Behavioral Ecology and Sociobiology

, Volume 57, Issue 3, pp 197–214 | Cite as

Complex signal function: developing a framework of testable hypotheses

  • Eileen A. Hebets
  • Daniel R. Papaj


The basic building blocks of communication are signals, assembled in various sequences and combinations, and used in virtually all inter- and intra-specific interactions. While signal evolution has long been a focus of study, there has been a recent resurgence of interest and research in the complexity of animal displays. Much past research on signal evolution has focused on sensory specialists, or on single signals in isolation, but many animal displays involve complex signaling, or the combination of more than one signal or related component, often serially and overlapping, frequently across multiple sensory modalities. Here, we build a framework of functional hypotheses of complex signal evolution based on content-driven (ultimate) and efficacy-driven (proximate) selection pressures (sensu Guilford and Dawkins 1991). We point out key predictions for various hypotheses and discuss different approaches to uncovering complex signal function. We also differentiate a category of hypotheses based on inter-signal interactions. Throughout our review, we hope to make three points: (1) a complex signal is a functional unit upon which selection can act, (2) both content and efficacy-driven selection pressures must be considered when studying the evolution of complex signaling, and (3) individual signals or components do not necessarily contribute to complex signal function independently, but may interact in a functional way.


Multimodal signal Multicomponent signal Communication Signal design Signal interactions 



We would like to thank R. Hoy, K. Reeve, J. Bradbury, N. Vander Sal, D. Elias, and members of the Papaj Lab for commenting on earlier drafts of this manuscript. We would also like to thank A. Cutter and W. Maddison for fruitful discussions and two anonymous reviewers for invaluable suggestions and insights.


