Worker division of labor and endocrine physiology are associated in the harvester ant, Pogonomyrmex californicus

Journal of Experimental Biology

Volumn 215, Issue 3, 2012, Pages 454-460

  Dolezal, Adam G ^a   Brent, Colin S ^b   Hölldobler, Bert ^a,c   Amdam, Gro V ^a,d  

^a ARIZONA STATE UNIVERSITY   (United States)

^b US Arid Land Agricultural Research Station   (United States)

^c UNIVERSITY OF WÜRZBURG   (Germany)

^d NORWEGIAN UNIVERSITY OF LIFE SCIENCES   (Norway)

Author keywords

Behavior; Division of labor; Ecdysteroids; Endocrine; Formicidae; Juvenile hormone

Indexed keywords

ECDYSTEROID; JUVENILE HORMONE;

ANIMAL; ANIMAL BEHAVIOR; ANT; ARTICLE; ENDOCRINE SYSTEM; PHYSIOLOGY; REPRODUCTION; SOCIAL BEHAVIOR;

ANIMALS; ANTS; BEHAVIOR, ANIMAL; ECDYSTEROIDS; ENDOCRINE SYSTEM; JUVENILE HORMONES; REPRODUCTION; SOCIAL BEHAVIOR;

FORMICIDAE; POGONOMYRMEX CALIFORNICUS;

EID: 84856623295     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.060822     Document Type: Article

References (60)

