SpringerLink
Log in

Meta-analysis reveals that animal sexual signalling behaviour is honest and resource based

  • Article
  • Published:

From Nature Ecology & Evolution

View current issue Submit your manuscript

Abstract

Animals often need to signal to attract mates and behavioural signalling may impose substantial energetic and fitness costs to signallers. Consequently, individuals often strategically adjust signalling effort to maximize the fitness payoffs of signalling. An important determinant of these payoffs is individual state, which can influence the resources available to signallers, their likelihood of mating and their motivation to mate. However, empirical studies often find contradictory patterns of state-based signalling behaviour. For example, individuals in poor condition may signal less than those in good condition to conserve resources (ability-based signalling) or signal more to maximize short-term reproductive success (needs-based signalling). To clarify this relationship, I systematically searched for published studies examining animal sexual signalling behaviour in relation to six aspects of individual state: age, mated status, attractiveness, body size, condition and parasite load. Across 228 studies and 147 species, individuals (who were predominantly male) invested more into behavioural signalling when in good condition. Overall, this suggests that animal sexual signalling behaviour is generally honest and ability-based. However, the magnitude of state-dependent plasticity was small and there was a large amount of between-study heterogeneity that remains unexplained.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Canada)

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1: Guide to the coding scheme for effect sizes used in this study.
Fig. 2: Summary of the dataset.
Fig. 3: Forest plot showing the mean effect size estimate (black circles) plus 95% CIs for each state factor category.
Fig. 4: Funnel plot showing the relationship between effect size (the correlation coefficient r) and inverse standard error after performing a trim-and-fill analysis.

Similar content being viewed by others

Data availability

The data that support the findings of this study are available from Figshare (https://doi.org/10.6084/m9.figshare.12973124).

Code availability

All code used for the analyses are available from Figshare (https://doi.org/10.6084/m9.figshare.12973124).

References

  1. Andersson, M. B. Sexual Selection (Princeton Univ. Press, 1994).

  2. Clark, C. J. The role of power versus energy in courtship: what is the ‘energetic cost’of a courtship display? Anim. Behav. 84, 269–277 (2012).

    Article  Google Scholar 

  3. Vehrencamp, S. L., Bradbury, J. W. & Gibson, R. M. The energetic cost of display in male sage grouse. Anim. Behav. 38, 885–896 (1989).

    Article  Google Scholar 

  4. Kotiaho, J. S. Costs of sexual traits: a mismatch between theoretical considerations and empirical evidence. Biol. Rev. 76, 365–376 (2001).

    Article  CAS  PubMed  Google Scholar 

  5. Mappes, J., Alatalo, R. V., Kotiaho, J. & Parri, S. Viability costs of condition-dependent sexual male display in a drumming wolf spider. Proc. R. Soc. Lond. B 263, 785–789 (1996).

    Article  Google Scholar 

  6. Zuk, M. & Kolluru, G. R. Exploitation of sexual signals by predators and parasitoids. Q. Rev. Biol. 73, 415–438 (1998).

    Article  Google Scholar 

  7. Woods, W. A. Jr, Hendrickson, H., Mason, J. & Lewis, S. M. Energy and predation costs of firefly courtship signals. Am. Nat.170, 702–708 (2007).

    Article  PubMed  Google Scholar 

  8. Lande, R. Models of speciation by sexual selection on polygenic traits. Proc. Natl Acad. Sci. USA 78, 3721–3725 (1981).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Cotton, S., Fowler, K. & Pomiankowski, A. Do sexual ornaments demonstrate heightened condition-dependent expression as predicted by the handicap hypothesis? Proc. R. Soc. Lond. B 271, 771–783 (2004).

    Article  Google Scholar 

  10. Tomkins, J. L., Radwan, J., Kotiaho, J. S. & Tregenza, T. Genic capture and resolving the lek paradox. Trends Ecol. Evol. 19, 323–328 (2004).

    Article  PubMed  Google Scholar 

  11. Grafen, A. Biological signals as handicaps. J. Theor. Biol. 144, 517–546 (1990).

    Article  CAS  PubMed  Google Scholar 

  12. Johnstone, R. A. Sexual selection, honest advertisement and the handicap principle: reviewing the evidence. Biol. Rev. 70, 1–65 (1995).

    Article  CAS  PubMed  Google Scholar 

  13. Seymour, R. M. & Sozou, P. D. Duration of courtship effort as a costly signal. J. Theor. Biol. 256, 1–13 (2009).

    Article  PubMed  Google Scholar 

  14. Byers, J., Hebets, E. & Podos, J. Female mate choice based upon male motor performance. Anim. Behav. 79, 771–778 (2010).

    Article  Google Scholar 

  15. Moran, N. P., Sánchez-Tójar, A., Schielzeth, H. & Reinhold, K. Poor nutritional condition promotes high-risk behaviours: a systematic review and meta-analysis. Biol. Rev. https://doi.org/10.1111/brv.12655 (2020).

  16. Cotton, S., Small, J. & Pomiankowski, A. Sexual selection and condition-dependent mate preferences. Curr. Biol. 16, R755–R765 (2006).

    Article  CAS  PubMed  Google Scholar 

  17. Kokko, H. Evolutionarily stable strategies of age-dependent sexual advertisement. Behav. Ecol. Sociobiol. 41, 99–107 (1997).

    Article  Google Scholar 

  18. Moore, F. R., Shuker, D. M. & Dougherty, L. Stress and sexual signaling: a systematic review and meta-analysis. Behav. Ecol. 27, 363–371 (2016).

    Article  Google Scholar 

  19. Dougherty, L. R. Meta-analysis shows the evidence for context-dependent mating behaviour is inconsistent or weak across animals. Ecol. Lett. https://doi.org/10.1111/ele.13679 (2021).

  20. Umbers, K. D., Symonds, M. R. & Kokko, H. The mathematics of female pheromone signaling: strategies for aging virgins. Am. Nat. 185, 417–432 (2015).

    Article  PubMed  Google Scholar 

  21. Simmons, L. W. Sexual signalling by females: do unmated females increase their signalling effort? Biol. Lett. https://doi.org/10.1098/rsbl.2015.0298 (2015).

  22. Reynolds, J. D. Should attractive individuals court more? Theory and a test. Am. Nat. 141, 914–927 (1993).

    Article  CAS  PubMed  Google Scholar 

  23. Jennions, M. D. & Backwell, P. R. Variation in courtship rate in the fiddler crab Uca annulipes: is it related to male attractiveness? Behav. Ecol. 9, 605–611 (1998).

    Article  Google Scholar 

  24. Candolin, U. The relationship between signal quality and physical condition: is sexual signalling honest in the three-spined stickleback? Anim. Behav. 58, 1261–1267 (1999).

    Article  CAS  PubMed  Google Scholar 

  25. Clutton-Brock, T. H. Reproductive effort and terminal investment in iteroparous animals. Am. Nat. 123, 212–229 (1984).

    Article  Google Scholar 

  26. Duffield, K. R., Bowers, E. K., Sakaluk, S. K. & Sadd, B. M. A dynamic threshold model for terminal investment. Behav. Ecol. Sociobiol. 71, 185 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  27. Buchanan, K. L., Spencer, K. A., Goldsmith, A. & Catchpole, C. Song as an honest signal of past developmental stress in the European starling (Sturnus vulgaris). Proc. R. Soc. Lond. B 270, 1149–1156 (2003).

    Article  CAS  Google Scholar 

  28. Chemnitz, J., Jentschke, P. C., Ayasse, M. & Steiger, S. Beyond species recognition: somatic state affects long-distance sex pheromone communication. Proc. R. Soc. B 282, 20150832 (2015).

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  29. Richardson, J. & Smiseth, P. T. Nutrition during sexual maturation and at the time of mating affects mating behaviour in both sexes of a burying beetle. Anim. Behav. 151, 77–85 (2019).

    Article  Google Scholar 

  30. Balsby, T. J. Song activity and variability in relation to male quality and female choice in whitethroats Sylvia communis. J. Avian Biol. 31, 56–62 (2000).

    Article  Google Scholar 

  31. Nickley, B., Saintignon, D. & Roberts, J. A. Influence of predator cues on terminal investment in courtship by male Schizocosa ocreata (Hentz, 1844) wolf spiders (Araneae: Lycosidae). J. Arachnol. 44, 176–181 (2016).

    Article  Google Scholar 

  32. Kehl, T. et al. Pheromone blend does not explain old male mating advantage in a butterfly. Ethology 120, 1137–1145 (2014).

    Article  Google Scholar 

  33. Houslay, T. M., Houslay, K. F., Rapkin, J., Hunt, J. & Bussiere, L. F. Mating opportunities and energetic constraints drive variation in age-dependent sexual signalling. Funct. Ecol. 31, 728–741 (2017).

