Is oxidative stress a physiological cost of reproduction? An experimental test in house mice

Proceedings of the Royal Society B: Biological Sciences

Volumn 278, Issue 1708, 2011, Pages 1098-1106

  Garratt, Michael ^a   Vasilaki, Aphrodite ^a   Stockley, Paula ^a   McArdle, Francis ^a   Jackson, Malcolm ^a   Hurst, Jane L ^a  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

Author keywords

Lactation; Life history; Mus musculus domesticus; Oxidative stress; Reproduction

Indexed keywords

BIOMARKER; CORRELATION; EXPERIMENTAL STUDY; FECUNDITY; FEMALE; LACTATION; OXIDATION; REPRODUCTIVE BEHAVIOR; RODENT; SURVIVAL;

BIOLOGICAL MARKER; GLUTATHIONE; MALONALDEHYDE; THIOL DERIVATIVE;

ANIMAL; ARTICLE; BLOOD; FEMALE; LACTATION; MOUSE; OXIDATIVE STRESS; PHYSIOLOGY; REPRODUCTION;

ANIMALS; BIOLOGICAL MARKERS; FEMALE; GLUTATHIONE; LACTATION; MALONDIALDEHYDE; MICE; OXIDATIVE STRESS; REPRODUCTION; SULFHYDRYL COMPOUNDS;

EID: 79958291850     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2010.1818     Document Type: Article

References (73)

