Skip to main content
Log in

Multivariate Phenotypic Evolution: Divergent Acoustic Signals and Sexual Selection in Gryllus Field Crickets

  • Research Article
  • Published:
Evolutionary Biology Aims and scope Submit manuscript

Abstract

Predicting the response to selection is at the core of evolutionary biology. Presently, thorough understanding of the effects of selection on the multivariate phenotype is lacking, in particular for behavioral traits. Here, we compared multivariate acoustic mating signals among seven field cricket species contrasting two selection regimes: (1) species producing songs with long trains of pulses for which preference functions for acoustic energy (chirp duty cycle) are linear and likely exert strong directional selection (‘trillers’); (2) species producing songs consisting of short chirps and for which preference functions for chirp duty cycle are concave and directional selection is likely weak or absent (‘chirpers’). We compared the phenotypic variance–covariance matrix (P) among species and uncovered two main patterns: First, surprisingly, pulse rate and chirp rate were positively correlated in six of seven species thus suggesting phenotypic coupling of timescales. Second, chirp rate and chirp duty cycle also covaried, but the direction of covariation differed between chirpers (positive) and trillers (negative). Multi-population Bayesian methods for matrix comparisons, Krzanowski’s subspace comparison and tensor analysis, revealed significant variation in P unrelated to phylogenetic distance, but strongly contrasting chirpers and trillers. We also found differences in the predicted selection response between chirpers and trillers. We thus report that variation in P is higher between than within selection regimes. Although effects from drift and shared ancestry cannot be fully excluded, these findings highlight a role for sexual selection in shaping patterns of phenotypic covariation that can ultimately affect the evolutionary trajectory of a multivariate mating signal.

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

Similar content being viewed by others

References

  • Aguirre, J. D., Hine, E., McGuigan, K., & Blows, M. W. (2014). Comparing G: Multivariate analysis of genetic variation in multiple populations. Heredity, 112(1), 21–29.

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Arnold, S. J., Bürger, R., Hohenlohe, P. A., Ajie, B. C., & Jones, A. G. (2008). Understanding the evolution and stability of the G-matrix. Evolution, 62(10), 2451–2461.

    Article  PubMed  PubMed Central  Google Scholar 

  • Bégin, M., & Roff, D. A. (2004). From micro- to macroevolution through quantitative genetic variation: Positive evidence from field crickets. Evolution, 58(10), 2287–2304.

    Article  PubMed  Google Scholar 

  • Bentsen, C. L., Hunt, J., Jennions, M. D., & Brooks, R. (2006). Complex multivariate sexual selection on male acoustic signaling in a wild population of Teleogryllus commodus. The American Naturalist, 167(4), E102–E116.

    Article  PubMed  Google Scholar 

  • Berner, D., Stutz, W. E., & Bolnick, D. I. (2010). Foraging trait (co)variances in stickleback evolve deterministically and do not predict trajectories of adaptive diversification. Evolution, 64(8), 2265–2277.

    PubMed  Google Scholar 

  • Bertram, S. M., Fitzsimmons, L. P., McAuley, E. M., Rundle, H. D., & Gorelick, R. (2012). Phenotypic covariance structure and its divergence for acoustic mate attraction signals among four cricket species. Ecology and Evolution, 2(1), 181–195.

    Article  PubMed  PubMed Central  Google Scholar 

  • Blankers, T., Hennig, R. M., & Gray, D. A. (2015). Conservation of multivariate female preference functions and preference mechanisms in three species of trilling field crickets. Journal of Evolutionary Biology, 28(3), 630–641.

    Article  CAS  PubMed  Google Scholar 

  • Blows, M. W., Chenoweth, S. F., & Hine, E. (2004). Orientation of the genetic variance–covariance matrix and the fitness surface for multiple male sexually selected traits. American Naturalist, 163, 329–340.

    Article  PubMed  Google Scholar 

  • Blows, M. W., & Higgie, M. (2003). Genetic constraints on the evolution of mate recognition under natural selection. American Naturalist, 161, 240–253.

