Intrapopulational variation of ejaculate traits and sperm depletion in red-sided garter snakes

Journal of Zoology

Volumn 292, Issue 3, 2014, Pages 192-201

  Friesen, C R ^a   Squire, M K ^a,b   Mason, R T ^a  

^a OREGON STATE UNIVERSITY   (United States)

^b TEXAS A AND M UNIVERSITY   (United States)

Author keywords

Copulatory plug; Ejaculate traits; Sperm competition; Sperm depletion; Sperm mobility

Indexed keywords

EID: 84894544682     PISSN: 09528369     EISSN: 14697998     Source Type: Journal    
DOI: 10.1111/jzo.12092     Document Type: Article

References (80)

1. Aleksiuk, M. (1976). Metabolic and behavioral adjustments to temperature change in the red-sided garter snake (Thamnophis sirtalis parietalis): an integrated approach. J. Therm. Biol. 1, 153-156.
2. Birkhead, T., Martinez, J., Burke, T. & Froman, D. (1999). Sperm mobility determines the outcome of sperm competition in the domestic fowl. Proc. R. Soc. London B Biol. Sci. 266, 1759-1764.
3. Birkhead, T.R. & Møller, A.P. (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.
4. Birkhead, T.R. & Møller, A.P. (1998). Sperm competition and sexual selection. San Diego, CA: Academic Press.
5. Birkhead, T.R. & Pizzari, T. (2002). Postcopulatory sexual selection. Nat. Rev. