Communication is ubiquitous. Developing a framework for the diversity of signals has important consequences for understanding alternative models of sexual selection and the processes contributing to speciation. In this article we review how models of neutral evolution in the perceptual space of signal perceivers provide a first step toward constructing a framework for signal diversity. We discuss how the distinction between additive and multiplicative effects of multimodal signaling represents a second step. We then assess how signal efficiency, reliability, and the aesthetics of perceivers provide distinct mechanisms for signals to be effective, thereby partly explaining signal diversity. Understanding the relative contribution of each of these mechanisms to the effectiveness of mate choice signals unravels the relative importance of alternative models of sexual selection. It can also help to distinguish whether divergence of communication is a driver or a consequence of speciation. Throughout the review we emphasize the importance of verification and learning in repeated interactions for understanding variation in signals.


Article metrics loading...

Loading full text...

Full text loading...


Literature Cited

  1. Alatalo RV, Mappes J. 1996. Tracking the evolution of warning signals. Nature 382:708–10 [Google Scholar]
  2. Andersson M. 1994. Sexual Selection Princeton, NJ: Princeton Univ. Press [Google Scholar]
  3. Armbruster WS, Antonsen L, Pélabon C. 2005. Phenotypic selection on Dalechampia blossoms: Honest signaling affects pollination success. Ecology 86:3323–33 [Google Scholar]
  4. Arnegard ME, McIntrye PB, Harmon LJ, Zelditch ML, Crampton WGR. et al. 2010. Sexual signal evolution outpaces ecological divergence during electric fish species radiation. Am. Nat. 176:335–56 [Google Scholar]
  5. Badyaev AV. 2004. Integration and modularity in the evolution of sexual ornaments. Phenotypic Integration: Studying the Ecology and Evolution of Complex Phenotype M Pigliucci, K Preston 50–79 Oxford, UK: Oxford Univ. Press [Google Scholar]
  6. Baker MC, Baker AEM. 1990. Reproductive behavior of female buntings: isolating mechanisms in a hybridizing pair of species. Evolution 44:332–38 [Google Scholar]
  7. Bascompte J, Jordano P. 2007. Plant-animal mutualistic networks: the architecture of biodiversity. Annu. Rev. Ecol. Evol. Syst. 38:567–93 [Google Scholar]
  8. Basolo AL. 1990. Female preference predates the evolution of the sword in swordtail fish. Science 250:808–10 [Google Scholar]
  9. Benitez-Vieyra S, Fornoni J, Pérez-Alquicira J, Boege K, Domínguez CA. 2014. The evolution of signal-reward correlations in bee- and hummingbird-pollinated species of Salvia. Proc. R. Soc. B 281:20132934 [Google Scholar]
  10. Benitez-Vieyra S, Ordano M, Fornoni J, Boege K, Domínguez CA. 2010. Selection on signal-reward correlation: limits and opportunities to the evolution of deceit in Turnera ulmifolia L. J. Evol. Biol. 23:2760–67 [Google Scholar]
  11. Berg RL. 1960. Ecological significance of correlation pleiades. Evolution 14:171–80 [Google Scholar]
  12. Boughman JW. 2001. Divergent sexual selection enhances reproductive isolation in sticklebacks. Nature 411:944–48 [Google Scholar]
  13. Boul KE, Funk CM, Darst CR, Cannatella DC, Ryan MJ. 2007. Sexual selection drives speciation in an Amazonian frog. Proc. R. Soc. B 274:399–406 [Google Scholar]
  14. Brandenburg A, Kuhlemeier C, Bshary R. 2012. Hawkmoth pollinators decrease seed set of a low-nectar Petunia axillaris line through reduced probing time. Curr. Biol. 22:1635–39 [Google Scholar]
  15. Bro-Jørgensen J. 2010. Dynamics of multiple signalling systems: animal communication in a world in flux. Trends Ecol. Evol. 25:292–300 [Google Scholar]
  16. Broom M, Ruxton GD, Schaefer HM. 2013. Signal verification can promote reliable signalling. Proc. R. Soc. B 280:20131560 [Google Scholar]
