Spatial and temporal variation in three call traits and preferences of the tree cricket Oecanthus forbesi

Original Article

Abstract

Multiple selective forces act on the evolution of mating preferences. While mating preferences are central to pre-zygotic isolation, certain preferences and traits may make greater contributions. For some traits, females may exhibit preferences, but accept heterospecifics trait values when preferred values are scarce. For other traits, females may fail to reproduce before accepting heterospecifics trait values. Understanding patterns of variation and divergence in this later class of traits is particularly relevant to understanding divergence and speciation. Here, I focus on three call traits of Forbes’ Tree Cricket (Oecanthus forbesi) to quantify their capacity to produce reproductive isolation and to compare patterns of variation and divergence in these traits. By generating female preference functions and measuring male call parameters, I test two hypotheses: (1) traits and preferences vary in their capacity to contribute to reproductive isolation and (2) traits that are important to reproductive isolation have lower intrapopulation, interpopulation, and interannual variation and weaker correlation with male body size. I find that female response to one trait (pulse rate) decreased sharply when trait values fell within the heterospecific range. This trait had low variation and no correlation with male morphology. For two other traits (pulse duration and dominant frequency), females responded to many values, including values characteristics of co-occurring heterospecifics. Trait variation was higher and pulse duration correlated with male leg length. These results indicate that the evolutionary dynamics of a low-variation trait (pulse rate) may be more important to speciation than changes in more conspicuously variable sexually selected traits.

Significance statement

Animals often attract and assess mates using complex signals. This paper tests whether some signal components contribute more to preventing mating between species. The data show that changes in a single trait [pulse rate of cricket calls] can eliminate female response to males, while other traits [dominant frequency (pitch) and pulse duration] can be changed to match the values produced by other species without reducing female response. Consequently, some traits may diverge without contributing to reproductive isolation between species. The paper then tests for correlations between trait function and patterns of trait variation within and between populations and species. Pulse rate has low variation within and between populations, but differs substantially between species. Dominant frequency and pulse rate are more variable within and between populations. Pulse duration also correlates with male body size, indicating that pulse duration could reflect male condition even if it is relatively unimportant for reproductive isolation.

Keywords

Insect communication Mate choice Orthoptera Sexual selection Speciation 

Notes

Acknowledgements

I thank Nancy Collins, Cathy and Don Balas, Laurel Kennedy, Rick Courson, and Robin and Barb Symes for their hospitality as well as Dawes Arboretum and Richard Bong State Recreation Area for access to their property. I acknowledge the National Evolutionary Synthesis Center (NESCent) speciation working group (NSF #EF- 412 0905606) for valuable discussions and insights. C. Cowdery provided useful discussion and assistance with morphological measurements. Matt Ayres provided statistical assistance and advice. Mark McPeek, Rebecca Safran, Ryan Calsbeek, Nathaniel Dominy, Tamra Mendelson, Elizabeth Reinke, Hannah ter Hofstede, and Robin Symes are gratefully acknowledged for their discussion or comments on the manuscript. Funding was provided by Dartmouth College, the NSF-GK12 program, and the Neukom Institute.

Compliance with ethical standards

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. This study did not use human participants.

Conflict of interest

The author declares that there is no conflict of interest.

Supplementary material

265_2018_2442_MOESM1_ESM.docx (1.5 mb)
ESM 1 (DOCX 1509 kb).
265_2018_2442_MOESM2_ESM.docx (91 kb)
ESM 2 (DOCX 90 kb).
265_2018_2442_MOESM3_ESM.xlsx (69 kb)
ESM 3 (XLSX 68 kb).
265_2018_2442_MOESM4_ESM.xlsx (43 kb)
ESM 4 (XLSX 42 kb).

