Physiological variation as a mechanism for developmental caste-biasing in a facultatively eusocial sweat bee

Proceedings of the Royal Society B: Biological Sciences

Volumn 279, Issue 1732, 2012, Pages 1437-1446

  Kapheim, Karen M ^a   Smith, Adam R ^b,e   Ihle, Kate E ^b,c   Amdam, Gro V ^c,d   Nonacs, Peter ^a   Wcislo, William T ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b SMITHSONIAN TROPICAL RESEARCH INSTITUTE   (Panama)

^c ARIZONA STATE UNIVERSITY   (United States)

^d NORWEGIAN UNIVERSITY OF LIFE SCIENCES   (Norway)

^e UNIVERSITY OF LEEDS   (United Kingdom)

Author keywords

Caste determination; Division of labour; Ground plan; Megalopta genalis; Social evolution; Vitellogenin

Indexed keywords

BEE; BODY SIZE; CASTE; EUSOCIALITY; HYPOTHESIS TESTING; LABOR DIVISION; ONTOGENY; PHYSIOLOGICAL RESPONSE;

APOIDEA; HALICTINAE; HEXAPODA; MEGALOPTA GENALIS;

EID: 84863275175     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2011.1652     Document Type: Article

References (72)

1. Hunt, J. H. & Amdam, G. V. 2005 Bivoltinism as an antecedent to eusociality in the paper wasp genus Polistes. Science 308, 264-267.
2. Amdam, G. V., Norberg, K., Fondrk, M. K. & Page Jr, 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, 11 350-11 355. (doi:10.1073/pnas.0403073101)
3. West-Eberhard, M. J. 1987 Flexible strategy and social evolution. In Animal societies: theories and facts (eds Y. Ito, J. L. Brown & J. Kikkawa), pp. 35-51. Tokyo, Japan: Japan Scientific Societies Press.
4. West-Eberhard, M. J. 1996 Wasp societies as microcosms for the study of development and evolution. In Natural history and evolution of paper wasps (eds S. Turillazzi & M. J. West Eberhard), pp. 290-317. Oxford, UK: Oxford University Press.
5. Linksvayer, T. A. & Wade, M. J. 2005 The evolutionary origin and elaboration of sociality in the aculeateHymenoptera: maternal effects, sib-social effects, and heterochrony. Q. Rev. Biol. 80, 317-336. (doi:10.1086/432266)
6. Corona, M., Estrada, E. & Zurita, M. 1999 Differential expression of mitochondrial genes between queens and workers during caste determination in the honeybee Apis mellifera. J. Exp. Biol. 202, 929-938.
7. Evans, J. D. & Wheeler, D. E. 1999 Differential gene expression between developing queens and workers in the honey bee, Apis mellifera. Proc. Natl Acad. Sci. USA 96, 5575-5580. (doi:10.1073/pnas.96.10.5575)
8. Hayashi, Y., Lo, N., Miyata, H. & Kitade, O. 2007 Sexlinked genetic influence on caste determination in a termite. Science 318, 985-987. (doi:10.1126/science.1146711)
9. Hughes, W. O. H., Sumner, S., Van Borm, S. & Boomsma, J. J. 2003 Worker caste polymorphism has a genetic basis in Acromyrmex leaf-cutting ants. Proc. Natl Acad. Sci. USA 100, 9394-9397. (doi:10.1073/pnas.1633701100)
10. Linksvayer, T. A., Wade, M. J. & Gordon, D. M. 2006 Genetic caste determination in harvester ants: possible origin and maintenance by cyto-nuclear epistasis. Ecology 87, 2185-2193. (doi:10.1890/0012-9658(2006)87[2185:GCDIHA]2.0.CO;2)
