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Sex steroid profiles and pair-maintenance behavior of captive wild-caught zebra finches (Taeniopygia guttata)

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Abstract

Here, we studied the life-long monogamous zebra finch, to examine the relationship between circulating sex steroid profiles and pair-maintenance behavior in pairs of wild-caught zebra finches (paired in the laboratory for >1 month). We used liquid chromatography–tandem mass spectrometry to examine a total of eight androgens and progestins [pregnenolone, progesterone, dehydroepiandrosterone (DHEA), androstenediol, pregnan-3,17-diol-20-one, androsterone, androstanediol, and testosterone]. In the plasma, only pregnenolone, progesterone, DHEA, and testosterone were above the limit of quantification. Sex steroid profiles were similar between males and females, with only circulating progesterone levels significantly different between the sexes (female > male). Circulating pregnenolone levels were high in both sexes, suggesting that pregnenolone might serve as a circulating prohormone for local steroid synthesis in zebra finches. Furthermore, circulating testosterone levels were extremely low in both sexes. Additionally, we found no correlations between circulating steroid levels and pair-maintenance behavior. Taken together, our data raise several interesting questions about the neuroendocrinology of zebra finches.

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References

  • Adkins-Regan E (2005) Hormones and Animal Social Behavior. Princeton University Press, NJ

    Google Scholar 

  • Adkins-Regan E, Tomaszycki ML (2007) Monogamy on the fast track. Biol Lett 3:617–619

    Article  PubMed  PubMed Central  Google Scholar 

  • Adkins-Regan E, Abdelnabi M, Mobarak M, Ottinger MA (1990) Sex steroid levels in developing and adult male and female zebra finches (Poephila guttata). Gen Comp Endocrinol 78:93–109

    Article  PubMed  CAS  Google Scholar 

  • Adomat HH, Bains OS, Lubieniecka JM, Gleave ME, Guns ES, Grgilatti TA, Reid RE, Riggs KW (2012) Validation of a sequential extraction and liquid chromatography–tandem mass spectrometric method for determination of dihydrotestosterone, androstenediol, and androstenediol-glucuronide in prostate tissues. J Chromatogr B 902:84–95

    Article  CAS  Google Scholar 

  • Aragona BJ, Liu Y, Yu YJ, Curtis JT, Detwiler JM, Insel TR, Wang Z (2006) Nucleus accumbens dopamine differentially mediates the formation and maintenance of monogamous pair bonds. Nat Neurosci 9:133–139

    Article  PubMed  CAS  Google Scholar 

  • Arnold AP (1975) The effects of castration and androgen replacement on song, courtship, and aggression in zebra finches (Poephila guttata). J Exp Zool 191:309–325

    Article  PubMed  CAS  Google Scholar 

  • Auchus RJ (2004) The backdoor pathway to dihydrotestosterone. Trends Endocrinol Metab 15:432–438

    Article  PubMed  CAS  Google Scholar 

  • Banerjee SB, Dias BG, Crews D, Adkins-Regan E (2013) Newly paired zebra finches have higher dopamine levels and immediate early gene Fos expression in dopaminergic neurons. Eur J Neurosci 38:3731–3739

    Article  PubMed  Google Scholar 

  • Beletsky LD (1983) Aggressive and pair-bond maintenance songs of female red-winged blackbirds (Agelaius phoeniceus). Z Tierpsychol 62:47–54

    Article  Google Scholar 

  • Black JM (1996) Partnerships in Birds: The Study of Monogamy. Oxford University Press, USA

    Google Scholar 

  • Calisi RM, Bentley GE (2009) Lab and field experiments: are they the same animal? Horm Behav 56:1–10

    Article  PubMed  Google Scholar 

  • Carter CS (1998) Neuroendocrine perspectives on social attachment and love. Psychoneuroendocrinology 23:779-818

    Article  PubMed  CAS  Google Scholar 

  • Dickens MJ, Bentley GE (2014) Stress, captivity, and reproduction in a wild bird species. Horm Behav 66:685–693

    Article  PubMed  CAS  Google Scholar 

  • Dunn AM, Zann R (1996) Undirected song encourages the breeding female zebra finch to remain in the nest. Ethology 102:540–548

    Article  Google Scholar 

  • Elie JE, Mathevon N, Vignal C (2011) Same-sex pair-bond is socially equivalent and as strong as male–female relationship in a life-long monogamous songbird. Behav Ecol Sociobiol 65:2197–2208

    Article  Google Scholar 

  • Ericsson M, Fallahsharoudi A, Bergquist J, Kushnir MM, Jensen P (2014) Domestication effects on behavioural and hormonal responses to acute stress in chickens. Physiol Behav 133:161–169

    Article  PubMed  CAS  Google Scholar 

  • Evans S, Poole TB (1984) Long-term changes and maintenance of the pair-bond in common marmosets, Callithrix jacchus jacchus. Folia Primatol 42:33–41

