Oxidative stress and the evolution of sex differences in life span and ageing in the decorated cricket, Gryllodes sigillatus

Evolution

Volumn 67, Issue 3, 2013, Pages 620-634

  Archer, Catharine R ^a   Sakaluk, Scott K ^b   Selman, Colin ^c   Royle, Nick J ^a   Hunt, John ^a  

^a UNIVERSITY OF EXETER   (United Kingdom)

^b ILLINOIS STATE UNIVERSITY   (United States)

^c UNIVERSITY OF ABERDEEN   (United Kingdom)

Author keywords

Age dependent reproductive effort; Ageing; Life span; Oxidative damage; Protein oxidation; Reactive oxygen species; Sexual selection; Total antioxidant capacity

Indexed keywords

ANTIOXIDANT;

AGING POPULATION; ANTIOXIDANT; CRICKET; ENVIRONMENTAL STRESS; FECUNDITY; GENETIC VARIATION; LIFE HISTORY TRAIT; OXIDATION; PROTEIN; REPRODUCTIVE EFFORT; SEX-RELATED DIFFERENCE; SEXUAL SELECTION; TRADE-OFF;

ANIMAL; ARTICLE; EVOLUTION; FEMALE; GENETICS; GRYLLIDAE; LONGEVITY; MALE; METABOLISM; OXIDATIVE STRESS; SEXUAL DEVELOPMENT;

ANIMALS; ANTIOXIDANTS; BIOLOGICAL EVOLUTION; FEMALE; GRYLLIDAE; LONGEVITY; MALE; OXIDATIVE STRESS; SEX CHARACTERISTICS;

GRYLLODES SIGILLATUS;

EID: 84874748802     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/j.1558-5646.2012.01805.x     Document Type: Article

References (121)