  17. Candolin U. 2003. The use of multiple cues in mate choice. Biol. Rev. 78:575–95 [Google Scholar]
  18. Cazetta E, Schaefer HM, Galetti M. 2009. Why are fruits colorful? The relative importance of achromatic and chromatic contrasts for detection by birds. Evol. Ecol. 23:233–44 [Google Scholar]
  19. Chaine AS, Lyon BE. 2007. Adaptive plasticity in female mate choice dampens sexual selection on male ornaments in the lark bunting. Science 319:459–62 [Google Scholar]
  20. Chittka L, Brockmann A. 2005. Perception space—the final frontier. PLOS Biol. 3:e137 [Google Scholar]
  21. Chittka L, Niven J. 2009. Are bigger brains better?. Curr. Biol. 19:R995–1008 [Google Scholar]
  22. Coleman SW, Patricelli GL, Borgia G. 2004. Variable female preferences drive complex male displays. Nature 428:742–45 [Google Scholar]
  23. Danchien E, Giraldeau L-A, Valone TJ, Wagner RH. 2004. Public information: from nosy neighbors to cultural evolution. Science 305:487–91 [Google Scholar]
  24. Darst CR, Cummings ME. 2006. Predator learning favours mimicry of a less-toxic model in poison frogs. Nature 440:208–11 [Google Scholar]
  25. Darst CR, Cummings ME, Cannatella DC. 2006. A mechanism for diversity in warning signals: conspicuousness versus toxicity in poison frogs. PNAS 103:5852–57 [Google Scholar]
  26. Dugatkin LA. 1992. Sexual selection and imitation: Females copy the mate choice of others. Am. Nat. 139:1384–89 [Google Scholar]
  27. Eltz T, Zimmermann Y, Pfeiffer C, Pech JR, Twele R. et al. 2008. An olfactory shift is associated with male perfume differentiation and species divergence in orchid bees. Curr. Biol. 18:1844–48 [Google Scholar]
  28. Endler JA. 1980. Natural selection on color patterns in Poecilia reticulata. Evolution 34:76–91 [Google Scholar]
  29. Endler JA. 2000. Evolutionary implications of the interaction between animal signals and the environment. Animal Signals Y Espmark, T Amundsen, G Rosenqvist 11–46 Trondheim, Nor: Tapir Academic [Google Scholar]
  30. Endler JA, Westcott DA, Madden JR, Robson T. 2005. Animal visual systems and the evolution of color patterns: Sensory processing illuminates signal evolution. Evolution 59:1795–818 [Google Scholar]
  31. Faivre B, Gregoire A, Préault M, Cezilly F, Sorci G. 2003. Immune activation rapidly mirrored in a secondary sexual trait. Science 300:103 [Google Scholar]
  32. Forstmeier W, Birkhead TR. 2004. Repeatability of mate choice in the zebra finch: consistency within and between females. Anim. Behav. 68:1017–28 [Google Scholar]
  33. Fuller RC, Houle D, Travis J. 2005. Sensory bias as an explanation for the evolution of mate preferences. Am. Nat. 166:437–66 [Google Scholar]
  34. Gardiner JM, Atema J, Hueter RE, Motta PJ. 2014. Multisensory integration and behavioral plasticity in sharks from different ecological niches. PLOS ONE 9:e93036 [Google Scholar]
  35. Getty T. 2006. Sexually selected signals are not similar to sports handicaps. Trends Ecol. Evol. 21:83–88 [Google Scholar]
  36. Gittleman JL, Harvey PH. 1980. Why are distasteful prey not cryptic?. Nature 286:149–50 [Google Scholar]
  37. Grafen A. 1990. Biological signals as handicaps. J. Theor. Biol. 144:517–46 [Google Scholar]
  38. Guerrieri F, Schubert M, Sandoz JC, Giurfa M. 2005. Perceptual and neural olfactory similarity in honeybees. PLOS Biol. 3:e60 [Google Scholar]
  39. Guilford T, Dawkins MS. 1991. Receiver psychology and the evolution of animal signals. Anim. Behav. 42:1–14 [Google Scholar]
  40. Hadfield JD, Burgess MD, Lord A, Phillimore AB, Clegg SM, Owens IPF. 2006. Direct versus indirect sexual selection: genetic basis of colour, size and recruitment in a wild bird. Proc. R. Soc. B 273:1347–53 [Google Scholar]
  41. Hadfield JD, Nutall A, Osorio D, Owens IPF. 2007. Testing the phenotypic gambit: phenotypic, genetic and environmental correlations of colour. J. Evol. Biol. 20:549–57 [Google Scholar]
