Effects of environment and juvenile hormone on ovaries of the wasp, Polistes metricus

Bohm, Marguerite K.

doi:10.1016/0022-1910(72)90158-8

Cited by 89 publications

(40 citation statements)

References 7 publications

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“…The absence or delay of worker activity in the controls could also indicate diapause, broken by methoprene treatment in the experimental group. In temperate species of primitively eusocial wasps (Polistes) and bees (Bombus) ''caste determination'' in the emerging adult females is achieved by the presence or absence of JH-mediated diapause, which when broken by JH application produces both worker behavior and ovarian development (11,28,56). Such findings accord with those of the present study and the split-function hypothesis in suggesting that both worker behavior and reproduction in primitively eusocial insects are inf luenced by JH.…”

Section: Discussionsupporting

confidence: 91%

Juvenile hormone, reproduction, and worker behavior in the neotropical social waspPolistes canadensis

Giray

Giovanetti²,

West‐Eberhard³

2005

Proc. Natl. Acad. Sci. U.S.A.

173

112

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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.behavioral development ͉ division of labor ͉ methoprene ͉ worker polyethism

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Section: Discussionsupporting

confidence: 91%

Juvenile hormone, reproduction, and worker behavior in the neotropical social waspPolistes canadensis

Giray

Giovanetti²,

West‐Eberhard³

2005

Proc. Natl. Acad. Sci. U.S.A.

173

112

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“…Hexamerins were recently implicated in regulation of caste differentiation in termites, where binding of juvenile hormone to the hexameric molecule results in physiological silencing of hormone action (44). Diapause is characterized by low juvenile hormone levels (45), and application of a juvenile hormone analog can trigger P. metricus gynes to initiate ovarian development (46). Hexamerin 1 protein in Polistes offspring, therefore, might be directly responsible for the phenotype bias of adult females: low levels in workers would permit juvenile hormone action and expression of reproductive behaviors shortly after adult emergence.…”

Section: Resultsmentioning

confidence: 99%

A diapause pathway underlies the gyne phenotype inPolisteswasps, revealing an evolutionary route to caste-containing insect societies

Hunt

Kensinger

Kossuth

et al. 2007

Proc. Natl. Acad. Sci. U.S.A.

146

125

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Colonies of social wasps, ants, and bees are characterized by the production of two phenotypes of female offspring, workers that remain at their natal nest and nonworkers that are potential colony reproductives of the next generation. The phenotype difference includes morphology and is fixed during larval development in ants, honey bees, and some social wasps, all of which represent an advanced state of sociality. Paper wasps (Polistes) lack morphological castes and are thought to more closely resemble an ancestral state of sociality wherein the phenotype difference between workers and nonworkers is established only during adult life. We address an alternative hypothesis: a bias toward the potential reproductive (gyne) phenotype among Polistes female offspring occurs during larval development and is based on a facultatively expressed ancestral life history trait: diapause. We show that two signatures of diapause (extended maturation time and enhanced synthesis and sequestration of a hexameric storage protein) characterize the development of gyne offspring in Polistes metricus. Hexameric storage proteins are implicated in silencing juvenile hormone signaling, which is a prerequisite for diapause. Diverging hexamerin protein dynamics driven by changes in larval provisioning levels thereby provide one possible mechanism that can cause an adaptive shift in phenotype bias during the Polistes colony cycle. This ontogenetic basis for alternative female phenotypes in Polistes challenges the view that workers and gynes represent behavior options equally available to every female offspring, and it exemplifies how social insect castes can evolve from casteless lineages.caste development ͉ hexameric storage proteins ͉ juvenile hormone ͉ life-history pleiotropy ͉ social behavior S ocial insects often show pronounced differences in behavior, physiology, and morphology between castes of workers (functionally sterile helpers) and reproductives (1).

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“…This is consistent with the fact that reproductive physiology differs fundamentally between these two species. In Polistes, ovary development and reproductive behaviours are regulated by the insect gonadotropin, juvenile hormone ( JH) (Bohm 1972;Roseler et al 1985;Sledge et al 2004). In honeybees, JH levels are uncoupled from ovarian development and egg-laying behaviour in queens, a situation that may also characterize advanced eusocial stingless bees (Hartfelder et al 2001), but not primitively eusocial bumble bees (Geva et al 2005).…”

Section: Discussionmentioning

confidence: 99%

Brain transcriptomic analysis in paper wasps identifies genes associated with behaviour across social insect lineages

et al. 2010

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Comparative sociogenomics has the potential to provide important insights into how social behaviour evolved. We examined brain gene expression profiles of the primitively eusocial wasp Polistes metricus and compared the results with a growing base of brain gene expression information for the advanced eusocial honeybee, Apis mellifera. We studied four female wasp groups that show variation in foraging/provisioning behaviour and reproductive status, using our newly developed microarray representing approximately 3248 P. metricus genes based on sequences generated from high-throughput pyrosequencing. We found differences in the expression of approximately 389 genes across the four groups. Pathways known from Drosophila melanogaster to be related to lipid metabolism, heat and stress response, and various forms of solitary behaviour were associated with behavioural differences among wasps. Fortyfive per cent of differentially expressed transcripts showed significant associations with foraging/provisioning status, and 14 per cent with reproductive status. By comparing these two gene lists with lists of genes previously shown to be differentially expressed in association with honeybee division of labour, we found a significant overlap of genes associated with foraging/provisioning, but not reproduction, across the two species. These results suggest common molecular roots for foraging division of labour in two independently evolved social insect species and the possibility of more lineage-specific roots of reproductive behaviour. We explore the implications of these findings for the idea that there is a conserved 'genetic toolkit' for division of labour across multiple lineages.

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Effects of environment and juvenile hormone on ovaries of the wasp, Polistes metricus

Cited by 89 publications

References 7 publications

Juvenile hormone, reproduction, and worker behavior in the neotropical social waspPolistes canadensis

Juvenile hormone, reproduction, and worker behavior in the neotropical social waspPolistes canadensis

A diapause pathway underlies the gyne phenotype inPolisteswasps, revealing an evolutionary route to caste-containing insect societies

Brain transcriptomic analysis in paper wasps identifies genes associated with behaviour across social insect lineages

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