1. Ali, S. S., C. Xiong, J. Lucero, M. M. Behrens, L. L. Dugan, and K. L. Quick 2006. Gender differences in free radical homeostasis during aging: shorter-lived female C57BL6 mice have increased oxidative stress. Aging Cell 5:565-574.
2. Alonso-Alvarez, C., S. Bertrand, G. Devevey, J. Prost, B. Faivre, and G. Sorci 2004. Increased susceptibility to oxidative stress as a proximate cost of reproduction. Ecol. Lett. 7:363-368.
3. Archer, C. R., F. Zajitschek, S. K. Sakaluk, N. J. Royle, J. C. Hunt Sexual selection affects the evolution of lifespan and ageing in the decorated cricket Gryllodes sigillatus. Evolution: In press doi:10.1111/j.1558-5646.2012.01673x
4. Arking, R., V. Burde, K. Graves, R. Hari, E. Feldman, A. Zeevi, S. Soliman, A. Saraiya, S. Buck, J. Vettraino, et al. 2000. Forward and reverse selection for longevity in Drosophila is characterized by alteration of antioxidant gene expression and oxidative damage patterns. Exp. Geront. 35:167-185.
5. Barja, G. 2007. Mitochondrial oxygen consumption and reactive oxygen species production are independently modulated: implications for aging studies. Rejuvenation Res. 10:215-224.
6. Barnes, A. I., and L. Partridge 2003. Costing reproduction. Anim. Behav. 66:199-204.
7. Becker, W. A. 1984. Manual of quantitative genetics. 4th ed. Academic Enterprises, Washington State University, Washington, DC
8. Beckman, K. B., and B. N. Ames 1998. The free radical theory of aging matures. Physiol. Rev. 78: 547-581.
9. Bentsen, C. L., J. Hunt, M. D. Jennions, and R. Brooks 2006. Complex multivariate sexual selection on male acoustic signaling in a wild population of Teleogryllus commodus. Am. Nat. 167:E102-E116.
10. Bertrand, S., C. Alonso-Alvarez, G. Devevey, B. Faivre, J. Prost, and G. Sorci 2006. Carotenoids modulate the trade-off between egg production and resistance to oxidative stress in zebra finches. Oecologia 147:576-584.
11. Blount, J. D., N. B. Metcalfe, T. R. Birkhead, and P. F. Surai 2003. Carotenoid modulation of immune function and sexual attractiveness in zebra finches. Science 300:125-127.
12. Bonduriansky, R., and S. F. Chenoweth 2009. Intralocus sexual conflict. Trends Ecol. Evol. 24:280-288.
13. Bonduriansky, R., A. Maklakov, F. Zajitschek, and R. Brooks 2008. Sexual selection, sexual conflict and the evolution of ageing and life span. Funct. Ecol. 22:443-453.
14. Borrás, C., J. Sastre, D. García-Sala, A. Lloret, F. V. Pallardó, and J. Viña 2003. Mitochondria from females exhibit higher antioxidant gene expression and lower oxidative damage than males. Free Radic. Biol. Med. 34:546-552.
15. Borrás, C., J. Gambini, and J. Viña 2007. Mitochondrial oxidant generation is involved in determining why females live longer than males. Front Biosci. 12:1008-1013.
16. Bradford, M. M. 1976. A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248-254.
17. Buttemer, W. A., D. Abele, and D. Costantini 2010. From bivalves to birds: oxidative stress and longevity. Funct. Ecol. 24:971-983.
18. Cabreiro, F., D. Ackerman, R. Doonan, C. Araiz, P. Back, D. Papp, B. P. Braeckman, and D. Gems 2011. Increased lifespan from over-expression of superoxide dismutase in C. elegans is not caused by decreased oxidative damage. Free Rad. Biol. Med. 51:1575-1582.
19. Caple, F., E. A. Williams, A. Spiers, J. Tyson, B. Burtle, A. K. Daly, J. C. Mathers, and J. E. Hesketh 2010. Inter-individual variation in DNA damage and base excision repair in young, healthy non-smokers: effects of dietary supplementation and genotype. Br. J. Nutr. 103:1585-1593.
20. Charlesworth, B. 1994. Evolution in Age-structured Populations. Vol. 2. Cambridge Univ. Press, Cambridge, U.K
21. Christe, P., O. Glaizot, N. Strepparava, G. Devevey, and L. Fumagalli 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. R. Soc. Lond. B. 279:1142-1149.
22. Clifford, C. W., and J. P. Woodring 1986. The effects of virginity and ovariectomy on growth, food consumption, fat body mass and oxygen consumption in the house cricket, Acheta domesticus. J. Insect Physiol. 32:425-427.
23. Clutton-Brock, T. H., and K. Isvaran 2007. Sex differences in ageing in natural populations of vertebrates. Proc. R. Soc. Lond. B. 274:3097-3104.
