Skip to main content
Log in

Immune challenged male Iberian green lizards may increase the expression of some sexual signals if they have supplementary vitamin E

  • Original Article
  • Published:
Behavioral Ecology and Sociobiology Aims and scope Submit manuscript

Abstract

Honesty of sexual signals demands a link between the signal and fitness of the signalers, which can be based on the costs of the signal and trade-offs between signal development and essential physiological functions, such as the immune defense or the antioxidant system. We experimentally challenged the immune system of male lizards Lacerta schreiberi with a bacterial antigen (lipopolysaccharide; LPS). We explored whether the immune activation influenced structural- and pigment-based visual signals and chemical signals. Furthermore, we examined the interactive effects of the immune activation with a vitamin E dietary supplementation, as this vitamin has important antioxidant functions in an immune challenged situation. Contrary to expected, lizards that suffered an immune challenge alone did not decrease the brightness or saturation of visual signals, and even, when challenged lizards had supplementary vitamin E, they were able to increase saturation of UV-blue throat coloration. Similarly, vitamin E supplementation allowed challenged males to maintain high levels of secretion of this vitamin in chemical signals. Males with an immune challenge would have low long-term expectatives of survival and future reproduction and, therefore, these challenged males, especially those with supplementary resources (vitamin E), might try to maximize their current fitness by investing in costly sexual signals, instead of compensating the negative physiological effects of the immune activation. Surprisingly, vitamin E alone did not affect structural and/or melanin-based coloration, but decreased carotenoid-based coloration, which was opposite to a previous experiment when climatic conditions in the year of study were more favorable. This might be explained if females showed flexible mate choice, selecting the type of signals that more reliably indicate male quality under different environmental circumstances.

Significance statement

The trade-offs between sexual signals and the immune and antioxidant systems, which allow honesty of signals, are little investigated, especially in reptiles. We examined in a lizard with multiple types of signals (UV-blue throat, yellow chest and green dorsal coloration, and chemical signals) the effects of a simulated immune challenge on these signals. Furthermore, we studied the interactions with vitamin E in the diet, as this is an important antioxidant and immunostimulant. Surprisingly, carotenoid-based signals were not influenced by the immune activation, but throat blue and UV of color patches increased when challenged males had more available vitamin E. This suggests that challenged, apparently ill, males might try to maximize their current mating success because their survivorship probabilities were low. Additionally, climatic differences and flexible female mate choice might explain the different effects of vitamin E observed in different years.

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

Access this article

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
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

References

  • Abd Hamid N, Hasrul MA, Ruzanna RJ, Ibrahim IA, Baruah PS, Mazlan M, Mohd Yusof YA, Wan Ngah WZ (2011) Effect of vitamin E (Tri E®) on antioxidant enzymes and DNA damage in rats following eight weeks exercise. Nutr J 10:37

  • Aguiló A, Tauler P, Fuentespina E, Tur JA, Córdova A, Pons A (2005) Antioxidant response to oxidative stress induced by exhaustive exercise. Physiol Behav 84:1–7

    Article  PubMed  CAS  Google Scholar 

  • Aitchison J (1986) The statistical analysis of compositional data. Chapman and Hall, London

    Book  Google Scholar 

  • Allen DG, Pringle JK, Smith DA, Pasloske K, Day K (2004) Handbook of veterinary drugs. Lippincott-Raven Publishers, Philadelphia

  • Alonso-Alvarez C, Bertrand S, Devevey G, Gaillard M, Prost J, Faivre B, Sorci G (2004) An experimental test of the dose-dependent effect of carotenoids and immune activation on sexual signals and antioxidant activity. Am Nat 164:651–659

    PubMed  Google Scholar 

  • Amar EC, Kiron V, Satoh S, Okamoto N, Watanabe T (2000) Effects of dietary β-carotene on the immune response of rainbow trout Oncorhynchus mykiss. Fisheries Sci 66:1068–1075

    Article  CAS  Google Scholar 

  • Anderson ME (1998) Glutathione: an overview of biosynthesis and modulation. Chem Biol Interact 111:1–14

    Article  PubMed  Google Scholar 

  • Andersson S, Prager M (2006) Quantifying colors. In: Hill GE, McGraw KJ (eds) Bird coloration, vol. 1. Mechanisms and measurements. Harvard University Press, Cambridge, pp 41–89

    Google Scholar 

  • Aydilek N, Aksakal M, Karakılçık AZ (2004) Effects of testosterone and vitamin E on the antioxidant system in rabbit testis. Andrologia 36:277–281

