Hostname: page-component-586b7cd67f-t8hqh Total loading time: 0 Render date: 2024-11-22T17:03:57.522Z Has data issue: false hasContentIssue false

Current immunity markers in insect ecological immunology: assumed trade-offs and methodological issues

Published online by Cambridge University Press:  29 August 2012

M. Moreno-García
Affiliation:
Departamento de Ecología Evolutiva, Instituto de Ecología, Universidad Nacional Autónoma de México, Apdo. P. 70-275, Circuito Exterior, Ciudad Universitaria, 04510, Coyoacán, Distrito Federal, México Centro de Investigaciones Sobre Enfermedades Infecciosas, Instituto Nacional de Salud Pública, Avenida Universidad 655, Santa María Ahuacatitlán, 62100 Cuernavaca, Morelos, México
A. Córdoba-Aguilar
Affiliation:
Departamento de Ecología Evolutiva, Instituto de Ecología, Universidad Nacional Autónoma de México, Apdo. P. 70-275, Circuito Exterior, Ciudad Universitaria, 04510, Coyoacán, Distrito Federal, México
R. Condé
Affiliation:
Centro de Investigaciones Sobre Enfermedades Infecciosas, Instituto Nacional de Salud Pública, Avenida Universidad 655, Santa María Ahuacatitlán, 62100 Cuernavaca, Morelos, México
H. Lanz-Mendoza*
Affiliation:
Centro de Investigaciones Sobre Enfermedades Infecciosas, Instituto Nacional de Salud Pública, Avenida Universidad 655, Santa María Ahuacatitlán, 62100 Cuernavaca, Morelos, México
*
*Author for correspondence Fax: +52 777 317 5485 E-mail: [email protected]

Abstract

The field of ecological immunology currently relies on using a number of immune effectors or markers. These markers are usually used to infer ecological trade-offs (via conflicts in resource allocation), though physiological nature of these markers remains elusive. Here, we review markers frequently used in insect evolutionary ecology research: cuticle darkening, haemocyte density, nodule/capsule formation, phagocytosis and encapsulation/melanization via use of nylon filaments and beads, phenoloxidase activity, nitric oxide production, lysozyme and antimicrobial peptide production. We also provide physiologically based information that may shed light on the probable trade-offs inferred when these markers are used. In addition, we provide a number of methodological suggestions to improve immune marker assessment.

Type
Research Paper
Copyright
Copyright © Cambridge University Press 2012

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abrams, J.M., White, K., Fessler, L.I. & Steller, H. (1993) Programmed cell death during Drosophila embryogenesis. Development 117, 2943.Google Scholar
Adamo, S.A. (1999) Evidence for adaptive changes in egg laying in crickets exposed to bacteria and parasites. Animal Behaviour 57, 117124.Google Scholar
Adamo, S.A. (2004) Estimating disease resistance in insects: phenoloxidase and lysozyme-like activity and disease resistance in the cricket Gryllus texensis. Journal of Insect Physiology 50, 209216.Google Scholar
Adamo, S.A. & Parsons, N.M. (2006) The emergency life-history stage and immunity in the cricket, Gryllus texensis. Animal Behaviour 72, 235244.Google Scholar
Agaisse, H. & Perrimon, N. (2004) The roles of JAK/STAT signaling in Drosophila immune responses. Immunological Reviews 198, 7782.Google Scholar
Ahtiainen, J.J., Alatalo, R.V., Kortet, R. & Rantala, M.J. (2005) A trade-off between sexual signalling and immune function in a natural population of the drumming wolf spider Hygrolycosa rubrofasciata. Journal of Evolutionary Biology 18, 985991.CrossRefGoogle Scholar
