Effects of reproduction on immuno-suppression and oxidative damage, and hence support or otherwise for their roles as mechanisms underpinning life history trade-offs, are tissue and assay dependent

Journal of Experimental Biology

Volumn 216, Issue 22, 2013, Pages 4242-4250

  Yang, Deng Bao ^a,b   Xu, Yan Chao ^a,b   Wang, De Hua ^a   Speakman, John R ^c,d  

^a INSTITUTE OF ZOOLOGY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c INSTITUTE OF GENETICS AND DEVELOPMENTAL BIOLOGY   (China)

^d UNIVERSITY OF ABERDEEN   (United Kingdom)

Author keywords

Environmental temperature; Immune function; Lactation; Meriones unguiculatus; Mongolian gerbil; Oxidative damage; Trade offs

Indexed keywords

GLUTATHIONE PEROXIDASE; PHYTOHEMAGGLUTININ; SUPEROXIDE DISMUTASE; THIOBARBITURIC ACID REACTIVE SUBSTANCE;

ANALYSIS OF VARIANCE; ANIMAL; ARTICLE; BACTERICIDAL ACTIVITY; BLOOD; ENVIRONMENTAL TEMPERATURE; FEMALE; GERBIL; IMMUNE FUNCTION; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; LACTATION; MERIONES UNGUICULATUS; METABOLISM; NONPARAMETRIC TEST; ORGAN SIZE; OXIDATIVE DAMAGE; OXIDATIVE STRESS; PHYSIOLOGY; REPRODUCTION; TEMPERATURE; THYMUS; TRADE-OFFS;

ENVIRONMENTAL TEMPERATURE; IMMUNE FUNCTION; LACTATION; MERIONES UNGUICULATUS; MONGOLIAN GERBIL; OXIDATIVE DAMAGE; TRADE-OFFS;

ANALYSIS OF VARIANCE; ANIMALS; FEMALE; GERBILLINAE; GLUTATHIONE PEROXIDASE; IMMUNE TOLERANCE; ORGAN SIZE; OXIDATIVE STRESS; PHYTOHEMAGGLUTININS; REPRODUCTION; SERUM BACTERICIDAL TEST; STATISTICS, NONPARAMETRIC; SUPEROXIDE DISMUTASE; TEMPERATURE; THIOBARBITURIC ACID REACTIVE SUBSTANCES; THYMUS GLAND;

EID: 84887305021     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.092049     Document Type: Article

References (85)