11. Pereboom, J. J. M., Jordan, W. C., Sumner, S., Hammond, R. L. & Bourke, A. F. G. 2005 Differential gene expression in queen-worker caste determination in bumble-bees. Proc. R. Soc. B 272, 1145-1152. (doi:10.1098/rspb.2005.3060)
12. Wheeler, D. E., Buck, N. & Evans, J. D. 2006 Expression of insulin pathway genes during the period of caste determination in the honey bee, Apis mellifera. Insect Mol. Biol. 15, 597-602. (doi:10.1111/j.1365-2583.2006.00681.x)
13. Maleszka, R. 2008 Epigenetic integration of environmental and genomic signals in honey bees. Epigenetics 3, 188-192. (doi:10.4161/epi.3.4.6697)
14. Amdam, G., Nilsen, K. A., Norberg, K., Fondrk, M. K. & Hartfelder, K. 2007 Variation in endocrine signaling underlies variation in social life history. Am. Nat. 170, 37-46. (doi:10.1086/518183)
15. Amdam, G. V., Csondes, A., Fondrk, M. K. & Page, R. E. 2006 Complex social behaviour derived from maternal reproductive traits. Nature 439, 76-78. (doi:10.1038/nature04340)
16. Amdam, G. V., Norberg, K., Hagen, A. & Omholt, S. W. 2003 Social exploitation of vitellogenin. Proc. Natl Acad. Sci. USA 100, 1799-1802. (doi:10.1073/pnas.0333979100)
17. Amdam, G. V. & Omholt, S.W. 2003 The hive bee to forager transition in honeybee colonies: the double repressor hypothesis. J. Theor. Biol. 223, 451-464. (doi:10.1016/ S0022-5193(03)00121-8)
18. Nelson, C. M., Ihle, K. E., Fondrk, M. K., Page, R. E. & Amdam, G. V. 2007 The gene vitellogenin has multiple coordinating effects on social organization. PLoS Biol. 5, e62. (doi:10.1371/journal.pbio.0050062)
19. Page, R. E. & Amdam, G. V. 2007 The making of a social insect: developmental architectures of social design. BioEssays 29, 334-343. (doi:10.1002/bies.20549)
20. Patel, A., Fondrk, M. K., Kaftanoglu, O., Emore, C., Hunt, G., Frederick, K., Amdam, G. V. & Michalak, P. 2007 The making of a queen: TOR pathway is a key player in diphenic caste development. PLoS ONE, 2e509. (doi:10.1371/journal.pone.0000509)
21. Wcislo, W. T. 1997 Behavioral environments of sweat bees (Halictinae) in relation to variability in social organization. In Social behavior in insects and arachnids (eds J. C. Choe & B. J. Crespi), pp. 316-332. Cambridge, UK: Cambridge University Press.
22. Schwarz, M. P., Richards, M. H. & Danforth, B. N. 2007 Changing paradigms in insect social evolution: insights from Halictine and Allodapine bees. Annu. Rev. Entomol. 52, 127-150. (doi:10.1146/annurev.ento.51.110104.150950)
23. Nowak, M. A., Tarnita, C. E. & Wilson, E. O. 2010 The evolution of eusociality. Nature 466, 1057-1062. (doi:10.1038/nature09205)
24. Johnson, B. R. & Linksvayer, T. A. 2010 Deconstructing the superorganism: social physiology, groundplans, and sociogenomics. Q. Rev. Biol. 85, 57-79. (doi:10.1086/650290)
25. Sherman, P. W., Lacey, E. A., Reeve, H. K. & Keller, L. 1995 The eusociality continuum. Behav. Ecol. 6, 102-108. (doi:10.1093/beheco/6.1.102)
26. Michener, C. D. 1990 Reproduction and castes in social halictine bees. In Social insects: an evolutionary approach to castes and reproduction (ed. W. Engels). New York, NY: Springer.
27. O'Donnell, S. 1998 Reproductive caste determination in eusocial wasps (Hymenoptera: Vespidae). Annu. Rev. Entomol. 43, 323-346. (doi:10.1146/annurev.ento.43.1.323)