Andersen, S.O., Hojrup, P. & Roepstorff, P. (1995) Insect cuticular proteins. Insect Biochemistry and Molecular Biology 25, 153176.Google Scholar
Armitage, S.A.O. & Siva-Jothy, M.T. (2005) Immune function responds to selection for cuticular colour in Tenebrio molitor. Heredity 94, 650656.Google Scholar
Ashida, M. & Brey, P.T. (1997) Recent advances in research on the insect prophenoloxidase cascade. pp. 135172in Brey, P.T. & Hultmark, D. (Eds) Molecular Mechanisms of Immune Responses in Insects. New York, USA, Chapman & Hall.Google Scholar
Ayres, J.S. & Schneider, D.S. (2009) The role of anorexia in resistance and tolerance to infections in Drosophila. PLoS Biology 7, e1000150.Google Scholar
Bailey, N.W. & Zuk, M. (2010) Changes in immune effort of male field crickets infested with mobile parasitoid larvae. Journal of Insect Physiology 54, 96104.CrossRefGoogle Scholar
Barnard, C.J., Collins, S.A., Daisley, J.N. & Behnke, J.M. (2006) Odour learning and immunity costs in mice. Behavioural Processes 72, 7483.Google Scholar
Barnes, A.I. & Siva-Jothy, M.T. (2000) Density-dependent prophylaxis in the mealworm beetle Tenebrio molitor L. (Coleoptera: Tenebrionidae): cuticular melanization is an indicator of investment in immunity. Proceedings of the Royal Society of London, Series B 267, 177182.Google Scholar
Bocher, A., Doums, C., Millot, L. & Tirard, C. (2008) Reproductive conflicts affect labor and immune defense in the queenless ant diacam sp ‘Nilgiri. Evolution 62, 123134.Google Scholar
Boots, M. & Begon, M. (1993) Trade-offs with resistance to a granulosis virus in the indian meal moth, examined by a laboratory evolution experiment. Functional Ecology 7, 528534.Google Scholar
Bredt, D.S. & Snyder, S.H. (1994) Nitric oxide: a physiological messenger molecule. Annual Review of Biochemistry 63, 175195.Google Scholar
Brookman, J.L., Rowley, A.F. & Ratcliffe, N.A. (1989) Studies on nodule formation in locusts following injection of microbial products. Journal of Invertebrate Pathology 53, 315323.CrossRefGoogle Scholar
Brzek, P. & Konarzewski, M. (2007) Relationship between avian growth rate and immune response depends on food availability. Journal of Experimental Biology 210, 23612367.Google Scholar
Bulet, P., Charlet, M. & Hetru, C. (2003) Antimicrobial peptides in insect immunity. pp. 89108in Ezekowitz, R.A.B. & Hoffmann, J.A. (Eds) Innate Immunity. New Jersey, USA, Humana Press.Google Scholar
Bulet, P., Stöcklin, R. & Menin, L. (2004) Anti-microbial peptides: from invertebrates to vertebrates. Immunological Review 198, 169184.CrossRefGoogle ScholarPubMed
Bulet, P., Hetru, C., Dimarq, J.L. & Hoffmann, D. (1999) Antimicrobial peptides in insects: structure and function. Developmental and Comparative Immunology, 23, 329344.Google Scholar
Calleri, D.V., Rosengars, R.B. & Traniello, J.F.A. (2007) Immunity and reproduction during colony foundation in the dampwood termite, Zootermopsis angusticollis. Physiological Entomology 32, 136142.Google Scholar
Carton, Y. & Nappi, A.J. (1997) Drosophila cellular immunity against parasitoids. Parasitology Today 13, 218227.Google Scholar
Casteels, P. (1998) Immune response in Hymenoptera. pp. 92110in Brey, P.T. & Hultmark, D. (Eds) Molecular Mechanisms of Immune Responses in Insects. New York, USA, Chapman & Hall.Google Scholar
Cerenius, L. & Söderhäll, K. (2004) The prophenoloxidase.activating system in invertebrates. Immunological Review 198, 116126.Google Scholar
Chapman, R.F. (1998) The Insects: Structure and Function. Cambridge, UK, Cambridge University Press.Google Scholar
