Mechanisms and methods in ecoimmunology: Integrating within-organism and between-organism processes

Integrative and Comparative Biology

Volumn 54, Issue 3, 2014, Pages 340-352

  Downs, C J ^a   Adelman, J S ^b   Demas, G E ^c  

^a UNIVERSITY OF NEVADA   (United States)

^b VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

^c INDIANA UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL; COMMUNICABLE DISEASE; ECOSYSTEM; ENVIRONMENTAL HEALTH; EVOLUTION; GENETICS; IMMUNOLOGY; INTERDISCIPLINARY EDUCATION; PROCEDURES;

ANIMALS; BIOLOGICAL EVOLUTION; COMMUNICABLE DISEASES; ECOSYSTEM; ENVIRONMENTAL HEALTH; INTERDISCIPLINARY STUDIES;

EID: 84906331392     PISSN: 15407063     EISSN: 15577023     Source Type: Journal    
DOI: 10.1093/icb/icu082     Document Type: Conference Paper

References (124)

1. Adamo SA. 2004. How should behavioural ecologists interpret measurements of immunity? Anim Behav 68:1443-9.
2. Adamo SA. 2014. The effects of stress hormones on immune function may be vital for the adaptive reconfiguration of the immune system during fight-or-flight behavior. Integr Comp Biol 54:419-26.
3. Adelman JS. Forthcoming 2015. Immune systems: linking organisms, populations, and evolution through disease. In: Martin LB, Ghalambor CK, Woods HA, editors. Integrative organismal biology. Hoboken (NJ): Wiley.
4. Adelman JS, Cordoba-Cordoba S, Spoelstra K, Wikelski M, Hau M. 2010. Radiotelemetry reveals variation in fever and sickness behaviours with latitude in a free-living passerine. Funct Ecol 24:813-23.
5. Adelman JS, Kirkpatrick L, Grodio JL, Hawley DM. 2013. House finch populations differ in early inflammatory signaling and pathogen tolerance at the peak of Mycoplasma gallisepticum infection. Am Nat 181:674-89.
6. Adelman JS, Moyers SC, Hawley DM. 2014. Using remote biomonitoring to understand heterogeneity in immuneresponses and disease-dynamics in small, free-living animals. Integr Comp Biol 54:377-86.
7. Ahmed SA, Penhale WJ, Talal N. 1985. Sex hormones, immune responses, and autoimmune diseases: mechanisms of sex hormone action. Am J Pathol 121:531-51.
8. Alizon S, van Baalen M. 2008. Acute or chronic? within-host models with immune dynamics, infection outcome, and parasite evolution. Am Nat 172:E244-56.
9. Anderson RM, May RM. 1979. Population biology of infectious diseases: Part I. Nature 280:361-7.
10. Ardia DR, Parmentier HK, Vogel LA. 2011. The role of constraints and limitation in driving individual variation in immune response. Funct Ecol 25:61-73.
11. Ardia DR, Schat KA, Winkler DW. 2003. Reproductive effort reduces long-term immune function in breeding tree swallows (Tachycineta bicolor). Proc R Soc Lond Ser B Biol Sci 270:1679-83.
12. Ashley NT, Weil ZM, Nelson RJ. 2012. Inflammation: mechanisms, costs, and natural variation. Annu Rev Ecol Evol Syst 43:385-406.
13. Bashir-Tanoli S, Tinsley MC. 2014. Immune response costs are associated with changes in resource acquisition and not resource reallocation. Funct Ecol 28:1011-9.
14. Baze MM, Schlauch K, Hayes JP. 2010. Gene expression of the liver in response to chronic hypoxia. Physiol Genomics 41:275-88.
15. Besedovsky HO, del Rey A. 1996. Immune-neuro-endocrine interactions: facts and hypotheses. Endocr Rev 17:64-102.
16. Best A, White A, Boots M. 2009. The implications of coevolutionary dynamics to host-parasite interactions. Am Nat 173:779-91.
17. Bonneaud C, Balenger SL, Russell AF, Zhang JW, Hill GE, Edwards SV. 2011. Rapid evolution of disease resistance is accompanied by functional changes in gene expression in a wild bird. Proc Natl Acad Sci USA 108:7866-71.
