Pharaoh ant colonies dynamically regulate reproductive allocation based on colony demography

  • Michael R. Warner
  • Jessica Lipponen
  • Timothy A. Linksvayer
Original Article


The success of social insect colonies is dependent upon efficient and dynamic allocation of resources to alternate queen and worker castes. The developmental and molecular mechanisms regulating the caste fate of individual larvae in response to environmental cues have been the focus of intense study. However, the mechanisms regulating colony-level resource allocation into alternate castes (i.e., caste allocation ratios) are less well studied. Here, we systematically manipulate colony demography to elucidate the social regulatory mechanisms of caste allocation in the ant Monomorium pharaonis. By measuring the effects of demographic manipulation on colony productivity, we infer that caste allocation results from differences in timing and efficiency of culling of very young reproductive-destined larvae, which are always present in colonies. Based on our results, we develop a conceptual model depicting how colonies integrate numerous individual-level caste determination decisions to regulate colony-level caste allocation. We propose that adult workers make decisions about culling larvae based on the ratio of the number of workers to the number of eggs contained in colonies, likely signaled by pheromone present on eggs. This strategy enables the dynamic alteration of colony demography in response to internal and external conditions, which is likely key to the ability of M. pharaonis and similar ants to thrive in disturbed habitats and to become widespread invasive species.

Significance statement

The defining feature of social insect societies is the presence of alternate queen (reproductive) and worker (non-reproductive) castes of individuals. The fitness of social insect colonies is dependent upon efficient allocation of resources to alternate castes, particularly in the case of highly polygynous (multiqueen) societies. However, the mechanisms by which such societies regulate caste allocation are largely unknown. In this study, we perform a range of manipulative studies to disentangle social mechanisms of caste allocation in polygynous ant societies. Based on our results, we develop a model in which colonies manipulate their production of queens (and also males) versus workers according to the present density of eggs in the colony, a reliable indicator of queens’ fertility. Provided egg density is high, colonies kill queen- and male-destined larvae; when egg density falls, colonies begin to rear queens and males. This flexible resource allocation strategy is key to the ability of highly polygynous species to thrive in marginal (often human-associated) habitats.


Caste regulation Superorganism Resource allocation Adaptive demography 



We thank Rohini Singh and Justin Walsh for comments on previous drafts of the manuscript. This research was funded by National Science Foundation award IOS-1452520. MRW was funded by National Science Foundation award DGE-1321851.

Supplementary material

265_2017_2430_MOESM1_ESM.bmp (17.2 mb)
Fig. S1 Colonies that were established with similar sizes (~1.2 mL; ~175 adult workers) but different numbers of queens differed in caste allocation. A) Colonies began producing reproductives before queen removal when started with fewer queens. B) Colonies which we observed producing reproductive pupae in the presence of queens contained fewer eggs two weeks prior to the given observation (approximately the developmental time between caste regulation of 1st instar larvae and pupation), demonstrating that number of eggs affects caste regulation (BMP 17578 kb)
265_2017_2430_MOESM2_ESM.bmp (17.2 mb)
Fig. S2 Initially equal-sized (~1.2 mL; ~175 adult workers) colonies differed in colony productivity according to the number of queens they contained at colony creation. At the time of queen removal (6 weeks after colony creation), there was a positive relationship between the number of queens and the number of A) worker pupae, and B) eggs present in colonies, demonstrating that queen number strongly affects colony productivity (BMP 17578 kb)
