Trade-offs between acquired and innate immune defenses in humans

Evolution, Medicine and Public Health

Volumn 2016, Issue 1, 2016, Pages 1-16

  McDade, Thomas W ^a,b   Georgiev, Alexander V ^a   Kuzawa, Christopher W ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b CANADIAN INSTITUTE FOR ADVANCED RESEARCH   (Canada)

Author keywords

Developmental origins of health and disease; Ecological immunology; Immune function; Inflammation

Indexed keywords

ADAPTIVE IMMUNITY; CLINICAL EFFECTIVENESS; COST EFFECTIVENESS ANALYSIS; ECOLOGICAL IMMUNOLOGY; ENVIRONMENTAL EXPOSURE; HIGH RISK POPULATION; HUMAN; IMMUNE RESPONSE; IMMUNOLOGY; INNATE IMMUNITY; LIFE HISTORY; MALNUTRITION; MEDICAL RESEARCH; MORTALITY RISK; NONHUMAN; NUTRITIONAL ASSESSMENT; PRIORITY JOURNAL; REVIEW; RISK ASSESSMENT; RISK FACTOR; THEORY;

EID: 85032027276     PISSN: None     EISSN: 20506201     Source Type: Journal    
DOI: 10.1093/EMPH/EOV033     Document Type: Review

References (113)

