Caste-biased Expression of fem and Amdsx Genes in Apis mellifera ligustica (Hymenoptera: Apidae)

Authors

  • Lu-Xia Pan Honeybee Research Institute, Jiangxi Agricultural University.
  • Fu-Ping Cheng Honeybee Research Institute, Jiangxi Agricultural University.
  • Zi-Long Wang Honeybee Research Institute, Jiangxi Agricultural University.

DOI:

https://doi.org/10.13102/sociobiology.v68i2.5654

Keywords:

sex determination, caste differentiation, gene expression, quantitative RT-PCR, juvenile hormone

Abstract

Sex determination and caste differentiation are two crucial processes for morphology building in honeybees. It is unclear whether there is an interaction between these two processes. Here, we investigated the expression of fem and Amdsx genes between female castes of honeybees. We found that the expression of fem and Amdsx is significantly higher in queens than in workers, and this expression was positively regulated by juvenile hormone (JH). Our results suggest that sex-determining genes fem and Amdsx are also involved in honeybee caste differentiation.

Downloads

Download data is not yet available.

References

Asencot, M. & Lensky, Y. (1976). The effect of sugars and juvenile hormone on the differentiation of the female honeybee larvae (Apis mellifera L.) to queens. Life Science, 18: 693-699. doi: 10.1016/0024-3205(76)90180-6.

Beye, M., Hasselmann, M., Fondrk, M.K., Page, R.E. & Omholt, S.W. (2003). The gene csd is the primary signal for sexual development in the honeybee and encodes an SR-type protein. Cell, 114: 419-429. doi: 10.1016/s0092-86 74(03)00606-8.

Brito, D.V., Silva, C.G.N., Hasselmann, M., Viana, L.S., Astolfi-Filho, S. & Carvalho-Zilse, G.A. (2015). Molecular characterization of the gene feminizer in the stingless bee Melipona interrupta (Hymenoptera: Apidae) reveals association to sex and caste development. Insect Biochemistry and Molecular Biology, 66: 24-30. doi: 10.1016/j.ibmb. 2015.09.008.

Cho, S., Huang, Z.Y. & Zhang, J. (2007). Sex-specific splicing of the honeybee doublesex gene reveals 300 million years of evolution at the bottom of the insect sex-determination pathway. Genetics, 177: 1733-1741. doi: 10.1534/genetics. 107.078980.

De Oliveira Campos, L.A., Velthuiskluppell, F.M. & Velthuis, H.H.W. (1975). Juvenile hormone and caste determination in a stingless bee. Natunwissenschaften, 62: 98-99. doi:10.1007/bf00592188.

Dorn, A. (1985). Comprehensive insect physiology, biochemistry and pharmacology. International Journal of Biochemistry, 17: 1279. doi:10.1016/0020-711x(85)90021-7.

Gempe, T. & Beye, M. (2010). Function and evolution of sex determination mechanisms, genes and pathways in insects. Bioessays, 33: 52-60. doi: 10.1002/bies.201000043.

Gempe, T., Hasselmann, M., Schiøtt, M., Hause, G., Otte, M. & Beye, M. (2009). Sex determination in honeybees: Two separate mechanisms induce and maintain the female pathway. PLoS Biology, 7: e1000222. doi: 10.1371/journal.pbio.1000222.

Hasselmann, M., Gempe, T., Schiøtt, M., Nunes-Silva, C.G., Otte, M. & Beye, M. (2008). Evidence for the evolutionary nascence of a novel sex determination pathway in honeybees. Nature, 454: 519-522. doi: 10.1038/nature07052.

Haydak, M.H. (1970). Honey bee nutrition. Annual Review of Entomology. 15: 143-156. doi:10.1146/annurev.en.15.010 170.001043.

Kamakura, M. (2011). Royalactin induces queen differentiation in honeybees. Nature, 473: 478-483. doi: 10.1038/nature10093.

Klein, A., Schultner, E., Lowak, H., Schrader, L., Heinze, J., Holman, L. & Oettler, J. (2016). Evolution of social insect polyphenism facilitated by the sex differentiation cascade. PLoS Genetics, 12: e1005952. doi: 10.1371/journal.pgen.1005952.

Kucharski, R., Maleszka, J., Foret, S. & Maleszka, R. (2008). Nutritional control of reproductive status in honeybees via DNA methylation. Science, 319: 1827-1830. doi: 10.1126/science.1153069.

Mao, W., Schuler, M.A. & Berenbaum, M.R. (2015). A dietary phytochemical alters caste-associated gene expression in honey bees. Science Advances, 1: e1500795. doi: 10.1126/sciadv.1500795.

Mutti, N. S., Dolezal, A.G., Wolschin, F., Mutti, J.S., Gill, K.S. & Amdam, G.V. (2011). IRS and TOR nutrient-signaling pathways act via juvenile hormone to influence honey bee caste fate. Journal of Experimental Biology, 214: 3977-3984. doi: 10.1242/jeb.061499.