265_2017_2430_MOESM3_ESM.bmp (17.2 mb)
Fig. S3 When queens were removed, caste allocation differed between experimental colonies created with two versus four or eight queens. Colonies created with two queens produced higher A) caste ratios (gynes/[gynes + workers]) and B) reproductive ratios ((gynes + males)/(gynes + males + workers)) than those created with four or eight queens. This was the result of increased production of worker pupae in colonies with four and eight queens (B) (BMP 17578 kb)
265_2017_2430_MOESM4_ESM.bmp (8.6 mb)
Fig. S4 When equal-sized colonies were established with two or eight queens, the number of queens that laid the eggs did not affect production of any caste after queen removal. After removing queens, the number of young brood (eggs and 1st instar larvae) was standardized, such that colonies were demographically equivalent, but differed in the number of queens that laid eggs. This demonstrates that the the shift in caste allocation accompanying increased colony size is not dependent upon a maternal effect (BMP 8789 kb)
265_2017_2430_MOESM5_ESM.txt (11 kb)
ESM 1 (TXT 10 kb)
265_2017_2430_MOESM6_ESM.txt (11 kb)
ESM 2 (TXT 11 kb)
265_2017_2430_MOESM7_ESM.txt (1 kb)
ESM 3 (TXT 991 bytes)
265_2017_2430_MOESM8_ESM.txt (1 kb)
ESM 4 (TXT 691 bytes)
265_2017_2430_MOESM9_ESM.txt (1 kb)
ESM 5 (TXT 674 bytes)
265_2017_2430_MOESM10_ESM.txt (2 kb)
ESM 6 (TXT 1 kb)
265_2017_2430_MOESM11_ESM.txt (24 kb)
ESM 7 (TXT 24 kb)
265_2017_2430_MOESM12_ESM.txt (13 kb)
ESM 8 (TXT 13 kb)
265_2017_2430_MOESM13_ESM.r (19 kb)
ESM 9 (R 19 kb)


  1. Anderson KE, Linksvayer TA, Smith CR (2008) The causes and consequences of genetic caste determination in ants (Hymenoptera: Formicidae). Myrmecol News 11:119–132Google Scholar
  2. Arcila AM, Ulloa-Chacon P, Gomez LA (2002) Factors that influence individual fecundity of queens and queen production in crazy ant Paratrechina fulva (Hymenoptera: Formicidae). Sociobiology 39:323–334Google Scholar
  3. Aron S, Passera L, Keller L (1994) Queen-worker conflict over sex ratio: a comparison of primary and secondary sex ratios in the Argentine ant, Iridomyrmex humilis. J Evol Biol 7(4):403–418. CrossRefGoogle Scholar
  4. Aron S, Vargot EL, Passera L (1995) Primary and secondary sex ratios in monogyne colonies of the fire ant. Anim Behav 49(3):749–757. CrossRefGoogle Scholar
  5. Aron S, Keller L, Passera L (2001) Role of resource availability on sex, caste and reproductive allocation ratios in the Argentine ant Linepithema humile. J Anim Ecol 70(5):831–839. CrossRefGoogle Scholar
  6. Aron S, Passera L, Keller L (2004) Evolution of miniaturization in inquiline parasitic ants: timing of male elimination in Plagiolepis pygmaea, the host of Plagiolepis xene. Insect Soc 51(4):395–399. CrossRefGoogle Scholar
  7. Berndt KP, Kremer G (1986) Larvenmorphologie der Pharaoameise Monomorium pharaonis (L.) (Hymenoptera, Formicidae). Zool Anz 216:305–320Google Scholar
  8. Beye M, Hasselmann M, Fondrk MK, Page RE Jr, Omholt SW (2003) The gene csd is the primary signal for sexual development in the honeybee and encodes an SR-type protein. Cell 114(4):419–429. PubMedCrossRefGoogle Scholar
  9. Boonen S, Billen J (2017) Caste regulation in the ant Monomorium pharaonis (L.) with emphasis on the role of queens. Insect Soc 64(1):113–121. CrossRefGoogle Scholar
  10. Børgesen LW (2000) Nutritional function of replete workers in the pharaoh’s ant, Monomorium pharaonis (L.) Insect Soc 47(2):141–146. CrossRefGoogle Scholar
  11. 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(10):1531–1541. CrossRefGoogle Scholar
  12. Boulay R, Arnan X, Cerdá X, Retana J (2014) The ecological benefits of larger colony size may promote polygyny in ants. J Evol Biol 27(12):2856–2863. PubMedCrossRefGoogle Scholar
