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Rethinking vector immunology: the role of environmental temperature in shaping resistance

Abstract

Recent ecological research has revealed that environmental factors can strongly affect insect immunity and influence the outcome of host–parasite interactions. To date, however, most studies examining immune function in mosquitoes have ignored environmental variability. We argue that one such environmental variable, temperature, influences both vector immunity and the parasite itself. As temperatures in the field can vary greatly from the ambient temperature in the laboratory, it will be essential to take temperature into account when studying vector immunology.

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Figure 1: Environmental temperature profoundly affects the rates of a range of humoral and cellular immune responses.
Figure 2: Changes in ambient temperature differentially affect two parasite traits.

References

  1. Cirimotich, C. M., Dong, Y. M., Garver, L. S., Sim, S. Z. & Dimopoulos, G. Mosquito immune defenses against Plasmodium infection. Dev. Comp. Immunol. 34, 387–395 (2010).

    CAS  Article  PubMed  Google Scholar 

  2. Magalhaes, T. et al. Expression of defensin, cecropin, and transferrin in Aedes aegypti (Diptera: Culicidae) infected with Wuchereria bancrofti (Spirurida: Onchocercidae), and the abnormal development of nematodes in the mosquito. Exp. Parasitol. 120, 364–371 (2008).

    CAS  Article  PubMed  Google Scholar 

  3. Steinert, S. & Levashina, E. A. Intracellular immune responses of dipteran insects. Immunol. Rev. 240, 129–140 (2011).

    CAS  Article  PubMed  Google Scholar 

  4. Christophides, G. K., Vlachou, D. & Kafatos, F. C. Comparative and functional genomics of the innate immune system in the malaria vector Anopheles gambiae. Immunol. Rev. 198, 127–148 (2004).

    CAS  Article  PubMed  Google Scholar 

  5. Moreira, L. A. et al. A Wolbachia symbiont in Aedes aegypti limits infection with dengue, chikungunya, and Plasmodium. Cell 139, 1268–1278 (2009).

    Article  PubMed  Google Scholar 

  6. Crampton, J. M. Approaches to vector control: new and trusted prospects for genetic manipulation of insect vectors. Trans. R. Soc. Trop. Med. Hyg. 88, 141–143 (1994).

    CAS  Article  PubMed  Google Scholar 

  7. Speranca, M. A. & Capurro, M. L. Perspectives in the control of infectious diseases by transgenic mosquitoes in the post-genomic era - a review. Mem. Inst. Oswaldo Cruz 102, 425–433 (2007).

    CAS  Article  PubMed  Google Scholar 

  8. Jaramillo-Gutierrez, G. et al. Mosquito immune responses and compatibility between Plasmodium parasites and anopheline mosquitoes. BMC Microbiol. 9, 154 (2009).

    PubMed Central  Article  CAS  PubMed  Google Scholar 

  9. Thomson, R. C. M. The reactions of mosquitoes to temperature and humidity. Bull. Entomol. Res. 29, 125–140 (1938).

    Article  Google Scholar 

  10. Rund, S. S. C., Hou, T. Y., Ward, S. M., Collins, F. H. & Duffield, G. E. Genome-wide profiling of diel and circadian gene expression in the malaria vector Anopheles gambiae. Proc. Natl Acad. Sci. USA 108, E421–E430 (2011).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  11. Okech, B. A., Gouagna, L. C., Yan, G., Githure, J. I. & Beier, J. C. Larval habitats of Anopheles gambiae s. s. (Diptera: Culicidae) influences vector competence to Plasmodium falciparum parasites. Malaria J. 6, 50 (2007).

    Article  Google Scholar 

  12. Okech, B. A. et al. Influence of sugar availability and indoor microclimate on survival of Anopheles gambiae (Diptera: Culicidae) under semifield conditions in western Kenya. J. Med. Entomol. 40, 657–663 (2003).

    Article  PubMed  Google Scholar 

  13. Alto, B. W., Lounibos, L. P., Mores, C. N. & Reiskind, M. H. Larval competition alters susceptibility of adult Aedes mosquitoes to dengue infection. Proc. R. Soc. B 275, 463–471 (2008).

    Article  PubMed  Google Scholar 

  14. Impoinvil, D. E., Cardenas, G. A., Gihture, J. I., Mbogo, C. M. & Beier, J. C. Constant temperature and time period effects on Anopheles gambiae egg hatching. J. Am. Mosq. Control Assoc. 23, 124–130 (2007).

