The level of an intracellular antioxidant during development determines the adult phenotype in a bird species: A potential organizer role for glutathione

American Naturalist

Volumn 185, Issue 3, 2015, Pages 390-405

  Romero Haro, Ana Angela ^a   Alonso Alvarez, Carlos ^a,b  

^a UNIVERSITY OF CASTILLA LA MANCHA   (Spain)

^b MUSEO NACIONAL DE CIENCIAS NATURALES   (Spain)

Author keywords

Antioxidants; Carotenoids; Early development; Hormesis; Oxidative stress; Zebra finches

Indexed keywords

ADULT; ANTIOXIDANT; CAROTENOID; LIFE HISTORY TRAIT; PHENOTYPE; RESOURCE AVAILABILITY; SONGBIRD; TRADE-OFF;

AVES; TAENIOPYGIA GUTTATA;

ANTIOXIDANT; BUTHIONINE SULFOXIMINE; GLUTATHIONE;

ANIMAL; BLOOD; BODY WEIGHT; DRUG EFFECTS; ERYTHROCYTE; FEMALE; GROWTH, DEVELOPMENT AND AGING; MALE; METABOLISM; OXIDATIVE STRESS; PHENOTYPE; PHYSIOLOGY; PIGMENTATION; SEXUAL DEVELOPMENT; SIGNAL TRANSDUCTION; SONGBIRD;

ANIMALS; ANTIOXIDANTS; BODY WEIGHT; BUTHIONINE SULFOXIMINE; ERYTHROCYTES; FEMALE; GLUTATHIONE; MALE; OXIDATIVE STRESS; PHENOTYPE; PIGMENTATION; SEX CHARACTERISTICS; SIGNAL TRANSDUCTION; SONGBIRDS;

EID: 84922742153     PISSN: 00030147     EISSN: None     Source Type: Journal    
DOI: 10.1086/679613     Document Type: Article

References (120)