Chen, P.S., Mitchell, H.K. & Neuweg, M. (1978) Tyrosine glucoside in Drosophila busckii. Insect Biochemistry 8, 279286.Google Scholar
Christensen, B.M., Li, J., Ch.-Ch., Chen & Nappi, A.J. (2005) Melanization immune responses in mosquito vectors. Trends in Parasitology 21, 192199.Google Scholar
Contreras-Garduño, J., Canales-Lazcano, J. & Córdoba-Aguilar, A. (2006) Wing pigmentation, immune ability, fat reserves and territorial status in males of the rubyspot damselfly, Hetaerina americana. Journal of Ethology 24, 165173.Google Scholar
Contreras-Garduño, J., Lanz-Mendoza, H. & Córdoba-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, 612621.Google Scholar
Cotter, S.C., Hails, R.S., Cory, J.S. & Wilson, K. (2004) Density-dependent prophylaxis and condition-dependent immune function in Lepidopteran larvae: a multivariate approach. Journal of Animal Ecology 73, 283293.Google Scholar
da Silva, C.C.A., Dunphy, G.B. & Rau, M.E. (2000) Interaction of Xenorhabdus nematophilus (Enterobacteriaceae) with the Antimicrobial Defenses of the House Cricket, Acheta domesticus. Journal of Invertebrate Pathology 76, 285292.Google Scholar
Darwin, C. (1871) The Descent of Man and Selection in Relation to Sex. London, UK, John Murray.Google Scholar
Day, T., Graham, A.L. & Read, A.F. (2007) Evolution of parasite virulence when host responses cause disease. Proceedings of the Royal Society of London, Series B 274, 26852692.Google Scholar
Decker, H. & Jaenicke, E. (2004) Recent findings on phenoloxidase activity and aintimicrobial activity of hemocyanins. Developmental and Comparative Immunology 28, 673687.Google Scholar
Desjardins, M., Houde, M. & Gagnon, E. (2005) Phagocytosis: the convoluted way from nutrition to adaptive immunity. Immunological Reviews 207, 158165.CrossRefGoogle ScholarPubMed
Duffy, M.A. & Sivars-Becker, L. (2007) Rapid evolution and ecological host-parasite dynamics. Ecology Letters 10, 4453.Google Scholar
Eleftherianos, I., Baldwin, H., ffrench-Constant, R.H. & Reynolds, S.E. (2008) Developmental modulation of immunity: Changes within the feeding period of the fifth larval stage in the defence reactions of Manduca sexta to infection by Photorhabdus. Journal of Insect Physiology 54, 309318.Google Scholar
Falconer, D.S. & Mackay, T.F. (1996) Introduction to Quantitative Genetics. New York, USA, Dover.Google Scholar
Faraldo, A.C., Sá-Nunes, A., Del Bel, E.A., Faccioli, L.H. & Lello, E. (2005) Nitric oxide production in blowfly hemolymph after yeast inoculation. Nitric Oxide 13, 240246.Google Scholar
Fedorka, K.M., Zuk, M. & Mousseau, T.A. (2004) Immune supression and the cost of reproduction in the ground cricket, Allonemobius socius. Evolution 58, 24782485.Google Scholar
Fellowes, M.D.E., Kraaijeveld, A.R. & Godfray, H.C.J. (1998) Trade-off associated with selection for increased ability to resist parasitoid attack in Drosophila melanogaster. Proceedings of the Royal Society of London, Series B 265, 15531558.Google Scholar
Ferdig, M., Beerntsen, B., Spray, F., Li, J. & Christensen, B. (1993) Reproductive costs associated with resistance in a mosquito-filarial worm system. American Journal of Tropical Medicine & Hygiene 49, 756762.Google Scholar
Ferrandon, D., Imler, J.L., Hetru, C. & Hoffman, J.A. (2007) The Drosophila systemic immune response: a sensing and signalling during bacterial and fungal infections. Nature Reviews in Immunology 7, 863874.Google Scholar