    PubMed Central  Article  PubMed  Google Scholar 

  15. Lyimo, E. O., Takken, W. & Koella, J. C. Effect of rearing temperature and larval density on larval survival, age at pupation, and adult size of Anopheles gambiae. Entomol. Exp. Appl. 63, 265–271 (1992).

    Article  Google Scholar 

  16. Shelton, R. M. Effect of temperatures on development of eight mosquito species. Mosq. News 33, 1–12 (1973).

    Google Scholar 

  17. Zakharova, N. F., Losev, G. I. & Yakubovich, V. Y. The effect of density and temperature on larval populations of the malaria vector Anopheles sacharovi. Med. Parazitol. (Mosk.) 1990, 3–7 (1990) (in Russian).

    Google Scholar 

  18. Lardeux, F. J., Tejerina, R. H., Quispe, V. & Chavez, T. K. A physiological time analysis of the duration of the gonotrophic cycle of Anopheles pseudopunctipennis and its implications for malaria transmission in Bolivia. Malaria J. 7, 141 (2008).

    Article  Google Scholar 

  19. Lambrechts, L. et al. Impact of daily temperature fluctuations on dengue virus transmission by Aedes aegypti. Proc. Natl Acad. Sci. USA 108, 7460–7465 (2011).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  20. Kilpatrick, A. M., Meola, M. A., Moudy, R. M. & Kramer, L. D. Temperature, viral genetics, and the transmission of West Nile virus by Culex pipiens mosquitoes. PLoS Pathog. 4, e1000092 (2008).

    PubMed Central  Article  CAS  PubMed  Google Scholar 

  21. Johansson, M. A., Arana-Vizcarrondo, N., Biggerstaff, B. J. & Staples, J. E. Incubation periods of yellow fever virus. Am. J. Trop. Med. Hyg. 83, 183–188 (2010).

    PubMed Central  Article  PubMed  Google Scholar 

  22. Westbrook, C. J., Reiskind, M. H., Pesko, K. N., Greene, K. E. & Lounibos, L. P. Larval environmental temperature and the susceptibility of Aedes albopictus Skuse (Diptera: Culicidae) to chikungunya virus. Vector Borne Zoonotic Dis. 10, 241–247 (2010).

    PubMed Central  Article  PubMed  Google Scholar 

  23. Devaney, E. & Lewis, E. Temperature-induced refractoriness of Aedes aegypti mosquitoes to infection with the filaria Brugia pahangi. Med. Vet. Entomol. 7, 297–298 (1993).

    CAS  Article  PubMed  Google Scholar 

  24. Lardeux, F. & Cheffort, J. Temperature thresholds and statistical modelling of larval Wuchereria bancrofti (Filariidea: Onchocercidae) developmental rates. Parasitology 114, 123–134 (1997).

    Article  PubMed  Google Scholar 

  25. Okech, B. A. et al. Resistance of early midgut stages of natural Plasmodium falciparum parasites to high temperatures in experimentally infected Anopheles gambiae (Diptera: Culicidae). J. Parasitol. 90, 764–768 (2004).

    Article  PubMed  Google Scholar 

  26. Vanderberg, J. P. & Yoeli, M. Effects of temperature on sporogonic development of Plasmodium berghei. J. Parasitol. 52, 559–564 (1966).

    CAS  Article  PubMed  Google Scholar 

  27. Sato, Y., Matsuoka, H., Araki, M., Ando, K. & Chinzei, Y. Effect of temperature to Plasmodium berghei and P. yoelii on mosquito stage in Anopheles stephensi. Jpn J. Parasitol. 45, 98–104 (1996).

    Google Scholar 

  28. Ball, G. H. & Chao, J. Temperature stresses on mosquito phase of Plasmodium relictum. J. Parasitol. 50, 748–752 (1964).

    CAS  Article  PubMed  Google Scholar 

  29. Chao, J. & Ball, G. H. Effect of temperature on Plasmodium relictum in Culex tarsalis. J. Parasitol. 49, 28 (1962).

    Google Scholar 

  30. LaPointe, D. A., Goff, M. L. & Atkinson, C. T. Thermal constraints to the sporogonic development and altitudinal distribution of avian malaria Plasmodium relictum in Hawai'i. J. Parasitol. 96, 318–324 (2010).