1. Alonso-Álvarez, C., Bertrand, S., Devevey, G., Prost, J., Faivre, B. and Sorci, G. (2004). Increased susceptibility to oxidative stress as a proximate cost of reproduction. Ecol. Lett. 7, 363-368.
2. Andziak, B. and Buffenstein, R. (2006). Disparate patterns of age-related changes in lipid peroxidation in long-lived naked mole-rats and shorter-lived mice. Aging Cell 5, 525-532.
3. Balaban, R. S., Nemoto, S. and Finkel, T. (2005). Mitochondria, oxidants, and aging. Cell 120, 483-495.
4. Bergeron, P., Careau, V., Humphries, M. M., Reale, D., Speakman, J. R. and Garant, D. (2011). The energetic and oxidative costs of reproduction in a freeranging rodent. Funct. Ecol. 25, 1063-1071.
5. Boulinier, T. and Staszewski, V. (2008). Maternal transfer of antibodies: raising immuno-ecology issues. Trends Ecol. Evol. 23, 282-288.
6. Bronson, F. (1998). Energy balance and ovulation: small cages versus natural habitats. Reprod. Fertil. Dev. 10, 127-137.
7. Caldeira da Silva, C. C., Cerqueira, F. M., Barbosa, L. F., Medeiros, M. H. G. and Kowaltowski, A. J. (2008). Mild mitochondrial uncoupling in mice affects energy metabolism, redox balance and longevity. Aging Cell 7, 552-560.
8. Castillo, C., Hernandez, J., Bravo, A., Lopez-Alonso, M., Pereira, V. and Benedito, J. L. (2005). Oxidative status during late pregnancy and early lactation in dairy cows. Vet. J. 169, 286-292.
9. Chen, Z. Z. (1988). Topography and climate of Xilin River basin. In: Inner Mongolian Grassland Ecosystem Research Station of Academia Sinica (1979-1988) (ed. Y. Ba and P. Keli), pp. 13-22. Beijing: Science Press.
10. Christe, P., Arlettaz, R. and Vogel, P. (2000). Variation in intensity of a parasitic mite (Spinturnix myoti) in relation to the reproductive cycle and immunocompetence of its bat host (Myotis myotis). Ecol. Lett. 3, 207-212.
11. Christe, P., Glaizot, O., Strepparava, N., Devevey, G. and Fumagalli, L. (2012). Twofold cost of reproduction: An increase in parental effort leads to higher malarial parasitaemia and to a decrease in resistance to oxidative stress. Proc. Biol. Sci. 279, 1142-1149.
12. Costantini, D. (2008). Oxidative stress in ecology and evolution: lessons from avian studies. Ecol. Lett. 11, 1238-1251.
13. Costantini, D. and Dell'Omo, G. (2006). Environmental and genetic components of oxidative stress in wild kestrel nestlings (Falco tinnunculus). Comp. Biochem. Physiol. 145A, 137-142.
14. Dalle-Donne, I., Rossi, R., Giustarini, D., Milzani, A. and Colombo, R. (2003). Protein carbonyl groups as biomarkers of oxidative stress. Clin. Chim. Acta 329, 23- 38.
15. Del Rio, D., Stewart, A. J. and Pellegrini, N. (2005). A review of recent studies on malondialdehyde as toxic molecule and biological marker of oxidative stress. Nutr. Metab. Cardiovasc. Dis. 15, 316-328.
16. Demas, G. E., Zysling, D. A., Beechler, B. R., Muehlenbein, M. P. and French, S. S. (2011). Beyond phytohaemagglutinin: Assessing vertebrate immune function across ecological contexts. J. Anim. Ecol. 80, 710-730.
17. Dowling, D. K. and Simmons, L. W. (2009). Reactive oxygen species as universal constraints in life-history evolution. Proc. Biol. Sci. 276, 1737-1745.
18. Drazen, D. L., Trasy, A. and Nelson, R. J. (2003). Photoperiod differentially affects energetics of immunity in pregnant and lactating Siberian hamsters (Phodopus sungorus). Can. J. Zool. 81, 1406-1413.
19. Drent, R. and Daan, S. (1980). The prudent parent: energetic adjustments in avian breeding. Ardea 68, 225-252.
20. Eraud, C., Devevey, G., Gaillard, M., Prost, J., Sorci, G. and Faivre, B. (2007). Environmental stress affects the expression of a carotenoid-based sexual trait in male zebra finches. J. Exp. Biol. 210, 3571-3578.
21. Fletcher, Q. E., Selman, C., Boutin, S., McAdam, A. G., Woods, S. B., Seo, A. Y., Leeuwenburgh, C., Speakman, J. R. and Humphries, M. M. (2013). Oxidative damage increases with reproductive energy expenditure and is reduced by foodsupplementation. Evolution 67, 1527-1536.
