Not just a chastity belt: The functional significance of mating plugs in garter snakes, revisited

Biological Journal of the Linnean Society

Volumn 109, Issue 4, 2013, Pages 893-907

  Friesen, Christopher R ^a   Shine, Richard ^b   Krohmer, Randolph W ^c   Mason, Robert T ^a  

^a OREGON STATE UNIVERSITY   (United States)

^b UNIVERSITY OF SYDNEY   (Australia)

^c SAINT XAVIER UNIVERSITY   (United States)

Author keywords

Copulatory plug; Cryptic female choice; Mating plug; Mating system; Reptile; Sexual selection; Sperm competition

Indexed keywords

COPULATION; EXPERIMENTAL STUDY; FITNESS; HISTOLOGY; MATE GUARDING; MATING SUCCESS; REPRODUCTIVE SUCCESS; SEX RATIO; SEXUAL CONFLICT; SNAKE; SPERM;

CANADA; MANITOBA;

REPTILIA; SERPENTES; THAMNOPHIS; THAMNOPHIS SIRTALIS PARIETALIS;

EID: 84880327906     PISSN: 00244066     EISSN: 10958312     Source Type: Journal    
DOI: 10.1111/bij.12089     Document Type: Article

References (85)

1. Althaus S, Jacob A, Graber W, Hofer D, Nentwig W, Kropf C. 2010. A double role of sperm in scorpions: the copulatory plug of Euscorpius italicus (Scorpiones: Euscorpiidae) consists of sperm. Journal of Morphology 271: 383-393.
2. Arnqvist G, Rowe L. 2005. Sexual conflict. Princeton, NJ: Princeton University Press.
3. Asdell SA. 1946. Patterns of mammalian reproduction. Ithaca, NY: Comstock Publishing Co.
4. Birkhead TR, Møller AP. 1998. Sperm competition and sexual selection. San Diego, CA: Academic Press.
5. Bishop JE. 1959. A histological and histochemical study of the kidney tubule of the common garter snake, Thamnophis sirtalis, with special reference to the sexual segment in the male. Journal of Morphology 104: 307-357.
6. Blackburn DG. 1998. Structure, function, and evolution of the oviducts of squamate reptiles, with special reference to viviparity and placentation. Journal of Experimental Zoology 282: 560-617.
7. Blandau RJ. 1945. On the factors involved in sperm transport through the cervix uteri of the albino rat. American Journal of Anatomy 77: 253-272.
8. Burtner H, Floyd A, Longley J. 1965. Histochemistry of the 'sexual segment' granules of the male rattlesnake kidney. Journal of Morphology 116: 189-195.
9. Cuellar HS, Roth JJ, Fawcett JD, Jones RE. 1972. Evidence for sperm sustenance by secretions of the renal sexual segment of male lizards, Anolis carolinensis. Herpetologica 28: 53-57.
10. Devine MC. 1975. Copulatory plugs in snakes: enforced chastity. Science 187: 844-845.
11. Devine MC. 1977. Copulatory plugs, restricted mating opportunities and reproductive competition among male garter snakes. Nature 267: 345-346.
12. Devine MC. 1984. Potential for sperm competition in reptiles: behavioral and physiological consequences. In: Smith RL, ed. Sperm competition and the evolution of animal mating systems. Orlando: Academic Press, 509-521.
13. Dewsbury DA. 1982. Ejaculate cost and male choice. The American Naturalist 119: 601-610.
14. Dewsbury DA. 1988. A test of the role of copulatory plugs in sperm competition in deer mice (Peromyscus maniculatus). Journal of Mammalogy 69: 854-857.
15. Emlen ST, Oring LW. 1977. Ecology, sexual selection, and the evolution of mating systems. Science 197: 215-223.
16. Garner TWJ, Gregory PT, McCracken GF, Burghardt GM, Koop BF, McLain SE, Nelson RJ. 2002. Geographic variation of multiple paternity in the common garter snake (Thamnophis sirtalis). Copeia 2002: 15-23.
17. Garner TWJ, Pearman PB, Gregory PT, Tomio G, Wischniowski SG, Hosken DJ. 2004. Microsatellite markers developed from Thamnophis elegans and Thamnophis sirtalis and their utility in three species of garter snakes. Molecular Ecology Notes 4: 369-371.
18. Gillingham J. 1987. Social behavior. In: Seigel RA, Collins JT, Novak SS, eds. Snakes: ecology and evolutionary biology. New York, NY: Macmillan Publishing Company, 184-209.
