J, Blum M, Ross HI (1973) Biochemical evolution in fire ant venoms. Insect Biochem 3:45–51Google Scholar
  15. Brian MV (1970) Communication between queens and larvae in the ant Myrmica. Anim Behav 18:467–472Google Scholar
  16. Brian MV, Carr CAH (1960) The influence of the queen on brood rearing in ants of the genus Myrmica. J Insect Physiol 5:81–94.  https://doi.org/10.1016/0022-1910(60)90034-2 Google Scholar
  17. Brunner E, Kroiss J, Trindl A, Heinze J (2011) Queen pheromones in Temnothorax ants: control or honest signal? BMC Evol Biol 11:55.  https://doi.org/10.1186/1471-2148-11-55 PubMedPubMedCentralGoogle Scholar
  18. Cagniant H (1988) Étude expérimentale du rôle des ouvrières dans le développement des sexués ailés chez la fourmi Cataglyphis cursor (Fonsc.) (Hménoptères, Formicidae). Insect Soc 35:271–292Google Scholar
  19. Cerdá X, Dahbi A, Retana J (2002) Spatial patterns, temporal variability, and the role of multi-nest colonies in a monogynous Spanish desert ant. Ecol Entomol 27:7–15.  https://doi.org/10.1046/j.0307-6946.2001.00386.x Google Scholar
  20. Chen YP, Vinson SB (2000) Effects of queen attractiveness to workers on the queen nutritional status and egg production in the polygynous Solenopsis invicta (Hymenoptera: Formicidae). Ann Entomol Soc Am 93:295–302Google Scholar
  21. Crosland M (1990) The influence of the queen, colony size and worker ovarian development on nestmate recognition in the ant Rhytidoponera confusa. Anim Behav 39:413–425Google Scholar
  22. Cuvillier-Hot V, Lenoir A (2006) Biogenic amine levels, reproduction and social dominance in the queenless ant Streblognathus peetersi. Naturwissenschaften 93:149–153.  https://doi.org/10.1007/s00114-006-0086-1 PubMedGoogle Scholar
  23. Cuvillier-Hot V, Cobb M, Malosse C, Peeters C (2001) Sex, age and ovarian activity effect cuticular hydrocarbons in Diacamma ceylonense a queenless ant. J Insect Physiol 47:485–493PubMedGoogle Scholar
  24. Cuvillier-Hot V, Gadagkar R, Peeters C, Cobb M (2002) Regulation of reproduction in a queenless ant: aggression, pheromones and reduction in conflict. Proc R Soc B Biol Sci 269:1295–1300.  https://doi.org/10.1098/rspb.2002.1991 Google Scholar
  25. Cuvillier-Hot V, Lenoir A, Crewe R, Malosse C, Peeters C (2004) Fertility signalling and reproductive skew in queenless ants. Anim Behav 68:1209–1219.  https://doi.org/10.1016/j.anbehav.2003.11.026 Google Scholar
  26. D’Ettorre P (2004) Does she smell like a queen? Chemoreception of a cuticular hydrocarbon signal in the ant Pachycondyla inversa. J Exp Biol 207:1085–1091.  https://doi.org/10.1242/jeb.00865 PubMedGoogle Scholar
  27. D’Ettorre P, Heinze J, Ratnieks F (2004) Worker policing by egg eating in the ponerine ant Pachycondyla inversa. Proc R Soc B Biol Sci 271:1427–1434.  https://doi.org/10.1098/rspb.2004.2742 Google Scholar
  28. De Biseau JC, Passera L, Daloze D, Aron S (2004) Ovarian activity correlates with extreme changes in cuticular hydrocarbon profile in the highly polygynous ant, Linepithema humile. J Insect Physiol 50:585–593.  https://doi.org/10.1016/j.jinsphys.2004.04.005 PubMedGoogle Scholar
  29. Dietemann V, Peeters C (2000) Queen influence on the shift from trophic to reproductive eggs laid by workers of the ponerine ant Pachycondyla apicalis. Insect Soc 47:223–228.  https://doi.org/10.1007/PL00001707 Google Scholar
  30. Dietemann V, Peeters C, Liebig J, Thivet V, Holldobler B (2003) Cuticular hydrocarbons mediate discrimination of reproductives and nonreproductives in the ant Myrmecia gulosa. Proc Natl Acad Sci 100:10341–10346.  https://doi.org/10.1073/pnas.1834281100 PubMedGoogle Scholar
  31. Dietemann V, Peeters C, Hölldobler B (2005) Role of the queen in regulating reproduction in the bulldog ant Myrmecia gulosa: control or signalling? Anim Behav 69:777–784.  https://doi.org/10.1016/j.anbehav.2004.07.006 Google Scholar
  32. Edwards JP (1987) Caste regulation in the pharaoh’s ant Monomorium pharaonis: the influence of queens on the production of new sexual forms. Physiol Entomol 12:31–39.  https://doi.org/10.1111/j.1365-3032.1987.tb00721.x Google Scholar
  33. Edwards JP (1991a) Caste regulation in the pharaoh’s ant Monomorium pharaonis: recognition and cannibalism of sexual brood by workers. Physiol Entomol 16:263–271.  https://doi.org/10.1111/j.1365-3032.1991.tb00565.x Google Scholar
