Abstract
Several environmental factors have been shown to shape the pattern of investment of carotenoids into the expression of sexual signals. Surprisingly, the impact of the social environment has been neglected. If a carotenoid-based sexual trait is used by females to choose a mate or by males to assess the quality of potential competitors for mates, males, in the presence of females, should upregulate expression of the trait. We tested this hypothesis in male zebra finches that were housed either with females or in a male-only social environment. Additionally, to investigate whether the social modulation of the expression of a sexual trait depends on the physiological need of carotenoids, we challenged half of the males with Escherichia coli lipopolysaccharide (LPS). We found that the social environment modulated the expression of bill color, with males kept in the presence of females harboring a redder bill at the end of the 3 weeks that the experiment lasted. Males injected with LPS showed duller bill color regardless of the presence of females, and social interactions with females result in upregulated bill color similarly for phosphate-buffered saline (PBS) and LPS males. Thus, social environment and immune activation had an additive effect on the expression of bill color. The effect of social environment on plasma carotenoids was less clear. Indeed, a first replicate of the entire experiment showed that both immune challenge and social context affected bill color, with a negative effect of immune challenge and a positive effect of the presence of females on circulating carotenoids. However, a second replicate of the experiment showed only a negative effect of the immune challenge. These results, therefore, suggest that the social environment can affect the expression of carotenoid-based sexual traits under both benign and carotenoid-demanding conditions. Whatever the signaling function of bill color (female mate choice or male–male competition for mates), the observed flexibility may be adaptive because the expression of the signal can be modulated depending on the expected rewards or costs associated with the presence or absence of females. Nevertheless, the mechanisms underlying such an effect are still unknown.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Allen PC (1997) Production of free radical species during Eimeria maxima infections in chickens. Poult Sci 76:814–821
Alonso-Alvarez C, Bertrand S, Devevey G, Prost J, Faivre B, Sorci G (2004) Are carotenoids limiting ressources? An experimental test of dose-dependent effect of carotenoids and immune activation on sexual signals and antioxidant activity. Am Nat 164:651–659
Andersson M (1994) Sexual selection. Princeton University Press, Princeton
Blas J, Pérez-Rodriguez L, Bortolotti GR, Viñuela J, Marchand TA (2006) Testosterone increases bioavailability of carotenoids: insights into honesty of sexual signaling. PNAS 103:18633–18637
Blount JD, Metcalfe NB, Birkhead TR, Surai PF (2003) Carotenoid modulation of immune function and sexual attractiveness in zebra finches. Science 300:125–127
Bolund E, Schielzeth H, Forstmeier W (2007) Intraxexual competition in zebra finches, the role of beak colour and body size. Anim Behav 74:715–724
Bright A, Waas JR (2002) Effects of bill pigmentation and UV reflectance during territory establishment in blackbirds. Anim Behav 64:207–213
Budden AE, Wright J (2001) Falling on deaf ears: the adaptative significance of begging in the absence of a parent. Behav Ecoland Sociobiol 49:474–481
Burley N, Coopersmith CB (1987) Bill color preferences of zebra finches. Ethology 76:133–151
Chew BP, Park JS (2004) Carotenoid action on the immune response. J Nutr 134:257S–261S
Collins SA, Ten Cate C (1996) Does beak colour affect female preference in zebra finches. Anim Behav 52:105–112
Doutrelant C, McGregor PK, Oliveira RF (2001) The effect of an audience on intrasexual communication in male Siamese fighting fish, Betta splendens. Behav Ecol 12:283–286
Endler JA (1980) Natural selection on color patterns in Poecilia reticulata. J Nutr 134:257S–261S
Endler JA (1983) Natural and sexual selection on color pattern in poeciliid fishes. Env Biol Fish 9:173–190
Endler JA (1990) On the measurement and classification of colour in studies of animal colour patterns. Biol J Linn Soc 41:315–352
Faivre B, Grégoire A, Préault M, Cézilly F, Sorci G (2003) Immune activation rapidly mirrored in a secondary sexual trait. Science 300:103
Freeberg TD (2004) Social transmission of courtship behavior and mating preferences in brown–headed cowbirds Molothrus ater. Learn Behav 32:122–130
Furr HC, Clark RM (2004) Intestinal absorption and tissue distribution of carotenoids. J Nutr Biochem 8:364–377
Gwinner H, Van’t Hof T, Zeman M (2002) Hormonal and behavioral responses of starlings during a confrontation with males or females at nest boxes during the reproduction season. Hormo Behav 42:21–31
Hill GE (1990) Female house finches prefer colourful males: sexual selection for a condition-dependent trait. Anim Behav 40:563–572
