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Blue light-induced immunosuppression in Bactrocera dorsalis adults, as a carryover effect of larval exposure

  • K. Tariq (a1) (a2), M. Noor (a3), M. Hori (a4), A. Ali (a2), A. Hussain (a2), W. Peng (a1), C.-J. Chang (a5) and H. Zhang (a1)...


Detrimental effects of ultraviolet (UV) light on living organisms are well understood, little is known about the effects of blue light irradiation. Although a recent study revealed that blue light caused more harmful effects on insects than UV light and blue light irradiation killed insect pests of various orders including Diptera, the effects of blue light on physiology of insects are still largely unknown. Here we studied the effects of blue light irradiation on cuticular melanin in larval and the immune response in adult stage of Bactrocera dorsalis. We also evaluated the effects of blue light exposure in larval stage on various age and mass at metamorphosis and the mediatory role of cuticular melanin in carryover effects of larval stressors across metamorphosis. We found that larvae exposed to blue light decreased melanin contents in their exoskeleton with smaller mass and delayed metamorphosis than insects reared without blue light exposure. Across metamorphosis, lower melanotic encapsulation response and higher susceptibility to Beauveria bassiana was detected in adults that had been exposed to blue light at their larval stage, thereby constituting the first evidence that blue light impaired adult immune function in B. dorsalis as a carryover effect of larval exposure.


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Abrams, P.A., Leimar, O., Nylin, S. & Wiklund, C. (1996) The effect of flexible growth rates on optimal sizes and development times in a seasonal environment. American Naturalist 147, 381395.
Adamo, S.A. (2004) How should behavioural ecologists interpret measurements of immunity? Animal Behaviour 68, 14431449.
Allen, B.G.V., Briggs, V.S., McCoy, M.W. & Vonesh, J.R. (2010) Carry-over effects of the larval environment on post-metamorphic performance in two hylid frogs. Oecologia 164, 891898.
Bai, P.-P., Chen, E.-H., Shen, G.-M., Wei, D., Wei, D.-D. & Wang, J.-J. (2014) Inhibition of phenoloxidase activity delays development in Bactrocera dorsalis (Diptera: Tephritidae). Florida Entomologist 97, 477485.
Balasubramanian, N., Hao, Y.-J., Toubarro, D., Nascimento, G., Simões, N. (2009) Purification, biochemical and molecular analysis of a chymotrypsin protease with prophenoloxidase suppression activity from the entomopathogenic nematode Steinernema carpocapsae . International Journal of Parasitology 39, 975984.
Ben-Yakir, D., Antignus, Y., Offir, Y. & Shahak, Y. (2013) Optical manipulations: an advance approach for reducing sucking insect pests. pp. 249267 in Advanced Technologies for Managing Insect Pests. Netherlands, Springer.
Bonmati-Carrion, M.A., Arguelles-Prieto, R., Martinez-Madrid, M.J., Reiter, R., Hardeland, R., Rol, M.A. & Madrid, J.A. (2014) Protecting the melatonin rhythm through circadian healthy light exposure. International Journal of Molecular Sciences 15, 2344823500.
Campero, M., De Block, M., Ollevier, F. & Stoks, R. (2008a) Metamorphosis offsets the link between larval stress, adult asymmetry and individual quality. Functional Ecology 22, 271277.
Campero, M., Block, M.D., Ollevier, F. & Stoks, R. (2008b) Correcting the short-term effect of food deprivation in a damselfly: mechanisms and costs. Journal of Animal Ecology 77, 6673.
Carrillo-Vico, A., Lardone, P.J., Álvarez-Sánchez, N., Rodríguez-Rodríguez, A. & Guerrero, J.M. (2013) Melatonin: buffering the immune system. International Journal of Molecular Sciences 14, 86388683.
Chang, C.L., Vargas, R.I., Caceres, C., Jang, E. & Cho, I.K. (2006) Development and assessment of a liquid larval diet for Bactrocera dorsalis (Diptera: Tephritidae). Annals of the Entomological Society of America 99, 11911198.
Chiarelli-Neto, O., Ferreira, A.S., Martins, W.K., Pavani, C., Severino, D., Faião-Flores, F., Maria-Engler, S.S., Aliprandini, E., Martinez, G.R., Di Mascio, P., Medeiros, M.H.G., Baptista, M.S. (2014) Melanin photosensitization and the effect of visible light on epithelial cells. PLoS ONE 9, e113266.
Cossentine, J., Thistlewood, H., Goettel, M., Jaronski, S. (2010) Susceptibility of preimaginal western cherry fruit fly, Rhagoletis indifferens (Diptera: Tephritidae) to Beauveria bassiana (Balsamo) Vuillemin Clavicipitaceae (Hypocreales). Journal of Invertebrate Pathology 104, 105109.