    Article  Google Scholar 

  34. Smith, M. J. & Roberts, J. D. Call structure may affect male mating success in the quacking frog Crinia georgiana (Anura: Myobatrachidae). Behav. Ecol. Sociobiol. 53, 221–226 (2003).

    Article  Google Scholar 

  35. Lehtonen, T. K. Signal value of male courtship effort in a fish with paternal care. Anim. Behav. 83, 1153–1161 (2012).

    Article  Google Scholar 

  36. Bertram, S. M., Harrison, S. J., Thomson, I. R. & Fitzsimmons, L. P. Adaptive plasticity in wild field cricket’s acoustic signaling. PLoS ONE 8, e69247 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Rundus, A. S., Biemuller, R., DeLong, K., Fitzgerald, T. & Nyandwi, S. Age-related plasticity in male mate choice decisions by Schizocosa retrorsa wolf spiders. Anim. Behav. 107, 233–238 (2015).

    Article  Google Scholar 

  38. Koricheva, J., Gurevitch, J. & Mengeresen, K. Handbook of Meta-analysis in Ecology and Evolution (Princeton Univ. Press, 2013).

  39. Harts, A. M., Booksmythe, I. & Jennions, M. D. Mate guarding and frequent copulation in birds: a meta‐analysis of their relationship to paternity and male phenotype. Evolution 70, 2789–2808 (2016).

    Article  PubMed  Google Scholar 

  40. Partridge, C., Boettcher, A. & Jones, A. G. The role of courtship behavior and size in mate preference in the sex-role-reversed gulf pipefish, Syngnathus scovelli. Ethology 119, 692–701 (2013).

    Article  Google Scholar 

  41. Anderson, A. P. & Jones, A. G. Choosy Gulf pipefish males ignore age but prefer active females with deeply keeled bodies. Anim. Behav. 155, 37–44 (2019).

    Article  Google Scholar 

  42. Sundin, J., Rosenqvist, G. & Berglund, A. Hypoxia delays mating in the broad-nosed pipefish. Mar. Biol. Res. 11, 747–754 (2015).

    Article  Google Scholar 

  43. McLennan, D. A. & Shires, V. L. Correlation between the level of infection with Bunodera inconstans and Neoechinorhynchus rutili and behavioral intensity in female brook sticklebacks. J. Parasitol. 81, 675–682 (1995).

    Article  CAS  PubMed  Google Scholar 

  44. Simmons, L. W. Courtship role reversal in bush-crickets—another role for parasites. Behav. Ecol. 5, 259–266 (1994).

    Article  Google Scholar 

  45. Schatral, A. Diet influences male–female interactions in the bush-cricket Requena verticalis (Orthoptera, Tettigoniidae). J. Insect Behav. 6, 379–388 (1993).

    Article  Google Scholar 

  46. Serrano, J. M. & Penna, M. Sexual monomorphism in the advertisement calls of a neotropical frog. Biol. J. Linn. Soc. 123, 388–401 (2018).

    Article  Google Scholar 

  47. Yamane, T. & Yasuda, T. The effects of mating status and time since mating on female sex pheromone levels in the rice leaf bug, Trigonotylus caelestialium. Naturwissenschaften 101, 153–156 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Cohen, J. A power primer. Psychol. Bull. 112, 155–159 (1992).

    Article  CAS  PubMed  Google Scholar 

  49. Klein, S. L. Parasite manipulation of the proximate mechanisms that mediate social behavior in vertebrates. Physiol. Behav. 79, 441–449 (2003).

    Article  CAS  PubMed  Google Scholar 

  50. Poulin, R. in Advances in the Study of Behavior Vol. 41 (eds Mitani, J. et al.) 151–186 (Elsevier, 2010).

  51. Clancey, E. & Byers, J. A. The definition and measurement of individual condition in evolutionary studies. Ethology 120, 845–854 (2014).

    Article  Google Scholar 

  52. Wilgers, D. J. & Hebets, E. A. in Animal Signaling and Function: An Integrative Approach (eds Irschick, D. J. et al.) 229–252 (John Wiley & Sons, 2015).

  53. Řežucha, R. & Reichard, M. Strategic exploitation of fluctuating asymmetry in male Endler’s guppy courtship displays is modulated by social environment. J. Evol. Biol. 28, 356–367 (2015).

    Article  PubMed  Google Scholar 

  54. Oliveira, R. F., Taborsky, M. & Brockmann, H. J. Alternative Reproductive Tactics: An Integrative Approach (Cambridge Univ. Press, 2008).

  55. Gray, D. A. Female house crickets, Acheta domesticus, prefer the chirps of large males. Anim. Behav. 54, 1553–1562 (1997).

    Article  CAS  PubMed  Google Scholar 

  56. Lubanga, U., Peters, R. & Steinbauer, M. Substrate-borne vibrations of male psyllids vary with body size and age but females are indifferent. Anim. Behav. 120, 173–182 (2016).

    Article  Google Scholar 

  57. Ah‐King, M. & Gowaty, P. A. A conceptual review of mate choice: stochastic demography, within‐sex phenotypic plasticity, and individual flexibility. Ecol. Evol. 6, 4607–4642 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  58. Ouzzani, M., Hammady, H., Fedorowicz, Z. & Elmagarmid, A. Rayyan—a web and mobile app for systematic reviews. Syst. Rev. 5, 210 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  59. Adamo, S. A., Kovalko, I., Easy, R. H. & Stoltz, D. A viral aphrodisiac in the cricket Gryllus texensis. J. Exp. Biol. 217, 1970–1976 (2014).

    PubMed  Google Scholar 

  60. Aguilar, T. M., Maia, R., Santos, E. S. A. & Macedo, R. H. Parasite levels in blue-black grassquits correlate with male displays but not female mate preference. Behav. Ecol. 19, 292–301 (2008).

    Article  Google Scholar 

  61. Ahtiainen, J. J., Alataio, R. V., Mappes, J. & Vertainen, L. Fluctuating asymmetry and sexual performance in the drumming wolf spider Hygrolycosa rubrofasciata. Ann. Zool. Fenn. 40, 281–292 (2003).

    Google Scholar 

  62. Ahtiainen, J. J., Alatalo, R. V., Kortet, R. & Rantala, M. J. Immune function, dominance and mating success in drumming male wolf spiders Hygrolycosa rubrofasciata. Behav. Ecol. Sociobiol. 60, 826–832 (2006).

    Article  Google Scholar 

  63. Alonso, J. C., Magana, M., Martin, C. A. & Palacin, C. Sexual traits as quality indicators in lekking male great bustards. Ethology 116, 1084–1098 (2010).

    Article  Google Scholar 

  64. Alonso, J. C., Magana, M., Palacin, C. & Martin, C. A. Correlates of male mating success in great bustard leks: the effects of age, weight, and display effort. Behav. Ecol. Sociobiol. 64, 1589–1600 (2010).

    Article  Google Scholar 

  65. Amorim, M. C. P. & Almada, V. C. The outcome of male–male encounters affects subsequent sound production during courtship in the cichlid fish Oreochromis mossambicus. Anim. Behav. 69, 595–601 (2005).

    Article  Google Scholar 

  66. Amorim, M. C. P. & Neves, A. S. M. Acoustic signalling during courtship in the painted goby, Pomatoschistus pictus. J. Mar. Biol. Assoc. UK 87, 1017–1023 (2007).

    Article  Google Scholar 

  67. Amorim, M. C. P. et al. Painted gobies sing their quality out loud: acoustic rather than visual signals advertise male quality and contribute to mating success. Funct. Ecol. 27, 289–298 (2013).

    Article  Google Scholar 

  68. Amorim, M. C. P. et al. Lusitanian toadfish song reflects male quality. J. Exp. Biol. 213, 2997–3004 (2010).

    Article  PubMed  Google Scholar 

  69. Amundsen, T. & Forsgren, E. Male preference for colourful females affected by male size in a marine fish. Behav. Ecol. Sociobiol. 54, 55–64 (2003).

    Article  Google Scholar 

  70. An, D. & Waldman, B. Enhanced call effort in Japanese tree frogs infected by amphibian chytrid fungus. Biol. Lett. https://doi.org/10.1098/rsbl.2016.0018 (2016).

  71. Andersson, S. Costs of sexual advertising in the lekking Jackson’s Widowbird. Condor 96, 1–10 (1994).

    Article  Google Scholar 

  72. Andrade, M. C. B. & Mason, A. C. Male condition, female choice, and extreme variation in repeated mating in a scaly cricket, Ornebius aperta (Orthoptera: Gryllidae: Mogoplistinae). J. Insect Behav. 13, 483–497 (2000).