1. Amdam, G. V. and Omholt, S. W. (2003). The hive bee to forager transition in honeybee colonies: The double repressor hypothesis. J. Theor. Biol. 223, 451-464. (Pubitemid 36875741)
2. Amdam, G. V. and Page, R. E. (2010). The developmental genetics and physiology of honeybee societies. Anim. Behav. 79, 973-980.
3. Amdam, G. V., Norberg, K., Hagen, A. and Omholt, S. W. (2003). Social exploitation of vitellogenin. Proc. Natl. Acad. Sci. USA 100, 1799-1802. (Pubitemid 36254528)
4. Amdam, G. V., Norberg, K., Fondrk, M. K. and Page, R. E. (2004). Reproductive ground plan may mediate colony-level selection effects on individual foraging behavior in honey bees. Proc. Natl. Acad. Sci. USA 101, 11350-11355. (Pubitemid 39038350)
5. Amdam, G. V., Csondes, A., Fondrk, M. K. and Page, R. E. (2006). Complex social behavior derived from maternal reproductive traits. Nature 439, 76-78. (Pubitemid 43053631)
6. Ben-Shahar, Y., Robichon, A., Sokolowski, M. B. and Robinson, G. E. (2002). Influence of gene action across different time scales on behavior. Science 296, 741-744. (Pubitemid 34442003)
7. Beshers, S. N. and Fewell, J. H. (2001). Models of division of labor in social insects. Annu. Rev. Entomol 46, 413-440. (Pubitemid 32304995)
8. Bloch, G., Borst, D. W., Huang, Z.-Y., Robinson, G. E., Cnaani, J. and Hefetz, A. (2000a). Juvenile hormone titers, juvenile hormone biosynthesis, ovarian development and social environment in Bombus terrestris. J. Insect Physiol. 46, 47-57. (Pubitemid 29498172)
9. Bloch, G., Hefetz, A. and Hartfelder, K. (2000b). Ecdysteroid titer, ovary status, and dominance in adult worker and queen bumble bees (Bombus terrestris). J. Insect Physiol. 46, 1033-1040. (Pubitemid 30317772)
10. Bonasio, R., Zhang, G. J., Ye, C. Y., Mutti, N. S., Fang, X. D., Qin, N., Donahue, G., Yang, P. C., Li, Q. Y., Li, C. et al. (2010). Genomic comparison of the ants Camponotus floridanus and Harpegnathos saltator. Science 329, 1068-1071.
11. Brady, S. G., Schultz, T. R., Fisher, B. L. and Ward, P. S. (2006). Evaluating alternative hypotheses for the early evolution and diversification of ants. Proc. Natl. Acad. Sci. USA 103, 18172-18177. (Pubitemid 44871631)
12. Brent, C. S., Peeters, C., Dietemann, V., Crewe, R. and Vargo, E. L. (2006). Hormonal correlates of reproductive status in the queenless Ponerine ant, Streblognathus peetersi. J. Comp. Physiol. A 192, 315-320. (Pubitemid 43260977)
13. Crailsheim, K. and Stolberg, E. (1989). Influence of diet, age and colony condition upon intestinal proteolytic activity and size of the hypopharyngeal glands in the honeybee (Apis mellifera L). J. Insect Physiol. 35, 595-602.
14. Dolezal, A. G., Brent, C. S., Gadau, J., Holldobler, B. and Amdam, G. V. (2009). Endocrine physiology of the division of labour in Pogonomyrmex californicus founding queens. Anim. Behav. 77, 1005-1010.
15. Dong, S. Z., Ye, G. Y., Guo, J. Y. and Hu, C. (2009). Roles of ecdysteroid and juvenile hormone in vitellogenesis in an endoparasitic wasp, Pteromalus puparum (Hymenoptera: Pteromalidae). Gen. Comp. Endocrinol. 160, 102-108.
16. Ehrhardt, S. (1931). Über Arbeitsteilung bei Myrmica- und Messor-Arten. Zeitschrift für Morphologie und Ökologie der Tiere 20, 755-812.
17. Engels, W. and Imperatriz-Fonseca, V. L. (1990). Caste development, reproductive strategies, and control of fertility in honey bees and stingless bees. In Social Insects: An Evolutionary Approach to Castes and Reproduction (ed. W. Engels). Berlin: Springer-Verlag.
18. Giray, T., Giovanetti, M. and West-Eberhard, M. J. (2005). Juvenile hormone, reproduction, and worker behavior in the neotropical social wasp Polistes canadensis. Proc. Natl. Acad. Sci. USA 102, 3330-3335. (Pubitemid 40328045)
19. Gobin, B. and Ito, F. (2000). Queens and major workers of Acanthomyrmex ferox redistribute nutrients with trophic eggs. Naturwissenschaften 87, 323-326.