24. Cohen, A. A., K. J. McGraw, and W. D. Robinson 2009. Serum antioxidant levels in wild birds vary in relation to diet, season, life history strategy and species. Oecologia 161:673-683.
25. Comfort, A. 1979. The biology of senescence. 3rd ed. Churchill Livingstone, Edinburgh.
26. Costantini, D. 2008. Oxidative stress in ecology and evolution: lessons from avian studies. Ecol. Lett. 11:1238-1251.
27. Costantini, D., and A. P Möller 2009. Does immune response cause oxidative stress in birds? A meta-analysis. Comp. Biochem. Physiol. A 153:339-344.
28. Costantini, D., and S. Verhulst 2009. Does high antioxidant capacity indicate low oxidative stress Funct. Ecol. 23:506-509.
29. Costantini, D., S. Casagrande, S. De Filippis, G. Brambilla, A. Fanfani, J. Tagliavini, and G. Dell'Omo 2006. Correlates of oxidative stress in wild kestrel nestlings (Falco tinnunculus). J. Comp. Physiol. [B] 176:329-337.
30. Curtsinger, J. W., and A. A. Khazaeli 2002. Lifespan, QTLs, age-specificity, and pleiotropy in Drosophila. Mech. Ageing Dev. 123:81-93.
31. D'Autreaux, B., and M. B. Toledano 2007. ROS as signalling molecules: mechanisms that generate specificity in ROS homeostasis. Nat. Rev. Mol. Cell Biol. 8:813-824.
32. Dalle-Donne, I., R. Rossi, D. Giustarini, A. Milzani, and R. Colombo 2003. Protein carbonyl groups as biomarkers of oxidative stress. Clinica Chimica Acta 329:23-38.
33. David, J. R., L. O. Araripe, B. C. Bitner-Mathe, P. Capy, B. Goñi, L. B. Klaczko, H. Legout, M. B. Martins, J. Vouidibio, A. Yassin, et al. 2005. Quantitative trait analysis and geographic variability of natural populations of Zaprionus indianus, a recent invader in Brazil. Heredity 96: 53-62.
34. Desikan, R., A. H. Soheila, J. T. Hancock, and S. J. Neill 2001. Regulation of the Arabidopsis transcriptome by oxidative stress. Plant Physiol. 127:159-172.
35. Dickinson, B. C, and C. J. Chang 2011. Chemistry and biology of reactive oxygen species in signalling or stress responses. Nat. Chem. Biol. 7:504-511.
36. Doonan, R., J. J. McElwee, F. Matthijssens, G. A. Walker, K. Houthoofd, P. Back, A. Matscheski, J. R. Vanfleteren, and D. Gems 2008. Against the oxidative damage theory of aging: superoxide dismutases protect against oxidative stress but have little or no effect on life span in Caenorhabditis elegans. Genes Dev. 22:3236-3241.
37. Dowling, D. K., and L. W. Simmons 2009. Reactive oxygen species as universal constraints in life-history evolution. Proc. R. Soc. Lond. B 276:1737-1745.
38. Ernsting, G., and J. A. Isaaks 1991. Accelerated ageing: a cost of reproduction in the Carabid beetle Notiophilus biguttatus F. Funct. Ecol. 5:299-303.
39. Falconer, D. S., and T. F. C. Mackay 1996. Introduction to quantitative genetics. Longman, Essex
40. Finch, C. E. 1990. Senescence and the Genome. Univ. of Chicago Press, Chicago, IL.
41. Finkel, T., and N. J. Holbrook 2000. Oxidants, oxidative stress and the biology of ageing. Nature 408:239-247.
42. Fleming, J. E., J. Miquel, S. F. Cottrell, L. S. Yengoyan, and A. C. Economos 1982. Is cell aging caused by respiration-dependent injury to the mitochondrial genome Gerontology 28:44-53.
43. Galtier, N., R. W Jobson, B. Nabholz, S. Glémin, and P. U. Blier 2009. Mitochondrial whims: metabolic rate, longevity and the rate of molecular evolution. Biol. Lett. 5:413-416.
44. Graves, B. 2007. Sexual selection effects on the evolution of senescence. Evol. Ecol. 21:663-668.
45. Hack, M. A. 1998. The energetics of male mating strategies in field crickets (Orthoptera: Gryllinae: Gryllidae). J. Insect Behav. 11:853-867.
46. Harman, D. 1956. A theory based on free radical and radiation chemistry. J. Gerontol. 11:298-300.
47. Harman, D. 1972. The biologic clock: the mitochondria J. Am. Geriatr. Soc. 20:145-147.
48. Harman, D. 1992. Free radical theory of aging. Mutat Res. 275:257-266.
49. Harshman, L. G, and B. A. Haberer 2000. Oxidative stress resistance a robust correlated response to selection in extended longevity lines of Drosophila melanogaster J. Geront. (A Biol. Med. Sci.) 55:B415-B417.
