Behavioral Ecology and Sociobiology

, Volume 67, Issue 2, pp 273–281 | Cite as

Influence of mating order on courtship displays and stored sperm utilization in Hermann's tortoises (Testudo hermanni hermanni)

  • Giulia Cutuli
  • Stefano Cannicci
  • Marco Vannini
  • Sara Fratini
Original Paper

Abstract

Sperm storage is widespread in many vertebrate groups, and it is frequently associated with promiscuous mating systems. Chelonian species are one of the most outstanding examples of a promiscuous group capable of long-term sperm storage; specialized structures have evolved within the oviducts of these vertebrates to ensure sperm vitality across reproductive cycles. Thus far, few studies have investigated the factors regulating multiple paternity, sperm usage by females and paternity distribution in successive clutches. This study aimed to investigate the effect of mating order on male mounting and reproductive success in Testudo hermanni hermanni, combining behavioural and genetic data. A series of planned matings were performed, within which experimental females were mated sequentially to two different males under controlled conditions. Observations conducted during experimental matings revealed that courtship displays did not significantly differ between the first and second males to mate with a female. Interactions ending with a mount were characterized by a significantly higher intensity and occurrence of determinate courtship behaviours, for example biting and running after the female. Paternity analysis performed on hatchlings produced from experimental females revealed that 46 % of the clutches were multi-sired. A significant contribution of previous years' partners was still found, thus confirming the long-term sperm storage within the female oviduct in this species. Finally, mating order did not significantly affect the reproductive success of experimental males during the on-going reproductive season.

Keywords

Testudo hermanni Mating success Sperm storage Female promiscuity Paternity distribution 

