Advertisement

Behavioral Ecology and Sociobiology

, Volume 69, Issue 5, pp 765–775 | Cite as

Multiple colour traits signal performance and immune response in the Dickerson’s collared lizard Crotaphytus dickersonae

  • Melissa Plasman
  • Víctor Hugo Reynoso
  • Leticia Nicolás
  • Roxana Torres
Original Paper

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.

Keywords

Honest signal Coloration Temperature Testosterone Immune condition Resource-holding power 

Notes

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.

Ethical standards

The study complies with the current regulations of Mexico regarding animal welfare.

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Adolph SC, Porter WP (1993) Temperature, activity, and lizard life histories. Am Nat 142:273–295CrossRefPubMedGoogle Scholar
  2. 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 276:2093–2101CrossRefGoogle Scholar
  3. Anderson M (1994) Sexual selection. Princeton University Press, Princeton, NJGoogle Scholar
  4. Anderson DR (2008) Model based inference in the life sciences: a primer on evidence. Springer, New YorkCrossRefGoogle Scholar
  5. Angilletta MJ, Niewiarowski PH, Navas CA (2002) The evolution of thermal physiology in ectotherms. J Therm Biol 27:249–268CrossRefGoogle Scholar
  6. Baird TA (2008) A growth cost of experimentally induced conspicuous coloration in first-year collared lizard males. Behav Ecol 19:589–593CrossRefGoogle Scholar
  7. Baird TA (2013) Male collared lizards, Crotaphytus collaris (Sauria: Crotaphytidae), signal females by broadcasting visual displays. Biol J Linn Soc 108:636–646CrossRefGoogle Scholar
  8. Baird TA, Hews DK (2007) Hormone levels in territorial and non-territorial male collared lizards. Physiol Behav 92:755–763CrossRefPubMedGoogle Scholar
  9. 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 8:506–517CrossRefGoogle Scholar
  10. 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:e34359CrossRefPubMedCentralPubMedGoogle Scholar
  11. 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:411–418CrossRefGoogle Scholar
  12. Bennett AF (1980) The thermal dependence of lizard behaviour. Anim Behav 28:752–762CrossRefGoogle Scholar
  13. Bentler PM (1989) EQS structural equations program manual. BMDP Statistical Software, Los Angeles, CAGoogle Scholar
  14. 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 47:419–429CrossRefPubMedGoogle Scholar
  15. Candolin U (2003) The use of multiple cues in mate choice. Biol Rev 78:575–595CrossRefPubMedGoogle Scholar
  16. Carpenter GC (1995) Modeling dominance: the influence of size, coloration, and experience on dominance relations in tree lizards (Urosaurus ornatus). Herpetol Monogr 9:88–101CrossRefGoogle Scholar
  17. Claussen DL, Art GR (1981) Heating and cooling rates in Anolis carolinensis and comparisons with other lizards. Comp Biochem Physiol 69A:23–29CrossRefGoogle Scholar
  18. Clusella Trullas S, Van Wijk JH, Spotila JR (2007) Thermal melanism in ectotherms. J Therm Biol 32:235–245CrossRefGoogle Scholar
  19. 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 208:4679–4687CrossRefPubMedGoogle Scholar
  20. Cox RM, John-Alder HB (2007) Increased mite parasitism as a cost of testosterone in male striped plateau lizards Sceloporus virgatus. Funct Ecol 21:327–334CrossRefGoogle Scholar
  21. 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:505–514CrossRefGoogle Scholar
  22. Ducrest AL, Keller L, Roulin A (2008) Pleiotropy in the melanocortin system, coloration and behavioural syndromes. Trends Ecol Evol 23:502–510CrossRefPubMedGoogle Scholar
  23. Dunham AE, Grant BW, Overall KL (1989) Interfaces between biophysical and physiological ecology and the population ecology of terrestrial vertebrate ectotherms. Physiol Zool 62:335–355Google Scholar