    Article  Google Scholar 

  73. Anichini, M., Frommolt, K. H. & Lehmann, G. U. C. To compete or not to compete: bushcricket song plasticity reveals male body condition and rival distance. Anim. Behav. 142, 59–68 (2018).

    Article  Google Scholar 

  74. Arak, A. Female mate selection in the natterjack toad: active choice or passive atraction? Behav. Ecol. Sociobiol. 22, 317–327 (1988).

    Article  Google Scholar 

  75. Arvidsson, B. L. & Neergaard, R. Mate choice in the willow warbler—a field experiment. Behav. Ecol. Sociobiol. 29, 225–229 (1991).

    Article  Google Scholar 

  76. Atagan, Y. & Forstmeier, W. Protein supplementation decreases courtship rate in the zebra finch. Anim. Behav. 83, 69–74 (2012).

    Article  Google Scholar 

  77. Backwell, P. R. Y., Jennions, M. D., Christy, J. H. & Schober, U. Pillar building in the fiddler-crab Uca beebei—evidence for a condition dependent ornament. Behav. Ecol. Sociobiol. 36, 185–192 (1995).

    Article  Google Scholar 

  78. Bakker, T. C. M. & Milinski, M. Sequential female choice and the previous male effect in sticklebacks. Behav. Ecol. Sociobiol. 29, 205–210 (1991).

    Article  Google Scholar 

  79. Becker, L. J. S., Aspbury, A. S. & Gabor, C. R. Body size dependent male sexual behavior in a natural population of sailfin mollies (Poecilia latipinna). Am. Midl. Nat. 167, 366–372 (2012).

    Article  Google Scholar 

  80. Bee, M. A. et al. Assessing acoustic signal variability and the potential for sexual selection and social recognition in boreal chorus frogs (Pseudacris maculata). Ethology 116, 564–576 (2010).

    Article  Google Scholar 

  81. Beeler, A. E., Rauter, C. M. & Moore, A. J. Pheromonally mediated mate attraction by males of the burying beetle Nicrophorus orbicollis: alternative calling tactics conditional on both intrinsic and extrinsic factors. Behav. Ecol. 10, 578–584 (1999).

    Article  Google Scholar 

  82. Bertram, S. M. & Bowen, M. Field cricket species differences in the temporal patterns of long-distance mate attraction signals. Ethology 112, 850–857 (2006).

    Article  Google Scholar 

  83. Bertram, S. M., Whattam, E. M., Visanuvimol, L., Bennett, R. & Lauzon, C. Phosphorus availability influences cricket mate attraction displays. Anim. Behav. 77, 525–530 (2009).

    Article  Google Scholar 

  84. Birkhead, T. R., Fletcher, F. & Pellatt, E. J. Sexual selection in the zebra finch Taeniopygia guttata: condition, sex traits and immune capacity. Behav. Ecol. Sociobiol. 44, 179–191 (1998).

    Article  Google Scholar 

  85. Biro, P. A., Fanson, K. V. & Santostefano, F. Stress-induced peak (but not resting) metabolism correlates with mating display intensity in male guppies. Ecol. Evol. 6, 6537–6545 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  86. Bolund, E., Martin, K., Kempenaers, B. & Forstmeier, W. Inbreeding depression of sexually selected traits and attractiveness in the zebra finch. Anim. Behav. 79, 947–955 (2010).

    Article  Google Scholar 

  87. Bolund, E., Schielzeth, H. & Forstmeier, W. No heightened condition dependence of zebra finch ornaments—a quantitative genetic approach. J. Evol. Biol. 23, 586–597 (2010).

    Article  CAS  PubMed  Google Scholar 

  88. Bosholn, M., Fecchio, A., Silveira, P., Braga, E. M. & Anciaes, M. Effects of avian malaria on male behaviour and female visitation in lekking blue-crowned manakins. J. Avian Biol. 47, 457–465 (2016).

    Article  Google Scholar 

  89. Brandt, L. S. E., Ludwar, B. C. & Greenfield, M. D. Co-occurrence of preference functions and acceptance thresholds in female choice: mate discrimination in the lesser wax moth. Ethology 111, 609–625 (2005).

    Article  Google Scholar 

  90. Briggs, V. S. Call trait variation in Morelett’s tree frog, Agalychnis moreletii, of Belize. Herpetologica 66, 241–249 (2010).

    Article  Google Scholar 

  91. Buchanan, K. L., Catchpole, C. K., Lewis, J. W. & Lodge, A. Song as an indicator of parasitism in the sedge warbler. Anim. Behav. 57, 307–314 (1999).

    Article  CAS  PubMed  Google Scholar 

  92. Buchinger, T. J. et al. Increased pheromone signaling by small male sea lamprey has distinct effects on female mate search and courtship. Behav. Ecol. Sociobiol. 71, 155 (2017).

  93. Callander, S., Jennions, M. D. & Backwell, P. R. Y. The effect of claw size and wave rate on female choice in a fiddler crab. J. Ethol. 30, 151–155 (2012).

    Article  Google Scholar 

  94. Candolin, U. & Salesto, T. Does competition allow male mate choosiness in threespine sticklebacks? Am. Nat. 173, 273–277 (2009).

    Article  PubMed  Google Scholar 

  95. Castellano, S., Rosso, A., Doglio, S. & Giacoma, C. Body size and calling variation in the green toad (Bufo viridis). J. Zool. 248, 83–90 (1999).

    Article  Google Scholar 

  96. Chiswell, R., Girard, M., Fricke, C. & Kasumovic, M. M. Prior mating success can affect allocation towards future sexual signaling in crickets. PeerJ 2, e657 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  97. Churchill, E. R., Dytham, C. & Thom, M. D. F. Differing effects of age and starvation on reproductive performance in Drosophila melanogaster. Sci. Rep. 9, 2167 (2019).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  98. Clark, D. C., DeBano, S. J. & Moore, A. J. The influence of environmental quality on sexual selection in Nauphoeta cinerea (Dictyoptera: Blaberidae). Behav. Ecol. 8, 46–53 (1997).

    Article  Google Scholar 

  99. Clark, D. C. & Moore, A. J. Social communication in the Madagascar hissing cockroach—features of male courtship hisses and a comparison of courtship and agonistic hisses. Behaviour 132, 401–417 (1995).

    Article  Google Scholar 

  100. Clayton, D. H. Mate choice in experimentally parasitized rock doves: lousy males lose. Am. Zool. 30, 251–262 (1990).

    Article  Google Scholar 

  101. Cobb, M., Connolly, K. & Burnet, B. The relationship between locomotor activity and courtship in the melanogaster species sub-group of Drosophila. Anim. Behav. 35, 705–713 (1987).

    Article  Google Scholar 

  102. Cordes, N. et al. Larval food composition affects courtship song and sperm expenditure in a lekking moth. Ecol. Entomol. 40, 34–41 (2015).

    Article  Google Scholar 

  103. Cornuau, J. H., Schmeller, D. S., Courtois, E. A., Jolly, T. & Loyau, A. It takes two to tango: relative influence of male and female identity and morphology on complex courtship display in a newt species. Ethology 121, 218–226 (2015).

    Article  Google Scholar 

  104. Costa, F. J. V. & Macedo, R. H. Coccidian oocyst parasitism in the blue-black grassquit: influence on secondary sex ornaments and body condition. Anim. Behav. 70, 1401–1409 (2005).

    Article  Google Scholar 

  105. Crocker-Buta, S. P. & Leary, C. J. Hormonal and social correlates of courtship signal quality and behaviour in male green treefrogs. Anim. Behav. 146, 13–22 (2018).

    Article  Google Scholar 

  106. da Rocha, S. M. C., Lima, A. P. & Kaefer, I. L. Territory size as a main driver of male-mating success in an Amazonian nurse frog (Allobates paleovarzensis, Dendrobatoidea). Acta Ethol. 21, 51–57 (2018).

    Article  Google Scholar 

  107. David, M., Auclair, Y., Dall, S. R. X. & Cezilly, F. Pairing context determines condition-dependence of song rate in a monogamous passerine bird. Proc. R. Soc. B 280, 20122177 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  108. Deb, R., Bhattacharya, M. & Balakrishnan, R. Females of a tree cricket prefer larger males but not the lower frequency male calls that indicate large body size. Anim. Behav. 84, 137–149 (2012).

    Article  Google Scholar 

  109. Devigili, A., Kelley, J. L., Pilastro, A. & Evans, J. P. Expression of pre- and postcopulatory traits under different dietary conditions in guppies. Behav. Ecol. 24, 740–749 (2013).

