Behavioral Ecology and Sociobiology

, Volume 67, Issue 9, pp 1483–1498 | Cite as

The dominance of seismic signaling and selection for signal complexity in Schizocosa multimodal courtship displays

  • Eileen A. Hebets
  • Cor J. Vink
  • Laura Sullivan-Beckers
  • Malcolm F. Rosenthal
Original Paper

Abstract

Schizocosa wolf spiders show tremendous diversity in courtship complexity, with different species employing varying numbers of components within and across sensory modalities. Using a comparative approach, we investigate the importance of each signaling modality in the courtship display of five Schizocosa species (three stridulating and two drumming) by assessing mating success under manipulated signaling environments. Irrespective of the degree of male ornamentation, the three stridulating species exhibit a dependence on the seismic, but not visual, signaling environment for mating success. Mating was independent of signaling environment for the two drumming species. We next ask whether the degree to which each species depends upon a signaling modality for mating (i.e., modality importance) is correlated with the estimated modality-specific signal complexity. We first calculate effect sizes for the influence of seismic versus visual signaling environments on the likelihood to mate for ten Schizocosa species and then use an element-counting approach to calculate seismic and visual signal complexity scores. We use a phylogenetic regression analysis to test two predictions: (1) the importance of seismic signaling is correlated with seismic signal complexity and (2) the importance of visual signaling is correlated with visual signal complexity. We find a significant relationship between visual signal importance and visual signal complexity, but no relationship between seismic signal importance and seismic signal complexity. Finally, we test the hypothesis that selection acts on complexity per se by determining whether seismic and visual signal complexity is correlated across species. We find support for this hypothesis in a significant relationship between seismic and visual signal complexity.

Keywords

Communication Female choice Repertoire size Sexual selection Signal efficacy Diversification 

Supplementary material

265_2013_1519_MOESM1_ESM.ppt (358 kb)
ESM 1(PPT 357 kb)
265_2013_1519_MOESM2_ESM.docx (16 kb)
ESM 2(DOCX 16 kb)
265_2013_1519_Fig4_ESM.jpg (61 kb)
Fig. 1

Bayesian consensus tree based on cytochrome c oxidase subunit 1 (COI) sequence data. Values on branches are posterior probabilities. Branch lengths are proportional to the expected number of substitutions per site (see scale bar). (JPEG 61 kb)

265_2013_1519_MOESM3_ESM.tif (516 kb)
High-resolution image (TIFF 516 kb)