18. Bonneaud C, Mazuc J, Gonzalez G, Haussy C, Chastel O, Faivre B, Sorci G. 2003. Assessing the cost of mounting an immune response. Am Nat 161:367-79.
19. Bonter DN, Bridge ES. 2011. Applications of radio frequency identification (RFID) in ornithological research: a review. J Field Ornithol 82:1-10.
20. Boots M, Best A, Miller MR, White A. 2009. The role of ecological feedbacks in the evolution of host defence: what does theory tell us? Philos Trans R Soc B Biol Sci 364:27-36.
21. Boughton RK, Joop G, Armitage SAO. 2011. Outdoor immunology: methodological considerations for ecologists. Funct Ecol 25:81-100.
22. Bracken CP, Whitelaw ML, Peet DJ. 2003. The hypoxiainducible factors: key transcriptional regulators of hypoxic responses. Cell Mol Life Sci 60:1376-93.
23. Bridge ES, Bonter DN. 2011. A low-cost radio frequency identification device for ornithological research. J Field Ornithol 82:52-9.
24. Brown EA, Pilkington JG, Nussey DH, Watt KA, Hayward AD, Tucker R, Graham AL, Paterson S, Beraldi D, Pemberton JM, et al. 2013. Detecting genes for variation in parasite burden and immunological traits in a wild population: testing the candidate gene approach. Mol Ecol 22:757-73.
25. Buchanan KL. 2000. Stress and the evolution of conditiondependent signals. Trends Ecol Evol 15:156-60.
26. Buehler DM, Piersma T, Matson K, Tieleman BI. 2008. Seasonal redistribution of immune function in a migrant shorebird: annual-cycle effects override adjustments to thermal regime. Am Nat 172:783-96.
27. Buehler DM, Versteegh MA, Matson KD, Tieleman BI. 2011. One problem, many solutions: simple statistical approaches help unravel the complexity of the immune system in an ecological context. PLoS One 6:e18592.
28. Caldwell RM, Schafer JF, Compton LE, Patterson FL. 1958. Tolerance to cereal leaf rusts. Science 128:714-5.
29. Cohen AA, Martin LB, Wingfield JC, McWilliams SR, Dunne JA. 2012. Physiological regulatory networks: ecological roles and evolutionary constraints. Trends Ecol Evol 27:428-35.
30. Cummins EP, Oliver KM, Lenihan CR, Fitzpatrick SF, Bruning U, Scholz CC, Slattery C, Leonard MO, McLoughlin P, Taylor CT. 2010. NF-kappa B links CO2 sensing to innate immunity and inflammation in mammalian cells. J Immunol 185:4439-45.
31. Daszak P, Cunningham AA, Hyatt AD. 2000. Emerging infectious diseases of wildlife-threats to biodiversity and human health. Science 287:443-9.
32. Day T, Alizon S, Mideo N. 2011. Bridging scales in the evolution of infectious disease life histories: theory. Evolution 65:3448-61.
33. De Jong G, Van Noordwijk AJ. 1992. Acquisition and allocation of resources: genetic (co)variances, selection, and life histories. Am Nat 139:749-70.
34. Demas GE, Adamo SA, French SS. 2011a. Neuroendocrineimmune crosstalk in vertebrates and invertebrates: implications for host defence. Funct Ecol 25:29-39.
35. Demas GE, Greives TJ, Chester EM, French SS. 2012. The energetics of immunity:mechanisms mediating trade-offs in eco-immunology. In: Demas GE, Nelson RJ, editors. Ecoimmunology. New York (NY): Oxford University Press. p. 257-96.
36. Demas GE, Nelson RJ, editors. 2012a. Ecoimmunology. New York (NY): Oxford University Press.
37. Demas GE, Nelson RJ. 2012b. Introduction to ecoimmunology. In: Demas GE, Nelson RJ, editors. Ecoimmunology. New York (NY): Oxford University Press. p. 3-6.
38. Demas GE, Zysling DA, Beechler BR, Muehlenbein MP, French SS. 2011b. Beyond phytohaemagglutinin: assessing vertebrate immune function across ecological contexts. J Anim Ecol 80:710-30.
39. Downs CJ, Brown JL, Wone B, Donovan ER, Hunter K, Hayes JP. 2013. Selection for increased mass-independent maximal metabolic rate suppresses innate but not adaptive immune function. Proc R Soc B Biol Sci 280:20122636.
40. Downs CJ, Dochtermann NA. 2014. Testing hypotheses in ecoimmunology using mixed models: disentangling hierarchical correlations. Integr Comp Biol 54:407-18.
41. Downs CJ, Schutz H, Meek TH, Dlugosz EM, Acosta W, de Wolski KS, Malisch JL, Hayes JP, Garland T. 2012. Within-lifetime trade-offs but evoutionary freedom for hormonal and immunological traits: evidence from mice bred for high voluntary exercise. J Exp Biol 215: 1651-61.
42. Fassbinder-Orth CA. 2014. Methods for quantifying gene expression in ecoimmunology: from qPCR to RNA-Seq. Integr Comp Biol 54:396-406.
43. Flatt T, Heyland A, Stearns SC. 2011. What mechanistic insighs can or cannot contribute to life history evolution: an exchange between Stearns, Heyland, and Flatt. In: Flatt T, Heyland A, editors. Mechanisms of life history evolution: the genetics and physiology of life history traits and trade-offs. New York (NY): Oxford University Press. p. 375-9.
44. French SS, Dearing MD, Demas GE. 2011. Leptin as a physiological mediator of energetic trade-offs in ecoimmunology: implications for disease. Integr Comp Biol 51:505-13.
45. French SS, DeNardo DF, Moore MC. 2007a. Trade-offs between the reproductive and immune systems: facultative responses to resources or obligate responses to reproduction? Am Nat 170:79-89.
46. French SS, Johnston GIH, Moore MC. 2007b. Immune activity suppresses reproduction in food-limited female tree lizards Urosaurus ornatus. Funct Ecol 21:1115-22.
47. French SS, Moore MC, Demas GE. 2009. Ecological immunology: the organism in context. Integr Comp Biol 49:246-53.
48. Garnier R, Graham AL. 2014. Insights from parasite-specific serological tools in eco-immunology. Integr Comp Biol 54:363-76.
49. Girard I, Garland T. 2002. Plasma corticosterone response to acute and chronic voluntary exercise in female house mice. J Appl Physiol 92:1553-61.
50. Graham AL. 2013. Optimal immunity meets natural variation: the evolutionary biology of host defence. Parasite Immunol 35:315-7.
51. Graham AL, Hayward AD, Watt KA, Pilkington JG, Pemberton JM, Nussey DH. 2010. Fitness correlates of heritable variation in antibody responsiveness in a wild mammal. Science 330:662-5.
52. Graham AL, Shuker DM, Pollitt LC, Auld S, Wilson AJ, Little TJ. 2011. Fitness consequences of immune responses: strengthening the empirical framework for ecoimmunology. Funct Ecol 25:5-17.
53. Gross WG, Siegel PB, Hall RW, Domermuth CH, Duboise RT. 1980. Production and persistence of antibodies in chickens to sheep erythrocytes 2. Resistance to infectious-diseases. Poult Sci 59:205-10.
54. Gustafsson L, Nordling D, Andersson MS, Sheldon BC, Qvarnstrom A. 1994. Infectious diseases, reproductive effort and the cost of reproduction in birds. Phil Trans R Soc Lond Ser B Biol Sci 346:323-31.
55. Hasselquist D, Nilsson JA. 2012. Physiological mechanisms mediating costs of immune responses: what can we learn from studies of birds? Anim Behav 83:1303-12.
56. Hawley DM, Altizer SM. 2011. Disease ecology meets ecological immunology: understanding the links between organismal immunity and infection dynamics in natural populations. Funct Ecol 25:48-60.
57. Hayden MS, Ghosh S. 2008. Shared principles in NF- signaling. Cell 132:344-62.
58. Hõrak P, Tegelmann L, Ots I, Moller AP. 1999. Immune function and survival of great tit nestlings in relation to growth conditions. Oecologia 121:316-22.
