Abstract
Sex differences in animal ornamentation are thought largely genetically fixed due to stronger sexual selection on males of species with conventional sex roles. But, other types of sex differences are not genetically fixed. For example, several differences in human social behavior result instead from sociocultural or economic constraints on women. Since gregarious animals use ornamentation for various social functions, perhaps some of their sex differences are, similarly to human behavior, due to social coercion or ecological constraint (their closest equivalents to human social and economic constraints, respectively). We found sex differences in ornamentation that disappear plastically in a social species with conventional sex roles. The red bill of common waxbills (Estrilda astrild) is on average more saturated in males, but in our experiment female bill color correlated with night temperature, an important energetic stressor, suggesting that sexual dichromatism disappears when ecological conditions are favorable to females. Female ornamentation may be more adversely affected by ecology because of their life history that requires balancing investment in ornamentation with maintaining reproductive condition. Manipulation of stress-related physiology (ACTH challenge) suggests that this effect was not mediated by stress mechanisms. Social coercion appears to not explain sexual dichromatism: males were not more aggressive than females, aggressiveness was not related to bill color, and manipulation of reproductive axis’ physiology (GnRH challenge, which in many species mediates aggressiveness) did not increase bill color. Our results show parallels to the plastic sex differences of humans in social animals and suggest that studying their ecological vs. social causes provides a biological backdrop for understanding the human case as well.
Significance statement
Many sex differences in human social behavior result from economic or sociocultural constraints on women, while sex differences in the ornamentation of animals with conventional sex roles are thought largely genetically fixed. We show that a sex difference in ornamentation—the redder bills of male than female common waxbills—disappears plastically in an animal with conventional sex roles due to, in part, changes in female ornamentation. Social coercion did not explain reduced female ornamentation: aggressiveness did not predict bill color, and males were not dominant over females. Instead, female bill color was reduced during colder weather, perhaps because females under energetic stress need to balance investment in social ornamentation vs. maintaining reproductive condition. Similarly to humans, some sex differences of gregarious animals may be due to females requiring appropriate conditions to express their full social potential.
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References
Andersson M (1994) Sexual selection. Princeton University Press, Princeton
Ardia DR, Broughton DR, Gleicher MJ (2010) Short-term exposure to testosterone propionate leads to rapid bill color and dominance changes in zebra finches. Horm Behav 58:526–532
Bakken GS, Murphy MT, Erskine DJ (1991) The effect of wind and air temperature on metabolism and evaporative water loss rates of dark-eyed juncos, Junco hyemalis: a standard operative temperature scale. Physiol Biochem Zool 64:1023–1049
Burley NT, Price DK, Zann RA (1992) Bill color, reproduction and condition effects in wild and domesticated zebra finches. Auk 109:13–23
Butler MW, Toomey MB, McGraw KJ (2011) How many color metrics do we need? Evaluating how different color-scoring procedures explain carotenoid pigment content in avian bare-part and plumage ornaments. Behav Ecol Sociobiol 65:401–413
Cardoso GC, Gomes ACR (2015a) Using reflectance ratios to study animal coloration. Evol Biol 42:387–394
Cardoso GC, Gomes ACR (2015b) Erratum to: using reflectance ratios to study animal coloration. Evol Biol 42:511–512
Cardoso GC, Batalha HR, Reis S, Lopes RJ (2014a) Increasing sexual ornamentation during a biological invasion. Behav Ecol 25:916–923
Cardoso GC, Leitão AV, Funghi C, Batalha HR, Lopes RJ, Mota PG (2014b) Similar preferences for ornamentation in opposite- and same-sex choice experiments. J Evol Biol 27:2798–2806
Clement P, Harris A, Davies J (1993) Finches and sparrows. Princeton University Press, Princeton
Clutton-Brock TH, Huchard E (2013) Social competition and selection in males and females. Philos Trans R Soc B 368:20130074
Darwin C (1871) The descent of man, and selection in relation to sex. John Murray, London
DeVries MS, Holbrook AL, Winters CP, Jawor JM (2011) Non-breeding gonadal testosterone production of male and female northern cardinals (Cardinalis cardinalis) following GnRH challenge. Gen Comp Endocrinol 174:370–378
DeWitt TJ, Sih A, Wilson DS (1998) Costs and limits of phenotypic plasticity. Trends Ecol Evol 13:77–81
