The role of juvenile hormone in dominance behavior, reproduction and cuticular pheromone signaling in the caste-flexible epiponine wasp, Synoeca surinama

Frontiers in Zoology

Volumn 11, Issue 1, 2014, Pages

  Kelstrup, Hans C ^a,c   Hartfelder, Klaus ^b   Nascimento, Fabio S ^b   Riddiford, Lynn M ^a  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

^c STELLENBOSCH UNIVERSITY   (South Africa)

Author keywords

Cuticular hydrocarbons; Ecdysteroids; Endocrine; Epiponini; Juvenile hormone; Swarm founding; Wasps

Indexed keywords

EID: 84988499073     PISSN: None     EISSN: 17429994     Source Type: Journal    
DOI: 10.1186/s12983-014-0078-5     Document Type: Article

References (82)

1. West-überhard MJ: Intragroup selection and the evolution of insect societies. In Natural Selection and Social Behavior. Edited by Alexander RD, Tinkle DW. New York: Chiron Press; 1981:3-17.
2. West-überhard MJ: The Establishment of Dominance of the Queen in Social Wasp Colonies. Netherlands: Wageningen; 1977:223-227.
3. West-überhard MJ: Temporary queens in Metapolybia wasps-nonreproductive helpers without altruism. Science 1978, 200:441-443.
4. Platt TG, Queller DC, Strassmann JE: Aggression and worker control of caste fate in a multiple-queen wasp, Parachartergus colobopterus. Anim Behav 2004, 67:1-10.
5. West-überhard MJ: The nature and evolution of swarming in tropical social wasps (Vespidae, Polistinae, Polybiini). In Social Insects in the Tropics. Edited by Jaisson P. Paris: University of Paris Press; 1982:97-128.
6. Forsyth AB: Studies on the Behavioral Ecology of Polygynous Social Wasps. Cambridge, MA: Harvard Universtiy; 1978.
7. West MJ: The Social Biology of Polistine Wasps, Ph.D. Thesis. Ann Harbor, Michigan: University of Michigan; 1969.
8. Pardi L: Dominance order in Polistes wasps. Physiol Zool 1948, 21:1-13.
9. Reeve H: Polistes. In The Social Biology of Wasps. Edited by Ross K, Matthews R. Ithaca, NY: Cornell University Press; 1991.
10. Spraüberry J: Evolution of queen nuüber and queen control. In The Social Biology of Wasps. Edited by Ross K, Matthews R. Ithaca, NY: Cornell University Press; 1991:366-388.
11. West-überhard M: Sexual selection, social competition, and evolution. Proc Am Phil Soc 1979, 123:222-234.
12. Hughes CR, Queller DC, Negrón-Stomayor JA, Strassmann JE, Solis C, Gastreich KR: The maintenance of high genetic relatedness in multiqueen colonies of social wasps. In Queen Nuüber and Sociality in Insects. Edited by Keller L. Oxford: Oxford University Press; 1993:153-170.
13. Strassman J, Sullender B, Queller DC: Caste totipotency and conflict in a large-colony social insect. Proc R Soc Lond B Biol Sci 2001, 269:263-270.
14. Hartfelder K, Emlen D: Endocrine control of insect polyphenism. In Insect Endocrinology. Edited by Giübert LI. San Diego: Academic Press; 2012:464-522.
15. Riddiford LM: Cellular and molecular actions of juvenile hormone. 1. general considerations and premetamorphic actions. Adv Insect Physiol 1994, 24:213-274.
16. Jindra M, Palli SR, Riddiford LM: The juvenile hormone signaling pathway in insect development. Annu Rev Entomol 2013, 58:181-204.
17. Raikhel A, Brown M, Bellés X: Hormonal control of reproductive processes. In Comprehensive Molecular Insect Science. Edited by Giübert L, Iatrou K, Gill S. Oxford: Elsevier; 2005:433-491.
18. Wyatt GR, Davey KG: Cellular and molecular actions of juvenile hormone. 2. roles of juvenile hormone in adult insects. Adv Insect Physiol 1996, 26:1-155.
19. Tibbetts EA, Levy S, Donajkowski K: Reproductive plasticity in Polistes paper wasp workers and the evolutionary origins of sociality. J Insect Physiol 2011, 57:995-999.
20. West-überhard MJ: Wasp societies as microcosms for the study of development and evolution. In Natural History and Evolution of Paper Wasps. Edited by Turillazzi S, West-überhard MJ. London, England: Oxford University Press; 1996:290-317.
