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Within- and between-individual (co)variance partitioning reveals limited pleiotropic effects of testosterone on immune function, sexual signaling, and parental investment

  • Arne Iserbyt
  • Marcel Eens
  • Wendy Baetens
  • Anke Vermeulen
  • Wendt Müller
Original Article

Abstract

How and why individuals differ from each other is a central question in behavioral and evolutionary ecology, because selection particularly acts on this among-individual variation. It is therefore important to accurately partition phenotypic variances into their within- and between-individual components. Partitioning covariances into both components can also inform about underlying mechanistic pathways that potentially interlink trait expression. In the current study, we applied such a (co)variance partitioning approach to test key predictions of two central hypotheses in behavioral ecology, namely the immunocompetence handicap hypothesis and the challenge hypothesis. To this end, we assessed potential pleiotropic effects of testosterone on male sexual signaling, immune function, and parental care. We here repeatedly measured a set of relevant traits in 47 breeding pairs of captive canaries (Serinus canaria). We found that a within-individual increase in female testosterone level suppressed immune function. Furthermore, testosterone levels were positively related to male song repertoire size as an important component of sexual signaling at the between-male level. These were, however, the only relevant significant correlations. Overall, our data do therefore not convincingly support the hypotheses tested and suggest rather limited hormonal pleiotropic effects of testosterone on immune function, parental care, and male sexual signaling, at least in our study system.

Significance statement

Phenotypic variances and covariances can nowadays be partitioned easily into within- and between-individual components. These components inform about trait repeatability and the extent to which multiple traits form phenotypic suites of traits, as well as about their joint underlying mechanistic pathways. Testosterone for example, may be key to mediate the expression of suites of traits in many vertebrate species. We here used captive canaries and repeatedly measured male and female traits, relevant in the context of endocrinology, sexual signaling, immune function, and parental investment. For both sexes, we report particularly weak correlations between testosterone and all other measured traits at both within- and between-individual levels. Our case study thus questions the pleiotropic effects of testosterone, but exemplifies the applicability and relevance of (co)variance partitioning in behavioral ecological research.

Keywords

Challenge hypothesis Hormonal pleiotropy Immunocompetence handicap hypothesis Parental care Sexual signaling Suites of traits Trade-off 

Notes

Acknowledgments

We thank Geert Eens and Peter Scheys for their assistance in taking care of the birds, as well as the entire Family Ecology Unit for their general support and discussion during the breeding season. Bert Thys and four anonymous reviewers provided constructive comments, which helped to improve the clarity of this manuscript. This research was financially supported by FWO Flanders (project ID: 1517815N and 12I1916N to AI and project ID: G.0102.12N to WM and ME) and the University of Antwerp (project ID: 22959 to WM).

Compliance with ethical standards

All experiments were carried out in accordance with the guidelines of the Ethical Committee of the University of Antwerp, Belgium (ID: 2014-72).

