Skip to main content
SpringerLink
Log in

The challenge hypothesis: behavioral ecology to neurogenomics

  • Review
  • Published:
Journal of Ornithology Aims and scope Submit manuscript

Abstract

Male song sparrows (Melospiza melodia) are territorial year-round. However, neuroendocrine responses to simulated territorial intrusions (STI) differ between breeding (spring) and non-breeding seasons (autumn). In spring, exposure to STI leads to increases in plasma levels of luteinizing hormone and testosterone (consistent with the challenge hypothesis), but not in autumn. This suggests that there are fundamental differences in the mechanisms driving neuroendocrine responses to STI between seasons despite apparently identical behavioral responses. Recent studies have also shown that areas of the telencephalon and diencephalon involved with singing behavior and aggression express the enzymes necessary to synthesize sex steroids de novo from cholesterol. Of these, aromatase (that regulates the conversion of testosterone to estradiol) and 3β-hydroxysteroid dehydrogenase (that regulates the synthesis of biologically active steroids) are regulated seasonally, whereas receptors for sex steroids such as androgen receptor and estrogen receptor alpha and beta are not. Functional analyses indicate specific genes that may be involved in the mechanisms of differential neuroendocrine responses to aggressive interactions in different life-history stages. Microarrays were used to test the hypothesis that gene expression profiles in the hypothalamus after territorial aggression differ between the seasons. Over 150 genes were differentially expressed between spring and autumn in the control birds and 59 genes were significantly affected by STI in autumn, but only 14 genes in spring. Real-time PCR was performed for validation, and it indicated that STI drives differential genomic responses in the hypothalamus in the breeding versus non-breeding seasons. The results suggest major underlying seasonal effects in the hypothalamus that determine the differential response upon social interaction.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Adkins-Regan E (2005) Hormones and animal social behavior. Princeton University Press, Princeton

    Google Scholar 

  • Ball GF, Balthazart J (2008) Individual variation and the endocrine regulation of behavior and physiology in birds: a cellular/molecular perspective. Phil Trans R Soc B 363:1699–1710

    Google Scholar 

  • Bentley GE, Tsutsui K, Wingfield JC (2007) Endocrinology of reproduction. In: Jamieson BGM (eds) Reproductive biology and phylogeny of Aves (birds). Science, Enfield, pp 181–242

  • Buntin JD (1996) Neural and hormonal control of parental behavior in birds. Adv Study Behav 25:161–213

    Article  Google Scholar 

  • Canoine V, Fusani L, Schlinger BA, Hau M (2007) Low sex steroids, high steroid receptors: increasing the sensitivity of the non-reproductive brain. J Neurobiol 67:57–67

    Article  CAS  Google Scholar 

  • Dawson A, King VM, Bentley GE, Ball GF (2001) Photoperiodic control of seasonality in birds. J Biol Rhythms 16:365–380

    Article  PubMed  CAS  Google Scholar 

  • Duckworth RA (2009) The role of behavior in evolution: a search for mechanism. Evol Ecol 23:513–531

    Article  Google Scholar 

  • Dufty AM (1989) Testosterone and survival. Horm Behav 23:185–193

    Article  PubMed  CAS  Google Scholar 

  • Edwards DP (2000) The role of coactivators and corepressors in the biology and mechanism of action of steroid hormone receptors. J Mamm Gland Biol Neoplasia 5:307–324

    Article  CAS  Google Scholar 

  • Goodson JL (2005) The vertebrate social behavior network: evolutionary themes and variations. Horm Behav 48:11–22

    Article  PubMed  Google Scholar 

  • Goodson JL, Evans AK (2004) Neural responses to territorial challenge and nonsocial stress in male song sparrows: segregation, integration, and modulation by a vasopressin V1 antagonist. Horm Behav 46:371–381

    Article  PubMed  CAS  Google Scholar 

  • Goodson JL, Evans AK, Wang Y (2006) Neuropeptide binding reflects convergent and divergent evolution in species-typical group sizes. Horm Behav 50:223–236