1. Adkins-Regan, E., and M. Tomaszycki. 2007. Monogamy on the fast track. Biology Letters 3:617-619.
2. Agarwal, R., and S. D. Chase. 2002. Rapid, fluorimetric-liquid chromatographic determination of malondialdehyde in biological samples. Journal of Chromatography B 775:121-126.
3. Alonso-Alvarez, C., S. Bertrand, G. Devevey, J. Prost, B. Faivre, O. Chastel, and G. Sorci. 2006. An experimental manipulation of lifehistory trajectories and resistance to oxidative stress. Evolution 60: 1913-1924.
4. Alonso-Alvarez, C., S. Bertrand, B. Faivre, and G. Sorci. 2007. Increased susceptibility to oxidative damage as a cost of accelerated somatic growth in zebra finches. Functional Ecology 21:873-879.
5. Alonso-Alvarez, C., and I. Galván. 2011. Free radical exposure creates paler carotenoid-based ornaments: a possible interaction in the expression of black and red traits. PLoS ONE 6:e19403.
6. Alonso-Alvarez, C., L. Pérez-Rodríguez, R. Mateo, O. Chastel, and J. Viñuela. 2008. The oxidation handicap hypothesis and the carotenoid allocation trade-off. Journal of Evolutionary Biology 21: 1789-1797.
7. Alonso-Alvarez, C., and A. Velando. 2012. Benefits and costs of parental care. Pages 40-61 in N. J. Royle, P. T. Smiseth, and M. Kolliker, eds. The evolution of parental care. Oxford University Press, Oxford.
8. Barnes, A. I., and L. Partridge. 2003. Costing reproduction. Animal Behaviour 66:199-204.
9. Braendle, C., A. Heyland, and T. Flatt. 2011. Integrating mechanistic and evolutionary analysis of life history variation. Pages 3-10 in T. Flatt and A. Heyland, eds. Mechanisms of life history evolution. Oxford University Press, Oxford.
10. Burley, N. 1986. Sexual selection for aesthetic traits in species with biparental care. American Naturalist 127:415-445.
11. Chen, J. H., M. S. Martin-Gronert, J. Tarry-Adkins, and S. E. Ozanne. 2009. Maternal protein restriction affects postnatal growth and the expression of key proteins involved in lifespan regulation in mice. PLoS ONE 4:e4950.
12. Chung, T. K., M. A. Funk, and D. H. Baker. 1990. L-2-oxothiazolidine-4-carboxylate as a cysteine precursor: efficacy for growth and hepatic glutathione synthesis in chicks and rats. Journal of Nutrition 120:158-165.
13. Cohen, A., K. Klasing, and R. Ricklefs. 2007. Measuring circulating antioxidants in wild birds. Comparative Biochemistry and Physiology B 147:110-121.
14. Cohen, A., L. B. Martin, J. C. Wingfield, S. R. McWilliams, and J. A. Dunne. 2012. Physiological regulatory networks: ecological roles and evolutionary constraints. Trends in Ecology and Evolution 27: 428-435.
15. Cohen, J. 1992. A power primer. Psychological Bulletin 112:155-159.
16. Costantini, D. 2011. On the measurement of circulating antioxidant capacity and the nightmare of uric acid. Methods in Ecology and Evolution 2:321-325.
17. Costantini, D. 2014. Oxidative stress and hormesis in evolutionary ecology and physiology. Springer, Berlin.
18. Costantini, D., N. B. Metcalfe, and P. Monaghan. 2010. Ecological processes in a hormetic framework. Ecology Letters 13:1435-1447.
19. Cotgreave, I. A., and R. G. Gerdes. 1998. Recent trends in glutathione biochemistry-glutathione-protein interactions: A molecular link between oxidative stress and cell proliferation? Biochemical and Biophysical Research Communications 242:1-9.
20. Dalle-Donne, I., R. Rossi, G. Colombo, D. Giustarini, and A. Milzani. 2009. Protein S-glutathionylation: a regulatory device from bacteria to humans. Trends in Biochemical Sciences 34:85-96.
21. De Jong, G., and A. J. Van Noordwijk. 1992. Acquisition and allocation of resources: Genetic (co)variances, selections and life histories. American Naturalist 139:749-770.