21. Giray T, Giovanetti M, West-überhard MJ: Juvenile hormone, reproduction, and worker behavior in the neotropical social wasp Polistes canadensis. Proc Natl Acad Sci U S A 2005, 102:3330-3335.
22. Tibbetts EA, Izzo AS: Endocrine mediated phenotypic plasticity: conditiondependent effects of juvenile hormone on dominance and fertility of wasp queens. Horm Behav 2009, 56:527-531.
23. Barth RH, Lester LJ, Sroka P, Kessler T, Hearn R: Juvenile-hormone promotes dominance behavior and ovarian development in social wasps (Polistes annularis). Experientia 1975, 31:691-692.
24. Röseler PF: Reproductive competition during colony establishment. In The Social Biology of Wasps. Edited by Ross K, Matthews R. Cornell, Ithaca: Cornell University Press; 1991:309-335.
25. Strambi A: Physiology and reproduction in social wasps. In Social Insects-an Evolutionary Approach to Castes and Reproduction. Edited by Engels W. Heideüberg: Spring; 1990:59-75.
26. Tibbetts EA, Huang ZY: The challenge hypothesis in an insect: juvenile hormone increases during reproductive conflict following queen loss in Polistes wasps. Am Nat 2010, 176:123-130.
27. Izzo A, Wells M, Huang Z, Tibbetts E: Cuticular hydrocarbons correlate with fertility, not dominance, in a paper wasp, Polistes dominulus. Behav Ecol Sociobiol 2010, 64:857-864.
28. Röseler PF, Röseler I, Strambi A: Role of ovaries and ecdysteroids in dominance hierarchy establishment among foundresses of the primitively social wasp, Polistes gallicus. Behav Ecol Sociobiol 1985, 18:9-13.
29. Röseler PF, Röseler I: Dominance of ovariectomized foundresses of the paper wasp, Polistes gallicus. Insectes Sociaux 1989, 36:219-234.
30. Shorter JR, Tibbetts EA: The effect of juvenile hormone on temporal polyethism in the paper wasp Polistes dominulus. Insectes Sociaux 2009, 56:7-13.
31. Pickett KM, Carpenter JM: Simultaneous analysis and the origin of eusociality in the Vespidae (Insecta: Hymenoptera). Arthropod Syst Phylogeny 2010, 68:3-33.
32. Noll FB, Wenzel JW: Caste in the swarming wasps: 'queenless' societies in highly social insects. Biol J Linn Soc 2008, 93:509-522.
33. O'Donnell S, Jeanne RL: Methoprene accelerates age polyethism in workers of a social wasp (Polybia occidentalis). Physiol Entomol 1993, 18:189-194.
34. Kelstrup HCP, Hartfelder K, Nascimento FS, Riddiford LM: Reproductive status, endocrine physiology and chemical signaling in the Neotropical, swarm-founding eusocial wasp, Polybia micans Ducke (Vespidae: Epiponini). J Exp Biol 2014, 217:2399-2410.
35. Wingfield JC, Hegner RE, Dufty AM, Ball GF: The challenge hypothesis-theoretical implications for patterns of testosterone secretion, mating systems, and breeding strategies. Am Nat 1990, 136:829-846.
36. Tibbetts EA, Crocker KC: The challenge hypothesis across taxa: social modulation of hormone titres in vertebrates and insects. Anim Behav 2014, 281-290.
37. Shpigler H, Amsalem E, Huang ZY, Cohen M, Siegel AJ, Hefetz A, Bloch G: Gonadotropic and physiological functions of juvenile hormone in bumblebee (Bombus terrestris) workers. PLoS One 2014, 9(6):e100650.
38. Geva S, Hartfelder K, Bloch G: Reproductive division of labor, dominance, and ecdysteroid levels in hemolymph and ovary of the bumble bee Bombus terrestris. J Insect Physiol 2005, 51:811-823.
39. Bloch G, Wheeler D, Robinson G: Endocrine influences on the organization of insect societies. In Hormones, Brains and Behavior. Edited by Pfaff D, Arnold A, Etgen A, Fahrbach S, Moss R, et al. New York, NY: Academic Press; 2002.
40. Hartfelder K, Bitondi MMG, Santana WC, Simoes ZLP: 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 2002, 32:211-216.
41. Penick CA, Liebig J, Brent CS: Reproduction, dominance, and caste: endocrine profiles of queens and workers of the ant Harpegnathos saltator. J Comp Physiol A 2011, 197:1063-1071.