    Article  PubMed  CAS  Google Scholar 

  • Goodson JL, Schrock SE, Klatt JD, Kabelik D, Kingsbury MA (2009) Mesotocin and nonapeptide receptors promote estrildid flocking behavior. Science 235:862–865

    Article  Google Scholar 

  • Hau M, Wingfeld JC (2011) Hormonally-regulated trade-offs: evolutionary variability and phenotypic plasticity in testosterone signaling pathways. In: Flatt T, Heyland A (eds) Mechanisms of life history evolution. Oxford University Press, Oxford

    Google Scholar 

  • Hegner RE, Wingfield JC (1987) Effects of experimental manipulation of testosterone levels on parental investment and breeding success in male house sparrows. Auk 104:462–469

    Google Scholar 

  • Hirschenhauser K, Oliveira RF (2006) Social modulation of androgens in males vertebrates: meta-analyses of the challenge hypothesis. Anim Behav 71:265–277

    Article  Google Scholar 

  • Hirschenhauser K, Winkler H, Oliveira RF (2003) Comparative analysis of male androgen responsiveness to social environment in birds: the effects of mating system and paternal incubation. Horm Behav 43:508–519

    Article  PubMed  CAS  Google Scholar 

  • Ketterson ED, Nolan V Jr, Wolf L, Ziegenfus C (1992) Testosterone and avian life histories: effects of experimentally elevated testosterone on behavior and correlates of fitness in the dark-eyed junco (Junco hyemalis). Am Nat 140:980–999

    Google Scholar 

  • Ketterson ED, Nolan V Jr, Cawthorn MJ, Parker PG, Ziegenfus C (1996) Phenotypic engineering: using hormones to explore the mechanistic and functional bases of phenotypic variation in nature. Ibis 138:70–86

    Google Scholar 

  • Kitaysky AS, Kitaiskaia EV, Piatt JF, Wingfield JC (2003) Benefits and costs of increased levels of corticosterone in seabird chicks. Horm Behav 43:140–149

    Article  PubMed  CAS  Google Scholar 

  • Leshner AI (1978) An introduction to behavioral endocrinology. Oxford University Press, New York

    Google Scholar 

  • Leshner AI (1981) The role of hormones in the control of submissiveness. In: Brain PF, Denton D (eds) Multidisciplinary approaches to aggression research. Elsevier, Amsterdam, pp 302–322

    Google Scholar 

  • Lynn SE, Walker BG, Wingfield JC (2005) A phylogenetically controlled test of hypotheses for behavioral insensitivity to testosterone in birds. Horm Behav 47:170–177

    Article  PubMed  CAS  Google Scholar 

  • Martin LB, Weil ZM, Nelson RJ (2008) Seasonal changes in vertebrate immune activity: mediation by physiological trade-offs. Phil Trans R Soc Lond B 363:321–339

    Article  Google Scholar 

  • Mukai M, Replogle K, Drnevich J, Wang G, Wacker D, Band M, Clayton DF, Wingfield JC (2009) Seasonal differences of gene expression profiles in song sparrow (Melospiza melodia) hypothalamus in relation to territorial aggression. PLoS ONE 4(12):e8182

    Article  PubMed  Google Scholar 

  • Owen-Ashley NT, Turner M, Hahn TP, Wingfield JC (2006) Hormonal, behavioral, and thermoregulatory responses to bacterial lipopolysaccharide in captive and free-living white-crowned sparrows (Zonotrichia leucophrys gambelii). Horm Behav 49:15–19

    Article  PubMed  CAS  Google Scholar 

  • Owen-Ashley NT, Hasselquist D, Råberg L, Wingfield JC (2008) Latitudinal variation of immune defense and sickness behavior in the white-crowned sparrow (Zonotrichia leucophrys). Brain Behav Immun 22:614–625

    Article  PubMed  Google Scholar 

  • Owens IPF, Short RV (1995) Hormonal basis of sexual dimorphism in birds: implications for new theories of sexual selection. Trends Ecol Evol 10:44–47