    Article  PubMed  CAS  Google Scholar 

  • Bagnara JT, Taylor JD, Hadley ME (1968) The dermal chromatophore unit. J Cell Biol 38:67–79

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bajer K, Molnár O, Török J, Herczeg G (2010) Female European green lizards (Lacerta viridis) prefer males with high ultraviolet throat reflectance. Behav Ecol Sociobiol 64:2007–2014

    Article  Google Scholar 

  • Bajer K, Molnár O, Török J, Herczeg G (2011) Ultraviolet nuptial colour determines fight success in male European green lizard (Lacerta viridis). Biol Lett 7:866–868

    Article  PubMed  PubMed Central  Google Scholar 

  • Bajer K, Molnár O, Török J, Herczeg G (2012) Temperature, but not available energy, affects the expression of a sexually selected ultraviolet (UV) colour trait in male European green lizards. PLoS One 7:e34359

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ballen C, Healey M, Wilson M, Tobler M, Wapstra E, Olsson M (2012) Net superoxide levels: steeper increase with activity in cooler female and hotter male lizards. J Exp Biol 215:731–735

    Article  PubMed  Google Scholar 

  • Basu HN, Del Vecchio AJ, Flider F, Orthoeter FT (2001) Nutritional and potential disease prevention properties of carotenoids. J Am Oil Chem Soc 78:665–675

    Article  CAS  Google Scholar 

  • Bender DA (2009) Nutritional biochemistry of the vitamins. Cambridge University Press, Cambridge

  • Biard C, Surai PF, Møller AP (2006) Carotenoid availability in diet and phenotype of blue and great tit nestlings. J Exp Biol 209:1004–1015

    Article  PubMed  CAS  Google Scholar 

  • Blount JD, Metcalfe NB, Birkhead TR, Surai PF (2003) Carotenoid modulation of immune function and sexual attractiveness in zebra finches. Science 300:125–127

    Article  PubMed  CAS  Google Scholar 

  • Boillat M, Challet L, Rossier D, Kan C, Carleton A, Rodriguez I (2015) The vomeronasal system mediates sick conspecific avoidance. Curr Biol 25:251–255

    Article  PubMed  CAS  Google Scholar 

  • Bonneaud C, Mazuc J, Gonzalez G, Haussy C, Chastel O, Faivre B, Sorci G (2003) Assessing the cost of mounting an immune response. Am Nat 161:367–379

    Article  PubMed  Google Scholar 

  • Bonser RH (1995) Melanin and the abrasion resistance of feathers. Condor 97:590–591

    Article  Google Scholar 

  • Boonekamp JJ, Ros AH, Verhulst S (2008) Immune activation suppresses plasma testosterone level: a meta-analysis. Biol Lett 4:741–744

    Article  PubMed  PubMed Central  Google Scholar 

  • Boswell T, Takeuchi S (2005) Recent developments in our understanding of the avian melanocortin system: its involvement in the regulation of pigmentation and energy homeostasis. Peptides 26:1733–1743

    Article  PubMed  CAS  Google Scholar 

  • Bowers RR, Biboso A, Chavez O (1997) The role of alpha-MSH, its agonists, and c-AMP in in vitro avian melanocytes. Pigment Cell Res 10:41–45

  • Brigelius-Flohe R, Traber MG (1999) Vitamin E: function and metabolism. FASEB J 13:1145–1155

    Article  PubMed  CAS  Google Scholar 

  • Bruno RS, Ramakrishnan R, Montine TJ, Bray TM, Traber MG (2005) α-tocopherol disappearance is faster in cigarette smokers and is inversely related to their ascorbic acid status. Am J Clin Nutr 81:95–103

    Article  PubMed  CAS  Google Scholar 

  • Buettner GR (1993) The pecking order of free radicals and antioxidants: lipid peroxidation, α-tocopherol, and ascorbate. Arch Biochem Biophys 300:535–543

    Article  PubMed  CAS  Google Scholar 

  • Chaine AS, Lyon BE (2008) Adaptive plasticity in female mate choice dampens sexual selection on male ornaments in the lark bunting. Science 319:459–462

    Article  PubMed  CAS  Google Scholar 

  • Chew BP, Park JS (2004) Carotenoid action on the immune response. J Nutr 134:257–261

    Article  Google Scholar 

  • Clotfelter ED, Ardia DR, McGraw KJ (2007) Red fish, blue fish: trade-offs between pigmentation and immunity in Betta splendens. Behav Ecol 18:1139–1145

    Article  Google Scholar 

  • Cloudsley-Thompson JL (1999) Multiple factors in the evolution of animal coloration. Naturwissenschaften 86:123–132

