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Journal of Insect Behavior

, Volume 28, Issue 4, pp 369–386 | Cite as

Mating Behavior and Spermatophore Characteristics in Two Closely Related Bushcricket Species of the Genus Phonochorion (Orthoptera: Phaneropterinae)

  • Hasan SevgiliEmail author
  • Hülya Önal
  • Arzu Yiğit
Article

Abstract

Bushcrickets comprise an important group of model organisms, which are intensively studied to understand the evolution of mating behavior. During the mating process, the male bushcricket transfers a costly and edible spermatophore consisting of two parts to the female. This unique behavior makes bushcricket species appropriate study organisms for investigating spermatophore size variations across entire bushcricket family (Tettigoniidae). The functions of the spermatophylax and the ampulla, which constitute the spermatophore, have been addressed in many studies. Although the costs and benefits of mating for male and female bushcrickets may vary depending on species, there are some common evolutionary traits. In the present study, mating behaviors and spermatophore characteristics of two endemic bushcricket species, Phonochorion uvarovi and P. artvinensis, distributed at the high altitudes of the Kaçkar Mountains, northeastern Turkey, were examined. The data on two closely related species belonging to the genus of Phonochorion show that they have different reproductive investments in terms of spermatophore and sperm numbers in spite of similar habitat and nutritional preferences. P. artvinensis had a larger spermatophore, spermatophylax and ampulla, but transferred fewer sperm. Male age and weight had a significant effect on spermatophore, spermatophylax and ampulla investments in P. uvarovi while only male weight was a significant factor in P. artvinensis. A positive relationship between the spermatophylax and the ampulla weights in both species supports the ejaculate protection hypothesis in the Phonochorion species. Even though further studies on Phonochorion should be conducted to provide a more clear comparison with other groups in the barbitistine, this study demonstrates that both P. uvarovi and P. artvinensis make little spermatophore investment relative to their body size in comparison to other barbitistines.

Keywords

Spermatophore sperm number mating bushcricket Barbitistini Phonochorion orthoptera Turkey 

Notes

Acknowledgments

This research was partly supported by Ordu University (Scientific Research Projects Coordination Unit, TF-1201). We thank Gülşah Yılmaz for assistance with collecting bushcrickets and animal maintenance. Thanks to Hüseyin Sevgili for statistical advice and discussion. We also thank Klaus-Gerhard Heller, Klaus Reinhold, Ian Kutch, Molly Grace and anonymous referees for their comments on an earlier version of the manuscript.

