Abstract
In crickets acoustic communication serves mate selection. Female crickets have to perceive and integrate male cues relevant for mate choice while confronted with several different signals in an acoustically diverse background. Overall female decisions are based on the attractiveness of the temporal pattern (informative about the ‘what’) and on signal intensity (informative about the ‘where’) of male calling songs. Here, we investigated how the relevant cues for mate choice are integrated during the decision process by females of five different species of chirping and trilling field crickets. Using a behavioral design, female preferences in no-choice and choice situations for male calling songs differing in pulse rate, modulation depth, intensities, chirp/trill arrangements and temporal shifts were examined. Sensory processing underlying decisions in female field crickets is rather similar as combined evidence suggested that incoming song patterns were analyzed separately by bilaterally paired networks for pattern attractiveness and pattern intensity. A downstream gain control mechanism leads to a weighting of the intensity cue by pattern attractiveness. While remarkable differences between species were observed with respect to specific processing steps, closely related species exhibited more similar preferences than did more distantly related species.
Similar content being viewed by others
References
Alexander RD (1957) The taxonomy of the field crickets of the eastern United States (Orthoptera: Gryllidae: Acheta). Ann Entomol Soc Am 50:584–602
Alexander RD (1962) Evolutionary change in cricket acoustical communication. Evolution 16:443–467
Benda J, Hennig RM (2008) Spike-frequency adaptation generates intensity invariance in a primary auditory interneuron. J Comp Neurosci 24:113–136
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
Blankers T, Vilaca S, Waurick I, Gray DA, Hennig RM, Mazzoni C, Mayer F, Berdan E (2016) Demography and selection shape transcriptomic divergence in field crickets. Mol Ecol (in review)
Clemens J, Hennig RM (2013) Computational principles underlying the recognition of acoustic signals in insects. J Comput Neurosci. doi:10.1007/s10827-013-0441-0
Dahmen HJ (1980) A simple apparatus to investigate the orientation of walking insects. Experientia 36:685–687
Deily JA, Schul J (2004) Recognition of calls with exceptionally fast pulse rates: female phonotaxis in the genus Neoconocephalus (Orthoptera: Tettigoniidae). J Exp Biol 207:3523–3529
Deily JA, Schul J (2009) Selective phonotaxis in Neoconocephalus nebrascensis (Orthoptera: Tettigoniidae): call recognition at two temporal scales. J Comp Physiol A 195:31–37
Doherty JA (1985) Phonotaxis in the cricket, Gryllus bimaculatus DeGeer: comparison of choice and no-choice paradigms. J Comp Physiol A 157:279–289
Doherty JA, Storz MM (1992) Calling song and selective phonotaxis in the field crickets Gryllus firmus and G. pennsylvanicus (Orthoptera: Gryllidae). J Insect Behav 5(5):555–569
Gabel E, Kuntze J, Hennig RM (2015) Decision making and preferences for acoustic signals in choice situations by female crickets. J Exp Biol 218:2641–2650. doi:10.1242/jeb.120378
Gabel E, Vural P, Mariot L, Hennig RM (2016) A gain control mechanism governs the weighting of acoustic signal intensity and attractiveness during female decisions. Anim Behav (in revision)
Gerhardt HC, Huber F (2002) Acoustic communication in insects and anurans. The University of Chicago Press, Chicago
Gollisch T, Schütze H, Benda J, Herz VM (2002) Energy integration describes sound intensity coding in an insect auditory system. J Neurosci 22:10434–10448
Gray DA (2005) Does courtship behavior contribute to species level reproductive isolation in field crickets? Behav Ecol 16(1):201–206
Gray DA, Cade WH (2000) Sexual selection and speciation in field crickets. PNAS 97(26):14449–14454
Gray DA, Huang H, Knowles LL (2008) Molecular evidence of a peripatric origin for two sympatric species of field crickets (Gryllus rubens and G. texensis) revealed from coalescent simulations and population genetic tests. Mol Ecol 17:3836–3855. doi:10.1111/j.1365-294X.2008.03827.x
Gray DA, Gabel E, Blankers T, Hennig RM (2016a) Multivariate female preference tests reveal latent perceptual biases. Proc R Soc B (in revision)
Gray DA, Gutierrez NJ, Chen TL, Gonzalez C, Weissman DB, Cole JA (2016b) Species divergence in field crickets: genetics, song, ecomorphology, and pre- and postzygotic isolation. Biol J Linnean Soc 117:192–205
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
Harrison RG, Arnold J (1982) A narrow hybrid zone between closely related cricket species. Evolution 36(3):535–552
Hartbauer M, Römer H (2016) Rhythm generation and rhythm perception in insects: the evolution of synchronous choruses. Front Neurosci. doi:10.3389/fnins.2016.00223
Hedwig B, Poulet JFA (2004) Complex auditory behavior emerges from simple reactive steering. Nature 430:781–785
Hedwig B, Poulet JFA (2005) Mechanisms underlying phonotactic steering in the cricket Gryllus bimaculatus revealed with a fast trackball system. J Exp Biol 208:915–927
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
Hennig RM, Heller KG, Clemens J (2014) Time and timing in the acoustic recognition system oft crickets. Front Physiol. doi:10.3389/fphys.2014.00286
Hennig RM, Blankers T, Gray DA (2016) Divergence in male cricket song and female preference functions in three allopatric sister species. J Comp Physiol A. doi:10.1007/s00359-016-1083-2
