Skip to main content
Log in

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

  • Original Paper
  • Published:
Journal of Comparative Physiology A Aims and scope Submit manuscript

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.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Abbreviations

dB:

Decibel

SPL:

Sound pressure level

References

  • Alexander RD (1962) Evolutionary change in cricket acoustical communication. Evolution 16:443–467

    Article  Google Scholar 

  • Andersson MB (1994) Sexual selection. Princeton University Press, Princeton

    Google Scholar 

  • Barth FG, Schmitt A (1991) Species recognition and species isolation in wandering spiders (Cupiennius spp; Ctenidae). Behav Ecol Sociobiol 29:333–339

    Article  Google Scholar 

  • Beckers OM, Wagner WE (2011) Mate sampling strategy in a field cricket: evidence for a fixed threshold strategy with last chance option. Anim Behav 81:519–527

    Article  Google Scholar 

  • 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 167:102–116

    Article  Google Scholar 

  • 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 28:630–641

    Article  CAS  PubMed  Google Scholar 

  • Brooks R, Hunt J, Blows MW, Smith MJ, Bussiere LF, Jennions MD (2005) Experimental evidence for multivariate stabilizing sexual selection. Evolution 59:871–880

    Article  PubMed  Google Scholar 

  • Clemens J, Hennig RM (2013) Computational principles underlying the recognition of acoustic signals in insects. J Comp Neurosci 35:75–85

    Article  Google Scholar 

  • 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 84:137–149

    Google Scholar 

  • Doherty JA (1985) Trade-off phenomena in calling song recognition and phonotaxis in the cricket, Gryllus bimaculatus (Orthoptera, Gryllidae). J Comp Physiol A 156:787–801

    Article  Google Scholar 

  • Fowler-Finn KD, Rodriguez RL (2012) Experience-mediated plasticity in mate preferences: mating assurance in a variable environment. Evolution 66:459–468

    Article  PubMed  Google Scholar 

  • Gerhardt HC (1991) Female choice in treefrogs: static and dynamic acoustic criteria. Anim Behav 42:615–636

    Article  Google Scholar 

  • Gerhardt CH, Brooks R (2009) Experimental analysis of multivariate female choice in Gray treefrogs (Hyla versicolor): evidence for directional and stabilizing selection. Evolution 63:2504–2512

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 

  • Grobe B, Rothbart MM, Hanschke A, Hennig RM (2012) Auditory processing at two time scales by the cricket Gryllus bimaculatus. J Exp Biol 215:1681–1690

    Article  PubMed  Google Scholar 

  • 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 73–111

    Google Scholar 

  • Hebets EA, Papaj DR (2005) Complex signal function: developing a framework of testable hypotheses. Behav Ecol Sociobiol 57:197–214

    Article  Google Scholar 

  • Hedwig B, Poulet JFA (2004) Complex auditory behaviour emerges from simple reactive steering. Nature 430:781–785

    Article  CAS  PubMed  Google Scholar 

  • Hennig RM (2003) Acoustic feature extraction by cross-correlation in crickets? J Comp Physiol A 189:589–598

    Article  CAS  Google Scholar 

  • 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 195:971–987

    Article  Google Scholar 

  • 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 180:621–630

    Article  Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • Hirtenlehner S, Küng S, Kainz F, Römer H (2013) Asymmetry in cricket song: female preference and proximate mechanism of discrimination. J Exp Biol 216:2046–2054

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 52:1383–1393

    Article  Google Scholar 

  • 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 84:73–80

    Article  PubMed  Google Scholar 

  • Kostarakos K, Hedwig B (2012) Calling song recognition in female crickets: temporal tuning of identified brain neurons matches behavior. J Neurosci 32:9601–9612

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Michelsen A, Löhe G (1995) Tuned directionality in cricket ears. Nature 375:639

    Article  CAS  Google Scholar 

  • Oh KP, Shaw KL (2013) Multivariate sexual selection in a rapidly evolving speciation phenotype. Proc R Soc B 280:20130482

    Article  PubMed  PubMed Central  Google Scholar 

  • Otte D (1992) Evolution of cricket songs. J Orthopt Res 1:25–49

    Article  Google Scholar 

  • Paton JA, Capranica RR, Dragsten PR, Webb WW (1977) Physical basis for auditory frequency analysis in field crickets (Gryllidae). J Comp Physiol 119:221–240

    Article  Google Scholar 

  • Pollack GS, Kim JS (2013) Selective phonotaxis to high sound-pulse rate in the cricket Gryllus assimilis. J Comp Physiol A 199:285–293

    Article  Google Scholar 

  • 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/.