50. Head, M. L., J. Hunt, M. D. Jennions, and R. Brooks 2005. The indirect benefits of mating with attractive males outweigh the direct costs. PLoS Biol. 3:e33.
51. Hoffmann, A. A., and P. A. Parsons 1988. The analysis of quantitative variation in natural populations with isofemale strains. Genet. Sel. Evol. 20:87-98.
52. Hughes, K. A., and R. M. Reynolds 2005. Evolutionary and mechanistic theories of aging. Annu. Rev. Entomol. 50:421-445.
53. Hulbert, A. J., R. Pamplona, R. Buffenstein, and W. A. Buttemer 2007. Life and death: metabolic rate, membrane composition, and life span of animals. Physiol. Rev. 87:1175-1213.
54. Hunt, J., R. Brooks, M. D. Jennions, M. J. Smith, C. L. Bentsen, and L. F. Bussiere 2004. High-quality male field crickets invest heavily in sexual display but die young. Nature 432:1024-1027.
55. Hunt, J., M. D. Jennions, N. Spyrou, and R. Brooks 2006. Artificial selection on male longevity influences age-dependent reproductive effort in the black field cricket Teleogryllus commodus. Am. Nat. 168:E72-E86.
56. Ide, T., H. Tsutsui, N. Ohashi, S. Hayashidani, N. Suematsu, M. Tsuchihashi, H. Tamai, and A. Takeshita 2002. Greater oxidative stress in healthy young men compared with premenopausal women. Arterioscler. Thromb. Vasc. Biol. 22:438-442.
57. Isaksson, C., B. C. Sheldon, and T. Uller 2011. The challenges of integrating oxidative stress into life-history biology. BioScience 61:194-202.
58. Jacot, A., H. Scheuber, B. Holzer, O. Otti, and M. W. G. Brinkhof 2008. Diel variation in a dynamic sexual display and its association with female mate-searching behaviour. Proc. R. Soc. Lond. B 275:579-585.
59. Jang, Y. C., and H. V. Remmen 2009. The mitochondrial theory of aging: insight from transgenic and knockout mouse models. Exp. Geront. 44:256-260.
60. Jedlička, P., J. Cvačka, and K. Sláma 2009. Juvenile hormone-stimulated synthesis of acyl-glycerols and vitamin E in female accessory sexual glands of the fire bug, Pyrrhocoris apterus L. Arch. Insect Biochem. Physiol. 72:48-59.
61. Judge, K. A., J. J. Ting, and D. T. Gwynne 2008. Condition dependence of male life span and calling effort in a field cricket. Evolution 62:868-878.
62. Kaneko, T., S. Tahara, and M. Matsuo 1997. Retarding effect of dietary restriction on the accumulation of 8-hydroxy-2'-deoxyguanosine in organs of Fischer 344 rats during aging. Free Rad. Biol. Med. 23:76-81.
63. Kasapoglu, M., and T. Özben 2001. Alterations of antioxidant enzymes and oxidative stress markers in aging. Exp. Geront. 36:209-220.
64. Kavanagh, M. W. 1987. The efficiency of sound production in two cricket species, Gryllotalpa australis and Teleogryllus commodus (Orthoptera: Grylloidea). J. Exp. Biol. 130:107-119.
65. Kokko, H. 1997. Evolutionarily stable strategies of age-dependent sexual advertisement. Behav. Ecol. Sociobiol. 41:99-107.
66. Lambert, A. J., H. M. Boysen, J. A. Buckingham, T. Yang, A. Podlutsky, S. N. Austad, T. H. Kunz, R. Buffenstein, and M. D. Brand 2007. Low rates of hydrogen peroxide production by isolated heart mitochondria associate with long maximum lifespan in vertebrate homeotherms. Aging Cell 6:607-618.
67. Lessells, C. K. 2008. Neuroendocrine control of life histories: what do we need to know to understand the evolution of phenotypic plasticity Phil. Trans. R. Soc. Lond. B 363:1589-1598.
68. Levine, R. L., D. Garland, C. N. Oliver, A. Amici, I. Climent, A. G. Lenz, B. W. Ahn, S. Shaltiel, and E. R. Stadtman 1990. Determination of carbonyl content in oxidatively modified proteins. Methods Enzymol. 186:464-478.
69. Lewis, Z., N. Wedell, and J. Hunt 2011. Evidence for strong intralocus sexual conflict in the Indian meal moth, Plodia interpunctella. Evolution 65:2085-2097.
70. Lin, M. T., and M. F. Beal 2006. Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature 443:787-795.
71. Losdat, S., H. Richner, J. D. Blount, and F. Helfenstein 2011. Immune activation reduces sperm quality in the great tit. PloS One 6:e22221.
72. Magwere, T., M. West, K. Riyahi, M. P. Murphy, R. A. J. Smith, and L. Partridge 2006. The effects of exogenous antioxidants on lifespan and oxidative stress resistance in Drosophila melanogaster. Mech. Ageing Dev. 127:356-370.