References

  1. Basolo AL (1990) Female preference predates the evolution of the sword in swordtail fish. Science 250(4982):808–810PubMedCrossRefGoogle Scholar
  2. Beckers OM, Wagner WE (2011) Mate sampling strategy in a field cricket: evidence for a fixed threshold strategy with last chance option. Anim Behav 81(3):519–527. doi:10.1016/j.anbehav.2010.11.022 CrossRefGoogle Scholar
  3. Bell PD (1980) Transmission of vibrations along plant stems: implications for insect communication. J N Y Entomol Soc 88:210–216Google Scholar
  4. Bern MD (2011) Exploring sources of selection on the multimodal courtship displays of two sister species of wolf spiders: Schizocosa crassipalpata and Schizocosa bilineata. University of Nebraska, LincolnGoogle Scholar
  5. Blomberg SP, Garland T, Ives AR (2003) Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57(4):717–745. doi:10.1111/j.0014-3820.2003.tb00285.x PubMedGoogle Scholar
  6. Botero CA, Mudge AE, Koltz AM, Hochachka WM, Vehrencamp SL (2008) How reliable are the methods for estimating repertoire size? Ethology 114(12):1227–1238. doi:10.1111/j.1439-0310.2008.01576.x PubMedCrossRefGoogle Scholar
  7. Boughman JW (2002) How sensory drive can promote speciation. Trends Ecol Evol 17(12):571–577CrossRefGoogle Scholar
  8. Brandley MC, Schmitz A, Reeder TW (2005) Partitioned Bayesian analyses, partition choice, and the phylogenetic relationships of scincid lizards. Syst Biol 54:373–390PubMedCrossRefGoogle Scholar
  9. Byers J, Hebets E, Podos J (2010) Female mate choice based upon male motor performance. Anim Behav 79:771–778CrossRefGoogle Scholar
  10. Candolin U (2003) The use of multiple cues in mate choice. Biol Rev 78(4):575–595PubMedCrossRefGoogle Scholar
  11. Chang J, Song D, Zhou K (2007) Incongruous nuclear and mitochondrial phylogeographic patterns in two sympatric lineages of the wolf spider Pardosa astrigera (Araneae; Lycosidae) from China. Mol Phylogenet Evol 42:104–121PubMedCrossRefGoogle Scholar
  12. Chen I, Stuart-Fox DM, Hugall AF, Symonds MRE (2012) Sexual selection and the evolution of complex color patterns in dragon lizards. Evolution 66:3605–3614PubMedCrossRefGoogle Scholar
  13. Cocroft RB, Rodriguez RL (2005) The behavioral ecology of insect vibrational communication. Bioscience 55(4):323–334. doi:10.1641/0006-3568(2005)055[0323:tbeoiv]2.0.co;2 CrossRefGoogle Scholar
  14. Darwin C (1871) The descent of man, and selection in relation to sex. J. Murray, LondonCrossRefGoogle Scholar
  15. Dondale CD, Redner JH (1978) Revision of nearctic wolf spider genus Schizocosa (Arachneida Lycosidae). Can Entomol 110(2):143–181CrossRefGoogle Scholar
  16. Douglas SB, Mennill DJ (2010) A review of acoustic playback techniques for studying avian vocal duets. J Field Ornithol 81(2):115–129. doi:10.1111/j.1557-9263.2010.00268.x CrossRefGoogle Scholar
  17. Elias DO, Mason AC, Hoy RR (2004) The effect of substrate on the efficacy of seismic courtship signal transmission in the jumping spider Habronattus dossenus (Araneae: Salticidae). J Exp Biol 207(23):4105–4110PubMedCrossRefGoogle Scholar
  18. Elias DO, Land BR, Mason AC, Hoy RR (2006a) Measuring and quantifying dynamic visual signals in jumping spiders. Comp Physiol A Neuroethol Sens Neural Behav Physiol 192(8):785–797. doi:10.1007/s00359-006-0116-7 CrossRefGoogle Scholar
  19. Elias DO, Lee N, Hebets EA, Mason AC (2006b) Seismic signal production in a wolf spider: parallel versus serial multi-component signals. J Exp Biol 209(6):1074–1084. doi:10.1242/jeb.02104 PubMedCrossRefGoogle Scholar
  20. Elias DO, Mason AC, Hebets EA (2010) A signal-substrate match in the substrate-borne component of a multimodal courtship display. Curr Zool 56(3):370–378Google Scholar
  21. Elias DO, Maddison WP, Peckmezian C, Girard MB, Mason AC (2012) Orchestrating the score: complex multimodal courtship in the Habronattus coecatus group of Habronattus jumping spiders (Araneae: Slaticidae). Biol J Linnean Soc 105:522–547CrossRefGoogle Scholar
  22. Endler JA (1992) Signals, signal conditions, and the direction of evolution. Am Nat 139:S125–S153CrossRefGoogle Scholar
  23. Endler JA, Basolo AL (1998) Sensory ecology, receiver biases and sexual selection. Trends Ecol Evol 13(10):415–420PubMedCrossRefGoogle Scholar
  24. Felsenstein J (1981) Evolutionary trees from DNA sequences: a miximum likelihood approach. J Mol Evol 17:368–376PubMedCrossRefGoogle Scholar