  34. Edwards JP (1991b) Caste regulation in the pharaoh’s ant Monomorium pharaonis: recognition and cannibalism of sexual brood by workers. Physiol Entomol 16:263–271.  https://doi.org/10.1111/j.1365-3032.1991.tb00565.x Google Scholar
  35. Edwards JP, Chambers J (1984) Queen specific chemical in the Pharaoh’s ant, Monomorium pharaonis (L.). J Chem Ecol 10:1731–1747PubMedGoogle Scholar
  36. Eliyahu D, Ross KG, Haight KL, Keller L, Liebig J (2011) Venom alkaloid and cuticular hydrocarbon profiles are associated with social organization, queen fertility status, and queen genotype in the fire ant Solenopsis invicta. J Chem Ecol 37:1242–1254.  https://doi.org/10.1007/s10886-011-0037-y PubMedPubMedCentralGoogle Scholar
  37. Endler A, Liebig J, Schmitt T, Parker JE, Jones GR, Schreier P, Holldobler B (2004) Surface hydrocarbons of queen eggs regulate worker reproduction in a social insect. Proc Natl Acad Sci U S A 101:2945–2950.  https://doi.org/10.1073/pnas.0308447101 PubMedPubMedCentralGoogle Scholar
  38. Endler A, Liebig J, Hölldobler B (2006) Queen fertility, egg marking and colony size in the ant Camponotus floridanus. Behav Ecol Sociobiol 59:490–499.  https://doi.org/10.1007/s00265-005-0073-0 Google Scholar
  39. Evison SEF, Ferreira RS, D’Ettorre P, Fresneau D, Poteaux C (2012) Chemical signature and reproductive status in the facultatively polygynous ant Pachycondyla Verenae. J Chem Ecol 38:1441–1449.  https://doi.org/10.1007/s10886-012-0195-6 PubMedGoogle Scholar
  40. Fletcher DJC, Blum MS (1981) Pheromonal control of dealation and oogenesis in virgin queen fire ants. Science 212:73–76PubMedGoogle Scholar
  41. Fletcher DJC, Blum MS (1983) The inhibitory pheromone of queen fire ants: effects of disinhibition on dealation and oviposition by virgin queens. J Comp Physiol A 153:467–475.  https://doi.org/10.1007/BF00612601 Google Scholar
  42. Foitzik S, Froba J, Ruger MH, Witte V (2011) Competition over workers: fertility signalling in wingless queens of Hypoponera opacior. Insect Soc 58:271–278Google Scholar
  43. Ghaninia M, Haight K, Berger SL, Reinberg D, Zwiebel LJ, Ray A, Liebig J (2017) Chemosensory sensitivity reflects reproductive status in the ant Harpegnathos saltator. Sci Rep 7:1–9.  https://doi.org/10.1038/s41598-017-03964-7 Google Scholar
  44. Glancey BM, Glover AR, Lofgren CS (1981) Pheormone production by virgin queens of Solenopsis invicta Buren. Sociobiology 6:119–127Google Scholar
  45. Gobin B, Billen J, Peeters C (1999) Policing behaviour towards virgin egg layers in a polygynous ponerine ant. Anim Behav 58:1117–1122.  https://doi.org/10.1006/anbe.1999.1245 PubMedGoogle Scholar
  46. Gotoh H, Miyakawa H, Ishikawa A, Ishikawa Y, Sugime Y, Emlen DJ, Lavine LC, Miura T (2014) Developmental link between sex and nutrition; doublesex regulates sex-specific mandible growth via juvenile hormone signaling in stag beetles. PLoS Genet 10:1–9.  https://doi.org/10.1371/journal.pgen.1004098 Google Scholar
  47. Grüter C, Keller L (2016) Inter-caste communication in social insects. Curr Opin Neurobiol 38:6–11.  https://doi.org/10.1016/j.conb.2016.01.002 PubMedGoogle Scholar
  48. Hammond RL, Keller L (2004) Conflict over male parentage in social insects. PLoS Biol 2:e248–e211.  https://doi.org/10.1007/s00040-003-0707-z PubMedPubMedCentralGoogle Scholar
  49. Hannonen M, Sledge MF, Turillazzi S, Sundström L (2002) Queen reproduction, chemical signalling and worker behaviour in polygyne colonies of the ant Formica fusca. Anim Behav 64:477–485.  https://doi.org/10.1006/anbe.2002.4001 Google Scholar
  50. Hartmann A, Wantia J, Torres JA, Heinze J (2003) Worker policing without genetic conflicts in a clonal ant. Proc Natl Acad Sci U S A 100:12836–12840.  https://doi.org/10.1073/pnas.2132993100 PubMedPubMedCentralGoogle Scholar
  51. Heinze J (2004) Reproductive conflicts in insect societies. Adv Study Behav 34:1–57Google Scholar
  52. Heinze J, d’Ettorre P (2009) Honest and dishonest communication in social Hymenoptera. J Exp Biol 212:1775–1779.  https://doi.org/10.1242/jeb.015008 PubMedGoogle Scholar
  53. Heinze J, Oberstadt B, Tentschert J, Hölldobler B, Bestmann HJ (1998) Colony specificity of Dufour gland secretions in a functionally monogynous ant. Chemoecol 8:169–174.  https://doi.org/10.1007/s000490050022 Google Scholar