Patel, A., Fondrk, M.K., Kaftanoglu, O., Emore, C., Hunt, G., Frederick, K. & Amdam, G.V. (2007). The making of a queen: TOR pathway is a key player in diphenic caste development. PLoS One, 2: e509. doi:10.1371/journal.pone.0000509.

Rachinsky, A. & Hartfelder, K. (1990). Corpora allata activity, a prime regulating element for caste-specific juvenile hormone titer in honey bee larvae (Apis mellifera carnica). Journal of Insect Physiology, 36: 189-194. doi: 10.1016/0022-1910(90) 90121-u.

Rachinsky, A., Strambi, C., Strambi, A. & Hartfelder, K. (1990). Caste and metamorphosis: Hemolymph titers of juvenile hormone and ecdysteroids in last instar honeybee larvae. General and Comparative Endocrinology, 79: 31-38. doi:10.1016/0016-6480(90)90085-z.

Rembold, H., Czoppelt, C. & Rao, P.J. (1974). Effect of juvenile hormone treatment on caste differentiation in the honeybee, Apis mellifera. Journal of Insect Physiology, 20: 1193-1202. doi: 10.1016/0022-1910(74)90225-x.

Rembold, H. & Dietz, A. (1965). Biologically active substances in Royal Jelly. Vitamins & Hormones, 23: 359-382. doi: 10. 1016/s0083-6729(08)60385-4.

Roth, A., Vleurinck, C., Netschitailo, O., Bauer, V., Otte, M., Kaftanoglu, O., Page, R.E. & Beye, M. (2019). A genetic switch for worker nutrition-mediated traits in honeybees. PLoS Biology, 17: e3000171. doi: 10.1371/journal.pbio.3000171.

Schmittgen, T.D. & Livak, K.J. (2008). Analyzing real-time PCR data by the comparative CT method. Nature Protocols, 3: 1101-1108. doi: 10.1038/nprot.2008.73.

Spannhoff, A., Kim, Y.K., Raynal, N.J.M., Gharibyan, V., Su, M.B., Zhou, Y.Y., Li, J., Castellano, S., Sbardella, G., Issa, J.P. & Bedford, M.T. (2011). Histone deacetylase inhibitor activity in royal jelly might facilitate caste switching in bees. Embo Reports, 12: 238-243. doi:10.1038/embor.2011.9.

SPSS. (2010). Statistical software SPSS 17.0. SPSS Inc., Chicago, IL, USA.

Wang, Y., Azevedo, S.V., Hartfelder, K. & Amdam, G.V. (2013). Insulin-like peptides (AmILP1 and AmILP2) differentially affect female caste development in the honey bee (Apis mellifera L.). Journal of Experimental Biology, 216: 4347-4357. doi: 10.1242/jeb.085779. doi: 10.1242/jeb. 085779.

Winston, M.L. (1987). The biology of the honey bee. Cambridge, MA: Harvard University Press. doi: 10.1093/arclin/acr108.

Wirtz, P. & Beetsma, J. (1972). Induction of caste differentiation in the honeybee (Apis mellifera) by juvenile hormone. Entomologia Experimentalis et Applicata. 15: 517-520. doi:10.1111/j.1570-7458.1972.tb00239.x.

Wittmann, D. & Engels, W. (1987). Welche Diät ergibt Arbeiterinnenbei in vitro Aufzucht von Honigbienen? Apidologie, 18: 279-288. doi:10.1051/apido:19870307.

Wojciechowski, M., Lowe, R., Maleszka, J., Conn, D., Maleszka, R. & Hurd, P.J. (2018). Phenotypically distinct female castes in honey bees are defined by alternative chromatin states during larval development. Genome Research, 28: 1532-1542. doi:10.1101/gr.236497.118.

Wolschin, F., Mutti, N.S. & Amdam, G.V. (2010). Insulin receptor substrate influences female caste development in honeybees. Biology Letters, 7: 112-115. doi: 10.1098/rsbl. 20100463.

Zhu, K., Liu, M., Fu, Z., Zhou, Z., Kong, Y., Liang, H., Lin, Z., Luo, J., Zheng, H., Wan, P., Zhang, J., Zen, K., Chen, J., Hu, F., Zhang, C.Y., Ren, J. & Chen, X. (2017). Plant microRNAs in larval food regulate honeybee caste development. PLoS Genetics, 13: e1006 946. doi: 10.1371/journal.pgen.1006946.

Downloads

Published

2021-04-15

How to Cite

Pan, L.-X., Cheng, F.-P., & Wang, Z.-L. (2021). Caste-biased Expression of fem and Amdsx Genes in Apis mellifera ligustica (Hymenoptera: Apidae). Sociobiology, 68(2), e5654. https://doi.org/10.13102/sociobiology.v68i2.5654

Issue

Section

Research Article - Bees