References

  1. Anderson MJ, Gorley RN, Clarke KR (2008) PERMANOVA + for PRIMER: guide to software and statistical methods. PRIMER-E Ltd, PlymouthGoogle Scholar
  2. Baer B, Schmid-Hempel P, Høeg JT, Boomsma JJ (2003) Sperm length, sperm storage and mating system characteristics in bumblebees. Insect Soc 50:101–108CrossRefGoogle Scholar
  3. Birkhead TR (1998a) Sperm competition in birds: mechanisms and function. In: Birkhead TR, Møller AP (eds) Sperm competition and sexual selection. Academic, San Diego, pp 579–612CrossRefGoogle Scholar
  4. Birkhead TR (1998b) Cryptic female choice: criteria for establishing female sperm choice. Evolution 52:1212–1218CrossRefGoogle Scholar
  5. Birkhead TR, Biggins JD (1998) Sperm competition mechanisms in birds: models and data. Behav Ecol 9:253–260CrossRefGoogle Scholar
  6. Birkhead TR, Møller AP (1992a) Sperm competition in birds: evolutionary causes and consequences. Academic, LondonGoogle Scholar
  7. Birkhead TR, Møller AP (1992b) Number and size of sperm storage tubules and the duration of sperm storage in birds: a comparative study. Biol J Linn Soc 45:363–372CrossRefGoogle Scholar
  8. Birkhead TR, Møller AP (1993) Sexual selection and the temporal separation of reproductive events: sperm storage data from reptiles, birds and mammals. Biol J Linn Soc 50:295–311CrossRefGoogle Scholar
  9. Boorman E, Parker GA (1976) Sperm (ejaculate) competition in Drosophila melanogaster, and the reproductive value of females to males in relation to female age and mating status. Ecol Entomol 1:145–155CrossRefGoogle Scholar
  10. Briskie JV (1996) Spatiotemporal patterns of sperm storage and last-male sperm precedence in birds. Funct Ecol 10:375–383CrossRefGoogle Scholar
  11. Broquet T, Berset-Braendli L, Emaresi G, Fumagalli L (2007) Buccal swabs allow efficient and reliable microsatellite genotyping in amphibians. Conserv Genet 8:509–511CrossRefGoogle Scholar
  12. Chevrier C, Bressac C (2002) Sperm storage and use after multiple mating in Dinarmus basalis (Hymenoptera: Pteromalidae). J Insect Behav 15:385–398CrossRefGoogle Scholar
  13. Clarke KR, Gorley RN (2006) PRIMER v.6: user manual/tutorial. PRIMER-E, PlymouthGoogle Scholar
  14. Córdoba-Aguilar A, Uhia E, Cordero-Rivera A (2003) Sperm competition in Odonata (Insecta): the evolution of female sperm storage and rivals' sperm displacement. J Zool 261:381–398CrossRefGoogle Scholar
  15. Cutuli G, Pierpaoli M, Cardoso S, Vannini M, Fratini S (2012) Cross-amplification of microsatellite loci for species of the genus Testudo. Herpetol J 22:195–198Google Scholar
  16. Davy CM, Edwards T, Lathrop A, Bratton M, Hagan M, Henen B, Nagy KA, Stone J, Hillard LS, Murphy RW (2011) Polyandry and multiple paternities in the threatened Agassiz's desert tortoise, Gopherus agassizii. Conserv Genet 12:1313–1322CrossRefGoogle Scholar
  17. Diesel R (1989) Structure and function of the reproductive system of the symbiotic spider crab Inachus phalangium (Decapoda: Majidae): observations on sperm transfer, sperm storage, and spawning. J Crustac Biol 9:266–277CrossRefGoogle Scholar
  18. Eberhard WG (1996) Female control: sexual selection by cryptic female choice. Princeton University Press, PrincetonGoogle Scholar
  19. Eberhard WG (1998) Female roles in sperm competition. In: Birkhead TR, Møller AP (eds) Sperm competition and sexual selection. Academic, San Diego, pp 91–116CrossRefGoogle Scholar
  20. Ernst CH, Barbour RW (1989) Turtles of the world. Smithsonian Institution, Washington, DCGoogle Scholar
  21. Fitzsimmons NN (1998) Single paternity of clutches and sperm storage in the promiscuous green sea turtle (Chelonia mydas). Mol Ecol 7:575–584PubMedCrossRefGoogle Scholar
  22. Franck P, Solignac M, Vautrin D, Cornuet JM, Koeniger G, Koeniger N (2002) Sperm competition and last-male precedence in the honeybee. Anim Behav 64:503–509CrossRefGoogle Scholar
  23. Galeotti P, Sacchi R, Pellitteri-Rosa D, Fasola M (2004) Female preference for fast-rate, high-pitched calls in Hermann's tortoises Testudo hermanni. Behav Ecol 16:301–308CrossRefGoogle Scholar
  24. Galeotti P, Sacchi R, Fasola M, Pellitteri-Rosa D, Marchesi M, Ballasina D (2005a) Courtship displays and mounting calls are honest, condition-dependent signals that influence mounting success in Hermann's tortoises. Can J Zool 83:1306–1313CrossRefGoogle Scholar
  25. Galeotti P, Sacchi R, Fasola M, Ballasina D (2005b) Do mounting vocalizations in tortoises have a communication function? A comparative analysis. Herpetol J 15:61–71Google Scholar