  24. Ellis L (1995) Dominance and reproductive success among nonhuman animals: a cross-species comparison. Ethol Sociobiol 16:257–333CrossRefGoogle Scholar
  25. Endler JA (1990) On the measurement and classification of colour in studies of animal colour patterns. Biol J Linn Soc 41:315–352CrossRefGoogle Scholar
  26. Endler JA (1992) Signals, signal conditions, and the direction of evolution. Am Nat 139:S125–S153CrossRefGoogle Scholar
  27. Folstad I, Karter AJ (1992) Parasites, bright males and the immunocompetence handicap hypothesis. Am Nat 139:603–622CrossRefGoogle Scholar
  28. Goldberg SR, Holshuh HJ (1992) Ectoparasite-induced lesions in mite pockets of the Yarrow’s spiny lizard, Sceloporus jarrovii (Phrynosomatidae). J Wildlife Dis 28:537–541CrossRefGoogle Scholar
  29. Greenberg N (2002) Ethological aspects of stress in a model lizard, Anolis carolinensis. Integr Comp Biol 42:526–540CrossRefPubMedGoogle Scholar
  30. Grether GF, Kolluru GR, Nersissian K (2004) Individual colour patches as multiple component signals. Biol Rev 79:583–610CrossRefPubMedGoogle Scholar
  31. Guilford T, Stamp Dawkins M (1991) Receiver psychology and the evolution of animal signals. Anim Behav 42:1–14CrossRefGoogle Scholar
  32. Hamilton WD, Zuk M (1982) Heritable true fitness and bright birds: a role for parasites? Science 218:384–387CrossRefPubMedGoogle Scholar
  33. Herbst KL, Bhasin S (2004) Testosterone action on skeletal muscle. Curr Opin Clin Nutr 7:271–277CrossRefGoogle Scholar
  34. 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 13:287–297CrossRefGoogle Scholar
  35. 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 30:37–43CrossRefGoogle Scholar
  36. Hews DK, Moore MC (1996) A critical period for the organization of alternative male phenotypes of tree lizards by exogenous testosterone. Physiol Behav 60:425–429CrossRefPubMedGoogle Scholar
  37. Hews DK, Knapp R, Moore MC (1994) Early exposure to androgens affects adult expression of alternative male types in tree lizards. Horm Behav 28:96–115CrossRefPubMedGoogle Scholar
  38. Hill GE (2011) Condition-dependent traits as signals of the functionality of vital cellular processes. Ecol Lett 14:625–634CrossRefPubMedGoogle Scholar
  39. Hu L, Bentler PM (1999) Cut-off criteria for fit indexes in covariance structure analysis: conventional criteria versus new alternatives. Struct Equ Model 6:1–55CrossRefGoogle Scholar
  40. 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 25–91Google Scholar
  41. Husak JF (2004) Signal use by collared lizards, Crotaphytus collaris: the effects of familiarity and threat. Behav Ecol Sociobiol 55:602–607CrossRefGoogle Scholar
  42. Husak JF (2006) Does speed help you survive? A test with collared lizards of different ages. Funct Ecol 20:174–179CrossRefGoogle Scholar
  43. Husak JF, Fox SF (2006) Field use of maximal sprint speed by collared lizards (Crotaphytus collaris): compensation and sexual selection. Evolution 60:1888–1895CrossRefPubMedGoogle Scholar
  44. Husak JF, Fox SF (2008) Sexual selection on locomotor performance. Evol Ecol Res 10:213–228Google Scholar
  45. Husak JF, Fox SF, Lovern MB, Van Den Bussche RA (2006a) Faster lizards sire more offspring: sexual selection on whole-animal performance. Evolution 60:2122–2130CrossRefPubMedGoogle Scholar
  46. Husak JF, Lappin AK, Fox SF, Lemos-Espinal JA (2006b) Bite-force performance predicts dominance in the venerable collared lizard (Crotaphytus antiquus). Copeia 2006:301–306CrossRefGoogle Scholar
  47. Husak JF, Irschick DJ, Meyers JJ, Lailvaux SP, Moore IT (2007) Hormones, sexual signals, and performance of green anole lizards (Anolis carolinensis). Horm Behav 52:360–367CrossRefPubMedGoogle Scholar