  54. Helanterä H, Sundström L (2005) Worker reproduction in the ant Formica fusca. J Evol Biol 18:162–171.  https://doi.org/10.1111/j.1420-9101.2004.00777.x PubMedGoogle Scholar
  55. Helms Cahan S, Parker JD, Rissing SW et al (2002) Extreme genetic differences between queens and workers in hybridizing Pogonomyrmex harvester ants. Proc R Soc B Biol Sci 269:1871–1877.  https://doi.org/10.1098/rspb.2002.2061 Google Scholar
  56. Hölldobler B, Carlin NF (1989) Colony founding, queen control and worker reproduction in the ant Aphaenogaster (=Novomessor) cockerelli (Hymenoptera: Formicidae). Psyche 96:131–151Google Scholar
  57. Hölldobler B, Wilson EO (1983) Queen control in colonies of weaver ants (Hymenoptera: Formicidae). Ann Entomol Soc Am 76:235–238Google Scholar
  58. 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.  https://doi.org/10.1098/rspb.2009.2311 Google Scholar
  59. Holman L, Jorgensen CG, Nielsen J, D’Ettorre P (2010b) Identification of an ant queen pheromone regulating worker sterility. Proc R Soc B Biol Sci 277:3793–3800.  https://doi.org/10.1098/rspb.2010.0984 Google Scholar
  60. Holman L, Lanfear R, D’Ettorre P (2013a) The evolution of queen pheromones in the ant genus Lasius. J Evol Biol 26:1549–1558.  https://doi.org/10.1111/jeb.12162 PubMedGoogle Scholar
  61. Holman L, Leroy C, Jørgensen C, Nielsen J, d’Ettorre P (2013b) Are queen ants inhibited by their own pheromone? Regulation of productivity via negative feedback. Behav Ecol 24:380–385.  https://doi.org/10.1093/beheco/ars174 Google Scholar
  62. Holman L, Hanley B, Millar JG (2016a) Highly specific responses to queen pheromone in three Lasius ant species. Behav Ecol Sociobiol 70:387–392.  https://doi.org/10.1007/s00265-016-2058-6 Google Scholar
  63. Holman L, Trontti K, Helanterä H et al (2016b) Queen pheromones modulate DNA methyltransferase activity in bee and ant workers. Biol Lett 12:20151038.  https://doi.org/10.1098/rsbl.2015.1038 PubMedPubMedCentralGoogle Scholar
  64. Hora RR, Ionescu-Hirsh A, Simon T, Delabie J, Robert J, Fresneau D, Hefetz A (2008) Postmating changes in cuticular chemistry and visual appearance in Ectatomma tuberculatum queens (Formicidae: Ectatomminae). Naturwissenschaften 95:55–60.  https://doi.org/10.1007/s00114-007-0287-2 PubMedGoogle Scholar
  65. Ichinose K, Lenoir A (2009) Reproductive conflict between laying workers in the ant Aphaenogaster senilis. J Ethol 27:475–481.  https://doi.org/10.1007/s10164-008-0145-5 Google Scholar
  66. Iwanishi S, Hasegawa E, Ohkawara K (2003) Worker oviposition and policing behaviour in the myrmicine ant Aphaenogaster smythiesi japonica forel. Anim Behav 66:513–519.  https://doi.org/10.1006/anbe.2003.2222 Google Scholar
  67. Jemielity S, Gräff J, Keller L (2006) How to fool a virgin: artificial dealation triggers oviposition in virgin Lasius niger queens. Insect Soc 53:323–325.  https://doi.org/10.1007/s00040-006-0875-8 Google Scholar
  68. Jones WD, Cayirlioglu P, Grunwald Kadow I, Vosshall LB (2007) Two chemosensory receptors together mediate carbon dioxide detection in Drosophila. Nature 445:86–90.  https://doi.org/10.1038/nature05466 PubMedGoogle Scholar
  69. Kelber C, Rössler W, Kleineidam CJ (2010) Phenotypic plasticity in number of glomeruli and sensory innervation of the antennal lobe in leaf-cutting ant workers (Atta vollenweideri). Dev Neurobiol 70:222–234.  https://doi.org/10.1002/dneu.20782 PubMedGoogle Scholar
  70. Keller L (1988a) Pouvoir attractif des reines de la fourmi d’Argentine, Iridomyrmex humilis (Mayr). Rôle de la polygynie et du statut physiologique des reines. Bull Soc Vaud Sci Nat 79:93–102Google Scholar
  71. Keller L (1988b) Evolutionary implications of polygyny in the Argentine ant, Iridomyrmex humilis (Mayr) (Hymenoptera: Formicidae): an experimental study. Anim Behav 36:159–165.  https://doi.org/10.1016/S0003-3472(88)80259-8 Google Scholar
  72. Keller L (2009) Adaptation and the genetics of social behaviour. Phil Trans R Soc B: Biol Sci 364:3209–3216.  https://doi.org/10.1098/rstb.2009.0108 Google Scholar
  73. Keller L, Nonacs P (1993) The role of queen pheromones in social insects: queen control or queen signal? Anim Behav 45:787–794Google Scholar