Foley, E. & O'Farrell, P.H. (2003) Nitric oxide contributes to induction of innate immune responses to gram negative bacteria in Drosophila. Genes & Development 17, 115125.Google Scholar
Franc, N.C., Dimarcq, J.-L., Lagueux, M., Hoffmann, J. & Ezekowitz, R.A.B. (1996) Croquemort, a novel Drosophila hemocyte/macrophage receptor that recognizes apoptotic cells. Immunity 4, 431443.CrossRefGoogle ScholarPubMed
Gardiner, E.M. & Strand, M.R. (2000) Hematopoiesis in larval Pseudoplusia includens and Spodoptera frugiperda. Archives of Insect Biochemistry and Physiology 43, 147164.Google Scholar
Gillespie, J.P., Kanost, M.R. & Trenzeck, T. (1997) Biological mediators of insect immunity. Annual Review of Entomology 42, 611643.Google Scholar
Goldsworthy, G., Mullen, L., Opoku-Ware, K. & Chandrakant, S. (2003) Interactions between the endocrine and immune systems in locusts. Physiological Entomology 28, 5461.Google Scholar
González-Santoyo, I. & Córdoba-Aguilar, A. (2012) Phenoloxidase: a key component of the insect immune system. Entomologia Experimentalis et Applicata 142, 116.Google Scholar
Gosline, J., Lillie, M., Carrington, E., Guerette, P., Ortlepp, C. & Savage, K. (2002) Elastic proteins: biological roles and mechanical properties. Philosophical Transactions of the Royal Society of London, Series B 357, 121132.Google Scholar
Haas, F., Gorb, S. & Blickhan, R. (2000) The function of resilin in beetle wings. Proceedings of the Royal Society of London, Series B 267, 13751381.Google Scholar
Hernández-Martínez, S., Lanz, H., Rodrguez, M.H., González-Ceron, L. & Tsutsumi, V. (2002) Cellular-mediated reactions to foreign organisms inoculated into the hemocoel of Anopheles albimanus (Diptera: Culicidae). Journal of Medical Entomology 39, 6169.Google Scholar
Herrera-Ortiz, A., Lanz-Mendoza, H., Martínez-Barnetche, J., Hernández-Martínez, S., Villarreal-Treviño, C., Aguilar-Marcelino, L. & Rodríguez, M.H. (2004) Plasmodium berghei ookinetes induces nitric oxide production in Anopheles pseudopunctipennis midguts cultured in vitro. Insect Biochemistry and Molecular Biology 34, 893901.Google Scholar
Hetru, C., Hoffman, D. & Bulet, P. (1997) Antimicrobial peptides from insects. pp. 4066in Brey, P.T. & Hultmark, D. (Eds) Molecular Mechanisms of Immune Responses in Insects. New York, USA, Chapman & Hall.Google Scholar
Hillyer, J.F., Schmidt, S.L. & Christensen, B.M. (2003) Rapid phagocytosis and melanization of bacteria and Plasmodium sporozoites by hemocytes of the mosquito Aedes aegypti. Journal of Parasitology 89, 6269.Google Scholar
Hillyer, J.F., Schmidt, S.L. & Christensen, B.M. (2004) The antibacterial innate immune response by the mosquito Aedes aegypti is mediated by hemocytes and independent of Gram type and pathogenicity. Microbes and Infection 6, 448459.Google Scholar
Hillyer, J.F., Schmidt, S.L., Fuchs, J.F., Boyle, J.P. & Christensen, B.M. (2005) Age-associated mortality in immune challenged mosquitoes (Aedes aegypti) correlates with a decrease in haemocyte numbers. Cellular Microbiology 7, 3951.Google Scholar
Hoang, A. (2001) Immune response to parasitism reduces resistance of Drosophila melanogaster to desiccation and starvation. Evolution 55, 23522358.Google Scholar
Hoffmann, D., Brehelin, M. & Hoffmann, J.A. (1974) Modifications of the hemogram and of the hemocytopoietic tissue of male adults of Locusta migratoria (Orthoptera) after injection of Bacillus thuringiensis. Journal of Invertebrate Pathology 24, 238247.Google Scholar