59. Horrocks NPC, Hegemann A, Matson KD, Hine K, Jaquier S, Shobrak M, Williams JB, Tinbergen JM, Tieleman BI. 2012. Immune indexes of larks from desert and temperate regions show weak associations with life history but stronger links to environmental variation in microbial abundance. Physiol Biochem Zool 85:504-15.
60. Hotchkiss AK, Nelson RJ. 2002. Melatonin and immune function: hype or hypothesis? Crit Rev Immunol 22:351-71.
61. Iseri VJ, Klasing KC. 2013. Dynamics of the systemic components of the chicken (Gallus gallus domesticus) immune system following activation by Escherichia coli; implications for the costs of immunity. Dev Comp Immunol 40:248-57.
62. Jones KE, Patel NG, Levy MA, Storeygard A, Balk D, Gittleman JL, Daszak P. 2008. Global trends in emerging infectious diseases. Nature 451:990-4.
63. Keesing F, Belden LK, Daszak P, Dobson A, Harvell CD, Holt RD, Hudson P, Jolles A, Jones KE, Mitchell CE, et al. 2010. Impacts of biodiversity on the emergence and transmission of infectious diseases. Nature 468:647-52.
64. Keil D, Luebke RW, Pruett SB. 2001. Quantifying the relationship between multiple immunological parameters and host resistance: probing the limits of reductionism. J Immunol 167:4543-52.
65. Klasing KC, Leshchinsky TV. 1999. Functions, costs, and benefits of the immune system during development and growth. Johannesburg: BirdLife South Africa.
66. Klein EY, Graham AL, Llinas M, Levin S. 2014. Cross-reactive immune responses as primary drivers of malaria chronicity. Infect Immun 82:140-51.
67. Kurtenbach K, De Michelis S, Etti S, Schafer SM, Sewell HS, Brade V, Kraiczy P. 2002. Host association of Borrelia burgdorferi sensu lato-the key role of host complement. Trends Microbiol 10:74-9.
68. Lee KA. 2006. Linking immune defenses and life history at the levels of the individual and the species. Integr Comp Biol 46:1000-15.
69. Lee KA, Wikelski M, Robinson WD, Robinson TR, Klasing KC. 2008. Constitutive immune defences correlate with life-history variables in tropical birds. J Anim Ecol 77:356-63.
70. Lloyd-Smith JO, Schreiber SJ, Kopp PE, Getz WM. 2005. Superspreading and the effect of individual variation on disease emergence. Nature 438:355-9.
71. Lochmiller RL, Deerenberg C. 2000. Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos 88:87-98.
72. Long GH, Chan BHK, Allen JE, Read AF, Graham AL. 2008. Blockade of TNF receptor 1 reduces disease severity but increases parasite transmission during Plasmodium chabaudi chabaudi infection. Int J Parasitol 38:1073-81.
73. Longo AV, Burrowes PA, Zamudio KR. 2014. Genomic studies of disease-outcome in host-pathogen dynamics. Integr Comp Biol 54:427-38.
74. Love OP, Salvante KG, Dale J, Williams TD. 2008. Sexspecific variability in the immune system across life-history stages. Am Nat 172:E99-112.
75. Luciani F, Alizon S. 2009. The evolutionary dynamics of a rapidly mutating virus within and between hosts: the case of hepatitis C virus. PLoS Comput Biol 5:e1000565.
76. Majmundar AJ, Wong WJ, Simon MC. 2010. Hypoxia-inducible factors and the response to hypoxic stress. Mol Cell 40:294-309.
77. Malisch J, Breuner C, Gomes F, Chappell M, Garland T. 2008. Circadian pattern of total and free corticosterone concentrations, corticosteroid-binding globulin, and physical activity in mice selectively bred for high voluntary wheel-running behavior. Gen Comp Endocrinol 156:210-7.
78. Malisch JL, Saltzman W, Gomes FR, Rezende EL, Jeske DR, Garland T. 2007. Baseline and stress-induced plasma corticosterone concentrations of mice selectively bred for high voluntary wheel running. Physiol Biochem Zool 80:146-56.
79. Martin LB, Hawley DM, Ardia DR. 2011a. An introduction to ecological immunology. Funct Ecol 25:1-4.
80. Martin LB, Hopkins WA, Mydlarz LD, Rohr JR. 2010. The effects of anthropogenic global changes on immune functions and disease resistance. Ann N Y Acad Sci 1195:129-48.