References

  1. Andersson M (1986) Evolution of condition-dependent sex ornaments and mating references: sexual selection based on viability differences. Evolution 40:804–816CrossRefGoogle Scholar
  2. Andersson M (1994) Sexual selection. Princeton University Press, PrincetonGoogle Scholar
  3. Arnoud L, Haubruge E, Gage MJG (2001) Sperm size and number variation in the red flour beetle. Zool J Linn Soc 133:369–375CrossRefGoogle Scholar
  4. Boldyrev BT (1915) Contributions à l’étude de la structure des spermatophores et des particularitès de la copulation chez Locustodea et Gryllodea. Hor Soc Ent Ross 6:1–245Google Scholar
  5. Bolker BM, Brooks ME, Clark CJ, Geange SW, Poulsen JR, Stevens MHH, White JSS (2008) Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol 24:127–135CrossRefGoogle Scholar
  6. Busnel RG, Dumortier B (1955) Rapport entre la vitesse de de’placement et l’intensite’ du stimulus dans le comportement acoustico-sexuel de la femelle d’Ephippiger bitterensis. Se’ance 1956: 174–177Google Scholar
  7. Can E (1959) Zur Kenntnis von Isophya amplipennis Br.v.W. I. pavelii Br.v.W. und I. tenuicerca Rme. (Orth. Tettigoniidae), als Schädlinge von EichenniederwäIdern in Südosteuropa. Teil I. Teil II. [Isophya amplipennis, I. pavelii and I. tenuicerca as pests of oak scrub in South-East Europe]. Z Angew Entomol 43:387–411CrossRefGoogle Scholar
  8. Cook PA, Wedell N (1996) Ejaculate dynamics in butterflies: a strategy for maximizing fertilization success? Proc R Soc Lond B: Biol 263:1047–1051CrossRefGoogle Scholar
  9. Eades DC, Otte D, Cigliano MM, Braun H (2014) Orthoptera species file. Version 5.0/5.0. [retrieval date]. http://Orthoptera.SpeciesFile.org
  10. Eberhard WG (1996) Female control: sexual selection by cryptic female choice. Princeton University Press, New JerseyGoogle Scholar
  11. Engqvist L (2007) Nuptial gift consumption influences female remating in a scorpiomfly: male or female control of mating rate? Evol Ecol 21:49–61CrossRefGoogle Scholar
  12. Fedorka KM, Mousseau TA (2002) Nuptial gifts and the evolution of male body size. Evolution 56:590–596CrossRefPubMedGoogle Scholar
  13. Fisher RA (1958) The genetical theory of natural selection. Dover, New YorkGoogle Scholar
  14. Fleischman RR, Sakaluk SK (2004) Sexual conflict over remating in house crickets: no evidence of an anti-aphrodisiac in males’ ejaculates. Behaviour 141:633–646CrossRefGoogle Scholar
  15. Gage MJG (1994) Associations between body size, mating pattern, testis size and sperm lengths across butterflies. Proc R Soc Lond B: Biol 258:247–253CrossRefGoogle Scholar
  16. Gage MJG, Cook PA (1994) Sperm size or numbers? Effects of nutritional stress upon eupyrene and apyrene sperm production strategies in the moth Plodia interpunctella (Lepidoptera: Pyralidae). Funct Ecol 8:594–599CrossRefGoogle Scholar
  17. Gao Y, Kang L (2006) Operational sex ratio and alternative reproductive behaviours in Chinese bushcricket, Gampsocleis gratiosa. Ethology 112:325–331CrossRefGoogle Scholar
  18. Gerhardt U (1913) Copulation und spermatophoren von Grylliden und Locustiden II. Zool Jahrb (Syst) 35:415–532Google Scholar
  19. Gerhardt U (1914) Copulation und spermatophoren von Grylliden und Locustiden I. Zool Jahrb (Syst) 37:1–64Google Scholar
  20. Gwynne DT (1981) Sexual difference theory: Mormon crickets show role reversal in mate choice. Science 213:779–780CrossRefPubMedGoogle Scholar
  21. Gwynne DT (1984) Courtship feding increases female reproductive success in bushcrickets. Nature 307:361–362CrossRefGoogle Scholar
  22. Gwynne DT (1988) Courtship feeding and the fitness of female katydids. Evolution 42:545–555CrossRefGoogle Scholar
  23. Gwynne DT (1990) The katydid spermatophore: evolution of a parental investment. In: Bailey WJ, Rentz DC (eds) The tettigoniidae: biology, Systematics and evolution. Crawford House, Bathurst, pp 9–27Google Scholar
  24. Gwynne DT (1995) Variation in bushcricket nuptial gifts may be due to common ancestry rather than ecology as taxonomy and diet are almost perfectly confounded. Behav Ecol 6:458CrossRefGoogle Scholar
  25. Gwynne DT (2001) Katydids and Bushcrickets: reproductive Behavior and the evolution of the Tettigoniidae. Cornell University Press, IthakaGoogle Scholar
  26. Gwynne DT (2008) Sexual conflict over nuptial gifts in insects. Annu Rev Entomol 53:83–101CrossRefPubMedGoogle Scholar
  27. Gwynne DT, Bowen BJ, Codd CG (1984) The function of the katydid spermatophore and its role in fecundity and insemination (Orthoptera: Tettigoniidae). Aust J Zool 32:15–22CrossRefGoogle Scholar
