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The relative importance of body size and UV coloration in influencing male-male competition in a lacertid lizard

Abstract

Communication via color signals is common in natural systems. Ultraviolet (UV)-blue patches located on the outer-ventral scales of some lacertid lizards are thought to be involved in male-male competition. However, the mechanisms that maintain their honesty remain unknown. Here, we use the common wall lizard Podarcis muralis to test whether the lateral UV-blue spots are conventional signals, the honesty of which is guaranteed by receiver-dependent costs, and discuss their potential role as an amplifier of body size. We first described the morphology and reflectance properties of lateral UV-blue spots in common wall lizards and investigated how they influence male-male competition. Spot size and number, UV chroma, and conspicuousness (calculated using vision models) were significantly greater in adult males relative to adult females and adult males relative to juveniles. Total spot area (and not spot number) of adult males was positively correlated with body size. We conducted staged competition encounters between focal males and smaller or larger rivals with control or manipulated spots. Spots were enlarged in small rivals and reduced in large rivals to disrupt the phenotypic correlation between spot area and body size. Aggressiveness and dominance were positively influenced by body size in control encounters. Spot manipulations resulted in greater submission and less aggressiveness in focal males. These results contradict the predictions associated with conventional signals and amplifiers, but suggest that spots contributed to opponent evaluation during short-distance encounters between competing males.

Significance statement

Many animals use color to communicate. During intraspecific resource competition, some species use color signals as an assessment tool to determine if they should engage in or avoid conflicts. Studies have found that in non-mammalian vertebrates, UV coloration can be a good indicator of fighting ability or aggressiveness. We tested whether and how the UV-blue spots of common wall lizards play a role in male-male competition by studying the properties of their spots, and then used that information to design and conduct competition experiments between males involving spot manipulation. Both body size and spot manipulation influenced aggression and submission during encounters. In particular, results suggest that spot manipulation disrupted mutual assessment and thus that spots play a role in competition signaling in male common wall lizards.

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References

  1. Abalos J, Pérez i de Lanuza G, Carazo P, Font E (2016) The role of male coloration in the outcome of staged contests in the European common wall lizard (Podarcis muralis). Behaviour 153:607–631

    Google Scholar 

  2. Andersson MB (1994) Sexual selection. Princeton University Press, Princeton

    Google Scholar 

  3. Andrade P, Pinho C, Pérez i de Lanuza G, Afonso S, Brejcha J, Rubin CJ, Wallerman O, Pereira P, Sabatino SJ, Bellati A, Pellitteri-Rosa D, Bosakova Z, Bunikis I, Carretero MA, Feiner N, Marsik P, Paupério F, Salvi D, Soler L, While GM, Uller T, Font E, Andersson L, Carneiro M (2019) Regulatory changes in pterin and carotenoid genes underlie balanced color polymorphisms in the wall lizard. Proc Natl Acad Sci USA 116:5633–5642

    CAS  PubMed  Google Scholar 

  4. Aronsson M, Gamberale-Stille G (2009) Importance of internal pattern contrast and contrast against the background in aposematic signals. Behav Ecol 20:1356–1362

    Google Scholar 

  5. Badiane A, Pérez i de Lanuza G, García-Custodio MC, Carazo P, Font E (2017) Colour patch size and measurement error using reflectance spectrophotometry. Methods Ecol Evol 8:1585–1593

    Google Scholar 

  6. Baeckens S, Driessens T, Huyghe K, Vanhooydonck B, Van Damme R (2018) Intraspecific variation in the information content of an ornament: why relative dewlap size signals bite force in some, but not all island populations of Anolis sagrei. Integr Comp Biol 58:25–37

    PubMed  Google Scholar 

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

    PubMed  PubMed Central  Google Scholar 

  8. 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

    CAS  PubMed  PubMed Central  Google Scholar 

  9. Bennett A, Cuthill I, Norris K (1994) Sexual selection and the mismeasure of color. Am Nat 144:848–860

    Google Scholar 

  10. Blumstein DT, Daniel JC (2007) Quantifying behavior the JWatcher way. Sinauer Associates, Sunderland

  11. Bogaardt L, Johnstone RA (2016) Amplifiers and the origin of animal signals. Proc R Soc B 283:20160324

    Google Scholar 

  12. Bonnaffé W, Martin M, Mugabo M, Meylan S, Le Galliard JF (2018) Ontogenetic trajectories of body coloration reveal its function as a multicomponent nonsenescent signal. Ecol Evol 8:12299–12307