  74. Keller L, Passera L, Suzzoni JP (1989) Queen execution in the argentine ant, Iridomyrmex humilis. Physiol Entomol 14:157–163Google Scholar
  75. Kidokoro-Kobayashi M, Iwakura M, Fujiwara-Tsujii N, Fujiwara S, Sakura M, Sakamoto H, Higashi S, Hefetz A, Ozaki M (2012) Chemical discrimination and aggressiveness via cuticular hydrocarbons in a supercolony-forming ant, Formica yessensis. PLoS One 7:e46840.  https://doi.org/10.1371/journal.pone.0046840 PubMedPubMedCentralGoogle Scholar
  76. Kikuta N, Tsuji K (1999) Queen and worker policing in the monogynous and monandrous ant, Diacamma sp. Behav Ecol Sociobiol 46:180–189.  https://doi.org/10.1007/s002650050608 Google Scholar
  77. Klein A, Schultner E, Lowak H, Schrader L, Heinze J, Holman L, Oettler J (2016) Evolution of social insect polyphenism facilitated by the sex differentiation cascade. PLoS Genet 12:1–16.  https://doi.org/10.1371/journal.pgen.1005952 Google Scholar
  78. Klobuchar EA, Deslippe RJ (2002) A queen pheromone induces workers to kill sexual larvae in colonies of the red imported fire ant (Solenopsis invicta). Naturwissenschaften 89:302–304.  https://doi.org/10.1007/s00114-002-0331-1 PubMedGoogle Scholar
  79. Larsson MC, Domingos AI, Jones WD, Chiappe ME, Amrein H, Vosshall LB (2004) Or83b encodes a broadly expressed odorant receptor essential for Drosophila olfaction. Neuron 43:703–714.  https://doi.org/10.1016/j.neuron.2004.08.019 PubMedGoogle Scholar
  80. Leboeuf AC, Waridel P, Brent CS et al (2016) Oral transfer of chemical cues, growth proteins and hormones in social insects. eLife 5:1–27.  https://doi.org/10.7554/eLife.20375 Google Scholar
  81. Ledoux A (1976) Inhibition exercée sur l’apparition de nouvelles femelles ailées par la femelle reine pondeux chez Aphaenogaster senilis (Hyménoptère formicoidea). Comptes Rendus de l’Académie des Sciences de Paris-Série D 283:1197–1200Google Scholar
  82. Ledoux A, Dargagnon D (1973) La formation des castes chez la fourmi Aphaenogaster senilis. C R Ac Sc Paris - Serie D 276:551–553Google Scholar
  83. Leniaud L, Darras H, Boulay R, Aron S (2012) Social hybridogenesis in the clonal ant Cataglyphis hispanica. Curr Biol 22:1188–1193.  https://doi.org/10.1016/j.cub.2012.04.060 PubMedGoogle Scholar
  84. Liebig J, Peeters C, Holldobler B (1999) Worker policing limits the number of reproductives in a ponerine ant. Proc R Soc B Biol Sci 266:1865–1870.  https://doi.org/10.1098/rspb.1999.0858 Google Scholar
  85. Liebig J, Peeters C, Oldham NJ, Markstadter C, Holldobler B (2000) Are variations in cuticular hydrocarbons of queens and workers a reliable signal of fertility in the ant Harpegnathos saltator? Proc Natl Acad Sci U S A 97:4124–4131.  https://doi.org/10.1073/pnas.97.8.4124 PubMedPubMedCentralGoogle Scholar
  86. Lommelen E, Johnson CA, Drijfhout FP, Billen J, Wenseleers T, Gobin B (2006) Cuticular hydrocarbons provide reliable cues of fertility in the ant Gnamptogenys striatula. J Chem Ecol 32:2023–2034.  https://doi.org/10.1007/s10886-006-9126-8 PubMedGoogle Scholar
  87. Manfredini F, Lucas C, Nicolas M, Keller L, Shoemaker DW, Grozinger CM (2014) Molecular and social regulation of worker division of labour in fire ants. Mol Ecol 23:660–672.  https://doi.org/10.1111/mec.12626 PubMedGoogle Scholar
  88. McKenzie SK, Fetter-Pruneda I, Ruta V, Kronauer DJC (2016) Transcriptomics and neuroanatomy of the clonal raider ant implicate an expanded clade of odorant receptors in chemical communication. Proc Natl Acad Sci U S A 113:14091–14096.  https://doi.org/10.1073/pnas.1610800113 PubMedPubMedCentralGoogle Scholar
  89. Mercier B, Passera J, Suzzoni J-P (1985) Étude de la polygynie chez la fourmi Plagiolepis pygmaea Latr. (Hym. Formicidae) II. La fécondité des reines en condition expérimentale polygyne. Insect Soc 32:349–362Google Scholar
  90. Monnin T, Peeters C (1997) Cannibalism of subordinates’ eggs in the monogynous queenless ant Dinoponera quadriceps. Naturwissenschaften 84:499–502.  https://doi.org/10.1007/s001140050433 Google Scholar
  91. Monnin T, Ratnieks FLW, Jones GR, Beard R (2002) Pretender punishment induced by chemical signalling in a queenless ant. Nature 419:61–65.  https://doi.org/10.1038/nature00997.1. PubMedGoogle Scholar