Hoffmann, J.A. (1973) Blood-forming tissues in orthopteran insects: An analogue to vertebrate hemopoietic organs. Cellular and Molecular Life Sciences 29, 5051.Google Scholar
Hoffmann, J.A. & Reichhart, J.M. (2002) Drosophila innate immunity: an evolutionary perspective. Nature Immunology 3, 121126.Google Scholar
Hogg, J.C. & Hurd, H. (1995) Malaria-induced reduction of fecundity during the first gonotrophic cycle of Anopheles stephensi mosquitoes. Medical and Veterinary Entomology 9, 176180.Google Scholar
Hoi-Leitner, M., Romero-Pujante, M., Hoy, H. & Pavlova, A. (2001) Food availability and immune capacity in serin (Serinus serinus) nestlings. Behavioral Ecology and Sociobiology 49, 333339.Google Scholar
Holz, A., Bossinger, B., Strasser, T., Janning, W. & Klapper, R. (2003) The two origins of hemocytes in Drosophila. Development 130, 49554962.Google Scholar
Howard, R.W., Miller, J.S. & Stanley, D.W. (1998) The influence of bacterial species and intensity of infections on nodule formation in insects. Journal of Insect Physiology 44, 157164.Google Scholar
Ilango, K. (2005) Structure and function of the spermathecal complex in the phlebotomine sandfly Phlebotomus papatasi Scopoli (Diptera: Psychodidae): I. ultrastructure and histology. Journal of Bioscience 30, 101131.Google Scholar
Jacot, A., Scheuber, H., Kurtz, J. & Brinkhof, M.W.G. (2005) Juvenile immune system activation induces a costly upregulation of adult immunity in field crickets Gryllus campestris. Proceedings of the Royal Society of London, Series B 272, 6369.Google ScholarPubMed
Jollès, P. (1996) Lysozymes: Model Enzymes in Biochemistry and Biology. Switzerland, Birkhäuser Verlag.Google Scholar
Koskimaki, J., Rantala, M.J., Taskinen, J., Tynkkynen, K. & Suhonen, J. (2004) Immunocompetence and resource holding potential in the damselfly, Calopteryx virgo L. Behavioral Ecology 15, 169173.Google Scholar
Kraaijeveld, A.R. & Godfray, H.C.J. (1997) Trade-off between parasitoid resistance and larval competitive ability in Drosophila melanogaster. Nature 389, 278280.Google Scholar
Kraaijeveld, A.R., Limentani, E.C. & Godfray, H.C.J. (2001) Basis of the trade-off between parasitoid resistance and larval competitive ability in Drosophila melanogaster. Proceedings of the Royal Society of London, Series B 268, 259261.Google ScholarPubMed
Krishnana, N., Hyršl, P. & Šimek, V. (2006) Nitric oxide production by hemocytes of larva and pharate prepupa of Galleria mellonella in response to bacterial lipopolysaccharide: Cytoprotective or cytotoxic? Comparative Biochemistry and Physiology, Part C 142, 103110.Google Scholar
Kumar, S., Christophides, G.K., Cantera, R., Charles, B., Soo Han, Y., Meister, S., Dimopoulos, G., Kafatos, F.C. & Barillas-Mury, C. (2003) The role of reactive oxygen species on Plasmodium melanotic encapsulation in Anopheles gambiae. Proceedings of the National Academy of Science USA 100, 1413914144.Google Scholar
Kurtz, J. (2002) Phagocytosis by invertebrate hemocytes: Causes of individual variation in Panorpa vulgaris scorpionflies. Microscopy Research and Technique 57, 456468.Google Scholar
Kurtz, J. & Sauer, K.P. (1999) The immunocompetence handicap hypothesis: testing the genetic predictions. Proceedings of the Royal Society of London, Series B 266, 25152522.Google Scholar
Kurtz, J., Wiesner, A., Götz, P. & Sauer, K.P. (2000) Gender differences and individual variation in the immune system of the scorpionfly Panorpa vulgaris (Insecta: Mecoptera). Developmental and Comparative Immunology 24, 112.Google Scholar
Lackie, A.M. (1988) Hemocyte behaviour. Advances in Insect Physiology 21, 85178.Google Scholar