1. Ridker PM, Buring JE, CookNRet al. C-reactive protein, the metabolic syndrome, and risk of incident cardiovascular events: an 8-Year follow-up of 14 719 initially healthy American women. Circulation 2003;107:391-7
2. Pradhan AD, Manson JE, Rifai N et al. C-reactive protein, interleukin 6, and risk of developing type 2 diabetes mellitus. J Am Med Assoc 2001;286:327-34
3. Kuo H-K, Bean JF, Yen C-J et al. Linking C-reactive protein to late-life disability in the National Health and Nutrition Examination Survey (NHANES) 1999-2002. J Gerontol Ser A Biol Sci Med Sci 2006;61:380-7
4. Li QT, Verma IM. NF-kappa B regulation in the immune system (vol 2, pg 725, 2002). Nat Rev Immunol 2002;2:975
5. Rather LJ. Disturbance of function (functio laesa): the legendary fifth cardinal sign of inflammation, added by Galen to the four cardinal signs of Celsus. Bull N Y Acad Med 1971;47:303-22
6. McDade TW. Early environments and the ecology of inflammation. Proc Natl Acad Sci 2012;109:17281-8
7. Weinberger B, Herndler Brandstetter D, Schwanninger A et al. Biology of immune responses to vaccines in elderly persons. Clin Infect Dis 2008;46:1078-84
8. Bhaskaram P. Micronutrient malnutrition, infection, and immunity: an overview. Nutr Rev 2002;60:S40-5
9. Kaech SM, Wherry EJ, Ahmed R. Vaccines: effector and memory T-cell differentiation: implications for vaccine development. Nat Rev Immunol 2002;2:251-62
10. McDade TW. Life history theory and the immune system: steps toward a human ecological immunology. Am J Phys Anthropol 2003;37:100-25
11. McDade TW, Reyes Garc�a V, Tanner S et al. Maintenance versus growth: investigating the costs of immune activation among children in lowland Bolivia. Am J Phys Anthropol 2008;136:478-84
12. Charnov EL. Life History Invariants. Oxford: Oxford University Press, 1993
13. Stearns SC. The Evolution of Life Histories. Oxford, New York: Oxford University Press, 1992, xii-249
14. Hill K, Hurtado AM. Ache Life History. New York: Aldine de Gruyter, 1996
15. Promislow DEL, Harvey PH. Mortality rates and the evolution of mammal life histories. Acta Oecologica 1991;12:119-37
16. Kirkwood TBL, Rose MR. Evolution of senescence: late survival sacrificied for reproduction. Philos Trans R Soc Lond 1991;332:15-24
17. Charnov EL, Berrigan D. Why do female primates have such long lifespans and so few babies? Or life in the slow lane. Evol Anthropol Issues 1993;1:191-94
18. Stearns SC, Koella JC. The evolution of phenotypic plasticity in life-history traits: predictions of reaction norms for age and size at maturity. Q Rev Biol 1986;40: 893-910
19. Sheldon BC, Verhulst S. Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol Evol 1996;11:317-21
20. Lochmiller RL, Deerenberg C. Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos 2000;88:87-98
21. Norris K, Evans MR. Ecological immunology: life history trade-offs and immune defense in birds. Behav Ecol 2000;11:19-26
22. Demas GE, Greives T, Chester E et al. The energetics of immunity: mechanisms mediating trade-offs in ecoimmunology. In: Demas GE, Nelson RJ (eds.). Ecoimmunology. Oxford: Oxford University Press, 2012
23. Sandland GJ, Minchella DJ. Costs of immune defense: an enigma wrapped in an environmental cloak? Trends Parasitol 2003;19:571-4
24. Zuk M, Stoehr AM. Immune defense and host life history. Am Nat 2002;160:S9-22
25. Rauw WM. Immune response from a resource allocation perspective. Front Genet 2012;3:1-14
26. Eraud C, Jacquet A, Faivre B. Survival cost of an early immune soliciting in nature. Evolution 2009;63:1036-43
27. Lee KA. Linking immune defenses and life history at the levels of the individual and the species. Integr Comp Biol 2006;46:1000-15
28. Moret Y. Explaining variable costs of the immune response: selection for specific versus non-specific immunity and facultative life history change. Oikos 2003;102:213-6
29. Klasing KC, Leshchinsky TV. Functions, costs, and benefits of the immune system during development and growth. Ostrich 1999;69:2817-32
30. Klasing KC. The costs of immunity. Dong Wu Xue Bao[Acta Zoologica Sinica] 2004;50:961-9
31. Allen LC, Turmelle AS, Mendon�a MT et al. Roosting ecology and variation in adaptive and innate immune system function in the Brazilian free-tailed bat (Tadarida brasiliensis). J Comp Physiol B 2009;179:315-23