81. Martin LB, Liebl AL, Trotter JH, Richards CL, McCoy K, McCoy MW. 2011b. Integrator networks: illuminating the black box linking genotype and phenotype. Integr Comp Biol 51:514-27.
82. Martin LB, Weil ZM, Nelson RJ. 2006. Refining approaches and diversifying directions in ecoimmunology. Integr Comp Biol 46:1030-9.
83. Martin LB, Weil ZM, Nelson RJ. 2007. Immune defense and reproductive pace of life in Peromyscus mice. Ecology 88:2516-28.
84. Martin LB, Weil ZM, Nelson RJ. 2008. Seasonal changes in vertebrate immune activity: mediation by physiological trade-offs. Phil Trans R Soc B Biol Sci 363:321-39.
85. Matson KD, Cohen AA, Klasing KC, Ricklefs RE, Scheuerlein A. 2006. No simple answers for ecological immunology: relationships among immune indices at the individual level break down at the species level in waterfowl. Proc R Soc B Biol Sci 273:815-22.
86. Mideo N, Alizon S, Day T. 2008. Linking within- and between- host dynamics in the evolutionary epidemiology of infectious diseases. Trends Ecol Evol 23:511-7.
87. Moreno J, Merino S, Sanz JJ, Arriero E, Morales J, Tomas G. 2005. Nestling cell-mediated immune response, body mass and hatching date as predictors of local recruitment in the pied flycatcher Ficedula hypoleuca. J Avian Biol 36:251-60.
88. Moreno J, Sanz JJ, Merino S, Arriero E. 2001. Daily energy expenditure and cell-mediated immunity in pied flycatchers while feeding nestlings: interaction with moult. Oecologia 129:492-7.
89. Nordling D, Andersson M, Zohari S, Gustafsson L. 1998. Reproductive effort reduces specific immune response and parasite resistance. Proc R Soc B Biol Sci 265:1291-8.
90. Norris K, Evans MR. 2000. Ecological immunology: life history trade-offs and immune defense in birds. Behav Ecol 11:19-26.
91. Nussey DH, Watt KA, Clark A, Pilkington JG, Pemberton JM, Graham AL, McNeilly TN. 2014. Multivariate immune defences and fitness in the wild: complex but ecologically important associations among plasma antibodies, health and survival. Proc R Soc B Biol Sci 281:20132931.
92. Parmentier HK, Lammers A, Hoekman JJ, Reilingh GD, Zaanen ITA, Savelkoul HFJ. 2004. Different levels of natural antibodies in chickens divergently selected for specific antibody responses. Dev Comp Immunol 28:39-49.
93. Pedersen AB, Babayan SA. 2011. Wild immunology. Mol Ecol 20:872-80.
94. Previtali MA, Ostfeld RS, Keesing F, Jolles AE, Hanselmann R, Martin LB. 2012. Relationship between pace of life and immune responses in wild rodents. Oikos 121:1483-92.
95. Prokop JW, Schmidt C, Gasper D, Duff RJ, Milsted A, Ohkubo T, Ball HC, Shawkey MD, Mays HL Jr, Cogburn LA. 2014. Discovery of the elusive leptin in birds: identification of several 'missing links' in the evolution of leptin and its receptor. PLoS One 9:e92751.
96. Råberg L, Graham AL, Read AF. 2009. Decomposing health: tolerance and resistance to parasites in animals. Phil Trans R Soc B Biol Sci. 364, 37-49.
97. Reznick D, Bryant MJ, Bashey F. 2002. r- and K-selection revisited: the role of population regulation in life-history evolution. Ecology 83:1509-20.
98. Ricklefs RE, Wikelski M. 2002. The physiology/life-history nexus. Trends Ecol Evol 17:462-8.
99. Rigaud T, Perrot-Minnot MJ, Brown MJF. 2010. Parasite and host assemblages: embracing the reality will improve our knowledge of parasite transmission and virulence. Proc R Soc B Biol Sci 277:3693-702.
100. Robinson DP, Klein SL. 2012. Sex differences in immune responses to viruses. In: Demas GE, Nelson RJ, editors. Ecoimmunology. New York (NY): Oxford University Press. p. 497-529.