1. Dufresne, F., FitzGerald, G. J. & Lachance, S. 1990 Age and size-related differences in reproductive success and reproductive costs in threespine sticklebacks (Gasterosteus aculeatus). Behav. Ecol. 1, 140-147. (doi:10.1093/ beheco/1.2.140)
2. Stearns, S. C. 1992 The evolution of life histories. Oxford, UK: Oxford University Press.
3. Nilsson, J. A. & Svensson, E. 1996 The cost of reproduction: a new link between current reproductive effort and future reproductive success. Proc. R. Soc. Lond. B 263, 711-714. (doi:10.1098/rspb.1996.0106)
4. Pike, T. W., Blount, J. D., Bjerkeng, B., Lindstrom, J. & Metcalfe, N. B. 2007 Carotenoids, oxidative stress and female mating preference for longer lived males. Proc. R. Soc. B 274, 1591-1596. (doi:10.1098/rspb. 2007.0317)
5. Harshman, L. G. & Zera, A. J. 2007 The cost of reproduction: the devil in the details. Trends Ecol. Evol. 22, 80-86. (doi:10.1016/j.tree.2006.10.008)
6. Kirkwood, T. B. L. & Holliday, R. 1979 Evolution of aging and longevity. Proc. R. Soc. Lond. B 205, 531-546. (doi:10.1098/rspb.1979.0083)
7. Partridge, L., Gems, D. & Withers, D. J. 2005 Sex and death: what is the connection? Cell 120, 461-472. (doi:10.1016/j.cell.2005.01.026)
8. Costantini, D. 2008 Oxidative stress in ecology and evolution: lessons from avian studies. Ecol. Lett. 11, 1238-1251.
9. Speakman, J. R. 2008 The physiological costs of reproduction in small mammals. Phil. Trans. R. Soc. B 363, 375-398. (doi:10.1098/rstb.2007.2145)
10. Dowling, D. K. & Simmons, L. W. 2009 Reactive oxygen species as universal constraints in life-history evolution. Proc. R. Soc. B 276, 1737-1745. (doi:10.1098/rspb. 2008.1791)
11. Monaghan, P., Metcalfe, N. B. & Torres, R. 2009 Oxidative stress as a mediator of life history trade-offs: mechanisms, measurements and interpretation. Ecol. Lett. 12, 75-92. (doi:10.1111/j.1461-0248.2008.01258.x)
12. Balaban, R. S., Nemoto, S. & Finkel, T. 2005 Mitochondria, oxidants, and aging. Cell 120, 483-495. (doi:10. 1016/j.cell.2005.02.001)
13. Halliwell, B. & Whiteman, M. 2004 Measuring reactive species and oxidative damage in vivo and in cell culture: how should you do it and what do the results mean? Br. J. Pharmacol. 142, 231-255. (doi:10.1038/sj.bjp. 0705776)
14. Harman, D. 1956 Aging: a theory based on free-radical and radiation-chemistry. J. Gerontol. 11, 298-300.
15. Beckman, K. B. & Ames, B. N. 1998 The free radical theory of aging matures. Physiol. Rev. 78, 547-581.
16. Halliwell, B. & Gutteridge, J. M. 1999 Free radicals in biology and medicine. Oxford, UK: Oxford University Press.
17. Metcalfe, N. B. & Alonso-Alvarez, 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. (doi:10.1111/j.1365-2435.2010.01750.x)
18. Alonso-Alvarez, C., Bertrand, S., Devevey, G., Prost, J., Faivre, B. & Sorci, G. 2004 Increased susceptibility to oxidative stress as a proximate cost of reproduction. Ecol. Lett. 7, 363-368. (doi:10.1111/j.1461-0248.2004.00594.x)
19. Speakman, J. R. et al. 2004 Uncoupled and surviving: individual mice with high metabolism have greater mitochondrial uncoupling and live longer. Aging Cell 3, 87-95. (doi:10.1111/j.1474-9728.2004.00097.x)
20. Vasilaki, A., McArdle, F., Iwanejko, L. M. & McArdle, A. 2006 Adaptive responses of mouse skeletal muscle to contractile activity: the effect of age. Mech. Ageing Dev. 127, 830-839. (doi:10.1016/j.mad.2006.08.004)
21. Valko, M., Leibfritz, D., Moncol, J., Cronin, M. T. D., Mazur, M. & Telser, J. 2007 Free radicals and antioxidants in normal physiological functions and human disease. Int. J. Biochem. Cell. Biol. 39, 44-84. (doi:10. 1016/j.biocel.2006.07.001)
22. Wiersma, P., Selman, C., Speakman, J. R. & Verhulst, S. 2004 Birds sacrifice oxidative protection for reproduction. Proc. R. Soc. Lond. B 271, S360-S363. (doi:10. 1098/rsbl.2004.0171)
23. Alonso-Alvarez, C., Bertrand, S., Devevey, G., Prost, J., Faivre, B., Chastel, O. & Sorci, G. 2006 An experimental manipulation of life-history trajectories and resistance to oxidative stress. Evolution 60, 1913-1924.
24. Cluttonbrock, T. H., Guinness, F. E. & Albon, S. D. 1983 The costs of reproduction to red deer hinds. J. Anim. Ecol. 52, 367-383.
25. Lambin, X. & Yoccoz, N. G. 2001 Adaptive precocial reproduction in voles: reproductive costs and multivoltine life-history strategies in seasonal environments. J. Anim. Ecol. 70, 191-200. (doi:10.1046/j.1365-2656.2001. 00494.x)
