Abstract
Conspicuous male coloration is often an honest signal of individual quality. In Dickerson’s collared lizard (Crotaphytus dickersonae), males are striking blue, have a black and white collar and have white spots on their bodies. In this study, we investigated whether this extravagant colour pattern is an indicator of male performance in variables related to resource-holding power (bite force, running speed and endurance) and immune condition (cellular response and ectoparasite load). Also, we assessed direct and indirect effects of testosterone levels and body temperature on colour traits. We found that males with bluer skin, and darker and bigger black collars performed better in variables related to resource-holding power. Also, the black colour of the collar was related to immune condition. Blue chroma was positively related to temperature, yet males with bigger and darker black collars had lower body temperatures. Testosterone had minor effects on immune response and colour traits. Our results suggest that multiple colour traits in the Dickerson’s collared lizard may honestly indicate physical and physiological performance.
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References
Adolph SC, Porter WP (1993) Temperature, activity, and lizard life histories. Am Nat 142:273–295
Alonso-Alvarez C, Pérez-Rodríguez L, Garcia JT, Viñuela J (2009) Testosterone-mediated trade-offs in the old age: a new approach to the immunocompetence handicap and carotenoid-based sexual signalling. Proc R Soc Lond B 276:2093–2101
Anderson M (1994) Sexual selection. Princeton University Press, Princeton, NJ
Anderson DR (2008) Model based inference in the life sciences: a primer on evidence. Springer, New York
Angilletta MJ, Niewiarowski PH, Navas CA (2002) The evolution of thermal physiology in ectotherms. J Therm Biol 27:249–268
Baird TA (2008) A growth cost of experimentally induced conspicuous coloration in first-year collared lizard males. Behav Ecol 19:589–593
Baird TA (2013) Male collared lizards, Crotaphytus collaris (Sauria: Crotaphytidae), signal females by broadcasting visual displays. Biol J Linn Soc 108:636–646
Baird TA, Hews DK (2007) Hormone levels in territorial and non-territorial male collared lizards. Physiol Behav 92:755–763
Baird TA, Fox SF, McCoy JK (1997) Population differences in the roles of size and coloration in intra- and intersexual selection in the collared lizard, Crotaphytus collaris: influence of habitat and social organization. Behav Ecol 8:506–517
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
Belliure J, Smith L, Sorci G (2004) Effect of testosterone on T cell-mediated immunity in two species of Mediterranean lacertid lizards. J Exp Zool 301A:411–418
Bennett AF (1980) The thermal dependence of lizard behaviour. Anim Behav 28:752–762
Bentler PM (1989) EQS structural equations program manual. BMDP Statistical Software, Los Angeles, CA
Berger S, Martin LB II, Wikelski M, Romero LM, Kalko EK, Vitousek MN, Rodl T (2005) Corticosterone suppresses immune activity in territorial Galapagos marine iguanas during reproduction. Horm Behav 47:419–429
Candolin U (2003) The use of multiple cues in mate choice. Biol Rev 78:575–595
Carpenter GC (1995) Modeling dominance: the influence of size, coloration, and experience on dominance relations in tree lizards (Urosaurus ornatus). Herpetol Monogr 9:88–101
Claussen DL, Art GR (1981) Heating and cooling rates in Anolis carolinensis and comparisons with other lizards. Comp Biochem Physiol 69A:23–29
Clusella Trullas S, Van Wijk JH, Spotila JR (2007) Thermal melanism in ectotherms. J Therm Biol 32:235–245
Cox RM, John-Alder HB (2005) Testosterone has opposite effects on male growth in lizards (Sceloporus spp.) with opposite patterns of sexual size dimorphism. J Exp Biol 208:4679–4687
Cox RM, John-Alder HB (2007) Increased mite parasitism as a cost of testosterone in male striped plateau lizards Sceloporus virgatus. Funct Ecol 21:327–334
Cox RM, Zilberman V, John-Alder HB (2008) Testosterone stimulates the expression of a social colour signal in Yarrow’s spiny lizard, Sceloporus jarrovii. J Exp Zool 309A:505–514
Ducrest AL, Keller L, Roulin A (2008) Pleiotropy in the melanocortin system, coloration and behavioural syndromes. Trends Ecol Evol 23:502–510