19. Gould SJ, Lewontin RC. 1979. The spandrels of San Marco and the Panglossian paradigm: a critique of the adaptationist programme. Proceedings of the Royal Society of London. Series B. Biological Sciences 205: 581-598.
20. Gowaty P. 1997. Sexual dialectics, sexual selection, and variation in reproductive behavior. In: Feminism and evolutionary biology: boundaries, intersections and frontiers. New York: Chapman & Hill, 351-384.
21. Gregory PT. 1974. Patterns of spring emergence of the red-sided garter snake (Thamnophis sirtalis parietalis) in the Interlake region of Manitoba. Canadian Journal of Zoology 52: 1063-1069.
22. Halpert AP, Garstka WR, Crews D. 1982. Sperm transport and storage and its relation to the annual sexual cycle of the female red-sided garter snake, Thamnophis sirtalis parietalis. Journal of Morphology 174: 149-159.
23. Happ GM. 1969. Multiple sex pheromones of the mealworm beetle, Tenebrio molitor. Nature 222: 180-181.
24. Hawley AWL, Aleksiuk M. 1975. Thermal regulation of spring mating behavior in the red-sided garter snake (Thamnophis sirtalis parietalis). Canadian Journal of Zoology 53: 768-776.
25. Jia Z, Duan E, Jiang Z, Wang Z. 2002. Copulatory plugs in masked palm civets: prevention of semen leakage, sperm storage, or chastity enhancement? Journal of Mammalogy 83: 1035-1038.
26. Joy JE, Crews D. 1985. Social dynamics of group courtship behavior in male red-sided garter snakes (Thamnophis sirtalis parietalis). Journal of Comparative Psychology 99: 145-149.
27. King RB, Jadin RC, Grue M, Walley HD. 2009. Behavioural correlates with hemipenis morphology in New World natricine snakes. Biological Journal of the Linnean Society 98: 110-120.
28. Kitchell JF. 1969. Thermophilic and thermophobic responses of snakes in a thermal gradient. Copeia 1969: 189-191.
29. Koprowski JL. 1992. Removal of copulatory plugs by female tree squirrels. Journal of Mammalogy 73: 572-576.
30. Krohmer RW. 2004. Variation in seasonal ultrastructure of sexual granules in the renal sexual segment of the northern water snake, Nerodia sipedon sipedon. Journal of Morphology 261: 70-80.
31. LeMaster MP, Mason RT. 2002. Variation in a female sexual attractiveness pheromone controls male mate choice in garter snakes. Journal of Chemical Ecology 28: 1269-1285.
32. Leuckart R. 1847. Zur Morphologie und Anatomie der Geschlechtsorgane. Göttingen: Vandenhoeck und Ruprecht.
33. Long JA, Evans HML. 1922. The oestrous cycle in the rat and its associated phenomena. Berkeley, CA: University of California Press.
34. Mann T. 1984. Spermatophores: development, structure, biochemical attributes, and role in the transfer of spermatozoa. Berlin; New York: Springer-Verlag.
35. Martan J, Shepherd BA. 1976. The role of the copulatory plug in reproduction of the guinea pig. Journal of Experimental Zoology 196: 79-83.
36. Matson PL, Myssonski K, Yovich S, Morrison L, Irving J, Bakos HW. 2010. The density of human semen and the validation of weight as an indicator of volume: a multicentre study. Reproductive Biology 10: 141-153.
37. Mattson KJ, Vries AD, McGuire SM, Krebs J, Louis EE, Loskutoff NM. 2007. Successful artificial insemination in the corn snake, Elaphe gutatta, using fresh and cooled semen. Zoo Biology 26: 363-369.
38. McCracken GF, Burghardt GM, Houts SE. 1999. Microsatellite markers and multiple paternity in the garter snake Thamnophis sirtalis. Molecular Ecology 8: 1475-1479.
39. Michener G. 1984. Age, sex, and species differences in the annual cycles of ground-dwelling sciurids: implications for sociality. In: Murie J, Michener G, eds. The biology of the ground-dwelling squirrels: annual cycles, behavioral ecology, and sociality. Lincoln, NE: University of Nebraska Press, 81-107.
