期刊论文详细信息
BMC Evolutionary Biology
Exploring the role of juvenile hormone and vitellogenin in reproduction and social behavior in bumble bees
Abraham Hefetz2  Christina Grozinger1  Osnat Malka2  Etya Amsalem1 
[1] Department of Entomology, Center for Pollinator Research, Center for Chemical Ecology, The Pennsylvania State University, University Park, PA 16802, USA;Department of Zoology, George S. Wise Faculty of Life Sciences, Tel Aviv University, Tel Aviv, Israel
关键词: Reproduction;    Social insects;    Bombus terrestris;    Aggression;    Vitellogenin;   
Others  :  857789
DOI  :  10.1186/1471-2148-14-45
 received in 2013-11-18, accepted in 2014-02-21,  发布年份 2014
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【 摘 要 】

Background

The genetic and physiological pathways regulating behavior in solitary species are hypothesized to have been co-opted to regulate social behavior in social species. One classic example is the interaction between vitellogenin (an egg-yolk and storage protein) and juvenile hormone, which are positively correlated in most insect species but have modified interactions in highly eusocial insects. In some of these species (including some termites, ants, and the honey bee), juvenile hormone and vitellogenin levels are negatively correlated and juvenile hormone has shifted its role from a gonadotropin to a regulator of maturation and division of labor in the primarily sterile workers. The function of vitellogenin also seems to have broadened to encompass similar roles. Thus, the functions and molecular interactions of juvenile hormone and vitellogenin are hypothesized to have undergone changes during the evolution of eusociality, but the mechanisms underlying these changes are unknown.

Bumble bees offer an excellent model system for testing how the relationship between juvenile hormone and vitellogenin evolved from solitary to social species. Bumble bee colonies are primitively eusocial and comprised of a single reproductive queen and facultatively sterile workers. In Bombus terrestris, juvenile hormone retains its ancestral role as a gonadotropin and is also hypothesized to regulate aggressive behavior. However, the function of vitellogenin and its interactions with juvenile hormone have not yet been characterized.

Results

By characterizing vitellogenin RNA expression levels (vg) in B. terrestris we show that vg is not associated with task and only partially associated with worker age, queen presence, and caste (queen vs worker). The correlations of vg with ovarian activation were not consistent across experiments, but both vg and ovarian activation were significantly associated with levels of aggression experienced by workers. Treatment with juvenile hormone did not affect vg levels in queenless groups.

Conclusions

We suggest that social interactions affect vg levels more strongly than a worker’s reproductive physiological state, and that juvenile hormone and vg are uncoupled in this species. Thus, although juvenile hormone maintains its traditional role as gonadotropin in B. terrestris, vg has already been co-opted into a novel role, consistent with the model that Bombus represents an intermediate stage in the evolution of eusociality.

【 授权许可】

   
2014 Amsalem et al.; licensee BioMed Central Ltd.

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Figure 5.