  1. Acquistapace P, Aquiloni L, Hazlett BA, Gherardi F (2002) Multimodal communication in crayfish: sex recognition during mate search by male Austropotamobius pallipes. Can J Zool 80:2041–2045CrossRefGoogle Scholar
  2. Andersson M (1982) Female choice selects for extreme tail length in a Widowbird. Nature 299:818–820Google Scholar
  3. Badyaev AV, Hill GE (2000) Evolution of sexual dichromatism: contribution of carotenoid- versus melanin-based coloration. Biol J Linn Soc 69:153–172CrossRefGoogle Scholar
  4. Bailey WJ (1991) Acoustic behaviour of insects: an evolutionary perspective. Chapman and Hall, LondonGoogle Scholar
  5. Bailey WJ, Cunningham RJ, Lebel L (1990) Song power, spectral distribution and female phonotaxis in the bushcricket Requena-Verticalis (Tettigoniidae, Orthoptera) - active female choice or passive attraction. Anim Behav 40:33–42Google Scholar
  6. Balakrishnan R, Helversen D von, Helversen O von (2001) Song pattern recognition in the grasshopper Chorthippus biguttulus: the mechanism of syllable onset and offset detection. J Comp Physiol A 187:255–264CrossRefPubMedGoogle Scholar
  7. Basolo AL (1990) Female preference predates the evolution of the sword in swordtail fish. Science 250:808–810Google Scholar
  8. Baurecht D, Barth FG (1992) Vibratory communication in spiders .1. Representation of male courtship signals by female vibration receptor. J Comp Physiol A 171:231–243CrossRefGoogle Scholar
  9. Birkhead TR, Fletcher F, Pellatt EJ (1998) Sexual selection in the zebra finch Taeniopygia guttata: condition, sex traits and immune capacity. Behav Ecol Sociobiol 44:179–191CrossRefGoogle Scholar
  10. Bischoff RJ, Gould JL, Rubenstein DI (1985) Tail size and female choice in the guppy (Poecilia reticulata). Behav Ecol Sociobiol 17:253–255CrossRefGoogle Scholar
  11. Blanco G, De la Puente J (2002) Multiple elements of the black-billed magpie’s tail correlate with variable honest information on quality in different age/sex classes. Anim Behav 63:217–225CrossRefGoogle Scholar
  12. Borgia G, Presgraves DC (1998) Coevolution of elaborated male display traits in the spotted bowerbird: an experimental test of the threat reduction hypothesis. Anim Behav 56:1121–1128CrossRefPubMedGoogle Scholar
  13. Bradbury JW, Vehrencamp SL (1998) Principles of animal communication. Sinauer, Sunderland, Mass.Google Scholar
  14. Brodie ED (1992) Correlational selection for color pattern and antipredator behavior in the garter snake Thamnophis ordinoides. Evolution 46:1284–1298Google Scholar
  15. Brooks R, Caithness N (1995) Does a males attractiveness to a female depend on her previous experience. S Afr J Sci 91:156–158Google Scholar
  16. Buchholz R (1991) Older males have bigger knobs—Correlates of ornamentation in 2 species of curassow. Auk 108:153–160Google Scholar
  17. Candolin U (2003) The use of multiple cues in mate choice. Biol Rev 78:575–595CrossRefPubMedGoogle Scholar
  18. Candolin U, Reynolds JD (2001) Sexual signaling in the European bitterling: females learn the truth by direct inspection of the resource. Behav Ecol 12:407–411CrossRefGoogle Scholar
  19. Coleman SW, Patricelli GL, Borgia G (2004) Variable female preferences drive complex male displays. Nature 428:742–745CrossRefPubMedGoogle Scholar
  20. Cooper BG, Goller F (2004) Multimodal signals: enhancement and constraint of song motor patterns by visual display. Science 303:544–546CrossRefPubMedGoogle Scholar
  21. Cott HB (1940) Adaptive coloration in animals. Methuen, LondonGoogle Scholar
  22. Cynx J, Lewis R, Tavel B, Tse H (1998) Amplitude regulation of vocalizations in noise by a songbird, Taeniopygia guttata. Anim Behav 56:107–113CrossRefPubMedGoogle Scholar
  23. De caprona MDC, Ryan MJ (1990) Conspecific mate recognition in swordtails, Xiphophorus nigrensis and X. pygmaeus (Poeciliidae)—Olfactory and visual cues. Anim Behav 39:290–296Google Scholar
  24. Doucet SM, Montgomerie R (2003) Multiple sexual ornaments in satin bowerbirds: ultraviolet plumage and bowers signal different aspects of quality. Behav Ecol 14:503–509CrossRefGoogle Scholar
  25. Draganoiu TI, Nagle L, Kreutzer M (2002) Directional female preference for an exaggerated male trait in canary (Serinus canaria) song. Proc R Soc Lond B Biol Sci 269:2525–2531CrossRefPubMedGoogle Scholar
  26. Dukas R (2002) Behavioural and ecological consequences of limited attention. Philos Trans R Soc Lond B Biol Sci 357:1539–1547CrossRefPubMedGoogle Scholar