    PubMed  PubMed Central  Google Scholar 

  13. Bradbury J, Vehrencamp S (2011) Principles of animal communication. 2nd edn. Sinauer, Sunderland

    Google Scholar 

  14. Cabido C, Galán P, López P, Martín J (2009) Conspicuousness-dependent antipredatory behavior may counteract coloration differences in Iberian rock lizards. Behav Ecol 20:362–370

    Google Scholar 

  15. Candolin U (2000) Male-male competition ensures honest signaling of male parental ability in the three-spined stickleback (Gasterosteus aculeatus). Behav Ecol Sociobiol 49:57–61

    Google Scholar 

  16. Candolin U (2003) The use of multiple cues in mate choice. Biol Rev 78:575–595

    PubMed  Google Scholar 

  17. Carleton KL, Hárosi FI, Kocher TD (2000) Visual pigments of African cichlid fishes: evidence for ultraviolet vision from microspectrophotometry and DNA sequences. Vis Res 40:879–890

    CAS  PubMed  Google Scholar 

  18. Castellano S, Cermelli P (2010) Attractive amplifiers in sexual selection: where efficacy meets honesty. Evol Ecol 24:1187–1197

    Google Scholar 

  19. Dawkins MS, Guilford T (1991) The corruption of honest signalling. Anim Behav 41:865–873

    Google Scholar 

  20. Doucet SM, Montgomerie R (2003) Multiple sexual ornaments in satin bowerbirds: ultraviolet plumage and bowers signal different aspects of male quality. Behav Ecol 14:503–509

    Google Scholar 

  21. Edsman L (1990) Territoriality and competition in wall lizards. Dissertation. University of Stockholm, Sweden

  22. Etman EJ, Lelieveld HM, ten Cate C (2001) Male bill colour and competition in zebra finches. Behav Process 55:119–124

    Google Scholar 

  23. Fitzpatrick S (1998) Colour schemes for birds: structural coloration and signals of quality in feathers. Ann Zool Fenn 35:67–77

    Google Scholar 

  24. Fleishman L (2000) Signal function, signal efficiency and the evolution of anoline lizard dewlap color. In: Epsmark Y, Amundsen TGR (eds) Animal signals: signalling and signal design in animal communication. Tapir Academic, Trondheim, pp 209–236

    Google Scholar 

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

    Google Scholar 

  26. Galeotti P, Pellitteri-Rosa D, Sacchi R, Gentilli A, Pupin F, Rubolini D, Fasola M (2010) Sex-, morph-and size-specific susceptibility to stress measured by haematological variables in captive common wall lizard Podarcis muralis. Comp Biochem Physiol A Mol Integr Physiol 157:354–363

    PubMed  Google Scholar 

  27. Goldsmith TH (1990) Optimization, constraint, and history in the evolution of eyes. Q Rev Biol 65:281–322

    CAS  PubMed  Google Scholar 

  28. Gomez D (2006) AVICOL, a program to analyse spectrometric data. Available from the author upon request at dodogomez@yahoofr

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

    PubMed  Google Scholar 

  30. Guilford T, Dawkins MS (1995) What are conventional signals? Anim Behav 49:1689–1695

    Google Scholar 

  31. Harper D (2006) Maynard Smith: amplifying the reasons for signal reliability. J Theor Biol 239:203–209

    CAS  PubMed  Google Scholar 

  32. Hasson O (1989) Amplifiers and the handicap principle in sexual selection: a different emphasis. Proc R Soc Lond B 235:383–406

    CAS  PubMed  Google Scholar 

  33. Hasson O (1990) The role of amplifiers in sexual selection: an integration of the amplifying and the Fisherian mechanisms. Evol Ecol 4:277–289

    Google Scholar 

  34. Hasson O (1991) Sexual displays as amplifiers: practical examples with an emphasis on feather decorations. Behav Ecol 2:189–197

