Behavioral Ecology and Sociobiology

, Volume 67, Issue 12, pp 1891–1901 | Cite as

Ostrich chick humoral immune responses and growth rate are predicted by parental immune responses and paternal colouration

  • Maud Bonato
  • Matthew R. Evans
  • Dennis Hasselquist
  • Richard B. Sherley
  • Schalk W. P. Cloete
  • Michael I. Cherry
Original Paper

Abstract

One of the most important measures of offspring performance is growth rate, which is often traded off against another important survival trait, immune function. A particular feature of ostrich chicks maintained in farmed environments is that cohorts of chicks vary widely in size. As parents can have a profound effect on the phenotype and fitness of their offspring, we investigated whether chick growth and immune defence were related to variation in levels of immune defence in their genetic parents. As secondary sexual traits of sires could serve as indicators of male quality, and be used in female mating decisions, we also investigated whether chick growth rate and immune defence were related to male plumage and integumentary colouration. We found that offspring growth rates and humoral responses were related to the humoral responses of their parents, suggesting that at least some components of humoral immune capacity are heritable. The white colour of male ostrich feathers was correlated to the humoral response and growth rate of their offspring, suggesting that this visual cue involved in the male courtship display could serve as an important signal to females of male quality, thereby forming the basis of mate choice in this species.

Keywords

Struthio camelus PHA injection Diphtheria Tetanus Plumage colouration Spectrophotometry Immunocompetence 

Notes

Acknowledgments

We gratefully thank the National Research Foundation of South Africa for financial support, and the Western Cape Department of Agriculture for maintaining the research flock at the Oudtshoorn Research farm, and especially Stefan Engelbrecht and Basie Pfister for assistance in taking care of the birds and data collection. DH was supported by grants from the Swedish Research Council (VR), and partially from the Linnaeus excellence research project CAnMove financed by the Swedish Research Council and Lund University.

Ethical standards

Ethical clearance for these experiments, which comply with the laws of South Africa, was granted by the Stellenbosch University ethics committee (2006B03001).