32. Wegner KM, Kalbe M, Reusch TBH. Innate versus adaptive immunity in sticklebacks: evidence for trade-offs from a selection experiment. Evol Ecol 2007;21:473-83
33. Blackwell AD, Snodgrass JJ, Madimenos FC et al. Life history, immune function, and intestinal helminths: tradeoffs among immunoglobulin E, C-reactive protein, and growth in an Amazonian population. Am J Hum Biol 2010;22:836-48
34. Muehlenbein MP, Bribiescas RG. Testosterone-mediated immune functions and male life histories. Am J Hum Biol 2005;17:527-58
35. Paul WE (ed.). Fundamental Immunology, 7th edn. Philadelphia: Lippincott Williams & Wilkins, 2013, 1-1828
36. Goldsby RA, Kindt TJ, Osborne BA. Kuby Immunology.New York: WH Freeman, 2000
37. McDade TW, Worthman CM. Evolutionary process and the ecology of human immune function. Am J Hum Biol 1999;11:705-17
38. Muehlenbein MP, Hirschtick JL, Bonner JZ et al. Toward quantifying the usage costs of human immunity: altered metabolic rates and hormone levels during acute immune activation in men. Am J Hum Biol 2010;22:546-56
39. George AJT, Ritter MA. Thymic involution with ageing: obsolescence or good housekeeping? Immunol Today 1996;17:267-72
40. Steinmann GG, Klaus B, Muller-Hermelink HK. The involution of the ageing human thymic epithelium is independent of puberty. A morphometric study. Scand J Immunol 1985;22:563-75
41. Elia M. Organ and tissue conribution to metabolic rate. In: McKinney JM, TuckerHN(eds.). Energy Metabolism: Tissue Determinants and Cellular Corollaries. New York: Raven, 1992, 61-80
42. Martin LB, Scheuerlein A, Wikelski M. Immune activity elevates energy expenditure of house sparrows: a link between direct and indirect costs? Proc R Soc Lond 2002;270:153-8
43. Mata L. Diarrheal disease as a cause of malnutrition. Am J Trop Med Hyg 1992;47:16-27
44. Solomons NW. Pathways to the impairment of human nutritional status by gastrointestinal pathogens. Parasitology 1993;107:S19-35
45. Bois DEF. The basal metabolism in fever. J Am Med Assoc 1921;77:352-5
46. Rohner GB, SnapeMD, Kelly DF et al. Themagnitude of the antibody andmemory b cell responses during primingwith a protein-polysaccharide conjugate vaccine in human infants is associated with the persistence of antibody and the intensity of booster response. J Immunol 2008;180:2165-73
47. Linderkamp O, Versmold HT, Riegel KP et al. Estimation and prediction of blood volume in infants and children. Eur J Pediatr 1977;125:227-34
48. Mayo Clinic. Pediatric Test Reference Values. http://wwwmayomedicallaboratoriescomtest-infopediatricrefvaluesreferencephp. 2015 (19 November 2015, date last accessed)
49. Waterlow JC. Protein turnover with special reference to man. Quart J Exp Phys 1984;69:409-38
50. Darzynkiewicz Z, Dokov VK, Pienkowski M. Dry mass of lymphocytes during transformation after stimulation by phytohaemagglutinin. Nature 1967;214:1265-6
51. Lee KA, Wikelski M, Robinson WD et al. Constitutive immune defences correlate with life-history variables in tropical birds. J Animal Ecol 2008;77:356-63
52. Previtali MA, Previtali MA, Ostfeld RS et al. Relationship between pace of life and immune responses in wild rodents. Oikos 2012;121:1483-92
53. Martin LBI, Weil ZM, Nelson RJ. Immune defense and reproductive pace of life in Peromyscus mice. Ecology 2007;88:2516-28
54. Lindstrom KM, Foufopoulos J, Parn H et al. Immunological investments reflect parasite abundance in island populations of Darwin's finches. Proc R Soc B Biol Sci 2004;271:1513-9
55. Shudo E, Iwasa Y. Inducible defense against pathogens and parasites: optimal choice among multiple options. J Theor Biol 2001;209:233-47
56. Frank SA. Specific and non-specific defense against parasitic attack. J Theor Biol 2000;202:283-304
57. Horrocks NPC, Hegemann A, Ostrowski S et al. Environmental proxies of antigen exposure explain variation in immune investment better than indices of pace of life. Oecologia 2015;177:281-90
58. VersteeghMA, Schwabl I, Jaquier S et al.Doimmunological, endocrine and metabolic traits fall on a single Pace-of-Life axis? Covariation and constraints among physiological systems. J Evol Biol 2012;25:1864-76
59. Brzek P, Konarzewski M. Relationship between avian growth rate and immune response depends on food availability. J Exp Biol 2007;210:2361-7