  25. Fowler-Finn KD (2009) Exploring the maintenance of and selection on two distinct male morphs in a Schizocosa wolf spider. University of Nebraska, LincolnGoogle Scholar
  26. Framenau VW, Hebets EA (2007) A review of leg ornamentation in male wolf spiders, with the description of a new species from Australia, Artoria schizocoides (Araneae, Lycosidae). J Arachnol 35(1):89–101CrossRefGoogle Scholar
  27. Gerhardt HC (1982) Sound pattern-recognition in some North-American treefrogs (Anura, Hylidae)—implications for mate choice. Am Zool 22(3):581–595Google Scholar
  28. Gerhardt HC, Huber F (2002) Acoustic communication in insects and anurans. University of Chicago Press, ChicagoGoogle Scholar
  29. Gibson JS, Uetz GW (2008) Seismic communication and mate choice in wolf spiders: components of male seismic signals and mating success. Anim Behav 75:1253–1262CrossRefGoogle Scholar
  30. Gibson JS, Uetz GW (2012) Effect of rearing environment and food availability on seismic signalling in male wolf spiders (Araneae: Lycosidae). Anim Behav 84(1):85–92. doi:10.1016/j.anbehav.2012.04.010 CrossRefGoogle Scholar
  31. Gordon SD, Uetz GW (2011) Multimodal communication of wolf spiders on different substrates: evidence for behavioural plasticity. Anim Behav 81:367–375CrossRefGoogle Scholar
  32. Grant PR, Grant BR (1997) Genetics and the origin of bird species. Proc Natl Acad Sci U S A 94(15):7768–7775. doi:10.1073/pnas.94.15.7768 PubMedCrossRefGoogle Scholar
  33. Hasegawa M, Kishino K, Yano T (1985) Dating the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 22:160–174PubMedCrossRefGoogle Scholar
  34. 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 U S A 100(23):13390–13395PubMedCrossRefGoogle Scholar
  35. Hebets EA (2005) Attention-altering signal interactions in the multimodal courtship display of the wolf spider Schizocosa uetzi. Behav Ecol 16(1):75–82. doi:10.1093/beheco/arh133 CrossRefGoogle Scholar
  36. Hebets EA (2007) Subadult female experience does not influence species recognition in the wolf spider Schizocosa uetzi Stratton 1997. J Arachnol 35(1):1–10CrossRefGoogle Scholar
  37. Hebets EA (2008) Seismic signal dominance in the multimodal courtship display of the wolf spider Schizocosa stridulans Stratton 1991. Behav Ecol 19(6):1250–1257PubMedCrossRefGoogle Scholar
  38. Hebets EA (2011) Current status and future directions of research in complex signaling. Current Zoology 57:i–vGoogle Scholar
  39. Hebets EA, Papaj DR (2005) Complex signal function: developing a framework of testable hypotheses. Behav Ecol Sociobiol 57(3):197–214CrossRefGoogle Scholar
  40. 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 57:865–872PubMedCrossRefGoogle Scholar
  41. 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(4):280–286CrossRefGoogle Scholar
  42. Hebets EA, Vink CJ (2007) Experience leads to preference: experienced females prefer brush-legged males in a population of syntopic wolf spiders. Behav Ecol 18:1010–1020CrossRefGoogle Scholar
  43. Hebets EA, Stratton GE, Miller GL (1996) Habitat and courtship behavior of the wolf spider Schizocosa retrorsa (Banks) (Araneae, Lycosidae). J Arachnol 24(2):141–147Google Scholar
  44. Hebets EA, Elias DO, Mason AC, Miller GL, Stratton GE (2008a) Substrate-dependent signalling success in the wolf spider, Schizocosa retrorsa. Anim Behav 75:605–615CrossRefGoogle Scholar
  45. Hebets EA, Wesson J, Shamble PS (2008b) Diet influences mate choice selectivity in adult female wolf spiders. Anim Behav 76:355–363CrossRefGoogle Scholar
  46. Hebets EA, Stafstrom JA, Rodriguez RL, Wilgers DJ (2011) Enigmatic ornamentation eases male reliance on courtship performance for mating success. Anim Behav 81:963–972CrossRefGoogle Scholar
  47. Johnstone RA (1996) Multiple displays in animal communication: ‘backup signals’ and ‘multiple messages’. Philos Trans R Soc Lond Ser B-Biol Sci 351(1337):329–338CrossRefGoogle Scholar
  48. Kembel S, Cowan P, Helmus M, Cornwell W, Morlon H, Ackerly D, Blomberg S, Webb C (2010) Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26:1463–1464PubMedCrossRefGoogle Scholar
  49. Kraaijeveld K, Kraaijeveld-Smit FJL, Maan ME (2011) Sexual selection and speciation: the comparative evidence revisited. Biol Rev 86(2):367–377. doi:10.1111/j.1469-185X.2010.00150.x PubMedCrossRefGoogle Scholar
  50. 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