20. Gronenberg, W., Heeren, S. and Holldobler, B. (1996). Age-dependent and taskrelated morphological changes in the brain and the mushroom bodies of the ant Camponotus floridanus. J. Exp. Biol. 199, 2011-2019. (Pubitemid 26352509)
21. Haight, K. L. (2006). Defensiveness of the fire ant, Solenopsis invicta, is increased during colony rafting. Insectes Sociaux 53, 32-36.
22. Haight, K. L. (2008). Ontogeny of the defensive stinging behavior of the fire ant, Solenopsis invicta. J. Insect Behav. 21, 147-152.
23. Hartfelder, K. (2000). Insect juvenile hormone: From ?status quo' to high society. Braz. J. Med. Biol. Res. 33, 157-177.
24. Hartfelder, K., Bitondi, M. M. G., Santana, W. C. and Simões, Z. L. P. (2002). Ecdysteroid titer and reproduction in queens and workers of the honey bee and of a stingless bee: Loss of ecdysteroid function at increasing levels of sociality? Insect Biochem. Mol. Biol. 32, 211-216. (Pubitemid 34076085)
25. Hölldobler, B. and Wilson, E. O. (1990). The Ants. Cambridge MA: Belknap Press of Harvard University Press.
26. Hölldobler, B. and Wilson, E. O. (2009). The Superorganism: The Beauty, Elegance, and Strangeness of Insect Societies. New York: W. W. Norton.
27. Huang, Z.-Y. and Robinson, G. E. (1995). Seasonal changes in juvenile hormone titers and rates of biosynthesis in honey bees. J. Comp. Physiol. B 165, 18-28.
28. Hunt, G. J., Amdam, G. V., Schlipalius, D., Emore, C., Sardesai, N., Williams, C. E., Rueppell, O., Guzman-Novoa, E., Arechavaleta-Velasco, M., Chandra, S. et al. (2007). Behavioral genomics of honeybee foraging and nest defense. Naturwissenschaften 94, 247-267. (Pubitemid 46452155)
29. Ihle, K. E., Page, R. E., Frederick, K., Fondrk, M. K. and Amdam, G. V. (2010). Genotype effect on regulation of behaviour by vitellogenin supports reproductive origin of honeybee foraging bias. Anim. Behav. 79, 1001-1006.
30. Jaycox, E. R., Skowronek, W. and Guynn, G. (1974). Behavioral changes in worker honey bees (Apis mellifera) induced by injections of a juvenile hormone mimic. Ann. Entomol. Soc. Am. 67, 529-534.
31. Johnson, R. A. (2000). Seed-harvester ants (Hymenoptera: Formicidae) of North America: An overview of ecology and biogeography. Sociobiology 36, 89-122. (Pubitemid 33223938)
32. Khila, A. and Abouheif, E. (2008). Reproductive constraint is a developmental mechanism that maintains social harmony in advanced ant societies. Pro. Natl. Acad. Sci. USA 105, 17884-17889.
33. Moreau, C. S., Bell, C. D., Vila, R., Archibald, S. B. and Pierce, N. E. (2006). Phylogeny of the ants: Diversification in the age of angiosperms. Science 312, 101-104.
34. Naiem, E. S., Hrassnigg, N. and Crailsheim, K. (1999). Nurse bees support the physiological development of young bees (Apis mellifera L.). J. Comp. Physiol. B 169, 271-279. (Pubitemid 29358141)
35. Nelson, F. C. (1927). Adaptability of young bees under adverse conditions. Am. Bee J. 67, 242-243.
36. Raikhel, A. S., Brown, M. and Belles, X. (2005). Hormonal control of reproductive processes. In Comprehensive Molecular Insect Science (ed. L. Gilbert, S. Gill and K. Iatrou) pp. 433-491. Boston, MA, USA: Elsevier Press.
37. Robinson, G. E. (1987). Regulation of honey bee age polyethism by juvenile hormone. Behav. Ecol. Sociobiol. 20, 329-338.
38. Robinson, G. E. (1992). Regulation of division of labor in insect societies. Annu. Rev. Entomol. 37, 637-665. (Pubitemid 24406665)
39. Robinson, G. E. and Vargo, E. L. (1997). Juvenile hormone in adult eusocial Hymenoptera: Gonadotropin and behavioral pacemaker. Arch. Insect Biochem. Physiol. 35, 559-583. (Pubitemid 127705854)
40. Robinson, G. E., Page, R. E., Strambi, C. and Strambi, A. (1989). Hormonal and genetic control of behavioral integration in honey bee colonies. Science 246, 109-111.
41. Robinson, G. E., Strambi, C., Strambi, A. and Feldlaufer, M. F. (1991). Comparison of juvenile hormone and ecdysteroid hemolymph titers in adult worker and queen honey-bees (Apis mellifera). J. Insect Physiol. 37, 929-935.