  13. Bourke AFG (1991) Queen behaviour, reproduction and egg cannibalism in multiple-queen colonies of the ant Leptothorax acervorum. Anim Behav 42(2):295–310. CrossRefGoogle Scholar
  14. Bourke AFG (1997) Sex ratios in bumble bees. Philos Trans R Soc Lond Ser B Biol Sci 352(1364):1921–1933. CrossRefGoogle Scholar
  15. Bourke AFG, Franks NR (1995) Social evolution in ants. Princeton University Press, PrincetonGoogle Scholar
  16. Bourke AFG, Ratnieks FLW (1999) Kin conflict over caste determination in social Hymenoptera. Behav Ecol Sociobiol 46(5):287–297. CrossRefGoogle Scholar
  17. Brian MV (1973) Caste control through worker attack in the ant Myrmica. Insect Soc 20(2):87–102. CrossRefGoogle Scholar
  18. Brian MV (1975) Larval recognition by workers of the ant Myrmica. Anim Behav 23 Part 4:745–756CrossRefGoogle Scholar
  19. Brown WD, Keller L, Sundström L (2002) Sex allocation in mound-building ants: the roles of resources and queen replenishment. Ecology 83(7):1945–1952.[1945:SAIMBA]2.0.CO;2CrossRefGoogle Scholar
  20. Chapuisat M, Liselotte S, Keller L (1997) Sex–ratio regulation: the economics of fratricide in ants. Proc R Soc Lond B Biol Sci 264(1385):1255–1260. CrossRefGoogle Scholar
  21. Cook JM (1993) Sex determination in the Hymenoptera: a review of models and evidence. Heredity London 71(4):421–435. CrossRefGoogle Scholar
  22. Cook JM, Crozier RH (1995) Sex determination and population biology in the hymenoptera. Trends Ecol Evol 10(7):281–286. PubMedCrossRefGoogle Scholar
  23. Creemers B, Billen J, Gobin B (2003) Larval begging behaviour in the ant Myrmica rubra. Ethol Ecol Evol 15(3):261–272. CrossRefGoogle Scholar
  24. Cronin AL, Molet M, Doums C, Monnin T, Peeters C (2013) Recurrent evolution of dependent colony foundation across eusocial insects. Annu Rev Entomol 58(1):37–55. PubMedCrossRefGoogle Scholar
  25. Dussutour A, Simpson SJ (2008) Description of a simple synthetic diet for studying nutritional responses in ants. Insect Soc 55(3):329–333. CrossRefGoogle Scholar
  26. 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(1):31–39. CrossRefGoogle Scholar
  27. Edwards JP (1991) Caste regulation in the pharaoh’s ant Monomorium pharaonis: recognition and cannibalism of sexual brood by workers. Physiol Entomol 16:263–271CrossRefGoogle Scholar
  28. 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(9):2945–2950. PubMedPubMedCentralCrossRefGoogle Scholar
  29. Fersch R, Buschinger A, Heinze J (2000) Queen polymorphism in the Australian ant Monomorium sp.10. Insect Soc 47(3):280–284. CrossRefGoogle Scholar
  30. Fowler HG, Alves LE, Bueno OC (1993) Reproductive strategies of the exotic pharaoh’s ant, Monomorium pharaonis (L.) (Hymenoptera: Formicidae) in Brazil. Invertebr Reprod Dev 23(2-3):235–238. CrossRefGoogle Scholar
  31. Glancey BM, Lofgren CS (1988) Adoption of newly-mated queens: a mechanism for proliferation and perpetuation of polygynous red imported fire ants, Solenopsis invicta Buren. Fla Entomol 71(4):581–587. CrossRefGoogle Scholar
  32. Gordon DM (1996) The organization of work in social insect colonies. Nature 380(6570):121–124. CrossRefGoogle Scholar
  33. Gordon DM, Mehdiabadi NJ (1999) Encounter rate and task allocation in harvester ants. Behav Ecol Sociobiol 45:370–377CrossRefGoogle Scholar
  34. Heimpel GE, de Boer JG (2008) Sex determination in the hymenoptera. Annu Rev Entomol 53(1):209–230. PubMedCrossRefGoogle Scholar
  35. Helanterä H, Strassmann JE, Carrillo J, Queller DC (2009) Unicolonial ants: where do they come from, what are they and where are they going? Trends Ecol Evol 24(6):341–349. PubMedCrossRefGoogle Scholar
  36. Helms KR (1999) Colony sex ratios, conflict between queens and workers, and apparent queen control in the ant Pheidole desertorum. Evolution 53(5):1470–1478. PubMedCrossRefGoogle Scholar
  37. Helms KR, Fewell JH, Rissing SW (2000) Sex ratio determination by queens and workers in the ant Pheidole desertorum. Anim Behav 59(3):523–527. PubMedCrossRefGoogle Scholar
