OJE  Vol.3 No.1 , February 2013
In the monarch butterfly the juvenile hormone effect upon immune response depends on the immune marker and is sex dependent
Abstract: In insects, juvenile hormone (JH) decreases or has any effect upon the phenoloxidase (PO) activity, and favors or decreases the Antimicrobial Peptides (AMPs) expression. Although there is no information about the differential effect of such hormone, two possibilities are that it depends on (a) the immune marker recorded and (b) sexual differences. Here, three commonly used immune markers, Phenoloxidase (PO), hydrogen peroxide (H2O2), and lytic activity, were measured 3, 6 and 24 hours after administration of methoprene (JHa, an analog of juvenile hormone) in male and female monarch butterflies (Danaus plexippus). At 3 and 6 h post-JHa administration, the PO activity increased in females but it only increased at 3 h in males, whereas H2O2 levels increased only in females at 3 h. For the remaining times the JHa had a null effect on POand H2O2. On the other hand, the JHa had a null effect for lytic activity in both sexes at 3, 6 and 24 h. To our knowledge, this is the first report of a positive effect of a JHa onPOand H2O2 and suggests that this effect is sex dependent.
Cite this paper: Villanueva, G. , Lanz-Mendoza, H. , Hernández-Martínez, S. , Zavaleta, M. , Manjarrez, J. , Contreras-Garduño, J. and Contreras-Garduño, J. (2013) In the monarch butterfly the juvenile hormone effect upon immune response depends on the immune marker and is sex dependent. Open Journal of Ecology, 3, 53-58. doi: 10.4236/oje.2013.31007.

[1]   Nelson, R.J. (2011) An introduction to behavioral endocrinology. 4th Edition, Sinauer Associated Inc., Sunderland.

[2]   Flatt, T., Tu, M.P. and Tatar, M. (2005) Hormonal pleiotropy and the juvenile hormone regulation of Drosophila development and life history. Bioessays, 27, 999-1010. doi:10.1002/bies.20290

[3]   Zera, A.J., Harshman, L.G. and Williams, T.D. (2007) Evolutionary endocrinology: The developing synthesis between endocrinology and evolutionary genetics. Annual Review of Ecology, Evolution and Systematics, 38, 793-817. doi:10.1146/annurev.ecolsys.38.091206.095615

[4]   Adamo, S.A. (2009) The impact of physiological state on immune function in insects. In: Reynolds, S. and Rolff, J., Eds., Insect Infection and Immunity, Oxford University Press, Oxford. doi:10.1093/acprof:oso/9780199551354.003.0011

[5]   Nijhout, H.F. (1994) Insect hormones. Princeton University Press, Princeton.

[6]   Zhou, X.F., Coll, M. and Applebaum, S.W. (2000) Effect of temperature and photoperiod on juvenile hormone bio-synthesis and sexual maturation in the cotton bollworm, Helicoverpa armigera: Implications for life history traits. Insect Biochemistry and Molecular Biology, 30, 863-868. doi:10.1016/S0965-1748(00)00059-X

[7]   Tatar, M., Chien, S. and Preist, N. (2001) Negligible senescence during reproductive diapause in Drosophila melanogaster. American Naturalist, 158, 248-258. doi:10.1086/321320

[8]   Noriega, F.G. (2004) Nutritional regulation of JH synthesis: a mechanism to control reproductive maturation in mosquitoes? Insect Biochemistry and Molecular Biology, 34, 687-693. doi:10.1016/j.ibmb.2004.03.021

[9]   Hernandez-Martinez, S., Mayoral, J.G., Li, Y. and Noriega, F.G. (2007) Role of Juvenile hormone and allatotropin on nutrient allocation, ovarian development and survivorship in mosquitoes. Journal of Insect Physiology, 53, 230-234. doi:10.1016/j.jinsphys.2006.08.009

[10]   Rantala, M.J., Vainikka, A. and Kortet, R. (2003) The role of juvenile hormone in immune function and pheromone production trade-offs: A test of the immunocompetence handicap principle. Proceedings of the Royal Society, 270, 2257-2261. doi:10.1098/rspb.2003.2472