References

  1. Amundsen T, Forsgren E, Hansen LTT (1997) On the function of female ornaments: male bluethroats prefer colourful females. Proc R Soc Lond B 264:1579–1586CrossRefGoogle Scholar
  2. Andersson M (1994) Sexual selection. Princeton University Press, Princeton, New JerseyGoogle Scholar
  3. Ariyomo TO, Carter M, Watt PJ (2013) Heritability of boldness and aggressiveness in the zebrafish. Behav Genet 43:161–167PubMedCrossRefGoogle Scholar
  4. Bertram BCR (1992) The ostrich communal nesting system. Princeton University Press, Princeton, New JerseyGoogle Scholar
  5. Birkhead TR, Fletcher F, Pellat EJ (1999) Nestling diet, secondary sexual traits and fitness in zebra finch. Proc R Soc Lond B 266:385–390CrossRefGoogle Scholar
  6. Bonato M, Evans MR, Cherry MI (2009a) Investment in eggs is influenced by male coloration in the ostrich (Struthio camelus). Anim Behav 77:1027–1032CrossRefGoogle Scholar
  7. Bonato M, Evans MR, Hasselquist D, Cherry MI (2009b) Male coloration reveals different components of immunocompetence in ostriches, Struthio camelus. Anim Behav 77:1033–1039CrossRefGoogle Scholar
  8. Bonato M, Evans MR, Hasselquist D, Cloete SWP, Cherry MI (2009c) Growth rate and hatching date in ostrich chicks reflect humoral but not cell-mediated immune function. Behav Ecol Sociobiol 64:183–191CrossRefGoogle Scholar
  9. Boonekamp JJ, Ros AHF, Verhulst S (2008) Immune activation suppresses plasma testosterone levels: a meta analysis. Biol Lett 4:741–744PubMedCrossRefGoogle Scholar
  10. Bortolotti GR, Blas J, Negro JJ, Tella JL (2006) A complex plumage pattern as an honest social signal. Anim Behav 72:423–430CrossRefGoogle Scholar
  11. Brinkhof MWG, Heeb P, Kolliker M, Richner H (1999) Immunocompetence of nestling great tits in relation to rearing environment and parentage. Proc R Soc Lond B 266:2315–2322CrossRefGoogle Scholar
  12. Bunter KL, Cloete SWP (2004) Genetic parameters for egg-, chick- and live-weight traits recorded in farmed ostriches (Struthio camelus). Livest Prod Sci 91:9–22CrossRefGoogle Scholar
  13. Cheng S, Lamont SJ (1988) Genetic analysis of immunocompetence measures in a white leghorn chicken line. Poult Sci 67:989–995PubMedCrossRefGoogle Scholar
  14. Cichon M, Sendecka J, Gustafsson L (2006) Genetic and environmental variation in immune response of collared flycatcher nestlings. J Evol Biol 19:1701–1706PubMedCrossRefGoogle Scholar
  15. Cilliers SC, du Preez JJ, Maritz JS, Hayes JP (1995) Growth curves of ostriches (Struthio camelus) from Oudtshoorn in South Africa. Anim Sci 6:161–164CrossRefGoogle Scholar
  16. Cornwallis CK, Birkhead TR (2006) Social status and availability of females determine patterns of sperm allocation in the fowl. Evolution 60:1486–1493PubMedGoogle Scholar
  17. Cornwallis CK, Birkhead TR (2007) Experimental evidence that female ornamentation increases the acquisition of sperm and signals fecundity. Proc R Soc Lond B 274:583–590CrossRefGoogle Scholar
  18. Cotton S, Small J, Pomiankowski A (2006) Sexual selection and condition-dependent mate preferences. Curr Biol 16:R755–R765PubMedCrossRefGoogle Scholar
  19. Cunningham EJ, Russell AF (2000) Egg investment is influenced by male attractiveness in the mallard. Nature 404:74–77PubMedCrossRefGoogle Scholar
  20. Deeming DC (1996) Production, fertility and hatchability of ostrich (Struthio camelus) eggs on a farm in the United Kingdom. Anim Sci 67:329–336CrossRefGoogle Scholar
  21. Deeming DC, Ayres L (1994) Factors affecting the rate of growth of ostrich (Struthio camelus) chicks in captivity. Vet Rec 135:617–622PubMedGoogle Scholar
  22. Deeming DC, Ayres L, Ayres FJ (1993) Observations on the first commercial production of ostrich (Struthio camelus) eggs in the UK: rearing of chicks. Vet Rec 132:627–631PubMedCrossRefGoogle Scholar
  23. Doucet SM (2002) Structural plumage coloration, male body size, and condition in the blue-black grassquit. Condor 104:30–38CrossRefGoogle Scholar
  24. Doutrelant C, Grégoire A, Grnac N, Gomez D, Lambrechts MM, Perret P (2008) Female coloration indicates female reproductive capacity in blue tits. J Evol Biol 21:226–233PubMedGoogle Scholar
  25. Endler JA (1990) On the measurement and classification of colour in studies of animal colour patterns. Biol J Linn Soc Lond 41:315–352CrossRefGoogle Scholar