    Article  PubMed  CAS  Google Scholar 

  • Pradhan DS, Newman AEM, Wacker DW, Wingfield JC, Schlinger BA, Soma KK (2010) Aggressive interactions rapidly increase androgen synthesis in the brain during the non-breeding season. Horm Behav 57:381–389

    Article  PubMed  CAS  Google Scholar 

  • Remage-Healey L, London SE, Schlinger BA (2010) Birdsong and the neural production of steroids. J Chem Neuroanat 39:72–81

    Article  PubMed  CAS  Google Scholar 

  • Schlinger BA (1994) Estrogens to song: picograms to sonograms. Horm Behav 28:191–198

    Article  PubMed  CAS  Google Scholar 

  • Schlinger BA, Brenowitz EA (2002) Neural and hormonal control of birdsong. In: Pfaff D et al (eds) Hormones, brain and behavior, vol 2. Elsevier, Amsterdam, pp 799–839

    Chapter  Google Scholar 

  • Schlinger BA, Pradhan DS, Soma KK (2008) 3-HSD activates DHEA in the songbird brain. Neurochem Int 52:611–620

    Article  PubMed  CAS  Google Scholar 

  • Shibata H, Spencer TE, Oñate SA, Jenster G, Tsai SY, O’Malley BW (1997) Role of co-activators and co-repressors in the mechanism of steroid/thyroid receptor action. Rec Prog Horm Res 52:141–164

    PubMed  CAS  Google Scholar 

  • Silverin B (1980) Effects of long-acting testosterone treatment on free-living pied flycatchers, Ficedula hypoleuca, during the breeding period. Anim Behav 28:906–912

    Article  Google Scholar 

  • Soma K (2006) Testosterone and aggression: Berthold, birds and beyond. J Neuroendocrinol 18:543–551

    Google Scholar 

  • Soma KK, Wingfield JC (2001) Dehydroepiandrosterone in songbird plasma: seasonal regulation and relationship to territorial aggression. Gen Comp Endocrinol 123:144–155

    Article  PubMed  CAS  Google Scholar 

  • Soma KK, Wingfield JC (2003) Brain aromatase, 5α-reductase, and 5β-reductase change seasonally in wild male song sparrows: relationship to territorial aggression. J Neurobiol 56:209–221

    Article  PubMed  CAS  Google Scholar 

  • Soma KK, Bindra R, Gee J, Wingfield J, Schlinger B (1999a) Androgen-metabolizing enzymes show region-specific changes across the breeding season in the brain of a wild songbird. J Neurobiol 41:176–188

    Article  PubMed  CAS  Google Scholar 

  • Soma KK, Sullivan K, Wingfield JC (1999b) Combined aromatase inhibitor and antiandrogen treatment decreases territorial aggression in a wild songbird during the non-breeding season. Gen Comp Endocrinol 115:442–453

    Article  PubMed  CAS  Google Scholar 

  • Soma KK, Sullivan KA, Tramontin AD, Saldanha CJ, Schlinger BA, Wingfield JC (2000a) Acute and chronic effects of an aromatase inhibitor on territorial aggression in breeding and non-breeding male song sparrows. J Comp Physiol A 186:759–769

    Article  PubMed  CAS  Google Scholar 

  • Soma KK, Tramontin AD, Wingfield JC (2000b) Oestrogen regulates male aggression in the non-breeding season. Proc R Soc Lond Ser B 267:1089–1096

    Article  CAS  Google Scholar 

  • Soma KK, Wissman AM, Brenowitz EA, Wingfield JC (2002) Dehydroepiandrosterone (DHEA) increases male aggression and the size of an associated brain region. Horm Behav 41:203–212

    Article  PubMed  CAS  Google Scholar 

  • Sperry TS, Wacker DW, Wingfield JC (2010) The role of androgen receptors in regulating territorial aggression in male song sparrows. Horm Behav 57:86–95

    Article  PubMed  CAS  Google Scholar 

  • Swett MB, Breuner CW (2008) Interaction of testosterone, corticosterone and corticosterone-binding globulin in the white-throated sparrow (Zonotrichia albicollis). Comp Biochem Physiol A Mol Integr Physiol 151:226–231