    Article  PubMed  CAS  Google Scholar 

  • Coleman JW (2001) Nitric oxide in immunity and inflammation. Int Immunopharmacol 1:1397–1406

    Article  PubMed  CAS  Google Scholar 

  • Costagliola C, Luliano G, Menzione M, Rinaldi E, Vito P, Auricchio G (1986) Effect of vitamin E on glutathione content in red blood cells, aqueous humor and lens of humans and other species. Exp Eye Res 43:905–914

    Article  PubMed  CAS  Google Scholar 

  • Cote J, Meylan S, Clobert J, Voituron Y (2010) Carotenoid-based coloration, oxidative stress and corticosterone in common lizards. J Exp Biol 213:2116–2124

    Article  PubMed  CAS  Google Scholar 

  • Cuthill IC, Bennett ATD, Partridge JC, Maier EJ (1999) Plumage reflectance and the objective assessment of avian sexual dichromatism. Am Nat 153:183–200

    Article  PubMed  CAS  Google Scholar 

  • Dantzer R (2001) Cytokine-induced sickness behavior: where do we stand? Brain Behav Immun 15:7–24

    Article  PubMed  CAS  Google Scholar 

  • Deen CM, Hutchison VH (2001) Effects of lipopolysaccharide and acclimation temperature on induced behavioral fever in juvenile Iguana iguana. J Therm Biol 26:55–63

    Article  PubMed  CAS  Google Scholar 

  • de Pérez i Lanuza G, Font E (2014a) Ultraviolet vision in lacertid lizards: evidence from retinal structure, eye transmittance, SWS1 visual pigment genes, and behaviour. J Exp Biol 217:2899–2909

  • de Pérez i Lanuza G, Font E (2014b) Now you see me, now you don’t: iridescence increases the efficacy of lizard chromatic signals. Naturwissenschaften 101:831–837

  • de Pérez i Lanuza G, Font E (2016) The evolution of colour pattern complexity: selection for conspicuousness favours contrasting within-body colour combinations in lizards. J Evol Biol 29:942–951

  • de Pérez i Lanuza G, Carazo P, Font E (2014) Colours of quality: structural (but not pigment) coloration informs about male quality in a polychromatic lizard. Anim Behav 90:73–81

  • Di Mascio P, Murphy ME, Sies H (1991) Antioxidant defense systems: the role of carotenoids, tocopherols, and thiols. Am J Clin Nutr 53:194–200

    Article  Google Scholar 

  • Diep SK, Westneat DF (2013) The integration of function and ontogeny in the evolution of status signals. Behaviour 150:1015–1044

    Google Scholar 

  • Doucet SM, Meadows MG (2009) Iridescence: a functional perspective. J R Soc Interface 6:115–132

    Article  Google Scholar 

  • Ducrest A-L, Keller L, Roulin A (2008) Pleiotropy in the melanocortin system, coloration and behavioural syndromes. Trends Ecol Evol 23:502–510

    Article  PubMed  Google Scholar 

  • Endler JA (1990) On the measurement and classification of colour in studies of animal colour patterns. Biol J Linn Soc 41:315–352

    Article  Google Scholar 

  • Faivre B, Grégoire A, Préault M, Cézilly F, Sorci G (2003) Immune activation rapidly mirrored in a secondary sexual trait. Science 300:103

    Article  PubMed  CAS  Google Scholar 

  • Feingold KR, Grunfeld C (1992) Role of cytokines in inducing hyperlipidemia. Diabetes 41:97–101

    Article  PubMed  CAS  Google Scholar 

  • Fitze PS, Tschirren B, Gasparini J, Richner H (2007) Carotenoid-based plumage colors and immune function: is there a trade-off for rare carotenoids? Am Nat 169:137–144

    Google Scholar 

  • Fleishman LJ, Loew ER, Leal M (1993) Ultraviolet vision in lizards. Nature 365:397

    Article  Google Scholar 

  • Fox DL (1979) Biochromy, natural coloration of living things. University of California Press, Berkeley

    Google Scholar 

  • French SS, DeNardo DF, Moore MC (2007) Trade-offs between the reproductive and immune systems: facultative responses to resources or obligate responses to reproduction? Am Nat 170:79–89

    PubMed  Google Scholar 

  • Galván I, Alonso-Alvarez C (2008) An intracellular antioxidant determines the expression of a melanin-based signal in a bird. PLoS One 3:e3335

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Galván I, Alonso-Alvarez C (2009) The expression of melanin-based plumage is separately modulated by exogenous oxidative stress and a melanocortin. Proc R Soc Lond B 276:3089–3097

