Oxidative status and social dominance in a wild cooperative breeder

Functional Ecology

Volumn 29, Issue 2, 2015, Pages 229-238

  Cram, Dominic L ^a,b   Blount, Jonathan D ^a   Young, Andrew J ^a  

^a UNIVERSITY OF EXETER   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Plocepasser mahali; Animal societies; Antioxidants; Cooperative breeding; Oxidative status; Oxidative stress; Reproductive skew; Social dominance; Social rank

Indexed keywords

ANTIOXIDANT; BREEDING SEASON; COOPERATIVE BEHAVIOR; DOMINANCE; LIFE HISTORY TRAIT; OXIDATION; PASSERINE; REPRODUCTIVE EFFORT; WILD POPULATION;

SOUTH AFRICA;

ANIMALIA; AVES; PLOCEPASSER MAHALI;

EID: 85028145974     PISSN: 02698463     EISSN: 13652435     Source Type: Journal    
DOI: 10.1111/1365-2435.12317     Document Type: Article

References (89)

1. Aamodt, R.M. (2009) Age-and caste-dependent decrease in expression of genes maintaining DNA and RNA quality and mitochondrial integrity in the honeybee wing muscle. Experimental Gerontology, 44, 586-593.
2. Alonso-Alvarez, C. & Ferrer, M. (2001) A biochemical study of fasting, subfeeding, and recovery processes in yellow-legged gulls. Physiological and Biochemical Zoology, 74, 703-713.
3. Arnold, K.E. & Owens, I.P.F. (1999) Cooperative breeding in birds: the role of ecology. Behavioral Ecology, 10, 465.
4. de Ayala, R.M., Martinelli, R. & Saino, N. (2006) Vitamin E supplementation enhances growth and condition of nestling barn swallows (Hirundo rustica). Behavioral Ecology and Sociobiology, 60, 619-630.
5. Barja, G. (2007) Mitochondrial oxygen consumption and reactive oxygen species production are independently modulated: implications for aging studies. Rejuvenation Research, 10, 215-224.
6. Beauchamp, G.U.Y. (1998) The effect of group size on mean food intake rate in birds. Biological Reviews, 73, 449-472.
7. Beaulieu, M., Reichert, S., Le Maho, Y., Ancel, A. & Criscuolo, F. (2011) Oxidative status and telomere length in a long-lived bird facing a costly reproductive event. Functional Ecology, 25, 577-585.
8. Beckman, K.B. & Ames, B.N. (1998) The free radical theory of aging matures. Physiological Reviews, 78, 547-581.
9. Bergeron, P., Careau, V., Humphries, M.M., Reale, D., Speakman, J.R. & Garant, D. (2011) The energetic and oxidative costs of reproduction in a free-ranging rodent. Functional Ecology, 25, 1063-1071.
10. Bertrand, S., Alonso-Alvarez, C., Devevey, G., Faivre, B., Prost, J. & Sorci, G. (2006) Carotenoids modulate the trade-off between egg production and resistance to oxidative stress in zebra finches. Oecologia, 147, 576-584.
11. Bize, P., Devevey, G., Monaghan, P., Doligez, B. & Christe, P. (2008) Fecundity and survival in relation to resistance to oxidative stress in a free-living bird. Ecology, 89, 2584-2593.
12. Blount, J.D., Houston, D.C. & Møller, A.P. (2000) Why egg yolk is yellow. Trends in Ecology & Evolution, 15, 47-49.
13. Blount, J.D., Metcalfe, N.B., Arnold, K.E., Surai, P.F., Devevey, G.L. & Monaghan, P. (2003) Neonatal nutrition, adult antioxidant defences and sexual attractiveness in the zebra finch. Proceedings of the Royal Society of London. Series B: Biological Sciences, 270, 1691-1696.
14. Blount, J.D., Houston, D.C., Surai, P.F. & Møller, A.P. (2004) Egg-laying capacity is limited by carotenoid pigment availability in wild gulls Larus fuscus. Proceedings of the Royal Society of London. Series B: Biological Sciences, 271, S79-S81.
15. Carey, J. (2001) Demographic mechanisms for the evolution of long life in social insects. Experimental Gerontology, 36, 713-722.
16. Catoni, C., Peters, A. & Martin Schaefer, H. (2008) Life history trade-offs are influenced by the diversity, availability and interactions of dietary antioxidants. Animal Behaviour, 76, 1107-1119.
17. Clutton-Brock, T.H., Hodge, S.J., Spong, G., Russell, A.F., Jordan, N.R., Bennett, N.C. et al. (2006) Intrasexual competition and sexual selection in cooperative mammals. Nature, 444, 1065-1068.
18. Cohen, A., Hau, M. & Wikelski, M. (2008) Stress, metabolism, and antioxidants in two wild passerine bird species. Physiological and Biochemical Zoology, 81, 463-472.