[11]   Contreras-Garduno, J., Cordoba-Aguilar, A., Lanz-Mendoza, H. and Cordero, A. (2009) Territorial behaviour and immunity are mediated by juvenile hormone: The physiological basis of honest signaling? Functional Ecology, 23, 157-63. doi:10.1111/j.1365-2435.2008.01485.x

[12]   Cerenius, L. and Soderhall, K. (2004) The prophenoloxidase-activating system in invertebrates. Immunological Reviews, 198, 116-126. doi:10.1111/j.0105-2896.2004.00116.x

[13]   Lemaitre, B. and Hoffmann, J. (2007) The host defense of Drosophila melanogaster. Annual Review of Immunology, 25, 697-743. doi:10.1146/annurev.immunol.25.022106.141615

[14]   Khafagi, W.E. and Hegazi, E.M. (2001) Effects of juvenile hormones and precocenes on the immune response of Spodoptera littoralis larvae to supernumerary larvae of the solitary parasitoid, Microplitis rufiventris Kok. Journal of Insect Physiology, 47, 1249-1259. doi:10.1016/S0022-1910(01)00110-X

[15]   Contreras-Garduno, J., Villanueva-Guerra, G. and Alonso-Salgado, A. (2012) Phenoloxidase production: The importance of time after juvenile hormone analogue administration in Hetaerina americana Fabricius. Odonatologica, 41, 1-6.

[16]   Flatt, T., Heyland, A., Porpiglia, F.R.E., Sherlock, C., Yamamoto, R., Garbuzov, A., Palli, S.R. and Silverman, N. (2008) Hormonal regulation of the humoral innate immune response in Drosophila melanogaster. Journal of Experimental Biology, 211, 2712-2724. doi:10.1242/jeb.014878

[17]   Tian, l., Guo, E., Diao, Y., Zhou, S., Peng, Q., Cao, Y., Ling, E. and Li, S. (2010) Genome-wide regulation of innate immunity by juvenile hormone and 20-hydroxyecdysone in the Bombyx fat body. BMC Genomics, 11, 549. doi:10.1186/1471-2164-11-549

[18]   Zera, A. (2007) Endocrine analysis in evolutionary-developmental studies of insect polymorphism: Hormone manipulation versus direct measurement of hormonal regulators. Evolution and Development, 9, 499-513. doi:10.1111/j.1525-142X.2007.00181.x

[19]   Lessman, C.A., Herman, W.S., Schooley, D.A., Tsai, L.W., Bergot, B.J. and Baker, F.C. (1989) Detection of juvenile hormone I, II and III in adult monarch butterflies (Danaus plexippus). Insect Biochemistry, 19, 431-433. doi:10.1016/0020-1790(89)90049-8

[20]   Lessman, C.A. and Herman, W.S. (1983) Seasonal variation in hemolymph juvenile hormone of adult monarchs (Danaus p. plexippus: Lepidoptera). Canadian Journal of Zoology, 61, 88-94. doi:10.1139/z83-009

[21]   Nappi, A.J. and Vass, E. (1998) Hydrogen peroxide production in immune-reactive Drosophila melanogaster. Journal of Parasitology, 84, 1150-1157. doi:10.2307/3284664

[22]   Nappi, A.J., Vass, E., Frey, F. and Carton, Y. (1995) Superoxide anion generation in Drosophila melanotic encapsulation of parasites. European Journal of Cell Biology, 68, 450-456.

[23]   Lanz-Mendoza, H., Hernández-Martínez, S., Ku, M., Gil, A., Rodríguez, M.N. and Rodríguez, M.H. (2002) Superoxide anion in Anopheles albimanus hemolymph and midgut is toxic to Plasmodium berghei ookinetes. Journal of Parasitology, 88, 702-706.