  92. Monnin T, Helft F, Leroy C et al (2018) Chemical characterization of young virgin queens and mated egg-laying queens in the ant Cataglyphis cursor : random forest classification analysis for multivariate datasets. J Chem Ecol 44:127–136PubMedGoogle Scholar
  93. Motais de Narbonne M, van Zweden JS, Bello JE, Wenseleers T, Millar JG, d'Ettorre P (2016) Biological activity of the enantiomers of 3-methylhentriacontane, a queen pheromone of the ant Lasius niger. J Exp Biol 219:1632–1638.  https://doi.org/10.1242/jeb.136069 PubMedGoogle Scholar
  94. Nakanishi A, Nishino H, Watanabe H, Yokohari F, Nishikawa M (2010) Sex-specific antennal sensory system in the ant Camponotus japonicus: glomerular organizations of antennal lobes. J Comp Neurol 518:2186–2201.  https://doi.org/10.1002/cne.22326 PubMedGoogle Scholar
  95. Obin MS, Glancey BM, Banks WA, Vander Meer RK (1988) Queen pheromone production and its physiological correlates in fire ant queens (Hymenoptera: Formicidae) treated with fenoxycarb. Ann Entomol Soc Am 81:808–815.  https://doi.org/10.1093/aesa/81.5.808 Google Scholar
  96. Olejarz J, Veller C, Nowak MA (2017) The evolution of queen control over worker reproduction in the social Hymenoptera. Ecol Evol 7:8427–8441.  https://doi.org/10.1002/ece3.3324 PubMedPubMedCentralGoogle Scholar
  97. Oliveira RC, Vollet-Neto A, Akemi Oi C, van Zweden JS, Nascimento F, Sullivan Brent C, Wenseleers T (2017) Hormonal pleiotropy helps maintain queen signal honesty in a highly eusocial wasp. Sci Rep 7:1–12.  https://doi.org/10.1038/s41598-017-01794-1 Google Scholar
  98. Oppelt A, Heinze J (2009) Mating is associated with immediate changes of the hydrocarbon profile of Leptothorax gredleri ant queens. J Insect Physiol 55:624–628.  https://doi.org/10.1016/j.jinsphys.2009.03.010 PubMedGoogle Scholar
  99. Ortius D, Heinze J (1999) Fertility signaling in queens of a North American ant. Behav Ecol Sociobiol 45:151–159.  https://doi.org/10.1007/s002650050548 Google Scholar
  100. Oxley PR, Ji L, Fetter-Pruneda I, McKenzie SK, Li C, Hu H, Zhang G, Kronauer DJC (2014) The genome of the clonal raider ant Cerapachys biroi. Curr Biol 24:451–458.  https://doi.org/10.1016/j.cub.2014.01.018 PubMedPubMedCentralGoogle Scholar
  101. Ozaki M, Wada-katsumata A, Fujikawa K et al (2005) Ant nestmate and non-Nestmate discrimination by a chemosensory sensillum. Science 311:311–315.  https://doi.org/10.1126/science.1105244 Google Scholar
  102. Pask GM, Slone JD, Millar JG, Das P, Moreira JA, Zhou X, Bello J, Berger SL, Bonasio R, Desplan C, Reinberg D, Liebig J, Zwiebel LJ, Ray A (2017) Specialized odorant receptors in social insects that detect cuticular hydrocarbon cues and candidate pheromones. Nat Commun 8:1–10.  https://doi.org/10.1038/s41467-017-00099-1 Google Scholar
  103. Passera L (1969) Biologie de la reproduction chez Plagiolepis pygmaea Latreille et ses deux parasites sociaux Plagiolepis grassei Le Masne et Passera et Plagiolepis xene Stärcke (Hym. Formicidae). Ann Sc Nat - Zool 11:327–482Google Scholar
  104. Passera L (1980a) La fonction inhibitrice des reines de la fourmi Plagiolepis pygmaea Latr.: Role des pheromones. Insect Soc 27:212–225.  https://doi.org/10.1007/BF02223665 Google Scholar
  105. Passera L (1980b) La ponte d’oeufs préorientés chez la fourmi Pheidole pallidula (Nyl.) (Hymenoptera - Formicidae). Insect Soc 27:79–95.  https://doi.org/10.1093/beheco/7.3.292 Google Scholar
  106. Passera L, Aron S (1993) Factors controling dealation and egg laying in virgin queens of the Argentine ant Linepithema humile, Mayr (=Iridomyrmex humilis). Psyche 100:51–63Google Scholar
  107. Passera L, Aron S, Bach D (1995) Elimination of sexual brood in the Argentine ant Linepithema humile: queen effect and brood recognition. Entomol Exp Appl 75:203–212.  https://doi.org/10.1111/j.1570-7458.1995.tb01928.x Google Scholar
  108. Peeters C, Monnin T, Malosse C (1999) Cuticular hydrocarbons correlated with reproductive status in a queenless ant. Proc R Soc B Biol Sci 266:1323–1327.  https://doi.org/10.1098/rspb.1999.0782 Google Scholar
  109. Penick CA, Liebig J (2012) Regulation of queen development through worker aggression in a predatory ant. Behav Ecol 23:992–998.  https://doi.org/10.1093/beheco/ars062 Google Scholar