19. Cohen, A., Klasing, K. & Ricklefs, R. (2007) Measuring circulating antioxidants in wild birds. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 147, 110-121.
20. Cohen, A.A. & McGraw, K.J. (2009) No simple measures for antioxidant status in birds: complexity in inter-and intraspecific correlations among circulating antioxidant types. Functional Ecology, 23, 310-320.
21. Cohen, A.A., McGraw, K.J. & Robinson, W.D. (2009) Serum antioxidant levels in wild birds vary in relation to diet, season, life history strategy, and species. Oecologia, 161, 673-683.
22. Costantini, D. (2008) Oxidative stress in ecology and evolution: lessons from avian studies. Ecology Letters, 11, 1238-1251.
23. Costantini, D., Marasco, V. & Møller, A.P. (2011) A meta-analysis of glucocorticoids as modulators of oxidative stress in vertebrates. Journal of Comparative Physiology B, 181, 447-456.
24. Costantini, D. & Møller, A.P. (2009) Does immune response cause oxidative stress in birds? A meta-analysis. Comparative Biochemistry and Physiology, Part A: Molecular & Integrative Physiology, 153, 339-344.
25. Costantini, D. & Verhulst, S. (2009) Does high antioxidant capacity indicate low oxidative stress? Functional Ecology, 23, 506-509.
26. Costantini, D., Carere, C., Caramaschi, D. & Koolhaas, J.M. (2008) Aggressive and non-aggressive personalities differ in oxidative status in selected line of mice (Mus musculus). Biology Letters, 4, 119-122.
27. Côté, I.M. & Poulin, R. (1995) Parasitism and group size in social animals: a meta-analysis. Behavioral Ecology, 6, 159-165.
28. Cram, D., Blount, J. & Young, A. (2014) Data from: oxidative status and social dominance in a wild cooperative breeder. Dryad Digital Repository, http://dx.doi.org/10.5061/dryad.ss1d1
29. Crawley, M. (2007) The R Book. John Wiley and Sons, Chichester, UK.
30. Creel, S. (2001) Social dominance and stress hormones. Trends in Ecology & Evolution, 16, 491-497.
31. Crick, H.Q.P. (1992) Load-lightening in cooperatively breeding birds and the cost of reproduction. Ibis, 134, 56-61.
32. van de Crommenacker, J., Komdeur, J. & Richardson, D.S. (2011) Assessing the cost of helping: the roles of body condition and oxidative balance in the Seychelles warbler (Acrocephalus sechellensis). PLoS One, 6, e26423.
33. van de Crommenacker, J., Komdeur, J., Burke, T. & Richardson, D.S. (2011) Spatio-temporal variation in territory quality and oxidative status: a natural experiment in the Seychelles warbler (Acrocephalus sechellensis). Journal of Animal Ecology, 80, 668-680.
34. van de Crommenacker, J., Richardson, D.S., Koltz, A.M., Hutchings, K. & Komdeur, J. (2012) Parasitic infection and oxidative status are associated and vary with breeding activity in the Seychelles warbler. Proceedings of the Royal Society B: Biological Sciences, 279, 1466-1476.
35. Dammann, P. & Burda, H. (2006) Sexual activity and reproduction delay ageing in a mammal. Current Biology, 16, 117-118.
36. Dowling, D.K. & Simmons, L.W. (2009) Reactive oxygen species as universal constraints in life-history evolution. Proceedings of the Royal Society B: Biological Sciences, 276, 1737-1745.
37. Dröge, W. (2002) Free radicals in the physiological control of cell function. Physiological Reviews, 82, 47-95.
38. Finkel, T. & Holbrook, N.J. (2000) Oxidants, oxidative stress and the biology of ageing. Nature, 408, 239-247.
39. Fletcher, Q.E., Selman, C., Boutin, S., McAdam, A.G., Woods, S.B., Seo, A.Y. et al. (2013) Oxidative damage increases with reproductive energy expenditure and is reduced by food supplementation. Evolution, 67, 1527-1536.
40. Franco, R., Schoneveld, O., Georgakilas, A.G. & Panayiotidis, M.I. (2008) Oxidative stress, DNA methylation and carcinogenesis. Cancer Letters, 266, 6-11.
41. Garratt, M., McArdle, F., Stockley, P., Vasilaki, A., Beynon, R.J., Jackson, M.J. et al. (2012) Tissue-dependent changes in oxidative damage with male reproductive effort in house mice. Functional Ecology, 26, 423-433.
42. Haddad, L.S., Kelbert, L. & Hulbert, A. (2007) Extended longevity of queen honey bees compared to workers is associated with peroxidation-resistant membranes. Experimental Gerontology, 42, 601-609.