    Article  CAS  Google Scholar 

  • Galván I, Alonso-Alvarez C (2010) Yolk testosterone shapes the expression of a melanin-based signal in great tits: an antioxidant-mediated mechanism? J Exp Biol 213:3127–3130

    Article  PubMed  CAS  Google Scholar 

  • Galván I, Solano F (2009) The evolution of eu-and pheomelanic traits may respond to an economy of pigments related to environmental oxidative stress. Pigm cell. Melanoma Res 22:339–342

    Article  CAS  Google Scholar 

  • Galván I, Solano F (2015) Melanin chemistry and the ecology of stress. Physiol Biochem Zool 88:352–355

    Article  PubMed  Google Scholar 

  • Garant D, Sheldon BC, Gustafsson L (2004) Climatic and temporal effects on the expression of secondary sexual characters: genetic and environmental components. Evolution 58:634–644

    Article  PubMed  Google Scholar 

  • Garbe A, Buck J, Hämmerling U (1992) Retinoids are important cofactors in T cell activation. J Exp Med 176:109–117

    Article  PubMed  CAS  Google Scholar 

  • Geissmann F, Revy P, Brousse N, Lepelletier Y, Folli C, Durandy A, Chambon P, Dy M (2003) Retinoids regulate survival and antigen presentation by immature dendritic cells. J Exp Med 198:623–634

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Goodwin TW (1986) Metabolism, nutrition, and function of carotenoids. Annu Rev Nutr 6:273–297

    Article  PubMed  CAS  Google Scholar 

  • Grether GF, Kolluru GR, Nersissian K (2004) Individual colour patches as multicomponent signals. Biol Rev 79:583–610

    Article  PubMed  Google Scholar 

  • Grill CP, Rush VN (2000) Analysing spectral data: comparison and application of two techniques. Biol J Linn Soc 69:121–138

    Article  Google Scholar 

  • Halliwell B, Gutteridge JM (2015) Free radicals in biology and medicine. Oxford University Press, Oxford

    Book  Google Scholar 

  • Hartley RC, Kennedy MW (2004) Are carotenoids a red herring in sexual display? Trends Ecol Evol 19:353–354

    Article  PubMed  Google Scholar 

  • Hegyi G, Török J, Garamszegi LZ, Rosivall B, Szöllősi E, Hargitai R (2007) Dynamics of multiple sexual signals in relation to climatic conditions. Evol Ecol Res 9:905–920

    Google Scholar 

  • Hong JH, Kim M-J, Park MR, Kwag OG, Lee IS, Byun BH, Leef SC, Leeg KB, Rhee SJ (2004) Effects of vitamin E on oxidative stress and membrane fluidity in brain of streptozotocin-induced diabetic rats. Clin Chim Acta 340:107–115

    Article  PubMed  CAS  Google Scholar 

  • Hõrak P, Zilmer M, Saks L, Ots I, Karu U, Zilmer K (2006) Antioxidant protection, carotenoids and the costs of immune challenge in greenfinches. J Exp Biol 209:4329–4338

    Article  PubMed  CAS  Google Scholar 

  • Huang Q-H, Hruby VJ, Tatro JB (1999) Role of central melanocortins in endotoxin-induced anorexia. Am J Physiol-Reg I 276:864–871

    Google Scholar 

  • Husvéth F, Manilla HA, Gaál T, Vajdovich P, Balogh N, Wágner L, Lóth I, Németh K (2000) Effects of saturated and unsaturated fats with vitamin E supplementation on the antioxidant status of broiler chicken tissues. Acta Veter Hung 48:69–79

    Article  Google Scholar 

  • Ibáñez A, Polo-Cavia N, López P, Martín J (2014) Honest sexual signaling in turtles: experimental evidence of a trade-off between immune response and coloration in red-eared sliders Trachemys scripta elegans. Naturwissenschaften 101:803–811

    Article  PubMed  CAS  Google Scholar 

  • Jacot A, Romero-Diaz C, Tschirren B, Richner H, Fitze PS (2010) Dissecting carotenoid from structural components of carotenoid-based coloration: a field experiment with great tits (Parus major). Am Nat 176:55–62

    Article  PubMed  Google Scholar 

  • Jacquin L, Lenouvel P, Haussy C, Ducatez S, Gasparini J (2011) Melanin-based coloration is related to parasite intensity and cellular immune response in an urban free living bird: the feral pigeon Columba livia. J Avian Biol 42:11–15

    Article  Google Scholar 

  • Janeway CA, Travers P, Walport M, Shlomchik M (2001) Immunobiology. The immune system in health and disease, 5th edn. Garland Publishing, New York