    Article  Google Scholar 

  110. Drayton, J. M., Hunt, J., Brooks, R. & Jennions, M. D. Sounds different: inbreeding depression in sexually selected traits in the cricket Teleogryllus commodus. J. Evol. Biol. 20, 1138–1147 (2007).

    Article  CAS  PubMed  Google Scholar 

  111. Drayton, J. M., Milner, R. N. C., Hunt, J. & Jennions, M. D. Inbreeding and advertisement calling in the cricket Teleogryllus commodus: laboratory and field experiments. Evolution 64, 3069–3083 (2010).

    PubMed  Google Scholar 

  112. Droney, D. C. Environmental influences on male courtship and implications for female choice in a lekking Hawaiian Drosophila. Anim. Behav. 51, 821–830 (1996).

    Article  Google Scholar 

  113. Droney, D. C. The influence of the nutritional content of the adult male diet on testis mass, body condition and courtship vigour in a Hawaiian Drosophila. Funct. Ecol. 12, 920–928 (1998).

    Article  Google Scholar 

  114. Duffield, K. R. et al. Age-dependent variation in the terminal investment threshold in male crickets. Evolution 72, 578–589 (2018).

    Article  PubMed  Google Scholar 

  115. Eastwood, L. & Burnet, B. Courtship latency in male Drosophila melanogaster. Behav. Genet. 7, 359–372 (1977).

    Article  CAS  PubMed  Google Scholar 

  116. Engqvist, L. & Sauer, K. P. Influence of nutrition on courtship and mating in the scorpionfly Panorpa cognata (Mecoptera, insecta). Ethology 109, 911–928 (2003).

    Article  Google Scholar 

  117. Forrest, T. G. et al. Mate choice in ground crickets (Gryllidae, Nemoiinae). Fla. Entomol. 74, 74–80 (1991).

    Article  Google Scholar 

  118. Galeotti, P. et al. Courtship displays and mounting calls are honest, condition-dependent signals that influence mounting success in Hermann’s tortoises. Can. J. Zool. 83, 1306–1313 (2005).

    Article  Google Scholar 

  119. Gibson, J. S. & Uetz, G. W. Effect of rearing environment and food availability on seismic signalling in male wolf spiders (Araneae: Lycosidae). Anim. Behav. 84, 85–92 (2012).

    Article  Google Scholar 

  120. Gibson, R. M. Relationships between blood parasites, mating success and phenotypic cues in male sage grouse Centrocercus urophasianus. Am. Zool. 30, 271–278 (1990).

    Article  Google Scholar 

  121. Gilbert, R., Karp, R. D. & Uetz, G. W. Effects of juvenile infection on adult immunity and secondary sexual characters in a wolf spider. Behav. Ecol. 27, 946–954 (2016).

    Article  Google Scholar 

  122. Gilbert, R. & Uetz, G. W. Courtship and male ornaments as honest indicators of immune function. Anim. Behav. 117, 97–103 (2016).

    Article  Google Scholar 

  123. Given, M. Interrelationships among calling effort, growth rate, and chorus tenure in Bufo fowleri. Copeia 2002, 979–987 (2002).

    Article  Google Scholar 

  124. Greenspan, S. E., Roznik, E. A., Schwarzkopf, L., Alford, R. A. & Pike, D. A. Robust calling performance in frogs infected by a deadly fungal pathogen. Ecol. Evol. 6, 5964–5972 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  125. Gumulka, M. & Rozenboim, I. Effect of the age of ganders on reproductive behavior and fertility in a competitive mating structure. Ann. Anim. Sci. 17, 733–746 (2017).

    Article  Google Scholar 

  126. Hankison, S. J. & Ptacek, M. B. Within and between species variation in male mating behaviors in the Mexican sailfin mollies Poecilia velifera and P. petenensis. Ethology 113, 802–812 (2007).

    Article  Google Scholar 

  127. Harrison, S. J., Thomson, I. R., Grant, C. M. & Bertram, S. M. Calling, courtship, and condition in the fall field cricket, Gryllus pennsylvanicus. PLoS ONE 8, e60356 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  128. Hausfater, G., Gerhardt, H. C. & Klump, G. M. Parasites and mate choice in gray treefrogs, Hyla versicolor. Am. Zool. 30, 299–311 (1990).

    Article  Google Scholar 

  129. Hay, D. E. & McPhail, J. D. Courtship behaviour of male threespine sticklebacks (Gasterosteus aculeatus) from old and new hybrid zones. Behaviour 137, 1047–1063 (2000).

    Article  Google Scholar 

  130. Head, M. L., Fox, R. J. & Barber, I. Environmental change mediates mate choice for an extended phenotype, but not for mate quality. Evolution 71, 135–144 (2017).

    Article  PubMed  Google Scholar 

  131. Hegde, S. N. & Krishna, M. S. Size-assortative mating in Drosophila malerkotliana. Anim. Behav. 54, 419–426 (1997).

    Article  CAS  PubMed  Google Scholar 

  132. Hegyi, G. et al. Nutritional correlates and mate acquisition role of multiple sexual traits in male collared flycatchers. Naturwissenschaften 97, 567–576 (2010).

    Article  CAS  PubMed  Google Scholar 

  133. Henderson, L. J., Brazeal, K. R. & Hahn, T. P. Plumage coloration and social context influence male investment in song. Biol. Lett. 14, 20180300 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  134. Hermann, C. M., Brudermann, V., Zimmermann, H., Vollmann, J. & Sefc, K. M. Female preferences for male traits and territory characteristics in the cichlid fish Tropheus moorii. Hydrobiologia 748, 61–74 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  135. Hoefler, C. D., Carlascio, A. L., Persons, M. H. & Rypstra, A. L. Male courtship repeatability and potential indirect genetic benefits in a wolf spider. Anim. Behav. 78, 183–188 (2009).

    Article  Google Scholar 

  136. Hoefler, C. D., Moore, J. A., Reynolds, K. T. & Rypstra, A. L. The effect of experience on male courtship and mating behaviors in a cellar spider. Am. Midl. Nat. 163, 255–268 (2010).

    Article  Google Scholar 

  137. Hoefler, C. D., Persons, M. H. & Rypstra, A. L. Evolutionarily costly courtship displays in a wolf spider: a test of viability indicator theory. Behav. Ecol. 19, 974–979 (2008).

    Article  Google Scholar 

  138. Hoileitner, M., Nechtelberger, H. & Hoi, H. Song rate as a signal for nest-site quality in blackcaps (Sylvia atricapilla). Behav. Ecol. Sociobiol. 37, 399–405 (1995).

    Article  Google Scholar 

  139. Holzer, B., Jacot, A. & Brinkhof, M. W. G. Condition-dependent signaling affects male sexual attractiveness in field crickets, Gryllus campestris. Behav. Ecol. 14, 353–359 (2003).

    Article  Google Scholar 

  140. Honarmand, M., Riebel, K. & Naguib, M. Nutrition and peer group composition in early adolescence: impacts on male song and female preference in zebra finches. Anim. Behav. 107, 147–158 (2015).

    Article  Google Scholar 

  141. Houde, A. E. & Torio, A. J. Effect of parasitic infection on male color pattern and female choice in guppies. Behav. Ecol. 3, 346–351 (1992).

    Article  Google Scholar 

  142. Howard, R. D. & Young, J. R. Individual variation in male vocal traits and female mating preferences in Bufo americanus. Anim. Behav. 55, 1165–1179 (1998).

    Article  CAS  PubMed  Google Scholar 

  143. Hughes, A. L. Male size, mating success, and mating strategy in the mosquitofish Gambusia affinis (Poeciliidae). Behav. Ecol. Sociobiol. 17, 271–278 (1985).

    Article  Google Scholar 

  144. Humfeld, S. C. Condition-dependent signaling and adoption of mating tactics in an amphibian with energetic displays. Behav. Ecol. 24, 859–870 (2013).

    Article  Google Scholar 

  145. Jacot, A., Scheuber, H. & Brinkhof, M. W. G. Costs of an induced immune response on sexual display and longevity in field crickets. Evolution 58, 2280–2286 (2004).

    PubMed  Google Scholar 

  146. Jacot, A., Scheuber, H., Holzer, B., Otti, O. & Brinkhof, M. W. G. Diel variation in a dynamic sexual display and its association with female mate-searching behaviour. Proc. R. Soc. B 275, 579–585 (2008).

    Article  PubMed  Google Scholar 

  147. Jennions, M. D. Tibial coloration, fluctuating asymmetry and female choice behaviour in the damselfly Platycypha caligata. Anim. Behav. 55, 1517–1528 (1998).

    Article  CAS  PubMed  Google Scholar 

  148. Jha, N. A. & Kumar, V. Protein-rich food does not affect singing behaviour and song quality in adult zebra finches, Taeniopygia guttata. Curr. Sci. 111, 1693–1696 (2016).