    Article  PubMed  Google Scholar 

  31. Schmid-Hempel, P. Evolutionary ecology of insect immune defenses. Annu. Rev. Entomol. 50, 529–551 (2005).

    CAS  Article  PubMed  Google Scholar 

  32. Dimopoulos, G. Insect immunity and its implication in mosquito–malaria interactions. Cell. Microbiol. 5, 3–14 (2003).

    CAS  Article  PubMed  Google Scholar 

  33. Yassine, H. & Osta, M. A. Anopheles gambiae innate immunity. Cell. Microbiol. 12, 1–9 (2010).

    CAS  Article  PubMed  Google Scholar 

  34. Agaisse, H. & Perrimon, N. The roles of JAK/STAT signaling in Drosophila immune responses. Immunol. Rev. 198, 72–82 (2004).

    CAS  Article  PubMed  Google Scholar 

  35. Garver, L. S., Dong, Y. M. & Dimopoulos, G. Casper controls resistance to Plasmodium falciparum in diverse anopheline species. PLoS Pathog. 5, e1000335 (2009).

    PubMed Central  Article  CAS  PubMed  Google Scholar 

  36. Chown, S. L. & Nicolson, S. W. Insect Physiological Ecology: Mechanisms and Patterns. (Oxford Univ. Press, 2004).

    Book  Google Scholar 

  37. Angilletta, M. J., Huey, R. B. & Frazier, M. R. Thermodynamic effects on organismal performance: is hotter better? Physiol. Biochem. Zool. 83, 197–206 (2010).

    Article  PubMed  Google Scholar 

  38. Catalan, T., Wozniak, A., Niemeyer, H. M., Kalergis, A. M. & Bozinovic, F. Interplay between thermal and immune ecology: effect of environmental temperature on insect immune response and energetic costs after an immune challenge. J. Insect Physiol. 58, 310–317 (2011).

    Article  CAS  PubMed  Google Scholar 

  39. Adamo, S. A. & Lovett, M. M. E. Some like it hot: the effects of climate change on reproduction, immune function and disease resistance in the cricket Gryllus texensis. J. Exp. Biol. 214, 1997–2004 (2011).

    Article  PubMed  Google Scholar 

  40. Linder, J. E., Owers, K. A. & Promislow, D. E. L. The effects of temperature on host–pathogen interactions in D. melanogaster: who benefits? J. Insect Physiol. 54, 297–308 (2008).

    CAS  Article  PubMed  Google Scholar 

  41. Triggs, A. & Knell, R. J. Interactions between environmental variables determine immunity in the Indian meal moth Plodia interpunctella. J. Anim. Ecol. 81, 386–394 (2012).

    Article  PubMed  Google Scholar 

  42. Fischer, K., Koelzow, N., Hoeltje, H. & Karl, I. Assay conditions in laboratory experiments: is the use of constant rather than fluctuating temperatures justified when investigating temperature-induced plasticity? Oecologia 166, 23–33 (2011).

    Article  PubMed  Google Scholar 

  43. Suwanchaichinda, C. & Paskewitz, S. M. Effects of larval nutrition, adult body size, and adult temperature on the ability of Anopheles gambiae (Diptera: Culicidae) to melanize sephadex beads. J. Med. Entomol. 35, 157–161 (1998).

    CAS  Article  PubMed  Google Scholar 

  44. Murdock, C. C. et al. Complex effects of temperature on mosquito immune function. Proc. R. Soc. B 279, 3357–3366 (2012).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  45. Oliveira, G., Lieberman, J. & Barillas-Mury, C. Epithelial nitration by a peroxidase/NOX5 system mediates mosquito antiplasmodial immunity. Science 335, 856–859 (2012).

    CAS  Article  Google Scholar 

  46. Mitchell, S. E., Rogers, E. S., Little, T. J. & Read, A. F. Host-parasite and genotype-by-environment interactions: temperature modifies potential for selection by a sterilizing pathogen. Evolution 59, 70–80 (2005).

    Article  PubMed  Google Scholar 

  47. Stacey, D. A. et al. Genotype and temperature influences pea aphid resistance to a fungal entomopathogen. Physiol. Entomol. 28, 75–81 (2003).

    Article  Google Scholar 

  48. Paaijmans, K. P. et al. Influence of climate on malaria transmission depends on daily temperature variation. Proc. Natl Acad. Sci. USA 107, 15135–15139 (2010).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  49. Fialho, R. F. & Schall, J. J. Thermal ecology of a malarial parasite and its insect vector: consequences for the parasites transmission success. J. Anim. Ecol. 64, 553–562 (1995).