  • 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 66:435–461

    Article  Google Scholar 

  • Rodríguez RL, Hallett AC, Kilmer JT, Fowler-Finn KD (2013) Curves as traits: genetic and environmental variation in mate preference functions. J Evol Biol 26:434–442

    Article  PubMed  Google Scholar 

  • Rothbart MM, Hennig RM (2012) The Steppengrille (Gryllus spec./assimilis): Selective filters and signal mismatch on two time scales. PLoS One 7(9):e43975

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sakaguchi KM, Gray DA (2011) Host song selection by an acoustically-orienting parasitoid fly exploiting a multi-species assemblage of cricket hosts. Anim Behav 81:851–858

    Article  Google Scholar 

  • Schildberger K (1984) Temporal selectivity of identified auditory neurons in the cricket brain. J Comp Physiol A 155:171–185

    Article  Google Scholar 

  • Schmidt AKD, Riede K, Romer H (2011) High background noise shapes selective auditory filters in a tropical cricket. J Exp Biol 214:1754–1762

    Article  PubMed  PubMed Central  Google Scholar 

  • Schöneich S, Kostarakos K, Hedwig B (2015) An auditory feature detection circuit for sound pattern recognition. Sci Adv 1:e1500325

    Article  PubMed  PubMed Central  Google Scholar 

  • Schul J (1998) Song recognition by temporal cues in a group of closely related bushcricket species (genus Tettigonia). J Comp Physiol A 183:401–410

    Article  Google Scholar 

  • 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 167–184

    Chapter  Google Scholar 

  • Simmons LW, Ritchie MG (1996) Symmetry in the songs of crickets. Proc Roy Soc Lond B 263:305-311

    Google Scholar 

  • 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 146:361–378

    Article  Google Scholar 

  • Tolle AE, Wagner WE (2011) Costly signals in a field cricket can indicate high- or low-quality direct benefits depending upon the environment. Evolution 65:283–294

    Article  PubMed  Google Scholar 

  • van Doorn GS, Edelaar P, Weissing FJ (2009) On the origin of species by natural and sexual selection. Science 326:1704–1707

    Article  PubMed  Google Scholar 

  • Venables WN, Ripley BD (2002a) Modern applied statistics with S, 4th edn. Springer, New York

    Book  Google Scholar 

  • 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 253–284

    Google Scholar 

  • Venables WN, Ripley BD (2002b) Modern applied statistics with S, 4th edn. Springer, New York

    Book  Google Scholar 

  • Wagner WE Jr (1996) Convergent song preferences between female field crickets and acoustically orienting parasitoid flies. Behav Ecol 7:279–285

    Article  Google Scholar 

  • 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 59:1219–1226

    Article  PubMed  Google Scholar 

  • 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 106:327–356

    Google Scholar 

  • Weissman DB, Walker TJ, Gray DA (2009) The field cricket Gryllus assimilis and two new sister species (Orthoptera: Gryllidae). Ann Entomol Soc A 102:367–380

    Article  CAS  Google Scholar 

  • West-Eberhard MJ (1983) Sexual selection, social competition, and speciation. Quart Rev Biol 58:155–183

    Article  Google Scholar 

  • 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.

Download references

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ralf Matthias Hennig.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hennig, R.M., Blankers, T. & Gray, D.A. Divergence in male cricket song and female preference functions in three allopatric sister species. J Comp Physiol A 202, 347–360 (2016). https://doi.org/10.1007/s00359-016-1083-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00359-016-1083-2

Keywords

Navigation