73. McNamara, J. M., and K. L. Buchanan 2005. Stress, resource allocation, and mortality. Behav. Ecol. 16:1008-1017.
74. Medawar, P. B. 1946. Old age and natural death. Modern Quart. 1:17-43.
75. Medawar, P. B. 1952. An unsolved problem of biology. HK Lewis, London
76. Mehrad, B., and M. Sudagar 2010. Dietary vitamin E requirement, fish performance and reproduction of guppy (Poecilia reticulata). AACL Bioflux 3:239-246.
77. Mittler, R. 2002. Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci. 7:405-410.
78. Monaghan, P., N. B. Metcalfe, and R. Torres 2009. Oxidative stress as a mediator of life history trade-offs: mechanisms, measurements and interpretation. Ecol. Lett. 12:75-92.
79. Morales, J., A. Velando, and J. Moreno 2008. Pigment allocation to eggs decreases plasma antioxidants in a songbird. Behav. Ecol. Sociobiol. 63:227-233.
80. Mysterud, A., R. Langvatn, and N. C. Stenseth 2004. Patterns of reproductive effort in male ungulates. J. Zool. 264:209-215.
81. Ogilvy, V., R. F. Preziosi, and A. L. Fidgett 2012. A brighter future for frogs? The influence of carotenoids on the health, development and reproductive success of the red-eye tree frog. Anim. Conserv. DOI: 10.1111/j.1469-1795.2012.00536.
82. Okada, K., W. R. Pitchers, M. D. Sharma, J. Hunt, and D. J. Hosken 2011. Longevity, calling effort, and metabolic rate in two populations of cricket. Behav. Ecol. Sociobiol. 65:1-6.
83. Pal, S., S. J. Polyak, N. Bano, W. C. Qiu, R. L. Carithers, M. Shuhart, D. R Gretch, and A. Das 2010. Hepatitis C virus induces oxidative stress, DNA damage and modulates the DNA repair enzyme NEIL1. J. Gastroen. Hepatol. 25:627-634.
84. Partridge, L. 2010. The new biology of ageing. Phil. Trans. R. Soc. Lond. B 365:147-154.
85. Partridge, L., and D. Gems 2006. Beyond the evolutionary theory of ageing, from functional genomics to evo-gero. Trends Ecol. Evol. 21:334-340.
86. Pérez, V. I., A. Bokov, H. V. Remmen, J. Mele, Q. Ran, Y. Ikeno, and A. Richardson 2009. Is the oxidative stress theory of aging dead? BBA-Gen. Subjects. 1790:1005-1014.
87. Pike, T. W., J. D. Blount, J. Lindström, and N. B. Metcalfe 2007. Availability of non-carotenoid antioxidants affects the expression of a carotenoid-based sexual ornament. Biol. Lett. 3:353-356.
88. Pletcher, S. D., A. A. Khazaeli, and J. W. Curtsinger 2000. Why do life spans differ? Partitioning mean longevity differences in terms of age-specific mortality parameters. J. Gerontol (A Biol. Med. Sci.) 55:B381-B389.
89. Promislow, D. E. L. 1992. Costs of sexual selection in natural populations of mammals. Proc. R. Soc. Lond. B 247:203-210.
90. Promislow, D. E. L. 2003. Mate choice, sexual conflict, and evolution of senescence. Behav. Genet. 33:191-201.
91. Promislow, D. E. L., and P. H. Harvey 1990. Living fast and dying young: a comparative analysis of life-history variation among mammals. J. Zool. 220:417-437.
92. Radák, Z., R. Takahashi, A. Kumiyama, H. Nakamoto, H. Ohno, T. Ookawara, and S. Goto 2002. Effect of aging and late onset dietary restriction on antioxidant enzymes and proteasome activities, and protein carbonylation of rat skeletal muscle and tendon. Exp. Geront. 37:1423-1430.
93. Ristow, M., K. Zarse, A. Oberbach, N. Klöting, M. Birringer, M. Kiehntopf, M. Stumvoll, C. R. Kahn, and M. Blüher 2009. Antioxidants prevent health-promoting effects of physical exercise in humans. Proc. Natl. Acad. Sci. USA 106:8665-8670.
94. Robert, K. A., and A. M. Bronikowski 2010. Evolution of senescence in nature: physiological evolution in populations of garter snake with divergent life histories. Am. Nat. 175:147-159.
95. Robert, K. A, A. Brunet-Rossinni, and A. M Bronikowski 2007. Testing the "free radical theory of aging" hypothesis: physiological differences in long-lived and short-lived colubrid snakes. Aging Cell 6:395-404.
96. Rodríguez-Muňoz, R., A. Bretman, J. Slate, C. A. Walling, and T. Tregenza 2010. Natural and sexual selection in a wild insect population. Science 328:1269-1272.
97. Roff, D. A. 1993. The evolution of life histories: theory and analysis. Chapman and Hall, New York.
98. Roff, D. A., and R. Preziosi 1994. The estimation of the genetic correlation: the use of the jackknife. Heredity 73:544-548.
