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1.
Horm Behav ; 85: 67-75, 2016 09.
Article in English | MEDLINE | ID: mdl-27503109

ABSTRACT

A hallmark of insect societies is a division of labor among workers specializing in different tasks. In bumblebees the division of labor is related to body size; relatively small workers are more likely to stay inside the nest and tend ("nurse") brood, whereas their larger sisters are more likely to forage. Despite their ecological and economic importance, very little is known about the endocrine regulation of division of labor in bumblebees. We studied the influence of juvenile hormone (JH) on task performance in the bumblebee Bombus terrestris. We first used a radioimmunoassay to measure circulating JH titers in workers specializing in nursing and foraging activities. Next, we developed new protocols for manipulating JH titers by combining a size-adjusted topical treatment with the allatotoxin Precocene-I and replacement therapy with JH-III. Finally, we used this protocol to test the influence of JH on task performance. JH levels were either similar for nurses and foragers (three colonies), or higher in nurses (two colonies). Nurses had better developed ovaries and JH levels were typically positively correlated with ovarian state. Manipulation of JH titers influenced ovarian development and wax secretion, consistent with earlier allatectomy studies. These manipulations however, did not affect nursing or foraging activity, or the likelihood to specialize in nursing or foraging activity. These findings contrast with honeybees in which JH influences age-related division of labor but not adult female fertility. Thus, the evolution of complex societies in bees was associated with modifications in the way JH influences social behavior.


Subject(s)
Bees , Biological Evolution , Juvenile Hormones/metabolism , Juvenile Hormones/pharmacology , Motor Activity/drug effects , Social Behavior , Work/physiology , Animals , Bees/drug effects , Bees/physiology , Cooperative Behavior , Female , Signal Transduction/drug effects
2.
PLoS One ; 9(6): e100650, 2014.
Article in English | MEDLINE | ID: mdl-24959888

ABSTRACT

The evolution of advanced sociality in bees is associated with apparent modifications in juvenile hormone (JH) signaling. By contrast to most insects in which JH is a gonadotropin regulating female fertility, in the highly eusocial honey bee (Apis mellifera) JH has lost its gonadotrophic function in adult females, and instead regulates age-related division of labor among worker bees. In order to shed light on the evolution of JH signaling in bees we performed allatectomy and replacement therapies to manipulate JH levels in workers of the "primitively eusocial" bumblebee Bombus terrestris. Allatectomized worker bees showed remarkable reduction in ovarian development, egg laying, Vitellogenin and Krüppel homolog 1 fat body transcript levels, hemolymph Vitellogenin protein abundance, wax secretion, and egg-cell construction. These effects were reverted, at least partially, by treating allatectomized bees with JH-III, the natural JH of bees. Allatectomy also affected the amount of ester component in Dufour's gland secretion, which is thought to convey a social signal relating to worker fertility. These findings provide a strong support for the hypothesis that in contrast to honey bees, JH is a gonadotropin in bumblebees and lend credence to the hypothesis that the evolution of advanced eusociality in honey bees was associated with major modifications in JH signaling.


Subject(s)
Bees/physiology , Juvenile Hormones/metabolism , Animals , Behavior, Animal , Corpora Allata/surgery , Female , Fertility , Gene Expression , Gonadotropins/metabolism , Hemolymph/metabolism , Oogenesis , RNA, Messenger , Reproduction , Signal Transduction , Vitellogenins/genetics , Vitellogenins/metabolism
3.
Behav Ecol Sociobiol ; 67: 1623-1632, 2013.
Article in English | MEDLINE | ID: mdl-24031117