  27. Dyer FC (2002) The biology of the dance language. Annu Rev Entomol 47:917–949CrossRefPubMedGoogle Scholar
  28. Edmunds M (1974) Defense in animals. Longman, HarlowGoogle Scholar
  29. Endler JA (1992) Signals, signal conditions, and the direction of evolution. Am Nat 139:S125-S153CrossRefGoogle Scholar
  30. Endler JA, Thery M (1996) Interacting effects of lek placement, display behavior, ambient light, and color patterns in three neotropical forest-dwelling birds. Am Nat 148:421–452CrossRefGoogle Scholar
  31. Endler JA, Basolo AL, Glowacki S, Zerr J (2001) Variation in response to artificial selection for light sensitivity in guppies (Poecilia reticulata). Am Nat 158:36–48CrossRefGoogle Scholar
  32. Ewing A (1989) Arthropod bioacoustics: neurobiology and behavior. Cornell University, IthacaGoogle Scholar
  33. Fleishman LJ (2000) Signal function, signal efficiency and the evolution of anoline lizard dewlap color. In: Epsmark Y, Amundsen T GR (eds) Animal Signals: signalling and signal design in animal communication. Tapir Academic, Trondheim, pp 209–236Google Scholar
  34. Fox D (1976) Animal biochromes and structural colors. University of California Press, Berkeley, Calif.Google Scholar
  35. Gerhardt HC (1991) Female mate choice in treefrogs—static and dynamic acoustic criteria. Anim Behav 42:615–635Google Scholar
  36. Gerhardt HC, Huber F (2002) Acoustic communication in insects and anurans. University of Chicago Press, ChicagoGoogle Scholar
  37. Glassey B, Forbes S (2002) Muting individual nestlings reduces parental foraging for the brood. Anim Behav 63:779–786CrossRefGoogle Scholar
  38. Gong A, Gibson RM (1996) Reversal of a female preference after visual exposure to a predator in the guppy, Poecilia reticulata. Anim Behav 52:1007–1015CrossRefGoogle Scholar
  39. Grahn M, Vonschantz T (1994) Fashion and age in pheasants—age-differences in mate choice. Proc R Soc Lond B Biol Sci 255:237–241Google Scholar
  40. Grether GF (1996) Sexual selection and survival selection on wing coloration and body size in the rubyspot damselfly Hetaerina americana. Evolution 50:1939–1948Google Scholar
  41. Grether GF, Hudon J, Millie DF (1999) Carotenoid limitation of sexual coloration along an environmental gradient in guppies. Proc R Soc Lond B Biol Sci 266:1317–1322CrossRefGoogle Scholar
  42. Guilford T, Dawkins MS (1991) Receiver psychology and the evolution of animal signals. Anim Behav 42:1–14Google Scholar
  43. Halliday TR, Slater PJB (1983) Animal behaviour, vol 2. Freeman, New YorkGoogle Scholar
  44. Hankison SJ, Morris MR (2002) Sexual selection and species recognition in the pygmy swordtail, Xiphophorus pygmaeus: conflicting preferences. Behav Ecol Sociobiol 51:140–145CrossRefGoogle Scholar
  45. Hasson O (1989) Amplifiers and the handicap principle in sexual selection: a different emphasis. Proc R Soc Lond B Biol Sci 235Google Scholar
  46. Hasson O (1991) Sexual displays as amplifiers—practical examples with an emphasis on feather decorations. Behav Ecol 2:189–197Google Scholar
  47. Hasson O (1994) Cheating signals. J Theor Biol 167:223–238CrossRefGoogle Scholar
  48. Hasson O (1997) Towards a general theory of biological signaling. J Theor Biol 185:139–156CrossRefPubMedGoogle Scholar
  49. Hauser M (1996) The evolution of communication. MIT Press, Cambridge, Mass.Google Scholar
  50. Hebets EA (2002) The evolution and function of complex signaling in spider courtship behavior. Ecology and evolutionary biology. PhD dissertation, University of Arizona, Tucson, Ariz.Google Scholar
  51. Hebets E (2003) Subadult experience influences adult mate choice in an arthropod: exposed female wolf spiders prefer males of a familiar phenotype. Proc Natl Acad Sci USA 100:13390–13395CrossRefPubMedGoogle Scholar
  52. Hebets EA (2004) Attention-altering interaction in the multimodal courtship display of the wolf spider Schizocosa uetzi. Behav Ecol (in press)Google Scholar
  53. Hebets EA, Uetz GW (1999) Female responses to isolated signals from multimodal male courtship displays in the wolf spider genus Schizocosa (Araneae : Lycosidae). Anim Behav 57:865–872CrossRefPubMedGoogle Scholar
  54. Hebets EA, Uetz GW (2000) Leg ornamentation and the efficacy of courtship display in four species of wolf spider (Araneae : Lycosidae). Behav Ecol Sociobiol 47:280–286CrossRefGoogle Scholar