[24]   Herrera-Ortiz, A., Martínez-Barnetche, J., Smit, N., Rodriguez, M.H. and Lanz-Mendoza, H. (2011) The effect of Nitric Oxide and Hydrogen Peroxide in the activation of the systemic immune response of Anopheles albimanus infected with Plasmodium berghei. Developmental and Comparative Immunology, 35, 44-50. doi:10.1016/j.dci.2010.08.004

[25]   Wilson, R. and Ratcliffe, N.A. (2000) Effect of lysozyme on the lectin-mediated phagocytosis of Bacillus cereus by haemocytes of the cockroach, Blaberus discoidalis. Journal of Insect Physiology, 46, 663-670. doi:10.1016/S0022-1910(99)00154-7

[26]   Oberhauser, K.S. and Solensky, M.J. (2004). The monarch butterfly. Biology and conservation. Cornell University Press, Ithaca.

[27]   Butcher, F.R. and Perdue, J.F. (1973) Cytochalasina B. Effect on hormone-mediated responses in cultured cells. Journal Cell Biology, 56, 857-861. doi:10.1083/jcb.56.3.857

[28]   Wigby, S., Domanitskaya, E.V., Choffat, Y., Kubli, E. and Chapman, T. (2008) The effect of mating on immunity can be masked by experimental piercing in female Drosophila melanogaster. Journal of Insect Physiology, 54, 414-420. doi:10.1016/j.jinsphys.2007.10.010

[29]   Rodrigues, J., Brayner, F.A., Alves, L.C., Dixit, R. and Barillas-Mury, C. (2010) Hemocyte differentiation mediates innate immune memory in Anopheles gambiae mos- quitoes. Science, 329, 1353-1355. doi:10.1126/science.1190689

[30]   Rolff, J. and Siva-Jothy, M.T. (2002) Copulation corrupts immunity: A mechanism for a cost of mating in insects. Proceedings of the National Academy of Sciences USA, 99, 9916-9918. doi:10.1073/pnas.152271999

[31]   Contreras-Garduno, J., Lanz-Mendoza, H. and Cordoba-Aguilar, A. (2007) The expression of a sexually selected trait correlates with different immune defense components and survival in males of the American rubyspot. Journal of Insect Physiology, 53, 612-621. doi:10.1016/j.jinsphys.2007.03.003

[32]   Adamo, S.A. (2011) The importance of physiology for ecoimmunlogy: Lessons from the insects. In: Demas, G. and Nelson, R., Eds., Ecoimmunology, Oxford University Press, Oxford.

[33]   Braude, S., Tang-Martinez, Z. and Taylor, G.T. (1999) Stress, testosterone, and the immunoredistribution hypothesis. Behavioral Ecology, 10, 345-350. doi:10.1093/beheco/10.3.345

[34]   Chapman, R.F. (1998) The insects: Structure and function. Cambridge University Press, Cambridge. doi:10.1017/CBO9780511818202

[35]   Nation, J. L. (2002) Insect physiology and biochemistry. CRC Press, Boca Raton.

[36]   Lawniczak, M.K. N., Barnes, A.I., Linklater, J.R., Boone, J.M., Wigby, S.W. and Chapman, T. (2007) Mating and immunity in invertebrates. Trends in Ecology and Evolution, 22, 48-55. doi:10.1016/j.tree.2006.09.012

[37]   Fellous, S. and Lazzaro, B.P. (2011) Potential for evolutionary coupling and decoupling of larval and adult immune gene expression. Molecular Ecology, 20, 1558-1567. doi:10.1111/j.1365-294X.2011.05006.x

[38]   Belgacem, Y.H. and Martin, J.R. (2002) Neuroendocrine control of a sexually dimorphic behavior by a few neurons of the pars intercerebralis in Drosophila. Proceedings of the National Academy of Sciences USA, 99, 15154-15158. doi:10.1073/pnas.232244199

[39]   Emlen, D.J. and Nijhout, H.F. (1999) Hormonal control of male horn length dimorphism in the horned beetle Onthophagus taurus. Journal of Insect Physiology, 45, 45-53. doi:10.1016/S0022-1910(98)00096-1