References

  1. Abernethy K, Abt G, Reyer H-U et al (2008) The fish eye view: are cichlids conspicuous? Evolution (N Y) 20:223–231.  https://doi.org/10.1111/j.1558-5646.2007.00019.x Google Scholar
  2. Andersson MB (1994) Sexual selection. Princeton University Press, PrincetonGoogle Scholar
  3. Arbuthnott D, Crespi BJ (2009) Courtship and mate discrimination within and between species of Timema walking-sticks. Anim Behav 78:53–59CrossRefGoogle Scholar
  4. Bailey NW (2008) Love will tear you apart: different components of female choice exert contrasting selection pressures on male field crickets. Behav Ecol 19(5):960–966.  https://doi.org/10.1093/beheco/arn054 CrossRefGoogle Scholar
  5. Boake CR, DeAngelis MP, Andreadis DK (1997) Is sexual selection and species recognition a continuum? Mating behavior of the stalk-eyed fly Drosophila heteroneura. Proc Natl Acad Sci 94(23):12442–12445.  https://doi.org/10.1073/pnas.94.23.12442 CrossRefPubMedPubMedCentralGoogle Scholar
  6. Brown WD, Wideman J, Andrade MCB, Mason AC, Gwynne DT (1996) Female choice for an indicator of male size in the song of the black-horned tree cricket, Oecanthus nigricornis (Orthoptera: Gryllidae: Oecanthinae). Evolution 50(6):2400–2411.  https://doi.org/10.1111/j.1558-5646.1996.tb03627.x CrossRefPubMedGoogle Scholar
  7. Burnham KP, Anderson DR (2010) Model selection and multimodel inference: a practical information-theoretical approach, 2nd edn. Springer-Verlag, New YorkGoogle Scholar
  8. 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. Anim Behav 84:137–149CrossRefGoogle Scholar
  9. Desutter-Grandcolas L, Robillard T (2003) Phylogeny and the evolution of calling songs in Gryllus (Insecta, Orthoptera, Gryllidae). Zool Scr 32(2):173–183.  https://doi.org/10.1046/j.1463-6409.2003.00107.x CrossRefGoogle Scholar
  10. Ferreira M, Ferguson J (2002) Geographic variation in the calling song of the field cricket Gryllus bimaculatus (Orthoptera: Gryllidae) and its relevance to mate recognition and mate choice.Google Scholar
  11. Forrest T (1994) From sender to receiver: propagation and environmental effects on acoustic-signals. Am Zool 34(6):644–654.  https://doi.org/10.1093/icb/34.6.644 CrossRefGoogle Scholar
  12. Gerhardt HC (1991) Female mate choice in treefrogs: static and dynamic acoustic criteria. Anim Behav 42(4):615–635.  https://doi.org/10.1016/S0003-3472(05)80245-3 CrossRefGoogle Scholar
  13. Gerhardt HC (2001) Acoustic communication in two groups of closely related treefrogs. Adv Study Behav 30:99–167.  https://doi.org/10.1016/S0065-3454(01)80006-1 CrossRefGoogle Scholar
  14. Gerhardt HC, Huber F (2002) Acoustic communication in insects and anurans: common problems and diverse solutions. University of Chicago Press, ChicagoGoogle Scholar
  15. Gray DA, Cade WH (2000) Sexual selection and speciation in field crickets. Proc Natl Acad Sci 97(26):14449–14454.  https://doi.org/10.1073/pnas.97.26.14449 CrossRefPubMedPubMedCentralGoogle Scholar
  16. Head ML, Hunt J, Jennions MD, Brooks R (2005) The indirect benefits of mating with attractive males outweigh the direct costs. PLoS Biol 3(2):e33.  https://doi.org/10.1371/journal.pbio.0030033 CrossRefPubMedPubMedCentralGoogle Scholar
  17. Hebets EA, Papaj DR (2005) Complex signal function: developing a framework of testable hypotheses. Behav Ecol Sociobiol 57(3):197–214.  https://doi.org/10.1007/s00265-004-0865-7 CrossRefGoogle Scholar
  18. Hedrick AV (1986) Female preferences for male calling bout duration in a field cricket. Behav Ecol Sociobiol 19(1):73–77.  https://doi.org/10.1007/BF00303845 CrossRefGoogle Scholar