  110. Penick CA, Liebig J (2017) A larval “princess pheromone” identifies future ant queens based on their juvenile hormone content. Anim Behav 128:33–40.  https://doi.org/10.1016/j.anbehav.2017.03.029 Google Scholar
  111. Penick CA, Brent CS, Dolezal K, Liebig J (2014) Neurohormonal changes associated with ritualized combat and the formation of a reproductive hierarchy in the ant Harpegnathos saltator. J Exp Biol 217:1496–1503.  https://doi.org/10.1242/jeb.098301 PubMedGoogle Scholar
  112. Peso M, Elgar MA, Barron AB (2015) Pheromonal control: reconciling physiological mechanism with signalling theory. Biol Rev 90:542–559.  https://doi.org/10.1111/brv.12123 PubMedGoogle Scholar
  113. Plateaux L (1971) Sur le polymorphisme social de la fourmi Leptothorax nylanderi (Förster) II.-Activité des ouvrières et déterminisme des castes. Ann Sc Nat - Zool 12:1–90Google Scholar
  114. Ratnieks FLW (1988) Reproductive harmony via mutual policing by workers in Eusocial Hymenoptera. Am Nat 132:217–236Google Scholar
  115. Röseler PF (1991) Soziale und reproduktive dominanz bei insekten. Naturwissenschaften 78:114–120.  https://doi.org/10.1007/BF01131485 Google Scholar
  116. Ruel C, Hefetz A, Cerdá X, Boulay R (2013a) Recognition of caste and mating status maintains monogyny in the ant Aphaenogaster senilis. Behav Ecol Sociobiol 67:1295–1305.  https://doi.org/10.1007/s00265-013-1558-x Google Scholar
  117. Ruel C, Lenoir A, Cerdá X, Boulay R (2013b) Surface lipids of queen-laid eggs do not regulate queen production in a fission-performing ant. Naturwissenschaften 100:91–100.  https://doi.org/10.1007/s00114-012-0997-y PubMedGoogle Scholar
  118. Sato K, Pellegrino M, Nakagawa T, Nakagawa T, Vosshall LB, Touhara K (2008) Insect olfactory receptors are heteromeric ligand-gated ion channels. Nature 452:1002–1006.  https://doi.org/10.1038/nature06850 PubMedGoogle Scholar
  119. Schneirla TC (1971) Army ants: a study in social organization. W. H. Freeman and Company, San FranciscoGoogle Scholar
  120. Schrader L, Simola DF, Heinze J, Oettler J (2015) Sphingolipids, transcription factors, and conserved toolkit genes: developmental plasticity in the ant Cardiocondyla obscurior. Mol Biol Evol 32:1474–1486.  https://doi.org/10.1093/molbev/msv039 PubMedPubMedCentralGoogle Scholar
  121. Schrempf A, Heinze J (2006) Proximate mechanisms of male morph determination in the ant Cardiocondyla obscurior. Evol Dev 8:266–272.  https://doi.org/10.1111/j.1525-142X.2006.00097.x PubMedGoogle Scholar
  122. Seeley TD (1979) Queen substance dispersal by messenger workers in honeybee colonies. Behav Ecol Sociobiol 5:391–415.  https://doi.org/10.1007/BF00292527 Google Scholar
  123. Seeley T (1985) Honeybee ecology: a study of adaptation in social life. Princeton University Press, PrincetonGoogle Scholar
  124. Sharma KR, Enzmann BL, Schmidt Y, Moore D, Jones GR, Parker J, Berger SL, Reinberg D, Zwiebel LJ, Breit B, Liebig J, Ray A (2015) Cuticular hydrocarbon pheromones for social behavior and their coding in the ant antenna. Cell Rep 12:1261–1271.  https://doi.org/10.1016/j.celrep.2015.07.031 PubMedGoogle Scholar
  125. Smith AA, Liebig J (2017) The evolution of cuticular fertility signals in eusocial insects. Cur Op Ins Sc 22:79–84.  https://doi.org/10.1016/j.cois.2017.05.017 Google Scholar
  126. Smith CR, Suarez AV (2010) The trophic ecology of castes in harvester ant colonies. Funct Ecol 24:122–130.  https://doi.org/10.1111/j.1365-2435.2009.01604.x Google Scholar
  127. Smith AA, Hölldobler B, Liebig J (2008a) Hydrocarbon signals explain the pattern of worker and egg policing in the ant Aphaenogaster cockerelli. J Chem Ecol 34:1275–1282.  https://doi.org/10.1007/s10886-008-9529-9 PubMedGoogle Scholar
  128. Smith CR, Anderson KE, Tillberg CV, Gadau J, Suarez AV (2008b) Caste determination in a polymorphic social insect: nutritional, social, and genetic factors. Am Nat 172:497–507.  https://doi.org/10.1086/590961 PubMedGoogle Scholar
  129. 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.  https://doi.org/10.1016/j.cub.2008.11.059 PubMedGoogle Scholar