  48. 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 19:800–807CrossRefGoogle Scholar
  49. 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 96:13–22CrossRefGoogle Scholar
  50. 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 163:867–874CrossRefPubMedGoogle Scholar
  51. 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 10:177–196Google Scholar
  52. Jawor JM, Breitwisch R (2003) Melanin ornaments, honesty and sexual selection. Auk 120:249–265CrossRefGoogle Scholar
  53. 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 49:393–407CrossRefPubMedGoogle Scholar
  54. Johnstone RA (1995) Honest advertisement of multiple qualities using multiple signals. J Theor Biol 177:87–94CrossRefGoogle Scholar
  55. Kimball RT (2006) Hormonal control of coloration. In: Hill GE, McGraw KJ (eds) Bird coloration: mechanisms and measurements. Harvard University Press, Cambridge, pp 431–468Google Scholar
  56. Kimball FA, Erpino MJ (1971) Hormonal control of pigmentary sexual dimorphism in Sceloporus occidentalis. Gen Comp Endocr 16:375–384CrossRefPubMedGoogle Scholar
  57. 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 33:197–204CrossRefPubMedGoogle Scholar
  58. 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 71:506–514CrossRefPubMedGoogle Scholar
  59. 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 23:793–799CrossRefPubMedGoogle Scholar
  60. Lailvaux SP, Irschick DJ (2007) The evolution of performance-based male fighting ability in Caribbean anolis lizards. Am Nat 170:573–586CrossRefPubMedGoogle Scholar
  61. Langkilde T, Boronow KE (2012) Hot boys are blue: temperature-dependent colour change in male Eastern fence lizards. J Herpetol 46:461–465CrossRefGoogle Scholar
  62. Lappin AK, Husak JF (2005) Weapon performance, not size, determines mating success and potential reproductive output in the collared lizard (Crotaphytus collaris). Am Nat 166:426–436CrossRefPubMedGoogle Scholar
  63. 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 168:100–113CrossRefPubMedGoogle Scholar
  64. Lozano GA (1994) Carotenoids, parasites, and sexual selection. Oikos 70:309–311CrossRefGoogle Scholar
  65. 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 38:340–354CrossRefGoogle Scholar
  66. 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 97:749–765CrossRefGoogle Scholar
  67. Macintosh JA (2001) The antimicrobial properties of melanocytes, melanosomes and melanin and the evolution of black skin. J Theor Biol 211:101–113CrossRefGoogle Scholar
  68. Martín J, López P (2001) Risk of predation may explain the absence of nuptial coloration in the wall lizard, Podarcis muralis. Evol Ecol Res 3:889–898Google Scholar
  69. Maynard Smith J (1991) Honest signalling: the Philip Sidney game. Anim Behav 42:1034–1035CrossRefGoogle Scholar
  70. McGuire JA (1996) Phylogenetic systematics of crotaphytid lizards (Reptilia: Iguana: Crotaphytidea). Bull Carnegie Mus Nat His 32:1–143Google Scholar
  71. 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 171:339–357CrossRefPubMedGoogle Scholar
  72. Møller AP, Pomiankowski A (1993) Why birds got multiple sexual ornaments? Behav Ecol Sociobiol 32:167–176Google Scholar
  73. 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 81:217–226CrossRefPubMedGoogle Scholar
  74. 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 1996:806–812CrossRefGoogle Scholar
  75. 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 267:2339–2343CrossRefGoogle Scholar
  76. 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 215:575–577CrossRefPubMedGoogle Scholar