    Article  Google Scholar 

  50. Noden, B. H., Kent, M. D. & Beier, J. C. The impact of variations in temperature on early Plasmodium falciparum development in Anopheles stephensi. Parasitology 111, 539–545 (1995).

    Article  PubMed  Google Scholar 

  51. Afrane, Y. A., Little, T. J., Lawson, B. W., Githeko, A. K. & Yan, G. Y. Deforestation and vectorial capacity of Anopheles gambiae giles mosquitoes in malaria transmission, Kenya. Emerg. Infect. Dis. 14, 1533–1538 (2008).

    PubMed Central  Article  PubMed  Google Scholar 

  52. Reisen, W. K., Fang, Y. & Martinez, V. M. Effects of temperature on the transmission of West Nile virus by Culex tarsalis (Diptera: Culicidae). J. Med. Entomol. 43, 309–317 (2006).

    Article  PubMed  Google Scholar 

  53. Paaijmans, K. P., Blanford, S., Chan, B. H. K. & Thomas, M. B. Warmer temperatures reduce the vectorial capacity of malaria mosquitoes. Biol. Lett. 8, 465–468 (2012).

    Article  PubMed  Google Scholar 

  54. Kutz, S. J. et al. The Arctic as a model for anticipating, preventing, and mitigating climate change impacts on host–parasite interactions. Vet. Parasitol. 163, 217–228 (2009).

    Article  PubMed  Google Scholar 

  55. Mitri, C. et al. Fine pathogen discrimination within the APL1 gene family protects Anopheles gambiae against human and rodent malaria species. PLoS Pathog. 5, e10000576 (2009).

    Article  CAS  Google Scholar 

  56. Dong, Y. M. et al. Anopheles gambiae immune responses to human and rodent Plasmodium parasite species. PLoS Pathog. 2, 513–525 (2006).

    CAS  Article  Google Scholar 

  57. Poudel, S. S., Newman, R. A. & Vaughan, J. A. Rodent Plasmodium: population dynamics of early sporogony within Anopheles stephensi mosquitoes. J. Parasitol. 94, 999–1008 (2008).

    Article  PubMed  Google Scholar 

  58. Vaughan, J. A. Population dynamics of Plasmodium sporogony. Trends Parasitol. 23, 63–70 (2007).

    Article  PubMed  Google Scholar 

  59. Rastogi, M., Pal, N. L. & Sen, A. B. Effect of variation in temperature on development of Plasmodium berghei (NK-65 strain) in Anopheles stephensi. Folia Parasitol. 34, 289–297 (1987).

    CAS  Google Scholar 

  60. Garver, L. S. et al. Anopheles Imd pathway factors and effectors in infection intensity-dependent anti-Plasmodium action. PLoS Pathog. 8, e1002737 (2012).

    CAS  PubMed Central  Article  PubMed  Google Scholar 

  61. Thomas, M. B. et al. Lessons from agriculture for the sustainable management of malaria vectors. PLoS Med. 9, e1001262 (2012).

    PubMed Central  Article  PubMed  Google Scholar 

  62. van den Berg, H., Cham, M. K. & Ichimori, K. Handbook for Integrated Vector Management. (WHO, 2012).

    Google Scholar 

  63. Vinson, E. B. & Kearns, C. W. Temperature and the action of DDT on the American roach. J. Econ. Entomol. 45, 484–496 (1952).

    CAS  Article  Google Scholar 

  64. Blum, M. S. & Kearns, C. W. Temperature and the action of pyrethrum in the American cockroach. J. Econ. Entomol. 49, 862–865 (1956).

    CAS  Article  Google Scholar 

  65. Sparks, T. C., Pavloff, A. M., Rose, R. L. & Clower, D. F. Temperature-toxicity relationships of pyrethroids on Heliothis virescens (F) (Lepidoptera, Noctuidae) and Anthonomus grandis grandis Boheman (Coleoptera, Curculionidae). J. Econ. Entomol. 76, 243–246 (1983).

    CAS  Article  Google Scholar 

  66. Sparks, T. C., Shour, M. H. & Wellemeyer, E. G. Temperature-toxicity relationships of pyrethroids on three lepidopterans. J. Econ. Entomol. 75, 643–646 (1982).