    Google Scholar 

  • Ji LL (1999) Antioxidants and oxidative stress in exercise. Exp Biol Med 222:283–292

    Article  CAS  Google Scholar 

  • Kahn AT, Dolstra T, Jennions MD, Backwell PR (2013) Strategic male courtship effort varies in concert with adaptive shifts in female mating preferences. Behav Ecol 24:906–913

    Article  Google Scholar 

  • Kemp DJ, Rutowski RL (2007) Condition dependence, quantitative genetics, and the potential signal content of iridescent ultraviolet butterfly coloration. Evolution 61:168–183

    Article  PubMed  Google Scholar 

  • Kimball BA, Opiekun M, Yamazaki K, Beauchamp GK (2014) Immunization alters body odor. Physiol Behav 128:80–85

    Article  PubMed  CAS  Google Scholar 

  • Klukowski M, Nelson CE (2001) Ectoparasite loads in free-ranging northern fence lizards, Sceloporus undulatus hyacinthinus: effects of testosterone and sex. Behav Ecol Sociobiol 49:289–295

    Article  Google Scholar 

  • Kopena R, Martín J, López P, Herczeg G (2011) Vitamin E supplementation increases the attractiveness of males’ scent for female European green lizards. PLoS One 6:e19410

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kopena R, López P, Martín J (2014a) Relative contribution of dietary carotenoids and vitamin E to visual and chemical sexual signals of male Iberian green lizards: an experimental test. Behav Ecol Sociobiol 68:571–581

    Article  Google Scholar 

  • Kopena R, López P, Martín J (2014b) What are carotenoids signaling? Immunostimulatory effects of dietary vitamin E, but not of carotenoids, in Iberian green lizards. Naturwissenschaften 101:1107–1114

    Article  PubMed  CAS  Google Scholar 

  • Krinsky NI, Yeum KJ (2003) Carotenoid–radical interactions. Biochem Biophys Res Commun 305:754–760

    Article  PubMed  CAS  Google Scholar 

  • Lewis AC, Rankin KJ, Pask AJ, Stuart-Fox D (2017) Stress-induced changes in color expression mediated by iridophores in a polymorphic lizard. Ecol Evol 7:8262–8272

  • Ligon RA, McCartney KL (2016) Biochemical regulation of pigment motility in vertebrate chromatophores: a review of physiological color change mechanisms. Curr Zool 62:237–252

    Article  PubMed  PubMed Central  Google Scholar 

  • Lin SM, Nieves-Puigdoller K, Brown AC, McGraw KJ, Clotfelter ED (2010) Testing the carotenoid trade-off hypothesis in the polychromatic midas cichlid, Amphilophus citrinellus. Physiol Biochem Zool 83:333–342

    Article  PubMed  CAS  Google Scholar 

  • Loew ER, Fleishman LJ, Foster RG, Provencio I (2002) Visual pigments and oil droplets in diurnal lizards: a comparative study of Caribbean anoles. J Exp Biol 205:927–938

    PubMed  Google Scholar 

  • López P, Martín J (2006) Lipids in the femoral gland secretions of male Schreiber’s green lizards, Lacerta schreiberi. Z Naturforsch C 61:763–768

    Article  PubMed  Google Scholar 

  • López P, Amo L, Martín J (2006) Reliable signaling by chemical cues of male traits and health state in male lizards, Lacerta monticola. J Chem Ecol 32:473–488

    Article  PubMed  CAS  Google Scholar 

  • López P, Gabirot M, Martín J (2009a) Immune challenge affects sexual coloration of male Iberian wall lizards. J Exp Zool A 311:96–104

    Article  Google Scholar 

  • López P, Gabirot M, Martín J (2009b) Immune activation affects chemical sexual ornaments of male Iberian wall lizards. Naturwissenschaften 96:65–69

    Article  PubMed  CAS  Google Scholar 

  • Loyau A, Saint Jalme M, Cagniant C, Sorci G (2005) Multiple sexual advertisements honestly reflect health status in peacocks (Pavo cristatus). Behav Ecol Sociobiol 58:552–557

    Article  Google Scholar 

  • Mackintosh JA (2001) The antimicrobial properties of melanocytes, melanosomes and melanin and the evolution of black skin. J Theor Biol 211:101–113

    Article  PubMed  CAS  Google Scholar 

  • Mader DR (1996) Reptile medicine and surgery. WB Saunders, Philadelphia

    Google Scholar 

  • Martín J, López P (2006) Vitamin D supplementation increases the attractiveness of males’ scent for female Iberian rock lizards. Proc R Soc Lond B 273:2619–2624

