Juvenile hormone, reproduction, and worker behavior in the neotropical social wasp Polistes canadensis.
Previous studies of the division of labor in colonies of eusocial Hymenoptera (wasps and bees) have led to two hypotheses regarding the evolution of juvenile hormone (JH) involvement. The novel- or single-function hypothesis proposes that the role of JH has changed from an exclusively reproductive function in primitively eusocial species (those lacking morphologically distinct queen and worker castes), to an exclusively behavioral function in highly eusocial societies (those containing morphologically distinct castes). In contrast, the split-function hypothesis proposes that JH originally functioned in the regulation of both reproduction and behavior in ancestral solitary species. Then, when reproductive and brood-care tasks came to be divided between queens and workers, the effects of JH were divided as well, with JH involved in regulation of reproductive maturation of egg-laying queens, and behavioral maturation, manifested as age-correlated changes in worker tasks, of workers. We report experiments designed to test these hypotheses. After documenting age-correlated changes in worker behavior (age polyethism) in the neotropical primitively eusocial wasp Polistes canadensis, we demonstrate that experimental application of the JH analog methoprene accelerates the onset of guarding behavior, an age-correlated task, and increases the number of foraging females; and we demonstrate that JH titers correlate with both ovarian development of queens and task differentiation in workers, as predicted by the split-function hypothesis. These findings support a view of social insect evolution that sees the contrasting worker and queen phenotypes as derived via decoupling of reproductive and brood-care components of the ancestral solitary reproductive physiology.
Giray
Tugrul
T
Smithsonian Tropical Research Institute, Ancon, Panama Unit 0948, APO AA 34002, Panama. tgiray2@yahoo.com
Giovanetti
Manuela
M
West-Eberhard
Mary Jane
MJ
D000375:Aging / Q000502:physiology; D000818:Animals; D006927:Hymenoptera / Q000502:physiology*; D007605:Juvenile Hormones / Q000502:physiology*; D012098:Reproduction / Q000502:physiology*
D007605:Juvenile Hormones
Proc Natl Acad Sci U S A. 1992 Dec 15;89(24):11726-9
1465390
Neurobiol Learn Mem. 1995 Mar;63(2):181-91
7663892
Proc Natl Acad Sci U S A. 1990 Mar;87(6):2072-6
2107540
J Insect Physiol. 2000 Jun 1;46(6):1033-1040
10802116
Horm Behav. 2000 Feb;37(1):1-14
10712853
Science. 1989 Oct 6;246(4926):109-12
17837770
Insect Biochem Mol Biol. 2002 Feb;32(2):211-6
11755066
J Theor Biol. 2003 Aug 21;223(4):451-64
12875823
Science. 1978 Apr 28;200(4340):441-3
17757302
Proc Natl Acad Sci U S A. 2004 Aug 3;101(31):11350-5
15277665
J Comp Physiol A. 1994 Jun;174(6):731-9
8014920
Science. 1990 Nov 30;250(4985):1283
17829216
Proc Natl Acad Sci U S A. 1996 Oct 15;93(21):11718-22
8876203
Arch Insect Biochem Physiol. 1991;17(2-3):143-55
1802030
Monogr Popul Biol. 1978;12:1-352
740003
Arch Insect Biochem Physiol. 1997;35(4):559-83
9210289
J Theor Biol. 1999 Mar 7;197(1):123-33
10036212
Annu Rev Entomol. 1998;43:323-46
15012393
Curr Top Dev Biol. 1998;40:45-77
9673848
J Insect Physiol. 2000 Jan;46(1):47-57
12770258
Proc Natl Acad Sci U S A. 1998 Jul 21;95(15):8665-9
9671735
Annu Rev Entomol. 1992;37:637-65
1539941
J Comp Physiol A. 2001 Jun;187(5):327-33
11529476
Physiol Zool. 1948 Jan;21(1):1-13
18898533
Annu Rev Entomol. 1996;41:407-31
15012335
Gen Comp Endocrinol. 1992 Sep;87(3):471-80
1426950
Proc Natl Acad Sci U S A. 1998 Mar 17;95(6):2761-6
9501163
J Insect Physiol. 2003 Mar;49(3):217-22
12769996