    Article  Google Scholar 

  149. Jiguet, F. & Bretagnolle, V. Sexy males and choosy females on exploded leks: correlates of male attractiveness in the Little Bustard. Behav. Process. 103, 246–255 (2014).

    Article  Google Scholar 

  150. Jones, K. M., Monaghan, P. & Nager, R. G. Male mate choice and female fecundity in zebra finches. Anim. Behav. 62, 1021–1026 (2001).

    Article  Google Scholar 

  151. Joshi, A. M., Narayan, E. J. & Gramapurohit, N. P. Interrelationship among steroid hormones, energetics and vocalisation in the Bombay night frog (Nyctibatrachus humayuni). Gen. Comp. Endocrinol. 246, 142–149 (2017).

    Article  CAS  PubMed  Google Scholar 

  152. Joyce, A. L., Bernal, J. S., Vinson, S. B. & Lomeli-Flores, R. Influence of adult size on mate choice in the solitary and gregarious parasitoids, Cotesia marginiventris and Cotesia flavipes. J. Insect Behav. 22, 12–28 (2009).

    Article  Google Scholar 

  153. Junca, F. A. et al. Advertisement call of species of the genus Frostius Cannatella 1986 (Anura: Bufonidae). Acta Herpetol. 7, 189–201 (2012).

    Google Scholar 

  154. Kaefer, I. L. & Lima, A. P. Sexual signals of the Amazonian frog Allobates paleovarzensis: geographic variation and stereotypy of acoustic traits. Behaviour 149, 15–33 (2012).

    Article  Google Scholar 

  155. Kahn, A. T., Dolstra, T., Jennions, M. D. & Backwell, P. R. Y. Strategic male courtship effort varies in concert with adaptive shifts in female mating preferences. Behav. Ecol. 24, 906–913 (2013).

    Article  Google Scholar 

  156. Karl, I., Heuskin, S. & Fischer, K. Dissecting the mechanisms underlying old male mating advantage in a butterfly. Behav. Ecol. Sociobiol. 67, 837–849 (2013).

    Article  Google Scholar 

  157. Kaspi, R., Taylor, P. W. & Yuval, B. Diet and size influence sexual advertisement and copulatory success of males in Mediterranean fruit fly leks. Ecol. Entomol. 25, 279–284 (2000).

    Article  Google Scholar 

  158. Kennedy, C. E. J., Endler, J. A., Poynton, S. L. & McMinn, H. Parasite load predicts mate choice in guppies. Behav. Ecol. Sociobiol. 21, 291–295 (1987).

    Article  Google Scholar 

  159. Ketola, T., Kortet, R. & Kotiaho, J. S. Endurance in exercise is associated with courtship call rate in decorated crickets, Gryllodes sigillatus. Evol. Ecol. Res. 11, 1131–1139 (2009).

    Google Scholar 

  160. Ketola, T. & Kotiaho, J. S. Inbreeding, energy use and sexual signaling. Evol. Ecol. 24, 761–772 (2010).

    Article  Google Scholar 

  161. Kim, T. W. & Choe, J. C. The effect of food availability on the semilunar courtship rhythm in the fiddler crab Uca lactea (de Haan) (Brachyura: Ocypodidae). Behav. Ecol. Sociobiol. 54, 210–217 (2003).

    Article  Google Scholar 

  162. Kim, T. W., Sakamoto, K., Henmi, Y. & Choe, J. C. To court or not to court: reproductive decisions by male fiddler crabs in response to fluctuating food availability. Behav. Ecol. Sociobiol. 62, 1139–1147 (2008).

    Article  Google Scholar 

  163. King, B. H., Saporito, K. B., Ellison, J. H. & Bratzke, R. M. Unattractiveness of mated females to males in the parasitoid wasp Spalangia endius. Behav. Ecol. Sociobiol. 57, 350–356 (2005).

    Article  Google Scholar 

  164. Kitsunezuka, K., Okutani-Akamatsu, Y., Watanabe, T. & Oku, K. Effects of male age on the mating behavior of both sexes in the sorghum plant bug, Stenotus rubrovittatus (Hemiptera: Miridae). Appl. Entomol. Zool. 48, 73–77 (2013).

    Article  Google Scholar 

  165. Knapp, R. A. Influence of energy reserves on the expression of a secondary sexual trait in male bicolor damselfish, Stegastes partitus. Bull. Mar. Sci. 57, 672–681 (1995).

    Google Scholar 

  166. Kodric-Brown, A. Dietary carotenoids and male mating success in the guppy: an environmental component to female choice. Behav. Ecol. Sociobiol. 25, 393–401 (1989).

    Article  Google Scholar 

  167. Kolluru, G. R., Bertram, S. M., China, E. H., Dunmeyer, C. V. & Graves, J. S. Mating behavior and its morphological correlates in two color morphs of Girardinus metallicus (Pisces: Poeciliidae), a species previously thought not to exhibit courtship display. Behav. Process. 106, 44–52 (2014).

    Article  Google Scholar 

  168. Kotiaho, J. S. Testing the assumptions of conditional handicap theory: costs and condition dependence of a sexually selected trait. Behav. Ecol. Sociobiol. 48, 188–194 (2000).

    Article  Google Scholar 

  169. Kotiaho, J. S. Sexual selection and condition dependence of courtship display in three species of horned dung beetles. Behav. Ecol. 13, 791–799 (2002).

    Article  Google Scholar 

  170. Kotiaho, J. S., Alatalo, R. V., Mappes, J. & Parri, S. Sexual signalling and viability in a wolf spider (Hygrolycosa rubrofasciata): measurements under laboratory and field conditions. Behav. Ecol. Sociobiol. 46, 123–128 (1999).

    Article  Google Scholar 

  171. Kotiaho, J. S., Simmons, L. W. & Tomkins, J. L. Towards a resolution of the lek paradox. Nature 410, 684–686 (2001).

    Article  CAS  PubMed  Google Scholar 

  172. Krishna, M. S. & Hegde, S. N. Influence of body size in mating success in three sympatric species of Drosophila. Ital. J. Zool. 70, 47–52 (2003).

    Article  Google Scholar 

  173. Kuczynski, M. C., Bello-DeOcampo, D. & Getty, T. No evidence of terminal investment in the gray treefrog (Hyla versicolor): older males do not signal at greater effort. Copeia 103, 530–535 (2015).

    Article  Google Scholar 

  174. Kuczynski, M. C., Storks, L., Gering, E. & Getty, T. Male treefrogs in low condition resume signaling faster following simulated predator attack. Behav. Ecol. Sociobiol. 70, 347–355 (2016).

    Article  Google Scholar 

  175. Kuriwada, T. Horn length is not correlated with calling efforts in the horn-headed cricket Loxoblemmus doenitzi (Orthoptera: Gryllidae). Entomol. Sci. 19, 228–232 (2016).

    Article  Google Scholar 

  176. Kuriwada, T. & Kasuya, E. Age-dependent changes in calling effort in the bell cricket Meloimorpha japonica. J. Ethol. 29, 99–105 (2011).

    Article  Google Scholar 

  177. Leary, C. J., Lippincott, J., Harris, S. & Hawkins, D. L. A test of the energetics-hormone vocalization model in the green treefrog. Gen. Comp. Endocrinol. 213, 32–39 (2015).

    Article  CAS  PubMed  Google Scholar 

  178. Lehtonen, T. K., Svensson, P. A. & Wong, B. B. M. The influence of recent social experience and physical environment on courtship and male aggression. BMC Evol. Biol. 16, 18 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  179. Lehtonen, T. K., Svensson, P. A. & Wong, B. B. M. Aggressive desert goby males also court more, independent of the physiological demands of salinity. Sci. Rep. 8, 9352 (2018).

  180. Lode, T. & Le Jacques, D. Influence of advertisement calls on reproductive success in the male midwife toad Alytes obstetricans. Behaviour 140, 885–898 (2003).

    Article  Google Scholar 

  181. Lomborg, J. P. & Toft, S. Nutritional enrichment increases courtship intensity and improves mating success in male spiders. Behav. Ecol. 20, 700–708 (2009).

    Article  Google Scholar 

  182. Lopez, P. T. & Narins, P. M. Mate choice in the neotropical frog, Eleutherodactylus coqui. Anim. Behav. 41, 757–772 (1991).

    Article  Google Scholar 

  183. Lynn, S. E., Stamplis, T. B., Barrington, W. T., Weida, N. & Hudak, C. A. Food, stress, and reproduction: short-term fasting alters endocrine physiology and reproductive behavior in the zebra finch. Horm. Behav. 58, 214–222 (2010).