40. Moreira P, Birkhead T. 2004. Copulatory plug displacement and prolonged copulation in the Iberian rock lizard (Lacerta monticola). Behavioral Ecology and Sociobiology 56: 290-297.
41. Moreira PL, Birkhead TR. 2003. Copulatory plugs in the Iberian rock lizard do not prevent insemination by rival males. Functional Ecology 17: 796-802.
42. Moreira PL, Nunes VL, Martín J, Paulo OS. 2007. Copulatory plugs do not assure high first male fertilisation success: sperm displacement in a lizard. Behavioral Ecology and Sociobiology 62: 281-288.
43. Nelson RJ, Mason RT, Krohmer RW, Crews D. 1987. Pinealectomy blocks vernal courtship behavior in red-sided garter snakes. Physiology & Behavior 39: 231-233.
44. Nilson G, Andrén C. 1982. Function of renal sex secretion and male hierarchy in the adder, Vipera berus, during reproduction. Hormones and Behavior 16: 404-413.
45. O'Donnell RP, Shine R, Mason RT. 2004. Seasonal anorexia in the male red-sided garter snake, Thamnophis sirtalis parietalis. Behavioral Ecology and Sociobiology 56: 413-419.
46. Oku K, Kitsunezuka K. 2011. Effects of male mating interval on spermatophore formation, transfer, and subsequent female receptivity and fecundity in the sorghum plant bug, Stenotus rubrovittatus. Entomologia Experimentalis et Applicata 140: 134-138.
47. Olsson M, Gullberg A, Tegelström H. 1994. Sperm competition in the sand lizard, Lacerta agilis. Animal Behaviour 48: 193-200.
48. Olsson M, Madsen T. 1998. Sexual selection and sperm competition in reptiles. In: Birkhead TR, Moller AP, eds. Sperm competition and sexual selection. San Diego, CA: Academic Press, 503-578.
49. Parker G. 1990. Sperm competition games: raffles and roles. Proceedings of the Royal Society of London. Series B: Biological Sciences 242: 120-126.
50. Parker GA. 1970. Sperm competition and its evolutionary consequences in the insects. Biological Reviews 45: 525-567.
51. Perry-Richardson JJ, Schofield CW, Ford NB. 1990. Courtship of the Garter Snake, Thamnophis marcianus, with a Description of a Female Behavior for Coitus Interruption. Journal of Herpetology 24: 76-78.
52. Pizzari T, Birkhead T. 2000. Female feral fowl eject sperm of subdominant males. Nature 405: 787-789.
53. Poiani A. 2006. Complexity of seminal fluid: a review. Behavioral Ecology and Sociobiology 60: 289-310.
54. Preston DL, Mosley CAE, Mason RT. 2010. Sources of variability in recovery time from Methohexital Sodium anesthesia in snakes. Copeia 2010: 496-501.
55. Ramm SA, Parker GA, Stockley P. 2005. Sperm competition and the evolution of male reproductive anatomy in rodents. Proceedings of the Royal Society B: Biological Sciences 272: 949-955.
56. Ross P, Crews D. 1977. Influence of the seminal plug on mating behaviour in the garter snake. Nature 267: 344-345.
57. Ross P, Crews D. 1978. Stimuli Influencing Mating Behavior in the Garter Snake, Thamnophis radix. Behavioral Ecology and Sociobiology 4: 133-142.
58. Schwartz JM, McCracken GF, Burghardt GM. 1989. Multiple paternity in wild populations of the garter snake, Thamnophis sirtalis. Behavioral Ecology and Sociobiology 25: 269-273.
59. Shine R. 2012. Sex at the snake den: lust, deception and conflict in the mating system of red-sided gartersnakes. Advances in the Study of Behaviour 44: 1-51.
60. Shine R, Elphick MJ, Harlow PS, Moore IT, LeMaster MP, Mason RT. 2001. Movements, mating, and dispersal of red-sided gartersnakes (Thamnophis sirtalis parietalis) from a communal den in Manitoba. Copeia 2001: 82-91.
61. Shine R, Langkilde T, Mason R. 2004. Courtship tactics in garter snakes: how do a male's morphology and behaviour influence his mating success? Animal Behaviour 67: 477-483.