    Google Scholar 

  35. Hasson O (1997) Towards a general theory of biological signaling. J Theor Biol 185:139–156

    CAS  PubMed  Google Scholar 

  36. Hebets EA (2004) Attention-altering signal interactions in the multimodal courtship display of the wolf spider Schizocosa uetzi. Behav Ecol 16:75–82

    Google Scholar 

  37. Hebets EA, Papaj DR (2005) Complex signal function: developing a framework of testable hypotheses. Behav Ecol Sociobiol 57:197–214

    Google Scholar 

  38. Henningsen JP, Irschick DJ (2012) An experimental test of the effect of signal size and performance capacity on dominance in the green anole lizard. Funct Ecol 26:3–10

    Google Scholar 

  39. 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

    Google Scholar 

  40. Johnsen A, Delhey K, Schlicht E, Peters A, Kempenaers B (2005) Male sexual attractiveness and parental effort in blue tits: a test of the differential allocation hypothesis. Anim Behav 70:877–888

    Google Scholar 

  41. Johnstone RA (1998) Game theory and communication. In: Dugatkin LA, Reeve HK (eds) Game theory and animal behavior. Oxford University Press, Oxford, pp 94–117

    Google Scholar 

  42. Keyser AJ, Hill GE (2000) Structurally based plumage coloration is an honest signal of quality in male blue grosbeaks. Behav Ecol 11:202–209

    Google Scholar 

  43. Kokko H, López-Sepulcre A, Morrell LJ (2006) From hawks and doves to self-consistent games of territorial behavior. Am Nat 167:901–912

    PubMed  Google Scholar 

  44. Kurvers RH, Delhey K, Roberts ML, Peters A (2010) No consistent female preference for higher crown UV reflectance in blue tits Cyanistes caeruleus: a mate choice experiment. Ibis 152:393–396

    Google Scholar 

  45. 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

    PubMed  Google Scholar 

  46. LeBas NR, Marshall NJ (2000) The role of colour in signalling and male choice in the agamid lizard Ctenophorus ornatus. Proc R Soc Lond B 267:445–452

    CAS  Google Scholar 

  47. Ligon RA, McGraw KJ (2016) Social costs enforce honesty of a dynamic signal of motivation. Proc R Soc B 283:20161873

    PubMed  Google Scholar 

  48. López P, Martín J (2001) Fighting rules and rival recognition reduce costs of aggression in male lizards, Podarcis hispanica. Behav Ecol Sociobiol 49:111–116

    Google Scholar 

  49. López P, Muñoz A, Martín J (2002) Symmetry, male dominance and female mate preferences in the Iberian rock lizard, Lacerta monticola. Behav Ecol Sociobiol 52:342–347

    Google Scholar 

  50. López P, Martín J, Cuadrado M (2004) The role of lateral blue spots in intrasexual relationships between male Iberian rock-lizards, Lacerta monticola. Ethology 110:543–561

    Google Scholar 

  51. Marshall KL, Stevens M (2014) Wall lizards display conspicuous signals to conspecifics and reduce detection by avian predators. Behav Ecol 25:1325–1337

    PubMed  PubMed Central  Google Scholar 

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

    PubMed  Google Scholar 

  53. Martin M, Meylan S, Perret S, Le Galliard J-F (2015b) UV coloration influences spatial dominance but not agonistic behaviors in male wall lizards. Behav Ecol Sociobiol 69:1483–1491

    Google Scholar 

  54. Martin M, Meylan S, Haussy C, Decencière B, Perret S, Le Galliard J-F (2016) UV color determines the issue of conflicts but does not covary with individual quality in a lizard. Behav Ecol 27:262–270

    Google Scholar 

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

    Google Scholar 

  56. McGraw KJ, Mackillop EA, Dale J, Hauber ME (2002) Different colors reveal different information: how nutritional stress affects the expression of melanin-and structurally based ornamental plumage. J Exp Biol 205:3747–3755

    PubMed  Google Scholar 

  57. Mugabo M, Perret S, Legendre S, Galliard JF (2013) Density-dependent life history and the dynamics of small populations. J Anim Ecol 82:1227–1239