    Article  CAS  PubMed  Google Scholar 

  184. Magellan, K., Pettersson, L. B. & Magurran, A. E. Quantifying male attractiveness and mating behaviour through phenotypic size manipulation in the Trinidadian guppy, Poecilia reticulata. Behav. Ecol. Sociobiol. 58, 366–374 (2005).

    Article  Google Scholar 

  185. Magoolagan, L., Mawby, P. J., Whitehead, F. A. & Sharp, S. P. The effect of early life conditions on song traits in male dippers (Cinclus cinclus). PLoS ONE 13, e0205101 (2018).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  186. Manica, L. T., Maia, R., Dias, A., Podos, J. & Macedoc, R. H. Vocal output predicts territory quality in a neotropical songbird. Behav. Process. 109, 21–26 (2014).

    Article  Google Scholar 

  187. Mariette, M., Kelley, J. L., Brooks, R. & Evans, J. P. The effects of inbreeding on male courtship behaviour and coloration in guppies. Ethology 112, 807–814 (2006).

    Article  Google Scholar 

  188. Mateos, C. & Carranza, J. Effects of male dominance and courtship display on female choice in the ring-necked pheasant. Behav. Ecol. Sociobiol. 45, 235–244 (1999).

    Article  Google Scholar 

  189. Matsuo, T. Effect of social condition on behavioral development during early adult phase in Drosophila prolongata. J. Ethol. 36, 15–22 (2018).

    Article  PubMed  Google Scholar 

  190. McAuley, E. M. & Bertram, S. M. Field crickets compensate for unattractive static long-distance call components by increasing dynamic signalling effort. PLoS ONE 11, e0167311 (2016).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  191. McCullough, E. L. & Simmons, L. W. Selection on male physical performance during male–male competition and female choice. Behav. Ecol. 27, 1288–1295 (2016).

    Article  Google Scholar 

  192. McLean, M. J., Bishop, P. J., Hero, J. M. & Nakagawa, S. Assessing the information content of calls of Litoria chloris: quality signalling versus individual recognition. Aust. J. Zool. 60, 120–126 (2012).

    Article  Google Scholar 

  193. McNeil, G. V., Friesen, C. N., Gray, S. M., Aldredge, A. & Chapman, L. J. Male colour variation in a eurytopic African cichlid: the role of diet and hypoxia. Biol. J. Linn. Soc. 118, 551–568 (2016).

    Article  Google Scholar 

  194. Memmott, R. & Briffa, M. Exaggerated displays do not improve mounting success in male seaweed flies Fucellia tergina (Diptera: Anthomyiidae). Behav. Process. 120, 73–79 (2015).

    Article  Google Scholar 

  195. Milazzo, M. et al. Ocean acidification affects fish spawning but not paternity at CO2 seeps. Proc. R. Soc. B 283, 20161021 (2016).

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  196. Morales, M. B., Alonso, J. C., Martin, C., Martin, E. & Alonso, J. Male sexual display and attractiveness in the great bustard Otis tarda: the role of body condition. J. Ethol. 21, 51–56 (2003).

    Article  Google Scholar 

  197. Morris, M. R. Female choice of large males in the treefrog Hyla ebraccata. J. Zool. 223, 371–378 (1991).

    Article  Google Scholar 

  198. Morris, M. R., Rios-Cardenas, O. & Darrah, A. Male mating tactics in the northern mountain swordtail fish (**phophorus nezahualcoyotl): coaxing and coercing females to mate. Ethology 114, 977–988 (2008).

    Article  Google Scholar 

  199. Muramatsu, D. The function of the four types of waving display in Uca lactea: effects of audience, sand structure, and body size. Ethology 117, 408–415 (2011).

    Article  Google Scholar 

  200. Murphy, C. G. Nightly timing of chorusing by male barking treefrogs (Hyla gratiosa): the influence of female arrival and energy. Copeia 1999, 333–347 (1999).

    Article  Google Scholar 

  201. Naguib, M., Heim, C. & Gil, D. Early developmental conditions and male attractiveness in zebra finches. Ethology 114, 255–261 (2008).

    Article  Google Scholar 

  202. O’Hanlon, J. C., Wignall, A. E. & Herberstein, M. E. Short and fast vs long and slow: age changes courtship in male orb-web spiders (Argiope keyserlingi). Sci. Nat. 105, 3 (2018).

    Article  CAS  Google Scholar 

  203. Ohata, M., Wada, K. & Koga, T. Waving display by male Scopimera globosa (Brachyura: Ocypodoidea) as courtship behavior. J. Crustac. Biol. 25, 637–639 (2005).

    Article  Google Scholar 

  204. Olsson, K. H., Kvarnemo, C. & Svensson, O. Relative costs of courtship behaviours in nest-building sand gobies. Anim. Behav. 77, 541–546 (2009).

    Article  Google Scholar 

  205. Ortiz-Santaliestra, M. E., Marco, A., Fernández-Benéitez, M. J. & Lizana, M. Alteration of courtship behavior because of water acidification and minor effect of ammonium nitrate in the Iberian newt (Lissotriton boscai). Environ. Toxicol. Chem. 28, 1500–1505 (2009).

    Article  CAS  PubMed  Google Scholar 

  206. Papadopoulos, N. T., Katsoyannos, B. I., Kouloussis, N. A., Economopoulos, A. P. & Carrey, J. R. Effect of adult age, food, and time of day on sexual calling incidence of wild and mass-reared Ceratitis capitata males. Entomol. Exp. Appl. 89, 175–182 (1998).

    Article  Google Scholar 

  207. Pariser, E. C., Mariette, M. M. & Griffith, S. C. Artificial ornaments manipulate intrinsic male quality in wild-caught zebra finches (Taeniopygia guttata). Behav. Ecol. 21, 264–269 (2010).

    Article  Google Scholar 

  208. Partridge, L., Ewing, A. & Chandler, A. Male size and mating success in Drosophila melanogaster: the roles of male and female behaviour. Anim. Behav. 35, 555–562 (1987).

    Article  Google Scholar 

  209. Passmore, N. I., Bishop, P. J. & Caithness, N. Calling behavior influences mating success in male painted reed frogs, Hyperolius marmoratus. Ethology 92, 227–241 (1992).

    Article  Google Scholar 

  210. Pedroso, S. S., Barber, I., Svensson, O., Fonseca, P. J. & Amorim, M. C. P. Courtship sounds advertise species identity and male quality in sympatric Pomatoschistus spp. gobies. PLoS ONE 8, e64620 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  211. Pelabon, C. et al. Do microsporidian parasites affect courtship in two-spotted gobies? Mar. Biol. 148, 189–196 (2005).

    Article  Google Scholar 

  212. Pellitteri-Rosa, D., Sacchi, R., Galeotti, P., Marchesi, M. & Fasola, M. Courtship displays are condition-dependent signals that reliably reflect male quality in Greek tortoises, Testudo graeca. Chelonian Conserv. Biol. 10, 10–17 (2011).

    Article  Google Scholar 

  213. Perezlachaud, G. & Campan, M. Influence of previous sexual experience and postemergence rearing conditions on the mating-behavior of Chryseida bennetti. Entomol. Exp. Appl. 76, 163–170 (1995).

    Article  Google Scholar 

  214. Poole, K. G. & Murphy, C. G. Preferences of female barking treefrogs, Hyla gratiosa, for larger males: univariate and composite tests. Anim. Behav. 73, 513–524 (2007).

    Article  Google Scholar 

  215. Prathibha, M., Krishna, M. S. & Jayaramu, S. C. Male age influence on male reproductive success in Drosophila ananassae (Diptera: Drosophilidae). Ital. J. Zool. 78, 168–173 (2011).

    Article  Google Scholar 

  216. Pruett-jones, S. G., Pruett-jones, M. A. & Jones, H. I. Parasites and sexual selection in birds of paradise. Am. Zool. 30, 287–298 (1990).

    Article  Google Scholar 

  217. Pryke, S. R. & Andersson, S. Experimental evidence for female choice and energetic costs of male tail elongation in red-collared widowbirds. Biol. J. Linn. Soc. 86, 35–43 (2005).

    Article  Google Scholar 

  218. Ptacek, M. B. & Travis, J. Inter-population variation in male mating behaviours in the sailfin mollie, Poecilia latipinna. Anim. Behav. 52, 59–71 (1996).