  130. Smith CD, Zimin A, Holt C, Abouheif E, Benton R, Cash E, Croset V, Currie CR, Elhaik E, Elsik CG, Fave MJ, Fernandes V, Gadau J, Gibson JD, Graur D, Grubbs KJ, Hagen DE, Helmkampf M, Holley JA, Hu H, Viniegra ASI, Johnson BR, Johnson RM, Khila A, Kim JW, Laird J, Mathis KA, Moeller JA, Munoz-Torres MC, Murphy MC, Nakamura R, Nigam S, Overson RP, Placek JE, Rajakumar R, Reese JT, Robertson HM, Smith CR, Suarez AV, Suen G, Suhr EL, Tao S, Torres CW, van Wilgenburg E, Viljakainen L, Walden KKO, Wild AL, Yandell M, Yorke JA, Tsutsui ND (2011a) Draft genome of the globally widespread and invasive Argentine ant (Linepithema humile). Proc Natl Acad Sci U S A 108:5673–5678.  https://doi.org/10.1073/pnas.1008617108 PubMedPubMedCentralGoogle Scholar
  131. Smith CR, Smith CD, Robertson HM, Helmkampf M, Zimin A, Yandell M, Holt C, Hu H, Abouheif E, Benton R, Cash E, Croset V, Currie CR, Elhaik E, Elsik CG, Fave MJ, Fernandes V, Gibson JD, Graur D, Gronenberg W, Grubbs KJ, Hagen DE, Viniegra ASI, Johnson BR, Johnson RM, Khila A, Kim JW, Mathis KA, Munoz-Torres MC, Murphy MC, Mustard JA, Nakamura R, Niehuis O, Nigam S, Overson RP, Placek JE, Rajakumar R, Reese JT, Suen G, Tao S, Torres CW, Tsutsui ND, Viljakainen L, Wolschin F, Gadau J (2011b) Draft genome of the red harvester ant Pogonomyrmex barbatus. Proc Natl Acad Sci 108:5667–5672.  https://doi.org/10.1073/pnas.1007901108 PubMedGoogle Scholar
  132. Smith AA, Hölldobler B, Liebig J (2012a) Queen-specific signals and worker punishment in the ant Aphaenogaster cockerelli: the role of the Dufour’s gland. Anim Behav 83:587–593.  https://doi.org/10.1016/j.anbehav.2011.12.024 Google Scholar
  133. Smith AA, Millar JG, Hanks LM, Suarez AV (2012b) Experimental evidence that workers recognize reproductives through cuticular hydrocarbons in the ant Odontomachus brunneus. Behav Ecol Sociobiol 66:1267–1276.  https://doi.org/10.1007/s00265-012-1380-x Google Scholar
  134. Stroeymeyt N, Brunner E, Heinze J (2007) “Selfish worker policing” controls reproduction in a Temnothorax ant. Behav Ecol Sociobiol 61:1449–1457.  https://doi.org/10.1007/s00265-007-0377-3 Google Scholar
  135. Suefuji M, Cremer S, Oettler J, Heinze J (2008) Queen number influences the timing of the sexual production in colonies of Cardiocondyla ants. Biol Lett 4:670–673.  https://doi.org/10.1098/rsbl.2008.0355 PubMedPubMedCentralGoogle Scholar
  136. Trible W, Olivos-Cisneros L, McKenzie SK et al (2017) Orco mutagenesis causes loss of antennal lobe glomeruli and impaired social behavior in ants. Cell 170:727–735.e10.  https://doi.org/10.1016/j.cell.2017.07.001 PubMedGoogle Scholar
  137. Tsuji K, Kikuta N, Kikuchi T (2011) Determination of the coest of worker reproduction via diminished life span in the ant Diacamma sp. Evolution 45:1322–1331.  https://doi.org/10.5061/dryad.jq203737 Google Scholar
  138. Van Oystaeyen A, Oliveira RC, Holman L et al (2014) Conserved class of queen pheromones stops social insect workers from reproducing. Science 343:287–290.  https://doi.org/10.1126/science.1244899 PubMedGoogle Scholar
  139. van Zweden JS, Furst MA, Heinze J, D’Ettorre P (2007) Specialization in policing behaviour among workers in the ant Pachycondyla inversa. Proc R Soc B Biol Sci 274:1421–1428.  https://doi.org/10.1098/rspb.2007.0113 Google Scholar
  140. 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 4:1–7.  https://doi.org/10.1371/journal.pone.0004718 Google Scholar
  141. Vander Meer RK, Alonso LE (2002) Queen primer pheromone affects conspecific fire ant (Solenopsis invicta) aggression. Behav Ecol Sociobiol 51:122–130.  https://doi.org/10.1007/s002650100417 Google Scholar
  142. Vander Meer RK, Morel L (1995) Ant queens deposit pheromones and antimicrobial agents on eggs. Naturwissenschaften 82:93–95.  https://doi.org/10.1007/BF01140150 Google Scholar
  143. Vander Meer RK, Glancey BM, Lofgren CS et al (1980) The poison sac of red imported fire ant queens: source of a pheromone attractant. Ann Entomol Soc Am 73:609–612.  https://doi.org/10.1093/aesa/73.5.609 Google Scholar
  144. Vander Meer RK, Morel L, Lofgren CS (1992) A comparison of queen oviposition rates from monogyne and polygyne fire ant, Solenopsis invicta, colonies. Physiol Entomol 17:384–390.  https://doi.org/10.1111/j.1365-3032.1992.tb01036.x Google Scholar
  145. Vander Meer RK, Preston CA, Hefetz A (2008) Queen regulates biogenic amine level and nestmate recognition in workers of the fire ant, Solenopsis invicta. Naturwissenschaften 95:1155–1158.  https://doi.org/10.1007/s00114-008-0432-6 PubMedGoogle Scholar