  26. Endler JA, Théry M (1996) Interacting effects of lek placement, display behavior, ambient light and color patterns in three neotropical forest-dwelling birds. Am Nat 148:421–452CrossRefGoogle Scholar
  27. Fair JM, Hansen ES, Ricklefs RE (1999) Growth, developmental stability and immune response in juvenile Japanese quails (Coturnix coturnix japonica). Proc R Soc Lond B 266:1735–1742CrossRefGoogle Scholar
  28. Faivre B, Préault M, Salvadori F, Théry M, Gaillard M, Cézilly F (2003) Bill colour and immunocompetence in the European blackbird. Anim Behav 65:1125–1131CrossRefGoogle Scholar
  29. Falconer D, Mackay T (1996) Introduction to quantitative genetics. Longman, Essex, UKGoogle Scholar
  30. Folstad I, Karter AJ (1992) Parasites, bright males and the immunocompetence handicap. Am Nat 139:603–622CrossRefGoogle Scholar
  31. Gandini GCM, Keffen RH (1985) Sex determination of the South African ostrich (Struthio camelus). J S Afr Vet Assoc 56:209–210Google Scholar
  32. Gil D, Culver R (2011) Male ornament size in a passerine predicts the inhibitory effect of testosterone on macrophage phagocytosis. Funct Ecol 25:1278–1283CrossRefGoogle Scholar
  33. Gil D, Graves J, Hazon N, Wells A (1999) Male attractiveness and differential testosterone investment in zebra finch eggs. Science 286:126–128PubMedCrossRefGoogle Scholar
  34. Griffith SC, Pryke SR (2006) Benefits of females assessing color display. In: Hill GE, McGraw KJ (eds) Bird coloration: function and evolution, Harvard University Press, pp 233–279Google Scholar
  35. Grindstaff JL, Brodie ED, Ketterson ED (2003) Immune function across generations: integrating mechanism and evolutionary process in maternal antibody transmission. Proc R Soc Lond B 270:2309–2319CrossRefGoogle Scholar
  36. Gross WB, Siegel HS (1983) Evaluation of the heterophil/lymphocyte ratio as a measure of stress in chickens. Avian Dis 27:972–979PubMedCrossRefGoogle Scholar
  37. Hanssen SA, Hasselquist D, Folstad I, Erikstad KE (2004) Cost of immunity: immune responsiveness reduces survival in a vertebrate. Proc R Soc Lond B 271:925–930CrossRefGoogle Scholar
  38. Hanssen SA, Folstad I, Hasselquist D, Erikstad KE (2008) A label of health: the expression of a female plumage trait signals previous immune challenge. Biol Lett 4:379–381PubMedCrossRefGoogle Scholar
  39. Hasselquist D (2007) Comparative immunoecology in birds: hypotheses and tests. J Ornithol 148(suppl 2):S571–S582CrossRefGoogle Scholar
  40. Hasselquist D, Nilsson JÅ (2009) Maternal transfer of antibodies in vertebrates: trans-generational effects on offspring immunity. Philos T Roy Soc B 364:51–60CrossRefGoogle Scholar
  41. Hasselquist D, Nilsson JÅ (2012) Physiological mechanisms mediating costs of immune responses: what can we learn from studies of birds? Anim Behav 83:1303–1312CrossRefGoogle Scholar
  42. Hasselquist D, Marsh JA, Sherman PW, Wingfield JC (1999) Is avian humoral immunocompetence suppressed by testosterone? Behav Ecol Sociobiol 45:167–175CrossRefGoogle Scholar
  43. Hasselquist D, Tobler M, Nilsson J-Å (2012) Maternal modulation of offspring immune function in vertebrates. In: Nelson RM, Demas G (eds) Eco-immunology. Oxford University Press, Oxford, pp 165–224Google Scholar
  44. Heywood JS (1989) Sexual selection by the handicap mechanism. Evolution 43:1387–1397CrossRefGoogle Scholar
  45. Hill GE (1991) Plumage coloration is a sexually selected indicator of male quality. Nature 350:337–339CrossRefGoogle Scholar
  46. Iwasa Y, Pomiankowski A (1994) The evolution of mate preferences for multiple handicaps. Evolution 48:853–867CrossRefGoogle Scholar
  47. Jacquin L, Lenouvel P, Haussy C, Ducatez S, Gasparini J (2011) Melanin-based coloration is related to parasite intensity and cellular immune response in an urban free living bird: the feral pigeon Columba livia. J Avian Biol 42:1–5CrossRefGoogle Scholar
  48. Johnsen A, Andersen V, Sunding C, Lifjeld JT (2000) Female bluethroats enhance offspring immunocompetence through extra-pair copulations. Nature 406:296–299PubMedCrossRefGoogle Scholar
  49. Johnstone RA, Reynolds JD, Deutsch JC (1996) Mutual mate choice and sex differences in choosiness. Evolution 50:1382–1391CrossRefGoogle Scholar