    Article  Google Scholar 

  • Fokidis HB, Prior NH, Soma KK (2013) Fasting increases aggression and differentially modulates local and systemic steroid levels in male zebra finches. Endocrinology 154:4328–4339

    Article  PubMed  CAS  Google Scholar 

  • Fokidis HB, Adomat HH, Kharmate G, Hosseini-Beheshti E, Guns ES, Soma KK (2015) Regulation of local steroidogenesis in the brain and in prostate cancer: Lessons learned from interdisciplinary collaboration. Front Neuroendocrinol 36:108–129

    PubMed  CAS  Google Scholar 

  • Griffith SC, Holleley CE, Mariette MM, Pryke SR, Svedin N (2010) Low level of extrapair parentage in wild zebra finches. Anim Behav 79:261–264

    Article  Google Scholar 

  • Griffith SC, Pryke SR, Mariette M (2008) Nest box use by the zebra finch Taeniopygia guttata: implications for reproductive success and research. Emu 108:311–319

    Article  Google Scholar 

  • Heimovics SA, Riters LV (2008) Evidence that dopamine within motivation and song control brain regions regulates birdsong context-dependently. Physiol Behav 95:258–266

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Hessler NA, Doupe AJ (1999) Social context modulates singing-related neural activity in the songbird forebrain. Nat Neurosci 2:209–211

    Article  PubMed  CAS  Google Scholar 

  • Kabelik D, Schrock SE, Ayres LC, Goodson JL (2011) Estrogenic regulation of dopaminergic neurons in the opportunistically breeding zebra finch. Gen Comp Endocrinol 173:96–104

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Kikkawa J (1980) Seasonality of nesting by zebra finches at Armidale, NSW. Emu 80:13–20

    Article  Google Scholar 

  • Klatt JD, Goodson JL (2013) Oxytocin-like receptors mediate pair bonding in a socially monogamous songbird. Proc R Soc B 280:2012–2396

    Google Scholar 

  • Koren L, Ng ESM, Soma KK, Wynne-Edwards KE (2012) Sample preparation and liquid chromatography–tandem mass spectrometry for multiple steroids in mammalian and avian circulation. PLoS ONE 7(2):e32496

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Lynn SE (2015) Endocrine and neuroendocrine regulation of fathering behavior in birds. Horm Behav. doi:10.1016/j.yhbeh.2015.04.005

    PubMed  Google Scholar 

  • Mariette MM, Griffith SC (2012) Nest visit synchrony is high and correlates with reproductive success in the wild Zebra finch Taeniopygia guttata. J Avian Biol 43:131–140

    Article  Google Scholar 

  • Oliveira RF (2009) Social behavior in context: hormonal modulation of behavioral plasticity and social competence. Integr Comp Biol 49:423–440

    Article  PubMed  Google Scholar 

  • Perfito N, Zann RA, Bentley GE, Hau M (2007) Opportunism at work: habitat predictability affects reproductive readiness in free-living zebra finches. Funct Ecol 21:291–301

    Article  Google Scholar 

  • Pradhan DS, Yan Y, Soma KK (2008) Rapid estrogen regulation of DHEA metabolism in the male and female songbird brain. J Neurochem 104:244–253

    PubMed  CAS  PubMed Central  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  PubMed Central  Google Scholar 

  • Prior NH, Soma KK (2015) Neuroendocrine regulation of long-term pair maintenance in the monogamous zebra finch. Horm Behav. doi:10.1016/j.yhbeh.2015.04.014

  • Prior NH, Heimovics SA, Soma KK (2013) Effects of water restriction on reproductive physiology and affiliative behavior in an opportunistically-breeding and monogamous songbird, the zebra finch. Horm Behav 63:462–474

    Article  PubMed  CAS  Google Scholar 

  • Prior NH, Yap KN, Soma KK (2014) Acute and chronic effects of an aromatase inhibitor on pair-maintenance behavior of water-restricted zebra finch pairs. Gen Comp Endocrinol 196:62–71

    Article  PubMed  CAS  Google Scholar 

  • Pröve E (1983) Hormonal correlates of behavioural development in male zebra finches. In: Balthazart J, Pröve E, Gilles R (eds) Hormones and behaviour in higher vertebrates. Springer, Berlin, pp 368–374

    Chapter  Google Scholar 

  • R Core Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org/

  • Reichard UH, Boesch C (2003) Monogamy: Mating Strategies and Partnerships in Birds, Humans and Other Mammals. Cambridge University Press, UK

    Book  Google Scholar 

  • Remage-Healey L, Oyama RK, Schlinger BA (2009) Elevated aromatase activity in forebrain synaptic terminals during song. J Neuroendocrinol 2:191–199

    Article  Google Scholar 

  • Resendez SL, Aragona BJ (2013) Aversive motivation and the maintenance of monogamous pair bonding. Rev Neurosci 24:51–60