42. Röseler, P. F., Röseler, I. and Strambi, A. (1985). Role of ovaries and ecdysteroids in dominance hierarchy establishment among foundresses of the primitively social wasp, Polistes gallicus. Behav. Ecol. Sociobiol. 18, 9-13.
43. Rueppell, O., Pankiw, T. and Page, R. E. (2004). Pleiotropy, epistasis and new QTL: The genetic architecture of honey bee foraging behavior. J. Heredity 95, 481-491. (Pubitemid 39383156)
44. Shu, S. Q., Park, Y. I., Ramaswamy, S. B. and Srinivasan, A. (1997). Hemolymph juvenile hormone titers in pupal and adult stages of southwestern corn borer [Diatraea grandiosella (Pyralidae)] and relationship with egg development. J. Insect Physiol. 43, 719-726. (Pubitemid 27430221)
45. Smith, C. D., Zimin, A., Holt, C., Abouheif, E., Benton, R., Cash, E., Croset, V., Currie, C. R., Elhaik, E., Elsik, C. G. et al. (2011). Draft genome of the globally widespread and invasive Argentine ant (Linepithema humile). Proc. Natl. Acad. Sci. USA 108, 5673-5678.
46. Smith, C. R., Dolezal, A. G., Eliyahu D., Holbrook C. T. and Gadau, J. (2009). Ants (Formicidae): Models for social complexity. CSH Protocols, Vol. 3, issue 7.
47. Smith, C. R., Smith, C. D., Robertson, H. M., Helmkampf, M., Zimin, A., Yandell, M., Holt, C., Hu, H., Abouheif, E., Benton, R. et al. (2011). Draft genome of the red harvester ant Pogonomyrmex barbatus. Proc. Natl. Acad. Sci. USA 108, 5667-5672.
48. Suen, G., Teiling, C., Li, L., Holt, C., Abouheif, E., Bornberg-Bauer, E., Bouffard, P., Caldera, E. J., Cash, E., Cavanaugh, A. et al. (2011). The genome sequence of the leaf-cutter ant Atta cephalotes reveals insights into its obligate symbiotic lifestyle. PLoS Genetics 7, 1-11.
49. Sullivan, J. P., Jassim, O., Fahrbach, S. E. and Robinson, G. E. (2000). Juvenile hormone paces behavioral development in the adult worker honey bee. Hormon. Behav. 37, 1-14. (Pubitemid 30155445)
50. Tschinkel, W. R. (2006). The Fire Ants. Cambridge, MA: The Belknap Press of Harvard University Press.
51. Velarde, R. A., Robinson, G. E. and Fahrbach, S. E. (2009). Coordinated responses to developmental hormones in the Kenyon cells of the adult worker honey bee brain (Apis mellifera L.). J. Insect Physiol. 55, 59-69.
52. Wang, Y., Amdam, G. V., Rueppell, O., Wallrichs, M. A., Fondrk, M. K., Kaftanoglu, O. and Page, R. E. (2009). PDK1 and HR46 gene homologs tie social behavior to ovary signals. PLoS One 4, e4899.
53. Wang, Y., Kaftanoglu, O., Siegel, A. J., Page, R. E. and Amdam, G. V. (2010). Surgically increased ovarian mass in the honey bee confirms link between reproductive physiology and worker behavior. J. Insect Physiol. 56, 1816-1824.
54. West-Eberhard, M. J. (1987). Flexible strategy and social evolution. In Animal Societies: Theories and Facts (ed. Y. Itô, J. L. Brown and J. Kikkawa), pp. 35-51. Tokyo: Japan Science Society Press.
55. West-Eberhard, M. J. (1996). Wasp societies as microcosms for the study of development and evolution. In Natural History and Evolution of Paper Wasp (ed. S. Turillazzi and M. J. West-Eberhard), pp. 290-317. New York: Oxford University Press.
56. Wilson, E. O. (1971). The Insect Societies. Cambridge, MA: Belknap Press of Harvard University Press.
57. Wilson, E. O. and Eisner, T. (1957). Quantitative studies of liquid food transmission in ants. Insectes Sociaux 4, 157-166.
58. Winston, M. L. (1987). The Biology of the Honey Bee. Cambridge, MA: Harvard University Press.
59. Wurm, Y., Wang, J., Riba-Grognuz, O., Corona, M., Nygaard, S., Hunt, B. G., Ingram, K. K., Falquet, L., Nipitwattanaphon, M., Gotzek, D. et al. (2011). The genome of the fire ant Solenopsis invicta. Proc. Natl. Acad. Sci. USA 108, 5679-5684.
60. Yamazaki, Y., Kiuchi, M., Takeuchi, H. and Kubo, T. (2011). Ecdysteroid biosynthesis in workers of the European honeybee Apis mellifera L. Insect Biochem. Mole. Biol. 41, 283-293.