    PubMed  Google Scholar 

  58. Ord T, Klomp D, Garcia-Porta J, Hagman M (2015) Repeated evolution of exaggerated dewlaps and other throat morphology in lizards. J Evol Biol 28:1948–1964

    CAS  PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  60. Pérez i de Lanuza G, Font E (2015) Differences in conspicuousness between alternative color morphs in a polychromatic lizard. Behav Ecol 26:1432–1446

    Google Scholar 

  61. Pérez i de Lanuza G, Font E, Monterde J (2013) Using visual modelling to study the evolution of lizard coloration: sexual selection drives the evolution of sexual dichromatism in lacertids. J Evol Biol 26:1826–1835

    PubMed  Google Scholar 

  62. Pérez i de 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

    Google Scholar 

  63. Promislow DE, Montgomerie R, Martin TE (1992) Mortality costs of sexual dimorphism in birds. Proc R Soc Lond B 250:143–150

    Google Scholar 

  64. Pryke SR, Griffith SC (2006) Red dominates black: agonistic signalling among head morphs in the colour polymorphic Gouldian finch. Proc R Soc Lond B 273:949–957

    Google Scholar 

  65. Pryke S, Griffith S (2007) The relative role of male vs. female mate choice in maintaining assortative pairing among discrete colour morphs. J Evol Biol 20:1512–1521

    CAS  PubMed  Google Scholar 

  66. R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org

  67. Rémy A, Grégoire A, Perret P, Doutrelant C (2010) Mediating male–male interactions: the role of the UV blue crest coloration in blue tits. Behav Ecol Sociobiol 64:1839–1847

    Google Scholar 

  68. Rick IP, Bakker TCM (2008) Males do not see only red: UV wavelengths and male territorial aggression in the three-spined stickleback (Gasterosteus aculeatus). Naturwissenschaften 95:631–638

    CAS  PubMed  Google Scholar 

  69. 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

    Google Scholar 

  70. Rohwer S (1975) The social significance of avian winter plumage variability. Evolution 29:593–610

    PubMed  Google Scholar 

  71. Rowe C (1999) Receiver psychology and the evolution of multicomponent signals. Anim Behav 58:921–931

    CAS  PubMed  Google Scholar 

  72. Sacchi R, Pupin F, Gentilli A, Rubolini D, Scali S, Fasola M, Galeotti P (2009) Male–male combats in a polymorphic lizard: residency and size, but not color, affect fighting rules and contest outcome. Aggress Behav 35:274–283

    PubMed  Google Scholar 

  73. Salvador A, Díaz JA, Veiga JP, Bloor P, Brown RP (2007) Correlates of reproductive success in male lizards of the alpine species Iberolacerta cyreni. Behav Ecol 19:169–176

    Google Scholar 

  74. Schneider CA, Rasband WS, Eliceiri KW (2012) NIH image to ImageJ: 25 years of image analysis. Nat Methods 9:671

    CAS  PubMed  PubMed Central  Google Scholar 

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

    Google Scholar 

  76. Seehausen O, Schluter D (2004) Male–male competition and nuptial–colour displacement as a diversifying force in Lake Victoria cichlid fishes. Proc R Soc Lond B 271:1345–1353

    Google Scholar 

  77. Senar JC (1999) Plumage coloration as a signal of social status. In: Adams NJ, Slotow RH (eds) Proceedings of the 22nd International Ornithological Congress, BirdLife South Africa, Johannesburg, pp 1669–1686

  78. Siddiqi A, Cronin TW, Loew ER, Vorobyev M, Summers K (2004) Interspecific and intraspecific views of color signals in the strawberry poison frog Dendrobates pumilio. J Exp Biol 207:2471–2485

    PubMed  Google Scholar 

  79. Siebeck UE (2004) Communication in coral reef fish: the role of ultraviolet colour patterns in damselfish territorial behaviour. Anim Behav 68:273–282

    Google Scholar 

  80. Siebeck UE, Parker AN, Sprenger D, Mäthger LM, Wallis G (2010) A species of reef fish that uses ultraviolet patterns for covert face recognition. Curr Biol 20:407–410