  42. Halfwerk W, Page RA, Taylor RC, Wilson PS, Ryan MJ. 2014. Crossmodal comparisons of signal components allow for relative-distance assessment. Curr. Biol. 24:1751–55 [Google Scholar]
  43. Hankison SJ, Morris MR. 2003. Avoiding a compromise between sexual selection and species recognition: female swordtail fish assess multiple species-specific cues. Behav. Ecol. 14:282–87 [Google Scholar]
  44. Hebets EA, Papaj DR. 2005. Complex signal function: developing a framework of testable hypotheses. Behav. Ecol. Sociobiol. 57:197–214 [Google Scholar]
  45. Higginson AD, Reader T. 2009. Environmental heterogeneity, genotype-by-environment interactions and the reliability of sexual traits as indicators of mate quality. Proc. R. Soc. B 276:1153–59 [Google Scholar]
  46. Hoballah ME, Gübitz T, Stuurman J, Broger L, Barone M. et al. 2007. Single gene-mediated shift in pollinator attraction in Petunia. Plant Cell 19:779–90 [Google Scholar]
  47. Hoskin CJ, Higgie M, McDonald KR, Moritz C. 2005. Reinforcement drives rapid allopatric speciation. Nature 437:1353–56 [Google Scholar]
  48. Ingleby FC, Hosken DJ, Flowers K, Hawkes MF, Lane SM. et al. 2013. Genotype-by-environment interactions for cuticular hydrocarbon expression in Drosophlia simulans. J. Evol. Biol. 26:94–107 [Google Scholar]
  49. Katzenberger TD, Lunau K, Junker RR. 2013. Salience of multimodal flower cues manipulates initial responses and facilitates learning performance of bumblebees. Behav. Ecol. Sociobiol. 67:1587–99 [Google Scholar]
  50. Kirkpatrick M. 1982. Sexual selection and the evolution of female choice. Evolution 36:1–12 [Google Scholar]
  51. Kokko H, Brooks R, McNamara JM, Houston AI. 2002. The sexual selection continuum. Proc. R. Soc. B 269:1331–40 [Google Scholar]
  52. Kolm N, Amcoff M, Mann RP, Arnqvist G. 2012. Diversification of a food-mimicking male ornament via sensory drive. Curr. Biol. 22:1440–43 [Google Scholar]
  53. Krakauer DC, Johnstone RA. 1995. The evolution of exploitation and honesty in animal communication: a model using artificial neural networks. Philos. Trans. R. Soc. B 348:355–61 [Google Scholar]
  54. Kulahci IG, Dornhaus A, Papaj DR. 2008. Multimodal signals enhance decision making in foraging bumble-bees. Proc. R. Soc. B 275:797–802 [Google Scholar]
  55. Kunze J, Gumbert A. 2001. The combined effect of color and odor on flower choice behavior of bumble bees in flower mimicry systems. Behav. Ecol. 12:447–56 [Google Scholar]
  56. Lachmann M, Számado S, Bergstrom CT. 2001. Cost and conflict in animal signals and human language. PNAS 98:13189–94 [Google Scholar]
  57. Lande R. 1981. Models of speciation by sexual selection on polygenic traits. PNAS 78:3721–25 [Google Scholar]
  58. Macias Garcia C, Ramirez E. 2005. Evidence that sensory traps can evolve into honest signals. Nature 434:501–5 [Google Scholar]
  59. Majectic CJ, Raguso RA, Ashman T-L. 2009. The sweet smell of success: floral scent affects pollinator attraction and seed fitness in Hesperis matronalis. Funct. Ecol. 23:480–87 [Google Scholar]
  60. Maynard-Smith J, Harper DGC. 1995. Animal signals: models and terminology. J. Theor. Biol. 177:305–11 [Google Scholar]
  61. Mazur JE. 1994. Learning and Behavior Englewood Cliffs, NJ: Prentice Hall [Google Scholar]
  62. Milinski M, Bakker TCM. 1990. Female sticklebacks use male coloration in mate choice and hence avoid parasitized males. Nature 344:330–33 [Google Scholar]
  63. Morehouse NI, Rutowski RL. 2010. In the eyes of the beholders: Female choice and avian predation risk associated with an exaggerated male butterfly color. Am. Nat. 176:768–84 [Google Scholar]
  64. Mullen SP, Mendelson TC, Schal C, Shaw KL. 2007. Rapid evolution of cuticular hydrocarbons in a species radiation of acoustically diverse Hawaiian crickets (Gryllidae: Trigonidiinae: Laupala). Evolution 61:223–31 [Google Scholar]
  65. Naug D, Arathi HS. 2007. Receiver bias for exaggerated signals in honeybees and its implications for the evolution of floral displays. Biol. Lett. 3:635–37 [Google Scholar]