62. Shine R, Langkilde T, Mason RT. 2003. Cryptic forcible insemination: male snakes exploit female physiology, anatomy and behavior to obtain coercive matings. The American Naturalist 162: 653-667.
63. Shine R, Langkilde T, Wall M, Mason RT. 2006a. Temporal dynamics of emergence and dispersal of garter snakes from a communal den in Manitoba. Wildlife Research 33: 103-111.
64. Shine R, Mason RT. 2005. Do a male garter snake's energy stores limit his reproductive effort? Canadian Journal of Zoology 83: 1265-1270.
65. Shine R, O'Connor D, Mason RT. 2000b. Sexual conflict in the snake den. Behavioral Ecology and Sociobiology 48: 392-401.
66. Shine R, Olsson MM, Mason RT. 2000a. Chastity belts in gartersnakes: the functional significance of copulatory plugs. Biological Journal of the Linnean Society 70: 377-390.
67. Shine R, Webb JK, Lane A, Mason RT. 2006b. Flexible mate choice: a male snake's preference for larger females is modified by the sizes of females encountered. Animal Behaviour 71: 203-209.
68. Siegel DS, Miralles A, Trauth SE, Aldridge RD. 2011. The phylogenetic distribution and morphological variation of the 'pouch' in female snakes. Acta Zoologica 93: 400-408.
69. Siegel DS, Sever DM. 2006. Utero-muscular twisting and sperm storage in viperids. Herpetological Conservation and Biology 1: 87-92.
70. Simmons L, Parker G. 1992. Individual variation in sperm competition success of yellow dung flies, Scatophaga stercoraria. Evolution 46: 366-375.
71. Simmons LW. 2001. Sperm competition and its evolutionary consequences in the insects. Princeton, NJ: Princeton University Press.
72. Smith RL. 1984. Sperm competition and the evolution of animal mating systems. Orlando: Academic Press.
73. Stockley P. 1997. Sexual conflict resulting from adaptations to sperm competition. Trends in Ecology & Evolution 12: 154-159.
74. Suarez S, Pacey A. 2006. Sperm transport in the female reproductive tract. Human Reproduction Update 12: 23-37.
75. Takami Y, Sasabe M, Nagata N, Sota T. 2008. Dual function of seminal substances for mate guarding in a ground beetle. Behavioral Ecology 19: 1173-1178.
76. Uhl G, Busch M. 2009. Securing paternity: mating plugs in the dwarf spider Oedothorax retusus (Araneae: Erigoninae). Biological Journal of the Linnean Society 96: 574-583.
77. Uhl G, Nessler SH, Schneider JM. 2010. Securing paternity in spiders? A review on occurrence and effects of mating plugs and male genital mutilation. Genetica 138: 75-104.
78. Uller T, Olsson M. 2008. Multiple paternity in reptiles: patterns and processes. Molecular Ecology 17: 2566-2580.
79. Uller T, Stuart-Fox D, Olsson M. 2010. Evolution of primary sexual characters in reptiles. In: Leonard JL, Córdoba-Aguilar A, eds. Evolution of primary sexual characters in animals. Oxford: Oxford University Press, 425-452.
80. Venzon DJ, Moolgavkar SH. 1988. A method for computing profile likelihood based confidence intervals. Applied Statistics 37: 87-94.
81. Volsøe H. 1944. Structure and seasonal variation of the male reproductive organs of Vipera berus B. Copenhagen: Lunos Bogtrykkeri.
82. Voss RS. 1979. Male accessory glands and the evolution of copulatory plugs in rodents. Ann Arbor, MI: Museum of Zoology, University of Michigan.
83. Whittier JM, Crews D. 1986. Effects of prostaglandin F2 alpha on sexual behavior and ovarian function in female garter snakes (Thamnophis sirtalis parietalis). Endocrinology 119: 787-792.
84. Whittier JM, Mason RT, Crews D. 1985. Mating in the red-sided garter snake, Thamnophis sirtalis parietalis: differential effects on male and female sexual behavior. Behavioral Ecology and Sociobiology 16: 257-261.
85. Wusterbarth T, King RB, Duvall MR, Grayburn WS, Burghardt GM. 2010. Phylogenetically widespread multiple paternity in New World natricine snakes. Herpetological Conservation and Biology 2010: 86-93.