43. Halliwell, B. & Gutteridge, J. (2007) Free Radicals in Biology and Medicine, 4th edn. Oxford University Press, Oxford, UK.
44. Hardeland, R., Coto-Montes, A. & Poeggeler, B. (2003) Circadian rhythms, oxidative stress, and antioxidative defense mechanisms. Chronobiology International, 20, 921-962.
45. Harrison, X.A., York, J.E., Cram, D.L. & Young, A.J. (2013a) Extra-group mating increases inbreeding risk in a cooperatively breeding bird. Molecular Ecology, 22, 5700-5715.
46. Harrison, X.A., York, J.E., Cram, D.L., Hares, M.C. & Young, A.J. (2013b) Complete reproductive skew within white-browed sparrow weaver groups despite outbreeding opportunities for subordinates of both sexes. Behavioral Ecology and Sociobiology, 67, 1915-1929.
47. Heinsohn, R.G. (2004) Parental care, load-lightening, and costs. Ecology and Evolution of Cooperative Breeding in Birds (eds W.D. Koenig & J.L. Dickinson ), pp. 67-80. Cambridge University Press, Cambridge, UK.
48. Heiss, R.S. & Schoech, S.J. (2012) Oxidative cost of reproduction is sex specific and correlated with reproductive effort in a cooperatively breeding bird, the Florida scrub jay. Physiological and Biochemical Zoology, 85, 499-503.
49. Hodge, S. (2009) Understanding variation in reproductive skew: directions for future empirical research. Reproductive Skew in Vertebrates: Proximate and Ultimate Causes (eds R. Hager & C. Jones ), pp. 439-466. Cambridge University Press, Cambridge, UK.
50. Hõrak, P. & Cohen, A. (2010) How to measure oxidative stress in an ecological context: methodological and statistical issues. Functional Ecology, 24, 960-970.
51. Keller, L. & Reeve, H.K. (1994) Partitioning of reproduction in animal societies. Trends in Ecology & Evolution, 9, 98-102.
52. Kilgas, P., Tilgar, V., Külavee, R., Saks, L., Hõrak, P. & Mänd, R. (2010) Antioxidant protection, immune function and growth of nestling great tits Parus major in relation to within-brood hierarchy. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 157, 288-293.
53. Koenig, W.D., Shen, S.-F., Krakauer, A.H. & Haydock, J. (2009) Reproductive skew in avian societies. Reproductive Skew in Vertebrates: Proximate and Ultimate Causes (eds R. Hager & C. Jones ), pp. 227-264. Cambridge University Press, Cambridge, UK.
54. Leitner, S., Mundy, P. & Voigt, C. (2009) Morphometrics of white-browed sparrow-weavers Plocepasser mahali in south western Zimbabwe. Ostrich, 80, 99-102.
55. Lessells, C. & Boag, P.T. (1987) Unrepeatable repeatabilities: a common mistake. The Auk, 104, 116-121.
56. Lewis, D.M. (1981) Determinants of reproductive success of the white-browed sparrow weaver, Plocepasser mahali. Behavioral Ecology and Sociobiology, 9, 83-93.
57. Lewis, D.M. (1982) Cooperative breeding in a population of White Browed Sparrow Weavers Plocepasser mahali. Ibis, 124, 511-522.
58. Lin, M.T. & Beal, M.F. (2006) Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature, 443, 787-795.
59. Magrath, R., Johnstone, R. & Heinsohn, R. (2004) Reproductive skew. Ecology and Evolution of Cooperative Breeding in Birds (eds W. Koenig & J. Dickinson ), pp. 157-176. Cambridge University Press, Cambridge, UK.
60. Mass, V., Heistermann, M. & Kappeler, P.M. (2009) Mate-guarding as a male reproductive tactic in Propithecus verreauxi. International Journal of Primatology, 30, 389-409.
61. 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. Functional Ecology, 24, 984-996.
62. Møller, A., Merino, S., Brown, C. & Robertson, R. (2001) Immune defense and host sociality: a comparative study of swallows and martins. The American Naturalist, 158, 136-145.
63. Monaghan, P., Metcalfe, N.B. & Torres, R. (2009) Oxidative stress as a mediator of life history trade-offs: mechanisms, measurements and interpretation. Ecology Letters, 12, 75-92.
64. Monaghan, P., Charmantier, A., Nussey, D. & Ricklefs, R. (2008) The evolutionary ecology of senescence. Functional Ecology, 22, 371-378.
65. 2 from generalized linear mixed-effects models. Methods in Ecology and Evolution, 4, 133-142.
66. 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. Functional Ecology, 23, 809-817.