28. Keller, L. 2009 Adaptation and the genetics of social behaviour. Phil. Trans. R. Soc. B 364, 3209-3216. (doi:10.1098/rstb.2009.0108)
29. West-Eberhard, M. J. 2003 Developmental plasticity and evolution. Oxford, UK: Oxford University Press.
30. Wcislo, W. T. 2000 Environmental hierarchy, behavioral contexts, and social evolution in insects. In Ecologia e comportameno de insetos (eds R. P. Martins, T. M. Lewinsohn & M. S. Barbeitos), pp. 49-84. Rio de Janeiro, Brasil: PPGE-UFRJ.
31. Wcislo, W. T., Arneson, L., Roesch, K., Gonzalez, V., Smith, A. & Fernandez, H. 2004 The evolution of nocturnal behaviour in sweat bees, Megalopta genalis and M. ecuadoria (Hymenoptera: Halictidae): an escape from competitors and enemies? Biol. J. Linn. Soc. 83, 377-387. (doi:10.1111/j.1095-8312.2004.00399.x)
32. Kapheim, K. M. 2010 Maternal effects and the evolution of sociality in a facultatively eusocial sweat bee, Megalopta genalis. PhD dissertation, University of California, Los Angeles, CA.
33. Smith, A. R., Wcislo, W. T. & O'Donnell, S. 2007 Survival and productivity benefits to social nesting in the sweat bee Megalopta genalis (Hymenoptera: Halictidae). Behav. Ecol. Sociobiol. 61, 1111-1120. (doi:10.1007/s00265-006-0344-4)
34. Wcislo, W. T. & Gonzalez, V. H. 2006 Social and ecological contexts of trophallaxis in facultatively social sweat bees, Megalopta genalis and M. ecuadoria (Hymenoptera, Halictidae). Insect Sociaux 53, 220-225. (doi:10.1007/ s00040-005-0861-6)
35. Kapheim, K., Bernal, S., Smith, A. R., Nonacs, P. & Wcislo, W. 2011 Support for maternal manipulation of developmental nutrition in a facultatively eusocial bee, Megalopta genalis (Halictidae). Behav. Ecol. Sociobiol. 65, 1179-1190. (doi:10.1007/s00265-010-1131-9)
36. Frank, S. A. 1995 Sex allocation in solitary bees and wasps. Am. Nat. 146, 316-323. (doi:10.1086/285802)
37. Charnov, E. L. 1982 The theory of sex allocation. Princeton, NJ: Princeton University Press.
38. Rosenheim, J. A., Nonacs, P. & Mangel, M. 1996 Sex ratios and multifaceted parental investment. Am. Nat. 148, 501-535. (doi:10.1086/285937)
39. Smith, A. R., Wcislo, W. & O'Donnell, S. 2008 Body size shapes caste expression, and cleptoparasitism reduces body size in the facultatively eusocial bees Megalopta (Hymenoptera: Halictidae). J. Insect Behav. 21, 394-406. (doi:10.1007/s10905-008-9136-1)
40. Smith, A. R., Kapheim, K. M., O'Donnell, S. & Wcislo, W. T. 2009 Social competition but not subfertility leads to a division of labour in the facultatively social sweat bee Megalopta genalis (Hymenoptera: Halictidae). Anim. Behav. 78, 1043-1050. (doi:10.1016/j.anbehav.2009.06.032)
41. Tierney, S. M., Gonzales-Ojeda, T. & Wcislo, W. T. 2008 Nesting biology and social behavior of Xenochlora bees (Hymenoptera: Halictidae: Augochlorini). J. Kansas Entomol. Soc. 81, 61-72. (doi:10.2317/JKES-704.24.1)
42. Smith, A. R., Seid, M. A., Jiménez, L. C. & Wcislo, W. T. 2010 Socially induced brain development in a facultatively eusocial sweat bee Megalopta genalis (Halictidae). Proc. R. Soc. B 277, 2157-2163. (doi:10.1098/rspb.2010.0269)