Daniel, C. & Wyss, E. (2009) Susceptibility of different life stages of the European cherry fruit fly, Rhagoletis cerasi, to entomopathogenic fungi. Journal of applied entomology 133, 473483.
Debecker, S., Sommaruga, R., Maes, T. & Stoks, R. (2015) Larval UV exposure impairs adult immune function through a trade-off with larval investment in cuticular melanin. Functional Ecology 29, 12921299.
De La Rosa, W., Lopez, F.L. & Liedo, P. (2002) Beauveria bassiana as a pathogen of the Mexican fruit fly (Diptera: Tephritidae) under laboratory conditions. Journal of Economic Entomology 95, 3643.
Dimbi, S., Maniania, N.K., Lux, S.A., Ekesi, S. & Mueke, J.K. (2003) Pathogenicity of Metarhizium anisopliae (Metsch.) Sorokin and Beauveria bassiana (Balsamo) Vuillemin, to three adult fruit fly species: Ceratitis capitata (Weidemann), C. rosa var. fasciventris Karsch and C. cosyra (Walker) (Diptera :Tephritidae). Mycopathologia 156, 375382.
Ekesi, S., Maniania, N., Lux, S. (2002) Mortality in three African tephritid fruit fly puparia and adults caused by the entomopathogenic fungi, Metarhizium anisopliae and Beauveria bassiana . Biocontrol Science and Technology 12, 717.
González-Santoyo, I. & Córdoba-Aguilar, A. (2012) Phenoloxidase: a key component of the insect immune system. Entomologia Experimentalis et Applicata 142, 116.
Hagen, S.B., Sørlibråten, O., Ims, R.A. & Yoccoz, N.G. (2006) Density-dependent melanism in winter moth larvae (Lepidoptera: Geometridae): a countermeasure against parasitoids? Environmental Entomology 35, 12491253.
Hanife, G. (2008) Modified agar-based diet for small scale laboratory rearing of olive fruit fly, Bactrocera oleae (Diptera: Tephritidae). Florida Entomologist 91, 651656.
Hori, M., Shibuya, K., Sato, M. & Saito, Y. (2014) Lethal effects of short-wavelength visible light on insects. Scientific Reports 4, 7383.
Johansen, N., Vänninen, I., Pinto, D.M., Nissinen, A. & Shipp, L. (2011) In the light of new greenhouse technologies: 2. Direct effects of artificial lighting on arthropods and integrated pest management in greenhouse crops. Annals of Applied Biology 159, 127.
Jurkiewicz, B.A. & Buettner, G.R. (1994) Ultraviolet light-induced free radical formation in skin: an electron paramagnetic resonance study. Photochemistry and Photobiology 59, 14.
Lane, B.S., Humphreys, A.M., Thompson, K. & Trinci, A.P.J. (1988) ATP content of stored spores of Paecilomyces farinosus and the use of ATP as a criterion of spore viability. Transactions of the British Mycological Society 90, 109111.
Lee, K.P., Simpson, S.J. & Wilson, K. (2008) Dietary protein-quality influences melanization and immune function in an insect. Functional Ecology 22, 10521061.
Marjan De Block, R.S. (2005) Fitness effects from egg to reproduction: bridging the life history transition. Ecology 86, 185197.
Nagel, L., Mlynarek, J.J. & Forbes, M.R. (2011) Immune response to nylon filaments in two damselfly species that differ in their resistance to ectoparasitic mites. Ecological Entomology 36, 736743.
Neyen, C., Bretscher, A.J., Binggeli, O. & Lemaitre, B. (2014) Methods to study Drosophila immunity. Methods 68, 116128.
O'Connor, C.M., Norris, D.R., Crossin, G.T. & Cooke, S.J. (2014) Biological carryover effects: linking common concepts and mechanisms in ecology and evolution. Ecosphere 5, art28.
Ohara, M., Kawashima, Y., Watanabe, H. & Kitajima, S. (2002) Effects of blue-light-exposure on growth of extracorporeally circulated leukemic cells in rats with leukemia induced by 1-ethyl-1-nitrosourea. International Journal of Molecular Medicine 10, 407411.
Ohara, M., Kobayashi, M., Fujiwara, H., Kitajima, S., Mitsuoka, C. & Watanabe, H. (2004) Blue light inhibits melanin synthesis in B16 melanoma 4A5 cells and skin pigmentation induced by ultraviolet B in guinea-pigs. Photodermatology, Photoimmunology & Photomedicine 20, 8692.
Ortonne, J.P. (2002) Photoprotective properties of skin melanin. British Journal of Dermatology 146, 710.
Pechenik, J.A. (2006) Larval experience and latent effects – metamorphosis is not a new beginning. Integrative and Comparative Biology 46, 323333.