    Article  PubMed  Google Scholar 

  • Broughton, R. E., & Harrison, R. G. (2003). Nuclear gene genealogies reveal historical, demographic and selective factors associated with speciation in field crickets. Genetics, 163(4), 1389–1401.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cheverud, J. M. (1988). A comparison of genetic and phenotypic correlations. Evolution: International Journal of Organic Evolution, 42(5), 958–968.

    Article  Google Scholar 

  • Clemens, J., & Hennig, R. M. (2013). Computational principles underlying the recognition of acoustic signals in insects. Journal of Computational Neuroscience, 35, 75–85.

    Article  PubMed  Google Scholar 

  • Flury, B. (1988). Common principal components and related multivariate models. New York: Wiley.

    Google Scholar 

  • Gerhardt, H. C., & 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 

  • Gerhardt, H. C., & Huber, F. (2002). Acoustic communication in insects and anurans. Chicago: The University of Chicago Press.

    Google Scholar 

  • Gray, D. A., & Cade, W. H. (2000). Sexual selection and speciation in field crickets. Proceedings of the National Academy of Sciences, 97, 14449–14454.

    Article  CAS  Google Scholar 

  • Gray, D. A., Gabel, E., Blankers, T., & Hennig, R. M. (2016a). Multivariate female preference tests reveal latent perceptual biases. Proc R Soc B (in review)

  • Gray, D. A., Gutierrez, N. J., Chen, T. O. M. L., Weissman, D. B., & Cole, J. A. (2016b). Species divergence in field crickets: Genetics, song, ecomorphology, and pre- and postzygotic isolation. Biological Journal of the Linnean Society, 117(2), 192–205.

    Article  Google Scholar 

  • Gray, D. A., Huang, H., & Knowles, L. L. (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. Molecular Ecology, 17, 3836–3855.

    Article  PubMed  Google Scholar 

  • Grobe, B., Rothbart, M. M., Hanschke, A., & Hennig, R. M. (2012). Auditory processing at two time scales by the cricket Gryllus bimaculatus. The Journal of experimental biology, 215, 1681–1690.

    Article  PubMed  Google Scholar 

  • Haber, A. (2014). The evolution of morphological integration in the ruminant skull. Evolutionary Biology, 42(1), 99–114.

    Article  Google Scholar 

  • Hadfield, J. D. (2010). MCMC methods for multi-response generalized linear mixed models: The MCMCglmm R package. Journal of Statistical Software, 33, 1–22.

    Article  Google Scholar 

  • Hadfield, J. D. (2012). MCMCglmm course notes. http://cran.r-project.org/web/packages/MCMCglmm/vignettes/CourseNotes.pdf.

  • Hansen, T. F., & Houle, D. (2008). Measuring and comparing evolvability and constraint in multivariate characters. Journal of Evolutionary Biology, 21, 1201–1219.

    Article  CAS  PubMed  Google Scholar 

  • Hazel, L. N., Dickerson, G. E., & Freeman, A. E. (1994). The selection index—Then, now, and for the future. Journal of Dairy Science, 77(10), 3236–3251.

    Article  CAS  PubMed  Google Scholar 

  • Hedwig, B. (2000). Control of cricket stridulation by a command neuron: Efficacy depends on the behavioral state. Journal of Neurophysiology, 83, 712–722.

    CAS  PubMed  Google Scholar 

  • Heiberger, R. M., & Holland, B. (2004). Statistical analysis and data display: An intermediate course with examples in S-plus, R, and SAS., Springer texts in statistics New York: Springer.

    Book  Google Scholar 

  • Hennig, M. R., Blankers, T., & Gray, D. A. (2016). Divergence in male cricket song and multivariate female preference functions in three allopatric sister species. Journal of Comparative Physiology A, 202, 347–360.