Dey CJ, Valcu M, Kempenaers B, Dale J (2015) Carotenoid-based bill coloration functions as a social, not sexual, signal in songbirds (Aves: Passeriformes). J Evol Biol 28:250–258
Eagly AH, Wood W (2013) The nature-nurture debates: 25 years of challenges in understanding the psychology of gender. Perspect Psychol Sci 8:340–357
Enquist M (1985) Communication during aggressive interactions with particular reference to variation in choice of behaviour. Anim Behav 33:1152–1161
Forsgren E, Amundsen T, Borg AA, Bjelvenmark J (2004) Unusually dynamic sex roles in a fish. Nature 429:551–554
Funghi C, Leitão AV, Ferreira AC, Mota PG, Cardoso GC (2015) Social dominance in a gregarious bird is related to body size but not to standard personality assays. Ethology 121:84–93
Gautier P, Barroca M, Bertrand S, Eraud C, Gaillard M, Hamman M, Faivre B (2008) The presence of females modulates the expression of a carotenoid-based sexual signal. Behav Ecol Sociobiol 62:1159–1166
Gavasa S, Silva AC, Gonzalez E, Molina J, Stoddard PK (2012) Social competition masculinizes the communication signals of female electric fish. Behav Ecol Sociobiol 66:1057–1066
Gomes ACR, Sorenson MD, Cardoso GC (2016) Speciation is associated with changing ornamentation rather than stronger sexual selection. Evolution 70:2823–2838
Goymann W, Möstl E, Gwinner E (2002) Non-invasive methods to measure androgen metabolites in excrements of European stonechats, Saxicola torquata rubicola. Gen Comp Endocrinol 129:80–87
Gwynne DT, Simmons LW (1990) Experimental reversal of courtship roles in an insect. Nature 346:172–174
Hau M, Wikelski M, Soma KK, Wingfield JC (2000) Testosterone and year-round territorial aggression in a tropical bird. Gen Comp Endocrinol 117:20–33
Hill GE (2000) Energetic constraints on expression of carotenoid-based plumage coloration. J Avian Biol 31:559–566
Hill GE, Johnson JD (2012) The vitamin A-redox hypothesis: a biochemical basis for honest signaling via carotenoid pigmentation. Am Nat 180:E127–E150
Hill GE, Montgomerie R (1994) Plumage colour signals nutritional condition in the house finch. Proc R Soc Lond B 258:47–52
Hill GE, Hood WR, Huggins KA (2009) A multifactorial test of the effects of carotenoid access, food intake and parasite load on the production of ornamental feathers and bill coloration in American goldfinches. J Exp Biol 212:1225–1233
Hutchinson JMC, McNamara JM, Cuthill IC (1993) Song, sexual selection, starvation and strategic handicaps. Anim Behav 45:1153–1177
Iverson ENK, Karubian J (2017) The role of bare parts in avian signaling. Auk 134:587–611
Jawor JM, Mcglothlin JW, Casto JM, Greives TJ, Snajdr EA, Bntley GE, Ketterson E (2006) Seasonal and individual variation in response to GnRH challenge in male dark-eyed juncos (Junco hyemalis). Gen Comp Endocrinol 149:182–189
Jawor JM, Mcglothlin JW, Casto JM, Greives TJ, Snajdr EA, Bntley GE, Ketterson E (2007) Testosterone response to GnRH in a female songbird varies with stage of reproduction: implications for adult behaviour and maternal effects. Funct Ecol 21:767–775
Karubian J, Lindsay WR, Schwabl H, Webster MS (2011) Bill coloration, a flexible signal in a tropical passerine bird, is regulated by social environment and androgens. Anim Behav 81:795–800
Kelly R, Murphy TG, Tarvin KA, Burness G (2012) Carotenoid-based ornaments of female and male american goldfinches (Spinus tristis) show sex-specific correlations with immune function and metabolic rate. Physiol Biochem Zool 85:348–363
Kraaijeveld K, Kraaijeveld-Smit FJL, Komdeur J (2007) The evolution of mutual ornamentation. Anim Behav 74:657–677
Laucht S, Kempenaers B, Dale J (2010) Bill color, not badge size, indicates testosterone-related information in house sparrows. Behav Ecol Sociobiol 64:1461–1471
Lehikoinen E (1987) Seasonality of the daily weight cycle in wintering passerines and its consequences. Ornis Scand 18:216–226
Lessells CM, Boag PT (1987) Unrepeatable repeatabilities: a common mistake. Auk 104:116–121
Lyon BE, Montgomerie R (2012) Sexual selection is a form of social selection. Philos Trans R Soc B 367:2266–2273
Marques CIJ, Batalha HR, Cardoso GC (2016) Signalling with a cryptic trait: the regularity of barred plumage in common waxbills. R Soc Open Sci 3:160195
McGraw KJ, Schuetz JG (2004) The evolution of carotenoid coloration in estrildid finches: a biochemical analysis. Comp Biochem Physiol B 139:45–51
McGraw KJ, Toomey MB (2010) Carotenoid accumulation in the tissues of zebra finches: predictors of integumentary pigmentation and implications for carotenoid allocation strategies. Physiol Biochem Zool 83:97–109
McGraw KJ, Hill GE, Parker RS (2005) The physiological costs of being colourful: nutritional control of carotenoid utilization in the American goldfinch (Carduelis tristis). Anim Behav 69:653–660
McGraw KJ, Lee K, Lewin A (2011) The effect of capture-and-handling stress on carotenoid-based beak coloration in zebra finches. J Comp Physiol A 197:683–691