    Article  Google Scholar 

  219. Ptacek, M. B. & Travis, J. Mate choice in the sailfin molly, Poecilia latipinna. Evolution 51, 1217–1231 (1997).

    Article  PubMed  Google Scholar 

  220. Rahman, M. M., Kelley, J. L. & Evans, J. P. Condition-dependent expression of pre- and postcopulatory sexual traits in guppies. Ecol. Evol. 3, 2197–2213 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  221. Rahman, M. M., Turchini, G. M., Gasparini, C., Norambuena, F. & Evans, J. P. The expression of pre- and postcopulatory sexually selected traits reflects levels of dietary stress in guppies. PLoS ONE 9, e105856 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  222. Reifer, M. L., Harrison, S. J. & Bertram, S. M. How dietary protein and carbohydrate influence field cricket development, size and mate attraction signalling. Anim. Behav. 139, 137–146 (2018).

    Article  Google Scholar 

  223. Rezaei, A., Krishna, M. S. & Santhosh, H. T. Male age affects female mate preference, quantity of accessory gland proteins, and sperm traits and female fitness in D. melanogaster. Zool. Sci. 32, 16–24 (2015).

    Article  Google Scholar 

  224. Ritchie, M. G., Sunter, D. & Hockham, L. R. Behavioral components of sex role reversal in the tettigoniid bushcricket Ephippiger ephippiger. J. Insect Behav. 11, 481–491 (1998).

    Article  Google Scholar 

  225. Ritschard, M. & Brumm, H. Zebra finch song reflects current food availability. Evol. Ecol. 26, 801–812 (2012).

    Article  Google Scholar 

  226. Rodd, F. H. & Sokolowski, M. B. Complex origins of variation in the sexual-behavior of male Trinidadian guppies, Poecilia reticulata—interactions between social-environment, heredity, body-size and age. Anim. Behav. 49, 1139–1159 (1995).

    Article  Google Scholar 

  227. Rosenthal, M. F. & Hebets, E. A. Temporal patterns of nutrition dependence in secondary sexual traits and their varying impacts on male mating success. Anim. Behav. 103, 75–82 (2015).

    Article  Google Scholar 

  228. Sadowski, J. A., Grace, J. L. & Moore, A. J. Complex courtship behavior in the striped ground cricket, Allonemobius socius (Orthoptera: Gryllidae): does social environment affect male and female behavior? J. Insect Behav. 15, 69–84 (2002).

    Article  Google Scholar 

  229. Scheuber, H., Jacot, A. & Brinkhof, M. W. G. Condition dependence of a multicomponent sexual signal in the field cricket Gryllus campestris. Anim. Behav. 65, 721–727 (2003).

    Article  Google Scholar 

  230. Shakeel, M., He, X. Z., Martin, N. A., Hanan, A. & Wang, Q. Mating behaviour of the European leafminer Scaptomyza flava (Diptera: Drosophilidae). NZ Plant Prot. 63, 108–112 (2010).

    Google Scholar 

  231. Shelly, T. E., Edu, J. & Pahio, E. Female medflies mate selectively with young males but gain no apparent fitness benefits. J. Insect Behav. 24, 55–66 (2011).

    Article  Google Scholar 

  232. Shelly, T. E. & Kennelly, S. S. Starvation and the mating success of wild male Mediterranean fruit flies (Diptera: Tephritidae). J. Insect Behav. 16, 171–179 (2003).

    Article  Google Scholar 

  233. Shuker, D. et al. Mating behavior, sexual selection, and copulatory courtship in a promiscuous beetle. J. Insect Behav. 15, 617–631 (2002).

    Article  Google Scholar 

  234. Sikkel, P. C. Effects of nest quality on male courtship and female spawning-site choice in an algal-nesting damselfish. Bull. Mar. Sci. 57, 682–689 (1995).

    Google Scholar 

  235. Sisodia, S. & Singh, B. N. Size dependent sexual selection in Drosophila ananassae. Genetica 121, 207–217 (2004).

    Article  PubMed  Google Scholar 

  236. Smit, J. A. H., Loning, H., Ryan, M. J. & Halfwerk, W. Environmental constraints on size-dependent signaling affects mating and rival interactions. Behav. Ecol. 30, 724–732 (2019).

    Article  Google Scholar 

  237. Snekser, J. L., Leese, J., Ganim, A. & Itzkowitz, M. Caribbean damselfish with varying territory quality: correlated behaviors but not a syndrome. Behav. Ecol. 20, 124–130 (2009).

    Article  Google Scholar 

  238. Spencer, K. A., Buchanan, K. L., Goldsmith, A. R. & Catchpole, C. K. Song as an honest signal of developmental stress in the zebra finch (Taeniopygia guttata). Horm. Behav. 44, 132–139 (2003).

    Article  CAS  PubMed  Google Scholar 

  239. Spencer, K. A. et al. Developmental stress affects the attractiveness of male song and female choice in the zebra finch (Taeniopygia guttata). Behav. Ecol. Sociobiol. 58, 423–428 (2005).

    Article  Google Scholar 

  240. Sundin, J., Vossen, L. E., Nilsson-Sköld, H. & Jutfelt, F. No effect of elevated carbon dioxide on reproductive behaviors in the three-spined stickleback. Behav. Ecol. 28, 1482–1491 (2017).

    Article  Google Scholar 

  241. Suzaki, Y., Katsuki, M., Miyatake, T. & Okada, Y. Relationships among male sexually selected traits in the bean bug, Riptortus pedestris (Heteroptera: Alydidae). Entomol. Sci. 18, 278–282 (2015).

    Article  Google Scholar 

  242. Takeshita, F., Murai, M., Matsumasa, M. & Henmi, Y. Multimodal signaling in fiddler crab: waving to attract mates is condition-dependent but other sexual signals are not. Behav. Ecol. Sociobiol. 72, 140 (2018).

  243. Tarano, Z. Variation in male advertisement calls in the neotropical frog Physalaemus enesefae. Copeia 2001, 1064–1072 (2001).

    Article  Google Scholar 

  244. Taylor, M. I., Turner, G. F., Robinson, R. L. & Stauffer, J. R. Sexual selection, parasites and bower height skew in a bower-building cichlid fish. Anim. Behav. 56, 379–384 (1998).

    Article  CAS  PubMed  Google Scholar 

  245. Tejedo, M. Large male mating advantage in natterjack toads, Bufo calamita: sexual selection or energetic constraints? Anim. Behav. 44, 557–569 (1992).

    Article  Google Scholar 

  246. Tolle, A. E. & Wagner, W. E. Costly signals in a field cricket can indicate high- or low-quality direct benefits depending upon the environment. Evolution 65, 283–294 (2011).

    Article  PubMed  Google Scholar 

  247. Toth, C. A., Santure, A. W., Holwell, G. I., Pattemore, D. E. & Parsons, S. Courtship behaviour and display-site sharing appears conditional on body size in a lekking bat. Anim. Behav. 136, 13–19 (2018).

    Article  Google Scholar 

  248. Turiegano, E., Monedero, I., Pita, M., Torroja, L. & Canal, I. Effect of Drosophila melanogaster female size on male mating success. J. Insect Behav. 26, 89–100 (2013).

    Article  Google Scholar 

  249. Van Hout, A. J. M., Pinxten, R., Geens, A. & Eens, M. Non-breeding song rate reflects nutritional condition rather than body condition. PLoS ONE 7, e36547 (2012).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  250. Villarreal, A. E., Godin, J. G. J. & Bertram, S. M. Influence of the operational sex ratio on mutual mate choice in the Jamaican field cricket (Gryllus assimilis): testing the predictions of the switch point theorem. Ethology 124, 816–828 (2018).

    Article  Google Scholar 

  251. Wacker, S., de Jong, K., Forsgren, E. & Amundsen, T. Large males fight and court more across a range of social environments: an experiment on the two spotted goby Gobiusculus flavescens. J. Fish. Biol. 81, 21–34 (2012).

    Article  CAS  PubMed  Google Scholar 

  252. Wagner, W. E. & Hoback, W. W. Nutritional effects on male calling behaviour in the variable field cricket. Anim. Behav. 57, 89–95 (1999).

    Article  CAS  PubMed  Google Scholar 

  253. Walling, C. A., Stamper, C. E., Salisbury, C. L. & Moore, A. J. Experience does not alter alternative mating tactics in the burying beetle Nicrophorus vespilloides. Behav. Ecol. 20, 153–159 (2009).

    Article  Google Scholar 

  254. Watson, N. L. & Simmons, L. W. Mate choice in the dung beetle Onthophagus sagittarius: are female horns ornaments? Behav. Ecol. 21, 424–430 (2010).

    Article  Google Scholar 

  255. Whattam, E. M. & Bertram, S. M. Effects of juvenile and adult condition on long-distance call components in the Jamaican field cricket, Gryllus assimilis. Anim. Behav. 81, 135–144 (2011).

    Article  Google Scholar 

  256. Wilgers, D. J. & Hebets, E. A. Complex courtship displays facilitate male reproductive success and plasticity in signaling across variable environments. Curr. Zool. 57, 175–186 (2011).