  26. Galeotti P, Sacchi R, Pellitteri-Rosa D, Fasola M (2007) Olfactory discrimination of species, sex, and sexual maturity by the Hermann's tortoise Testudo hermanni. Copeia 2007:980–985CrossRefGoogle Scholar
  27. Girling JE (2002) The reptilian oviduct: a review of structure and function and directions for future research. J Exp Zool 293:141–170PubMedCrossRefGoogle Scholar
  28. Gist DH, Congdon JD (1998) Oviductal sperm storage as a reproductive tactic of turtles. J Exp Zool 282:526–534Google Scholar
  29. Gist DH, Fisher EN (1993) Fine structure of the sperm storage tubules in the box turtle oviduct. J Reprod Fertil 97:463–468PubMedCrossRefGoogle Scholar
  30. Gist DH, Jones JM (1987) Storage of sperm in the reptilian oviduct. Scanning Microsc 1:1839–1849PubMedGoogle Scholar
  31. Gist DH, Jones JM (1989) Sperm storage within the oviduct of turtles. J Morphol 199:379–384CrossRefGoogle Scholar
  32. Griffith SC, Owens IPF, Thuman KA (2002) Extra pair paternity in birds: a review of interspecific variation and adaptive function. Mol Ecol 11:2195–2212PubMedCrossRefGoogle Scholar
  33. Harry JL, Briscoe DA (1988) Multiple paternity in the loggerhead turtle (Caretta caretta). J Hered 79:96–99PubMedGoogle Scholar
  34. Harshman LG, Prout T (1994) Sperm displacement without sperm transfer in Drosophila melanogaster. Evolution 48:758–766CrossRefGoogle Scholar
  35. Howarth B (1974) Sperm storage as a function of the female reproductive tract. In: Johnson AD, Foley CE (eds) The oviduct and its functions. Academic, New York, pp 237–270CrossRefGoogle Scholar
  36. Johnston EE, Rand MS, Zweifel SG (2006) Detection of multiple paternity and sperm storage in a captive colony of the central Asian tortoise, Testudo horsfieldii. Can J Zool 84:520–526CrossRefGoogle Scholar
  37. Kalinowski ST, Taper ML, Marshall TC (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol 16:1099–1106PubMedCrossRefGoogle Scholar
  38. Kichler K, Holder MT, Davis SK, Marquez R, Owens DW (1999) Detection of multiple paternity in the Kemp's ridley sea turtle with limited sampling. Mol Ecol 8:819–830CrossRefGoogle Scholar
  39. Klowden MJ (2003) Spermatheca. In: Resh VH, Cardé RT (eds) Encyclopedia of insects. Academic, San Diego, pp 1058–1059Google Scholar
  40. Kraaijeveld-Smit FJL, Ward SJ, Temple-Smith PD, Paetkau D (2002) Factors influencing paternity success in Antechinus agilis: last-male sperm precedence, timing of mating and genetic compatibility. J Evol Biol 15:100–107CrossRefGoogle Scholar
  41. Kuchling G (1999) The reproductive biology of the Chelonia. Springer, BerlinCrossRefGoogle Scholar
  42. Lessells CM, Birkhead TR (1990) Mechanisms of sperm competition in birds: mathematical models. Behav Ecol Sociobiol 27:325–337CrossRefGoogle Scholar
  43. Liem KL, Bemis WE, Walker WF, Grande L (2001) Functional anatomy of the vertebrates: an evolutionary perspective, 3rd edn. Brooks/Cole-Thomson Learning, BelmontGoogle Scholar
  44. Loman J, Madsen T, Hakansson T (1988) Increased fitness from multiple mating, and genetic heterogeneity: a model of a possible mechanism. Oikos 52:69–72CrossRefGoogle Scholar
  45. Loy A, Cianfrani C (2010) The ecology of Eurotestudo h. hermanni in a mesic area of southern Italy: first evidence of sperm storage. Ethol Ecol Evol 22:1–16CrossRefGoogle Scholar
  46. Marshall TC, Slate J, Kruuk LEB, Pemberton JM (1998) Statistical confidence for likelihood-based paternity inference in natural populations. Mol Ecol 7:639–655PubMedCrossRefGoogle Scholar
  47. Olsson M, Madsen T (1995) Female choice on male quantitative traits in lizards—why is it so rare? Behav Ecol Sociobiol 36:179–184CrossRefGoogle Scholar
  48. Olsson M, Madsen T (1996) Costs of mating with infertile males selects for late emergence in female sand lizards. Copeia 1996:462–464CrossRefGoogle Scholar
  49. Olsson M, Madsen T (1998) Sexual selection and sperm competition in reptiles. In: Birkhead TR, Møller AP (eds) Sperm competition and sexual selection. Academic, Cambridge, pp 503–578CrossRefGoogle Scholar
  50. Olsson M, Shine R, Madsen T, Gullberg A, Tegelstrom H (1996) Sperm selection by females. Nature 383:585CrossRefGoogle Scholar
  51. Palmer KS, Rostal DC, Grumbles JS, Mulvey M (1998) Long-term sperm storage in the desert tortoise (Gopherus agassizii). Copeia 1998:702–705CrossRefGoogle Scholar