  66. Olito C, Fox JW. 2015. Species traits and abundances predict metrics of plant-pollinator network structure, but not pairwise interactions. Oikos 124:428–36 [Google Scholar]
  67. Ord TJ, Stamps JA. 2008. Alert signals enhance animal communication in “noisy” environments. PNAS 105:18830–35 [Google Scholar]
  68. Partan SR. 2013. Ten unanswered questions in multimodal communication. Behav. Ecol. Sociobiol. 67:1523–39 [Google Scholar]
  69. Pitchers WR, Brooks R, Jennions MD, Tregenza T, Dworkin I, Hunt J. 2013. Limited plasticity in the phenotypic variance-covariance matrix for male advertisement calls in the black field cricket, Teleogryllus commodus. J. Evol. Biol. 26:1060–78 [Google Scholar]
  70. Prum RO. 2010. The Lande-Kirkpatrick mechanism is the null model of evolution by intersexual selection: implications for meaning, honesty, and design in intersexual signals. Evolution 64:3085–100 [Google Scholar]
  71. Prum RO. 2012. Aesthetic evolution by mate choice: Darwin's really dangerous idea. Philos. Trans. R. Soc. B 367:2253–65 [Google Scholar]
  72. Raine NE, Chittka L. 2007. The correlation of learning speed and natural foraging success in bumble-bees. Proc. R. Soc. B 275:803–8 [Google Scholar]
  73. Renoult JP, Schaefer HM, Verrier D, Charpentier ME. 2011. The evolution of the multicoloured face of mandrills: insights from the perceptual space of colour vision. PLOS ONE 6:e29117 [Google Scholar]
  74. Renoult JP, Thomann M, Schaefer HM, Cheptou P-O. 2013. Selection on quantitative colour variation in Centaurea cyanus: the role of the pollinator's visual system. J. Evol. Biol. 26:2415–27 [Google Scholar]
  75. Ruxton GD, Schaefer HM. 2011. Resolving current disagreements and ambiguities in the terminology of animal communication. J. Evol. Biol. 24:2574–85 [Google Scholar]
  76. Ruxton GD, Schaefer HM. 2013. Game theory, multi-modal signalling and the evolution of communication. Behav. Ecol. Sociobiol. 67:1417–23 [Google Scholar]
  77. Ryan MJ, Fox JM, Wilczynski W, Rand AS. 1990. Sexual selection for sensory exploitation in the frog Physalaemus pustulosus. Nature 343:187–95 [Google Scholar]
  78. Ryan MJ, Rand AS. 1990. The sensory basis of sexual selection for complex calls in the Túngara frog, Physalaemus pustulosus (sexual selection for sensory exploitation). Evolution 44:305–14 [Google Scholar]
  79. Schaefer HM, Ruxton GD. 2012. By-product information can stabilize the reliability of communication. J. Evol. Biol. 25:2412–21 [Google Scholar]
  80. Schaefer HM, Spitzer K, Bairlein F. 2008. Long-term effects of previous experience determine nutrient discrimination abilities in birds. Front. Zool. 5:4 [Google Scholar]
  81. Schaefer HM, Valido A, Jordano P. 2014. Birds see the true colours of fruits to live off the fat of the land. Proc. R. Soc. B 281:20132516 [Google Scholar]
  82. Schmidt V, Schaefer HM. 2004. Unlearned preference for red may facilitate recognition of palatable food in young omnivorous birds. Evol. Ecol. Res. 6:919–25 [Google Scholar]
  83. Schmidt V, Schaefer HM, Winkler H. 2004. Conspicuousness, not colour as foraging cue in plant-animal signalling. Oikos 106:551–57 [Google Scholar]
  84. Scott-Phillips TC, Blythe RA, Gardner A, West SA. 2012. How do communication systems emerge?. Proc. R. Soc. B 279:1943–49 [Google Scholar]
  85. Searcy WA, Nowicki S. 2005. The Evolution of Animal Communication Princeton, NJ: Princeton Univ. Press [Google Scholar]
  86. Seddon N, Merrill RM, Tobias JA. 2008. Sexually selected traits predict patterns of species richness in a diverse clade of subobscine birds. Am. Nat. 171:620–31 [Google Scholar]
  87. Seehausen O, Terai Y, Magalhaes IS, Carleton KL, Mrosso HDJ. et al. 2008. Speciation through sensory drive in cichlid fish. Nature 455:620–26 [Google Scholar]