26. Koivula, M., Koskela, E., Mappes, T. & Oksanen, T. A. 2003 Cost of reproduction in the wild: manipulation of reproductive effort in the bank vole. Ecology 84, 398-405. (doi:10.1890/0012-9658(2003)084[0398: CORITW]2.0.CO;2)
27. Descamps, S., Boutin, S., Berteaux, D. & Gaillard, J. M. 2006 Best squirrels trade a long life for an early reproduction. Proc. R. Soc. B 273, 2369-2374. (doi:10.1098/rspb. 2006.3588)
28. Gittleman, J. L. & Thompson, S. D. 1988 Energy allocation in mammalian reproduction. Am. Zool. 28, 863-875.
29. Hammond, K. A. 1997 Adaptation of the maternal intestine during lactation. J. Mammary Gland Biol. Neoplasia 2, 243-252. (doi:10.1023/A:10263323 04435)
30. Krol, E. & Speakman, J. R. 2003 Limits to sustained energy intake. VI. Energetics of lactation in laboratory mice at thermoneutrality. J. Exp. Biol. 206, 4255-4266. (doi:10.1242/jeb.00674)
31. Speakman, J. R. & 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.
32. Upreti, K., Chaki, S. P. & Misro, M. 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.
33. Castillo, C., Hernandez, J., Bravo, A., Lopez-Alonso, M., Pereira, V. & Benedito, J. L. 2005 Oxidative status during late pregnancy and early lactation in dairy cows. Vet. J. 169, 286-292. (doi:10.1016/j.tvjl.2004.02.001)
34. Konig, B. & Markl, H. 1987 Maternal-care in house mice. 1. The weaning strategy as a means for parental manipulation of offspring quality. Behav. Ecol. Sociobiol. 20, 1-9. (doi:10.1007/BF00292161)
35. Perrigo, G. 1987 Breeding and feeding strategies in deer mice and house mice when females are challenged to work for their food. Anim. Behav. 35, 1298-1316. (doi:10.1016/S0003-3472(87)80002-7)
36. Griffith, O. W. 1999 Biologic and pharmacologic regulation of mammalian glutathione synthesis. Free Radical Biol. Med. 27, 922-935. (doi:10.1016/S0891- 5849(99)00176-8)
37. Berry, R. J. & Jakobson, M. E. 1971 Life and death in an island population of house mouse. Exp. Gerontol. 6, 187. (doi:10.1016/S0531-5565(71)80018-9)
38. Berry, R. J. & Bronson, F. H. 1992 Life-history and bioeconomy of the house mouse. Biol. Rev. 67, 519-550. (doi:10.1111/j.1469-185X.1992.tb01192.x)
39. Gosling, L. M., Roberts, S. C., Thornton, E. A. & Andrew, M. J. 2000 Life history costs of olfactory status signalling in mice. Behav. Ecol. Sociobiol. 48, 328-332. (doi:10.1007/s002650000242)
40. Radwan, J. et al. 2006 Metabolic costs of sexual advertisement in the bank vole (Clethrionomys glareolus). Evol. Ecol. Res. 8, 859-869.
41. Zala, S. M., Potts, W. K. & Penn, D. J. 2008 Exposing males to female scent increases the cost of controlling Salmonella infection in wild house mice. Behav. Ecol. Sociobiol. 62, 895-900. (doi:10.1007/s00265-007-0513-0)
42. Hurst, J. L. 1987 The functions of urine marking in a free-living population of house mice, Mus domesticus Rutty. Anim. Behav. 35, 1433-1442. (doi:10.1016/S0003-3472(87)80016-7)
43. Palanza, P., Re, L., Mainardi, D., Brain, P. F. & Parmigiani, S. 1996 Male and female competitive strategies of wild house mice pairs (Mus musculus domesticus) confronted with intruders of different sex and age in artificial territories. Behaviour 133, 863-882. (doi:10.1163/ 156853996X00288)
44. Hurst, J. L. & Beynon, R. J. 2004 Scent wars: the chemobiology of competitive signalling in mice. Bioessays 26, 1288-1298. (doi:10.1002/bies.20147)
45. Beynon, R. J. & Hurst, J. L. 2004 Urinary proteins and the modulation of chemical scents in mice and rats. Peptides 25, 1553-1563. (doi:10.1016/j.peptides.2003.12.025)
46. Cheetham, S. A., Smith, A. L., Armstrong, S. D., Beynon, R. J. & Hurst, J. L. 2009 Limited variation in the major urinary proteins of laboratory mice. Physiol. Behav. 96, 253-261. (doi:10.1016/j.physbeh.2008.10.005)
47. Johnson, M. S., Thomson, S. C. & Speakman, J. R. 2001 Limits to sustained energy intake. I. Lactation in the laboratory mouse Mus musculus. J. Exp. Biol. 204, 1925-1935.
48. Williams, E. & Scott, J. P. 1953 The development of social behavior patterns in the mouse, in relation to natural periods. Behaviour 6, 35-65. (doi:10.1163/ 156853954X00031)
49. Anderson, M. E. 1996 Measurement of antioxidants: glutathione. In Free radicals, a practical approach (eds N. A. Punchard & F. J. Kelly), pp. 213-226. Oxford, UK: Oxford University Press.