22. De Quiroga, G. B., M. Lopez-Torres, R. Perez-Campo, M. Abelenda, M. P. Nava, and M. L. Puerta. 1991. Effect of cold-acclimation on GSH, antioxidant enzymes and lipid-peroxidation in brown adipose-tissue. Biochemical Journal 277:289-292.
23. Del Vesco, A. P., E. Gasparino, D. O. Grieser, V. Zancanela, F. R. Gasparin, J. Constantin, and A. R. Oliveira Neto. 2014. Effects of methionine supplementation on the redox state of acute heat stress-exposed quails. Journal of Animal Science 92:806-815.
24. Dennery, P. A. 2010. Oxidative stress in development: Nature or nurture? Free Radical Biology and Medicine 49:1147-1151.
25. Dowling, D. K., and L. W. Simmons. 2009. Reactive oxygen species as universal constraints in life-history evolution. Proceedings of the Royal Society B: Biological Sciences 276:1737-1745.
26. Dunn, A. M., and R. A. Zann. 1996. Undirected song in wild zebra finch flocks: Contexts and effects of mate removal. Ethology 102: 529-539.
27. Enkvetchakul, B., and W. G. Bottje. 1995. Influence of diethyl maleate and cysteine on tissue glutathione and growth in broiler-chickens. Poultry Science 74:864-873.
28. Feoli, A. M., I. Siqueira, L. M. V. Almeida, A. C. Tramontina, C. Battu, S. T. Wofchuk, C. Gottfried, M. L. Perry, and C. A. Goncalves. 2006. Brain glutathione content and glutamate uptake are reduced in rats exposed to preand postnatal protein malnutrition. Journal of Nutrition 136:2357-2361.
29. Fetoui, H., A. Mahjoubi-Samet, K. Jamoussi, F. Ayadi, F. Ellouze, and N. Zeghal. 2007. Food restriction in pregnant and lactating rats induces anemia and increases plasma lipid peroxidation in their progeny. Nutrition Research 27:788-793.
30. Foley, J. D., and A. Van Dam. 1984. Fundamentals of interactive computer graphics. Addison-Wesley, Reading, MA.
31. Franz, M., and M. Goller. 2003. Respiratory patterns and oxygen consumption in singing zebra finches. Journal of Experimental Biology 206:967-978.
32. Galván, I., and C. Alonso-Alvarez. 2008. An intracellular antioxidant determines the expression of a melanin-based signal in a bird. PLoS ONE 3:e3335.
33. Galván, I., and C. Alonso-Alvarez. 2009. The expression of melanin-based plumage is separately modulated by exogenous oxidative stress and a melanocortin. Proceedings of the Royal Society B: Biological Sciences 276:3089-3097.
34. Galvani, P., P. Fumagalli, and A. Santagostino. 1998. Glutathione depletion by xenobiotics in Coturnix coturnix japonica. Bulletin of Environmental Contamination and Toxicology 60:909-915.
35. García-de Blas, E., R. Mateo, F. J. Guzmán Bernardo, R. C. Rodríguez Martín-Doimeadios, and C. Alonso-Alvarez. 2014. Astaxanthin and papilioerythrinone in the skin of birds: A chromatic convergence of two metabolic routes with different precursors? Naturwissenschaften 101:407-416.
36. Gerisch, B., and A. Antebi. 2011. Molecular basis of life history regulation in C. elegans and other organisms. Pages 284-298 in T. Flatt and A. Heyland, eds. Mechanisms of life history evolution. Oxford University Press, Oxford.
37. Ghezzi, P. 2013. Protein glutathionylation in health and disease. Biochimica et Biophysica Acta 1830:3165-3172.
38. Ghezzi, P., and P. Di Simplicio. 2009. Protein glutathiolation. Pages 123-142 in C. Jacob and P. G. Winyard, eds. Redox signaling and regulation in biology and medicine. Wiley, Weinheim.
39. Gibbs, P. 2008. An introduction to generalized linear mixed models using SAS PROC GLIMMIX. SAS Technical Support, University of California at Riverside, Riverside, CA.
40. Godwin, J., J. A. Luckenbach, and R. J. Borski. 2003. Ecology meets endocrinology: Environmental sex determination in fishes. Evolution and Development 5:40-49.
41. Gore, A. C. 2008. Developmental programming and endocrine disruptor effects on reproductive neuroendocrine systems. Frontiers in Neuroendocrinology 29:358-374.
