Advertisement

Naturwissenschaften

, Volume 101, Issue 10, pp 803–811 | Cite as

Honest sexual signaling in turtles: experimental evidence of a trade-off between immune response and coloration in red-eared sliders Trachemys scripta elegans

  • Alejandro Ibáñez
  • Nuria Polo-Cavia
  • Pilar López
  • José Martín
Original Paper

Abstract

Sexual signals can be evolutionarily stable if they are honest and condition dependent or costly to the signaler. One possible cost is the existence of a trade-off between maintaining the immune system and the elaboration of ornaments. This hypothesis has been experimentally tested in some groups of animals but not in others such as turtles. We experimentally challenged the immune system of female red-eared sliders Trachemys scripta elegans, with a bacterial antigen (lipopolysaccharide (LPS)) without pathogenic effects to explore whether the immune activation affected visual colorful ornaments of the head. The LPS injection altered the reflectance patterns of color ornaments. In comparison to the control animals, the yellow chin stripes of injected animals exhibited (1) reduced brightness, (2) lower long wavelength (>470 nm) reflectance, and (3) lower values for carotenoid chroma. The postorbital patches of injected individuals also showed reduced very long wavelength (>570 nm) reflectance but did not change in carotenoid chroma. Thus, experimental turtles showed darker and less “yellowish” chin stripes and less “reddish” postorbital patches at the end of the experiment, whereas control turtles did not change their coloration. This is the first experimental evidence supporting the existence of a trade-off between the immune system and the expression of visual ornaments in turtles. We suggest that this trade-off may allow turtles to honestly signal individual quality via characteristics of coloration, which may have an important role in intersexual selection processes.

Keywords

Visual signals Female ornaments Immune response Sexual selection Turtles 

Notes

Acknowledgments

We thank three anonymous reviewers for helpful comments and “El Ventorrillo” MNCN Field Station for use of their facilities. Financial support was provided by the project MICIIN-CGL2011-24150/BOS and by a FPI predoctoral grant (ref: BES-2009-025228) to AI.

Ethical standards

The experiments enforced all the present Spanish laws and were performed under license from the Environmental Organisms of Madrid Community where they were carried out.

Conflict of interest

None.