  19. Hennig R, 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(6):621–630.  https://doi.org/10.1007/s003590050078 CrossRefGoogle Scholar
  20. Hill K (1974) Carrier frequency as a factor in phonotactic behaviour of female crickets (Teleogryllus commodus). J Comp Physiol 93(1):7–18.  https://doi.org/10.1007/BF00608756 CrossRefGoogle Scholar
  21. Imaizumi K, Pollack GS (1999) Neural coding of sound frequency by cricket auditory receptors. J Neurosci 19(4):1508–1516CrossRefPubMedGoogle Scholar
  22. Johnson JB, Omland KS (2004) Model selection in ecology and evolution. Trends Ecol Evol 19(2):101–108.  https://doi.org/10.1016/j.tree.2003.10.013 CrossRefPubMedGoogle Scholar
  23. Klappert K, Reinhold K (2003) Acoustic preference functions and sexual selection on the male calling song in the grasshopper Chorthippus biguttulus. Anim Behav 65(1):225–233.  https://doi.org/10.1006/anbe.2002.2034 CrossRefGoogle Scholar
  24. Koch UT, Elliott CJH, Schäffner KH, Kleindienst HU (1988) The mechanics of stridulation of the cricket Gryllus campestris. J Comp Physiol 162(2):213–223.  https://doi.org/10.1007/BF00606086 CrossRefGoogle Scholar
  25. Maan ME, Seehausen O (2011) Ecology, sexual selection and speciation. Ecol Lett 14(6):591–602.  https://doi.org/10.1111/j.1461-0248.2011.01606.x CrossRefPubMedGoogle Scholar
  26. McPeek MA, Gavrilets S (2006) The evolution of female mating preferences: differentiation from species with promiscuous males can promote speciation. Evolution (N Y) 60:1967–1980Google Scholar
  27. McPeek MA, Shen L, Torrey JZ, Farid H (2008) The tempo and mode of three-dimensional morphological evolution in male reproductive structures. Am Nat 171:E158–E178.  https://doi.org/10.1086/587076 CrossRefPubMedGoogle Scholar
  28. McPeek MA, Symes LB, Zong DM, McPeek CL (2011) Species recognition and patterns of population variation in the reproductive structures of a damselfly genus. Evolution (N Y) 65:419–428Google Scholar
  29. Mendelson TC, Shaw KL (2012) The (mis) concept of species recognition. Trends Ecol Evol 27(8):421–427.  https://doi.org/10.1016/j.tree.2012.04.001 CrossRefPubMedGoogle Scholar
  30. Mhatre N, Bhattacharya M, Robert D, Balakrishnan R (2011) Matching sender and receiver: poikilothermy and frequency tuning in a tree cricket. J Exp Biol 214(15):2569–2578.  https://doi.org/10.1242/jeb.057612 CrossRefPubMedGoogle Scholar
  31. Mhatre N, Montealegre-Z F, Balakrishnan R, Robert D (2009) Mechanical response of the tympanal membranes of the tree cricket Oecanthus henryi. J Comp Physiol A 195(5):453–462.  https://doi.org/10.1007/s00359-009-0423-x CrossRefGoogle Scholar
  32. Mhatre N, Montealegre-Z F, Balakrishnan R, Robert D (2012) Changing resonator geometry to boost sound power decouples size and song frequency in a small insect. Proc Natl Acad Sci 109:1444–1452CrossRefGoogle Scholar
  33. Mhatre N, Robert D (2013) A tympanal insect ear exploits a critical oscillator for active amplification and tuning. Curr Biol 23(19):1952–1957.  https://doi.org/10.1016/j.cub.2013.08.028 CrossRefPubMedPubMedCentralGoogle Scholar
  34. Norris K (1990) Female choice and the quality of parental care in the great tit Parus major. Behav Ecol Sociobiol 27:275–281CrossRefGoogle Scholar
  35. Oh KP, Shaw KL (2013) Multivariate sexual selection in a rapidly evolving speciation phenotype. Proc R Soc B Biol Sci 280(1761):20130482.  https://doi.org/10.1098/rspb.2013.0482 CrossRefGoogle Scholar
  36. Olvido AE, Wagner WE (2004) Signal components, acoustic preference functions and sexual selection in a cricket. Biol J Linn Soc 83(4):461–472.  https://doi.org/10.1111/j.1095-8312.2004.00404.x CrossRefGoogle Scholar