    Article  Google Scholar 

  • Hennig, R. M., Heller, K.-G., & Clemens, J. (2014). Time and timing in the acoustic recognition system of crickets. Frontiers in Physiology, 5, 286. doi:10.3389/fphys.2014.00286.

    Article  PubMed  PubMed Central  Google Scholar 

  • Hine, E., Chenoweth, S. F., Rundle, H. D., & Blows, M. W. (2009). Characterizing the evolution of genetic variance using genetic covariance tensors. Philosophical Transactions of the Royal Society B: Biological Sciences, 364(1523), 1567–1578.

    Article  Google Scholar 

  • Hoback, W. W., & Wagner, W. E., Jr. (1997). The energetic cost of calling in the variable field cricket, Gryllus lineaticeps. Physiological Entomology, 22, 286–290.

    Article  Google Scholar 

  • Houle, D., Pelabon, C., Wagner, G. P., & Hansen, T. F. (2011). Measurement and meaning in biology. The Quarterly Review of Biology, 86(1), 3–34.

    Article  PubMed  Google Scholar 

  • Huang, Y., Ortí, G., Sutherlin, M., Duhachek, A., & Zera, A. (2000). Phylogenetic relationships of North American field crickets inferred from mitochondrial DNA data. Molecular Phylogenetics and Evolution, 17(1), 48–57.

    Article  CAS  PubMed  Google Scholar 

  • Jones, A. G., Arnold, S. J., & Bürger, R. (2003). Stability of the G-matrix in a population experiencing pleiotropic mutation, stabilizing selection, and genetic drift. Evolution, 57(8), 1747–1760.

    Article  PubMed  Google Scholar 

  • Kolbe, J. J., Revell, L. J., Szekely, B., Brodie, E. D., III, & Losos, J. B. (2011). Convergent evolution of phenotypic integration and its alignment with morphological diversification in caribbean Anolis ecomorphs. Evolution, 65(12), 3608–3624.

    Article  PubMed  Google Scholar 

  • Krzanowski, W. J. (1979). Between groups comparison of principal components. Journal of American Statistical Association, 74, 703–707.

    Article  Google Scholar 

  • Lande, R. (1979). Quantitative genetic analysis of multivariate evolution, applied to brain: Body size allometry. Evolution: International Journal of Organic Evolution, 33, 402–416.

    Article  Google Scholar 

  • Lande, R., & Arnold, S. J. (1983). The measurement of selection on correlated characters. Evolution, 37(6), 1210–1226.

    Article  Google Scholar 

  • Laughlin, D. C., & Messier, J. (2015). Fitness of multidimensional phenotypes in dynamic adaptive landscapes. Trends in Ecology & Evolution, 30(8), 1–10.

    Article  Google Scholar 

  • Lynch, M., & Walsh, B. (1998). Genetics and analysis of quantitative Traits. Sunderland, MA: Sinauer.

    Google Scholar 

  • Melo, D., & Marroig, G. (2014). Directional selection can drive the evolution of modularity in complex traits. Proceedings of the National Academy of Sciences, 112(2), 470–475.

    Article  Google Scholar 

  • Otte, D. (1992). Evolution of cricket songs. Journal of Orthoptera Research, 1, 25–49.

    Article  Google Scholar 

  • Phillips, P. C., & Arnold, S. J. (1989). Visualizing multivariate selection. Evolution, 43(6), 1209–1222.

    Article  Google Scholar 

  • R Development Core Team, R. (2015). R: A language and environment for statistical computing. In R. D. C. Team (Ed.), R foundation for statistical computing. R Foundation for Statistical Computing.

  • Ritchie, M. G. (2007). Sexual selection and speciation. Annual Review of Ecology Evolution and Systematics, 38(1), 79–102.

    Article  Google Scholar 

  • Rodríguez, R. L., Hallett, A. C., Kilmer, J. T., & Fowler-Finn, K. D. (2013). Curves as traits: Genetic and environmental variation in mate preference functions. Journal of Evolutionary Biology, 26, 434–442.