  88. Siddall EC, Marples NM. 2008. Better to be bimodal: the interaction of color and odor on learning and memory. Behav. Ecol. 19:425–32 [Google Scholar]
  89. Steiger S, Peschke K, Francke W, Müller JK. 2007. The smell of parents: Breeding status influences cuticular hydrocarbon pattern in the burying beetle Nicrophorus vespilloides. Proc. R. Soc. B 274:2211–20 [Google Scholar]
  90. Steiger S, Schmitt T, Schaefer HM. 2011. The origin and dynamic evolution of chemical information transfer. Proc. R. Soc. B 278:970–79 [Google Scholar]
  91. Stevens M. 2013. Sensory Ecology, Behaviour, and Evolution Oxford, UK: Oxford Univ. Press [Google Scholar]
  92. Stoddard MC, Prum RO. 2008. Evolution of avian plumage color in a tetrahedral color space: a phylogenetic analysis of New World buntings. Am. Nat. 171:755–76 [Google Scholar]
  93. Stoddard MC, Prum RO. 2011. How colorful are birds? Evolution of the avian plumage color gamut. Behav. Ecol. 22:1042–52 [Google Scholar]
  94. Stournaras KE, Lo E, Böhning-Gaese K, Cazetta E, Dehling DM. et al. 2013.. How colorful are fruits? Limited color diversity in fleshy fruits on local and global scales. New Phytol. 198:617–29 [Google Scholar]
  95. Számado S. 2011. The cost of honesty and the fallacy of the handicap principle. Anim. Behav. 81:3–10 [Google Scholar]
  96. Taylor RC, Ryan MJ. 2013. Interactions of multisensory components perceptually rescue Túngara frog mating signals. Science 341:273–74 [Google Scholar]
  97. Tibbetts EA, Dale J. 2004. A socially enforced signal of quality in a paper wasp. Nature 432:218–22 [Google Scholar]
  98. Tinbergen N. 1952. “Derived” activities; their causation, biological significance, origin, and emancipation during evolution. Q. Rev. Biol. 27:1–32 [Google Scholar]
  99. Uy JAC, Moyle RG, Filardi CE. 2009. Plumage and song differences mediate species recognition between incipient flycatcher species of the Solomon Islands. Evolution 63:153–64 [Google Scholar]
  100. Uy JAC, Safran RJ. 2013. Variation in the temporal and spatial use of signals and its implications for multimodal communication. Behav. Ecol. Sociobiol. 67:1499–511 [Google Scholar]
  101. Valido A, Schaefer HM, Jordano P. 2011. Colour, design and reward: phenotypic integration of fleshy fruit displays. J. Evol. Biol. 24:751–60 [Google Scholar]
  102. Valone TJ. 2007. From eavesdropping on performance to copying the behavior of others: a review of public information use. Behav. Ecol. Sociobiol. 62:1–14 [Google Scholar]
  103. Vazquez DP. 2009. Evaluating multiple determinants of the structure of plant-animal mutualistic networks. Ecology 90:2039–46 [Google Scholar]
  104. Vortman Y, Lotem A, Dor R, Lovette I, Safran RJ. 2013. Multiple sexual signals and behavioral reproductive isolation in a diverging population. Am. Nat. 182:514–23 [Google Scholar]
  105. Wang IJ, Shaffer HB. 2008. Rapid color evolution in an aposematic species: a phylogenetic analysis of color variation in the strikingly polymorphic strawberry poison-dart frog. Evolution 62:2742–59 [Google Scholar]
  106. Wang Z, Schaefer HM. 2014. Limits of selection against cheaters: Birds prioritise visual fruit advertisement over taste. Oecologia 174:1293–300 [Google Scholar]
  107. Watzlawick P, Bavelas JB, Jackson DD. 1967. Pragmatics of Human Communication. A Study of Interactional Patterns, Pathologies, and Paradoxes. New York: W.W. Norton [Google Scholar]
  108. Willson MF. 1994. Fruit choices by captive American Robins. Condor 96:494–502 [Google Scholar]
  109. Wilson AJ, Dean M, Higham JP. 2013. A game theoretic approach to multimodal communication. Behav. Ecol. Sociobiol. 69:1399–415 [Google Scholar]
  110. Zahavi A. 1975. Mate selection—a selection for a handicap. J. Theor. Biol. 53:205–14 [Google Scholar]
  111. Zufall RA, Rausher MD. 2004. Genetic changes associated with floral adaptation restrict future evolutionary potential.. Nature 428:847–50 [Google Scholar]

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error