  37. Ower GD, Hunt J, Sakaluk SK (2016) Multivariate sexual selection on male tegmina in wild populations of sagebrush crickets, Cyphoderris strepitans (Orthoptera: Haglidae). J Evol Biol 30(2):338–351.  https://doi.org/10.1111/jeb.13008 CrossRefPubMedGoogle Scholar
  38. Panhuis TM, Butlin R, Zuk M, Tregenza T (2001) Sexual selection and speciation. Trends Ecol Evol 16(7):364–371.  https://doi.org/10.1016/S0169-5347(01)02160-7 CrossRefPubMedGoogle Scholar
  39. Popov A, Shuvalov V (1977) Phonotactic behavior of crickets. J Comp Physiol A Neuroethol Sensory Neural Behav Physiol 119(1):111–126.  https://doi.org/10.1007/BF00655876 CrossRefGoogle Scholar
  40. Ritchie MG (1996) The shape of female mating preferences. Proc Natl Acad Sci 93(25):14628–14631.  https://doi.org/10.1073/pnas.93.25.14628 CrossRefPubMedPubMedCentralGoogle Scholar
  41. Ritchie MG (2000) The inheritance of female preference functions in a mate recognition system. Proc R Soc Lond B Biol Sci 267(1441):327–332.  https://doi.org/10.1098/rspb.2000.1004 CrossRefGoogle Scholar
  42. Ritchie MG (2007) Sexual selection and speciation. Annu Rev Ecol Evol Syst 38:79–102CrossRefGoogle Scholar
  43. Rodríguez RL, Ramaswamy K, Cocroft RB (2006) Evidence that female preferences have shaped male signal evolution in a clade of specialized plant-feeding insects. Proc R Soc Lond B Biol Sci 273(1601):2585–2593.  https://doi.org/10.1098/rspb.2006.3635 CrossRefGoogle Scholar
  44. Rodríguez RL, Boughman JW, Gray DA, Hebets EA, Höbel G, Symes LB (2013) Diversification under sexual selection: the relative roles of mate preference strength and the degree of divergence in mate preferences. Ecol Lett 16(8):964–974.  https://doi.org/10.1111/ele.12142 CrossRefPubMedPubMedCentralGoogle Scholar
  45. Ryan MJ, Rand AS (1990) The sensory basis of sexual selection for complex calls in the túngara frog, Physalaemus pustulosus (sexual selection for sensory exploitation). Evolution (N Y) 44:305–314.  https://doi.org/10.1111/j.1558-5646.1990.tb05200.x Google Scholar
  46. Ryan MJ, Rand AS (1993) Species Recognition and Sexual Selection as a Unitary Problem in Animal Communication. Evolution (N Y) 47:647.  https://doi.org/10.2307/2410076 Google Scholar
  47. Safran RJ, Scordato ES, Symes LB, Rodríguez RL, Mendelson TC (2013) Contributions of natural and sexual selection to the evolution of premating reproductive isolation: a research agenda. Trends Ecol Evol 28(11):643–650.  https://doi.org/10.1016/j.tree.2013.08.004 CrossRefPubMedGoogle Scholar
  48. Saveer AM, Becher PG, Birgersson G et al (2014) Mate recognition and reproductive isolation in the sibling species Spodoptera littoralis and Spodoptera litura. Front Ecol Evol 2:18.  https://doi.org/10.3389/fevo.2014.00018 CrossRefGoogle Scholar
  49. Shaw KL, Herlihy DP (2000) Acoustic preference functions and song variability in the Hawaiian cricket Laupala cerasina. Proc R Soc Lond B Biol Sci 267(1443):577–584.  https://doi.org/10.1098/rspb.2000.1040 CrossRefGoogle Scholar
  50. Simmons LW, Zuk M, Rotenberry JT (2001) Geographic variation in female preference functions and male songs of the field cricket Teleogryllus oceanicus. Evolution 55(7):1386–1394.  https://doi.org/10.1111/j.0014-3820.2001.tb00660.x CrossRefPubMedGoogle Scholar
  51. Sismondo E (1979) Stridulation and tegminal resonance in the tree cricketOecanthus nigricornis (Orthoptera: Gryllidae: Oecanthinae). J Comp Physiol A Neuroethol Sensory Neural Behav Physiol 129(3):269–279.  https://doi.org/10.1007/BF00657663 CrossRefGoogle Scholar