42. Griffith, O. W. 1980. Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinilpiridine. Analytical Biochemistry 106:207-212.
43. Griffith, O. W. 1982. Mechanism of action, metabolism, and toxicity of buthionine sulfoximine and its higher homologs, potent inhibitors of glutathione synthesis. Journal of Biological Chemistry 257: 13704-13712.
44. Hales, C. N., and D. J. Barker. 1992. Type 2 (non-insulin-dependent) diabetes mellitus: The thrifty phenotype hypothesis. Diabetologia 35:595-601.
45. Halliwell, B., and J. M. C. Gutteridge. 2007. Free radicals in biology and medicine. 4th ed. Oxford University Press, Oxford.
46. Hasselquist, D., and J. A. Nilsson. 2012. Physiological mechanisms mediating costs of immune responses: What can we learn from studies of birds? Animal Behaviour 83:1303-1312.
47. Hernández-García, D., C. D. Wood, S. Castro-Obregón, and L. Covarrubias. 2010. Reactive oxygen species: A radical role in development? Free Radical Biology and Medicine 49:130-143.
48. Hõrak, P., E. Sild, U. Soomets, T. Sepp, and K. Kilk. 2010. Oxidative stress and information content of black and yellow plumage coloration: An experiment with greenfinches. Journal of Experimental Biology 213:2225-2233.
49. Houston, D. C., D. Donnan, and P. J. Jones. 1995a. Use of labelled methionine to investigate the contribution of muscle protein to egg production in zebra finches. Journal of Comparative Physiology B 165:161-164.
50. Houston, D. C., D. Donnan, P. J. Jones, I. Hamilton, and D. Osborne. 1995b. Changes in the muscle condition of female zebra finches Poephila guttata during egg-laying and the role of protein storage in bird skeletal-muscle. Ibis 137:322-332.
51. Isaksson, C. 2013. Opposing effects on glutathione and reactive oxygen metabolites of sex habitat, and spring date, but no effect of increased breeding density in great tits (Parus major). Ecology and Evolution 3:2730-2738.
52. Isaksson, C., B. C. Sheldon, and T. Uller. 2011. The challenges of integrating oxidative stress into life-history biology. Bioscience 61: 194-202.
53. Jahoor, F., L. J. Wykes, P. J. Reeds, J. F. Henry, M. P. del Rosario, and M. E. Frazer. 1995. Protein-deficient pigs cannot maintain reduced glutathione homeostasis when subjected to the stress of inflammation. Journal of Nutrition 125:1462-1472.
54. Jenni-Eiermann, S., and L. Jenni. 1994. Plasma metabolite levels predict individual body mass changes in a small long-distance migrant, the garden warbler. Auk 111:888-899.
55. Johnson, J. D., and G. E. Hill. 2013. Is carotenoid ornamentation linked to the inner mitochondria membrane potential? a hypothesis for the maintenance of signal honesty. Biochimie 95:436-444.
56. Jones, D. 2006. Redefining oxidative stress. Antioxidants and Redox Signaling 8:1865-1879.
57. Kiani, A., and M. O. Nielsen. 2011. Metabolic programming: origin of non-communicable diseases in early life nutrition. International Journal of Endocrinology and Metabolism 9:409-415.
58. Kim, Y., Y. B. Song, T. Y. Kim, I. Kim, S. J. Han, Y. Ahn, S. H. Cho, et al. 2010. Redox regulation of the tumor suppressor PTEN by glutathione. FEBS Letters 584:3550-3556.
59. Kirkwood, T. B. L., and S. N. Austad. 2000. Why do we age? Nature 408:233-238.
60. Leggatt, R. A., C. J. Brauner, P. M. Schulte, and G. K. Iwama. 2007. Effects of acclimation and incubation temperature on the glutathione antioxidant system in killifish and RTH-149 cells. Comparative Biochemistry and Physiology A 146:317-326.
61. Leroi, A. 2001. Molecular signals versus the Loi de Balancement. Trends in Ecology and Evolution 16:24-29.
62. Lessells, C. K. M. 2008. Neuroendocrine control of life histories: what do we need to know to understand the evolution of phenotypic plasticity? Philosophical Transactions of the Royal Society B: Biological Sciences 363:1589-1598.