  146. Vargo EL (1992) Mutual pheromonal inhibition among queens in polygyne colonies of the fire ant Solenopsis invicta. Behav Ecol Sociobiol 31:205–210.  https://doi.org/10.1007/BF00168648 Google Scholar
  147. Vargo EL (1997) Poison gland of queen fire ants (Solenopsis invicta) is the source of a primer pheromone. Naturwissenschaften 84:507–510.  https://doi.org/10.1007/s001140050435 Google Scholar
  148. Vargo EL (1999) Reproductive development and ontogeny of queen pheromone production in the fire ant Solenopsis invicta. Physiol Entomol 24:370–376Google Scholar
  149. Vargo EL, Fletcher DJC (1986) Queen control over the production of sexuals in the fire ant, Solenopsis invicta. J Comp Physiol A 159:741–749Google Scholar
  150. Vargo EL, Hulsey CD (2000) Multiple glandular origins of queen pheromones in the fire ant Solenopsis invicta. J Insect Physiol 46:1151–1159.  https://doi.org/10.1016/S0022-1910(99)00226-7 PubMedGoogle Scholar
  151. Vargo EL, Laurel M (1994) Studies on the mode of action of a queen primer pheromone of the fire ant Solenopsis invicta. J Insect Physiol 40:601–610.  https://doi.org/10.1016/0022-1910(94)90147-3 Google Scholar
  152. Vargo EL, Passera L (1991) Pheromonal and behavioral queen control over the production of gynes in the Argentine ant Iridomyrmex humilis (Mayr). Behav Ecol Sociobiol 28:161–169.  https://doi.org/10.1007/BF00172167 Google Scholar
  153. Vasquez GM, Schal C, Silverman J (2008) Cuticular hydrocarbons as queen adoption cues in the invasive Argentine ant. J Exp Biol 211:1249–1256.  https://doi.org/10.1242/jeb.017301 PubMedGoogle Scholar
  154. Villalta I, Angulo E, Devers S, Cerdá X, Boulay R (2015) Regulation of worker egg laying by larvae in a fission-performing ant. Anim Behav 106:149–156.  https://doi.org/10.1016/j.anbehav.2015.05.021 Google Scholar
  155. Villalta I, Amor F, Cerdá X, Boulay R (2016) Social coercion of larval development in an ant species. Sc Nat 103:18.  https://doi.org/10.1007/s00114-016-1341-8 Google Scholar
  156. Wenseleers T, Ratnieks FLW (2006) Comparative analysis of worker reproduction and policing in eusocial hymenoptera supports relatedness theory. Am Nat 168:E163–E179.  https://doi.org/10.1086/508619 PubMedGoogle Scholar
  157. Willer DE, Fletcher DJC (1986) Differences in inhibitory capability among queens of the ant Solenopsis invicta. Physiol Entomol 11:475–482.  https://doi.org/10.1111/j.1365-3032.1986.tb00441.x Google Scholar
  158. Woyciechowski M, Łomnicki A (1987) Multiple mating of queens and the sterility of workers among eusocial hymenoptera. J Theor Biol 128:317–327.  https://doi.org/10.1016/S0022-5193(87)80074-7 Google Scholar
  159. Yamauchi K, Ishida Y, Hashim R, Heinze J (2007) Queen-queen competition and reproductive skew in a Cardiocondyla ant. Insect Soc 54:268–274.  https://doi.org/10.1007/s00040-007-0941-x Google Scholar
  160. Yan H, Opachaloemphan C, Reinberg D et al (2017) An engineered orco mutation produces aberrant social behavior and defective neural development in ants. Cell 170:736–747.  https://doi.org/10.1016/j.cell.2017.06.051 PubMedGoogle Scholar
  161. Zahavi A (1975) Mate selection—a selection for a handicap. J Theor Biol 53:205–214PubMedGoogle Scholar
  162. Zhou X, Slone JD, Rokas A, Berger SL, Liebig J, Ray A, Reinberg D, Zwiebel LJ (2012) Phylogenetic and transcriptomic analysis of chemosensory receptors in a pair of divergent ant species reveals sex-specific signatures of odor coding. PLoS Genet 8:e1002930.  https://doi.org/10.1371/journal.pgen.1002930 PubMedPubMedCentralGoogle Scholar
  163. Zube C, Rössler W (2008) Caste- and sex-specific adaptations within the olfactory pathway in the brain of the ant Camponotus floridanus. Arthropod Struct Dev 37:469–479.  https://doi.org/10.1016/j.asd.2008.05.004 PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Estación Biologica de Doñana, CSICSevilleSpain
  2. 2.Institut de Recherche sur la Biologie de l’InsecteUniversité de ToursToursFrance
  3. 3.Departament de Ciències AmbientalsUniversitat de GironaGironaSpain
  4. 4.IRBI CNRS UMR 7261, Faculté des Sciences et Techniques, Avenue Monge, Parc de GrandmontUniversité de ToursToursFrance

Personalised recommendations