Journal of Comparative Physiology A

, Volume 202, Issue 5, pp 347–360 | Cite as

Divergence in male cricket song and female preference functions in three allopatric sister species

  • Ralf Matthias Hennig
  • Thomas Blankers
  • David A. Gray
Original Paper
First Online:
Received:
Revised:
Accepted:

Abstract

Multivariate female preference functions for male sexual signals have rarely been investigated, especially in a comparative context among sister species. Here we examined male signal and female preference co-variation in three closely related, but allopatric species of Gryllus crickets and quantified male song traits as well as female preferences. We show that males differ conspicuously in either one of two relatively static song traits, carrier frequency or pulse rate; female preference functions for these traits also differed, and would in combination enhance species discrimination. In contrast, the relatively dynamic song traits, chirp rate and chirp duty cycle, show minimal divergence among species and relatively greater conservation of female preference functions. Notably, among species we demonstrate similar mechanistic rules for the integration of pulse and chirp time scales, despite divergence in pulse rate preferences. As these are allopatric taxa, selection for species recognition per se is unlikely. More likely sexual selection combined with conserved properties of preference filters enabled divergent coevolution of male song and female preferences.

Keywords

Acoustic communication Sensory filter Field cricket Phonotaxis Evolution 

Abbreviations

dB

Decibel

SPL

Sound pressure level

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

Notes

Acknowledgments

We much appreciate the assistance with behavioural experiments by Elisa Becker, Darja Hahn and Vivienne Kremling. Comments by Emma Berdan and Michael Reichert improved the manuscript. The performed experiments comply with the “Principles of animal care”, publication No. 86-23, revised 1985 of the National Institute of Health, and also with the current laws of Germany. Funded by DFG/SFB 618, ‘Theoretical Biology’, and GENART speciation network from the Leibniz Association.