63. Levin, B. E. 2006. Metabolic imprinting: Critical impact of the perinatal environment on the regulation of energy homeostasis. Philosophical Transactions of the Royal Society B: Biological Sciences 361:1107-1121.
64. Lin, Y. C., G. D. Huang, C. W. Hsieh, and B. S. Wung. 2012. The glutathionylation of p65 modulates NF-kB activity in 15-deoxyd(1)(2), (1)(4)-prostaglandin J(2)-treated endothelial cells. Free Radical Biology and Medicine 52:1844-1853.
65. Lind, J., S. Jakobsson, and C. Kullberg. 2010. Impaired predator evasion in the life history of birds: behavioral and physiological adaptations to reduced flight ability. Pages 1-30 in C. F. Thompson, ed. Current ornithology. Springer, Berlin.
66. Littell, R. C., G. A. Milliken, W. W. Stroup, R. D. Wolfinger, and O. Schabenberger. 2006. SAS system for mixed models. SAS Institute, Cary, NC.
67. López-Torres, M., and G. Barja. 2008. Lowered methionine ingestion as responsible for the decrease in rodent mitochondrial oxidative stress in protein and dietary restriction possible implications for humans. Biochimica et Biophysica Acta 1780:1337-1347.
68. Lu, S. C. 2013. Glutathione synthesis. Biochimica et Biophysica Acta 1830:3143-3153.
69. Luo, Z. C., W. D. Fraser, P. Julien, C. L. Deal, F. Audibert, G. N. Smith, X. Xiong, and M. Walker. 2006. Tracing the origins of “fetal origins” of adult diseases: programming by oxidative stress? Medical Hypotheses 66:38-44.
70. Mandin, C., and F. Vézina. 2012. Daily variation in markers of nutritional condition in wintering black-capped chickadees Poecile atricapillus. Ibis 1859:791-802.
71. Marchionatti, A., A. Alisio, G. Díaz de Barboza, V. Baudino, and N. Tolosa de Talamoni. 2001. DL-Buthionine-S,R-sulfoximine affects intestinal alkaline phosphatase activity. Comparative Biochemistry and Physiology C 129:85-91.
72. Markovic, J., J. L. García-Gimenez, A. Gimeno, J. Viña, and F. V. Pallardó. 2010. Role of glutathione in cell nucleus. Free Radical Research 44:721-733.
73. Mårtensson, J., A. Jain, E. Stole, W. Frayer, P. A. Auld, and A. Meister. 1991. Inhibition of glutathione synthesis in the newborn rat: A model for endogenously produced oxidative stress. Proceedings of the National Academy of Sciences of the USA 88:9360-9364.
74. Martin, L. B., A. L. Liebl, J. H. Trotter, C. L. Richards, K. McCoy, and M. W. McCoy. 2011. Integrator networks: Illuminating the black box linking genotype and phenotype. Integrative and Comparative Biology 51:514-527.
75. McArdle, H. J., H. S. Andersen, H. Jones, and L. Gambling. 2006. Fetal programming: causes and consequences as revealed by studies of dietary manipulation in rats: A review. Placenta 27(suppl.):S56S60.
76. McGraw, K. J. 2006. Mechanics of carotenoid-based coloration. Pages 177-242 in G. E. Hill and K.J. McGraw, eds. Bird coloration: mechanisms and measurements. Harvard University Press, Cambridge, MA.
77. McGraw, K. J., and M. B. Toomey. 2010. Carotenoid accumulation in the tissues of zebra finches: predictors of integumentary pigmentation and implications for carotenoid allocation strategies. Physiological and Biochemical Zoology 83:97-109.
78. McMillen, I. C., and J. S. Robinson. 2005. Developmental origins of the metabolic syndrome: Prediction, plasticity, and programming. Physiological Reviews 85:571-633.
79. Metcalfe, N. B., and C. Alonso-Alvarez. 2010. Oxidative stress as a life-history constraint: The role of reactive oxygen species in shaping phenotypes from conception to death. Functional Ecology 24: 984-996.
80. Metcalfe, N. B., and P. Monaghan. 2001. Compensation for a bad start: Grow now, pay later? Trends in Ecology and Evolution 16: 254-260.
81. Miller, N. J., C. A. Rice-Evans, M. J. Davies, V. Gopinathan, and A. Milner. 1993. A novel method for measuring antioxidant capacity and its application to monitoring the antioxidant status in premature neonates. Clinical Science 84:407-412.