    Article  PubMed  CAS  Google Scholar 

  • Thompson CK, Brenowitz E (2009) Neurogenesis in an adult avian song nucleus is reduced by decreasing caspase-mediated apoptosis. J Neurosci 29:4586–4591

    Article  PubMed  CAS  Google Scholar 

  • Thompson CK, Bentley GE, Brenowitz E (2007) Rapid seasonal-like regression of the adult avian song control system. Proc Nat Acad Sci USA104:15520–15525

    Google Scholar 

  • Tsutsui K, Saigoh E, Yin H, Ubuka T, Chowdhury VS, Osugi T, Ukena K, Sharp PJ, Wingfield JC, Bentley GE (2009) A new key hormone controlling reproduction, gonadotrophin-inhibitory hormone in birds: discovery, progress and prospects. J Neuroendocrinol 21:271–275

    Article  PubMed  CAS  Google Scholar 

  • Wacker DW, Schlinger BA, Wingfield JC (2008) Combined effects of DHEA and fadrozole on aggression and neural VIP immunoreactivity in the non-breeding male song sparrow. Horm Behav 53:287–294

    Article  PubMed  CAS  Google Scholar 

  • Wacker DW, Wingfield JC, Davis JE, Meddle SL (2010) Seasonal changes in aromatase and androgen receptor, but not estrogen receptor mRNA expression in the brain of the free-living male Song Sparrow, Melospiza melodia morphna. J Comp Neurol 518:3819–3835

    Article  PubMed  CAS  Google Scholar 

  • Watanabe T, Yamamura T, Watanabe M, Yasuo S, Nakao N, Dawson A, Ebihara S, Yoshimura T (2007) Hypothalamic expression of thyroid hormone-activating and inactivating enzyme genes in relation to photorefractoriness in birds and mammals. Am J Physiol Regul Integr Comp Physiol 292:R568–R572

    Article  PubMed  CAS  Google Scholar 

  • Wikelski M, Lynn S, Breuner C, Wingfield JC, Kenagy GJ (1999) Energy metabolism, testosterone and corticosterone in white-crowned sparrows. J Comp Physiol A 185:463–470

    Article  CAS  Google Scholar 

  • Wingfield JC (1984a) Environmental and endocrine control of reproduction in the song sparrow, Melospiza melodia. I. Temporal organization of the breeding cycle. Gen Comp Endocrinol 56:406–416

    Article  PubMed  CAS  Google Scholar 

  • Wingfield JC (1984b) Environmental and endocrine control of reproduction in the song sparrow, Melospiza melodia. II. Agonistic interactions as environmental information stimulating secretion of testosterone. Gen Comp Endocrinol 56:417–424

    Article  PubMed  CAS  Google Scholar 

  • 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 19:174–187

    Article  PubMed  CAS  Google Scholar 

  • Wingfield JC (1994) Control of territorial aggression in a changing environment. Psychoneuroendocrinol 19:709–721

    Article  CAS  Google Scholar 

  • Wingfield JC (2006) Communicative behaviors, hormone-behavior interactions, and reproduction in vertebrates. In: Neill JD (ed) Physiology of reproduction. Academic Press, New York, pp 1995–2040

  • Wingfield JC (2008a) Comparative endocrinology, environment and global change. Gen Comp Endocrinol 157:207–216

    Article  PubMed  CAS  Google Scholar 

  • Wingfield JC (2008b) Organization of vertebrate annual cycles: implications for control mechanisms. Phil Trans R Soc B 363:425–441

    Article  PubMed  Google Scholar 

  • Wingfield JC, Farner DS (1993) The endocrinology of wild species. In: Farner DS, King JR, Parkes KC (eds) Avian biology, vol 9. Academic, New York, pp 163–327

  • Wingfield JC, Hahn TP (1994) Testosterone and territorial behavior in sedentary and migratory sparrows. Anim Behav 47:77–89

    Article  Google Scholar 

  • Wingfield JC, Monk D (1992) Control and context of year-round territorial aggression in the non-migratory song sparrow, Melospiza melodia morphna. Ornis Scand 23:298–303