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Adkins-Regan E (2005) Hormones and animal social behaviour. Princeton University Press, PrincetonGoogle Scholar
  2. Badyaev AV, Uller T (2009) Parental effects in ecology and evolution: mechanisms, processes and implications. Philos T Roy Soc B 364:1169–1177CrossRefGoogle Scholar
  3. Baugh AT, van Oers K, Dingemanse NJ, Hau M (2014) Baseline and stress-induced glucocorticoid concentrations are not repeatable but covary within individual great tits (Parus major). Gen Comp Endocrinol 208:154–163CrossRefPubMedGoogle Scholar
  4. Bell AM, Hankison SJ, Laskowski KL (2009) The repeatability of behaviour: a meta-analysis. Anim Behav 77:771–783CrossRefPubMedPubMedCentralGoogle Scholar
  5. Bowers EK, Nietz D, Thompson CF, Sakaluk SK (2014) Parental provisioning in house wrens: effects of varying brood size and consequences for offspring. Behav Ecol 25:1485–1493CrossRefGoogle Scholar
  6. Byers BE, Kroodsma DE (2009) Female mate choice and songbird song repertoires. Anim Behav 77:13–22CrossRefGoogle Scholar
  7. Cleasby IR, Nakagawa S, Schielzeth H (2015) Quantifying the predictability of behaviour: statistical approaches for the study of between-individual variation in the within-individual variance. Methods Ecol Evol 6:27–37CrossRefGoogle Scholar
  8. Dingemanse NJ, Dochtermann NA (2013) Quantifying individual variation in behaviour: mixed-effect modelling approaches. J Anim Ecol 82:39–54CrossRefPubMedGoogle Scholar
  9. Dingemanse NJ, Kazem AJN, Réale D, Wright J (2010) Behavioural reaction norms: animal personality meets individual plasticity. Trends Ecol Evol 25:81–89CrossRefPubMedGoogle Scholar
  10. Dochtermann NA, Dingemanse NJ (2013) Behavioral syndromes as evolutionary constraints. Behav Ecol 24:806–811CrossRefGoogle Scholar
  11. Dohm MR (2002) Repeatability estimates do not always set an upper limit to heritability. Funct Ecol 16:273–280CrossRefGoogle Scholar
  12. Duffy DL, Bentley GE, Drazen DL, Ball GF (2000) Effects of testosterone on cell-mediated and humoral immunity in non-breeding adult European starlings. Behav Ecol 11:654–662CrossRefGoogle Scholar
  13. Estramil N, Eens M, Müller W (2013) Coadaptation of offspring begging and parental provisioning—an evolutionary ecological perspective on avian family life. PLoS One 8:e70463CrossRefPubMedPubMedCentralGoogle Scholar
  14. Estramil N, Eens M, Müller W (2014) On the coadaptation of offspring begging and parental supply—a within-individual approach across life stages. Behav Ecol Sociobiol 68:1481–1491CrossRefGoogle Scholar
  15. Folstad I, Karter AJ (1992) Parasites, bright males, and the immunocompetence handicap. Am Nat 139:603–622CrossRefGoogle Scholar
  16. Galván I, Sanz JJ (2011) Mate-feeding has evolved as a compensatory energetic strategy that affects breeding success in birds. Behav Ecol 22:1088–1095CrossRefGoogle Scholar
  17. Garamszegi LZ, Markó G, Herczeg G (2012) A meta-analysis of correlated behaviours with implications for behavioural syndromes: mean effect size, publication bias, phylogenetic effects and the role of mediator variables. Evol Ecol 26:1213–1235CrossRefGoogle Scholar
  18. Gil D, Gahr M (2002) The honesty of bird song: multiple constraints for multiple traits. Trends Ecol Evol 17:133–141CrossRefGoogle Scholar
  19. Gil D, Leboucher G, Lacroix A, Cue R, Kreutzer M (2004) Female canaries produce eggs with greater amounts of testosterone when exposed to preferred male song. Horm Behav 45:64–70CrossRefPubMedGoogle Scholar
  20. Goymann W, Wingfield JC (2014) Male-to-female testosterone ratios, dimorphism, and life history—what does it really tell us? Behav Ecol 25:685–699CrossRefGoogle Scholar
  21. Goymann W, Landys MM, Wingfield JC (2007) Distinguishing seasonal androgen responses from male-male androgen responsiveness—revisiting the challenge hypothesis. Horm Behav 51:463–476CrossRefPubMedGoogle Scholar
  22. Grafen A (1990) Biological signals as handicaps. J Theor Biol 144:517–546CrossRefPubMedGoogle Scholar
  23. Greives TJ, Dochtermann NA, Stewart EC (2017) Estimating heritable genetic contributions to innate immune and endocrine phenotypic correlations: a need to explore repeatability. Horm Behav 88:106–111Google Scholar
  24. Hasselquist D, Bensch S, von Schantz T (1996) Correlation between male song repertoire, extra-pair paternity and offspring survival in the great reed warbler. Nature 381:229–232CrossRefGoogle Scholar