60. Peck HE, Costa DP, Crocker DE. Body reserves influence allocation to immune responses in capital breeding female northern elephant seals. Functional Ecology. 2015:1-9
61. Vera-Massieu C, Brock PM, Godinez-Reyes C et al. Activation of an inflammatory response is contextdependent during early development of the California sea lion. R Soc Open Sci 2015;2:150108
62. Pigeon G, B�lisle M, Garant D et al. Ecological immunology in a fluctuating environment: an integrative analysis of tree swallow nestling immune defense. Ecol Evol 2013;3:1091-103
63. Ricklefs RE, Wikelski M. The physiology/life-history nexus. Trends Ecol Evol 2002;17:462-8
64. Chisholm JS. Death, hope, sex: life-history theory and the development of reproductive strategies. Curr Anthropol 1993;34:1-24
65. Gluckman PD, Hanson MA, Spencer HG. Predictive adaptive responses and human evolution. Trends Ecol Evol 2005;20:527-33
66. Nettle D, Bateson M. Adaptive developmental plasticity: what is it, how can we recognize it and when can it evolve? Proc R Soc B Biol Sci 2015;282:20151005-9
67. Kuzawa CW. Developmental origins of life history: growth, productivity, and reproduction. Am J Hum Biol 2007;19:654-61
68. Kuzawa CW, McDade TW, Adair LS et al. Rapid weight gain after birth predicts life history and reproductive strategy in Filipino males. Proc Natl Acad Sci 2010;107: 16800-5
69. Kuzawa CW. Adipose tissue in human infancy and childhood: an evolutionary perspective. Yearbook Phys Anthropol 1998;41:177-210
70. Kuzawa CW, Chugani HT, Grossman LI et al. Metabolic costs and evolutionary implications of human brain development. Proc Natl Acad Sci 2014;111:13010-5
71. Popkin BM, Gordon-Larsen P. The nutrition transition: worldwide obesity dynamics and their determinants. Int J Obesity 2004;28:S2-9
72. Fredensborg BL, Poulin R. Parasitism shaping host life-history evolution: adaptive responses in amarine gastropod to infection by trematodes. J Animal Ecol 2006;75:44-53
73. St�rmer C. Sex differences in the consequences of earlylife exposure to epidemiological stress-a life-history approach. Am J Hum Biol 2011;23:201-8
74. Kuzawa CW, Bragg JM. Plasticity in human life history strategy. Curr Anthropol 2012;53:S369-82
75. Ellis BJ. Timing ofpubertalmaturation in girls: an integrated life history approach. Psychol Bull 2004;130:920-58
76. Ellis BJ, Figueredo AJ, Brumbach BH et al. Fundamental dimensions of environmental risk: the impact of harsh versus unpredictable environments on the evolution and development of life history strategies. Hum Nat 2009;20:204-68
77. Burton L. Teenage childbearing as an alternative lifecourse strategy in multigeneration black families. Hum Nat 1990;1:123-43
78. Chisholm JS, Quinlivan JA, Petersen RW et al. Early stress predicts age at menarche and first birth, adult attachment, and expected lifespan. Hum Nat 2005;16:233-65
79. Nettle D, Coall DA, Dickins TE. Birthweight and paternal involvement predict early reproduction in British women: evidence from the National Child Development Study. Am J Hum Biol 2010;22:172-9
80. Low BS, Hazel A, Parker N et al. Influences on women's reproductive lives unexpected ecological underpinnings. Cross Cultural Res 2008;42:201-19
81. Gettler LT, McDade TW, Bragg JM et al. 2015 Developmental energetics, sibling death, and parental instability as predictors of maturational tempo and life history scheduling in males from Cebu, Philippines. Am J Phys Anthropol. 2015;158:175-84
82. Sheppard P, Snopkowski K, Sear R. Father absence and reproduction-related outcomes in malaysia, a transitional fertility population. Hum Nat 2014;25:213-34
83. St�rmer C, Lummaa V. Increased mortality exposure within the family rather than individual mortality experiences triggers faster life-history strategies in historic human populations. PLoS One 2014;9:e83633-9
84. Salomon JA, Wang H, Freeman MK et al. Healthy life expectancy for 187 countries, 1990-2010: a systematic analysis for the Global Burden Disease Study 2010. Lancet 2012;380:2144-62
85. Wang H, Dwyer-Lindgren L, Lofgren KT et al. Age-specific and sex-specific mortality in 187 countries, 1970-2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet 2012;380:2071-94
86. Austad SN. Why women live longer than men: sex differences in longevity. Gend Med 2006;3:79-92
87. Guerra-Silveira F, Abad-Franch F. Sex bias in infectious disease epidemiology: patterns and processes. PLOS ONE 2013;8:e62390
