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

Published online by Cambridge University Press:  09 May 2017

K. Tariq ,
M. Noor ,
M. Hori ,
A. Ali ,
A. Hussain ,
W. Peng ,
C.-J. Chang  and
H. Zhang
K. Tariq
Affiliation:
State Key Laboratory of Agricultural Microbiology, Institute of Urban and Horticultural Entomology, College of Plant Science and Technology, Huazhong Agricultural University, Wuhan 430070, Hubei, People's Republic of China Department of Agriculture, Abdul Wali Khan University Mardan, Khyber Pakhtunkhwa, Pakistan
M. Noor
Affiliation:
Molecular Biotechnology Laboratory, College of Plant Science and Technology, Huazhong Agricultural University, Wuhan, Hubei 430070, People's Republic of China
M. Hori
Affiliation:
Graduate School of Agricultural Sciences, Tohoku University, Sendai 981-8555, Japan
A. Ali
Affiliation:
Department of Agriculture, Abdul Wali Khan University Mardan, Khyber Pakhtunkhwa, Pakistan
A. Hussain
Affiliation:
Department of Agriculture, Abdul Wali Khan University Mardan, Khyber Pakhtunkhwa, Pakistan
W. Peng
Affiliation:
State Key Laboratory of Agricultural Microbiology, Institute of Urban and Horticultural Entomology, College of Plant Science and Technology, Huazhong Agricultural University, Wuhan 430070, Hubei, People's Republic of China
C.-J. Chang
Affiliation:
Department of Plant Pathology, College of Agricultural and Environmental Sciences University of Georgia, Griffin, GA 30223, USA
H. Zhang*
Affiliation:
State Key Laboratory of Agricultural Microbiology, Institute of Urban and Horticultural Entomology, College of Plant Science and Technology, Huazhong Agricultural University, Wuhan 430070, Hubei, People's Republic of China
*
*Author for correspondence: Phone: +186 027 8728 0276 Fax: +186 027 8728 0796 E-mail: [email protected]
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Abstract

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.

Keywords

blue lightimmunocompetenceBactrocera dorsalismelanotic encapsulationcarryover effects
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 107 , Issue 6 , December 2017 , pp. 734 - 741
Copyright
Copyright © Cambridge University Press 2017 

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References

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, 381–395.Google Scholar
Adamo, S.A. (2004) How should behavioural ecologists interpret measurements of immunity? Animal Behaviour 68, 1443–1449.Google Scholar
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, 891–898.Google Scholar
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, 477–485.Google Scholar
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, 975–984.Google Scholar
Ben-Yakir, D., Antignus, Y., Offir, Y. & Shahak, Y. (2013) Optical manipulations: an advance approach for reducing sucking insect pests. pp. 249–267 in Advanced Technologies for Managing Insect Pests. Netherlands, Springer.Google Scholar
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, 23448–23500.Google Scholar
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, 271–277.Google Scholar
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, 66–73.Google Scholar
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, 8638–8683.Google Scholar
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, 1191–1198.Google Scholar
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.Google Scholar
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, 105–109.Google Scholar
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, 473–483.Google Scholar
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, 1292–1299.Google Scholar
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, 36–43.Google Scholar
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, 375–382.Google Scholar
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, 7–17.Google Scholar
González-Santoyo, I. & Córdoba-Aguilar, A. (2012) Phenoloxidase: a key component of the insect immune system. Entomologia Experimentalis et Applicata 142, 1–16.Google Scholar
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, 1249–1253.Google Scholar
Hanife, G. (2008) Modified agar-based diet for small scale laboratory rearing of olive fruit fly, Bactrocera oleae (Diptera: Tephritidae). Florida Entomologist 91, 651–656.Google Scholar
Hori, M., Shibuya, K., Sato, M. & Saito, Y. (2014) Lethal effects of short-wavelength visible light on insects. Scientific Reports 4, 7383.Google Scholar
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, 1–27.Google Scholar
Jurkiewicz, B.A. & Buettner, G.R. (1994) Ultraviolet light-induced free radical formation in skin: an electron paramagnetic resonance study. Photochemistry and Photobiology 59, 1–4.Google Scholar
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, 109–111.Google Scholar
Lee, K.P., Simpson, S.J. & Wilson, K. (2008) Dietary protein-quality influences melanization and immune function in an insect. Functional Ecology 22, 1052–1061.Google Scholar
Marjan De Block, R.S. (2005) Fitness effects from egg to reproduction: bridging the life history transition. Ecology 86, 185–197.Google Scholar
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, 736–743.Google Scholar
Neyen, C., Bretscher, A.J., Binggeli, O. & Lemaitre, B. (2014) Methods to study Drosophila immunity. Methods 68, 116–128.Google Scholar
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.Google Scholar
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, 407–411.Google Scholar
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, 86–92.Google Scholar
Ortonne, J.P. (2002) Photoprotective properties of skin melanin. British Journal of Dermatology 146, 7–10.Google Scholar
Pechenik, J.A. (2006) Larval experience and latent effects – metamorphosis is not a new beginning. Integrative and Comparative Biology 46, 323–333.Google Scholar
Pechenik, J.A., Wendt, D.E. & Jarrett, J.N. (1998) Metamorphosis is not a new beginning. Bioscience 48, 901–910.Google Scholar
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, 89–96.Google Scholar
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, 323–330.Google Scholar
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, 2453–2457.Google Scholar
Relyea, R.A. (2007) Getting out alive: how predators affect the decision to metamorphose. Oecologia 152, 389–400.Google Scholar
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, 738–746.Google Scholar
Roulin, A. (2014) Melanin-based colour polymorphism responding to climate change. Global Change Biology 20, 3344–3350.Google Scholar
Rowe, L. & Ludwig, D. (1991) Size and timing of metamorphosis in complex life cycles: time constraints and variation. Ecology 72, 413–427.Google Scholar
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, 1696–1701.Google Scholar
Siva-Jothy, M.T., Moret, Y. & Rolff, J. (2005) Insect immunity: an evolutionary ecology perspective. Advances in Insect Physiology 32, 1–48.Google Scholar
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, 1434–1440.Google Scholar
Stoks, R. & Cordoba-Aguilar, A. (2012) Evolutionary ecology of Odonata: a complex life cycle perspective. Annual Review of Entomology 57, 249–265.Google Scholar
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, 1034–1040.Google Scholar
Sugumaran, M. (2002) Comparative biochemistry of eumelanogenesis and the protective roles of phenoloxidase and melanin in insects. Pigment Cell Research 15, 2–9.Google Scholar
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, 360–366.Google Scholar
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, 1614–1618.Google Scholar
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, 141–152.Google Scholar
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, 905–913.Google Scholar
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, 721–730.Google Scholar
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, 697–702.Google Scholar
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.Google Scholar
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, 639–647.Google Scholar