  25. Hau M (2007) Regulation of male traits by testosterone: implications for the evolution of vertebrate life histories. BioEssays 29:133–144CrossRefPubMedGoogle Scholar
  26. Hirschenhauser K, Oliveira RF (2006) Social modulation of androgens in male vertebrates: meta-analyses of the challenge hypothesis. Anim Behav 71:265–277CrossRefGoogle Scholar
  27. Iserbyt A, Eens M, Müller W (2015a) Sexually antagonistic selection during parental care is not generated by a testosterone-related intralocus sexual conflict—insights from full-sib comparisons. Sci Rep 5:17715CrossRefPubMedPubMedCentralGoogle Scholar
  28. Iserbyt A, Farrell S, Eens M, Müller W (2015b) Sex-specific negotiation rules in a costly conflict over parental care. Anim Behav 100:52–58CrossRefGoogle Scholar
  29. Jawor JM, Young R, Ketterson ED (2006) Females competing to reproduce: dominance matters but testosterone may not. Horm Behav 49:362–368CrossRefPubMedGoogle Scholar
  30. Johnsen TS (1998) Behavioural correlates of testosterone and seasonal changes of steroids in red-winged blackbirds. Anim Behav 55:957–965CrossRefPubMedGoogle Scholar
  31. Johnstone RA, Hinde CA (2006) Negotiation over offspring care—how should parents respond to each other’s efforts? Behav Ecol 17:818–827CrossRefGoogle Scholar
  32. Kempenaers B, Peters A, Foerster K (2008) Sources of individual variation in plasma testosterone levels. Philos T Roy Soc B 363:1711–1723CrossRefGoogle Scholar
  33. Ketterson ED, Nolan V, Sandell M (2005) Testosterone in females: mediator of adaptive traits, constraint on sexual dimorphism, or both? Am Nat 166:S85–S98CrossRefPubMedGoogle Scholar
  34. Ketterson ED, Atwell JW, McGlothlin JW (2009) Phenotypic integration and independence: hormones, performance, and response to environmental change. Integr Comp Biol 49:365–379CrossRefPubMedPubMedCentralGoogle Scholar
  35. Leitner S, Voigt C, Gahr M (2001) Seasonal changes in the song pattern of the non-domesticated island canary (Serinus canaria) a field study. Behaviour 138:885–904CrossRefGoogle Scholar
  36. Lessells CM, Boag PT (1987) Unrepeatable repeatabilities: a common mistake. Auk 104:116–121CrossRefGoogle Scholar
  37. Lynn SE (2008) Behavioral insensitivity to testosterone: why and how does testosterone alter paternal and aggressive behavior in some avian species but not others? Gen Comp Endocrinol 157:233–240CrossRefPubMedGoogle Scholar
  38. Madison FN, Rouse ML, Balthazart J, Ball GF (2015) Reversing song behavior phenotype: Testosterone driven induction of singing and measures of song quality in adult male and female canaries (Serinus canaria). Gen Comp Endocrinol 61–75Google Scholar
  39. McGlothlin JW, Ketterson ED (2008) Hormone-mediated suites as adaptations and evolutionary constraints. Philos T Roy Soc B 363:1611–1620CrossRefGoogle Scholar
  40. Møller AP, Jennions MD (2002) How much variance can be explained by ecologists and evolutionary biologists? Oecologia 132:492–500CrossRefGoogle Scholar
  41. Møller AP, Pomiankowski A (1993) Why have birds got multiple sexual ornaments? Behav Ecol Sociobiol 32:167–176Google Scholar
  42. Mougeot F, Irvine JR, Seivwright L, Redpath SM, Piertney S (2004) Testosterone, immunocompetence, and honest sexual signaling in male red grouse. Behav Ecol 15:930–937CrossRefGoogle Scholar
  43. Mutzel A, Dingemanse NJ, Araya-Ajoy YG, Kempenaers B (2013) Parental provisioning behaviour plays a key role in linking personality with reproductive success. Proc R Soc B 280:20131019CrossRefPubMedPubMedCentralGoogle Scholar
  44. Nakagawa S, Schielzeth H (2010) Repeatability for Gaussian and non-Gaussian data: a practical guide for biologists. Biol Rev 85:935–956PubMedGoogle Scholar
  45. O’Neal DM, Reichard DG, Pavilis K, Ketterson ED (2008) Experimentally-elevated testosterone, female parental care, and reproductive success in a songbird, the Dark-eyed Junco (Junco hyemalis). Horm Behav 54:571–578CrossRefPubMedGoogle Scholar
  46. van Oers K, Buchanan KL, Thomas TE, Drent PJ (2011) Correlated response to selection of testosterone levels and immunocompetence in lines selected for avian personality. Anim Behav 81:1055–1061CrossRefGoogle Scholar
  47. Oliveira RF (2004) Social modulation of androgens in vertebrates: mechanisms and function. Adv Stud Behav 34:165–239CrossRefGoogle Scholar
  48. Owen-Ashley NT, Hasselquist D, Wingfield JC (2004) Androgens and the immunocompetence handicap hypothesis: unraveling direct and indirect pathways of immunosuppression in song sparrows. Am Nat 164:490–505CrossRefPubMedGoogle Scholar