99. Rose, M. R. 1991. Evolutionary theory of aging. Oxford Univ. Press, Oxford, U.K.
100. Schulz, T. J., K. Zarse, A. Voigt, N. Urban, M. Birringer, and M. Ristow 2007. Glucose restriction extends Caenorhabditis elegans life span by inducing mitochondrial respiration and increasing oxidative stress. Cell Metab. 6:280-293.
101. Seyahooei, M. A., J. J. M. Van Aalphen, and K. Kraaijeveld 2011. Metabolic rate affects adult life span independently of developmental rate in parasitoid wasps. Biol. J. Linn. Soc. 103:45-56.
102. Sohal, R. S., S. Agarwal, A. Dubey, and W. C. Orr 1993a. Protein oxidative damage is associated with life expectancy of houseflies. Proc. Natl. Acad. Sci. USA 90:7255-7259.
103. Sohal, R. S., H. H. Ku, and S. Agarwal 1993b. Biochemical correlates of longevity in two closely related rodent species. Biochem. Biophys. Res. Commun. 196:7-11.
104. Sohal, R. S., S. Agarwal, and B. H. Sohal 1995. Oxidative stress and aging in the Mongolian gerbil (Meriones unguiculatus). Mech. Ageing Dev. 81:15-25.
105. Sohal, R. S., R. J. Mockett, and W. C. Orr 2002. Mechanisms of aging: an appraisal of the oxidative stress hypothesis. Free Rad. Biol. Med. 33:575-586.
106. Speakman, J. R., and C. Selman 2011. The free radical damage theory: accumulating evidence against a simple link of oxidative stress to ageing and lifespan. Bio. Essays 33:255-259.
107. Speakman, J. R., D. A. Talbot, C. Selman, S. Snart, J. S. McLaren, P. Redman, E. Krol, D. M. Jackson, M. S. Johnson, and M. D. Brand 2004. Uncoupled and surviving: individual mice with high metabolism have greater mitochondrial uncoupling and live longer. Aging Cell 3:87-95.
108. Stadtman, E. R. 1992. Protein oxidation and aging. Science 257:1220-1224.
109. Stearns, S. 1992. The evolution of life histories. Oxford Univ. Press, Oxford, U.K.
110. Tabachnick, B. G., and L. S. Fidell 1989. Using multivariate statistics. Harper and Row. New York
111. Tapia, P. C. 2006. Sublethal mitochondrial stress with an attendant stoichiometric augmentation of reactive oxygen species may precipitate many of the beneficial alterations in cellular physiology produced by caloric restriction, intermittent fasting, exercise and dietary phytonutrients. Med. Hypotheses 66:832-843.
112. Trivers, R. 1972. Parental investment and sexual selection. Pp. 136-179 in B. Campbell, ed. Sexual selection and the descent of man 1871-1971. Aldine, Chicago, IL
113. Tyson, J., F. Caple, A. Spiers, B. Burtle, A. K. Daly, E. A. Williams, J. E. Hesketh, and J. C. Mathers 2010. Inter-individual variation in nucleotide excision repair in young adults: effects of age, adiposity, micronutrient supplementation and genotype. Br. J. Nutr. 101:1316-1323.
114. Viña, J., J. Sastre, F. Pallardó, and C. Borrás 2003. Mitochondrial theory of aging: importance to explain why females live longer than males. Antioxid. Redox Signal. 5:549-556.
115. Wang, Y., D. Pot, S. D. Kachman, S. V. Nuzhdin, and L. G. Harshman 2006. A quantitative trait locus analysis of natural genetic variation for Drosophila melanogaster oxidative stress survival. J. Hered. 97:355-366.
116. Wiersma, P., C. Selman, J. R. Speakman, and S. Verhulst 2004. Birds sacrifice oxidative protection for reproduction. Proc. R. Soc. Lond. B 271:S360-S363.
117. Williams, G. C. 1957. Pleiotropy, natural selection, and the evolution of senescence. Evolution 11:398-411.
118. Yearsley, J. M., I. Kyriazakis, I. J. Gordon, S. L. Johnston, J. R. Speakman, B. J. Tolkamp, and A. W. Illius 2005. A life history model of somatic damage associated with resource acquisition: damage protection or prevention J. Theor. Biol. 235:305-317.
119. Zajitschek F., J. Hunt, S. R. K. Zajitschek, M. D. Jennions, and R. Brooks 2007. No intra-locus sexual conflict over reproductive fitness or ageing in field crickets. PLoS One 2:e155.
120. Zar, J. H. 1999. Biostatistical analysis. Prentice Hall, NJ
121. Zeng, X., F. Wang, X. Fan, W. Yang, B. Zhou, P. Li, Y. Yin, G. Wu, and J. Wang 2008. Dietary arginine supplementation during early pregnancy enhances embryonic survival in rats. J. Nutr. 138:1421-1425.