Møller AP, Birkhead TR (1994) The evolution of plumage brightness in birds is related to extra pair paternity. Evolution 48:1089–1100
Montgomerie R (2006) Analyzing colors. In: Hill GE, McGraw KJ (eds) Bird coloration, vol. 1: mechanisms and measurements. Harvard University Press, Cambridge, pp 90–147
Mundy NI, Stapley J, Bennison C, Tucker R, Twyman H, Kim K, Burke T, Birkhead TR, Andersson S, Slate J (2016) Red carotenoid coloration in the zebra finch is controlled by a cytochrome p450 gene cluster. Curr Biol 26:1435–1440
Murphy TG, Hernández-Muciño D, Osorio-Beristain M, Montgomerie R, Omland KE (2009a) Carotenoid-based status signaling by females in the tropical streak-backed oriole. Behav Ecol 20:1000–1006
Murphy TG, Rosenthal MF, Montgomerie R, Tarvin KA (2009b) Female American goldfinches use carotenoid-based bill coloration to signal status. Behav Ecol 20:1348–1355
Observatório Astronómico de Lisboa (2014) Nascimento e Ocaso do Sol (Porto), http://oal.ul.pt
Olson VA, Owens IPF (1998) Costly sexual signals: are carotenoids rare, risky or required? Trends Ecol Evol 13:510–514
Pérez-Rodríguez L (2008) Carotenoid-based ornamentation as a dynamic but consistent individual trait. Behav Ecol Sociobiol 62:995–1005
Polo V, Bautista LM (2006) Daily routines of body mass gain in birds: 1. An exponential model. Anim Behav 72:503–516
Roberts ML, Ras E, Peters A (2009) Testosterone increases UV reflectance of sexually selected crown plumage in male blue tits. Behav Ecol 20:535–541
Romero LM (2004) Physiological stress in ecology: lessons from biomedical research. Trends Ecol Evol 19:249–255
Romero LM, Soma KK, Wingfield JC (1998) Hypothalamic-pituitary-adrenal axis changes allow seasonal modulation of corticosterone in a bird. Am J Phys 274:R1338–R1344
Rosen RF, Tarvin KA (2006) Sexual signals of the male American goldfinch. Ethology 112:1008–1019
Rosenthal MF, Murphy TG, Darling N, Tarvin KA (2012) Ornamental bill color rapidly signals changing condition. J Avian Biol 43:553–564
Santos ESA, Scheck D, Nakagawa S (2011) Dominance and plumage traits: meta-analysis and metaregression analysis. Anim Behav 82:3–19
Sanz-Aguilar A, Carrete M, Edelaar P, Potti J, Tella JL (2015) The empty temporal niche: breeding phenology differs between coexisting native and invasive birds. Biol Invasions 17:3275–3288
Schull Q, Dobson FS, Stier A, Robin JP, Bize P, Viblanc VA (2016) Beak color dynamically signals changes in fasting status and parasite loads in king penguins. Behav Ecol 27:1684–1693
Silva K, Vieira MN, Almada VC, Monteiro NM (2010) Reversing sex role reversal: compete only when you must. Anim Behav 79:885–893
Simons MJP, Cohen A, Verhulst S (2012) What does carotenoid-dependent coloration tell? Plasma carotenoid level signals immune-competence and oxidative stress state in birds—a meta-analysis. PLoS One 7:e43088
Számadó S (2011) Long-term commitment promotes honest status signalling. Anim Behav 82:295–302
Tarvin KA, Wong LJ, Lumpkin DC, Schroeder GM, D'Andrea D, Meade S, Rivers P, Murphy TG (2016) Dynamic status signal reflects outcome of social interactions, but not energetic stress. Front Ecol Evol 4:79
Tobias JA, Montgomerie R, Lyon BE (2012) The evolution of female ornaments and weaponry: social selection, sexual selection and ecological competition. Philos Trans R Soc B 367:2274–2293
West-Eberhard MJ (1979) Sexual selection, social competition, and evolution. PAm Philos Soc 123:222–234
West-Eberhard MJ (2003) Developmental plasticity and evolution. Oxford University Press, New York
Wharton AS (2012) The sociology of gender: an introduction to theory and research, 2nd edn. Wiley, Chichester
Wingfield JC (1984) Influence of weather on reproduction. J Exp Zool 232(3):589–594
Wingfield JC, O’Reilly KM, Astheimer LB (1995) Modulation of the adrenocortical responses to acute stress in arctic birds: a possible ecological basis. Integr Comp Biol 35:285–294
Wingfield JC, Lynn SE, Soma KK (2001) Avoiding the “costs” of testosterone: ecological bases of hormone-behavior interactions. Brain Behav Evol 57:239–251
Witter MS, Cuthill IC (1993) The ecological costs of avian fat storage. Philos Trans R Soc B 340:73–92
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We would like to thank the anonymous reviewers for valuable comments that much improved this article.
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This work was funded by grant PTDC/BIA-EVF/116758/2010, and fellowships SFRH/BPD/46873/2008 and SFRH/BPD/110165/2015 from the Fundação para a Ciência e a Tecnologia.
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Funghi, C., Trigo, S., Gomes, A.C.R. et al. Release from ecological constraint erases sex difference in social ornamentation. Behav Ecol Sociobiol 72, 67 (2018). https://doi.org/10.1007/s00265-018-2486-6
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DOI: https://doi.org/10.1007/s00265-018-2486-6