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      Gonadotropic and Physiological Functions of Juvenile Hormone in Bumblebee ( Bombus terrestris) Workers

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          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.

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          Most cited references 24

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          Social exploitation of vitellogenin.

          Vitellogenin is a female-specific glucolipoprotein yolk precursor produced by all oviparous animals. Vitellogenin expression is under hormonal control, and the protein is generally synthesized directly before yolk deposition. In the honeybee (Apis mellifera), vitellogenin is not only synthesized by the reproductive queen, but also by the functionally sterile workers. In summer, the worker population consists of a hive bee group performing a multitude of tasks including nursing inside the nest, and a forager group specialized in collecting nectar, pollen, water, and propolis. Vitellogenin is synthesized in large quantities by hive bees. When hive bees develop into foragers, their juvenile hormone titers increase, and this causes cessation of their vitellogenin production. This inverse relationship between vitellogenin synthesis and juvenile hormone is opposite to the norm in insects, and the underlying proximate processes and life-history reasons are still not understood. Here we document an alternative use of vitellogenin by showing that it is a source for the proteinaceous royal jelly that is produced by the hive bees. Hive bees use the jelly to feed larvae, queen, workers, and drones. This finding suggests that the evolution of a brood-rearing worker class and a specialized forager class in an advanced eusocial insect society has been directed by an alternative utilization of yolk protein.
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            Accumulation of yolk proteins in insect oocytes.

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              Krüppel homolog 1, an early juvenile hormone-response gene downstream of Methoprene-tolerant, mediates its anti-metamorphic action in the red flour beetle Tribolium castaneum.

              Juvenile hormone (JH) prevents ecdysone-induced metamorphosis in insects. However, our knowledge of the molecular mechanisms of JH action is still fragmented. Krüppel homolog 1 (Kr-h1) is a JH-inducible transcription factor in Drosophila melanogaster (Minakuchi, C., Zhou, X., Riddiford, L.M., 2008b. Krüppel homolog 1 (Kr-h1) mediates juvenile hormone action during metamorphosis of Drosophila melanogaster. Mech. Dev. 125, 91-105). Analysis of expression of the homologous gene (TcKr-h1) in the beetle Tribolium castaneum showed that its transcript was continuously present in the larval stage but absent in the pupal stage. Artificial suppression of JH biosynthesis in the larval stage caused a precocious larval-pupal transition and a down-regulation of TcKr-h1 mRNA. RNAi-mediated knockdown of TcKr-h1 in the larval stage induced a precocious larval-pupal transition. In the early pupal stage, treatment with an exogenous JH mimic (JHM) caused formation of a second pupa, and a rapid and large induction of TcKr-h1 transcription. JHM-induced formation of a second pupa was counteracted by the knockdown of TcKr-h1. RNAi experiments in combination with JHM treatment demonstrated that in the larval stage TcKr-h1 works downstream of the putative JH receptor Methoprene-tolerant (TcMet), and in the pupal stage it works downstream of TcMet and upstream of the pupal specifier broad (Tcbr). Therefore, TcKr-h1 is an early JH-response gene that mediates JH action linking TcMet and Tcbr.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2014
                24 June 2014
                : 9
                : 6
                Affiliations
                [1 ]Department of Ecology, Evolution, and Behavior, The Alexander Silberman Institute of Life Sciences, The Hebrew University of Jerusalem, Jerusalem, Israel
                [2 ]Department of Zoology, George S. Wise Faculty of Life Sciences, Tel Aviv University, Tel Aviv, Israel
                [3 ]Department of Entomology, Michigan State University, East Lansing, Michigan, United States of America
                University of Sussex, United Kingdom
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: HS GB. Performed the experiments: HS MC AJS. Analyzed the data: HS. Contributed reagents/materials/analysis tools: ZYH EA AH. Wrote the paper: HS GB.

                Article
                PONE-D-14-04351
                10.1371/journal.pone.0100650
                4069101
                24959888

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                Page count
                Pages: 10
                Funding
                This work was supported by United States - Israel Binational Agricultural Research and Development Fund, #IS-4418-11, http://www.bard-isus.com to GB; US-Israel Binational Science Foundation - BSF #2007465, http://www.bsf.org.il/BSFPublic/Default.aspx to GB and GVA; the "Hoffman Leadership and Responsibility" doctoral scholarship to HS; and the Vaadia-BARD Postdoctoral Fellowship Award No. FI-462-2012 from BARD to HS. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Anatomy
                Endocrine System
                Biochemistry
                Hormones
                Evolutionary Biology
                Organismal Evolution
                Animal Evolution
                Physiology
                Endocrine Physiology
                Reproductive Endocrinology
                Zoology
                Animal Behavior
                Animal Physiology
                Entomology

                Uncategorized

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