Hill GE (1991) Plumage coloration is a sexually selected indicator of male quality. Nature 350:337–339
Kodric-Brown A (1985) Female preference and sexual selection for male coloration in the guppy (Poecilia reticulata). Behav Ecol Sociobiol 17:199–206
Kodric-Brown A (1989) Dietary carotenoids and male mating success in guppy: an environmental component to female choice. Am Nat 124:309–323
Leonard ML, Horn AG (2001) Begging in the absence of parents by nestling tree swallows. Behav Ecol 12:501–505
Lozano GA (1994) Carotenoids, parasites, and sexual selection. Oikos 70:309–311
Lozano GA (2001) Carotenoids, immunity, and sexual selection: comparing apples and oranges. Am Nat 158:200–203
Maynard Smith J, Harper D (2003) Animal signals. Oxford University Press, Oxford
McGraw KJ (2005) Interspecific variation in dietary carotenoid assimilation in birds: links to phylogeny and color ornamentation. Comp Biochem Physiol, B 142:245–250
McGraw KJ (2006) Sex steroid dependence of carotenoid-based coloration in female zebra finches. Physiol Behav 88:347–352
McGraw KJ, Ardia DR (2003) Carotenoids, immunocompetence, and the information content of sexual colors: an experimental test. Am Nat 162:704–712
McGraw KJ, Ardia DR (2004) Immunoregulatory activity of different dietary carotenoids in male zebra finches. Chemoecology 14:25–29
McGraw KJ, Correa SM, Adkins-Regan E (2006) Testosterone upregulates lipoprotein status to control sexual attractiveness in a colorful songbird. Behav Ecol Sociobiol 60:117–122
McGraw KJ, Dale J, Mackillop EA (2003) Social environment during molt and the expression of melanin-based plumage pigmentation in male house sparrows (Passer domesticus). Behav Ecol Sociobiol 53:116–122
Milinski M, Bakker TCM (1990) Female sticklebacks use male coloration in mate choice and hence avoid parasitized males. Nature 344:330–333
Mortensen A, Skibsted LH, Sampson J, Rice-Evans C, Everett SA (1997) Comparative mechanisms and rates of free radical scavenging by carotenoid antioxidants. FEBS Lett 418:91–97
Mougeot F, Redpath SM, Leckie F (2005) Ultra-violet reflectance of male and female red grouse, Lagopus lagopus scoticus: sexual ornaments reflect nematode parasite intensities. J Avian Biol 36:203–209
Mougeot F, Arroyo BE (2006) Ultraviolet reflectance by the cere of raptors. Biol Lett 2:173–176
Navara KJ, Hill GE (2004) Dietary carotenoid pigments and immune function in a songbird with extensive carotenoid-based plumage coloration. Behav Ecol 14:909–916
Parker TH, Knapp R, Rosenfield JA (2002) Social mediation of sexually selected ornamentation and steroid hormone level in male jungle fowl. Anim Behav 64:291–298
Patricelli GL, Uy JAC, Walsh G, Borgia G (2002) Male displays adjusted to female response—macho courtship by the satin bowerbird is tempered to avoid frightening the females. Nature 415:279–280
Patricelli GL, Coleman SW, Borgia G (2006) Male satin bowerbirds Ptilonorhynchus violaceus adjust their display intensity in response to female startling: an experiment with a robotic female. Anim Behav 71:49–59
Setchell JM, Dixson AF (2001) Changes in secondary sexual adornments of male mandrills (Mandrillus sphinx) are associated with gain and loss of alpha status. Hormo Behav 39:177–184
Vignal C, Mathevon N, Mottin S (2004) Audience drives male songbird response to partner's voice. Nature 430:448–451
Von Schantz T, Bensch S, Grahn M, Hasselquist D, Wittzell H (1999) Good genes, oxidative stress and condition-dependent sexual signals. Proc R Soc Lond, B 266:1–12
West MJ, King AP (1988) Female visual displays affect the development of male song on the cowbird. Nature 334:244–246
Zann RA (1996) The Zebra Finch. A Synthesis of Field and Laboratory Studies. Oxford University Press, Oxford
Zuk M, Johnsen TS (2000) Social environment and immunity in male red jungle fowl. Behav Ecol 11:146–153
Zuk M, Thornhill R, Ligon D, Johnson K, Austad S, Ligon SH, Thornhill NW, Costin C (1990) The role of male ornaments and courtship behavior in female mate choice of red jungle fowl. Am Nat 136:459–473
Acknowledgments
We thank C. Doutrelant and E. Haine for helpful comments on the manuscript, S. Garnier and C. Mondet for their technical assistance, T. Rigaud for discussion of the experimental design, and Kevin McGraw and two anonymous referees for invaluable comments on the manuscript. This work was supported by the Office nacional de la chasse et de la faune sauvage (research fund to BF and CE), the Fond Social Européen (grant to CE) and the Conseil Régional de Bourgogne (grant to CE). This work was carried out in compliance with French laws governing experiments on animals (B. F. permit n°21-CAE-085).
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by K. McGraw
Rights and permissions
About this article
Cite this article
Gautier, P., Barroca, M., Bertrand, S. et al. The presence of females modulates the expression of a carotenoid-based sexual signal. Behav Ecol Sociobiol 62, 1159–1166 (2008). https://doi.org/10.1007/s00265-008-0544-1
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00265-008-0544-1