  28. Heller KG (1990) Evolution of song pattern in East Mediterranean Phaneropterinae: constraints by the communication system. In: Bailey WJ, Rentz DC (eds) The Tettigoniidae: biology, Systematics and evolution. Crawford House, Bathurst, pp 130–151CrossRefGoogle Scholar
  29. Heller KG, Reinhold K (1994) Matting effort function of the spermatophore in the bushcricket Poecilimon veluchianus (Orthoptera, Phaneropteridae): support from a comparison of the mating behaviour of two species. Biol J Linn Soc 53:153–163CrossRefGoogle Scholar
  30. Heller KG, von Helversen D (1991) Operational sex ratio and individual mating frequences in two bushcricket species (Orthoptera, Tettigonioidea, Poecilimon). Ethology 89:211–228CrossRefGoogle Scholar
  31. Heller KG, Faltin S, Fleischmann P, von Helversen O (1998) The chemical composition of the spermatophore in some species of phaneropterid bush crickets (Orthoptera: Tettigoniidae). J Insect Physiol 44:1001–1008CrossRefPubMedGoogle Scholar
  32. Heller KG, Willemse F, Sevgili H (2004) Poecilimon mytilenensis Werner, a polytypic phaneropterid bushcricket from the Aegean island of Lesbos (Orthoptera, Tettigonioidea), differing in male mating structures. J Orthop Res 13:221–230CrossRefGoogle Scholar
  33. Kerr AM, Gershman SN, Sakaluk SK (2010) Experimentally induced spermatophore production and immune responses reveal a trade-off in crickets. Behav Ecol 21:647–654CrossRefGoogle Scholar
  34. Lehmann GUC (2012) Weighing costs and benefits of mating in bushcrickets (Insecta: Orthoptera: Tettigoniidae), with an emphasis on nuptial gifts, protandry and mate density. Front Zool 9:19PubMedCentralCrossRefPubMedGoogle Scholar
  35. Lehmann GUC, Lehmann AW (2009) Condition-dependent spermatophore size is correlated with male’s age in abushcricket (Orthoptera: Phaneropteridae). Biol J Linn Soc 96:354–360CrossRefGoogle Scholar
  36. McCartney J, Heller KG, Potter MA, Robertson AW, Telscher K, Lehmann GUC, Lehmann AW, von Helversen D, Reinhold K, Achmann R (2008) Understanding nuptial gift size in bushcrickets: an analysis of the genus Poecilimon (Tettigoniidae; Orthoptera). J Orthop Res 17:231–242CrossRefGoogle Scholar
  37. McCartney J, Lehmann AW, Lehmann GUC (2010) Lifetime spermatophore investment in natural populations of two closely related bush-cricket species (Orthoptera: Tettigoniidae: Poecilimon). Behaviour 147:285–298CrossRefGoogle Scholar
  38. McCartney J, Kokko H, Heller KG, Gwynne DT (2011) The evolution of sex differences in mate searching when females benefit: new theory and a comparative test. Proc R Soc Lond B: Biol 279:1225–1232CrossRefGoogle Scholar
  39. McCartney J, Potter MA, Robertson AW, Heller KG, Gwynne DT (2013) Evidence of natural and sexual selection shaping the size of nuptial gifts among a bushcricket genus (Poecilimon; Tettigoniidae): an analysis of sperm transfer patterns. In: Geldani R, Davin M (eds) Sexual selection: evolutionary perspectives, mating strategies and long-term effects on genetic variation. Nova Science Publishing, pp 45–68Google Scholar
  40. Møller AP, Jennions MD (2001) How important are direct fitness benefits of sexual selection? Naturwissenschaften 88:401–415CrossRefPubMedGoogle Scholar
  41. Reinhold K (1994) Inheritance of body and testis in the bushcricket Poecilimon veluchianus Ramme (Orthoptera, Tettigoniidae) examined by means of subspecies hybrids. Biol J Linn Soc 52:305–316CrossRefGoogle Scholar
  42. Reinhold K (1999) Paternal investment in Poecilimon veluchianus bushcrickets: beneficial effects of nuptial feding on offspring viability. Behav Ecol Sociobiol 45:293–299CrossRefGoogle Scholar
  43. Reinhold K, Heller KG (1993) The ultimate function of nuptial feding in the bushcricket Poecilimon veluchianus (Orthoptera: Tettigoniidae: Phaneropterinae). Behav Ecol Sociobiol 45:293–299CrossRefGoogle Scholar
  44. Reinhold K, von Helversen D (1997) Sperm number, spermatophore weight and remating in the bushcricket Poecilimon veluchianus. Ethology 103:12–18CrossRefGoogle Scholar
  45. Roth S, Reinhardt K (2003) Facultative sperm storage in response to nutritional status in a female insect. Proc R Soc Lond B: Biol 270:54–56CrossRefGoogle Scholar
  46. Sakaluk SK (1987) Reproductive behaviour of the decorated crickets Gryllodes supplicans (Orthoptera: Gryllidae): calling schedules, spatial distribution and mating. Behaviour 100:202–225CrossRefGoogle Scholar
  47. Schaus JM, Sakaluk SK (2001) Ejaculate expenditures of male crickets in response to varying risk and intensity of sperm competition: not all species play games. Behav Ecol 12:740–745CrossRefGoogle Scholar