22. French, S. S., Greives, T. J., Zysling, D. A., Chester, E. M. and Demas, G. E. (2009). Leptin increases maternal investment. Proc. Biol. Sci. 276, 4003-4011.
23. Garratt, M., Vasilaki, A., Stockley, P., McArdle, F., Jackson, M. and Hurst, J. L. (2011). Is oxidative stress a physiological cost of reproduction? An experimental test in house mice. Proc. Biol. Sci. 278, 1098-1106.
24. Garratt, M., Pichaud, N., King, E. D. A. and Brooks, R. C. (2013). Physiological adaptations to reproduction. I. Experimentally increasing litter size enhances aspects of antioxidant defence but does not cause oxidative damage in mice. J. Exp. Biol. 216, 2879-2888.
25. Gems, D. and Partridge, L. (2013). Genetics of longevity in model organisms: debates and paradigm shifts. Annu. Rev. Physiol. 75, 621-644.
26. Goüy de Bellocq, J., Krasnov, B. R., Khokhlova, I. S. and Pinshow, B. (2006). Temporal dynamics of a T-cell mediated immune response in desert rodents. Comp. Biochem. Physiol. 145A, 554-559.
27. Greives, T., McGlothlin, J., Jawor, J., Demas, G. and Ketterson, E. (2006). Testosterone and innate immune function inversely covary in a wild population of breeding dark-eyed juncos (Junco hyemalis). Funct. Ecol. 20, 812-818.
28. Hammond, K. A. and Diamond, J. (1992). An experimental test for a ceiling on sustained metabolic-rate in lactating mice. Physiol. Zool. 65, 952-977.
29. Hammond, K. A. and Diamond, J. (1997). Maximal sustained energy budgets in humans and animals. Nature 386, 457-462.
30. Hasselquist, D. and Nilsson, J. A. (2009). Maternal transfer of antibodies in vertebrates: Trans-generational effects on offspring immunity. Philos. Trans. R. Soc. B 364, 51-60.
31. Isaksson, C., Sheldon, B. C. and Uller, T. (2011). The challenges of integrating oxidative stress into life-history biology. Bioscience 61, 194-202.
32. Johnson, M. S. and Speakman, J. R. (2001). Limits to sustained energy intake. V. Effect of cold-exposure during lactation in Mus musculus. J. Exp. Biol. 204, 1967-1977.
33. Johnson, M. S., Thomson, S. C. and Speakman, J. R. (2001a). Limits to sustained energy intake. I. Lactation in the laboratory mouse Mus musculus. J. Exp. Biol. 204, 1925-1935.
34. Johnson, M. S., Thomson, S. C. and Speakman, J. R. (2001b). Limits to sustained energy intake. II. Inter-relationships between resting metabolic rate, life-history traits and morphology in Mus musculus. J. Exp. Biol. 204, 1937-1946.
35. Keipert, S., Voigt, A. and Klaus, S. (2011). Dietary effects on body composition, glucose metabolism, and longevity are modulated by skeletal muscle mitochondrial uncoupling in mice. Aging Cell 10, 122-136.
36. Kennedy, G. C., Pearce, W. M. and Parrott, D. M. V. (1958). Liver growth in the lactating rat. J. Endocrinol. 17, 158-160.
37. Knowles, S. C. L., Nakagawa, S. and Sheldon, B. C. (2009). Elevated reproductive effort increases blood parasitaemia and decreases immune function in birds: A metaregression approach. Funct. Ecol. 23, 405-415.
38. Król, E., Johnson, M. S. and Speakman, J. R. (2003). Limits to sustained energy intake. VIII. Resting metabolic rate and organ morphology of laboratory mice lactating at thermoneutrality. J. Exp. Biol. 206, 4283-4291.
39. Król, E., Murphy, M. and Speakman, J. R. (2007). Limits to sustained energy intake. X. Effects of fur removal on reproductive performance in laboratory mice. J. Exp. Biol. 210, 4233-4243.
40. Leeuwenburgh, C. and Heinecke, J. W. (2001). Oxidative stress and antioxidants in exercise. Curr. Med. Chem. 8, 829-838.
41. Lochmiller, R. L. and Deerenberg, C. (2000). Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos 88, 87-98.
42. Martin, L. B., Weil, Z. M. and Nelson, R. J. (2008). Seasonal changes in vertebrate immune activity: mediation by physiological trade-offs. Philos. Trans. R. Soc. B 363, 321-339.
43. Mateos, R. and Bravo, L. (2007). Chromatographic and electrophoretic methods for the analysis of biomarkers of oxidative damage to macromolecules (DNA, lipids, and proteins). J. Sep. Sci. 30, 175-191.