【 参考文献 】
  • [1]Toth AL, Varala K, Newman TC, Miguez FE, Hutchison SK, Willoughby DA, Simons JF, Egholm M, Hunt JH, Hudson ME, Robinson GE: Wasp gene expression supports an evolutionary link between maternal behavior and eusociality. Science 2007, 318(5849):441-444.
  • [2]Robinson GE, Vargo EL: Juvenile hormone in adult eusocial Hymenoptera: gonadotropin and behavioral pacemaker. Arch Insect Biochem Physiol 1998, 35(4):559-583.
  • [3]Nijhout HF, Wheeler D: Juvenile hormone and the physiological basis of insect polymorphism. Q Rev Biol 1982, 57(2):109-133.
  • [4]Hartfelder K: Insect juvenile hormone: from “status quo” to high society. Brazil J Med Biolog Res 2000, 33(2):157-177.
  • [5]Brent CS, Schal C, Vargo EL: Endocrine changes in maturing primary queens of Zootermopsis angusticollis. J Insect Physiol 2005, 51(11):1200-1209.
  • [6]Elliott KL, Stay B: Juvenile hormone synthesis as related to egg development in neotenic reproductives of the termite Reticulitermes flavipes, with observations on urates in the fat body. Gen Comparat Endocrinol 2007, 152(1):102-110.
  • [7]Elliott KL, Stay B: Changes in juvenile hormone synthesis in the termite Reticulitermes flavipes during development of soldiers and neotenic reproductives from groups of isolated workers. J Insect Physiol 2008, 54(2):492-500.
  • [8]Cornette R, Gotoh H, Koshikawa S, Miura T: Juvenile hormone titers and caste differentiation in the damp-wood termite Hodotermopsis sjostedti (Isoptera, Termopsidae). J Insect Physiol 2008, 54(6):922-930.
  • [9]Korb J, Hoffmann K, Hartfelder K: Endocrine signatures underlying plasticity in postembryonic development of a lower termite, Cryptotermes secundus (Kalotermitidae). Evol Dev 2009, 11(3):269-277.
  • [10]Guidugli KR, Nascimento AM, Amdam GV, Barchuk AR, Omholt S, Simoes ZL, Hartfelder K: Vitellogenin regulates hormonal dynamics in the worker caste of a eusocial insect. FEBS Lett 2005, 579(22):4961-4965.
  • [11]Amdam GV, Page RE: The developmental genetics and physiology of honeybee societies. Anim Behav 2010, 79(5):973-980.
  • [12]Sommer K, Holldobler B, Rembol H: Behavioral and physiological aspects of reproductive control in a Diacamma species from Malaysia (Formicidae, Ponerinae). Ethology 1993, 94:162-170.
  • [13]Dong SZ, Ye GY, Guo JY, Hu C: Roles of ecdysteroid and juvenile hormone in vitellogenesis in an endoparasitic wasp, Pteromalus puparum (Hymenoptera: Pteromalidae). Gen Comparat Endocrinol 2009, 160(1):102-108.
  • [14]Delisle J, Cusson M: Juvenile hormone biosynthesis, oocyte growth and vitellogenin accumulation in Choristoneura fumiferana and C. rosaceana: a comparative study. J Insect Physiol 1999, 45(6):515-523.
  • [15]Panaitof SC, Scott MP: Effect of juvenile hormone on vitellogenin gene expression in the fat body of burying beetles, Nicrophorus orbicollis. Arch Insect Biochem Physiol 2006, 63(2):82-91.
  • [16]Wang ZW, Davey KG: The role of juvenile hormone in vitellogenin production in Rhodnius prolixus. J Insect Physiol 1993, 39(6):471-476.
  • [17]Martin D, Piulachs MD, Belles X: Patterns of hemolymph vitellogenin and ovarian vitellin in the German cockroach, and the role of juvenile hormone. Physiol Entomol 1995, 20(1):59-65.
  • [18]Glinka AV, Kleiman AM, Wyatt GR: Roles of juvenile-hormone, a brain factor and adipokinetic hormone in regulation of vitellogenin biosynthesis in Locusta-migratoria. Int J Biochem Mol Biol 1995, 35(2):323-328.
  • [19]Klowden MJ: Endocrine control of mosquito reproduction. Arch Insect Biochem Physiol 1997, 35:491-512.
  • [20]Parthasarathy R, Sun ZY, Bai H, Palli SR: Juvenile hormone regulation of vitellogenin synthesis in the red flour beetle, Tribolium castaneum. Insect Biochem Mol 2010, 40(5):405-414.