    Article  CAS  Google Scholar 

  • Martín J, López P (2009) Multiple color signals may reveal multiple messages in male Schreiber’s green lizards, Lacerta schreiberi. Behav Ecol Sociobiol 63:1743–1755

    Article  Google Scholar 

  • Martín J, López P (2010) Multimodal sexual signals in male ocellated lizards Lacerta lepida: vitamin E in scent and green coloration may signal male quality in different sensory channels. Naturwissenschaften 97:545–553

    Article  PubMed  CAS  Google Scholar 

  • Martin M, Le Galliard JF, Meylan S, Loew ER (2015) The importance of ultraviolet and near-infrared sensitivity for visual discrimination in two species of lacertid lizards. J Exp Biol 218:458–465

    Article  PubMed  Google Scholar 

  • Maynard-Smith J, Harper D (2003) Animal signals. Oxford University Press, Oxford

    Google Scholar 

  • McGraw KJ (2008) An update on the honesty of melanin-based color signals in birds. Pigm cell. Melanoma Res 21:133–138

    Article  Google Scholar 

  • McGraw KJ, Ardia DR (2003) Carotenoids, immunocompetence, and the information content of sexual colors: an experimental test. Am Nat 162:704–712

    Article  PubMed  Google Scholar 

  • McGraw KJ, Crino OL, Medina-Jerez W, Nolan PM (2006a) Effect of dietary carotenoid supplementation on food intake and immune function in a songbird with no carotenoid coloration. Ethology 112:1209–1216

    Article  Google Scholar 

  • McGraw KJ, Klasing KC, Dufty AM (2006b) Carotenoids, immunity, and integumentary coloration in red junglefowl (Gallus gallus). Auk 123:1161–1171

    Google Scholar 

  • Megía-Palma R (2016) Molecular characterization of lizard parasites and their influence on colour ornaments. Universidad Complutense de Madrid, Madrid, PhD Dissertation

    Google Scholar 

  • Megía-Palma R, Martínez J, Merino S (2016a) A structural colour ornament correlates positively with parasite load and body condition in an insular lizard species. Sci Nat 103:1–10

    Article  CAS  Google Scholar 

  • Megía-Palma R, Martínez J, Merino S (2016b) Structural- and carotenoid-based throat colour patches in males of Lacerta schreiberi reflect different parasitic diseases. Behav Ecol Sociobiol 70:2017–2025

    Article  Google Scholar 

  • Megía-PalmaR, MartínezJ, MerinoS (2017) Manipulation of parasite load induces significant changes in the structural-based throat color of male Iberian green lizards. Curr Zool: 1–10. https://doi.org/10.1093/cz/zox036

  • Mohagheghpour N, Waleh N, Garger SJ, Dousman L, Grill LK, Tusé D (2000) Synthetic melanin suppresses production of proinflammatory cytokines. Cell Immunol 199:25–36

    Article  PubMed  CAS  Google Scholar 

  • Molnár O, Bajer K, Török J, Herczeg G (2012) Individual quality and nuptial throat colour in male European green lizards. J Zool 287:233–239

    Article  Google Scholar 

  • Molnár O, Bajer K, Mészáros B, Török J, Herczeg G (2013) Negative correlation between nuptial throat colour and blood parasite load in male European green lizards supports the Hamilton–Zuk hypothesis. Naturwissenschaften 100:551–558

    Article  PubMed  CAS  Google Scholar 

  • Monaghan P, Metcalfe NB, Torres R (2009) Oxidative stress as a mediator of life history trade-offs: mechanisms, measurements and interpretation. Ecol Lett 12:75–92

    Article  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Moran NA, Jarvik T (2010) Lateral transfer of genes from fungi underlies carotenoid production in aphids. Science 328:624–627

    Article  PubMed  CAS  Google Scholar 

  • Nathan C, Shiloh MU (2000) Reactive oxygen and nitrogen intermediates in the relationship between mammalian hosts and microbial pathogens. P Natl Acad Sci USA 97:8841–8848

    Article  CAS  Google Scholar 

  • Navara KJ, Hill GE (2003) Dietary carotenoid pigments and immune function in a songbird with extensive carotenoid-based plumage coloration. Behav Ecol 14:909–916

    Article  Google Scholar 

  • Niki E, Tsuchiya J, Tanimura R, Kamiya Y (1982) Regeneration of vitamin E from α-chromanoxyl radical by glutathione and vitamin C. Chem Lett 11:789–792