    PubMed  CAS  Google Scholar 

  • Schmidt KL, Pradhan DS, Shah AH, Charlier TD, Chin EH, Soma KK (2008) Neurosteroids, immunosteroids, and the Balkanization of endocrinology. Gen Comp Endocrinol 157:266–274

    Article  PubMed  CAS  Google Scholar 

  • Shaw G, Renfree MB, Leihy MW, Shackleton CH, Roitman E, Wilson JD (2000) Prostate formation in a marsupial is mediated by the testicular androgen 5 alpha-androstane-3 alpha,17 beta-diol. Proc Natl Acad Sci USA 97:12256–12259

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Silcox AP, Evans SM (1982) Factors affecting the formation and maintenance of pair bonds in the zebra finch, Taeniopygia guttata. Anim Behav 30:1237–1243

    Article  Google Scholar 

  • Smiley KO, Vahaba DM, Tomaszycki ML (2012) Behavioral effects of progesterone on pair bonding and partner preference in the female zebra finch (Taeniopygia guttata). Behav Process 90:210–216

    Article  Google Scholar 

  • Soma KK, Alday NA, Hau M, Schlinger BA (2004) Dehydroepiandrosterone metabolism by 3β-hydroxysteroiddehydrogenase/Δ5–Δ4 isomerase in adult zebra finch brain: sex difference and rapid effect of stress. Endocrinology 145:1668–1677

    Article  PubMed  CAS  Google Scholar 

  • Soma KK, Scotti MAL, Newman AEM, Charlier TD, Demas GE (2008) Novel mechanisms for neuroendocrine regulation of aggression. Front Neuroendocrinol 29:476–489

    Article  PubMed  CAS  Google Scholar 

  • Taves MD, Losie JA, Rahim T, Schmidt KL, Sandkam BA, Ma C, Silversides FG, Soma KK (2016) Locally elevated cortisol in lymphoid organs of the developing zebra finch but not japanese quail or chicken. Dev Comp Immunol 54:116–125

    Article  PubMed  CAS  Google Scholar 

  • Tomaszycki ML, Adkins-Regan E (2006) Is male song quality important in maintaining pair bonds? Behaviour 143:549–567

    Article  Google Scholar 

  • Tomaszycki ML, Banerjee SB, Adkins-Regan E (2006) The role of sex steroids in courtship, pairing and pairing behaviors in the socially monogamous zebra finch. Horm Behav 50:141–147

    Article  PubMed  CAS  Google Scholar 

  • Tsutsui K, Yamazaki T (1995) Avian neurosteroids. I. Pregnenolone biosynthesis in the quail brain. Brain Res 678:1–9

    Article  PubMed  CAS  Google Scholar 

  • Vanson A, Arnold AP, Schlinger BA (1996) 3β-Hydroxysteroid dehydrogenase/isomerase and aromatase activity in primary cultures of developing zebra finch telencephalon: dehydroepiandrosterone as substrate for synthesis of androstenedione and estrogens. Gen Comp Endocrinol 102:342–350

    Article  PubMed  CAS  Google Scholar 

  • Vleck C, Priedkalns J (1985) Reproduction in zebra finches: hormone levels and effect of dehydration. Condor 87:37–46

    Article  Google Scholar 

  • Williams H, Connor DM, Hill JW (2003) Testosterone decreases the potential for song plasticity in adult male zebra finches. Horm Behav 44:402–412

    Article  PubMed  CAS  Google Scholar 

  • Zann RA (1996) The Zebra Finch: a Synthesis of Laboratory and Field Studies. Oxford University Press, USA

    Google Scholar 

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Acknowledgments

This research was made possible by an impressive support staff at Fowlers Gap Semi-Arid Zone Research Station, University of New South Wales Australia. Specifically, thank you to: Keith Leggett, Garry Dowling, Mark Tilley and Vicki Dowling for logistical support at Fowlers Gap. For help with the aviary set up, thank you to Dr. Emilie Perez, Ingrid Boucaud, and Dr. Clementine Vignal. For help with R Statistics and statistical analyses, thank you to Dr. Laura Weir and Dr. Jeffery Joy. For comments on the manuscript, thank you to Dr. Benjamin Sandkam, Dr. Matthew Taves, and three anonymous reviewers. Funding sources included: Canadian Institutes of Health Research (CIHR) Operating Grant 133606 to KKS; National Science Foundation graduate research fellowship (NSF GRFP) to NHP; and Australian Research Council Grant DP130100417 to SCG and KLB.

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Correspondence to Nora H. Prior.

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Prior, N.H., Yap, K.N., Adomat, H.H. et al. Sex steroid profiles and pair-maintenance behavior of captive wild-caught zebra finches (Taeniopygia guttata). J Comp Physiol A 202, 35–44 (2016). https://doi.org/10.1007/s00359-015-1050-3

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