  50. Jones MC, Taylor PC (1999) Statistical Modelling using GENSTAT. Arnold, LondonGoogle Scholar
  51. Kalinowski ST, Taper ML, Marshall TC (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol 16:1099–1106PubMedCrossRefGoogle Scholar
  52. Kilpimaa J, Van de Casteele T, Jokinen I, Mappes J, Alatalo RV (2005) Genetic and environmental variation in antibody and T-cell mediated responses in the great tit. Evolution 59:2483–2489PubMedGoogle Scholar
  53. Kimwele CN, Graves JA (2003) A molecular genetic analysis of the communal nesting of the ostrich (Struthio camelus). Mol Ecol 12:229–336PubMedCrossRefGoogle Scholar
  54. Klasing KC, Laurin DE, Peng RK, Fry D (1987) Immunologically mediated growth depression in chicks: influence of feed intake, corticosterone and interleukin-1. J Nutr 117:1629–1637PubMedGoogle Scholar
  55. Krams I, Vrublevska J, Cirule D, Kivleniece I, Krama T, Rantala MJ, Sild E, Hõrak P (2012) Heterophil/lymphocyte ratios predict the magnitude of humoral immune response to a novel antigen in great tits (Parus major). Comp Biochem Physio A 161:422–428CrossRefGoogle Scholar
  56. Lessells CM, Boag PT (1987) Unrepeatable repeatibilities: a common mistake. Auk 104:116–121CrossRefGoogle Scholar
  57. Lifjeld JT, Dunn PO, Whittingham LA (2002) Short term fluctuations in cellular immunity of tree swallows feeding nestlings. Oecologia 130:185–190Google Scholar
  58. Lihoreau M, Zimmer C, Rivault C (2008) Mutual mate choice: when it pays both sexes to avoid inbreeding. PLoS One 3:e3365PubMedCrossRefGoogle Scholar
  59. Martin LB, Han P, Lewittes J, Kuhlman JR, Klasing KC, Wiklelski M (2006) Phytohemagglutinin-induced skin swelling in birds: histological support for a classic immunoecological technique. Funct Ecol 20:290–299CrossRefGoogle Scholar
  60. McGraw KJ, Ardia DR (2003) Carotenoids, immunocompetence, and the information content of sexual colors: an experimental test. Am Nat 162:704–712PubMedCrossRefGoogle Scholar
  61. McGraw KJ, Correa SM, Adkins-Regan E (2006) Testosterone upregulates lipoprotein status to control sexual attractiveness in a colorful songbird. Behav Ecol Sociobiol 60:117–122CrossRefGoogle Scholar
  62. Møller AP, Petrie M (2002) Condition dependence, multiple sexual signals, and immunocompetence in peacocks. Behav Ecol 13:248–253CrossRefGoogle Scholar
  63. Mushi EZ, Isa JFW, Chabo RG, Segaise TT (1998) Growth rate of ostrich (Struthio camelus) chicks under intensive management in Botswana. Trop Anim Health Prod 30:197–203PubMedCrossRefGoogle Scholar
  64. Norris K, Evans MR (2000) Ecological immunology: life history trade-offs and immune defense in birds. Behav Ecol 11:19–26CrossRefGoogle Scholar
  65. Owen-Ashley NT, Hasselquist D, Wingfield JC (2004) Androgens and the immunocompetence handicap hypothesis: unravelling direct and indirect pathways of immunosuppression in song sparrows. Am Nat 164:490–505PubMedCrossRefGoogle Scholar
  66. Parmentier H, Nieuwland M, Rijke E, De Vries Reilingh G, Schrama J (1996) Divergent antibody responses to vaccines and divergent body weights of chicken lines selected for high and low humoral responsiveness to sheep red blood cells. Avian Dis 40:634–644PubMedCrossRefGoogle Scholar
  67. Payne RW, Murray DA, Harding SA, Baird DB, Soutar DM (2009) GenStat for Windows (12th Edition) Introduction. VSN, Hemel HempsteadGoogle Scholar
  68. Petrie M, Williams A (1993) Peahens lay more eggs for peacocks with larger trains. Proc R Soc Lond B 251:127–131CrossRefGoogle Scholar
  69. Pyke N (2011) Using false discovery rates for multiple comparisons in ecology and evolution. Methods Ecol Evol 2:278–282CrossRefGoogle Scholar
  70. Råberg L, Stjernman M, Hasselquist D (2003) Immune responsiveness in adult blue tits: heritability and effects of nutritional status during ontogeny. Oecologia 136:360–364PubMedCrossRefGoogle Scholar
  71. Ricklefs RE, Webb T (1985) Water content, thermogenesis, and growth rate of skeletal muscles in the European starling. Auk 102:369–376CrossRefGoogle Scholar
  72. Roberts ML, Buchanan KL, Evans MR (2004) Testing the immunocompetence handicap hypothesis: a review of the evidence. Anim Behav 68:227–239CrossRefGoogle Scholar