Laurent, M., Lepoivre, M. & Tenu, J.P. (1996) Kinetic modelling of the nitric oxide gradient generated in vitro by adherent cells expressing inducible nitric oxide synthase. Biochemistry Journal 314, 109113.Google Scholar
Lavine, M.D. & Strand, M.R. (2002) Insect hemocytes and their role in immunity. Insect Biochemistry and Molecular Biology 32, 12951309.Google Scholar
Lawniczak, M.K.N., Barnes, A.I., Linklater, J.R., Boone, J.M., Wigby, S. & Chapman, T. (2006) Mating and immunity in invertebrates. Trends in Ecology and Evolution 22, 4855.Google Scholar
Levenbook, L., Bodnaryk, R.P. & Spande, T.F. (1969) P-alanyl-L-tyrosine: Chemical synthesis, properties and occurrence in larvae of the fleshfly Sarcophaga bullata Parker. Biochemical Journal 113, 837841.Google Scholar
Li, J. & Christensen, B.M. (1993) Involvement of L-tyrosine and phenoloxidase in the tanning of Aedes aegypti eggs. Insect Biochemistry and Molecular Biology 23, 739748.Google Scholar
Ling, E. & Yu, X.Q. (2006) Cellular encapsulation and melanization are enhanced by immulectins, pattern recognition receptors from the tobacco hornworm Manduca sexta. Developmental and Comparative Immunology 30, 289299.Google Scholar
Luce-Fedrow, A., Von Ohlen, T. & Chapes, S.K. (2009) Ehrlichia chaffeensis infections in Drosophila melanogaster. Infection and Immunity 77, 48154826.Google Scholar
Luckhart, S., Vodovotz, Y., Cui, L. & Rosenberg, R. (1998) The mosquito Anopheles stephensi limits malaria parasite development with inducible synthesis of nitric oxide. Proceedings of the National Academy of Science USA 95, 57005705.Google Scholar
Manetti, A.G.O., Rosetto, M. & Marchini, D. (1998) Antibacterial peptides of the insect reproductive tract. pp. 6791in Brey, P.T. & Hultmark, D. (Eds) Molecular Mechanisms of Immune Responses in Insects. New York, USA, Chapman & Hall.Google Scholar
Mavrouli, M.D., Tsakas, S., Theodorou, G.L., Lampropoulou, M. & Marmaras, V.J. (2005) MAP kinases mediate phagocytosis and melanization via prophenoloxidase activation in medfly hemocytes. Biochimica et Biophysica Acta, Molecular Cell Research 1744, 145156.Google Scholar
McKean, K.A. & Nunney, L. (2001) Increased sexual activity reduces male immune function in Drosophila melanogaster. Proceedings of the National Academy of Science USA 98, 79047909.Google Scholar
Miller, J.S., Howard, R.W., Nguyen, A., Rosario, R.M.T. & Stanley-Samuelson, D.W. (1996) Eicosanoids mediate nodulation responses to bacterial infections in larvae of the tenebrionid beetle, Zophobas atratus. Journal of Insect Physiology 42, 312.Google Scholar
Mitchell, H.K. & Lunan, K.D. (1964) Tyrosine-O-phosphate in Drosophila. Archives of Biochemistry and Biophysics 106, 219222.Google Scholar
Moreno-García, M., Lanz-Mendoza, H. & Córdoba-Aguilar, A. (2010) Genetic variance and genotype-by-environment interaction of immune response in Aedes aegypti (Diptera: Culicidae). Journal of Medical Entomology 47, 111120.Google Scholar
Moret, Y. & Schmid-Hempel, P. (2000) Survival for immunity: the price of immune system activation for bumblebee workers. Science 290, 11661168.CrossRefGoogle Scholar
Müller, U. (1997) The nitric oxide system in insects. Progress in Neurobiology 51, 363381.Google Scholar
Nappi, A.J. & Christensen, B.M. (2005) Melanogenesis and associated cytotoxic reactions: applications to insect innate immunity. Insect Biochemistry and Molecular Biology 35, 443459.Google Scholar