Pechenik, J.A., Wendt, D.E. & Jarrett, J.N. (1998) Metamorphosis is not a new beginning. Bioscience 48, 901910.
Prokkola, J., Roff, D., Kärkkäinen, T., Krams, I. & Rantala, M.J. (2013) Genetic and phenotypic relationships between immune defense, melanism and life-history traits at different temperatures and sexes in Tenebrio molitor . Heredity 111, 8996.
Rantala, M.J., & Roff, D.A. (2005) An analysis of trade-offs in immune function, body size and development time in the Mediterranean Field Cricket, Gryllus bimaculatus . Functional Ecology 19, 323330.
Rantala, M.J., KoskimÌki, J., Taskinen, J., Tynkkynen, K. & Suhonen, J. (2000) Immunocompetence, developmental stability and wingspot size in the damselfly Calopteryx splendens L. Proceedings of the Royal Society of London B: Biological Sciences 267, 24532457.
Relyea, R.A. (2007) Getting out alive: how predators affect the decision to metamorphose. Oecologia 152, 389400.
Robb, T., Forbes, M.R. & Jamieson, I.G. (2003) Greater cuticular melanism is not associated with greater immunogenic response in adults of the polymorphic mountain stone weta, Hemideina maori . Ecological Entomology 28, 738746.
Roulin, A. (2014) Melanin-based colour polymorphism responding to climate change. Global Change Biology 20, 33443350.
Rowe, L. & Ludwig, D. (1991) Size and timing of metamorphosis in complex life cycles: time constraints and variation. Ecology 72, 413427.
Shi, Z.-H. & Sun, J.-H. (2010) Immunocompetence of the red turpentine beetle, Dendroctonus valens LeConte (Coleoptera: Curculionidae, Scolytinae): variation between developmental stages and sexes in populations in China. Journal of Insect Physiology 56, 16961701.
Siva-Jothy, M.T., Moret, Y. & Rolff, J. (2005) Insect immunity: an evolutionary ecology perspective. Advances in Insect Physiology 32, 148.
Smilanich, A.M., Dyer, L.A. & Gentry, G.L. (2009) The insect immune response and other putative defenses as effective predictors of parasitism. Ecology 90, 14341440.
Stoks, R. & Cordoba-Aguilar, A. (2012) Evolutionary ecology of Odonata: a complex life cycle perspective. Annual Review of Entomology 57, 249265.
Stoks, R., Swillen, I. & De Block, M. (2012) Behaviour and physiology shape the growth accelerations associated with predation risk, high temperatures and southern latitudes in Ischnura damselfly larvae. Journal of Animal Ecology 81, 10341040.
Sugumaran, M. (2002) Comparative biochemistry of eumelanogenesis and the protective roles of phenoloxidase and melanin in insects. Pigment Cell Research 15, 29.
Talloen, W., Van Dyck, H. & Lens, L. (2004) The cost of melanization: butterfly wing coloration under environmental stress. Evolution; International Journal of Organic Evolution 58, 360366.
Tariq, K., Noor, M., Saeed, S. & Zhang, H. (2015) The effect of ultraviolet-A radiation exposure on the reproductive ability, longevity, and development of the Dialeurodes citri (Homoptera: Aleyrodidae) F1 generation. Environmental entomology 44, 16141618.
Therry, L., Nilsson-Örtman, V., Bonte, D. & Stoks, R. (2014) Rapid evolution of larval life history, adult immune function and flight muscles in a poleward-moving damselfly. Journal of Evolutionary Biology 27, 141152.
Thompson, D.J., Hassall, C., Lowe, C.D. & Watts, P.C. (2011) Field estimates of reproductive success in a model insect: behavioural surrogates are poor predictors of fitness. Ecology Letters 14, 905913.
Vile, G.F. & Tyrrell, R.M. (1995) UVA radiation-induced oxidative damage to lipids and proteins in vitro and in human skin fibroblasts is dependent on iron and singlet oxygen. Free Radical Biology and Medicine 18, 721730.
Zhang, C.-Y., Meng, J.-Y., Wang, X.-P., Zhu, F. & Lei, C.-L. (2011) Effects of UV-A exposures on longevity and reproduction in Helicoverpa armigera, and on the development of its F1 generation. Insect Science 18, 697702.
Zheng, W., Peng, T., He, W. & Zhang, H. (2012) High-Throughput sequencing to reveal genes involved in reproduction and development in Bactrocera dorsalis (Diptera: Tephritidae). PLoS ONE 7, e36463.
Zhou, J., Shang, J., Ping, F. & Zhao, G. (2012) Alcohol extract from Vernonia anthelmintica (L.) willd seed enhances melanin synthesis through activation of the p38 MAPK signaling pathway in B16F10 cells and primary melanocytes. Journal of Ethnopharmacology 143, 639647.



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