82. Monaghan, P., N. B. Metcalfe, and R. Torres. 2009. Oxidative stress as a mediator of life history trade-offs: mechanisms, measurements and interpretation. Ecology Letters 12:75-92.
83. Németh, K., M. Mézes, T. Gaál, A. Bartos, K. Balogh, and F. Husvéth. 2004. Effect of supplementation with methionine and different fat sources on the glutathione redox system of growing chickens. Acta Veterinaria Hungarica 52:369-378.
84. Nussey, D. H., J. M. Pemberton, J. G. Pilkington, and J. D. Blount. 2009. Life history correlates of oxidative damage in a freeliving mammal population. Functional Ecology 23:809-817.
85. Nuyt, M. A., and B. T. Alexander. 2009. Developmental programming and hypertension. Current Opinion in Nephrology and Hypertension 18:144-152.
86. Owen, J., and D. Butterfield. 2010. Measurement of oxidized/reduced glutathione ratio. Pages 269-277 in P. Bross and N. Gregersen, eds. Methods in molecular biology. Vol. 648. Protein misfolding and cellular stress in diseases and aging: concepts and protocols. Springer, New York.
87. Partadiredja, G., S. Worrall, and K. S. Bedi. 2009. Early life undernutrition alters the level of reduced glutathione but not the activity levels of reactive oxygen species enzymes or lipid peroxidation in the mouse forebrain. Brain Research 1285:22-29.
88. Pérez, E. C., J. E. Elie, C. O. Soulage, H. A. Soula, N. Mathevon, and C. Vignal. 2012. The acoustic expression of stress in a songbird: Does corticosterone drive isolation-induced modifications of zebra finch calls? Hormones and Behavior 61:573-581.
89. Pike, T. W., and M. Petrie. 2003. Potential mechanisms of avian sex manipulation. Biological Reviews 78:553-574.
90. Reid, M., A. Badaloo, T. Forrester, J. F. Morlese, M. Frazer, W. C. Heird, and J. Jahoor. 2000. In vivo rates of erythrocyte glutathione synthesis in children with severe protein-energy malnutrition. American Journal of Physiology Endocrinology and Metabolism 278:E405-E412.
91. Remage-Healey, L., E. Adkins-Regan, and L. M. Romero. 2003. Behavioral and adrenocortical responses to mate separation and reunion in the zebra finch. Hormones and Behavior 43:108-114.
92. Rinaudo, P., and E. Wang. 2012. Fetal programming and metabolic syndrome. Annual Review of Physiology 74:107-130.
93. Roff, D. A. 2011. Genomic insights into life history evolution. Pages 11-25 in T. Flatt and A. Heyland, eds. Mechanisms of life history evolution. Oxford University Press, Oxford.
94. Rojas, R. R., and R. A. Leopold. 1996. Chilling injury in the housefly: Evidence for the role of oxidative stress between pupariation and emergence. Cryobiology 33:447-458.
95. Romero-Haro, A. A., and C. Alonso-Alvarez. 2014a. Covariation in oxidative stress markers in the blood of nestling and adult birds. Physiological and Biochemical Zoology 87:353-362.
96. Romero-Haro, A. A., and C. Alonso-Alvarez. 2014b. Data from: The level of an intracellular antioxidant during development determines the adult phenotype in a bird species: A potential organizer role for glutathione. American Naturalist, Dryad Digital Repository, http://dx.doi.org/10.5061/dryad.1rd58.
97. Round, P. D., B. Hansson, D. J. Pearson, P. R. Kennerley, and S. Bensch. 2007. Lost and found: The enigmatic large-billed reed warbler Acrocephalus orinus rediscovered after 139 years. Journal of Avian Biology 38:133-138.
98. Rozman, J., D. Runciman, and R. A. Zann. 2003. Seasonal variation in body mass and fat of zebra finches in south-eastern Australia. Emu 103:11-19.
99. Schielzeth, H., and W. Forstmeier. 2009. Conclusions beyond support: overconfident estimates in mixed models. Behavioral Ecology 20:416-420.