    CAS  Article  Google Scholar 

  67. Cutkomp, L. K. & Subramanyam, B. Toxicity of pyrethroids to Aedes aegypti larvae in relation to temperature. J. Am. Mosq. Control Assoc. 2, 347–349 (1986).

    CAS  PubMed  Google Scholar 

  68. Devries, D. H. & Georghiou, G. P. Influence of temperature on the toxicity of insecticides to susceptible and resistant house flies (Diptera, Muscidae). J. Econ. Entomol. 72, 48–50 (1979).

    CAS  Article  Google Scholar 

  69. Watters, F. L., White, N. D. G. & Cote, D. Effect of temperature on toxicity and persistence of three pyrethroid insecticides applied to fir plywood for the control of the red flour beetle (Coleoptera, Tenebrionidae). J. Econ. Entomol. 76, 11–16 (1983).

    CAS  Article  Google Scholar 

  70. Hodjati, M. H. & Curtis, C. F. Effects of permethrin at different temperatures on pyrethroid-resistant and susceptible strains of Anopheles. Med. Vet. Entomol. 13, 415–422 (1999).

    CAS  Article  PubMed  Google Scholar 

  71. Harwood, A. D., You, J. & Lydy, M. J. Temperature as a toxicity identification evaluation tool for pyrethroid insecticides: toxicokinetic confirmation. Environ. Toxicol. Chem. 28, 1051–1058 (2009).

    CAS  Article  PubMed  Google Scholar 

  72. Miller, T. A. & Adams, M. E. in Insecticide Mode of Action (ed. Coats, J. R.) 3–27 (Academic, 1982).

    Book  Google Scholar 

  73. Kokoza, V. et al. Blocking of Plasmodium transmission by cooperative action of Cecropin A and Defensin A in transgenic Aedes aegypti mosquitoes. Proc. Natl Acad. Sci. USA 107, 8111–8116 (2010).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  74. Dong, Y. et al. Engineered Anopheles immunity to Plasmodium infection. PLoS Pathog. 7, 1–12 (2011).

    Google Scholar 

  75. Li, C. Y., Marrelli, M. T., Yan, G. Y. & Jacobs-Lorena, M. Fitness of transgenic Anopheles stephensi mosquitoes expressing the SM1 peptide under the control of a vitellogenin promoter. J. Hered. 99, 275–282 (2008).

    CAS  Article  PubMed  Google Scholar 

  76. Yoshida, S. et al. Hemolytic C-type lectin CEL-III from sea cucumber expressed in transgenic mosquitoes impairs malaria parasite development. PLoS Pathog. 3, 1962–1970 (2007).

    CAS  Article  Google Scholar 

  77. Isaacs, A. T. et al. Engineered resistance to Plasmodium falciparum development in transgenic Anopheles stephensi. PLoS Pathog. 7, e1002017 (2011).

    CAS  PubMed Central  Article  PubMed  Google Scholar 

  78. Ferguson, H. M. & Read, A. F. Why is the effect of malaria parasites on mosquito survival still unresolved? Trends Parasitol. 18, 256–261 (2002).

    Article  PubMed  Google Scholar 

  79. Libert, S., Chao, Y., Chu, X. & Pletcher, S. D. Trade-offs between longevity and pathogen resistance in Drosophila melanogaster are mediated by NFκB. signaling. Aging Cell 5, 533–543 (2006).

    CAS  Article  PubMed  Google Scholar 

  80. Rodrigues, J., Brayner, F. A., Alves, L. C., Dixit, R. & Barillas-Mury, C. Hemocyte differentiation mediates innate immune memory in Anopheles gambiae mosquitoes. Science 329, 1353–1355 (2010).

    CAS  PubMed Central  Article  PubMed  Google Scholar 

  81. Roth, O. et al. Transgenerational immune priming as cryptic parental care. J. Anim. Ecol. 79, 722–722 (2010).

    Article  Google Scholar 

  82. Hurst, G. D. D., Jiggins, F. M. & Robinson, S. J. W. What causes inefficient transmission of male-killing Wolbachia in Drosophila? Heredity 87, 220–226 (2001).

    CAS  Article  PubMed  Google Scholar 

  83. Guruprasad, N. M., Mouton, L. & Puttaraju, H. P. Effect of Wolbachia infection and temperature variations on the fecundity of the Uzifly Exorista sorbillans (Diptera: Tachinidae). Symbiosis 54, 151–158 (2011).