88. Muenchhoff M, Goulder PJR. Sex differences in pediatric infectious diseases. J Infect Dis 2014;209:S120-6
89. Whitacre CC. Sex differences in autoimmune disease. Nat Immunol 2001;2:777-80
90. McDade TW, Beck MA, Kuzawa C et al. Prenatal undernutrition, postnatal environments, and antibody response to vaccination in adolescence. Am J Clin Nutr 2001;74:543-8
91. McDade TW, Rutherford J, Adair L et al. Early origins of inflammation: microbial exposures in infancy predict lower levels of C-reactive protein in adulthood. Proc R Soc B Biol Sci 2010; 277:1129-37
92. McDade TW, Metzger MW, Chyu L et al. Long-term effects of birth weight and breastfeeding duration on inflammation in early adulthood. Proc R Soc B Biol Sci 2014;281: 20133116
93. Sattar N, McConnachie A, O'Reilly D et al. Inverse association between birth weight and C-reactive protein concentrations in theMIDSPAN Family Study. Arterioscler Thromb Vasc Biol 2004;24:583-7
94. Danese A, Moffitt TE, Harrington H et al. Adverse childhood experiences and adult risk factors for age-related disease: depression, inflammation, and clustering of metabolic risk markers. Arch Pediatr Adolesc Med 2009;163:1135-43
95. Taylor SE, Lehman BJ, Kiefe CI et al. Relationship of early life stress and psychological functioning to adult C-reactive protein in the coronary artery risk development in young adults study. Biol Psychiatry 2006;60:819-24
96. Miller GE, Chen E, Fok AK et al. Low early-life social class leaves a biological residue manifested by decreased glucocorticoid and increased proinflammatory signaling. Proc Natl Acad Sci 2009;106:14716-21
97. Miller GE, Chen E. Harsh family climate in early life presages the emergence of a proinflammatory phenotype in adolescence. Psychol Sci 2010;21:848-56
98. Slopen N, McLaughlin KA, Dunn EC et al. Childhood adversity and cell-mediated immunity in young adulthood: does type and timing matter? Brain Behav Immun 2013;28:63-71
99. Shirtcliff EA, Coe CL, Pollak SD. Early childhood stress is associated with elevated antibody levels to herpes simplex virus type 1. Proc Natl Acad Sci 2009;106: 2963-7
100. McDade TW, Adair L, Feranil AB et al. Positive antibody response to vaccination in adolescence predicts lower Creactive protein concentration in young adulthood in the philippines. Am J Hum Biol 2011;23:313-8
101. Lasker GW. Human biological adaptability: the ecological approach in physical anthropology. Science 1969;166:1480-6
102. Martin LB, Weil ZM, Nelson RJ. Seasonal changes in vertebrate immune activity: mediation by physiological trade-offs. Philos Trans R Soc B Biol Sci 2008;363:321-39
103. Barker D. The developmental origins of adult disease. J Am Coll Nutr 2004;23:588S-95
104. Hamilton WD. The moulding of senescence by natural selection. J Theor Biol 1966;12:12-45
105. Rook G, Stanford JL. Give us our daily germs. Immunol Today 1998;19:113-6
106. Yazdanbakhsh M, Kremsner PG, van Ree R. Allergy, parasites, and the hygiene hypothesis. Science 2002;296:490-4
107. Radon K, Windstetter D, Poluda AL et al. Contact with farm animals in early life and juvenile inflammatory bowel disease: a case-control study. Pediatrics 2007;120:354-61
108. Rook GA, Adams V, Hunt J et al. Mycobacteria and other environmental organisms as immunomodulators for immunoregulatory disorders. Springer Semin Immunopathol 2004;25:237-55
109. Barrett R, Kuzawa CW, McDade T et al. Emerging and reemerging infectious diseases: the third epidemiologic transition. Annu Rev Anthropol 1998;27:247-71
110. Schaffler A, Muller-Ladner U, Scholmerich J et al. Role of adipose tissue as an inflammatory organ in human diseases. Endocr Rev 2006;27:449-67
111. McDade TW, Rutherford JN, Adair L et al. Population differences in associations between C-reactive protein concentration and adiposity: comparison of young adults in the Philippines and the United States. Am J Clin Nutr 2009;89:1237-45
112. McDade TW, Williams S, Snodgrass JJ. What a drop can do: dried blood spots as a minimally invasive method for integrating biomarkers into population-based research. Demography 2007;44:899-925
113. Demas GE, Zysling DA, Beechler BR et al. Beyond phytohaemagglutinin: assessing vertebrate immune function across ecological contexts. J Animal Ecol 2011;80: 710-30