  77. Perry G, Levering K, Girard I, Garland T Jr (2004) Locomotor performance and social dominance in male Anolis cristatellus. Anim Behav 67:37–47CrossRefGoogle Scholar
  78. Peterson CC, Husak JF (2006) Locomotor performance and sexual selection: individual variation in sprint speed of collared lizards (Crotaphytus collaris). Copeia 2006:216–224CrossRefGoogle Scholar
  79. Plasman M, Duchateau MJHM, Macedonia JM (2007) Anti-predation behaviour of Dickerson’s collared lizard, Crotaphytus dickersonae. Anim Biol 52:231–246CrossRefGoogle Scholar
  80. Quinn VS, Hews DK (2003) Positive relationship between abdominal coloration and dermal melanin density in Phrynosomatid lizards. Copeia 2003:858–864CrossRefGoogle Scholar
  81. Roberts ML, Buchanan KL, Evans MR (2004) Testing the immunocompetence handicap hypothesis: a review of the evidence. Anim Behav 68:227–239CrossRefGoogle Scholar
  82. Robson MA, Miles DB (2000) Locomotor performance and dominance in male tree lizards, Urosaurus ornatus. Funct Ecol 14:338–344CrossRefGoogle Scholar
  83. Rosseel Y (2012) Lavaan: an R package for structural equation modeling. J Stat Software 48:1–36Google Scholar
  84. 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 57:134–139CrossRefPubMedCentralPubMedGoogle Scholar
  85. 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 35:274–283CrossRefPubMedGoogle Scholar
  86. 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 8:135–139CrossRefGoogle Scholar
  87. Schmid-Hempel P (2011) Evolutionary parasitology. Oxford University Press, OxfordGoogle Scholar
  88. Sexton OJ, Andrews RM, Bramble JE (1992) Size and growth rate characteristics of a peripheral population of Crotaphytus collaris (Sauria: Crotaphytidae). Copeia 1992:968–980CrossRefGoogle Scholar
  89. Shawkey MD, Estes AM, Siefferman LM, Hill GE (2003) Nanostructure predicts intraspecific variation in ultraviolet-blue plumage colour. Proc R Soc Lond B 270:1455–1460CrossRefGoogle Scholar
  90. 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 38:222–233CrossRefPubMedGoogle Scholar
  91. Számadó S (2011) The cost of honesty and the fallacy of the handicap principle. Anim Behav 81:3–10CrossRefGoogle Scholar
  92. Tokarz RR (1985) Body size as a factor determining dominance in staged agonistic encounters between male brown anoles (Anolis sagrei). Anim Behav 33:746–753CrossRefGoogle Scholar
  93. Umbers KDL (2013) On the perception, production and function of blue coloration in animals. J Zool 289:229–242CrossRefGoogle Scholar
  94. Wright S (1921) Correlation and causation. J Agr Res 20:557–585Google Scholar
  95. Zahavi A (1975) Mate selection—a selection for a handicap. J Theor Biol 53:205–214CrossRefPubMedGoogle Scholar
  96. Zahavi A (1977) The cost of honesty (further remarks on the handicap principle). J Theor Biol 67:603–605CrossRefPubMedGoogle Scholar
  97. Zimmerman LM, Vogel LA, Bowden RM (2010) Understanding the vertebrate immune system: insight from the reptilian perspective. J Exp Biol 213:661–671CrossRefPubMedGoogle Scholar
  98. Zuk M, Johnsen TS (1998) Seasonal changes in the relationship between ornamentation and immune response in red jungle fowl. Proc R Soc Lond B 265:1631–1635CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Melissa Plasman
    • 1
  • Víctor Hugo Reynoso
    • 2
  • Leticia Nicolás
    • 3
  • Roxana Torres
    • 1
  1. 1.Laboratorio de Conducta Animal, Departamento de Ecología Evolutiva, Instituto de EcologíaUniversidad Nacional Autónoma de MéxicoMéxico DFMéxico
  2. 2.Departamento de Zoología, Instituto de BiologíaUniversidad Nacional Autónoma de MéxicoMéxicoMéxico
  3. 3.Centro Tlaxcala de Biología de la ConductaUniversidad Autónoma de TlaxcalaTlaxcalaMéxico

Personalised recommendations