42. van Zweden JS, Bonckaert W, Wenseleers T, d'Ettorre P: Queen signaling in social wasps. Evolution 2013. doi:10.1111/evo.12314.
43. Hagenguth H, Rembold H: Identification of juvenile hormone 3 as the only juvenile hormone homolog in all developmental stages of the honey bee. Zeitschrift für Naturforschung 1978, 33C:847-850.
44. Sommer K, Hölldobler B, Rembold H: Behavioral and physiological-aspects of reproductive control in a Diacamma species from Malaysia (Formicidae, Ponerinae). Ethol 1993, 94:162-170.
45. Burns SN, Teal PEA, Meer RKV, Nation JL, Vogt JT: Identification and action of juvenile hormone III from sexually mature alate females of the red imported fire ant, Solenopsis invicta. J Insect Physiol 2002, 48:357-365.
46. Mackert A, Hartfelder K, Bitondi MMG, Simões ZLP: The juvenile hormone (JH) epoxide hydrolase gene in the honey bee (Apis mellifera) genome encodes a protein which has negligible participation in JH degradation. J Insect Physiol 2010, 56:1139-1146.
47. Staal GB: Insect growth-regulators with juvenile-hormone activity. Annu Rev Entomol 1975, 20:417-460.
48. Röseler P: Endocrine basis of dominance and reproduction in polistine paper wasps. Fortschr Zool 1985, 31:259-272.
49. Tibbetts EA, Izzo A, Huang ZY: Behavioral and physiological factors associated with juvenile hormone in Polistes wasp foundresses. Behav Ecol Sociobiol 2011, 65:1123-1131.
50. Mackert A, Do Nascimento AM, Bitondi MMG, Hartfelder K, Simões ZLP: Identification of a juvenile hormone esterase-like gene in the honey bee, Apis mellifera L-expression analysis and functional studies. Comp Biochem Physiol B 2008, 150:33-44.
51. West-überhard MJ: Dominance relations in Polistes-canadensis (L), a tropical social wasp. Monit Zoologico Italiano-Italian J Zool 1986, 20:263-281.
52. Röseler PF, Röseler I, Strambi A: The activity of corpora-allata in dominant and subordinated females of the wasp Polistes gallicus. Insectes Sociaux 1980, 27:97-107.
53. Sasaki K, Yamasaki K, Nagao T: Neuro-endocrine correlates of ovarian development and egg-laying behaviors in the primitively eusocial wasp (Polistes chinensis). J Insect Physiol 2007, 53:940-949.
54. Sasaki K, Yamasaki K, Tsuchida K, Nagao T: Gonadotropic effects of dopamine in isolated workers of the primitively eusocial wasp, Polistes chinensis. Naturwissenschaften 2009, 96:625-629.
55. Bloch G, Simon T, Robinson GE, Hefetz A: Brain biogenic amines and reproductive dominance in bumble bees (Bombus terrestris). J Comp Physiol A 2000, 186:261-268.
56. Cuvillier-Hot V, Lenoir A: Biogenic amine levels, reproduction and social dominance in the queenless ant Streblognathus peetersi. Naturwissenschaften 2006, 93:149-153.
57. Robinson GE, Heuser LM, Le Conte Y, Lenquette F, Hollingworth RM: Neurochemicals aid bee nestmate recognition. Nature 1999, 399:534-535.
58. O'Donnell S: Polybia wasp biting interactions recruit foragers following experimental worker removals. Anim Behav 2006, 71:709-715.
59. Visscher PK, Dukas R: Honey-bees recognize development of nestmates ovaries. Anim Behav 1995, 49:542-544.
60. Blomquist G, Bagnères A: Introduction: history and overview of insect hydrocarbons. In Insect Hydrocarbons. Edited by Blomquist G, Bagnères A. Cambridge: Cambridge University Press; 2010:3-18.
61. van Oystaeyen A, Oliveira RC, Holman L, van Zweden JS, Romero C, Oi CA, d'Ettorre P, Khalesi M, Billen J, Wäckers F, Millar JG, Wenseleers T: Conserved class of queen pheromones stops social insect workers from reproducing. Science 2014, 343:287-290.
62. Singer T, Espelie K, Gamboa G: Nest and nestmate discrimination in independent-founding paper wasps. In Pheromone Communication in Social Insects. Edited by Vander Meer R, Breed M, Winston M, Espelie K. Boulder, CO: Westview Press; 1998:104-125.
63. Espelie KE, Hermann HR: Congruent cuticular hydrocarbons: biochemical convergence of a social wasp, an ant and a host plant. Biochem Syst Ecol 1988, 16:505-508.
