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

Behavioral Ecology and Sociobiology

Volumn 67, Issue 2, 2013, Pages 273-281

  Cutuli, Giulia ^a   Cannicci, Stefano ^a   Vannini, Marco ^a   Fratini, Sara ^a  

^a UNIVERSITY OF FLORENCE   (Italy)

Author keywords

Female promiscuity; Mating success; Paternity distribution; Sperm storage; Testudo hermanni

Indexed keywords

COURTSHIP; PATERNITY; REPRODUCTIVE CYCLE; REPRODUCTIVE STRATEGY; REPRODUCTIVE SUCCESS; SPERM; TURTLE;

TESTUDINES; TESTUDINIDAE; TESTUDO HERMANNI; TESTUDO HERMANNI HERMANNI; VERTEBRATA;

EID: 84872372514     PISSN: 03405443     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00265-012-1447-8     Document Type: Article

References (74)

1. Anderson MJ, Gorley RN, Clarke KR (2008) PERMANOVA + for PRIMER: guide to software and statistical methods. PRIMER-E Ltd, Plymouth.
2. Baer B, Schmid-Hempel P, Høeg JT, Boomsma JJ (2003) Sperm length, sperm storage and mating system characteristics in bumblebees. Insect Soc 50: 101-108.
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 579-612.
4. Birkhead TR (1998b) Cryptic female choice: criteria for establishing female sperm choice. Evolution 52: 1212-1218.
5. Birkhead TR, Biggins JD (1998) Sperm competition mechanisms in birds: models and data. Behav Ecol 9: 253-260.
6. Birkhead TR, Møller AP (1992a) Sperm competition in birds: evolutionary causes and consequences. Academic, London.
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: 363-372.
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: 295-311.
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: 145-155.
10. Briskie JV (1996) Spatiotemporal patterns of sperm storage and last-male sperm precedence in birds. Funct Ecol 10: 375-383.
11. Broquet T, Berset-Braendli L, Emaresi G, Fumagalli L (2007) Buccal swabs allow efficient and reliable microsatellite genotyping in amphibians. Conserv Genet 8: 509-511.
12. Chevrier C, Bressac C (2002) Sperm storage and use after multiple mating in Dinarmus basalis (Hymenoptera: Pteromalidae). J Insect Behav 15: 385-398.
13. Clarke KR, Gorley RN (2006) PRIMER v. 6: user manual/tutorial. PRIMER-E, Plymouth.
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: 381-398.
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: 195-198.
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: 1313-1322.
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: 266-277.
18. Eberhard WG (1996) Female control: sexual selection by cryptic female choice. Princeton University Press, Princeton.
19. Eberhard WG (1998) Female roles in sperm competition. In: Birkhead TR, Møller AP (eds) Sperm competition and sexual selection. Academic, San Diego, pp 91-116.
20. Ernst CH, Barbour RW (1989) Turtles of the world. Smithsonian Institution, Washington, DC.
21. Fitzsimmons NN (1998) Single paternity of clutches and sperm storage in the promiscuous green sea turtle (Chelonia mydas). Mol Ecol 7: 575-584.
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: 503-509.
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: 301-308.
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: 1306-1313.
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: 61-71.
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: 980-985.
27. Girling JE (2002) The reptilian oviduct: a review of structure and function and directions for future research. J Exp Zool 293: 141-170.
28. Gist DH, Congdon JD (1998) Oviductal sperm storage as a reproductive tactic of turtles. J Exp Zool 282: 526-534.
29. Gist DH, Fisher EN (1993) Fine structure of the sperm storage tubules in the box turtle oviduct. J Reprod Fertil 97: 463-468.
30. Gist DH, Jones JM (1987) Storage of sperm in the reptilian oviduct. Scanning Microsc 1: 1839-1849.
31. Gist DH, Jones JM (1989) Sperm storage within the oviduct of turtles. J Morphol 199: 379-384.
32. Griffith SC, Owens IPF, Thuman KA (2002) Extra pair paternity in birds: a review of interspecific variation and adaptive function. Mol Ecol 11: 2195-2212.
33. Harry JL, Briscoe DA (1988) Multiple paternity in the loggerhead turtle (Caretta caretta). J Hered 79: 96-99.