44. Metcalfe, N. B. and Alonso-Álvarez, C. (2010). Oxidative stress as a life-history constraint: The role of reactive oxygen species in shaping phenotypes from conception to death. Funct. Ecol. 24, 984-996.
45. Metcalfe, N. B. and Monaghan, P. (2013) Does reproduction cause oxidative stress? An open question. Trends Ecol. Evol. 28, 347-350.
46. Monaghan, P., Metcalfe, N. B. and Torres, R. (2009). Oxidative stress as a mediator of life history trade-offs: mechanisms, measurements and interpretation. Ecol. Lett. 12, 75-92.
47. Moore, K. and Roberts, L. J. (1998). Measurement of lipid peroxidation. Free Radic. Res. 28, 659-671.
48. Nordling, D., Andersson, M., Zohari, S. and Lars, G. (1998). Reproductive effort reduces specific immune response and parasite resistance. Proc. Biol. Sci. 265, 1291-1298.
49. Norris, K. and Evans, M. R. (2000). Ecological immunology: life history trade-offs and immune defense in birds. Behav. Ecol. 11, 19-26.
50. Nussey, D. H., Pemberton, J. M., Pilkington, J. G. and Blount, J. D. (2009). Life history correlates of oxidative damage in a free-living mammal population. Funct. Ecol. 23, 809-817.
51. Ołdakowski, L., Piotrowska, Z., Chrzaácik, K. M., Sadowska, E. T., Koteja, P. and Taylor, J. R. (2012). Is reproduction costly? No increase of oxidative damage in breeding bank voles. J. Exp. Biol. 215, 1799-1805.
52. Perez-Rodriguez, L., Mougeot, F., Alonso-Alvarez, C., Blas, J., Viñuela, J. and Bortolotti, G. R. (2008). Cell-mediated immune activation rapidly decreases plasma carotenoids but does not affect oxidative stress in red-legged partridges (Alectoris rufa). J. Exp. Biol. 211, 2155-2161.
53. Peterson, C. C., Nagy, K. A. and Diamond, J. (1990). Sustained metabolic scope. Proc. Natl. Acad. Sci. USA 87, 2324-2328.
54. Piersma, T. and Van Gils, J. A. (2011). The Flexible Phenotype: A Body-Centred Integration of Ecology, Physiology, and Behaviour. Oxford: Oxford University Press.
55. Salmon, A. B., Marx, D. B. and Harshman, L. G. (2001). A cost of reproduction in Drosophila melanogaster: stress susceptibility. Evolution 55, 1600-1608.
56. Selman, C., McLaren, J. S., Himanka, M. J. and Speakman, J. R. (2000). Effect of long-term cold exposure on antioxidant enzyme activities in a small mammal. Free Radic. Biol. Med. 28, 1279-1285.
57. Selman, C., McLaren, J. S., Collins, A. R., Duthie, G. G. and Speakman, J. R. (2008). The impact of experimentally elevated energy expenditure on oxidative stress and lifespan in the short-tailed field vole Microtus agrestis. Proc. Biol. Sci. 275, 1907-1916.
58. Selman, C., Blount, J. D., Nussey, D. H. and Speakman, J. R. (2012). Oxidative damage, ageing, and life-history evolution: where now? Trends Ecol. Evol. 27, 570- 577.
59. Sheldon, B. C. and Verhulst, S. (1996). Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol. Evol. 11, 317-321.
60. Simons, M. J. P., Reimert, I., van der Vinne, V., Hambly, C., Vaanholt, L. M., Speakman, J. R. and Gerkema, M. P. (2011). Ambient temperature shapes reproductive output during pregnancy and lactation in the common vole (Microtus arvalis): A test of the heat dissipation limit theory. J. Exp. Biol. 214, 38-49.
61. Sohal, R. S., Agarwal, S. and Sohal, B. H. (1995). Oxidative stress and aging in the Mongolian gerbil (Meriones unguiculatus). Mech. Ageing Dev. 81, 15-25.
62. Sorci, G. and Faivre, B. (2009). Inflammation and oxidative stress in vertebrate host-parasite systems. Philos. Trans. R. Soc. B 364, 71-83.
63. Speakman, J. R. (2008). The physiological costs of reproduction in small mammals. Philos. Trans. R. Soc. B 363, 375-398.
64. Speakman, J. R. and Garratt, M. (2014). Measuring oxidative stress as a cost of reproduction: some complexities in experimental design. Bioessays (in press).
65. Speakman, J. R. and Król, E. (2010). Maximal heat dissipation capacity and hyperthermia risk: neglected key factors in the ecology of endotherms. J. Anim. Ecol. 79, 726-746.