  38. Hölldobler B, Wilson EO (1977) The number of queens: an important trait in ant evolution. Naturwissenschaften 64(1):8–15. CrossRefGoogle Scholar
  39. Hölldobler B, Wilson EO (1990) The ants. Harvard University Press, Cambridge. CrossRefGoogle Scholar
  40. Hölldobler B, Wilson EO (2009) The superorganism: the beauty, elegance, and strangeness of insect societies. W. W. Norton & Company, New YorkGoogle Scholar
  41. Holman L (2012) Costs and constraints conspire to produce honest signaling: insights from an ant queen pheromone. Evolution 66(7):2094–2105. PubMedCrossRefGoogle Scholar
  42. Holman L, Jørgensen CG, Nielsen J, d’Ettorre P (2010) Identification of an ant queen pheromone regulating worker sterility. Proc Biol Sci 277(1701):3793–3800. PubMedPubMedCentralCrossRefGoogle Scholar
  43. Holman L, Lanfear R, d’Ettorre P (2013) The evolution of queen pheromones in the ant genus Lasius. J Evol Biol 26(7):1549–1558. PubMedCrossRefGoogle Scholar
  44. Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50(3):346–363. PubMedCrossRefGoogle Scholar
  45. Howe HF, Smallwood J (1982) Ecology of seed dispersal. Annu Rev Ecol Syst 13(1):201–228. CrossRefGoogle Scholar
  46. Ito F, Higashi S (1990) Tests of four hypotheses on soldier production, by using wild colonies of Pheidole fervida F. Smith (Hymenoptera: Formicidae). Res Popul Ecol 32(1):113–117. CrossRefGoogle Scholar
  47. Jeanne RL, Suryanarayanan S (2011) A new model for caste development in social wasps. Commun Integr Biol 4(4):373–377. PubMedPubMedCentralCrossRefGoogle Scholar
  48. Kaptein N, Billen J, Gobin B (2005) Larval begging for food enhances reproductive options in the ponerine ant Gnamptogenys striatula. Anim Behav 69(2):293–299. CrossRefGoogle Scholar
  49. Keeley JE (1987) Role of fire in seed germination of woody taxa in California chaparral. Ecology 68(2):434–443. CrossRefGoogle Scholar
  50. Keeley JE (1991) Seed germination and life history syndromes in the California chaparral. Bot Rev 57(2):81–116. CrossRefGoogle Scholar
  51. Keller L (1995) Social life: the paradox of multiple-queen colonies. Trends Ecol Evol 10(9):355–360. PubMedCrossRefGoogle Scholar
  52. Keller L, Genoud M (1997) Extraordinary lifespans in ants: a test of evolutionary theories of ageing. Nature 389(6654):958–960. CrossRefGoogle Scholar
  53. Keller L, Passera L (1990) Fecundity of ant queens in relation to their age and the mode of colony founding. Insect Soc 37(2):116–130. CrossRefGoogle Scholar
  54. Keller L, Passera L, Suzzoni JP (1989) Queen execution in the Argentine ant, Iridomyrmex humilis. Physiol Entomol 14(2):157–163. CrossRefGoogle Scholar
  55. Keller L, Aron S, Passera L (1996) Internest sex-ratio variation and male brood survival in the ant Pheidole pallidula. Behav Ecol 7(3):292–298. CrossRefGoogle Scholar
  56. Khila A, Abouheif E (2010) Evaluating the role of reproductive constraints in ant social evolution. Philos Trans R Soc Lond Ser B Biol Sci 365(1540):617–630. CrossRefGoogle Scholar
  57. 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(3):e1005952. PubMedPubMedCentralCrossRefGoogle Scholar
  58. Le Conte Y, Sreng L, Poitout SH (1995) Brood pheromone can modulate the feeding nehavior of Apis mellifera workers (Hymenoptera: Apidae). J Econ Entomol 88(4):798–804. CrossRefGoogle Scholar
  59. Libbrecht R, Corona M, Wende F, Azevedo DO, Serrao JE, Keller L (2013) Interplay between insulin signaling, juvenile hormone, and vitellogenin regulates maternal effects on polyphenism in ants. Proc Natl Acad Sci U S A 110(27):11050–11055. PubMedPubMedCentralCrossRefGoogle Scholar
  60. Lillico-Ouachour A, Abouheif E (2017) Regulation, development, and evolution of caste ratios in the hyperdiverse ant genus Pheidole. Curr Opin Insect Sci 19:43–51. PubMedCrossRefGoogle Scholar
  61. Linksvayer TA, Kaftanoglu O, Akyol E et al (2011) Larval and nurse worker control of developmental plasticity and the evolution of honey bee queen–worker dimorphism. J Evol Biol 24(9):1939–1948. PubMedPubMedCentralCrossRefGoogle Scholar