  • [21]Barth RH, Lester LJ, Sroka P, Kessler T, Hearn R: Juvenile hormone promotes dominance behavior and ovarian development in social wasps (Polistes annularis). Experientia 1974, 31(6):691-692.
  • [22]Bloch G, Borst DW, Huang ZY, Robinson GE, Cnaani J: Juvenile hormone titers, juvenile hormone biosynthesis, ovarian development and social environment in B. terrestris. J Insect Physiol 2000, 46:47-57.
  • [23]Giray T, Giovanetti M, West-Eberhard MJ: Juvenile hormone, reproduction, and worker behavior in the neotropical social wasp Polistes canadensis. Proc Natl Acad Sci USA 2005, 102(9):3330-3335.
  • [24]Chen TT, Hillen LJ: Expression of the vitellogenin genes in insects. Gamete Res 1983, 7:179-196.
  • [25]Hagedorn HH: Vitellogenin and vitellin in insects. Ann Rev Entomol 1979, 24:475-505.
  • [26]Engelmann F: Insect vitellogenin: identification, biosynthesis and role in Vitellogenesis. In Advanced in Insect Physiology, vol. 14. Edited by Treherne JE, Berridge MJ, Wigglesworth VB. New York: Academic Press INC; 1979:49-108.
  • [27]Borst DW, Eskew MR, Wagner SJ, Shores K, Hunter J, Luker L, Hatle JD, Hecht LB: Quantification of juvenile hormone III, vitellogenin, and vitellogenin-mRNA during the oviposition cycle of the lubber grasshopper. Insect Biochem Mol Biol 2000, 30(8):813-819.
  • [28]Adams TS, Filipi PA, Yi SX: Effect of age, diet, diapause and juvenile hormone on oogenesis and the of amount of vitellogenin and vitellin in the two spotted stink bug, Perillus bioculatus (Heteroptera :pentatomidae). J Insect Physiol 2002, 48(4):477-486.
  • [29]Sueren-Castillo S, Abrisqueta M, Maestro JL: FoxO inhibits juvenile hormone biosynthesis and vitellogenin production in the German cockroach. Insect Biochem Mol Biol 2012, 42(7):491-498.
  • [30]Chinzei Y, White BN, Wyatt GR: Vitellogenin mRNA in locust fat body: identification, isolation, and quantitative changes induced by juvenile hormone. Can J Biochem 1982, 60:243-251.
  • [31]Comas D, Piulachs MD, Belles X: Fast induction of vitellogenin gene expression by juvenile hormone III in the cockroach Blattella germanica (L.) (Dictyoptera, Blattellidae). Insect Biochem Mol 1999, 29(9):821-827.
  • [32]Comas D, Piulachs MD, Belles X: Induction of vitellogenin gene transcription in vitro by juvenile hormone in Blattella germanica. Mol Cell Endocrinol 2001, 183(1–2):93-100.
  • [33]Sheng Z, Xu J, Bai H, Zhu F, Palli SR: Juvenile hormone regulates vitellogenin gene expression through insulin-like peptide signaling pathway in the red flour beetle, Tribolium castaneum. J Biolog Chem 2011, 286(49):41924-41936.
  • [34]Nijhout HF: Insect Hormones. Princeton: Princeton University Press; 1994.
  • [35]Chen TT, Couble P, DeLuca FL, Wyatt GR: Juvenile Hormone Control of Vitellogenesis in Locusta migratoriaIn. New York: Plenum Press; 1976.
  • [36]Amdam GV, Omholt SW: The regulatory anatomy of honeybee lifespan. J Theor Biol 2002, 216(2):209-228.
  • [37]Pinto LZ, Bitondi MMG, Simoes ZLP: Inhibition of vitellogenin synthesis in Apis mellifera workers by a juvenile hormone analogue, pyriproxyfen. J Insect Physiol 2000, 46(2):153-160.
  • [38]Corona M, Velarde RA, Remolina S, Moran-Lauter A, Wang Y, Hughes KA, Robinson GE: Vitellogenin, juvenile hormone, insulin signaling, and queen honey bee longevity. Proc Natl Acad Sci USA 2007, 104(17):7128-7133.
  • [39]Wang Y, Brent CS, Fennern E, Amdam GV: Gustatory perception and fat body energy metabolism are jointly affected by vitellogenin and juvenile hormone in honey bees. PLoS Genet 2012, 8(6):e1002779.
  • [40]Amdam GV, Norberg K, Hagen A, Omholt SW: Social exploitation of vitellogenin. Proc Natl Acad Sci USA 2003, 100(4):1799-1802.
