Abstract
According to the immunocompetence handicap hypothesis, sexually selected characteristics predict immune function and this relationship is mediated by testosterone. In the present study, we investigated whether bird song could predict immunity in European starlings (Sturnus vulgaris). We recorded the singing and reproductive behaviours of 16 adult male starlings in an outdoor aviary and then assessed their cell-mediated and humoral immunity in vivo. The males were observed in groups of four for 2 h each day over a 4-day period. For each male, the number of songs produced was recorded and the average song-bout length was computed. Next, cell-mediated and humoral immunity were assessed via cutaneous swelling responses to the T-cell mitogen phytohaemagglutinin and antibody responses to a novel antigen, keyhole limpet haemocyanin. Song rate and song-bout length were positively correlated with cell-mediated and humoral immunity, respectively. Additionally, a negative relationship between plasma testosterone concentration and antibody response was observed. These data demonstrate that male starling song can be used as a predictor of immunocompetence, with more robust singers exhibiting enhanced immunity. Whether this relationship is mediated directly by testosterone requires further investigation.
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- Arnold A. P. The effects of castration and androgen replacement on song, courtship, and aggression in zebra finches (Poephila guttata). J Exp Zool. 1975 Mar;191(3):309–326. doi: 10.1002/jez.1401910302. [DOI] [PubMed] [Google Scholar]
- Bernard D. J., Ball G. F. Photoperiodic condition modulates the effects of testosterone on song control nuclei volumes in male European starlings. Gen Comp Endocrinol. 1997 Feb;105(2):276–283. doi: 10.1006/gcen.1996.6829. [DOI] [PubMed] [Google Scholar]
- Bernard D. J., Eens M., Ball G. F. Age- and behavior-related variation in volumes of song control nuclei in male European starlings. J Neurobiol. 1996 Jul;30(3):329–339. doi: 10.1002/(SICI)1097-4695(199607)30:3<329::AID-NEU2>3.0.CO;2-6. [DOI] [PubMed] [Google Scholar]
- Boulakoud M. S., Goldsmith A. R. Acquisition of photosensitivity in castrated male starlings (Sturnus vulgaris) under short day photoperiods. J Reprod Fertil. 1994 Jan;100(1):77–79. doi: 10.1530/jrf.0.1000077. [DOI] [PubMed] [Google Scholar]
- Dawson A., Goldsmith A. R. Plasma prolactin and gonadotrophins during gonadal development and the onset of photorefractoriness in male and female starlings (Sturnus vulgaris) on artificial photoperiods. J Endocrinol. 1983 May;97(2):253–260. doi: 10.1677/joe.0.0970253. [DOI] [PubMed] [Google Scholar]
- DeVoogd T. J. Endocrine modulation of the development and adult function of the avian song system. Psychoneuroendocrinology. 1991;16(1-3):41–66. doi: 10.1016/0306-4530(91)90070-a. [DOI] [PubMed] [Google Scholar]
- Deviche P., Breuner C., Orchinik M. Testosterone, corticosterone, and photoperiod interact to regulate plasma levels of binding globulin and free steroid hormone in dark-eyed juncos, Junco hyemalis. Gen Comp Endocrinol. 2001 Apr;122(1):67–77. doi: 10.1006/gcen.2001.7613. [DOI] [PubMed] [Google Scholar]
- Duckworth R. A., Mendonça M. T., Hill G. E. A condition dependent link between testosterone and disease resistance in the house finch. Proc Biol Sci. 2001 Dec 7;268(1484):2467–2472. doi: 10.1098/rspb.2001.1827. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Falk H., Gwinner E. Timing of photorefractoriness in the European starling: significance of photoperiod early and late in the reproductive cycle. Biol Reprod. 1988 Dec;39(5):1004–1008. doi: 10.1095/biolreprod39.5.1004. [DOI] [PubMed] [Google Scholar]
- Gentner TQ, Hulse SH. Female European starling preference and choice for variation in conspecific male song. Anim Behav. 2000 Feb;59(2):443–458. doi: 10.1006/anbe.1999.1313. [DOI] [PubMed] [Google Scholar]
- Goldsmith A. R., Nicholls T. J. Recovery of photosensitivity in photorefractory starlings is not prevented by testosterone treatment. Gen Comp Endocrinol. 1984 Nov;56(2):210–217. doi: 10.1016/0016-6480(84)90033-9. [DOI] [PubMed] [Google Scholar]
- Hamilton W. D., Zuk M. Heritable true fitness and bright birds: a role for parasites? Science. 1982 Oct 22;218(4570):384–387. doi: 10.1126/science.7123238. [DOI] [PubMed] [Google Scholar]
- Ketterson E. D., Nolan V., Jr, Wolf L., Ziegenfus C., Dufty A. M., Jr, Ball G. F., Johnsen T. S. Testosterone and avian life histories: the effect of experimentally elevated testosterone on corticosterone and body mass in dark-eyed juncos. Horm Behav. 1991 Dec;25(4):489–503. doi: 10.1016/0018-506x(91)90016-b. [DOI] [PubMed] [Google Scholar]
- Klukowski L. A., Cawthorn J. M., Ketterson E. D., Nolan V., Jr Effects of experimentally elevated testosterone on plasma corticosterone and corticosteroid-binding globulin in dark-eyed juncos (Junco hyemalis). Gen Comp Endocrinol. 1997 Oct;108(1):141–151. doi: 10.1006/gcen.1997.6956. [DOI] [PubMed] [Google Scholar]
- Marler P., Peters S., Wingfield J. Correlations between song acquisition, song production, and plasma levels of testosterone and estradiol in sparrows. J Neurobiol. 1987 Nov;18(6):531–548. doi: 10.1002/neu.480180605. [DOI] [PubMed] [Google Scholar]
- McGraw K. J., Hill G. E. Differential effects of endoparasitism on the expression of carotenoid- and melanin-based ornamental coloration. Proc Biol Sci. 2000 Aug 7;267(1452):1525–1531. doi: 10.1098/rspb.2000.1174. [DOI] [PMC free article] [PubMed] [Google Scholar]
- doi: 10.1098/rspb.1998.0405. [DOI] [PMC free article] [Google Scholar]
- doi: 10.1098/rspb.1998.0481. [DOI] [PMC free article] [Google Scholar]
- Peters A. Testosterone treatment is immunosuppressive in superb fairy-wrens, yet free-living males with high testosterone are more immunocompetent. Proc Biol Sci. 2000 May 7;267(1446):883–889. doi: 10.1098/rspb.2000.1085. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Riters L. V., Eens M., Pinxten R., Duffy D. L., Balthazart J., Ball G. F. Seasonal changes in courtship song and the medial preoptic area in male European starlings (Sturnus vulgaris). Horm Behav. 2000 Dec;38(4):250–261. doi: 10.1006/hbeh.2000.1623. [DOI] [PubMed] [Google Scholar]
- Schlinger B. A. Sex steroids and their actions on the birdsong system. J Neurobiol. 1997 Nov;33(5):619–631. [PubMed] [Google Scholar]