  62. McGlynn TP, Owen JP (2002) Food supplementation alters caste allocation in a natural population of Pheidole flavens, a dimorphic leaf-litter dwelling ant. Insect Soc 49(1):8–14. CrossRefGoogle Scholar
  63. McGlynn TP, Diamond SE, Dunn RR (2012) Tradeoffs in the evolution of caste and body size in the hyperdiverse ant genus Pheidole. PLoS One 7(10):e48202. PubMedPubMedCentralCrossRefGoogle Scholar
  64. Mehdiabadi NJ, Reeve HK, Mueller UG (2003) Queens versus workers: sex-ratio conflict in eusocial Hymenoptera. Trends Ecol Evol 18(2):88–93. CrossRefGoogle Scholar
  65. Meunier J, West SA, Chapuisat M (2008) Split sex ratios in the social Hymenoptera: a meta-analysis. Behav Ecol 19(2):382–390. CrossRefGoogle Scholar
  66. O’Donnell S (1998) Reproductive caste determination in eusocial wasps (Hymenoptera: Vespidae). Annu Rev Entomol 43(1):323–346. PubMedCrossRefGoogle Scholar
  67. Oster GF, Wilson EO (1978) Caste and ecology in the social insects. Monogr Popul Biol 12:1–352PubMedGoogle Scholar
  68. Pacala SW, Gordon DM, Godfray HCJ (1996) Effects of social group size on information transfer and task allocation. Evol Ecol 10(2):127–165. CrossRefGoogle Scholar
  69. Pamilo P (1991a) Evolution of colony characteristics in social insects. I. Sex allocation. Am Nat 137(1):83–107. CrossRefGoogle Scholar
  70. Pamilo P (1991b) Evolution of colony characteristics in social insects. II. Number of reproductive individuals. Am Nat 138(2):412–433. CrossRefGoogle Scholar
  71. Passera L, Aron S (1996) Early sex discrimination and male brood elimination by workers of the argentine ant. Proc R Soc Lond B Biol Sci 263(1373):1041–1046. CrossRefGoogle Scholar
  72. Passera L, Keller L, Suzzoni JP (1988) Control of brood male production in the Argentine ant Iridomyrmex humilis (Mayr). Insect Soc 35(1):19–33. CrossRefGoogle Scholar
  73. Passera L, Roncin E, Kaufmann B, Keller L (1996) Increased soldier production in ant colonies exposed to intraspecific competition. Nature 379(6566):630–631. CrossRefGoogle Scholar
  74. Passera L, Aron S, Vargo EL, Keller L (2001) Queen control of sex ratio in fire ants. Science 293(5533):1308–1310. PubMedCrossRefGoogle Scholar
  75. Peacock AD (1950) Studies in Pharaoh’s ant, Monomorium pharaonis (L.), 3: life history. Entomol Mon Mag 86:171–178Google Scholar
  76. Pearcy M, Aron S (2006) Local resource competition and sex ratio in the ant Cataglyphis cursor. Behav Ecol 17(4):569–574. CrossRefGoogle Scholar
  77. Penick CA, Liebig J (2012) Regulation of queen development through worker aggression in a predatory ant. Behav Ecol 23(5):992–998. CrossRefGoogle Scholar
  78. Penick CA, Liebig J (2017) A larval “princess pheromone” identifies future ant queens based on their juvenile hormone content. Anim Behav 128:33–40.
  79. Petersen-Braun M (1977) Untersuchungen zur sozialen Organisation der Pharaoameise Monomorium pharaonis L. (Hymenoptera, Formicidae) II. Die Kastendeterminierung. Insect Soc 24(4):303–318. CrossRefGoogle Scholar
  80. Queller DC, Strassmann JE (1998) Kin selection and social insects. Bioscience 48(3):165–175. CrossRefGoogle Scholar
  81. R Core Team (2017) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
  82. Rosset H, Chapuisat M (2006) Sex allocation conflict in ants: when the queen rules. Curr Biol 16(3):328–331. PubMedCrossRefGoogle Scholar
  83. Schmidt AM, Linksvayer TA, Boomsma JJ, Pedersen JS (2011) Queen–worker caste ratio depends on colony size in the pharaoh ant (Monomorium pharaonis). Insect Soc 58(2):139–144. CrossRefGoogle Scholar
  84. Schwander T, Humbert J-Y, Brent CS, Cahan SH, Chapuis L, Renai E, Keller L (2008) Maternal effect on female caste determination in a social insect. Curr Biol 18(4):265–269. PubMedCrossRefGoogle Scholar
  85. Schwander T, Lo N, Beekman M, Oldroyd BP, Keller L (2010) Nature versus nurture in social insect caste differentiation. Trends Ecol Evol 25(5):275–282. PubMedCrossRefGoogle Scholar