  55. Hebets EA, Stratton GE, Miller GL (1996) Habitat and courtship behavior of the wolf spider Schizocosa retrorsa (Banks) (Araneae, Lycosidae). J Arachnol 24:141–147Google Scholar
  56. Holland B, Rice WR (1998) Perspective: chase-away sexual selection: antagonistic seduction versus resistance. Evolution 52:1–7Google Scholar
  57. Hölldobler B (1999) Multimodal signals in ant communication. J Comp Physiol A 184:129–141CrossRefGoogle Scholar
  58. Hughes M (1996) The function of concurrent signals: visual and chemical communication in snapping shrimp. Anim Behav 52:247–257CrossRefGoogle Scholar
  59. Jackson J, Ingram WI, Campbell HW (1976) The dorsal pigmentation pattern of snakes as an antipredator strategy: a multivariate approach. Am Nat 110:1029–1053CrossRefGoogle Scholar
  60. Jacobs GH, Neitz J, Neitz M (1993) Genetic basis of polymorphism in the color vision of platyrrhine monkeys. Vision Res 33:269–274CrossRefPubMedGoogle Scholar
  61. Jawor JM, Gray N, Beall SM, Breitwisch R (2004) Multiple ornaments correlate with aspects of condition and behaviour in female northern cardinals, Cardinalis cardinalis. Anim Behav 67:875–882CrossRefGoogle Scholar
  62. Jetz W, Rowe C, Guilford T (2001) Non-warning odors trigger innate color aversions—as long as they are novel. Behav Ecol 12:134–139CrossRefGoogle Scholar
  63. Johnstone RA (1996) Multiple displays in animal communication: ‘backup signals’ and ‘multiple messages’. Philos Trans R Soc Lond B Biol Sci 351:329–338Google Scholar
  64. Kaye H, Mackintosh NJ, Rothschild M (1989) Odour of pyrazine potentiates an association between environmental cues and unpalatable taste. Anim Behav 37:563–568Google Scholar
  65. Leal M, Fleishman LJ (2004) Differences in visual signal design and detectability between allopatric populations of Anolis lizards. Am Nat 163:26–39CrossRefPubMedGoogle Scholar
  66. Lengagne T, Slater PJB (2002) The effects of rain on acoustic communication: tawny owls have good reason for calling less in wet weather. Proc R Soc Lond B Biol Sci 269:2121–2125CrossRefPubMedGoogle Scholar
  67. Lengagne T, Aubin T, Lauga J, Jouventin P (1999) How do king penguins (Aptenodytes patagonicus) apply the mathematical theory of information to communicate in windy conditions? Proc R Soc Lond B Biol Sci 266:1623–1628CrossRefGoogle Scholar
  68. Ligon JD, Zwartjes PW (1995) Ornate plumage of male red junglefowl does not influence mate choice by females. Anim Behav 49:117–125CrossRefGoogle Scholar
  69. Lindstrom L, Rowe C, Guilford T (2001) Pyrazine odour makes visually conspicuous prey aversive. Proc R Soc Lond B Biol Sci 268:159–162CrossRefPubMedGoogle Scholar
  70. Lloyd JE (1971) Bioluminescent communication in insects. Annu Rev Entomol 16:97–122CrossRefGoogle Scholar
  71. Macaluso E, Frith CD, Driver J (2000) Modulation of human visual cortex by crossmodal spatial attention. Science 289:1206–1208CrossRefPubMedGoogle Scholar
  72. Marchetti K (1998) The evolution of multiple male traits in the yellow-browed leaf warbler. Anim Behav 55:361–376CrossRefPubMedGoogle Scholar
  73. Markl H (1983) Vibrational communication. In: Huber R, Markl H (eds) Neuroethology and behavioral physiology. Springer, Berlin Heidelberg New York, pp 332–353Google Scholar
  74. Marples NM, Roper TJ (1996) Effects of novel colour and smell on the response of naive chicks towards food and water. Anim Behav 51:1417–1424CrossRefGoogle Scholar
  75. Marples NM, Van Veelen W, Brakefield PM (1994) The relative importance of colour, taste and smell in the protection of an aposematic insect Coccinella septempunctata. Anim Behav 48:967–974CrossRefGoogle Scholar
  76. Maynard Smith J, Harper DGC (1995) Animal signals: models and terminology. J Theor Biol 177:305–311CrossRefGoogle Scholar
  77. McClintock WJ, Uetz GW (1996) Female choice and pre-existing bias: visual cues during courtship in two Schizocosa wolf spiders (Araneae: Lycosidae). Anim Behav 52:167–181CrossRefGoogle Scholar
  78. McDonald CG, Hawryshyn CW (1995) Intraspecific variation of spectral sensitivity in threespine stickleback (Gasterosteus aculeatus) from different photic regimes. J Comp Physiol A 176:255–260CrossRefGoogle Scholar
  79. McGraw KJ, Hill GE (2000) Differential effects of endoparasitism on the expression of carotenoid- and melanin-based ornamental coloration. Proc R Soc Lond B Biol Sci 267:1525–1531CrossRefPubMedGoogle Scholar