    Article  Google Scholar 

  257. Wilgers, D. J. & Hebets, E. A. Age-related female mating decisions are condition dependent in wolf spiders. Behav. Ecol. Sociobiol. 66, 29–38 (2012).

    Article  Google Scholar 

  258. Wilson, A. D. M. et al. Behavioral correlations across activity, mating, exploration, aggression, and antipredator contexts in the European house cricket, Acheta domesticus. Behav. Ecol. Sociobiol. 64, 703–715 (2010).

    Article  Google Scholar 

  259. Win, A. T., Kojima, W. & Ishikawa, Y. Age-related male reproductive investment in courtship display and nuptial gifts in a moth, Ostrinia scapulalis. Ethology 119, 325–334 (2013).

    Article  Google Scholar 

  260. Woodhead, A. P. Male age: effect on mating behaviour and success in the cockroach Diploptera punctata. Anim. Behav. 34, 1874–1879 (1986).

    Article  Google Scholar 

  261. Yamada, K. & Soma, M. Diet and birdsong: short-term nutritional enrichment improves songs of adult Bengalese finch males. J. Avian Biol. 47, 865–870 (2016).

    Article  Google Scholar 

  262. Yuval, B., Kaspi, R., Shloush, S. & Warburg, M. S. Nutritional reserves regulate male participation in Mediterranean fruit fly leks. Ecol. Entomol. 23, 211–215 (1998).

    Article  Google Scholar 

  263. Zuk, M. et al. The role of male ornaments and courtship behavior in female mate choice of red jungle fowl. Am. Nat. 136, 459–473 (1990).

    Article  Google Scholar 

  264. Chargé, R., Saint Jalme, M., Lacroix, F., Cadet, A. & Sorci, G. Male health status, signalled by courtship display, reveals ejaculate quality and hatching success in a lekking species. J. Anim. Ecol. 79, 843–850 (2010).

    PubMed  Google Scholar 

  265. Lipsey, M. & Wilson, D. Practical Meta-analysis (Sage Publications, 2001).

  266. Hedges, L. V. & Olkin, I. Statistical Methods for Meta-analysis (Academic Press, 1985).

  267. Hinchliff, C. E. et al. Synthesis of phylogeny and taxonomy into a comprehensive tree of life. Proc. Natl Acad. Sci. USA 112, 12764–12769 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  268. R Core Team R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2020).

  269. Michonneau, F., Brown, J. W. & Winter, D. J. rotl: an R package to interact with the Open Tree of Life data. Methods Ecol. Evol. 7, 1476–1481 (2016).

    Article  Google Scholar 

  270. Paradis, E., Claude, J. & Strimmer, K. APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20, 289–290 (2004).

    Article  CAS  PubMed  Google Scholar 

  271. Grafen, A. The phylogenetic regression. Philos. Trans. R. Soc. Lond. B 326, 119–157 (1989).

    Article  CAS  Google Scholar 

  272. Tacutu, R. et al. Human Ageing Genomic Resources: integrated databases and tools for the biology and genetics of ageing. Nucleic Acids Res. 41, D1027–D1033 (2012).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  273. Carey, J. & Judge, D. Longevity Records: Life Spans of Mammals, Birds, Amphibians, Reptiles, and Fish (Odense Univ. Press, 2000).

  274. Höglund, J. & Alatalo, R. V. Leks (Princeton Univ. Press, 2005).

  275. Viechtbauer, W. Conducting meta-analyses in R with the metafor package. J. Stat. Softw. 36, 1–48 (2010).

    Article  Google Scholar 

  276. Noble, D. W., Lagisz, M., O’dea, R. E. & Nakagawa, S. Nonindependence and sensitivity analyses in ecological and evolutionary meta‐analyses. Mol. Ecol. 26, 2410–2425 (2017).

    Article  PubMed  Google Scholar 

  277. Borenstein, M., Hedges, L. V., Higgins, J. P. & Rothstein, H. Introduction to Meta-analysis (John Wiley, 2009).

  278. Higgins, J., Thompson, S. G., Deeks, J. J. & Altman, D. G. Measuring inconsistency in meta-analyses. Br. Med. J. 327, 557–560 (2003).

    Article  Google Scholar 

  279. Nakagawa, S. & Santos, E. S. Methodological issues and advances in biological meta-analysis. Evol. Ecol. 26, 1253–1274 (2012).

    Article  Google Scholar 

  280. Hothorn, T., Bretz, F. & Westfall, P. Simultaneous inference in general parametric models. Biom. J. 50, 346–363 (2008).

    Article  PubMed  Google Scholar 

  281. Nakagawa, S. & Schielzeth, H. A general and simple method for obtaining R2 from generalized linear mixed‐effects models. Methods Ecol. Evol. 4, 133–142 (2013).

    Article  Google Scholar 

  282. Duval, S. & Tweedie, R. Trim and fill: a simple funnel-plot–based method of testing and adjusting for publication bias in meta-analysis. Biometrics 56, 455–463 (2000).

    Article  CAS  PubMed  Google Scholar 

  283. Egger, M., Smith, G. D., Schneider, M. & Minder, C. Bias in meta-analysis detected by a simple, graphical test. Br. Med. J. 315, 629–634 (1997).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

I thank T. Price, Z. Lewis and L. Simmons for helpful comments on an earlier version of the manuscript. This work was funded by a Leverhulme Trust Early-Career Fellowship (grant no. ECF-2018-427).

Author information

Authors and Affiliations

  1. Department of Evolution, Ecology and Behaviour, University of Liverpool, Liverpool, UK

    Liam R. Dougherty

Authors
  1. Liam R. Dougherty
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Liam R. Dougherty.

Ethics declarations

Competing interests

The author declares no competing interests.

Additional information

Peer review information Nature Ecology & Evolution thanks the anonymous reviewers for their contribution to the peer review of this work. Peer reviewer reports are available.

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Extended data

Extended Data Fig. 1 Effect size heterogeneity (I2) when each of the six state factors are considered separately.

I2 values are presented for the overall model, as well as for each random factor in a multilevel mixed-effects meta-analysis model. k= the number of effect sizes for each dataset.

Extended Data Fig. 2 Mean effect size estimates (the correlation coefficient r), plus sample sizes, for each category for the seven categorical moderator variables.

Estimates were obtained using a minus-intercept meta-regression, performed separately for each moderator (see text for details).

Extended Data Fig. 3 Results from meta-regressions performed separately on just body size or condition data.

Each factor was tested using a separate meta-regression model. The QM statistic tests whether the moderator variable significantly influences the mean effect size. Marginal R2 is the amount of variance explained by each fixed factor. All models were run on the full dataset (k = 203 for body size, 178 for condition) with the exception of lifespan (k = 146 for body size, 136 for condition). Significant moderators are highlighted in grey.

Extended Data Fig. 4 Forest plot showing the effect of signalling type on the relationship between sexual signalling and body size (k = 203).

Black circles show the mean effect size estimate (correlation coefficient r) for each signalling category, bars show the 95% confidence intervals. Open circles show the raw effect sizes for each category, with the size of the circle corresponding to study precision (inverse standard error)). k= the number of effect sizes for each category.

Extended Data Fig. 5 Relationship between effect size (Z-transformed correlation coefficient, Zr) and study year.

Each bubble represents an effect size, and bubble size is scaled to effect size precision (inverse standard error; larger bubbles reflect larger sample sizes) for the full dataset (k = 520). The dashed line shows the predicted line from a meta-regression including study year as a covariate. Dotted lines show the 95% confidence intervals for the predicted line.

Extended Data Fig. 6 Results from meta-regression models testing the effect of study year separately for each of the six state factor categories.

Each model included study year as a fixed effect and phylogeny, species, study, experiment and observation ID as random effects.

Extended Data Fig. 7 Scatterplot showing the relationship between effect size (Z-transformed correlation coefficient, Zr) and precision (inverse standard error) for the full dataset (k = 520).

The line shows the prediction from a linear regression.

Extended Data Fig. 8 The phylogenetic tree used in the analysis (N = 147 species).

The taxonomic class categories used during meta-regressions are highlighted on the right-hand side of the tree.

Extended Data Fig. 9 PRISMA diagram showing the literature search and screening process.

Note that the search terms included a broader range of behaviours than presented in this study.

Supplementary information

Supplementary Information

Supplementary Methods, Note, Table 1, references and PRISMA checklist.

Reporting Summary

Peer Review Information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Dougherty, L.R. Meta-analysis reveals that animal sexual signalling behaviour is honest and resource based. Nat Ecol Evol 5, 688–699 (2021). https://doi.org/10.1038/s41559-021-01409-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41559-021-01409-z

  • Springer Nature Limited

Search

Navigation