ABSTRACT

Honey bee workers exhibit an age-based division of labor (temporal polyethism, DOL). Younger bees transition through sets of tasks within the nest; older bees forage outside. Components of temporal polyethism remain unrevealed. Here, we investigate the timing and pattern of pre-foraging behavior in distinct strains of bees to (1) determine if a general pattern of temporal DOL exists in honey bees, (2) to demonstrate a direct genetic impact on temporal pacing, and (3) to further elucidate the mechanisms controlling foraging initiation. Honey bees selected for differences in stored pollen demonstrate consistent differences in foraging initiation age. Those selected for increased pollen storage (high pollen hoarding strain, HSBs) initiate foraging earlier in life than those selected for decreased pollen storage (low pollen hoarding strain, LSBs). We found that HSBs both initiate and terminate individual pre-foraging tasks earlier than LSBs when housed in a common hive environment. Unselected commercial bees (wild type) generally demonstrated intermediate behavioral timing. There were few differences between genotypes for the proportion of pre-foraging effort dedicated to individual tasks, though total pre-foraging effort differences differed dramatically. This demonstrates that behavioral pacing can be accelerated or slowed, but the pattern of behavior is not fundamentally altered, suggesting a general pattern of temporal behavior in honey bees. This also demonstrates direct genetic control of temporal pacing. Finally, our results suggest that earlier HSB protein (pollen) consumption termination compared to LSBs may contribute to an earlier decline in hemolymph vitellogenin protein titers, which would explain their earlier onset of foraging.

4.
PLoS One ; 7(4): e33465, 2012.
Article in English | MEDLINE | ID: mdl-22558073

ABSTRACT

Honey bees are a model system for the study of division of labor. Worker bees demonstrate a foraging division of labor (DOL) by biasing collection towards carbohydrates (nectar) or protein (pollen). The Reproductive ground-plan hypothesis of Amdam et al. proposes that foraging DOL is regulated by the networks that controlled foraging behavior during the reproductive life cycle of honey bee ancestors. Here we test a proposed mechanism through which the ovary of the facultatively sterile worker impacts foraging bias. The proposed mechanism suggests that the ovary has a regulatory effect on sucrose sensitivity, and sucrose sensitivity impacts nectar loading. We tested this mechanism by measuring worker ovary size (ovariole number), sucrose sensitivity, and sucrose solution load size collected from a rate-controlled artificial feeder. We found a significant interaction between ovariole number and sucrose sensitivity on sucrose solution load size when using low concentration nectar. This supports our proposed mechanism. As nectar and pollen loading are not independent, a mechanism impacting nectar load size would also impact pollen load size.


Subject(s)
Appetitive Behavior/physiology , Bees/physiology , Models, Biological , Ovary/anatomy & histology , Sucrose/metabolism , Animals , Female , Linear Models , Observation , Organ Size , Ovary/physiology , Plant Nectar/chemistry , Time Factors
5.
J Insect Physiol ; 56(12): 1816-24, 2010 Dec.
Article in English | MEDLINE | ID: mdl-20688074

ABSTRACT

Honey bee (Apis mellifera L.) workers are essentially sterile females that are used to study how complex social behavior develops. Workers perform nest tasks, like nursing larvae, prior to field tasks, like foraging. Despite worker sterility, this behavioral progression correlates with ovary size: workers with larger ovaries (many ovary filaments) start foraging at younger ages on average. It is untested, however, whether the correlation confers a causal relationship between ovary size and behavioral development. Here, we successfully grafted supernumerary ovaries into worker bees to produce an artificial increase in the amount of ovary tissue. We next measured fat body mRNA levels for the yolk precursor gene vitellogenin, which influences honey bee behavioral development and can correlate with ovary size. Vitellogenin was equally expressed in surgical controls and bees with supernumerary ovaries, leading us to predict that these groups would be characterized by equal behavior. Contrary to our prediction, bees with supernumerary ovaries showed accelerated behavioral development compared to surgical controls, which behaved like reference bees that were not treated surgically. To explore this result we monitored fat body expression levels of a putative ecdysteroid-response gene, HR46, which is genetically linked to ovary size in workers. Our data establish that social insect worker behavior can be directly influenced by ovaries, and that HR46 expression changes with ovary size independent of vitellogenin.


Subject(s)
Bees/physiology , Behavior, Animal/physiology , Ovary/physiology , Animals , Bees/anatomy & histology , Ecdysteroids/genetics , Ecdysteroids/physiology , Fat Body/physiology , Female , Ovary/anatomy & histology , Ovary/surgery , RNA/chemistry , RNA/genetics , Reverse Transcriptase Polymerase Chain Reaction , Social Behavior , Statistics, Nonparametric , Vitellogenins/genetics , Vitellogenins/physiology
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