  80. McLennan DA (2003) The importance of olfactory signals in the gasterosteid mating system: sticklebacks go multimodal. Biol J Linn Soc 80:555–572CrossRefGoogle Scholar
  81. Meredith MA, Stein BE (1996) Spatial determinants of multisensory integration in cat superior colliculus neurons. J Neurophysiol 75:1843–1857PubMedGoogle Scholar
  82. Møller AP, Pomiankowski A (1993) Why have birds got multiple sexual ornaments. Behav Ecol Sociobiol 32:167–176Google Scholar
  83. Møller AP, Thornhill R (1998) Bilateral symmetry and sexual selection: a meta-analysis. Am Nat 151:174–192CrossRefGoogle Scholar
  84. Narins PM, Capranica RR (1976) Sexual differences in auditory-system of tree frog Eleutherodactylus coqui. Science 192:378–380PubMedGoogle Scholar
  85. Partan S, Marler P (1999) Behavior—communication goes multimodal. Science 283:1272–1273CrossRefPubMedGoogle Scholar
  86. Patricelli GL, Uy JAC, Walsh G, Borgia G (2002) Male displays adjusted to female’s response—macho courtship by the satin bowerbird is tempered to avoid frightening the female. Nature 415:279–280CrossRefPubMedGoogle Scholar
  87. Patricelli GL, Uy JAC, Borgia G (2003) Multiple male traits interact: attractive bower decorations facilitate attractive behavioural displays in satin bowerbirds. Proc R Soc Lond B Biol Sci 270:2389–2395CrossRefPubMedGoogle Scholar
  88. Petrie M, Halliday T, Sanders C (1991) Peahens prefer peacocks with elaborate trains. Anim Behav 41:323–331Google Scholar
  89. Pfennig KS (1998) The evolution of mate choice and the potential for conflict between species and mate-quality recognition. Proc R Soc Lond B Biol Sci 265:1743–1748CrossRefGoogle Scholar
  90. Podos J (1997) A performance constraint on the evolution of trilled vocalizations in a songbird family (Passeriformes:Emberizidae). Evolution 51:537–551Google Scholar
  91. Reid ML, Weatherhead PJ (1990) Mate-choice criteria of Ipswich sparrows—the importance of variability. Anim Behav 40:538–544Google Scholar
  92. Ronacher B, Rudiger K (2000) Temporal integration vs. parallel processing: coping with the variability of neuronal messages in directional hearing of insects. Eur J Neurosci 12:2147–2156CrossRefPubMedGoogle Scholar
  93. Ronacher B, Franz A, Wohlgemuth S, Hennig R (2004) Variability of spike trains and the processing of temporal patterns of acoustic signals—problems, constraints, and solutions. J Comp Physiol A 190:257–277CrossRefGoogle Scholar
  94. Roper TJ, Marples NM (1997) Odour and colour as cues for taste-avoidance learning in domestic chicks. Anim Behav 53:1241–1250CrossRefPubMedGoogle Scholar
  95. Rosenthal GG, Rand AS, Ryan MJ (2004) The vocal sac as a visual cue in anuran communication: an experimental analysis using video playback. Anim Behav 68:55–58CrossRefGoogle Scholar
  96. Rothschild M (1961) Defensive odours and Mullerian mimicry among insects. Trans R Entomol Soc Lond 113:101–121Google Scholar
  97. Rothschild M, Haskell PT (1966) Stridulation of the garden tiger moth Arctia caja audible to the human ear. Proc R Entomol Soc Lond A 41:167–170Google Scholar
  98. Rowe C (1999) Receiver psychology and the evolution of multicomponent signals. Anim Behav 58:921–931CrossRefPubMedGoogle Scholar
  99. Rowe C (2002) Sound improves visual discrimination learning in avian predators. Proc R Soc Lond B Biol Sci 269:1353–1357CrossRefPubMedGoogle Scholar
  100. Rowe C, Guilford T (1996) Hidden colour aversions in domestic clicks triggered by pyrazine odours of insect warning displays. Nature 383:520–522CrossRefGoogle Scholar
  101. Rowe C, Guilford T (1999a) The evolution of multimodal warning displays. Evol Ecol 13:655–671Google Scholar
  102. Rowe C, Guilford T (1999b) Novelty effects in a multimodal warning signal. Anim Behav 57:341–346CrossRefPubMedGoogle Scholar
  103. Rowe C, Guilford T (2001) The evolution of multimodal warning displays. Evol Ecol 13:655–671Google Scholar
  104. Ryan MJ (1980) Female mate choice in a neotropical frog. Science 209:523–525Google Scholar
  105. Ryan MJ (1985) Energetic efficiency of vocalization by the frog Physalaemus pustulosus. J Exp Biol 116:47–52Google Scholar
  106. Ryan MJ, Rand AS (1990) The sensory basis of sexual selection for complex calls in the Tungara frog, Physalaemus pustulosus (Sexual Selection for Sensory Exploitation). Evolution 44:305–314Google Scholar
  107. Ryan MJ, Wagner WE (1987) Asymmetries in mating preferences between species—female swordtails prefer heterospecific males. Science 236:595–597Google Scholar