Dunham AE, Grant BW, Overall KL (1989) Interfaces between biophysical and physiological ecology and the population ecology of terrestrial vertebrate ectotherms. Physiol Zool 62:335–355
Ellis L (1995) Dominance and reproductive success among nonhuman animals: a cross-species comparison. Ethol Sociobiol 16:257–333
Endler JA (1990) On the measurement and classification of colour in studies of animal colour patterns. Biol J Linn Soc 41:315–352
Endler JA (1992) Signals, signal conditions, and the direction of evolution. Am Nat 139:S125–S153
Folstad I, Karter AJ (1992) Parasites, bright males and the immunocompetence handicap hypothesis. Am Nat 139:603–622
Goldberg SR, Holshuh HJ (1992) Ectoparasite-induced lesions in mite pockets of the Yarrow’s spiny lizard, Sceloporus jarrovii (Phrynosomatidae). J Wildlife Dis 28:537–541
Greenberg N (2002) Ethological aspects of stress in a model lizard, Anolis carolinensis. Integr Comp Biol 42:526–540
Grether GF, Kolluru GR, Nersissian K (2004) Individual colour patches as multiple component signals. Biol Rev 79:583–610
Guilford T, Stamp Dawkins M (1991) Receiver psychology and the evolution of animal signals. Anim Behav 42:1–14
Hamilton WD, Zuk M (1982) Heritable true fitness and bright birds: a role for parasites? Science 218:384–387
Herbst KL, Bhasin S (2004) Testosterone action on skeletal muscle. Curr Opin Clin Nutr 7:271–277
Herrel A, Spithoven L, Van Damme R, De Vree F (1999) Sexual dimorphism of head size in Gallotia galloti: testing the niche divergence hypothesis by functional analyses. Funct Ecol 13:287–297
Hettyey A, Herczeg G, Laurila A, Crochet PA, Merilä J (2009) Body temperature, size, nuptial coloration and mating success in male Moor frogs (Rana arvalis). Amphibia-Reptilia 30:37–43
Hews DK, Moore MC (1996) A critical period for the organization of alternative male phenotypes of tree lizards by exogenous testosterone. Physiol Behav 60:425–429
Hews DK, Knapp R, Moore MC (1994) Early exposure to androgens affects adult expression of alternative male types in tree lizards. Horm Behav 28:96–115
Hill GE (2011) Condition-dependent traits as signals of the functionality of vital cellular processes. Ecol Lett 14:625–634
Hu L, Bentler PM (1999) Cut-off criteria for fit indexes in covariance structure analysis: conventional criteria versus new alternatives. Struct Equ Model 6:1–55
Huey RB (1982) Temperture, physiology, and the ecology of reptiles. In: Gans C, Pough FH (eds) Biology of the Reptilia, vol 12, Physiology (C). Academic, London, pp 25–91
Husak JF (2004) Signal use by collared lizards, Crotaphytus collaris: the effects of familiarity and threat. Behav Ecol Sociobiol 55:602–607
Husak JF (2006) Does speed help you survive? A test with collared lizards of different ages. Funct Ecol 20:174–179
Husak JF, Fox SF (2006) Field use of maximal sprint speed by collared lizards (Crotaphytus collaris): compensation and sexual selection. Evolution 60:1888–1895
Husak JF, Fox SF (2008) Sexual selection on locomotor performance. Evol Ecol Res 10:213–228
Husak JF, Fox SF, Lovern MB, Van Den Bussche RA (2006a) Faster lizards sire more offspring: sexual selection on whole-animal performance. Evolution 60:2122–2130
Husak JF, Lappin AK, Fox SF, Lemos-Espinal JA (2006b) Bite-force performance predicts dominance in the venerable collared lizard (Crotaphytus antiquus). Copeia 2006:301–306
Husak JF, Irschick DJ, Meyers JJ, Lailvaux SP, Moore IT (2007) Hormones, sexual signals, and performance of green anole lizards (Anolis carolinensis). Horm Behav 52:360–367
Huyghe K, Vanhooydonck B, Scheers H, Molina-Borja M, Van Damme R (2005) Morphology, performance and fighting capacity in male lizards, Gallotia galloti. Funct Ecol 19:800–807
Huyghe K, Herrel A, Adriaens D, Tadíc Z, Van Damme R (2009) It is all in the head: morphological basis for differences in bite force among colour morphs of the Dalmatian wall lizard. Biol J Linn Soc 96:13–22
Huyghe K, Van Oystaeyen A, Pasmans F, Tadíc Z, Vanhooydonck B, Van Damme R (2010) Seasonal changes in parasite load and cellular immune response in a colour polymorphic lizard. Oecologia 163:867–874
Irschick DJ, Meyers JJ, Husak JF, Le Galliard J (2008) How does selection operate on whole-organism functional performance capacities? A review and synthesis. Evol Ecol Res 10:177–196
Jawor JM, Breitwisch R (2003) Melanin ornaments, honesty and sexual selection. Auk 120:249–265