Nappi, A.J. & Ottaviani, E. (2000) Cytotoxicity and cytotoxic molecules in invertebrates. BioEssays 22, 469480.Google Scholar
Nappi, A.J., Vass, E., Frey, F. & Carton, Y. (2000) Nitric oxide involvement in Drosophila immunity. Nitric Oxide 4, 423430.Google Scholar
Narayanan, K. (2004) Insect defence: its impact on microbial control of insect pests. Current Science 86, 800814.Google Scholar
Nardi, J.B., Pilas, B., Ujhelyi, E., Garsha, K. & Kanost, M.R. (2003) Hematopoietic organs of Manduca sexta and hemocyte lineages. Development, Genes and Evolution 213, 477491.Google Scholar
Osanai, M. & Chen, P. (1993) A comparative study on the arginine degradation cascade for sperm maturation of Bombyx mori and Drosophila melanogaster. Amino Acids 5, 341350.Google Scholar
Otvos, L. Jr (2000) Antibacterial peptides isolated from insects. Journal of Peptide Science 6, 497511.Google Scholar
Packer, C., Holt, R.D., Hudson, P.J., Lafferty, K.D. & Dobson, A.P. (2003) Keeping the herds healthy and alert: implications of predator control for infectious disease. Ecology Letters 6, 797802.Google Scholar
Pech, L.L., Trudeau, D. & Strand, M.R. (1994) Separation and behavior in vitro of hemocytes from the moth, Pseudoplusia includens. Cell Tissue Research 277, 159167.Google Scholar
Pham, L.N., Dionne, M.S., Shirasu-Hiza, M. & Schneider, D.S. (2007) A specific primed immune response in Drosophila is dependent on phagocytes. PLoS Pathogens 3, e26.Google Scholar
Rantala, M.J. & Kortet, R. (2003) Courtship song and immune function in the field cricket Gryllus bimaculatus. Biological Journal of the Linnean Society 79, 503510.Google Scholar
Rantala, M.J. & Kortet, R. (2004) Male dominance and immunocompetence in a field cricket. Behavioral Ecology 15, 187191.Google Scholar
Rantala, M.J. & Roff, D.A. (2005) An analysis of trade-offs in immune function, body size, and developmental time in the Mediterranean Field Cricket, Gryllus bimaculatus. Functional Ecology 19, 323330.Google Scholar
Rantala, M.J. & Roff, D.A. (2007) Inbreeding and extreme outbreeding cause sex differences in immune defence and life history traits in Epirrita autumnata. Heredity 98, 329336.Google Scholar
Rantala, M.J., Koskimäki, 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, Series B 267, 24532457.Google Scholar
Read, A.F., Graham, A.L. & Råberg, L. (2008) Animal defenses against infectious agents: is damage control more important than pathogen control. PLoS Biology 6, e1000004.Google Scholar
Ribeiro, C. & Brehélin, M. (2006) Insect haemocytes: What type of cell is that? Journal of Insect Physiology 52, 417429.Google Scholar
Riddiford, L.M. & Hiruma, K. (1988) Regulation of melanization in insect cuticle. Program of Clinical Biological Research 256, 423436.Google Scholar
Rigby, M. & Jokela, J. (2000) Predator avoidance and immune defence: costs and trade-offs in snails. Proceedings of the Royal Society of London, Series B 267, 171176.Google Scholar
Rivero, A. (2006) Nitric oxide: an antiparasitic molecule of invertebrates. Trends in Parasitology 22, 219225.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, 738746.Google Scholar
Roberts, M.L., Buchanan, K.L. & Evans, M.R. (2004) Testing the immunocompetence hypothesis: a review of the evidence. Animal Behaviour 68, 227239.Google Scholar
Roff, D.A. (1992) The Evolution of Life Histories. New York, USA, Chapman & Hall.Google Scholar
Rolff, J., Armitage, S.A.O. & Coltman, D.W. (2005) Genetic constraints and sexual dimorphism in immune defence. Evolution 59, 18441850.Google Scholar