100. Simons, M. J. P., M. Briga, E. Koetsier, R. Folkertsma, M. D. Wubs, C. Dijkstra, and S. Verhuslt. 2012. Bill redness is positively associated with reproduction and survival in male and female zebra finches. PLoS ONE 7:e40721.
101. Sohal, R. S., and W. C. Orr. 2012. The redox stress hypothesis of aging. Free Radical Biology and Medicine 52:539-555.
102. Speakman, J. R., and M. Garratt. 2013. Oxidative stress as a cost of reproduction: Beyond the simplistic trade-off model. Bioessays 36: 93-106.
103. Stearns, S. C. 2011. Does impressive progress on understanding mechanisms advance life history theory? Pages 365-674 in T. Flatt and A. Heyland, eds. Mechanisms of life history evolution. Oxford University Press, Oxford.
104. Swennen, Q., P.-A. Geraert, Y. Mercier, N. Everaert, A. Stinckens, H. Willemsen, Y. Li, P. Decuypere, and J. Buyse. 2011. Effects of dietary protein content and 2-hydroxy-4-methylthiobutanoic acid or DLmethionine supplementation on performance and oxidative status of broiler chickens. British Journal of Nutrition 106:1845-1854.
105. Tarry-Adkins, J. L., J. A. Joles, J. H. Chen, M. S. Martin-Gronert, D. M. van der Giezen, R. Goldschmeding, C. N. Hales, and S. E. Ozanne. 2007. Protein restriction in lactation confers nephroprotective effects in the male rat and is associated with increased antioxidant expression. American Journal of Physiology 293: R1259-R1266.
106. Tarry-Adkins, J. L., J. H. Chen, N. S. Smith, R. H. Jones, H. Cherif, and S. E. Ozanne. 2009. Poor maternal nutrition followed by accelerated postnatal growth leads to telomere shortening and increased markers of cell senescence in rat islets. FASEB Journal 23:1521-1528.
107. Thomas, R. J. 2002. The costs of singing in nightingales. Animal Behaviour 63:959-966.
108. Thomas, R. J., I. C. Cuthill, A. R. Goldsmith, D. F. Cosgrove, H. C. Lidgate, and S. L. B. Proctor. 2003. The trade-off between singing and mass gain in a daytime-singing bird, the European robin. Behaviour 140:387-404.
109. Thompson, L. P., and Y. Al-Hasan. 2012. Impact of oxidative stress in fetal programming. Journal of Pregnancy 2012:582748.
110. Velando, A., R. Beamonte-Barrientos, and R. Torres. 2014. Enhanced male coloration after immune challenge increases reproductive potential. Journal of Evolutionary Biology 27:1582-1589.
111. Völker, O. 1957. Die experimentelle rotfärbung des Gefieders beim Fichtenkreuzschnabel (Loxia curvirostra). Journal of Ornithology 98:210-214.
112. Warner, M. J., and S. E. Ozanne. 2010. Mechanisms involved in the developmental programming of adulthood disease. Biochemical Journal 427:333-347.
113. Wells, J. C. K. 2007. The thrifty phenotype as an adaptive maternal effect. Biological Reviews 82:143-172.
114. West-Eberhard, M. J. 2003. Developmental plasticity and evolution. Oxford University Press, New York.
115. Włostowski, T., K. Dmowski, and E. Bonda-Ostaszewska. 2010. Cadmium accumulation, metallothionein and glutathione levels, and histopathological changes in the kidneys and liver of magpie (Pica pica) from a zinc smelter area. Ecotoxicology 19:1066-1073.
116. Woods, H. A., and J. K. Wilson. 2013. An information hypothesis for the evolution of homeostasis. Trends in Ecology and Evolution 28:283-289.
117. Wu, G., Y. Fang, S. Yang, J. R. Lupton, and N. D. Turner. 2004. Glutathione metabolism and its implications for health. Journal of Nutrition 134:489-492.
118. Zann, R. A. 1996. Zebra finch: A synthesis of field and laboratory studies. Oxford University Press, Oxford.
119. Zera, A. J., and L. G. Harshman. 2001. The physiology of life history trade-offs in animals. Annual Review of Ecology and Systematics 32:95-126.
120. Zhang, H., and H. J. Forman. 2012. Glutathione synthesis and its role in redox signaling. Seminars in Cell and Developmental Biology 23:722-728.