References

  1. Aguilera E, Amat JA (2007) Carotenoids, immune response and the expression of sexual ornaments in male greenfinches (Carduelis chloris). Naturwissenschaften 94:895–902PubMedCrossRefGoogle Scholar
  2. 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 164:651–659PubMedCrossRefGoogle Scholar
  3. Amundsen T (2000a) Female ornaments: genetically correlated or sexually selected? In: Espmark Y, Amundsen T, Rosenqvist G (eds) Animal signals: signaling and signal design in animal communication. Tapir Academic, Trondheim, pp 133–154Google Scholar
  4. Amundsen T (2000b) Why are female birds ornamented? Trends Ecol Evol 15:149–155PubMedCrossRefGoogle Scholar
  5. Amundsen T, Forsgren E (2001) Male mate choice selects for female coloration in a fish. Proc Natl Acad Sci U S A 98:13155–13160PubMedCentralPubMedCrossRefGoogle Scholar
  6. Andersson M (1994) Sexual selection. Princeton University Press, PrincetonGoogle Scholar
  7. Baeta R, Faivre B, Motreuil S, Gaillard M, Moreau J (2008) Carotenoid trade-off between parasitic resistance and sexual display: an experimental study in the blackbird (Turdus merula). Proc R Soc Lond B 275:427–434CrossRefGoogle Scholar
  8. Bertrand S, Faivre B, Sorci G (2006) Do carotenoid-based sexual traits signal the availability of non-pigmentary antioxidants? J Exp Biol 209:4414–4419PubMedCrossRefGoogle Scholar
  9. Blount JD (2004) Carotenoids and life-history evolution in animals. Arch Biochem Biophys 430:10–15PubMedCrossRefGoogle Scholar
  10. Blount JD, Metcalfe NB, Birkhead TR, Surai PF (2003) Carotenoid modulation of immune function and sexual attractiveness in zebra finches. Science 300:125–127PubMedCrossRefGoogle Scholar
  11. Bonneaud C, Mazuc J, González G, Haussy C, Faivre B, Sorci G (2003) Assessing the cost of mounting an immune response. Am Nat 161:367–379PubMedCrossRefGoogle Scholar
  12. Clutton-Brock T (2007) Sexual selection in males and females. Science 318:1882–1885PubMedCrossRefGoogle Scholar
  13. Cooper WE, Greenberg N (1992) Reptilian coloration and behavior. In: Gans C, Crews D (eds) Biology of the Reptilia, vol 18. University of Chicago Press, Chicago, pp 298–422Google Scholar
  14. Cuthill IC, Bennett ATD, Partridge JC, Maier EJ (1999) Plumage reflectance and the objective assessment of avian sexual dichromatism. Am Nat 153:183–200CrossRefGoogle Scholar
  15. Deen CM, Hutchison VH (2001) Effects of lipopolysaccharide and acclimation temperature on induced behavioral fever in juvenile Iguana iguana. J Therm Biol 26:55–63PubMedCrossRefGoogle Scholar
  16. do Amaral JPS, Marvin GA, Hutchison VH (2002) The influence of bacterial lipopolysaccharide on the thermoregulation of the box turtle Terrapene carolina. Physiol Biochem Zool 75:273–282PubMedCrossRefGoogle Scholar
  17. Ernst CH, Barbour RW (1989) Turtles of the world. Smithsonian Institution Press, Washington DCGoogle Scholar
  18. Faivre B, Grégoire A, Préault M, Cézilly F, Sorci G (2003) Immune activation rapidly mirrored in a secondary sexual trait. Science 300:103PubMedCrossRefGoogle Scholar
  19. Feldman ML (2007) Some options to induce oviposition in turtles. Chelonian Conserv Biol 6:313–320CrossRefGoogle Scholar
  20. Ferrara CR, Vogt RC, Sousa-Lima RS (2013) Turtle vocalizations as the first evidence of posthatching parental care in chelonians. J Comp Psychol 127:24–32PubMedCrossRefGoogle Scholar
  21. Fitze PS, Cote J, San-Jose LM, Meylan S, Isaksson C, Andersson S, Rossi J-M, Clobert J (2009) Carotenoid-based colours reflect the stress response in the common lizard. PLoS ONE 4:e5111PubMedCentralPubMedCrossRefGoogle Scholar
  22. Galeotti P, Sacchi R, Pellitteri-Rosa D, Fasola M (2005) Female preference for fast-rate, high-pitched calls in Hermann’s tortoises Testudo hermanni. Behav Ecol 16:301–308CrossRefGoogle Scholar
  23. Galeotti P, Sacchi R, Pellitteri-Rosa D, Fasola M (2007) Olfactory discrimination of species, sex, and sexual maturity by the Hermann’s Tortoise Testudo hermanni. Copeia 2007:980–985CrossRefGoogle Scholar
  24. Galeotti P, Sacchi R, Pellitteri-Rosa D, Fasola M (2011) The yellow cheek-patches of the Hermann’s tortoise (Reptilia, Chelonia): sexual dimorphism and relationship with body condition. Ital J Zool 78:464–470CrossRefGoogle Scholar
  25. Giles JC, Davis JA, McCauley RD, Kuchling R (2009) Voice of the turtle: the underwater acoustic repertoire of the long-necked freshwater turtle, Chelodina oblonga. J Acoust Soc Am 126:434–443PubMedCrossRefGoogle Scholar
  26. Grafen A (1990) Biological signals as handicaps. J Theor Biol 144:517–546PubMedCrossRefGoogle Scholar