    Article  Google Scholar 

  84. Mouton, L., Henri, H., Charif, D., Bouletrea, M. & Vavre, F. Interaction between host genotype and environmental conditions affects bacterial density in Wolbachia symbiosis. Biol. Lett. 3, 210–213 (2007).

    CAS  PubMed Central  Article  PubMed  Google Scholar 

  85. Wiwatanaratanabutr, I. & Kittayapong, P. Effects of crowding and temperature on Wolbachia infection density among life cycle stages of Aedes albopictus. J. Invertebr. Pathol. 102, 220–224 (2009).

    Article  PubMed  Google Scholar 

  86. Mouton, L., Henri, H., Bouletreau, M. & Vavre, F. Effect of temperature on Wolbachia density and impact on cytoplasmic incompatibility. Parasitology 132, 49–56 (2006).

    CAS  Article  PubMed  Google Scholar 

  87. Clancy, D. J. & Hoffmann, A. A. Environmental effects on cytoplasmic incompatibility and bacterial load in Wolbachia-infected Drosophila simulans. Entomol. Exp. Appl. 86, 13–24 (1998).

    Article  Google Scholar 

  88. Reynolds, K. T., Thomson, L. J. & Hoffmann, A. A. The effects of host age, host nuclear background and temperature on phenotypic effects of the virulent Wolbachia strain popcorn in Drosophila melanogaster. Genetics 164, 1027–1034 (2003).

    PubMed Central  PubMed  Google Scholar 

  89. Gething, P. et al. Modelling the global constraints of temperature on transmission of Plasmodium falciparum and P. vivax. Parasit. Vectors 4, 92 (2011).

    PubMed Central  Article  PubMed  Google Scholar 

  90. Smith, D. L., Smith, T. A. & Hay, S. I. in Shrinking the Malaria Map: a Prospectus on Malaria Elimination (eds Feachem, R. G. A., Phillips, A. A. & Targett, G. A.) 108–126 (The Global Health Group, 2009).

    Google Scholar 

  91. Klass, J. I., Blanford, S. & Thomas, M. B. Use of a geographic information system to explore spatial variation in pathogen virulence and the implications for biological control of locusts and grasshoppers. Agric. Forest Entomol. 9, 201–208 (2007).

    Article  Google Scholar 

  92. Klass, J. I., Blanford, S. & Thomas, M. B. Development of a model for evaluating the effects of environmental temperature and thermal behaviour on biological control of locusts and grasshoppers using pathogens. Agric. Forest Entomol. 9, 189–199 (2007).

    Article  Google Scholar 

  93. Ratte, H. T. in Environmental Physiology and Biochemistry of Insects (ed. Hoffmann, K. H.) 31–66 (Springer, 1985).

    Google Scholar 

  94. Cloudsley-Thompson, J. L. The significance of fluctuating temperatures on the physiology and ecology of insects. Entomologist 86, 183–189 (1953).

    Google Scholar 

  95. Eubank, W. P., Atmar, J. W. & Ellington, J. J. The significance and thermodynamics of fluctuating versus static thermal environments on Heliothis zea egg development rates. Environ. Entomol. 2, 491–496 (1973).

    Article  Google Scholar 

  96. Humpesch, U. H. Effect of fluctuating temperature on the duration of embryonic development in two Ecdyonurus spp. and Rhithrogena cf hybrida (Ephemeroptera) from Austrian streams. Oecologia 55, 285–288 (1982).

    Article  PubMed  Google Scholar 

  97. Lazzaro, B. P., Flores, H. A., Lorigan, J. G. & Yourth, C. P. Genotype-by-environment interactions and adaptation to local temperature affect immunity and fecundity in Drosophila melanogaster. PLoS Pathog. 4, e1000025 (2008).

    PubMed Central  Article  CAS  PubMed  Google Scholar 

  98. Raffel, T. R. et al. Disease and thermal acclimation in a more variable and unpredictable climate. Nature Clim. Change 12 Aug 2012 (doi:10.1038/nclimate1659).

    Article  Google Scholar 

  99. Ouedraogo, R. M., Cusson, M., Goettel, M. S. & Brodeur, J. Inhibition of fungal growth in thermoregulating locusts, Locusta migratoria, infected by the fungus Metarhizium anisopliae var acridum. J. Invertebr. Pathol. 82, 103–109 (2003).