  52. Parker GA (1970) Sperm competition and its evolutionary consequences in the insects. Biol Rev 45:525–567CrossRefGoogle Scholar
  53. Parker GA (1990) Sperm competition games. Raffles and Roles. Proc R Soc Lond B 242:120–126CrossRefGoogle Scholar
  54. Parker GA, Simmons LW (1991) A model of constant random sperm displacement during mating: evidence from Scatophaga. Proc R Soc Lond B 246:107–115CrossRefGoogle Scholar
  55. Pearse DE, Avise JC (2001) Turtle mating systems: behaviour, sperm storage, and genetic paternity. J Hered 92:206–211PubMedCrossRefGoogle Scholar
  56. Pearse DE, Janzen FJ, Avise JC (2001) Genetic markers substantiate long-term storage and utilization of sperm by female painted turtles. Heredity 86:378–384PubMedCrossRefGoogle Scholar
  57. Pearse DE, Janzen FJ, Avise JC (2002) Multiple paternity, sperm storage, and reproductive success of female and male painted turtles (Chrysemys picta) in nature. Behav Ecol Sociobiol 51:164–171CrossRefGoogle Scholar
  58. Pellitteri-Rosa D, Sacchi R, Galeotti P, Marchesi M, Fasola M (2011) Courtship displays are condition-dependent signals that reliably reflect male quality in Greek tortoises, Testudo graeca. Chelonian Conserv Biol 10:10–17CrossRefGoogle Scholar
  59. Poschadel JR, Møller D (2004) A versatile field method for tissue sampling on small reptiles and amphibians applied to pond turtles, newts, frogs and toads. Conserv Genet 5:865–867CrossRefGoogle Scholar
  60. Racey PA (1979) The prolonged storage and survival of spermatozoa in Chiroptera. J Reprod Fertil 56:391–402PubMedCrossRefGoogle Scholar
  61. Raveh S, Heg D, Dobson FS, Coltman DW, Gorrel JC, Balmer A, Neuhaus P (2010) Mating order and reproductive success in male Columbian ground squirrels (Urocitellus columbianus). Behav Ecol 21:537–547CrossRefGoogle Scholar
  62. Roig J, Carretero MA, Llorente GA (2000) Reproductive cycle in a Pyrenean oviparous population of the common lizard (Zootoca vivipara). Neth J Zool 50:15–27Google Scholar
  63. Roques S, Diaz-Paniagua C, Andreu AC (2004) Microsatellite markers reveal multiple paternity and sperm storage in the Mediterranean spur-thighed tortoise, Testudo graeca. Can J Zool 82:153–159CrossRefGoogle Scholar
  64. Sacchi R, Galeotti P, Fasola M, Ballasina D (2003) Vocalizations and courtship intensity correlate with mounting success in marginated tortoises, Testudo marginata. Behav Ecol Sociobiol 55:95–102CrossRefGoogle Scholar
  65. Sakaoka K, Yoshii M, Okamoto H, Sakai F, Nagasawa K (2011) Sperm utilization patterns and reproductive success in captive loggerhead turtles (Caretta caretta). Chelonian Conserv Biol 10:62–72CrossRefGoogle Scholar
  66. Swingland I, Stubbs D (1985) The ecology of a Mediterranean tortoise (Testudo hermanni): reproduction. J Zool Lond 205:595–610CrossRefGoogle Scholar
  67. Taylor PH, Kaspi ROY, Yuval B (2000) Copula duration and sperm storage in Mediterranean fruit flies from a wild population. Physiol Entomol 25:94–99CrossRefGoogle Scholar
  68. Theissinger K, Fitzsimmons NN, Limpus CJ, Parmenter CJ, Phillot AD (2009) Mating system, multiple paternity and effective population size in the endemic flatback turtle (Natator depressus) in Australia. Conserv Genet 10:329–346CrossRefGoogle Scholar
  69. Uller T, Ollson M (2008) Multiple paternity in reptiles: patterns and processes. Mol Ecol 17:2566–2580PubMedCrossRefGoogle Scholar
  70. Walker WF (1980) Sperm utilization strategies in nonsocial insects. Am Nat 115:780–799CrossRefGoogle Scholar
  71. Weaver WGJ (1970) Courtship and combat behavior in Gophems berlanderi. Bull Fla State Mus 15:1–43Google Scholar
  72. Wingfield JC (1999) Minor manipulative procedures. In: Gaunt AS, Oring LW (eds) Guidelines to the use of wild birds in research, 2nd edn. The Ornithological Council, Washington DC, pp 29–33Google Scholar
  73. Xiangkun H, Li Z, Meiying L, Huijun B, Nainan H, Qiusheng C (2008) Ultrastructure of anterior uterus of the oviduct and the stored sperm in female soft-shelled turtle, Trionyx sinensis. Anat Rec 291:335–351CrossRefGoogle Scholar
  74. Zeh JA, Zeh DW (1996) The evolution of polyandry. I. Intragenomic incompatibility. Proc R Soc Lond B 263:1711–1717CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  • Giulia Cutuli
    • 1
  • Stefano Cannicci
    • 1
  • Marco Vannini
    • 1
  • Sara Fratini
    • 1
  1. 1.Department of Evolutionary BiologyUniversity of FlorenceFlorenceItaly

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