    CAS  PubMed  Google Scholar 

  81. Siefferman L, Hill GE (2005) UV-blue structural coloration and competition for nestboxes in male eastern bluebirds. Anim Behav 69:67–72

    Google Scholar 

  82. Siitari H, Alatalo RV, Halme P, Buchanan KL, Kilpimaa J (2007) Color signals in the black grouse (Tetrao tetrix): signal properties and their condition dependency. Am Nat 169:S81–S92

    PubMed  Google Scholar 

  83. Smith EJ, Partridge JC, Parsons KN, White EM, Cuthill IC, Bennett AT, Church SC (2002) Ultraviolet vision and mate choice in the guppy (Poecilia reticulata). Behav Ecol 13:11–19

    Google Scholar 

  84. Speybroeck J, Beukema W, Bok B, van der Voort J (2016) Field guide to the amphibians and reptiles of Britain and Europe. Bloomsbury Publishing, London

    Google Scholar 

  85. Stapley J, Whiting MJ (2006) Ultraviolet signals fighting ability in a lizard. Biol Lett 2:169–172

    PubMed  PubMed Central  Google Scholar 

  86. Stoddard MC, Prum RO (2008) Evolution of avian plumage color in a tetrahedral color space: a phylogenetic analysis of new world buntings. Am Nat 171:755–776

    PubMed  Google Scholar 

  87. Taylor P, Hasson O, Clark D (2000) Body postures and patterns as amplifiers of physical condition. Proc R Soc Lond B 267:917–922

    CAS  Google Scholar 

  88. Vacher J-P, Geniez M (2010) Les reptiles de France, Belgique, Luxembourg et Suisse. Biotope, Mèze

    Google Scholar 

  89. Vanhooydonck B, Herrel A, Van Damme R, Irschick D (2005) Does dewlap size predict male bite performance in Jamaican Anolis lizards? Funct Ecol 19:38–42

    Google Scholar 

  90. Vedder O, Schut E, Magrath MJ, Komdeur J (2010) Ultraviolet crown colouration affects contest outcomes among male blue tits, but only in the absence of prior encounters. Funct Ecol 24:417–425

    Google Scholar 

  91. Vehrencamp SL (2000) Handicap, index, and conventional signal elements of bird song. In: Espmark Y, Amundsen T, Rossenqvist G (eds) Animal signals: signalling and signal design in animal communication. Tapir Academic Press, Trondheim, pp 277–300

    Google Scholar 

  92. Vervust B, Van Damme R (2009) Marking lizards by heat branding. Herpetol Rev 40:173

    Google Scholar 

  93. Vorobyev M, Osorio D (1998) Receptor noise as a determinant of colour thresholds. Proc R Soc Lond B 265:351–358

    CAS  Google Scholar 

  94. Whiting MJ, Stuart-Fox DM, O'Connor D, Firth D, Bennett NC, Blomberg SP (2006) Ultraviolet signals ultra-aggression in a lizard. Anim Behav 72:353–363

    Google Scholar 

  95. Zahavi A (1975) Mate selection—a selection for a handicap. J Theor Biol 53:205–214

    CAS  PubMed  Google Scholar 

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Acknowledgments

We thank Cécile Vande Maele, Samuel Perret, and Beatriz Decencière Ferrandière for their help in the laboratory. We also thank the reviewers for their comments, which helped to improve the quality of the manuscript.

Funding

This research was supported by the Centre National de la Recherche Scientifique (CNRS).

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Correspondence to Gabrielle Names.

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Authorization No. Ce5/2011/044 allowed us to capture and manipulate wild animals for this study. Ethical approval from an ethics committee was not necessary. All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All procedures performed in studies involving animals were in accordance with the ethical standards of the institution at which the studies were conducted.

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Names, G., Martin, M., Badiane, A. et al. The relative importance of body size and UV coloration in influencing male-male competition in a lacertid lizard. Behav Ecol Sociobiol 73, 98 (2019). https://doi.org/10.1007/s00265-019-2710-z

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Keywords

  • Intrasexual competition
  • Podarcis muralis
  • UV coloration
  • Territorial conflict