34. Harshman LG, Prout T (1994) Sperm displacement without sperm transfer in Drosophila melanogaster. Evolution 48: 758-766.
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 237-270.
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: 520-526.
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: 1099-1106.
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: 819-830.
39. Klowden MJ (2003) Spermatheca. In: Resh VH, Cardé RT (eds) Encyclopedia of insects. Academic, San Diego, pp 1058-1059.
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: 100-107.
41. Kuchling G (1999) The reproductive biology of the Chelonia. Springer, Berlin.
42. Lessells CM, Birkhead TR (1990) Mechanisms of sperm competition in birds: mathematical models. Behav Ecol Sociobiol 27: 325-337.
43. Liem KL, Bemis WE, Walker WF, Grande L (2001) Functional anatomy of the vertebrates: an evolutionary perspective, 3rd edn. Brooks/Cole-Thomson Learning, Belmont.
44. Loman J, Madsen T, Hakansson T (1988) Increased fitness from multiple mating, and genetic heterogeneity: a model of a possible mechanism. Oikos 52: 69-72.
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: 1-16.
46. Marshall TC, Slate J, Kruuk LEB, Pemberton JM (1998) Statistical confidence for likelihood-based paternity inference in natural populations. Mol Ecol 7: 639-655.
47. Olsson M, Madsen T (1995) Female choice on male quantitative traits in lizards-why is it so rare? Behav Ecol Sociobiol 36: 179-184.
48. Olsson M, Madsen T (1996) Costs of mating with infertile males selects for late emergence in female sand lizards. Copeia 1996: 462-464.
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 503-578.
50. Olsson M, Shine R, Madsen T, Gullberg A, Tegelstrom H (1996) Sperm selection by females. Nature 383: 585.
51. Palmer KS, Rostal DC, Grumbles JS, Mulvey M (1998) Long-term sperm storage in the desert tortoise (Gopherus agassizii). Copeia 1998: 702-705.
52. Parker GA (1970) Sperm competition and its evolutionary consequences in the insects. Biol Rev 45: 525-567.
53. Parker GA (1990) Sperm competition games. Raffles and Roles. Proc R Soc Lond B 242: 120-126.
54. Parker GA, Simmons LW (1991) A model of constant random sperm displacement during mating: evidence from Scatophaga. Proc R Soc Lond B 246: 107-115.
55. Pearse DE, Avise JC (2001) Turtle mating systems: behaviour, sperm storage, and genetic paternity. J Hered 92: 206-211.
56. Pearse DE, Janzen FJ, Avise JC (2001) Genetic markers substantiate long-term storage and utilization of sperm by female painted turtles. Heredity 86: 378-384.
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: 164-171.
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: 10-17.
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: 865-867.
60. Racey PA (1979) The prolonged storage and survival of spermatozoa in Chiroptera. J Reprod Fertil 56: 391-402.
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: 537-547.
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: 15-27.
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: 153-159.
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: 95-102.
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: 62-72.
66. Swingland I, Stubbs D (1985) The ecology of a Mediterranean tortoise (Testudo hermanni): reproduction. J Zool Lond 205: 595-610.
67. Taylor PH, Kaspi ROY, Yuval B (2000) Copula duration and sperm storage in Mediterranean fruit flies from a wild population. Physiol Entomol 25: 94-99.
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: 329-346.
69. Uller T, Ollson M (2008) Multiple paternity in reptiles: patterns and processes. Mol Ecol 17: 2566-2580.
70. Walker WF (1980) Sperm utilization strategies in nonsocial insects. Am Nat 115: 780-799.
71. Weaver WGJ (1970) Courtship and combat behavior in Gophems berlanderi. Bull Fla State Mus 15: 1-43.
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 29-33.
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: 335-351.
74. Zeh JA, Zeh DW (1996) The evolution of polyandry. I. Intragenomic incompatibility. Proc R Soc Lond B 263: 1711-1717.