101. Roy BA, Kirchner JW. 2000. Evolutionary dynamics of pathogen resistance and tolerance. Evolution 54:51-63.
102. Sadd BM, Schmid-Hempel P. 2009. PERSPECTIVE: principles of ecological immunology. Evol Appl 2:113-21.
103. Sandmeier FC, Tracy RC. 2014. The metabolic pace-of-life model: incorporating ectothermic organisms into the theory of vertebrate ecoimmunology. Integr Comp Biol 54:387-95.
104. Sanz JJ, Moreno J, Merino S, Tomas G. 2004. A trade-off between two resource-demanding functions: post-nuptial moult and immunity during reproduction in male pied flycatchers. J Anim Ecol 73:441-7.
105. Sapolsky RM, Romero LM, Munck AU. 2000. How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr Rev 21:55-89.
106. Schmid-Hempel P. 2003. Variation in immune defence as a question of evolutionary ecology. Proc R Soc Lond Ser B Biol Sci 270:357-66.
107. Schulenburg H, Kurtz J, Moret Y, Siva-Jothy MT. 2009. Ecological immunology. Phil Trans R Soc B Biol Sci 364:3-14.
108. Schuurs A, Verheul HAM. 1990. Effects of gender and sex steroids on the immune response. J Steroid Biochem Mol Biol 35:157-72.
109. Sears BF, Rohr JR, Allen JE, Martin LB. 2011. The economy of inflammation: when is less more? Trends Parasitol 27:382-7.
110. Sheldon BC, Verhulst S. 1996. Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol Evol 11:317-21.
111. Sibly RM, Calow P. 1986. Physiological ecology of animals: an evolutionary approach. Oxford: Blackwell Scientific Publications.
112. Siegel PB, Gross WB. 1980. Production and persistence of antibodies in chickens to sheep erythrocytes 1. Directional selection. Poult Sci 59:1-5.
113. Siegel PB, Gross WB, Cherry JA. 1982. Correlated responses of chickens to selection for production of antibodies to sheep erythrocytes. Anim Blood Groups Biochem Genet 13:291-7.
114. Simms EL. 2000. Defining tolerance as a norm of reaction. Evol Ecol 14:563-70.
115. Stearns SC. 1992. The evolution of life histories. New York (NY): Oxford University Press.
116. Stearns SC. 2011. Does impressive progress on understanding mechanisms advance life history theory? In: Flatt T, Heyland A, editors. Mechanisms of life history evolution: the genetics and physiology of life history traits and tradeoffs. New York (NY): Oxford University Press. p. 365-74.
117. Sun Y, Parmentier HK, Frankena K, van der Poel JJ. 2011. Natural antibody isotypes as predictors of survival in laying hens. Poult Sci 90:2263-74.
118. Swallow JG, Hayes JP, Koteja P, Garland T Jr. 2009. Selection experiments and experimental evolution of performance and physiology. In: Garland T Jr, Rose MR, editors. Experimental evolution: concepts, methods, and applications of selection experiments. Berkeley (CA): University of California Press. p. 752.
119. Van Noordwijk AJ, De Jong G. 1986. Acquisition and allocation of resources - their influence on variation in life-history tactics. Am Nat 128:137-42.
120. Viney ME, Riley EM, Buchanan KL. 2005. Optimal immune responses: immunocompetence revisited. Trends Ecol Evol 20:665-9.
121. Williams GC. 1966. Natural selection, the costs of reproduction, and a refinement of Lack's principle. Am Nat 100:687-90.
122. Woolhouse MEJ, Dye C, Etard JF, Smith T, Charlwood JD, Garnett GP, Hagan P, Hii JLK, Ndhlovu PD, Quinnell RJ, et al. 1997. Heterogeneities in the transmission of infectious agents: implications for the design of control programs. Proc Natl Acad Sci USA 94:338-42.
123. Zera AJ, Harshman LG. 2001. The physiology of life history trade-offs in animals. Annu Rev Ecol Syst 32:95-126.
124. Zimmerman LM, Bowden RM, Vogel LA. 2014. A vertebrate cytokine primer for eco-immunologists. Funct Ecol published online (doi:10.1111/1365-2435.12273).