43. Sappington, T. W. & Raikhel A. S. 1998 Molecular characteristics of insect vitellogenins and vitellogenin receptors. Insect Biochem. Mol. Biol. 28, 277-300. (doi:10.1016/S0965-1748(97)00110-0)
44. Tufail, M. & Takeda, M. 2008 Molecular characteristics of insect vitellogenins. J. Insect Physiol. 54, 1447-1458. (doi:10.1016/j.jinsphys.2008.08.007)
45. Ziegler, R. & Van Antwerpen, R. 2006 Lipid uptake by insect oocytes. Insect Biochem. Mol. Biol. 36, 264-272. (doi:10.1016/j.ibmb.2006.01.014)
46. Engels, W. 1974 Occurrence and significance of vitellogenins in female castes of social Hymenoptera. Am. Zool. 14, 1229-1237.
47. Byrne, B. M., Gruber, M. & Ab, G. 1989 The evolution of egg yolk proteins. Prog. Biophys. Mol. Biol. 53, 33-69. (doi:10.1016/0079-6107(89)90005-9)
48. Guidugli, K. R., Nascimento, A. M., Amdam, G. V., Barchuk, A. R., Omholt, S., Simoes, Z. L. P. & Hartfelder, K. 2005 Vitellogenin regulates hormonal dynamics in the worker caste of a eusocial insect. FEBS Lett. 579, 4961-4965. (doi:10.1016/j.febslet.2005.07.085)
49. MacQueen, J. 1967 Some methods for classification and analysis of multivariate observations. In Proc. Fifth Berkeley Symp. Mathematical Statistics and Probability (Berkeley, California, 1965/66), pp. 281-297. Berkeley, CA: University of California Press.
50. Brady, S. G., Sipes, S., Pearson, A. & Danforth, B. N. 2006 Recent and simultaneous origins of eusociality in halictid bees. Proc. R. Soc. B 273, 1643-1649. (doi:10.1098/rspb.2006.3496)
51. Danforth, B. N. 2002 Evolution of sociality in a primitively eusocial lineage of bees. Proc. Natl Acad. Sci. USA 99, 286-290. (doi:10.1073/pnas.012387999)
52. Toth, A., Bilof, K., Henshaw, M., Hunt, J. & Robinson, G. 2009 Lipid stores, ovary development, and brain gene expression in Polistes metricus females. Insectes Sociaux 56, 77-84. (doi:10.1007/s00040-008-1041-2)
53. Roma, G. C., Bueno, O. C. & Camargo-Mathias, M. I. 2010 Morpho-physiological analysis of the insect fat body: a review. Micron 41, 395-401. (doi:10.1016/j. micron.2009.12.007)
54. Michener, C. D. & Brothers, D. J. 1974 Were workers of eusocial Hymenoptera initially altruistic or oppressed? Proc. Natl Acad. Sci. USA 71, 671-674. (doi:10.1073/ pnas.71.3.671)
55. Keeping, M. G. 2002 Reproductive and worker castes in the primitively eusocial wasp Belonogaster petiolata (DeGeer) (Hymenoptera: Vespidae): evidence for preimaginal differentiation. J. Insect Physiol. 48, 867-879. (doi:10.1016/S0022-1910(02)00156-7)
56. Gadagkar, R., Bhagavan, S., Chandrashekara, K. & Vinutha, C. 1991 The role of larval nutrition in preimaginal biasing of caste in the primitively eusocial wasp Ropalidia marginata (Hymenoptera, Vespidae). Ecol. Entomol. 16, 435-440. (doi:10.1111/j.1365-2311.1991. tb00236.x)
57. Gadagkar, R., Vinutha, C., Shanubhogue, A. & Gore, A. P. 1988 Pre-imaginal biasing of caste in a primitively eusocial insect. Proc. R. Soc. Lond. B 233, 175-189. (doi:10.1098/rspb.1988.0017)