64. Bloch G, Borst DW, Huang ZY, Robinson GE, Cnaani J, Hefetz A: Juvenile hormone titers, juvenile hormone biosynthesis, ovarian development and social environment in Bombus terrestris. J Insect Physiol 2000, 46:47-57.
65. Van Doorn A: Factors influencing dominance behavior in queenless bumblebee workers Bombus terrestris. Physiol Entomol 1989, 14:211-222.
66. van Doorn A: Investigations into the regulation of dominance behavior and of the division of labor in bumblebee colonies Bombus terrestris. Neth J Zool 1987, 37:255-276.
67. Agrahari M, Gadagkar R: Juvenile hormone accelerates ovarian development and does not affect age polyethism in the primitively eusocial wasp, Ropalidia marginata. J Insect Physiol 2003, 49:217-222.
68. Zera AJ, Zhao Z, Kaliseck K: Hormones in the field: evolutionary endocrinology of juvenile hormone and ecdysteroids in field populations of the wing-dimorphic cricket Gryllus firmus. Physiol Biochem Zool 2007, 80:592-606.
69. Ferreira PG, Patalano S, Chauhan R, Ffrench-Constant R, Gabaldon T, Guigó R, Sumner S: Transcriptome analyses of primitively eusocial wasps reveal novel insights into the evolution of sociality and the origin of alternative phenotypes. Genome Biol 2013, 14:R20.
70. Simola DF, Wissler L, Donahue G, Waterhouse RM, Helmkampf M, Roux J, Nygaard S, Glastad K, Hagen DE, Viljakainen L, Reese JT, Hunt BG, Graur D, Elhaik E, Kriventseva E, Wen J, Parker BJ, Cash E, Privman E, Childers CP, Munos-Torres MC, Boomsma JJ, Borüberg-Bauer E, Currie C, Elsik CG, Suen G, Goodisman MAD, Keller L, Liebig J, Rawls A, et al: Social insect genomes exhibit dramatic evolution in gene composition and regulation while preserving regulatory features linked to sociality. Genome Res 2013, 23:1235-1247.
71. Nascimento FS, Tannure-Nascimento IC, Zucchi R: Behavioral mediators of cyclical oligogyny in the Amazonian swarmfounding wasp Asteloeca ujhelyii (Vespidae, Polistinae, Epiponini). Insectes Sociaux 2004, 51:17-23.
72. Zera AJ: Endocrine analysis in evolutionary-developmental studies of insect polymorphism: hormone manipulation versus direct measurement of hormonal regulators. Evol Dev 2007, 9:499-513.
73. Noda SCM, Shima SN, Noll FB: Morphological and physiological caste differences in Synoeca cyanea (Hymenoptera, Vespidae, Epiponini) according to the ontogenetic development of the colonies. Sociobiol 2003, 41:547-570.
74. Lin HR, Dusset C, Huang ZY: Short-term changes in juvenile hormone titers in honey bee workers due to stress. Apidologie 2004, 35:319-327.
75. Huang ZY, Robinson GE, Borst DW: Physiological correlates of division of labor among similarly aged honey bees. J Comp Physiol A 1994, 174:731-739.
76. Goodman WG, Coy DC, Baker FC, Xu L, Toong YC: Development and application of a radioimmunoassay for the juvenile hormones. Insect Biochem 1990, 20:357-364.
77. Hartfelder K, Bitondi M, Brent C, Guidugli-Lazzarini K, Simões Z, Stabentheiner A, Tanaka ED, Wang Y: Standard methods for physiology and biochemistry research in Apis mellifera. J Apicultural Res 2013, 52:1-47.
78. Hartfelder K, Feldlaufer MF: Relationship of the neutral sterols and ecdysteroids of the parasitic mite, Varroa jacobsoni to those of the honey bee, Apis mellifera. J Insect Physiol 1997, 43:541-545.
79. Bollenbacher WE, O'Brien MA, Katahira EJ, Giübert LI: A kinetic analysis of the action of the insect prothoracicotropic hormone. Mol Cell Endocrinol 1983, 32:27-46.
80. Warren JT, Giübert LI: Ecdysone metabolism and distribution during the pupal-adult development of Manduca sexta. Insect Biochem 1986, 16:65-82.
81. Carlson DA, Roan CS, Yost RA, Hector J: Dimethyl disulfide derivatives of long chain alkenes, alkadienes, and alkatrienes for gas chromatography/mass spectrometry. Anal Chem 1989, 61:1564-1571.
82. Aitchison J: The statistical analysis of compositional data. J R Stat Soc B 1982, 44:139-177.