John-Alder HB, Cox RM, Haenel GJ, Smith LC (2009) Hormones, performance and fitness: natural history and endocrine experiments on a lizard (Sceloporus undulatus). Integr Comp Biol 49:393–407
Johnstone RA (1995) Honest advertisement of multiple qualities using multiple signals. J Theor Biol 177:87–94
Kimball RT (2006) Hormonal control of coloration. In: Hill GE, McGraw KJ (eds) Bird coloration: mechanisms and measurements. Harvard University Press, Cambridge, pp 431–468
Kimball FA, Erpino MJ (1971) Hormonal control of pigmentary sexual dimorphism in Sceloporus occidentalis. Gen Comp Endocr 16:375–384
Klukowski M, Nelson CE (1998) The challenge hypothesis and seasonal changes in aggression and steroids in male northern fence lizards (Sceloporus undulatus hyacinthinus). Horm Behav 33:197–204
Klukowski M, Jenkinson NM, Nelson CE (1998) Effects of testosterone on locomotor performance and growth in the field-active northern fence lizards, Sceloporus undulatus hyacinthinus. Physiol Zool 71:506–514
Kuriyama T, Miyaji K, Sugimoto M, Hasegawa M (2006) Ultrastructure of the dermal chromatophores in a lizard (Scincidae: Plestiodon latiscutatus) with conspicuous body and tail coloration. Zool Sci 23:793–799
Lailvaux SP, Irschick DJ (2007) The evolution of performance-based male fighting ability in Caribbean anolis lizards. Am Nat 170:573–586
Langkilde T, Boronow KE (2012) Hot boys are blue: temperature-dependent colour change in male Eastern fence lizards. J Herpetol 46:461–465
Lappin AK, Husak JF (2005) Weapon performance, not size, determines mating success and potential reproductive output in the collared lizard (Crotaphytus collaris). Am Nat 166:426–436
Lappin AK, Brandt Y, Husak JF, Macedonia JM, Kemp DJ (2006) Gaping displays reveal and amplify a mechanically based index of weapon performance. Am Nat 168:100–113
Lozano GA (1994) Carotenoids, parasites, and sexual selection. Oikos 70:309–311
Macedonia JM, Husak JF, Brandt YM, Lappin AK, Baird TA (2004) Sexual dichromatism and colour conspicuousness in three populations of collared lizards (Crotaphytus collaris) from Oklahoma. J Herpetol 38:340–354
Macedonia JM, Lappin AK, Loew ER, McGuire JA, Hamilton PS, Plasman M, Brandt Y, Lemos-Espinal JA, Kemp DJ (2009) Conspicuousness of Dickerson’s collared lizard (Crotaphytus dickersonae) through the eyes of conspecifics and predators. Biol J Linn Soc 97:749–765
Macintosh JA (2001) The antimicrobial properties of melanocytes, melanosomes and melanin and the evolution of black skin. J Theor Biol 211:101–113
Martín J, López P (2001) Risk of predation may explain the absence of nuptial coloration in the wall lizard, Podarcis muralis. Evol Ecol Res 3:889–898
Maynard Smith J (1991) Honest signalling: the Philip Sidney game. Anim Behav 42:1034–1035
McGuire JA (1996) Phylogenetic systematics of crotaphytid lizards (Reptilia: Iguana: Crotaphytidea). Bull Carnegie Mus Nat His 32:1–143
Mills SC, Hazard L, Lancaster L, Mappes T, Miles D, Oksanen TA, Sinervo B (2008) Gonadotropin hormone modulation of testosterone, immune function, performance, and behavioral trade-offs among male morphs of the lizard Uta stansburiana. Am Nat 171:339–357
Møller AP, Pomiankowski A (1993) Why birds got multiple sexual ornaments? Behav Ecol Sociobiol 32:167–176
Moore CM, Thompson CW, Marler CA (1991) Reciprocal changes in corticosterone and testosterone levels following acute and chronic handling stress in the tree lizard, Urosaurus ornatus. Gen Comp Endocr 81:217–226
Morrison RL, Sherbrooke WC, Frost–Mason SK (1996) Temperature sensitive, physiologically active iridophores in the lizard Urosaurus ornatus: an ultrastructural analysis of colour change. Copeia 1996:806–812
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
Olsson M, Healey M, Wilson M, Tobler M (2012) Polymorphic male colour morphs visualized with steroids in monomorphic females: a tool for designing analysis of sex-limited trait inheritance. J Exp Biol 215:575–577
Perry G, Levering K, Girard I, Garland T Jr (2004) Locomotor performance and social dominance in male Anolis cristatellus. Anim Behav 67:37–47
Peterson CC, Husak JF (2006) Locomotor performance and sexual selection: individual variation in sprint speed of collared lizards (Crotaphytus collaris). Copeia 2006:216–224