  • [41]Formesyn EM, Cardoen D, Ernst UR, Danneels EL, Vaerenbergh MV, Koker DD, Verleyen P, Wenseleers T, Schoofs L, Graaf DCD: Reproduction of honeybee workers is regulated by epidermal growth factor receptor signaling. Gen Comparat Endocrinol 2014, 197(1):1-4.
  • [42]Pontona F, Wilsonc K, Holmesb AJ, Cottere SC, Raubenheimerf D, Simpsona SJ: Integrating nutrition and immunology: A new frontier. J Insect Physiol 2013, 59(2):130-137.
  • [43]Penick CA, Liebig J, Brent CS: Reproduction, dominance, and caste: endocrine profiles of queens and workers of the ant Harpegnathos saltator. J Comparat Physiol 2011, 197(11):1063-1071.
  • [44]Cuvillier-Hot V, Lenoir A, Peeters C: Reproductive monopoly enforced by sterile police workers in a queenless ant. Behav Ecol 2004, 15:970-975.
  • [45]Maekawa K, Ishitani K, Gotoh H, Cornette R, Miura T: Juvenile Hormone titre and vitellogenin gene expression related to ovarian development in primary reproductives compared with nymphs and nymphoid reproductives of the termiteReticulitermes speratus. Physiol Entomol 2010, 35(1):52-58.
  • [46]Duchateau MJ, Velthuis HHW: Development and reproductive strategies in Bombus terrestris colonies. Behavior 1988, 107:186-207.
  • [47]Roseler PF: Juvenile hormone control of oogenesis in bumblebee workers, Bombus terrestris. J Insect Physiol 1977, 23:985-992.
  • [48]Roseler PF, Roseler I: Influence of juvenile hormone on fat body metabolism in ovariolectomized queens of the bumblebee, Bombus terrestris. Insect Biochem Mol Biol 1988, 18(6):557-563.
  • [49]Van Doorn A: Factors influencing dominance behavior in queenless bumblebee workers Bombus terrestris. Physiol Entomol 1989, 14:211-222.
  • [50]Michener CD: The Social Behavior of the Bees. Cambridge, Massachusetts: Harvard University Press; 1974.
  • [51]Bourke AFG: Worker matricide in social bee and wasps. J Theor Biol 1994, 167:283-292.
  • [52]Van Honk CJK, Roeseler PF, Velthuis HHW, Hogeveen JC: Factors influencing egg laying of workers in a captive Bombus terrestris colony. Behav Ecol Sociobiol 1981, 9:9-14.
  • [53]Van Doorn A, Heringa J: The ontogeny of a dominance hierarchy in colonies of the bumblebee Bombus terrestris (Hymenoptera, Apidae). Insect Soc 1986, 33:3-25.
  • [54]Amsalem E, Hefetz A: The appeasement effect of sterility signaling in dominance contests among Bombus terrestris workers. Behav Ecol Sociobiol 2010, 64(10):1685-1694.
  • [55]Amsalem E, Hefetz A: The effect of group size on the interplay between dominance and reproduction in Bombus terrestris. PloS One 2011, 6(3):e18238.
  • [56]Amsalem E, Shamia D, Hefetz A: Aggression or ovarian development as determinants of reproductive dominance in Bombus terrestris: interpretation using a simulation model. Insect Soc 2013, 60(2):213-222.
  • [57]Duchateau MJ, Velthuis HHW: Ovarian development and egg-laying in workers of Bombus-terrestris. Entomologia Experimentalis Et Applicata 1989, 51(3):199-213.
  • [58]Amsalem E, Twele R, Francke W, Hefetz A: Reproductive competition in the bumble-bee Bombus terrestris: do workers advertise sterility? Proc Biol Sci 2009, 276(1660):1295-1304.
  • [59]Grozinger CM, Yongliang F, Hoover SER, Winston RL: Genome-wide analysis reveals differences in brain gene expression patterns associated with caste and reproductive status in honey bees (Apis mellifera). Mol Ecol 2007, 16(22):4837-4848.
  • [60]Niño EL, Tarpy DR, Grozinger CM: Differential effects of insemination volume and substance on reproductive changes in honey bee queens (Apis mellifera L.). Insect Mol Biol 2013, 22(3):233-244.