58. Murakami, A. S. N. & Shima, S. N. 2006 Nutritional and social hierarchy establishment of the primitively eusocial wasp Mischocyttarus cassununga (Hymenoptera, Vespidae, Mischocyttarini) and related aspects. Sociobiology 48, 184-207.
59. Hunt, J. H., Wolschin, F., Henshaw, M. T., Newman, T. C., Toth, A. L. & Amdam, G. V. 2010 Differential gene expression and protein abundance evince ontogenetic bias toward castes in a primitively eusocial wasp. PLoS ONE 5, e10674. (doi:10.1371/journal.pone.0010674)
60. Hunt, J. H., Kensinger, B. J., Kossuth, J. A., Henshaw, M. T., Norberg, K., Wolschin, F. & Amdam, G. V. 2007 A diapause pathway underlies the gyne phenotype in Polistes wasps, revealing an evolutionary route to caste-containing insect societies. Proc. Natl Acad. Sci. USA 104, 14 020-14 025. (doi:10.1073/pnas.0705660104)
61. Sullivan, J. D. & Strassmann, J. E. 1984 Physical variability among nest foundresses in the polygynous social wasp, Polistes annularis. Behav. Ecol. Sociobiol. 15, 249-256. (doi:10.1007/BF00292986)
62. Karsai, I. & Hunt, J. H. 2002 Food quantity affect traits of offspring in the paper wasp Polistes metricus (Hymenoptera: Vespidae). Environ. Entomol. 31, 99-106. (doi:10.1603/0046-225X-31.1.99)
63. Bell, W. J. 1973 Factors controlling initiation of vitellogenesis in a primitively social bee, Lasioglossum zephyrum (Hymenoptera: Halictidae). Insectes Sociaux 20, 253-260. (doi:10.1007/BF02223194)
64. Richards, M. H., von Wettberg, E. J. & Rutgers, A. C. 2003 A novel social polymorphism in a primitively eusocial bee. Proc. Natl Acad. Sci. USA 100, 7175-7180. (doi:10.1073/pnas.1030738100)
65. Richards, M. H. & Packer, L. 1994 Trophic aspects of caste determination in Halictus ligatus, a primitively eusocial sweat bee. Behav. Ecol. Sociobiol. 34, 385-391. (doi:10.1007/BF00167329)
66. Mueller, U. G. 1996 Life history and social evolution of the primitively eusocial bee Augochlorella striata (Hymenoptera: Halictidae). J. Kansas Entomol. Soc. 69, 116-138.
67. Mueller, U. G., Eickwort, G. C. & Aquadro, C. F. 1994 DNA-fingerprinting analysis of parent-offspring conflict in a bee. Proc. Natl Acad. Sci. USA 91, 5143-5147. (doi:10.1073/pnas.91.11.5143)
68. Amdam, G. V. & Page, R. E. 2010 The developmental genetics and physiology of honeybee societies. Anim. Behav. 79, 973-980. (doi:10.1016/j.anbehav.2010.02.007)
69. Corona, M., Velarde, R. A., Remolina, S., Moran- Lauter, A., Wang, Y., Hughes, K. A. & Robinson, G. E. 2007 Vitellogenin, juvenile hormone, insulin signaling, and queen honey bee longevity. Proc. Natl Acad. Sci. USA 104, 7128-7133. (doi:10.1073/pnas.0701909104)
70. Münch, D. & Amdam, G. V. 2010 The curious case of aging plasticity in honey bees. FEBS Lett. 584, 2496-2503. (doi:10.1016/j.febslet.2010.04.007)
71. Parthasarathy, R. & Palli, S. R. 2011 Molecular analysis of nutritional and hormonal regulation of female reproduction in the red flour beetle, Tribolium castaneum. Insect Biochem. Mol. Biol. 41, 294-305. (doi:10.1016/j. ibmb.2011.01.006)
72. Dallacqua, R., Simes, Z. & Bitondi, M. 2007 Vitellogenin gene expression in stingless bee workers differing in egg-laying behavior. Insectes Sociaux 54, 70-76. (doi:10.1007/s00040-007-0913-1)