50. Vasilaki, A., Mansouri, A., Van Remmen, H., Van der Meulen, J. H., Larkin, L., Richardson, A. G., McArdle, A., Faulkner, J. A. & Jackson, M. J. 2006 Free radical generation by skeletal muscle of adult and old mice: effect of contractile activity. Aging Cell 5, 109-117. (doi:10.1111/j.1474-9726.2006.00198.x)
51. Di Monte, D., Bellomo, G., Thor, H., Nicotera, P. & Orrenius, S. 1984 Menadione-induced cyto-toxicity is associated with protein thiol oxidation and alteration in intracellular Ca-2{thorn} homeostasis. Arch. Biochem. Biophys. 235, 343-350
52. Fukunaga, K., Suzuki, T. & Takama, K. 1993 Highly sensitive high-performance liquid-chromatography for the measurement of malondialdehyde in biological samples. J. Chromatogr.-Biomed. Appl. 621, 77-81
53. Millar, J. S. 1978 Energetics of reproduction in Peromyscus leucopus: cost of lactation. Ecology 59, 1055-1061. (doi:10.2307/1938558)
54. Hammond, K. A., Konarzewski, M., Torres, R. M. & Diamond, J. 1994 Metabolic ceilings under a combination of peak energy demands. Physiol. Zool. 67, 1479-1506.
55. Sikes, R. S. 1995 Costs of lactation and optimal litter size in northern grasshopper mice (Onychomys leucogaster). J. Mammal. 76, 348-357. (doi:10.2307/1382346)
56. Williamson, D. H. 1980 Integration of metabolism in tissues of the lactating rat. FEBS Lett. 117, K93-K105. (doi:10.1016/0014-5793(80)80574-6)
57. Canas, R., Romero, J. J. & Baldwin, R. L. 1982 Maintenance energy-requirements during lactation in rats. J. Nutr. 112, 1876-1880
58. Harper, J. M. 2008 Wild-derived mouse stocks: an underappreciated tool for aging research. Age 30, 135-145. (doi:10.1007/s11357-008-9057-0)
59. Cretegny, C. & Genoud, M. 2006 Rate of metabolism during lactation in small terrestrial mammals (Crocidura russula, Mus domesticus and Microtus arvalis). Comp. Biochem. Physiol. A-Mol. Integr. Physiol. 144, 125-134. (doi:10.1016/j.cbpa.2005.10.030)
60. Yu, B. P. 1994 Cellular defenses against damage from reactive oxygen species. Physiol. Rev. 74, 139-162.
61. Andziak, B., O'Connor, T. P., Qi, W. B., DeWaal, E. M., Pierce, A., Chaudhuri, A. R., Van Remmen, H. & Buffenstein, R. 2006 High oxidative damage levels in the longest-living rodent, the naked mole-rat. Aging Cell 5, 463-471. (doi:10.1111/j.1474-9726.2006.00237.x)
62. Ghezzi, P. 2005 Oxidoreduction of protein thiols in redox regulation. Biochem. Soc. Trans. 33, 1378-1381
63. Kim, J. R., Yoon, H.W., Kwon, K. S., Lee, S. R. & Rhee, S. G. 2000 Identification of proteins containing cysteine residues that are sensitive to oxidation by hydrogen peroxide at neutral pH. Anal. Biochem. 283, 214-221. (doi:10.1006/abio.2000.4623)
64. Eaton, P. 2006 Protein thiol oxidation in health and disease: techniques for measuring disulfides and related modifications in complex protein mixtures. Free Radic. Biol. Med. 40, 1889-1899. (doi:10.1016/j.freeradbiomed. 2005.12.037)
65. Drent, R. H. & Daan, S. 1980 The prudent parent: energetic adjustments in avian breeding. Ardea 68, 225-252
66. Hayes, J. P., Garland, T. & Dohm, M. R. 1992 Individual variation in metabolism and reproduction of Mus: are energetics and life-history linked? Funct. Ecol. 6, 5-14. (doi:10.2307/2389765)
67. Bronson, F. H. 1979 Reproductive ecology of the house mouse. Q. Rev. Biol. 54, 265-299. (doi:10.1086/ 411295)
68. Sahin, E. & Gumuslu, S. 2007 Stress-dependent induction of protein oxidation, lipid peroxidation and antioxidants in peripheral tissues of rats: comparison of three stress models (immobilization, cold and immobilization- cold). Clin. Exp. Pharmacol. Physiol. 34, 425-431. (doi:10.1111/j.1440-1681.2007.04584.x)
69. Gandelman, R. 1972 Mice: postpartum aggression elicited by the presence of an intruder. Horm. Behav. 3, 23-28.
70. Svare, B. & Gandelman, R. 1973 Postpartum aggression in mice: experiential and environmental factors. Horm. Behav. 4, 323-334. (doi:10.1016/0018-506X (73)90032-9)
71. Nussey, D. H., Pemberton, J. M., Pilkington, J. G. & Blount, J. D. 2009 Life history correlates of oxidative damage in a free-living mammal population. Funct. Ecol. 23, 809-817. (doi:10.1111/j.1365-2435.2009. 01555.x)
72. Ricklefs, R. E. & Cadena, C. D. 2007 Lifespan is unrelated to investment in reproduction in populations of mammals and birds in captivity. Ecol. Lett. 10, 867-872. (doi:10.1111/j.1461-0248.2007.01085.x)
73. Speakman, J. R. & Krol, E. In press. The heat dissipation limit theory and evolution of life histories in endotherms: time to dispose of the disposable soma theory? Integr. Comp. Biol. (doi:10.1093/icb/icq049)