  • [61]Li Z, Zhang S: Vitellogenin functions as a multivalent pattern recognition receptor with an opsonic activity. PloS One 2008, 3(4):e1940.
  • [62]Nelson CM, Ihle KE, Fondrk MK, Page RE, Amdam GV: The gene vitellogenin has multiple coordinating effects on social organization. Plos Biol 2007, 5(3):e62.
  • [63]Amdam GV, Omholt SW: The hive bee to forager transition in honeybee colonies: the double repressor hypothesis. J Theor Biol 2003, 223(4):451-464.
  • [64]Amdam GV, Norberg K, Page RE Jr, Erber J, Scheiner R: Downregulation of vitellogenin gene activity increases the gustatory responsiveness of honey bee workers (Apis mellifera). Behav Brain Res 2006, 169(2):201-205.
  • [65]Wheeler MM, Ament SA, Rodriguez-Zas SL, Robinson GE: Brain gene expression changes elicited by peripheral vitellogenin knockdown in the honey bee. Insect Mol Biol 2013, 22(5):562-573.
  • [66]Nakamura A, Yasuda K, Adachi H, Sakurai Y, Ishii N: Vitellogenin-6 is a major carbonylated protein in aged nematode, Caenorhabditis elegans. Biochem Biophys Res Commun 1999, 264:580-583.
  • [67]Shi XD, Zhang SC, Pang QX: Vitellogenin is a novel player in defense reactions. Fish Shellfish Immunol 2006, 20:769-772.
  • [68]Amdam GV, Hartfelder K, Norberg K, Hagen A, Omholt SW: Altered physiology in worker honey bees (Hymenoptera: Apidae) infested by the mite Varroa destructor (Acari: Varroidae): a factor in colony loss during over-wintering? J Econ Entomol 2004, 97:741-747.
  • [69]Corona M, Libbrecht R, Wurm Y, Riba-Grognuz O, Studer RA, Keller L: Vitellogenin underwent subfunctionalization to acquire caste and behavioral specific expression in the harvester ant Pogonomyrmex barbatus. PLoS Genet 2013, 9(8):e1003730.
  • [70]Wegener J, Huang ZY, Lorenz MW, Lorenz JI, Bienefeld K: New insights into the roles of juvenile hormone and ecdysteroids in honey bee reproduction. J Insect Physiol 2013, 59(7):655-661.
  • [71]Shpigler H, Patch HM, Cohen M, Fan Y, Grozinger CM, Bloch G: The transcription factor Kruppel homolog 1 is linked to hormone mediated social organization in bees. BMC Evol Biol 2010, 10:120. BioMed Central Full Text
  • [72]Van Doorn A: Investigations into the regulation of dominance behavior and of the division of labor in bumblebee colonies Bombus-terrestris. Netherl J Zool 1986, 37(3–4):255-276.
  • [73]Alaux C, Savarit F, Jaisson P, Hefetz A: Does the queen win it all? Queen-worker conflict over male production in the bumblebee, Bombus terrestris. Naturwissenschaften 2004, 91(8):400-403.
  • [74]Sibbald ED, Plowright CMS: On the relationship between aggression and reproduction in pairs of orphaned worker bumblebees (Bombus impatiens). Insect Soc 2012, 60(1):23-30.
  • [75]Amsalem E, Shpigler H, Bloch G, Hefetz A: Dufour’s gland secretion, sterility and foraging behavior: correlated behavior traits in bumblebee workers. J Insect Physiol 2013, 59(12):1250-1255.
  • [76]Lee YK, Yoom HJ, Lee SB, Park IG, Sohn HD, Jin BR: Molecular cloning and characterization of vitellogenin in Bombus ignitus. J Ind Entomol 2009, 18(1):33-40.
  • [77]Li J, Huang J, Cai W, Zhao Z, Peng W, Wu J: The vitellogenin of the bumblebee, Bombus hypocrita: studies on structural analysis of the cDNA and expression of the mRNA. J Comp Physiol B 2010, 180(2):161-170.
  • [78]Hornakova D, Matouskova P, Kindl J, Valterova I, Pichova I: Selection of reference genes for real-time polymerase chain reaction analysis in tissues from Bombus terrestris and Bombus lucorum of different ages. Analyt Biochem 2010, 397(1):118-120.
  • [79]Cameron SA, Robinson GE: Juvenile hormone does not affect division of labor in bumble bee colonies (Hymenoptera: Apidae). Ann Entomol Soc Am 1990, 83(3):626-631.
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