References

  1. Alexander RD (1962) Evolutionary change in cricket acoustical communication. Evolution 16:443–467CrossRefGoogle Scholar
  2. Andersson MB (1994) Sexual selection. Princeton University Press, PrincetonGoogle Scholar
  3. Barth FG, Schmitt A (1991) Species recognition and species isolation in wandering spiders (Cupiennius spp; Ctenidae). Behav Ecol Sociobiol 29:333–339CrossRefGoogle Scholar
  4. Beckers OM, Wagner WE (2011) Mate sampling strategy in a field cricket: evidence for a fixed threshold strategy with last chance option. Anim Behav 81:519–527CrossRefGoogle Scholar
  5. Bentsen CL, Hunt J, Jennions MD, Brooks R (2006) Complex multivariate sexual selection on male acoustic signaling in a wild population of Teleogryllus commodus. Amer Nat 167:102–116CrossRefGoogle Scholar
  6. Blankers T, Hennig RM, Gray DA (2015) Conservation of multivariate female preference functions and preference mechanisms in three species of trilling field crickets. J Evol Biol 28:630–641CrossRefPubMedGoogle Scholar
  7. Brooks R, Hunt J, Blows MW, Smith MJ, Bussiere LF, Jennions MD (2005) Experimental evidence for multivariate stabilizing sexual selection. Evolution 59:871–880CrossRefPubMedGoogle Scholar
  8. Clemens J, Hennig RM (2013) Computational principles underlying the recognition of acoustic signals in insects. J Comp Neurosci 35:75–85CrossRefGoogle Scholar
  9. Deb R, Bhattacharya M, Balakrishnan R (2012) Females of a tree cricket prefer larger males but not the lower frequency male calls that indicate large body size. J Exp Biol 84:137–149Google Scholar
  10. Doherty JA (1985) Trade-off phenomena in calling song recognition and phonotaxis in the cricket, Gryllus bimaculatus (Orthoptera, Gryllidae). J Comp Physiol A 156:787–801CrossRefGoogle Scholar
  11. Fowler-Finn KD, Rodriguez RL (2012) Experience-mediated plasticity in mate preferences: mating assurance in a variable environment. Evolution 66:459–468CrossRefPubMedGoogle Scholar
  12. Gerhardt HC (1991) Female choice in treefrogs: static and dynamic acoustic criteria. Anim Behav 42:615–636CrossRefGoogle Scholar
  13. Gerhardt CH, Brooks R (2009) Experimental analysis of multivariate female choice in Gray treefrogs (Hyla versicolor): evidence for directional and stabilizing selection. Evolution 63:2504–2512CrossRefPubMedPubMedCentralGoogle Scholar
  14. Gray DA, Gutierrez NJ, Chen TL, Gonzalez C, Weissman DB, Cole JA (2015) Species divergence in field crickets: genetics, song, ecomorphology, and pre- and postzygotic isolation. Biol J Linn Soc. doi: 10.1111/bij.12668 Google Scholar
  15. Grobe B, Rothbart MM, Hanschke A, Hennig RM (2012) Auditory processing at two time scales by the cricket Gryllus bimaculatus. J Exp Biol 215:1681–1690CrossRefPubMedGoogle Scholar
  16. Hafner DJ, Riddle BR (2011) Boundaries and barriers of North American warm deserts: an evolutionary perspective. In: Upchurch P, McGowan AJ, Slater CSC (eds) Palaeogeography and Palaeobiogeography: biodiversity in space and time. CRC Press, Boca Raton, pp 73–111Google Scholar
  17. Hebets EA, Papaj DR (2005) Complex signal function: developing a framework of testable hypotheses. Behav Ecol Sociobiol 57:197–214CrossRefGoogle Scholar
  18. Hedwig B, Poulet JFA (2004) Complex auditory behaviour emerges from simple reactive steering. Nature 430:781–785CrossRefPubMedGoogle Scholar
  19. Hennig RM (2003) Acoustic feature extraction by cross-correlation in crickets? J Comp Physiol A 189:589–598CrossRefGoogle Scholar
  20. Hennig RM (2009) Walking in Fourier’s space: algorithms for the computation of periodicities in song patterns by the cricket Gryllus bimaculatus. J Comp Physiol A 195:971–987CrossRefGoogle Scholar
  21. Hennig RM, Weber T (1997) Filtering of temporal parameters of the calling song by cricket females of two closely related species: a behavioral analysis. J Comp Physiol A 180:621–630CrossRefGoogle Scholar
  22. Hennig RM, Heller KG, Clemens J (2014) Time and timing in the acoustic recognition system of crickets. Front Physiol. doi: 10.3389/fphys.2014.00286 PubMedPubMedCentralGoogle Scholar
  23. Hirtenlehner S, Küng S, Kainz F, Römer H (2013) Asymmetry in cricket song: female preference and proximate mechanism of discrimination. J Exp Biol 216:2046–2054CrossRefPubMedPubMedCentralGoogle Scholar
  24. Jang Y, Greenfield M (1998) Absolute versus relative measurements of sexual selection: assessing the contributions of ultrasonic signal characters to mate attraction in lesser wax moths, Achroisa grisella (Lepidoptera: Pyralidae). Evolution 52:1383–1393CrossRefGoogle Scholar
  25. Jang Y, Greenfield M (2000) Quantitative genetics of female choice in an ultrasonic pyralid moth, Achroia grisella: variation and evolvability of preference along multiple dimensions of the male advertisement signal. Heredity 84:73–80CrossRefPubMedGoogle Scholar
  26. Kostarakos K, Hedwig B (2012) Calling song recognition in female crickets: temporal tuning of identified brain neurons matches behavior. J Neurosci 32:9601–9612CrossRefPubMedGoogle Scholar
  27. Kostarakos K, Hennig RM, Römer H (2009) Two matched filters and the evolution of mating signals in four species of cricket. Front Zool 6:22. doi: 10.1186/1742-9994-6-22 CrossRefPubMedPubMedCentralGoogle Scholar
  28. Lande R (1981) Models of speciation by sexual selection on polygenic traits. Proc Natl Acad Sci USA 78:3721–3725CrossRefPubMedPubMedCentralGoogle Scholar