  86. Slessor KN, Winston ML, Le Conte Y (2005) Pheromone communication in the honeybee (Apis mellifera L.) J Chem Ecol 31(11):2731–2745. PubMedCrossRefGoogle Scholar
  87. Suryanarayanan S, Hermanson JC, Jeanne RL (2011) A mechanical signal biases caste development in a social wasp. Curr Biol 21(3):231–235. PubMedCrossRefGoogle Scholar
  88. Tay JW, Neoh KB, Lee CY (2014) The roles of the queen, brood, and worker castes in the colony growth dynamics of the pharaoh ant, Monomorium pharaonis (Hymenoptera: Formicidae). Myrmecol News 20:87–94Google Scholar
  89. Trible W, Kronauer DJC (2017) Caste development and evolution in ants: it’s all about size. J Exp Biol 220(1):53–62. PubMedCrossRefGoogle Scholar
  90. Tschinkel WR (1993) Resource allocation, brood production and cannibalism during colony founding in the fire ant, Solenopsis invicta. Behav Ecol Sociobiol 33(4):209–223. CrossRefGoogle Scholar
  91. Van Oystaeyen A, Oliveira RC, Holman L, van Zweden JS, Romero C, Oi CA, d’Ettorre P, Khalesi M, Billen J, Wackers F, Millar JG, Wenseleers T (2014) Conserved class of queen pheromones stops social insect workers from reproducing. Science 343(6168):287–290. PubMedCrossRefGoogle Scholar
  92. Vargo EL (1992) Mutual pheromonal inhibition among queens in polygyne colonies of the fire ant Solenopsis invicta. Behav Ecol Sociobiol 31:205–210CrossRefGoogle Scholar
  93. Vargo EL, Fletcher DJC (1986) Queen number and the production of sexuals in the fire ant, Solenopsis invicta (Hymenoptera: Formicidae). Behav Ecol Sociobiol 19(1):41–47. CrossRefGoogle Scholar
  94. Vargo EL, Fletcher DJC (1987) Effect of queen number on the production of sexuals in natural populations of the fire ant, Solenopsis invicta. Physiol Entomol 12(1):109–116. CrossRefGoogle Scholar
  95. 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 28:161–169CrossRefGoogle Scholar
  96. Vargo EL, Passera L (1992) Gyne development in the Argentine ant Iridomyrmex humilis: role of overwintering and queen control. Physiol Entomol 17(2):193–201. CrossRefGoogle Scholar
  97. Villalta I, Angulo E, Devers S et al (2015) Regulation of worker egg laying by larvae in a fission-performing ant. Anim Behav 106:149–156CrossRefGoogle Scholar
  98. Villalta I, Amor F, Cerdá X, Boulay R (2016) Social coercion of larval development in an ant species. Naturwissenschaften 103(3-4):18. PubMedCrossRefGoogle Scholar
  99. Warner MR, Kovaka K, Linksvayer TA (2016) Late-instar ant worker larvae play a prominent role in colony-level caste regulation. Insect Soc 63(4):575–583. CrossRefGoogle Scholar
  100. Warner MR, Mikheyev AS, Linksvayer TA (2017) Genomic signature of kin selection in an ant with obligately sterile workers. Mol Biol Evol 34(7):1780–1787. PubMedPubMedCentralCrossRefGoogle Scholar
  101. Wheeler WM (1911) The ant-colony as an organism. J Morphol 22(2):307–325. CrossRefGoogle Scholar
  102. Wheeler DE (1986) Developmental and physiological determinants of caste in social hymenoptera: evolutionary implications. Am Nat 128(1):13–34. CrossRefGoogle Scholar
  103. Wheeler DE, Nijhout HF (1981) Soldier determination in ants: new role for juvenile hormone. Science 213(4505):361–363. PubMedCrossRefGoogle Scholar
  104. Wheeler DE, Nijhout HF (1984) Soldier determination in Pheidole bicarinata: inhibition by adult soldiers. J Insect Physiol 30(2):127–135. CrossRefGoogle Scholar
  105. Wickham H (2016) ggplot2: elegant graphics for data analysis. Springer, Berlin. CrossRefGoogle Scholar
  106. Wilson EO (1971) The insect societies. Harvard University Press, CambridgeGoogle Scholar
  107. Wilson EO (1985) The sociogenesis of insect colonies. Science 228(4707):1489–1495. PubMedCrossRefGoogle Scholar
  108. Yang AS, Martin CH, Nijhout HF (2004) Geographic variation of caste structure among ant populations. Curr Biol 14(6):514–519. PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of BiologyUniversity of PennsylvaniaPhiladelphiaUSA

Personalised recommendations