  49. Parisot M, Tanvez A, Lacroix A, Vallet E, Béguin N, Leboucher G (2005) Social competition and plasma testosterone profile in domesticated canaries: an experimental test of the challenge hypothesis. Horm Behav 48:225–232CrossRefPubMedGoogle Scholar
  50. Price EO (1999) Behavioral development in animals undergoing domestication. Appl Anim Behav Sci 65:245–271CrossRefGoogle Scholar
  51. Rands SA, Johnstone RA (2006) Statistical measures for defining an individual’s degree of independence within state-dependent dynamic games. BMC Evol Biol 6:81CrossRefPubMedPubMedCentralGoogle Scholar
  52. Rivera-Gutierrez HF, Pinxten R, Eens M (2010) Multiple signals for multiple messages: great tit, Parus major, song signals age and survival. Anim Behav 80:451–459CrossRefGoogle Scholar
  53. Roberts ML, Buchanan KL, Evans MR (2004) Testing the immunocompetence handicap hypothesis: a review of the evidence. Anim Behav 68:227–239CrossRefGoogle Scholar
  54. Sakata JT, Vehrencamp SL (2012) Integrating perspectives on vocal performance and consistency. J Exp Biol 215:201–209CrossRefPubMedPubMedCentralGoogle Scholar
  55. Searcy WA (1992) Song repertoire and mate choice in birds. Am Zool 32:71–80CrossRefGoogle Scholar
  56. Sinervo B, Svensson E (2002) Correlational selection and the evolution of genomic architecture. Heredity 89:329–338CrossRefPubMedGoogle Scholar
  57. Smits JE, Bortolotti GR, Tella JL (1999) Simplifying the phytohaemagglutinin skin-testing technique in studies of avian immunocompetence. Funct Ecol 13:567–572CrossRefGoogle Scholar
  58. Staub NL, De Beer M (1997) The role of androgens in female vertebrates. Gen Comp Endocrinol 108:1–24CrossRefPubMedGoogle Scholar
  59. Thys B, Eens M, Aerts S, Delory A, Iserbyt A, Pinxten R (2017) Exploration and sociability in a highly gregarious bird are repeatable across seasons and in the long term but are unrelated. Anim Behav 123:339–348CrossRefGoogle Scholar
  60. Trösch M, Müller W, Eens M, Iserbyt A (2017) Genes, environments and their interaction: song and mate choice in canaries. Anim Behav 126:261–269CrossRefGoogle Scholar
  61. Van Hout AJM, Pinxten R, Darras VM, Eens M (2012) Testosterone increases repertoire size in an open-ended learner: an experimental study using adult male European starlings (Sturnus vulgaris). Horm Behav 62:563–568CrossRefPubMedGoogle Scholar
  62. Vehrencamp SL, Yantachka J, Hall ML, de Kort SR (2013) Trill performance components vary with age, season, and motivation in the banded wren. Behav Ecol Sociobiol 67:409–419CrossRefPubMedGoogle Scholar
  63. Vergauwen J, Groothuis TGG, Eens M, Müller W (2014) Testosterone influences song behaviour and social dominance - but independent of prenatal yolk testosterone exposure. Gen Comp Endocrinol 195:80–87CrossRefPubMedGoogle Scholar
  64. Westneat DF, Wright J, Dingemanse NJ (2014) The biology hidden inside residual within-individual phenotypic variation. Biol Rev 90:729–743CrossRefPubMedGoogle Scholar
  65. Williams TD (2008) Individual variation in endocrine systems: moving beyond the “tyranny of the Golden Mean”. Philos T Roy Soc B 363:1687–1698CrossRefGoogle Scholar
  66. Wingfield JC (1985) Short-term changes in plasma levels of hormones during establishment and defense of a breeding territory in male song sparrows, Melospiza melodia. Horm Behav 19:174–187CrossRefPubMedGoogle Scholar
  67. Wingfield JC (2016) The challenge hypothesis: where it began and relevance to humans. Horm Behav (published online, doi: 10.1016/j.yhbeh.2016.11.008)
  68. Wingfield JC, Hegner RE, Dufty AM, Ball GF (1990) The “challenge hypothesis”: theoretical implications for patterns of testosterone secretion, mating systems, and breeding strategies. Am Nat 136:829–846CrossRefGoogle Scholar
  69. Wolf M, Weissing FJ (2012) Animal personalities: consequences for ecology and evolution. Trends Ecol Evol 27:452–461CrossRefPubMedGoogle Scholar
  70. Zahavi A, Zahavi A (1997) The handicap principle. Oxford University Press, OxfordGoogle Scholar
  71. Zysling DA, Greives TJ, Breuner CW, Casto JM, Demas GE, Ketterson ED (2006) Behavioral and physiological responses to experimentally elevated testosterone in female dark-eyed juncos (Junco hyemalis carolinensis). Horm Behav 50:200–207CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  1. 1.Department of Biology, Behavioural Ecology and Ecophysiology GroupUniversity of AntwerpWilrijkBelgium

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