Rolff, J. & Reynolds, S. (Eds) (2009) Insect Infection and Immunity: Evolution, Ecology and Mechanisms. Oxford, UK, Oxford University Press.Google Scholar
Roy, M. & Holt, R.D. (2008) Effects of predation on host-pathogen dynamics in SIR models. Theoretical Population Biology 73, 319331.CrossRefGoogle ScholarPubMed
Ryder, J.J. & Siva-Jothy, M.T. (2001) Quantitative genetics of immune function and body size in the house cricket, Acheta domesticus. Journal of Evolutionary Biology 14, 646653.Google Scholar
Saul, S. & Sugumaran, M. (1988) A novel quinone: quinone methide isomerase generates quinone methides in insect cuticle. FEBS Letter 237, 155158.Google Scholar
Schmid-Hempel, P. (2005a) Evolutionary ecology of insect immune defences. Annual Review of Entomology 50, 529551.Google Scholar
Schmid-Hempel, P. (2005b) Natural insect host-parasite systems show immune priming and specificity: puzzles to be solved. BioEssays 27, 10261034.Google Scholar
Schneider, D.S. & Ayres, J.S. (2008) Two ways to survive infection: what resistance and tolerance can teach us about treating infectious diseases. Nature Reviews Immunology 8, 889895.Google Scholar
Schwartz, A. & Koella, J.C. (2004) The cost of immunity in the yellow fever mosquito, Aedes aegypti depends on immune activation. Journal of Evolutionary Biology 17, 834840.Google Scholar
Sheldon, B.C. & Verhulst, S. (1996) Ecological immunology: costly parasite defences and trade offs in evolutionary ecology. Trends in Ecology and Evolution 11, 317321.Google Scholar
Simmons, L.W., Zuk, M. & Rotenberry, J.T. (2005) Immune function reflected in calling song characteristics in a natural population of the cricket Teleogryllus commodus. Animal Behaviour 69, 12351241.Google Scholar
Siva-Jothy, M.T. (2000) A mechanistic link between parasite resistance and expression of a sexually selected trait in a damselfly. Proceedings of the Royal Society of London, Series B 267, 25232527.Google Scholar
Söderhäll, K. & Cerenius, L. (1998) Role of the prophenoloxidase-activating system in invertebrate immunity. Current Opinion in Immunology 10, 2328.Google Scholar
Stearns, S.C. (1992) The Evolution of Life Histories. Oxford, UK, Oxford University Press.Google Scholar
Stevenson, R.D. (2006) Ecophysiology and conservation: the contribution to energetics – introduction to the symposium. Integrative and Comparative Biology 46, 10881092.Google Scholar
Sugumaran, M. & Kanost, M.R. (1993) Regulation of insect haemolymph phenoloxidases. pp. 317342in Beckage, N.E., Thompson, S.N. & Federico, B.A. (Eds) Parasites and Pathogens of Insects. Volume I. Parasites. San Diego, CA, USA, Academic Press.Google Scholar
Tarlow, E.M. & Blumsteid, D.T. (2007) Evaluating methods to quantify anthropogenic stressors on wild animals. Applied Animal Behaviour Science 102, 429451.Google Scholar
Thompson, J.J.W., Armitage, S.A.O. & Siva-Jothy, M.T. (2002) Cuticular colour change after imaginal eclosion is time constrained: blacker beetles darken faster. Physiological Entomology 27, 136141.CrossRefGoogle Scholar
Uchida, K. (1993) Balanced amino acid composition essential for infusion-induced egg development in the mosquito (Culex pipiens pallens). Journal of Insect Physiology 39, 615621.Google Scholar
Williams, M.J. (2007) Drosophila hemopoiesis and cellular immunity. Journal of Immunology 178, 47114715.Google Scholar
Wilson, K., Knell, R., Boots, M. & Koch-Osborne, J. (2003) Group living and investment in immune defence: an interspecific analysis. Journal of Animal Ecology 72, 133143.Google Scholar