  27. Grether GF, Kasahara S, Kolluru GR, Cooper EL (2004) Sex specific effects of carotenoid intake on the immunological response to allografts in guppies (Poecilia reticulata). Proc R Soc Lond B 271:45–49CrossRefGoogle Scholar
  28. Grill CP, Rush VN (2000) Analysing spectral data: comparison and application of two techniques. Biol J Linn Soc 69:121–138CrossRefGoogle Scholar
  29. Hamilton WD, Zuk M (1982) Heritable true fitness and bright birds: a role for parasites. Science 218:384–387PubMedCrossRefGoogle Scholar
  30. Hartley RC, Kennedy MW (2004) Are carotenoids a red herring in sexual display? Trends Ecol Evol 19:353–354PubMedCrossRefGoogle Scholar
  31. Hil GE (2011) Condition-dependent traits as signals of the functionality of vital cellular processes. Ecol Lett 14:625–634CrossRefGoogle Scholar
  32. Hõrak P, Ots I, Vellau H, Spottiswoode C, Møller AP (2001) Carotenoid-based plumage coloration reflects hemoparasite infection and local survival in breeding great tits. Oecologia 126:166–173CrossRefGoogle Scholar
  33. Hõrak P, Saks L, Zilmer M, Karu U, Zilmer K (2007) Do dietary antioxidants alleviate the cost of immune activation? An experiment with greenfinches. Am Nat 170:625–635PubMedCrossRefGoogle Scholar
  34. Ibáñez A, López P, Martín J (2012) Discrimination of conspecifics’ chemicals may allow Spanish terrapins to find better partners and avoid competitors. Anim Behav 83:1107–1113CrossRefGoogle Scholar
  35. Ibáñez A, Marzal A, López P, Martín J (2013a) Boldness and body size of male Spanish terrapins affect their responses to chemical cues of familiar and unfamiliar males. Behav Ecol Sociobiol 67:541–548CrossRefGoogle Scholar
  36. Ibáñez A, Marzal A, López P, Martín J (2013b) Sexually dichromatic coloration reflects size and immunocompetence in female Spanish terrapins, Mauremys leprosa. Naturwissenschaften 100:1137–1147PubMedCrossRefGoogle Scholar
  37. Isaksson C, Andersson S (2008) Oxidative stress does not influence carotenoid mobilization and plumage pigmentation. Proc R Soc Lond B 275:309–314CrossRefGoogle Scholar
  38. Janeway CA, Travers P, Walport M, Shlomchik M (2001) Immunobiology. The immune system in health and disease, 5th edn. Garland Publishing, New YorkGoogle Scholar
  39. Kopena R, López P, Martín J (2014) 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 68:571–581CrossRefGoogle Scholar
  40. Loew ER, Govardovskii VI (2001) Photoreceptors and visual pigments in the red-eared turtle, Trachemys scripta elegans. Vis Neurosci 18:753–757PubMedCrossRefGoogle Scholar
  41. López P, Gabirot M, Martín J (2009) Immune challenge affects sexual coloration of male Iberian wall lizards. J Exp Zool A 311:96–104CrossRefGoogle Scholar
  42. Lovich JE, McCoy CJ, Garstka WR (1990) The development and significance of melanism in the slider turtle. In: Gibbons JW (ed) Life history and ecology of the slider turtle. Smithsonian Institution Press, Washington, DC, pp 233–254Google Scholar
  43. Macedonia JM, James S, Wittle LW, Clark DL (2000) Skin pigments and coloration in the Jamaican radiation of Anolis lizards. J Herpetol 34:99–109CrossRefGoogle Scholar
  44. Martín J, López P (2009) Multiple color signals may reveal multiple messages in male Schreiber’s green lizards, Lacerta schreiberi. Behav Ecol Sociobiol 63:1743–1755CrossRefGoogle Scholar
  45. Marvin GA, Lutterschmidt WI (1997) Locomotor performance in juvenile and adult box turtles (Terrapene carolina): a reanalysis for effects of body size and extrinsic load using a terrestrial species. J Herpetol 31:582–586CrossRefGoogle Scholar
  46. McGraw KJ (2005) The antioxidant function of many animal pigments: are there consistent health benefits of sexually selected colourants? Anim Behav 69:757–764CrossRefGoogle Scholar
  47. McGraw KJ, Ardia DR (2003) Carotenoids, immunocompetence, and the information content of sexual colors: an experimental test. Am Nat 162:704–712PubMedCrossRefGoogle Scholar
  48. Milinski M, Bakker TCM (1990) Female sticklebacks use male coloration in mate choice and hence avoid parasitized males. Nature 344:330–333CrossRefGoogle Scholar
  49. Møller AP, Biard C, Blount JD, Houston DC, Ninni P, Saino N, Surai PF (2000) Carotenoid-dependent signals: indicators of foraging efficiency, immunocompetence or detoxification ability? Avian Poult Biol Rev 11:137–159Google Scholar
  50. Montgomerie R (2006) Analyzing colors. In: Hill GE, McGraw KJ (eds) Bird coloration vol 1. Mechanisms and measurements. Harvard University Press, Cambridge, pp 90–147Google Scholar
  51. Montgomerie R (2008) CLR, version 1.05. Queen’s University, Kingston, Canada. (Available at http://post.queensu.ca/~mont/color/analyze.html)