  51. Miller GL, Stratton GE, Miller PR, Hebets E (1998) Geographical variation in male courtship behaviour and sexual isolation in wolf spiders of the genus Schizocosa. Anim Behav 56:937–951PubMedCrossRefGoogle Scholar
  52. Møller AP, Pomiankowski A (1993) Why have birds got multiple sexual ornaments. Behav Ecol Sociobiol 32(3):167–176CrossRefGoogle Scholar
  53. Nakagawa S, Cuthill IC (2007) Effect size, confidence interval and statistical significance: a practical guide for biologists. Biol Rev 82(4):591–605. doi:10.1111/j.1469-185X.2007.00027.x PubMedCrossRefGoogle Scholar
  54. Nylander JAA (2008) MrModeltest 2.3. In. Department of Systematic Zoology, Uppsala University, UppsalaGoogle Scholar
  55. Page R (1996) TREEVIEW: an application to display phylogenetic trees on personal computers. Comp Appl Biol Sci 12:357–358Google Scholar
  56. Paradis E, Claude J, Strimmer K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289–290PubMedCrossRefGoogle Scholar
  57. Partan S, Marler P (1999) Behavior—communication goes multimodal. Science 283(5406):1272–1273PubMedCrossRefGoogle Scholar
  58. Persons MH, Uetz GW (2005) Sexual cannibalism and mate choice decisions in wolf spiders: influence of male size and secondary sexual characters. Anim Behav 69:83–94CrossRefGoogle Scholar
  59. Posada D, Buckley TR (2004) Model selection and model averaging in phylogenetics: advantages of Akaike information criterion and Bayesian approaches over likelihood ratio tests. Syst Biol 53:793–808PubMedCrossRefGoogle Scholar
  60. Rambaut A, Drummond AJ (2009) Tracerv1.5. In, 1.5 ednGoogle Scholar
  61. Ritchie MG (2007) Sexual selection and speciation. Annu Rev Ecol Evol Syst 38:79–102CrossRefGoogle Scholar
  62. Rodriguez RL, Boughman JW, Gray DA, Hebets EA, Hobel G, Symes LB (2013) Diversification under sexual selection: the relative importance of preference divergence versus preference strength (in review)Google Scholar
  63. Rodriguez RL, Ramaswamy K, Cocroft RB (2006) Evidence that female preferences have shaped male signal evolution in a clade of specialized plant-feeding insects. P Roy Soc B-Biol Sci 273(1601):2585–2593. doi:10.1098/rspb.2006.3635 CrossRefGoogle Scholar
  64. Ronquist F, Huelsenbeck JP (2003) MrBayes3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574PubMedCrossRefGoogle Scholar
  65. Rosenthal M, Hebets E (2012) Resource heterogeneity interacts with courtship rate to influence mating success in the wolf spier S. floridana. Anim Behav 84:1341–1346CrossRefGoogle Scholar
  66. Rowe C (1999) Receiver psychology and the evolution of multicomponent signals. Anim Behav 58:921–931PubMedCrossRefGoogle Scholar
  67. Rundus AS, Santer RD, Hebets EA (2010) Multimodal courtship efficacy of Schizocosa retrorsa wolf spiders: implications of an additional signal modality. Behav Ecol 21(4):701–707. doi:10.1093/beheco/arq042 CrossRefGoogle Scholar
  68. Rundus AS, Sullivan-Beckers L, Wilgers DJ, Hebets EA (2011) Females are choosier in the dark: environment-dependent reliance on courtship components and its impact on fitness. Evolution 65(1):268–282. doi:10.1111/j.1558-5646.2010.01125.x PubMedCrossRefGoogle Scholar
  69. 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(1):17–23CrossRefGoogle Scholar
  70. Servedio MR (2012) The relationship between sexual selection and speciation. Curr Zool 58(3):413–415Google Scholar
  71. Shamble PS, Wilgers DJ, Swoboda KA, Hebets EA (2009) Courtship effort is a better predictor of mating success than ornamentation for male wolf spiders. Behav Ecol 20(6):1242–1251. doi:10.1093/beheco/arp116 CrossRefGoogle Scholar
  72. Shaw KL, Parsons YM (2002) Divergence of mate recognition behavior and its consequences for genetic architectures of speciation. Am Nat 159:S61–S75. doi:10.1086/338373 PubMedCrossRefGoogle Scholar
  73. Stafstrom JA, Hebets EA (2013) Female mate choice for multimodal courtship and the importance of the signaling background for selection on male ornamentation. Current Zoology 59(2):200–209Google Scholar
  74. Stratton GE (1991) A new species of wolf spider, Schizocosa stridulans (Araneae, Lycosidae). J Arachnol 19(1):29–39Google Scholar
  75. Stratton GE (1997) A new species of Schizocosa from the southeastern USA (Araneae, Lycosidae). J Arachnol 25(1):84–92Google Scholar
  76. Stratton GE (2005) Evolution of ornamentation and courtship behavior in Schizocosa: insights from a phylogeny based on morphology (Araneae, Lycosidae). J Arachnol 33:347–376CrossRefGoogle Scholar