  48. Sevgili H (2004) A revision of Turkish species of Isophya Brunner von Wattenwyl (Orthoptera: Tettigoniidae: Phaneropterinae). PhD Thesis, Hacettepe University, Ankara, pp 1–387Google Scholar
  49. Sevgili H, Reinhold K (2007) No evidence for strategic male mating effort in response to female weight in a bushcricket. Behaviour 144:1179–1192CrossRefGoogle Scholar
  50. Sevgili H, Çağlar SS, Sağlam İK (2010) Re-evaluation of the genus Phonochorion (Orthoptera: Tettigoniidae: Phaneropterinae). Eur J Entomol 107:631–645CrossRefGoogle Scholar
  51. Sevgili H, Demirsoy A, Çıplak B (2012) Description and bioacoustics of a new species of the genus Isophya (Orthoptera: Tettigoniidae: Phaneropterinae) from Turkey. Zootaxa 3361:33–44Google Scholar
  52. Simmons LW (1990) Nuptial feeding in tettigoniids: male costs and rates of fecundity increase. Behav Ecol Sociobiol 27:43–47CrossRefGoogle Scholar
  53. Simmons LW, Gwynne DT (1991) The refractory period of female katydids (Orthoptera: Tettigoniidae): sexual conflict over the remating interval? Behav Ecol 2:267–282CrossRefGoogle Scholar
  54. Simmons LW, Parker GA (1989) Nuptial feeding in insects: mating effort versus paternal investment. Ethology 81:332–343CrossRefGoogle Scholar
  55. Simmons LW, Craig M, Llorens T, Schinzig M, Hosken D (1993) Bushcricket spermatophores vary in accord with sperm competition and parental investment theory. Proc R Soc Lond B: Biol 251:183–186CrossRefGoogle Scholar
  56. Thornhill R (1976) Sexual selection and nuptial feeding behavior in Bittacus apicalis (Insecta: Mecoptera). Am Nat 110:529–548CrossRefGoogle Scholar
  57. Thornhill R, Alcock J (1983) The evolution of insect mating systems. Harward University Press, CambridgeCrossRefGoogle Scholar
  58. Ullrich B, Reinhold K, Niehuis O, Misof B (2010) Secondary structure and phylogenetic analysis of the internal transcribed spacers 1 and 2 of bush crickets (Orthoptera: Tettigoniidae: Barbitistini). J Zool Syst Evol Res 48:219–228Google Scholar
  59. Uma R, Sevgili H (2015) Spermatophore allocation strategy over successive matings in the bushcricket Isophya sikorai (Orthoptera: Phaneropterinae). Ethol Ecol Evol 27:129–147CrossRefGoogle Scholar
  60. Vahed K (1995) The evolution and function of the spermatophylax in bushcrickets (Orthoptera: Tettigoniidae). PhD thesis, University of Nottingham, UKGoogle Scholar
  61. Vahed K (1998) The function of nuptial feeding in insects: a review of empirical studies. Biol Rev 73:43–78CrossRefGoogle Scholar
  62. Vahed K (2002) Coercive copulation in the Alpine bushcricket Anonconotus alpinus Yersin (Tettigoniidae: Tettigoniinae: Platycleidini). Ethology 108:1065–1075CrossRefGoogle Scholar
  63. Vahed K (2007) Comparative evidence for a cost to males of manipulating females in bushcrickets. Behav Ecol 18:105–127CrossRefGoogle Scholar
  64. Vahed K, Gilbert FS (1996) Differences across taxa in nuptial gift size correlate w, ith differences in sperm number and ejaculate volume in bushcrickets (Orthoptera: Tettigoniidae). Proc R Soc Lond B: Biol 263:1257–1265CrossRefGoogle Scholar
  65. Voigt CC, Kunz TH, Michener R (2005) The energetics of trading nuptial gifts with copulations in katydids. Physiol Biochem Zool 78:417–423CrossRefPubMedGoogle Scholar
  66. von Helversen D, von Helversen O (1991) Pre-mating sperm removal in the bushcricket Metaplastes ornatus Ramme, 1931 (Orthoptera: Tettigonioidea, Phaneropteridae). Behav Ecol Sociobiol 28:391–396CrossRefGoogle Scholar
  67. Wedell N (1993) Spermatophore size in bushcrickets: comparative evidence for nuptial gifts as a sperm protection device. Evolution 47:1203–1212CrossRefGoogle Scholar
  68. Wedell N (1994) Dual function of the bushcricket spermatophore. Proc R Soc Lond B: Biol 258:181–185CrossRefGoogle Scholar
  69. Wedell N (1997) Ejaculate size in bushcrickets: the importance of being large. J Evol Biol 10:315–325CrossRefGoogle Scholar
  70. Wedell N, Arak A (1989) The wartbiter spermatophore and its effect on female reproductive output (Orthoptera: Tettigoniidae, Decticus verrucivorus). Behav Ecol Sociobiol 24:117–125CrossRefGoogle Scholar
  71. Wedell N, Ritchie MG (2004) Male age, mating status and nuptial gift quality in a bushcricket. Anim Behav 67:1059–1065CrossRefGoogle Scholar
  72. Wedell N, Sandberg T (1995) Female preference for large males in the bushcricket Requena sp. 5 (Orthoptera: Tettigoniidae). J Insect Behav 8:513–522CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  1. 1.Faculty of Arts & Sciences, Department of BiologyOrdu UniversityOrduTurkey

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