  29. Michelsen A, Löhe G (1995) Tuned directionality in cricket ears. Nature 375:639CrossRefGoogle Scholar
  30. Oh KP, Shaw KL (2013) Multivariate sexual selection in a rapidly evolving speciation phenotype. Proc R Soc B 280:20130482CrossRefPubMedPubMedCentralGoogle Scholar
  31. Otte D (1992) Evolution of cricket songs. J Orthopt Res 1:25–49CrossRefGoogle Scholar
  32. Paton JA, Capranica RR, Dragsten PR, Webb WW (1977) Physical basis for auditory frequency analysis in field crickets (Gryllidae). J Comp Physiol 119:221–240CrossRefGoogle Scholar
  33. Pollack GS, Kim JS (2013) Selective phonotaxis to high sound-pulse rate in the cricket Gryllus assimilis. J Comp Physiol A 199:285–293CrossRefGoogle Scholar
  34. R Core Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. ISBN 3-900051-07-0. http://www.R-project.org/.
  35. Riddle BR, Hafner DJ (2006) A step-wise approach to integrating phylogeographic and phylogenetic biogeographic perspectives on the history of a core North American warm deserts biota. J Arid Environ 66:435–461CrossRefGoogle Scholar
  36. Rodríguez RL, Hallett AC, Kilmer JT, Fowler-Finn KD (2013) Curves as traits: genetic and environmental variation in mate preference functions. J Evol Biol 26:434–442CrossRefPubMedGoogle Scholar
  37. Rothbart MM, Hennig RM (2012) The Steppengrille (Gryllus spec./assimilis): Selective filters and signal mismatch on two time scales. PLoS One 7(9):e43975CrossRefPubMedPubMedCentralGoogle Scholar
  38. Sakaguchi KM, Gray DA (2011) Host song selection by an acoustically-orienting parasitoid fly exploiting a multi-species assemblage of cricket hosts. Anim Behav 81:851–858CrossRefGoogle Scholar
  39. Schildberger K (1984) Temporal selectivity of identified auditory neurons in the cricket brain. J Comp Physiol A 155:171–185CrossRefGoogle Scholar
  40. Schmidt AKD, Riede K, Romer H (2011) High background noise shapes selective auditory filters in a tropical cricket. J Exp Biol 214:1754–1762CrossRefPubMedPubMedCentralGoogle Scholar
  41. Schöneich S, Kostarakos K, Hedwig B (2015) An auditory feature detection circuit for sound pattern recognition. Sci Adv 1:e1500325CrossRefPubMedPubMedCentralGoogle Scholar
  42. Schul J (1998) Song recognition by temporal cues in a group of closely related bushcricket species (genus Tettigonia). J Comp Physiol A 183:401–410CrossRefGoogle Scholar
  43. Schul J, Bush S, Frederick KH (2014) Evolution of call patterns and pattern recognition mechanisms in Neoconocephalus katydids. In: Hedwig B (ed) Insect hearing and acoustic communication. Animal signals and communication. Springer, Heidelberg, pp 167–184CrossRefGoogle Scholar
  44. Simmons LW, Ritchie MG (1996) Symmetry in the songs of crickets. Proc Roy Soc Lond B 263:305-311Google Scholar
  45. Thorson J, Weber T, Huber F (1982) Auditory behavior of the cricket. II. Simplicity of calling song recognition in Gryllus, and anomalous phonotaxis at abnormal carrier frequencies. J Comp Physiol 146:361–378CrossRefGoogle Scholar
  46. Tolle AE, Wagner WE (2011) Costly signals in a field cricket can indicate high- or low-quality direct benefits depending upon the environment. Evolution 65:283–294CrossRefPubMedGoogle Scholar
  47. van Doorn GS, Edelaar P, Weissing FJ (2009) On the origin of species by natural and sexual selection. Science 326:1704–1707CrossRefPubMedGoogle Scholar
  48. Venables WN, Ripley BD (2002a) Modern applied statistics with S, 4th edn. Springer, New YorkCrossRefGoogle Scholar
  49. von Helversen O, von Helversen D (1994) Forces driving coevolution of song and song recognition in grasshoppers. In: Schildberger K, Elsner N (eds) Neural basis of behavioural adaptations. Fischer, Stuttgart, pp 253–284Google Scholar
  50. Venables WN, Ripley BD (2002b) Modern applied statistics with S, 4th edn. Springer, New YorkCrossRefGoogle Scholar
  51. Wagner WE Jr (1996) Convergent song preferences between female field crickets and acoustically orienting parasitoid flies. Behav Ecol 7:279–285CrossRefGoogle Scholar
  52. Wagner WE Jr, Reiser MG (2000) The importance of calling song and courtship song in female mate choice in the variable field cricket. Anim Behav 59:1219–1226CrossRefPubMedGoogle Scholar
  53. Weissman DB, Rentz DCF, Alexander RD, Loher W (1980) Field crickets (Gryllus and Acheta) of California and Baja California, Mexico (Orthoptera: Gryllidae: Gryllinae). Trans Am Entomol Soc 106:327–356Google Scholar
  54. Weissman DB, Walker TJ, Gray DA (2009) The field cricket Gryllus assimilis and two new sister species (Orthoptera: Gryllidae). Ann Entomol Soc A 102:367–380CrossRefGoogle Scholar
  55. West-Eberhard MJ (1983) Sexual selection, social competition, and speciation. Quart Rev Biol 58:155–183CrossRefGoogle Scholar
  56. Wood DA, Vandergast AG, Barr KR, Inman RD, Esque TC, Nussear KE, Fisher RN (2012) Comparative phylogeography reveals deep lineages and regional evolutionary hotspots in the Mojave and Sonoran deserts. Diversity and Distributions:1–16.Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Ralf Matthias Hennig
    • 1
  • Thomas Blankers
    • 1
    • 2
  • David A. Gray
    • 3
  1. 1.Behavioural Physiology, Department of BiologyHumboldt-Universität zu BerlinBerlinGermany
  2. 2.Museum für Naturkunde zu BerlinLeibniz Institute for Evolution and Biodiversity ScienceBerlinGermany
  3. 3.Department of BiologyCalifornia State University NorthridgeNorthridgeUSA

Personalised recommendations