  77. Stratton GE, Uetz GW (1981) Acoustic communication and reproductive isolation in 2 species of wolf spiders. Science 214(4520):575–577CrossRefGoogle Scholar
  78. Stratton GE, Uetz GW (1983) Communication via substratum-coupled stridulation and reproductive isolation in wolf spiders (Araneae, Lycosidae). Anim Behav 31(FEB):164–172CrossRefGoogle Scholar
  79. Sullivan-Beckers L, Hebets EA (2011) Modality-specific experience with female feedback increases the efficacy of courtship signalling in male wolf spiders. Anim Behav 82(5):1051–1057. doi:10.1016/j.anbehav.2011.07.040 CrossRefGoogle Scholar
  80. Swofford DL (2002) PAUP*: phylogenetic analysis using parsimony (*and other methods). In, 4.0b10 edn. Sinauer Associates, SunderlandGoogle Scholar
  81. Taylor PW, Roberts JA, Uetz GW (2005) Flexibility in the multi-modal courtship of a wolf spider, Schizocosa ocreata. J Ethol 23(1):71–75CrossRefGoogle Scholar
  82. Taylor PW, Roberts JA, Uetz GW (2006) Mating in the absence of visual cues by Schizocosa ocreata (Hentz 1844) wolf spiders (Araneae, Lycosidae). J Arachnol 34(3):501–505CrossRefGoogle Scholar
  83. Tietjen WJ (1979) Is the sex pheromone of Lycosa rabida (Araneae, Lycosidae) deposited on a substratum? J Arachnol 6:207–212Google Scholar
  84. Tobias JA, Aben J, Brumfield RT, Derryberry EP, Halfwerk W, Slabbekoorn H, Seddon N (2010) Song divergence by sensory drive in Amazonian birds. Evolution 64(10):2820–2839. doi:10.1111/j.1558-5646.2010.01067.x PubMedGoogle Scholar
  85. Uetz GW, Dondale CD (1979) New wolf spider in the genus Schizocosa (Araneae, Lycosidae) from Illinois. J Arachnol 7(1):86–88Google Scholar
  86. Uetz GW, Norton S (2007) Preference for male traits in female wolf spiders varies with the choice of available males, female age, and reproductive state. Behav Ecol Sociobiol 61:631–641CrossRefGoogle Scholar
  87. Uetz GW, Roberts JA (2002) Multisensory cues and multimodal communication in spiders: insights from video/audio playback studies. Brain Behav Evol 59(4):222–230PubMedCrossRefGoogle Scholar
  88. Uetz GW, Papke R, Kilinc B (2002) Influence of feeding regime on body size, body condition and a male secondary sexual character in Schizocosa ocreata wolf spiders (Araneae, Lycosidae): condition-dependence in a visual signaling trait. J Arachnol 30(3):461–469CrossRefGoogle Scholar
  89. Uetz GW, Roberts JA, Taylor PW (2009) Multimodal communication and mate choice in wolf spiders: female response to multimodal versus unimodal signals. Anim Behav 78(2):299–305. doi:10.1016/j.anbehav.2009.04.023 CrossRefGoogle Scholar
  90. Uy A, Safran RD (2013) Variation in the temporal and spatial use of signals and its implications for multimodal communication. Behav Ecol Sociobiol. doi:10.1007/s00265-013-1492-y
  91. Vaccaro R, Uetz GW, Roberts JA (2010) Courtship and mating behavior of the wolf spider Schizocosa bilineata (Araneae: Lycosidae). J Arachnol 38:452–459CrossRefGoogle Scholar
  92. Vink CJ, Paterson AM (2003) Combined molecular and morphological phylogenetic analyses of the New Zealand wolf spider genus Anoteropsis (Araneae: Lycosidae). Mol Phylogenet Evol 28:576–587PubMedCrossRefGoogle Scholar
  93. Vink CJ, Thomas SM, Paquin P, Hayashi CY, Hedin MC (2005) The effects of preservatives and temperatures on arachnid DNA. Invertebrate Systematics 19:99–104Google Scholar
  94. Wilgers DJ, Hebets EA (2011) Complex courtship displays facilitate male reproductive success and plasticity in signaling across variable environments. Current Zoology 57(2):175–186Google Scholar
  95. Wilgers DJ, Hebets EA (2012a) Age-related female mating decisions are condition dependent in wolf spiders. Behav Ecol Sociobiol 66(1):29–38. doi:10.1007/s00265-011-1248-5 CrossRefGoogle Scholar
  96. Wilgers DJ, Hebets EA (2012b) Seismic signaling is crucial for female mate choice in a multimodal signaling wolf spider. Ethology 118(4):387–397. doi:10.1111/j.1439-0310.2012.02023.x CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Eileen A. Hebets
    • 1
  • Cor J. Vink
    • 2
    • 3
  • Laura Sullivan-Beckers
    • 1
  • Malcolm F. Rosenthal
    • 1
  1. 1.School of Biological SciencesUniversity of NebraskaLincolnUSA
  2. 2.AgResearch, Lincoln Research CentreChristchurchNew Zealand
  3. 3.Entomology Research MuseumLincoln UniversityLincolnNew Zealand

Personalised recommendations