    Article  Google Scholar 

  • Wingfield JC, Monk D (1994) Behavioral and hormonal responses of male song sparrows to estrogenized females during the non-breeding season. Horm Behav 28:146–154

    Article  PubMed  CAS  Google Scholar 

  • Wingfield JC, Silverin B (1986) Effects of corticosterone on territorial behavior of free-living song sparrows, Melospiza melodia. Horm Behav 20:405–417

    Article  PubMed  CAS  Google Scholar 

  • Wingfield JC, Silverin B (2002) Ecophysiological studies of hormone-behavior relations in birds. In: Pfaff DW, Arnold AP, Etgen AM, Fahrbach SE, Rubin RT (eds) Hormones, brain and behavior, vol 2. Elsevier, Amsterdam, pp 587–647

  • Wingfield JC, Silverin B (2009) Ecophysiological studies of hormone–behavior relations in birds. In: Pfaff DW, Arnold AP, Etgen AM, Fahrbach SE, Rubin RT (eds) Hormones, brain and behavior, vol 2, 2nd edn. Academic, New York, pp 817–854

  • Wingfield JC, Soma KK (2002) Spring and autumn territoriality: same behavior different mechanisms? Integr Comp Biol 42:11–20

    Article  PubMed  Google Scholar 

  • Wingfield JC, Hegner RE, Dufty AM Jr, Ball GF (1990) The “challenge hypothesis”: theoretical implications for patterns of testosterone secretion, mating systems, and breeding strategies. Am Nat 136:829–846

    Article  Google Scholar 

  • Wingfield JC, Jacobs J, Hillgarth N (1997) Ecological constraints and the evolution of hormone–behavior interrelationships. Ann NY Acad Sci 807:22–41

    Google Scholar 

  • Wingfield JC, Lynn SE, Soma KK (2001) Avoiding the “costs” of testosterone: ecological bases of hormone–behavior interactions. Brain Behav Evol 57:239–251

    Google Scholar 

  • Wingfield JC, Moore IT, Goymann W, Wacker DW, Sperry T (2005) Contexts and ethology of vertebrate aggression: implications for the evolution of hormone–behavior interactions. In: Nelson RJ (ed) Biology of aggression. Oxford University Press, New York, pp 179–210

  • Yoshimura T (2004) Molecular bases for seasonal reproduction in birds. J Poultry Sci 41:251–258

    Article  CAS  Google Scholar 

Download references

Acknowledgments

JCW is grateful to the National Science Foundation for a series of grants that have supported much of the research and ideas discussed in this manuscript. The most current grant is IOS-0750540. He also acknowledges support from the Russell F. Stark Professorship from the University of Washington and the Endowed Chair in Physiology, University of California, Davis. The author is also grateful to the following people who worked on this project over the past 30 years: Lee B. Astheimer, Gregory F. Ball, Eliot Brenowitz, D. Shallin Busch, William Buttemer, David Clayton, Alfred M. Dufty Jr., Wolfgang Goymann, Thomas P. Hahn, Michaela Hau, Robert Hegner, Kathleen Hunt, Meta Landys, Sharon Lynn, Simone Meddle, Ignacio Moore, Michael C. Moore. Motoko Mukai, Devleena S. Pradhan, Marilyn Ramenofsky, Kiran Soma, Barney Schlinger, Todd Sperry, Douglas Wacker, Gang Wang, and Martin Wikelski. Their contributions were invaluable.

Author information

Authors and Affiliations

  1. Department of Neurobiology, Physiology and Behavior, University of California, Davis, CA, 95616, USA

    John C. Wingfield

Authors
  1. John C. Wingfield
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to John C. Wingfield.

Additional information

Communicated by Cristina Miyaki.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wingfield, J.C. The challenge hypothesis: behavioral ecology to neurogenomics. J Ornithol 153 (Suppl 1), 85–96 (2012). https://doi.org/10.1007/s10336-012-0857-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10336-012-0857-8

Keywords

Search

Navigation