  52. Mougeot F, Pérez-Rodríguez L, Sumozas N, Terraube J (2009) Parasites, condition, immune responsiveness and carotenoid-based ornamentation in male red-legged partridge Alectoris rufa. J Avian Biol 40:67–74CrossRefGoogle Scholar
  53. Muñoz A (2004) Chemo-orientation using conspecific chemical cues in the stripe-necked terrapin (Mauremys leprosa). J Chem Ecol 30:519–530PubMedCrossRefGoogle Scholar
  54. Peters A, Denk AG, Delhey K, Kempenaers B (2004) Carotenoid-based bill colour as an indicator of immunocompetence and sperm performance in male mallards. J Evol Biol 17:1111–1120PubMedCrossRefGoogle Scholar
  55. Pike TW, Blount JD, Lindström J, Metcalfe NB (2007) Availability of non-carotenoid antioxidants affects the expression of a carotenoid-based sexual ornament. Biol Lett 3:353–356PubMedCentralPubMedCrossRefGoogle Scholar
  56. Polo-Cavia N, López P, Martín J (2013) Head coloration reflects health state in the red-eared slider Trachemys scripta elegans. Behav Ecol Sociobiol 67:153–162CrossRefGoogle Scholar
  57. Pomiankowski AN (1988) The evolution of female mate preferences for male genetic quality. Oxf Surv Evol Biol 5:136–184Google Scholar
  58. Poschadel JR, Meyer-Lucht Y, Plath M (2006) Response to chemical cues from conspecifics reflects male mating preference for large females and avoidance of large competitors in the European pond turtle, Emys orbicularis. Behaviour 143:569–587CrossRefGoogle Scholar
  59. Roulin A, Jungi TW, Pfister H, Dijkstra C (2000) Female barn owls (Tyto alba) advertise good genes. Proc R Soc Lond B 267:937–941CrossRefGoogle Scholar
  60. Rowe JW, Gradel JR, Bunce CF, Clark DL (2013) Sexual dimorphism in size and shell shape, and dichromatism of spotted turtles (Clemmys guttata) in Southwestern Michigan. Amphibia-Reptilia 33:443–450CrossRefGoogle Scholar
  61. 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 181:396–409PubMedCrossRefGoogle Scholar
  62. Sheldon BC, Verhulst S (1996) Ecological immunology: costly parasite defence and trade-offs in evolutionary ecology. Trends Ecol Evol 11:317–321PubMedCrossRefGoogle Scholar
  63. Steffen JE, McGraw KJ (2007) Contributions of pterin and carotenoid pigments to dewlap coloration in two anole species. Comp Biochem Physiol B 146:42–46PubMedCrossRefGoogle Scholar
  64. Steffen JE, Learn KM, Drumheller JS, Boback SM, McGraw KJ (2014) Carotenoid composition of colorful body stripes and patches in the painted turtle (Chrysemys picta) and red-eared slider (Trachemys scripta). J HerpetolGoogle Scholar
  65. Sundberg J (1995) Female yellowhammers (Emberiza citrinella) prefer yellower males: a laboratory experiment. Behav Ecol Sociobiol 37:275–282CrossRefGoogle Scholar
  66. Svensson PA, Wong BBM (2011) Carotenoid-based signals in behavioural ecology: a review. Behaviour 148:131–189CrossRefGoogle Scholar
  67. Uller T, Isaksson C, Olsson M (2006) Immune challenge reduces reproductive output and growth in a lizard. Funct Ecol 20:873–879CrossRefGoogle Scholar
  68. 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 266:1–12CrossRefGoogle Scholar
  69. Wedekind C (1992) Detailed information about parasites revealed by sexual ornamentation. Proc R Soc Lond B 247:169–174CrossRefGoogle Scholar
  70. Wedekind C, Folstad I (1994) Adaptive or nonadaptive immunosuppression by sex hormones. Am Nat 143:936–938CrossRefGoogle Scholar
  71. Weiss SL (2006) Female-specific color is a signal of quality in the striped plateau lizard (Sceloporus virgatus). Behav Ecol 17:726–732CrossRefGoogle Scholar
  72. Weiss SL, Kennedy EA, Safran RJ, McGraw KJ (2011) Pterin-based ornamental coloration predicts yolk antioxidant levels in female striped plateau lizards (Sceloporus virgatus). J Anim Ecol 80:519–527PubMedCrossRefGoogle Scholar
  73. Westneat DF, Birkhead TR (1998) Alternative hypothesis linking the immune system and mate choice for good genes. Proc R Soc Lond B 265:1065–1073CrossRefGoogle Scholar
  74. Zahavi A (1975) Mate selection—a selection for a handicap. J Theor Biol 53:205–214PubMedCrossRefGoogle Scholar
  75. Zani PA, Claussen DL (1994) Voluntary and forced terrestrial locomotion in juvenile and adult painted turtles, Chrysemys picta. Copeia 1994:466–471CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Alejandro Ibáñez
    • 1
  • Nuria Polo-Cavia
    • 2
  • Pilar López
    • 1
  • José Martín
    • 1
  1. 1.Departamento de Ecología EvolutivaMuseo Nacional de Ciencias Naturales, C.S.I.C.MadridSpain
  2. 2.Departamento de BiologíaUniversidad Autónoma de MadridMadridSpain

Personalised recommendations