  52. Stange N, Page RA, Ryan MJ, Taylor R (2016) Interactions between complex multisensory signal components result in unexpected mate choice responses. Anim BehavGoogle Scholar
  53. Sueur J, Aubin T, Simonis C (2008) Seewave: a free modular tool for sound analysis and synthesis. Bioacoustics 18:213–226CrossRefGoogle Scholar
  54. Symes LB (2014) Community composition affects the shape of mate response functions. Evolution 68(7):2005–2013.  https://doi.org/10.1111/evo.12415 CrossRefPubMedGoogle Scholar
  55. Symes L, Ayres M, Cowdery C, Costello R (2015) Signal diversification in Oecanthus tree crickets is shaped by energetic, morphometric, and acoustic trade-offs. Evolution 69(6):1518–1527.  https://doi.org/10.1111/evo.12668 CrossRefPubMedGoogle Scholar
  56. Talyn BC, Dowse HB (2004) The role of courtship song in sexual selection and species recognition by female Drosophila melanogaster. Anim Behav 68:1165–1180.  https://doi.org/10.1016/j.anbehav.2003.11.023 CrossRefGoogle Scholar
  57. Taylor RC, Buchanan BW, Doherty JL (2007) Sexual selection in the squirrel treefrog Hyla squirella : the role of multimodal cue assessment in female choice. Anim Behav 74(6):1753–1763.  https://doi.org/10.1016/j.anbehav.2007.03.010 CrossRefGoogle Scholar
  58. Templeton AR (1977) Analysis of Head Shape Differences Between Two Interfertile Species of Hawaiian Drosophila. Evolution (N Y) 31:630.  https://doi.org/10.1111/j.1558-5646.1977.tb01052.x Google Scholar
  59. Toms RB (1993) Incidental effects and evolution of sound-producing organs in tree crickets (Orthoptera: Oecanthidae). Int J Insect Morphol Embryol 22(2-4):207–216.  https://doi.org/10.1016/0020-7322(93)90010-X CrossRefGoogle Scholar
  60. Tyler F, Fisher D, d’Ettorre P et al (2015) Chemical cues mediate species recognition in field crickets. Front Ecol Evol 3:48.  https://doi.org/10.3389/fevo.2015.00048 CrossRefGoogle Scholar
  61. Wagner W (1998) Measuring female mating preferences. Anim Behav 55(4):1029–1042.  https://doi.org/10.1006/anbe.1997.0635 CrossRefPubMedGoogle Scholar
  62. Walker TJ (1957) Specificity in the response of female tree crickets (Orthoptera, Gryllidae, Oecanthinae) to calling songs of the males. Ann Entomol Soc Am 50(6):626–636.  https://doi.org/10.1093/aesa/50.6.626 CrossRefGoogle Scholar
  63. Walker TJ (1963) The taxonomy and calling songs of United States tree crickets (Orthoptera: Gryllidae: Oecanthinae). II. The nigricornis group of the genus Oecanthus. Ann Entomol Soc Am 56(6):772–789.  https://doi.org/10.1093/aesa/56.6.772 CrossRefGoogle Scholar
  64. Walker TJ (1974) Character displacement and acoustic insects. Am Zool 14(4):1137–1150.  https://doi.org/10.1093/icb/14.4.1137 CrossRefGoogle Scholar
  65. Walker TJ (2000) Pulse rates in the songs of trilling field crickets (Orthoptera: Gryllidae: Gryllus). Ann Entomol Soc Am 93(3):565–572.Google Scholar
  66. Whattam EM, Bertram SM (2011) Effects of juvenile and adult condition on long-distance call components in the Jamaican field cricket, Gryllus assimilis. Anim Behav 81(1):135–144.  https://doi.org/10.1016/j.anbehav.2010.09.024 CrossRefGoogle Scholar
  67. Zuk M, Johnsen TS, Maclarty T (1995) Endocrine-immune interactions, ornaments and mate choice in red jungle fowl. Proc R Soc Lond B Biol Sci 260(1358):205–210.  https://doi.org/10.1098/rspb.1995.0081 CrossRefGoogle Scholar
  68. Zuk M, Rebar D, Scott SP (2008) Courtship song is more variable than calling song in the field cricket Teleogryllus oceanicus. Anim Behav 76:1065–1071.  https://doi.org/10.1016/j.anbehav.2008.02.018 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Biological SciencesDartmouth CollegeHanoverUSA

Personalised recommendations