Hildebrandt KJ, Benda J, Hennig RM (2015) Computational themes of peripheral processing in the auditory pathway of insects. J Comp Physiol A 201:39–50
Hirtenlehner S, Römer H (2014) Selective phonotaxis of female crickets under natural outdoor conditions. J Comp Physiol A 200:239–250
Horseman G, Huber F (1994) Sound localization in crickets. I. Contralateral inhibition of an ascending auditory interneuron (AN1) in the cricket Gryllus bimaculatus. J Comp Physiol A 175:389–398
Huang Y, Ortí G, Sutherlin M, Duhachek A, Zera A (2000) Phylogenetic relationships of North American field crickets inferred from mitochondrial DNA data. Mol Phylogenet Evol 17(1):48–57
Izzo AS, Gray DA (2004) Cricket song in sympatry: species specificity of song without reproductive character displacement in Gryllus rubens. Ann Entomol Soc 97(4):831–837
Joris PX, Schreiner CE, Rees A (2004) Neural processing of amplitude-modulated sounds. Physiol Rev 84:541–577
Leonard AS, Hedrick AV (2009) Male and female crickets use different decision rules in response to mating signals. Behav Ecol. doi:10.1093/beheco/arp115
Miller GF, Todd PM (1998) Mate choice turns cognitive. Trends Cogn Sci 2:190–198
Pollack GS (1986) Discrimination of calling song models by the cricket, Teleogryllus oceanicus: the influence of sound direction on neural encoding of the stimulus temporal pattern and on phonotactic behavior. J Comp Physiol A 158:549–561
Pollack GS (1988) Selective attention in an insect auditory neuron. J Neurosci 8(7):2635–2639
Popov AV, Shuvalov VF (1977) Phonotactic behavior of crickets. J Comp Physiol 119:111–126
Poulet J, Hedwig B (2005) Auditory orientation in crickets: pattern recognition controls reactive steering. PNAS 102:15665–15669
Prinz P, Ronacher B (2002) Temporal modulation transfer functions in auditory receptor fibres of the locust (Locusta migratoria L.). J Comp Physiol A 188:577–587
Regen J (1913) Über die Anlockung des Weibchens von Gryllus campestris L. durch telephonisch übertragene Stridulationslaute des Männchens. Pflug Arch Ges Phys 15:193–200
Römer H, Krusch M (2000) A gain-control mechanism for processing of chorus sounds in the afferent auditory pathway of the bushcricket Tettigonia virridissima (Orthoptera; Tettigoniidae). J Comp Physiol A 186:181–191
Römer H, Hedwig B, Ott SR (2002) Contralateral inhibition as a sensory bias: the neural basis for a female preference in a synchronously calling bushcricket, Mecopoda elongata. Eur J Neurosci 15:1655–1662
Ronacher B (1979) Beitrag einzelner Parameter zum wahrnehmungsgemäßen Unterschied von zusammengesetzten Reizen der Honigbiene. Biol Cybern 32:77–83
Ronacher B (1983) Unabhängigkeit der Bewertung zweier Musterparameter von deren Unterschiedlichkeitsgrad bei der Dressur. Biol Cybern 46:173–182
Schmidt AK, Riede K, Römer H (2011) High background noise shapes selective auditory filters in a tropical cricket. J Exp Biol 214:1754–1762. doi:10.1242/jeb.053819
Schöneich S, Kostarakos K, Hedwig B (2015) An auditory feature detection circuit for sound pattern recognition. Sci Adv 1:e1500325
Schul J, von Helversen D, Weber T (1998) Selective phonotaxis in Tettigonia cantans and T. viridissima in song recognition and discrimination. J Comp Physiol A 182:687–694
Selverston AI, Kleindienst HU, Huber F (1985) Synaptic connectivity between cricket auditory interneurons as studied by selective photoinactivation. J Neurosci 5(5):1283–1292
Stabel J, Wendler G, Scharstein H (1989) Cricket phonotaxis: localization depends on recognition of the calling song pattern. J Comp Physiol A 165:165–177
Von Helversen D, von Helversen O (1995) Acoustic pattern recognition and orientation in orthopteran insects: parallel or serial processing? J Comp Physiol A 177:767–774
Weber T, Thorson J, Huber F (1981) Auditory behavior of the cricket: I. Dynamics of compensated walking and discrimination paradigms on the Kramer treadmill. J Comp Physiol 141:215–232
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
Wendler G (1989) Acoustic orientation of crickets (Gryllus campestris) in the presence of two sound sources. Naturwissenschaften 76:128–129
Wohlgemuth S, Vogel A, Ronacher B (2011) Encoding of amplitude modulations by auditory neurons of the locust: influence of modulation frequency, rise time, and modulation depth. J Comp Physiol A 197:61–74
Wyttenbach RA, Hoy RR (1993) Demonstration of the precedence effect in an insect. J Acoust Soc Amer 94:777–784
Acknowledgments
We thank Bernhard Ronacher for critical and constructive discussions about the data analyses and the manuscript. We appreciate Elisa Becker, Pascal Kolja Haß, Anne Görlitz, Daria Ivanova and Ailyn Yilmaz for the help with some of the experiments. All applicable international, national and/or institutional guidelines for the care and use of animals were followed. This work was supported by the German Research Foundation [he2812/4-1].
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no competing or financial interest.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Gabel, E., Gray, D.A. & Matthias Hennig, R. How females of chirping and trilling field crickets integrate the ‘what’ and ‘where’ of male acoustic signals during decision making. J Comp Physiol A 202, 823–837 (2016). https://doi.org/10.1007/s00359-016-1124-x
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00359-016-1124-x