    Article  Google Scholar 

  • Olsson M, Wapstra E, Madsen T, Silverin B (2000) Testosterone, ticks and travels: a test of the immunocompetence-handicap hypothesis in free-ranging male sand lizards. Proc R Soc Lond B 267:2339–2343

    Article  CAS  Google Scholar 

  • Olsson MJ, Lundström JN, Kimball BA et al (2014) The scent of disease human body odor contains an early chemosensory cue of sickness. Psychol Sci 25:817–823

    Article  PubMed  Google Scholar 

  • Ortonne JP (2002) Photoprotective properties of skin melanin. Brit J Dermatol 146:7–10

    Article  CAS  Google Scholar 

  • Palozza P (1998) Prooxidant actions of carotenoids in biologic systems. Nutr Rev 56:257–265

    Article  PubMed  CAS  Google Scholar 

  • Pearson AK, Tsui HW, Licht P (1976) Effect of temperature on spermatogenesis, on the production and action of androgens and on the ultrastructure of gonadotropic cells in the lizard Anolis carolinensis. J Exp Zool A 195:291–303

    Article  CAS  Google Scholar 

  • Prota G (2012) Melanins and melanogenesis. Academic Press, San Diego

    Google Scholar 

  • Quinn VS, Hews DK Positive relationship between abdominal coloration and dermal melanin density in phrynosomatid lizards. Copeia 2003, 2003:858–864

  • Reguera S, Zamora-Camacho FJ, Moreno-Rueda G (2014) The lizard Psammodromus algirus (Squamata: Lacertidae) is darker at high altitudes. Biol J Linn Soc 112:132–141

    Article  Google Scholar 

  • Rohrlich S (1974) Fine structural demonstration of ordered arrays of cytoplasmic filaments in vertebrate iridophores. J Cell Biol 62:295–304

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rojas C, Cadenas S, Lopez-Torres M, PerezCampo R, Barja G (1996) Increase in heart glutathione redox ratio and total antioxidant capacity and decrease in lipid peroxidation after vitamin E dietary supplementation in guinea pigs. Free Radic Biol Med 21:907–915

    Article  PubMed  CAS  Google Scholar 

  • Ruiz M, Wang D, Reinke BA, Demas GE, Martins EP (2011) Trade-offs between reproductive coloration and innate immunity in a natural population of female sagebrush lizards, Sceloporus graciosus. Herpetol J 21:131–134

    PubMed  PubMed Central  Google Scholar 

  • Saenko SV, Teyssier J, Van Der Marel D, Milinkovitch MC (2013) Precise colocalization of interacting structural and pigmentary elements generates extensive color pattern variation in Phelsuma lizards. BMC Biol 11:105

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • San-Jose LM, Granado-Lorencio F, Sinervo B, Fitze PS (2013) Iridophores and not carotenoids account for chromatic variation of carotenoid-based coloration in common lizards (Lacerta vivipara). Am Nat 181:396–409

    Article  PubMed  Google Scholar 

  • Santos ES, Scheck D, Nakagawa S (2011) Dominance and plumage traits: meta-analysis and metaregression analysis. Anim Behav 82:3–19

    Article  Google Scholar 

  • Sasaki M, Horikoshi T, Uchiwa H, Miyachi Y (2000) Up-regulation of tyrosinase gene by nitric oxide in human melanocytes. Pigment Cell Res 13:248–252

    Article  PubMed  CAS  Google Scholar 

  • Seagle B-LL, Rezai KA, Kobori Y, Gasyna EM, Rezaei KA, Norris JR (2005) Melanin photoprotection in the human retinal pigment epithelium and its correlation with light-induced cell apoptosis. P Natl Acad Sci USA 102:8978–8983

    Article  CAS  Google Scholar 

  • Searcy WA, Nowicki S (2005) The evolution of animal communication: reliability and deception in signaling systems. Princeton University Press, Princeton

    Google Scholar 

  • Selman C, McLaren JS, Himanka MJ, Speakman JR (2000) Effect of long-term cold exposure on antioxidant enzyme activities in a small mammal. Free Radic Biol Med 28:1279–1285

    Article  PubMed  CAS  Google Scholar 

  • Sergeyev V, Broberger C, Hökfelt T (2001) Effect of LPS administration on the expression of POMC, NPY, galanin, CART and MCH mRNAs in the rat hypothalamus. Mol Brain Res 90:93–100

    Article  PubMed  CAS  Google Scholar 

  • Shawkey MD, Hill GE (2005) Carotenoids need structural colours to shine. Biol Lett 1:121–124