66. Speakman, J. R. and Król, E. (2011). Limits to sustained energy intake. XIII. Recent progress and future perspectives. J. Exp. Biol. 214, 230-241.
67. Speakman, J. R. and McQueenie, J. (1996). Limits to sustained metabolic rate: The link between food intake, basal metabolic rate, and morphology in reproducing mice, Mus musculus. Physiol. Zool. 69, 746-769.
68. Speakman, J. R., Talbot, D. A., Selman, C., Snart, S., McLaren, J. S., Redman, P., Krol, E., Jackson, D. M., Johnson, M. S. and Brand, M. D. (2004). Uncoupled and surviving: individual mice with high metabolism have greater mitochondrial uncoupling and live longer. Aging Cell 3, 87-95.
69. Stearns, S. C. (1992). The Evolution of Life Histories. Oxford: Oxford University Press.
70. Stier, A., Reichert, S., Massemin, S., Bize, P. and Criscuolo, F. (2012). Constraint and cost of oxidative stress on reproduction: correlative evidence in laboratory mice and review of the literature. Front. Zool. 9, 37.
71. Suzuki, K., Hirose, H., Hokao, R., Takemura, N. and Motoyoshi, S. (1993). Changes of plasma osmotic pressure during lactation in rats. J. Vet. Med. Sci. 55, 561-564.
72. Tieleman, I. B., Williams, J. B., Ricklefs, R. E. and Klasing, K. C. (2005). Constitutive innate immunity is a component of the pace-of-life syndrome in tropical birds. Proc. Biol. Sci. 272, 1715-1720.
73. Upreti, K., Chaki, S. and Misro, M. (2002). Evaluation of peroxidative stress and enzymatic antioxidant activity in liver and kidney during pregnancy and lactation in rats. Health Popul. Issues Perspect. 25, 177-185.
74. Venditti, P., Di Stefano, L. and Di Meo, S. (2010). Oxidative stress in cold-induced hyperthyroid state. J. Exp. Biol. 213, 2899-2911.
75. Wade, G. N. and Schneider, J. E. (1992). Metabolic fuels and reproduction in female mammals. Neurosci. Biobehav. Rev. 16, 235-272.
76. Walker, E. P. (1968). Mammals of the World, 2nd edn. Baltimore, MD: Johns Hopkins Press.
77. Wang, Y., Salmon, A. B. and Harshman, L. G. (2001). A cost of reproduction: oxidative stress susceptibility is associated with increased egg production in Drosophila melanogaster. Exp. Gerontol. 36, 1349-1359.
78. Wiersma, P., Selman, C., Speakman, J. R. and Verhulst, S. (2004). Birds sacrifice oxidative protection for reproduction. Proc. Biol. Sci. 271 Suppl. 5, S360-S363.
79. Xu, D. L. and Wang, D. H. (2010). Fasting suppresses T cell-mediated immunity in female Mongolian gerbils (Meriones unguiculatus). Comp. Biochem. Physiol. 155A, 25-33.
80. Yang, W., Li, J. and Hekimi, S. (2007). A Measurable increase in oxidative damage due to reduction in superoxide detoxification fails to shorten the life span of long-lived mitochondrial mutants of Caenorhabditis elegans. Genetics 177, 2063- 2074.
81. Yang, D. B., Xu, Y. C. and Wang, D. H. (2012). Partial removal of brown adipose tissue enhances humoral immunity in warm-acclimated Mongolian gerbils (Meriones unguiculatus). Gen. Comp. Endocrinol. 175, 144-152.
82. Yang, D. B., Li, L., Wang, L. P., Chi, Q. S., Hambly, C., Wang, D. H. and Speakman, J. R. (2013). Limits to sustained energy intake. XIX. A test of the heat dissipation limitation hypothesis in Mongolian gerbils (Meriones unguiculatus). J. Exp. Biol. 216, 3358-3368.
83. Zera, A. J. and Harshman, L. G. (2001). The physiology of life history trade-offs in animals. Annu. Rev. Ecol. Syst. 32, 95-126.
84. Zhang, Y., Ikeno, Y., Qi, W., Chaudhuri, A., Li, Y., Bokov, A., Thorpe, S. R., Baynes, J. W., Epstein, C., Richardson, A. et al. (2009). Mice deficient in both Mn superoxide dismutase and glutathione peroxidase-1 have increased oxidative damage and a greater incidence of pathology but no reduction in longevity. J. Gerontol. 64A, 1212-1220.
85. Zhao, Z. J., Song, D. G., Su, Z. C., Wei, W. B., Liu, X. B. and Speakman, J. R. (2013). Limits to sustained energy intake. XVIII. Energy intake and reproductive output during lactation in Swiss mice raising small litters. J. Exp. Biol. 216, 2349- 2358.