67. Olsson, M., Healey, M., Perrin, C., Wilson, M. & Tobler, M. (2012) Sex-specific SOD levels and DNA damage in painted dragon lizards (Ctenophorus pictus). Oecologia, 170, 917-924.
68. Parkes, T.L., Elia, A.J., Dickinson, D., Hilliker, A.J., Phillips, J.P. & Boulianne, G.L. (1998) Extension of Drosophila lifespan by overexpression of human SOD1 in motorneurons. Nature Genetics, 19, 171-174.
69. Patel, S.A., Velingkaar, N.S. & Kondratov, R.V. (2014) Transcriptional control of the antioxidant defense by the circadian clock. Antioxidants & Redox Signaling, 20, 2997-3006.
70. Peig, J. & Green, A.J. (2009) New perspectives for estimating body condition from mass/length data: the scaled mass index as an alternative method. Oikos, 118, 1883-1891.
71. Pike, T.W., Blount, J.D., Lindstrom, J. & Metcalfe, N.B. (2007) Dietary carotenoid availability influences a male's ability to provide parental care. Behavioral Ecology, 18, 1100-1105.
72. R Development Core Team. (2013) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.
73. Radak, Z., Chung, H.Y., Koltai, E., Taylor, A.W. & Goto, S. (2008) Exercise, oxidative stress and hormesis. Ageing Research Reviews, 7, 34-42.
74. Rammal, H., Bouayed, J. & Soulimani, R. (2010) A direct relationship between aggressive behavior in the resident/intruder test and cell oxidative status in adult male mice. European Journal of Pharmacology, 627, 173-176.
75. Saino, N., Caprioli, M., Romano, M., Boncoraglio, G., Rubolini, D., Ambrosini, R. et al. (2011) Antioxidant defenses predict long-term survival in a passerine bird. PLoS One, 6, e19593.
76. Sapolsky, R.M. (2005) The influence of social hierarchy on primate health. Science, 308, 648-652.
77. Selman, C., Blount, J.D., Nussey, D.H. & Speakman, J.R. (2012) Oxidative damage, ageing, and life-history evolution: where now? Trends in Ecology & Evolution, 27, 570-577.
78. Stier, A., Reichert, S., Massemin, S., Bize, P. & Criscuolo, F. (2012) Constraint and cost of oxidative stress on reproduction: correlative evidence in laboratory mice and review of the literature. Frontiers in Zoology, 9, 1-11.
79. Veskoukis, A.S., Nikolaidis, M.G., Kyparos, A. & Kouretas, D. (2009) Blood reflects tissue oxidative stress depending on biomarker and tissue studied. Free Radical Biology and Medicine, 47, 1371-1374.
80. Vitousek, M.N., Stewart, R.A. & Safran, R.J. (2013) Female plumage colour influences seasonal oxidative damage and testosterone profiles in a songbird. Biology Letters, 9, 20130539.
81. Voigt, C., Leitner, S. & Gahr, M. (2006) Repertoire and structure of duet and solo songs in cooperatively breeding white-browed sparrow weavers. Behaviour, 143, 159-182.
82. Wasser, S.K. & Barash, D.P. (1983) Reproductive suppression among female mammals - implications for biomedicine and sexual selection theory. Quarterly Review of Biology, 58, 513-538.
83. Wiersma, P., Selman, C., Speakman, J.R. & Verhulst, S. (2004) Birds sacrifice oxidative protection for reproduction. Proceedings of the Royal Society B: Biological Sciences, 271, S360-S363.
84. Wingfield, J.C. & Lewis, D.M. (1991) Hormonal and behavioural responses to simulated territorial intrusion in the cooperatively breeding white-browed sparrow weaver, Plocepasser mahali. Animal Behaviour, 45, 1-11.
85. York, J.E. (2012) The evolution and regulation of dawn song performance in white-browed sparrow weaver societies. PhD thesis, University of Bristol, Bristol, UK.
86. York, J.E., Young, A.J. & Radford, A.N. (2014) Singing in the moonlight: dawn song performance of a diurnal bird varies with lunar phase. Biology Letters, 10, 20130970.
87. Young, A.J. & Monfort, S.L. (2009) Stress and the costs of extra-territorial movement in a social carnivore. Biology Letters, 5, 439-441.
88. Young, A.J., Spong, G. & Clutton-Brock, T. (2007) Subordinate male meerkats prospect for extra-group paternity: alternative reproductive tactics in a cooperative mammal. Proceedings of the Royal Society B: Biological Sciences, 274, 1603-1609.
89. Young, A.J., Carlson, A.A., Monfort, S.L., Russell, A.F., Bennett, N.C. & Clutton-Brock, T. (2006) Stress and the suppression of subordinate reproduction in cooperatively breeding meerkats. Proceedings of the National Academy of Sciences, USA, 103, 12005-12010.