  73. Roulin A, Jungi TW, Pfister H, Dijkstra C (2000) Female barn owls (Tyto alba) advertise good genes. Proc R Soc Lond B 267:937–941CrossRefGoogle Scholar
  74. Saino N, Bolzern AM, Møller AP (1997) Immunocompetence, ornamentation, and viability of male barn swallows (Hirundo rustica). P Natl Acad Sci USA 94:549–552CrossRefGoogle Scholar
  75. Saino N, Incagli M, Martinelli R, Møller AP (2002) Immune response of male barn swallow in relation to parental effort, corticosterone plasma levels, and sexual ornamentation. Behav Ecol 13:169–174CrossRefGoogle Scholar
  76. Saks L, McGraw K, Horak P (2003a) How feather colour reflects its carotenoid content. Funct Ecol 17:555–561CrossRefGoogle Scholar
  77. Saks L, Ots I, Horak PH (2003b) Carotenoid-based plumage coloration of male greenfinches reflects health and immunocompetence. Oecologia 134:301–307PubMedGoogle Scholar
  78. Servedio MR, Lande R (2006) Population genetic models of male and mutual mate choice. Evolution 60:674–685PubMedGoogle Scholar
  79. Smits JE, Bortolotti GR, Tella JL (1999) Simplifying the phytohaemagglutinin skin-testing technique in studies of avian immunocompetence. Funct Ecol 13:567–572CrossRefGoogle Scholar
  80. Soler JJ, de Neve L, Perez-Contreras T, Soler M, Sorci G (2003) Trade-off between immunocompetence and growth in magpies: an experimental study. Proc R Soc Lond B 270:241–248CrossRefGoogle Scholar
  81. Stoehr AM, Kokko H (2006) Sexual dimorphism in immunocompetence: what does life-history theory predicts? Behav Ecol 17:751–756CrossRefGoogle Scholar
  82. Storey J (2003) The positive false discovery rate: a Bayesian interpretation and the q-value. Ann Stat 31:2013–2035CrossRefGoogle Scholar
  83. Tang G, Huang YH, Lin L, Hu XX, Feng JD, Yao P, Zhang L, Li N (2003) Isolation and characterization of 70 novel microsatellite markers from ostrich (Struthio camelus) genome. Genome 46:833–840PubMedCrossRefGoogle Scholar
  84. Tjørve KMC, Underhill LG (2009) Growth and its relationship to fledging success of African black oystercatcher Haematopus moquini chicks. Zoology 112:27–37PubMedCrossRefGoogle Scholar
  85. van der Most PJ, de Jong B, Parmentier HK, Verhulst S (2011) Trade-off between growth and immune function: a meta-analysis of selection experiments. Funct Ecol 25:74–80CrossRefGoogle Scholar
  86. Verwoerd DJ, Deeming DC, Angel CR, Perelman B (1999) Rearing environments around the world. In: Deeming DC (ed) The ostrich: biology, production and health. CABI, Manchester, pp 190–216Google Scholar
  87. Vinkler M, Bainova H, Albrecht T (2010) Functional analysis of the skin-swelling response to phytohaemagglutinin. Funct Ecol 24:1081–1086CrossRefGoogle Scholar
  88. von Schantz T, Bensch S, Grahn M, Hasselquist D, Wittzell H (1999) Good genes, oxidative stress and radical sexual signals. Proc R Soc Lond B 266:1–12CrossRefGoogle Scholar
  89. Westneat DF, Birkhead TR (1998) Alternative hypotheses linking the immune system and mate choice for good genes. Proc R Soc Lond B 265:1065–1073CrossRefGoogle Scholar
  90. Zanollo V, Griggio M, Roberston J, Kleindorfer S (2012) The number and coloration of white flank spots predict the strength of a cutaneous immune response in female Diamond Firetails, Stagonopleura guttata. J Ornithol 153:1233–1244CrossRefGoogle Scholar
  91. Zuk M (1994) Immunology and the evolution of behavior. In: Real D (ed) Behavioral mechanisms in ecology. Chicago University Press, Chicago, pp 354–368Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Maud Bonato
    • 1
    • 5
  • Matthew R. Evans
    • 2
  • Dennis Hasselquist
    • 3
  • Richard B. Sherley
    • 4
  • Schalk W. P. Cloete
    • 5
    • 6
  • Michael I. Cherry
    • 1
  1. 1.Department of Botany and ZoologyUniversity of StellenboschMatielandSouth Africa
  2. 2.School of Biological and Chemical Sciences, Queen Mary University of LondonLondonUK
  3. 3.Department of Animal BiologyLundSweden
  4. 4.Animal Demography Unit and Marine Research Institute, Department of Biological SciencesUniversity of Cape TownRondeboschSouth Africa
  5. 5.Department of Animal SciencesUniversity of StellenboschMatielandSouth Africa
  6. 6.Directorate Animal Sciences: ElsenburgElsenburgSouth Africa

Personalised recommendations