Plasman M, Duchateau MJHM, Macedonia JM (2007) Anti-predation behaviour of Dickerson’s collared lizard, Crotaphytus dickersonae. Anim Biol 52:231–246
Quinn VS, Hews DK (2003) Positive relationship between abdominal coloration and dermal melanin density in Phrynosomatid lizards. Copeia 2003:858–864
Roberts ML, Buchanan KL, Evans MR (2004) Testing the immunocompetence handicap hypothesis: a review of the evidence. Anim Behav 68:227–239
Robson MA, Miles DB (2000) Locomotor performance and dominance in male tree lizards, Urosaurus ornatus. Funct Ecol 14:338–344
Rosseel Y (2012) Lavaan: an R package for structural equation modeling. J Stat Software 48:1–36
Ruiz M, French SS, Demas GE, Martins EP (2010) Food supplementation and testosterone interact to influence reproductive behavior and immune function in Sceloporus graciosus. Horm Behav 57:134–139
Sacchi R, Pubin F, Gentilli A, Rubolini D, Scali S, Fasola M, Galeotti P (2009) Male-male combats in a polymorphic lizard: residency and size, but not colour, affect fighting rules and contest outcome. Aggress Behav 35:274–283
Salvador A, Veiga JP, Martín J, López P (1997) Testosterone supplementation in subordinate small male lizards: consequences for aggressiveness, colour development, and parasite load. Behav Ecol 8:135–139
Schmid-Hempel P (2011) Evolutionary parasitology. Oxford University Press, Oxford
Sexton OJ, Andrews RM, Bramble JE (1992) Size and growth rate characteristics of a peripheral population of Crotaphytus collaris (Sauria: Crotaphytidae). Copeia 1992:968–980
Shawkey MD, Estes AM, Siefferman LM, Hill GE (2003) Nanostructure predicts intraspecific variation in ultraviolet-blue plumage colour. Proc R Soc Lond B 270:1455–1460
Sinervo B, Miles DB, Frankino WA, Klukowski M, DeNardo DF (2000) Testosterone, endurance, and Darwinian fitness: natural and sexual selection on the physiological bases of alternative male behaviors in side-blotched lizards. Horm Behav 38:222–233
Számadó S (2011) The cost of honesty and the fallacy of the handicap principle. Anim Behav 81:3–10
Tokarz RR (1985) Body size as a factor determining dominance in staged agonistic encounters between male brown anoles (Anolis sagrei). Anim Behav 33:746–753
Umbers KDL (2013) On the perception, production and function of blue coloration in animals. J Zool 289:229–242
Wright S (1921) Correlation and causation. J Agr Res 20:557–585
Zahavi A (1975) Mate selection—a selection for a handicap. J Theor Biol 53:205–214
Zahavi A (1977) The cost of honesty (further remarks on the handicap principle). J Theor Biol 67:603–605
Zimmerman LM, Vogel LA, Bowden RM (2010) Understanding the vertebrate immune system: insight from the reptilian perspective. J Exp Biol 213:661–671
Zuk M, Johnsen TS (1998) Seasonal changes in the relationship between ornamentation and immune response in red jungle fowl. Proc R Soc Lond B 265:1631–1635
Acknowledgements
We thank Víctor E. Argaez Márquez, Gala E. Castro Mejías, Abigail Vera Ortega, Paola Flores Mejía and J. Alberto Cruz Silva for their help in the field. Lorayne Meltzer facilitated accommodation and space for field experiments at Prescott College Kino Bay station. We thank Diego Carmona Moreno Bello for his enthusiastic advice with the pathway analyses, Laura García Rivera and Natalia Gañan for their help with the testosterone analysis, and Ricardo Paredes León for the determination of the ectoparasites. We thank Alejandro Córdoba Aguilar and Andrés García Aguayo for their comments on earlier drafts of this paper. Financial support was provided by the Universidad Nacional Autónoma de México (UNAM, PAPIIT IN206713). Specimens were captured and released under collection permit SGPA/DGVS/03365/12 granted by Secretaría del Medio Ambiente y Recursos Naturales to RT. M. Plasman thanks the Consejo Nacional de Ciencia y Technología (CONACyT) for her PhD studies grant. This paper is a partial fulfilment for MP’s doctoral degree, Posgrado en Ciencias Biológicas, UNAM.
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Plasman, M., Reynoso, V.H., Nicolás, L. et al. Multiple colour traits signal performance and immune response in the Dickerson’s collared lizard Crotaphytus dickersonae . Behav Ecol Sociobiol 69, 765–775 (2015). https://doi.org/10.1007/s00265-015-1892-2
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DOI: https://doi.org/10.1007/s00265-015-1892-2