  108. Savalli UM (1994) Tail length affects territory ownership in the yellow-shouldered widowbird. Anim Behav 48:105–111CrossRefGoogle Scholar
  109. Scheffer SJ, Uetz GW, Stratton GE (1996) Sexual selection, male morphology, and the efficacy of courtship signalling in two wolf spiders (Araneae: Lycosidae). Behav Ecol Sociobiol 38:17–23CrossRefGoogle Scholar
  110. Scheuber H, Jacot A, Brinkhof MWG (2003a) Condition dependence of a multicomponent sexual signal in the field cricket Gryllus campestris. Anim Behav 65:721–727CrossRefGoogle Scholar
  111. Scheuber H, Jacot A, Brinkhof MWG (2003b) The effect of past condition on a multicomponent sexual signal. Proc R Soc Lond B Biol Sci 270:1779–1784CrossRefPubMedGoogle Scholar
  112. Schuler W, Roper TJ (1992) Responses to warning coloration in avian predators. Adv Stud Behav 21:111–146Google Scholar
  113. Smith C, Reynolds JD, Sutherland W, Jurajda P (2000) Adaptive host choice and avoidance of superparasitism in the spawning decisions of bitterling (Rhodeus sericeus). Behav Ecol Sociobiol 48:29–35CrossRefGoogle Scholar
  114. Smith JW (1965) Message, meaning, and context in ethology. Am Nat 97:405–409CrossRefGoogle Scholar
  115. Spence C, Nicholls MER, Gillespie N, Driver J (1998) Cross-modal links in exogenous covert spatial orienting between touch, audition, and vision. Percept Psychophys 60:544–557PubMedGoogle Scholar
  116. Stokes D (1979) Stokes nature guides: a guide to bird behavior, vol I. Little, Brown, BostonGoogle Scholar
  117. Stokes D, Stokes L (1983) Stokes nature guides: a guide to bird behavior, vol II. Little, Brown, BostonGoogle Scholar
  118. Stokes D, Stokes L (1998) Stokes nature guides: a guide to bird behavior, vol III. Little, Brown, BostonGoogle Scholar
  119. Sumby WH, Pollack I (1954) Visual contribution to speech intelligibility in noise. J Acoust Soc Am 26:1298–1319Google Scholar
  120. Tibbetts EA (2002) Visual signals of individual identity in the wasp Polistes fuscatus. Proc R Soc Lond B Biol Sci 269:1423–1428CrossRefPubMedGoogle Scholar
  121. Tregenza T, Wedell N (2000) Genetic compatibility, mate choice and patterns of parentage: invited review. Mol Ecol 9:1013–1027CrossRefPubMedGoogle Scholar
  122. Uetz GW, Roberts JA (2002) Multisensory cues and multimodal communication in spiders: insights from video/audio playback studies. Brain Behav Evol 59:222–230CrossRefPubMedGoogle Scholar
  123. Van Staaden MJ, Romer H (1997) Sexual signalling in bladder grasshoppers: tactical design for maximizing calling range. J Exp Biol 200:2597–2608PubMedGoogle Scholar
  124. Von Helversen D (1984) Parallel processing in auditory pattern recognition and directional analysis by the grasshopper Chorthippus biguttulus L. (Acrididae). J Comp Physiol 154:837–846Google Scholar
  125. Wedekind C, Meyer P, Frischknecht M, Niggli UA, Pfander H (1998) Different carotenoids and potential information content of red coloration of male three-spined stickleback. J Chem Ecol 24:787–801CrossRefGoogle Scholar
  126. Wells KD (1977) The courtship of frogs. In: Taylor DH, Sheldon IG (eds) The reproductive biology of amphibians. Plenum, New York, pp 233–262Google Scholar
  127. Wiley RH (1994) Errors, exaggeration, and deception in animal communication. In: Real L (ed) Behavioral mechanisms in evolutionary ecology. University of Chicago Press, ChicagoGoogle Scholar
  128. Wilson EO (1975) Sociobiology. The new synthesis. Harvard University Press, CambridgeGoogle Scholar
  129. Zahavi A (1975) Mate selection—selection for a handicap. J Theor Biol 53:205–214PubMedGoogle Scholar
  130. Zahavi A (1987) The theory of signal selection and some of its implications. In: Delfino V (ed) International symposium of biological evolution. Adriatica Editrice, Bari, pp 305–327Google Scholar
  131. Zuk M, Ligon JD, Thornhill R (1993) Effects of experimental manipulation of male secondary sex characteristics on female mate preference in red jungle fowl. Anim Behav 44:999–1006Google Scholar

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© Springer-Verlag 2004

Authors and Affiliations

  1. 1.Division of Insect Biology, Department of Environmental Science, Policy and ManagementUniversity of CaliforniaBerkeleyUSA
  2. 2.Department of Ecology and Evolutionary BiologyUniversity of ArizonaTucsonUSA

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