    Article  PubMed  Google Scholar 

  100. Parham, P. et al. Modeling the role of environmental variables on the population dynamics of the malaria vector Anopheles gambiae sensu stricto. Malaria J. 11, 271 (2012).

    Article  Google Scholar 

  101. Afrane, Y. A., Little, T. J., Lawson, B. W., Githeko, A. K. & Yan, G. Deforestation and vectorial capacity of Anopheles gambiae giles mosquitoes in malaria transmission, Kenya. Emerg. Infect. Dis. 14, 1533–1538 (2008).

    PubMed Central  Article  PubMed  Google Scholar 

  102. Paaijmans, K. P. & Thomas, M. B. The influence of mosquito resting behaviour and associated microclimate for malaria risk. Malaria J. 10, 183 (2011).

    Article  Google Scholar 

  103. Peterson, T. M. L., Gow, A. J. & Luckhart, S. Nitric oxide metabolites induced in Anopheles stephensi control malaria parasite infection. Free Rad. Biol. Med. 42, 132–142 (2007).

    CAS  Article  PubMed  Google Scholar 

  104. Luckhart, S., Vodovotz, Y., Cui, L. W. & Rosenberg, R. The mosquito Anopheles stephensi limits malaria parasite development with inducible synthesis of nitric oxide. Proc. Natl Acad. Sci. USA 95, 5700–5705 (1998).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  105. Kumar, S. & Barillas-Mury, C. Ookinete-induced midgut peroxidases detonate the time bomb in anopheline mosquitoes. Insect Biochem. Mol. Biol. 35, 721–727 (2005).

    CAS  Article  PubMed  Google Scholar 

  106. Collins, F. H. et al. Genetic selection of a Plasmodium-refractory strain of the malaria vector Anopheles gambiae. Science 234, 607–610 (1986).

    CAS  Article  PubMed  Google Scholar 

  107. Gorman, M. J., Cornel, A. J., Collins, F. H. & Paskewitz, S. M. A shared genetic mechanism for melanotic encapsulation of CM-Sephadex beads and a malaria parasite, Plasmodium cynomolgi B, in the mosquito, Anopheles gambiae. Exp. Parasitol. 84, 380–386 (1996).

    CAS  Article  PubMed  Google Scholar 

  108. Hillyer, J. F. & Estevez-Lao, T. Y. Nitric oxide is an essential component of the hemocyte-mediated mosquito immune response against bacteria. Dev. Comp. Immunol. 34, 141–149 (2010).

    CAS  Article  PubMed  Google Scholar 

  109. Hillyer, J. F., Barreau, C. & Vernick, K. D. Efficiency of salivary gland invasion by malaria sporozoites is controlled by rapid sporozoite destruction in the mosquito haemocoel. Int. J. Parasitol. 37, 673–681 (2007).

    Article  PubMed  Google Scholar 

  110. Dimopoulos, G., Richman, A., Muller, H. M. & Kafatos, F. C. Molecular immune responses of the mosquito Anopheles gambiae to bacteria and malaria parasites. Proc. Natl Acad. Sci. USA 94, 11508–11513 (1997).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

The authors thank members of the Thomas, Read and Julian F. Hillyer laboratory groups for discussion, and D. Kroczynski and J. Teeple for insectary support. The content of this article is solely the responsibility of the authors and does not necessarily represent the official views of the US National Institute of General Medical Sciences, the US National Institute of Allergy and Infectious Diseases or the US National Institutes of Health (NIH). Work in the authors' laboratories is funded, in part, by a grant from the US Pennsylvania Department of Health using Tobacco Settlement Funds. The Pennsylvania Department of Health specifically disclaims responsibility for any analyses, interpretations or conclusions. Work in the authors' laboratories was also funded by the following: the US National Science Foundation (NSF)–NIH Ecology of Infectious Diseases programme (grant EF-0914384) and the NIH R21 programme (grant AI096036-01).

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Correspondence to Courtney C. Murdock or Matthew B. Thomas.

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Ambient temperature shapes a suite of phenotypes in a diversity of parasite taxa (PDF 307 kb)

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Murdock, C., Paaijmans, K., Cox-Foster, D. et al. Rethinking vector immunology: the role of environmental temperature in shaping resistance. Nat Rev Microbiol 10, 869–876 (2012). https://doi.org/10.1038/nrmicro2900

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