    Article  PubMed  Google Scholar 

  • Roff, D. (2000). The evolution of the G matrix: Selection or drift? Heredity, 84, 135–142.

    Article  PubMed  Google Scholar 

  • Roff, D. A., & Fairbairn, D. J. (2012). The evolution of trade-offs under directional and correlational selection. Evolution, 66(8), 2461–2474.

    Article  PubMed  Google Scholar 

  • Roff, D., Mousseau, T., & Howard, D. (1999). Variation in genetic architecture of calling song among populations of Allonemobius socius, A. fasciatus, and a hybrid population: Drift or selection? Evolution, 53(1), 216–224.

    Article  Google Scholar 

  • Rothbart, M. M., & Hennig, R. M. (2012). Calling song signals and temporal preference functions in the cricket Teleogryllus leo. Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology, 198(11), 817–825.

    Article  CAS  PubMed  Google Scholar 

  • Sakaguchi, K. M., & Gray, D. A. (2011). Host song selection by an acoustically orienting parasitoid fly exploiting a multispecies assemblage of cricket hosts. Animal Behaviour, 81(4), 851–858.

    Article  Google Scholar 

  • Schöneich, S., & Hedwig, B. (2012). Cellular basis for singing motor pattern generation in the field cricket (Gryllus bimaculatus DeGeer). Brain and Behavior, 2(6), 707–725.

    Article  PubMed  PubMed Central  Google Scholar 

  • Schoneich, S., Kostarakos, K., & Hedwig, B. (2015). An auditory feature detection circuit for sound pattern recognition. Science Advances, 1(8), e1500325.

    Article  PubMed  PubMed Central  Google Scholar 

  • Steppan, S. J. (1997). Phylogenetic analysis of phenotypic covariance structure. I. Contrasting results from matrix correlation and common principal component analysis. Evolution, 51(2), 571–586.

    Article  Google Scholar 

  • Steppan, S. J., Phillips, P. C., & Houle, D. (2002). Comparative quantitative genetics: Evolution of the G matrix. Trends in Ecology & Evolution, 17(7), 320–327.

    Article  Google Scholar 

  • Swenson, N. G. (2014). Functional and phylogenetic ecology in R. New York, NY: Springer.

    Book  Google Scholar 

  • Turelli, M. (1988). Phenotypic evolution, constant covariances, and the maintenance of additive variance. Evolution, 42(6), 1342–1347.

    Article  Google Scholar 

  • Venables, W. N., & Ripley, B. D. (2002). Modern applied statistics with S. Statistics and computing. New York: Springer-Verlag.

    Book  Google Scholar 

  • Wagner, W. E., & Basolo, A. L. (2007). The relative importance of different direct benefits in the mate choices of a field cricket. Evolution, 61(3), 617–622.

    Article  PubMed  Google Scholar 

  • Walker, T. J. (2015). Crickets. In Singing insects of North America. http://entnemdept.ifas.ufl.edu/walker/Buzz/crickets.htm.

  • Willis, J. H., Coyne, J. A., & Kirkpatrick, M. (1991). Can one predict the evolution of quantitative characters without genetics. Evolution, 45(2), 441–444.

    Article  Google Scholar 

Download references

Acknowledgments

The manuscript strongly benefitted from comments by Emma Berdan, Jonas Finck, and Michael Reichert and peer review by Derek A. Roff, Katherine Willmore, and four anonymous reviewers. 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. The authors declare no conflict of interest. Data will be deposited in the Dryad Digital Repository. This study is part of the GENART project funded by the Leibniz Association (SAW-2012-MfN-3).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Thomas Blankers.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 42 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Blankers, T., Gray, D.A. & Matthias Hennig, R. Multivariate Phenotypic Evolution: Divergent Acoustic Signals and Sexual Selection in Gryllus Field Crickets. Evol Biol 44, 43–55 (2017). https://doi.org/10.1007/s11692-016-9388-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11692-016-9388-1

Keywords

Navigation