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Slominski A, Tobin DJ, Shibahara S, Wortsman J (2004) Melanin pigmentation in mammalian skin and its hormonal regulation. Physiol Rev 84:1155–1228

    Article  PubMed  CAS  Google Scholar 

  • Sokal RR, Rohlf FJ (1995) Biometry, 3rd edn. WHFreeman, New York

    Google Scholar 

  • Solano F, García-Borrón JC (2006) Enzymology of melanin formation. In: Nordlund JJ, Boissy RE, Hearing VJ, King RA, Oetting WS, Ortonne JP (eds) The pigmentary system: physiology and pathophysiology, 2nd edn. Blackwell, Oxford, pp 261–281

  • Staszewski V, Boulinier T (2004) Vaccination: a way to address questions in behavioral and population ecology? Trends Parasitol 20:17–22

    Article  PubMed  Google Scholar 

  • Surai PF (2002) Natural antioxidants in avian nutrition and reproduction. Nottingham University Press, Nottingham

    Google Scholar 

  • Sutherland JL, Thompson CF, Sakaluk SK (2012) No effect of carotenoid supplementation on phytohemagglutinin response or body condition of nestling house wrens. Physiol Biochem Zool 85:21–28

    Article  PubMed  CAS  Google Scholar 

  • Toomey MB, Butler MW, McGraw KJ (2010) Immune-system activation depletes retinal carotenoids in house finches (Carpodacus mexicanus). J Exp Biol 213:1709–1716

    Article  PubMed  CAS  Google Scholar 

  • Torres R, Velando A (2007) Male reproductive senescence: the price of immune-induced oxidative damage on sexual attractiveness in the blue-footed booby. J Anim Ecol 76:1161–1168

    Article  PubMed  Google Scholar 

  • Tsatmali M, Graham A, Szatkowski D, Ancans J, Manning P, McNeil CJ, Graham AM, Thody AJ (2000) α-melanocyte-stimulating hormone modulates nitric oxide production in melanocytes. J Invest Dermatol 114:520–526

    Article  PubMed  CAS  Google Scholar 

  • Uller T, Isaksson C, Olsson M (2006) Immune challenge reduces reproductive output and growth in a lizard. Funct Ecol 20:873–879

    Article  Google Scholar 

  • Umeda F, Kato K, Muta K, Ibayashi H (1982) Effect of vitamin E on function of pituitary-gonadal axis in male rats and human subjects. Endocrinol Jpn 29:287–292

    Article  PubMed  CAS  Google Scholar 

  • Vroonen J, Vervust B, Van Damme R (2013) Melanin-based colouration as a potential indicator of male quality in the lizard Zootoca vivipara (Squamata: Lacertidae). Amphibia-Reptilia 34:539–549

    Article  Google Scholar 

  • Wedekind C (1992) Detailed information about parasites revealed by sexual ornamentation. Proc R Soc Lond B 247:169–174

    Article  Google Scholar 

  • Wedekind C, Folstad I (1994) Adaptive or nonadaptive immunosuppression by sex hormones? Am Nat 143:936–938

    Article  Google Scholar 

  • Wu D, Meydani SN (1998) N-3 polyunsaturated fatty acids and immune function. Proc Nutr Soc 57:503–509

    Article  PubMed  CAS  Google Scholar 

  • Wu G, Fang Y-Z, Yang S, Lupton JR, Turner ND (2004) Glutathione metabolism and its implications for health. J Nutr 134:489–492

    Article  PubMed  CAS  Google Scholar 

  • Yoshida M, Takahashi Y, Inoue S (2000) Histamine induces melanogenesis and morphologic changes by protein kinase a activation via H2 receptors in human normal melanocytes. J Invest Dermatol 114:334–342

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank four anonymous reviewers for helpful comments and “El Ventorrillo” MNCN Field Station for use of their facilities.

Funding

Financial support was provided by the Spanish’s Ministerio de Economía y Competitividad projects MICIIN-CGL2011-24150/BOS and MINECO CGL2014-53523-P and a JAE-pre-grant to RK.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to José Martín.

Ethics declarations

Ethical statement

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. Captures and experiments were performed under license (Ref. 10/016732.9/13) from the Environmental Agency of Madrid Government (“Consejería del Medio Ambiente y Ordenación del Territorio de la Comunidad de Madrid”, Spain).

Conflicts of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by S. J. Downes

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kopena, R., López, P. & Martín, J. Immune challenged male Iberian green lizards may increase the expression of some sexual signals if they have supplementary vitamin E. Behav Ecol Sociobiol 71, 173 (2017). https://doi.org/10.1007/s00265-017-2401-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00265-017-2401-6

Keywords

Navigation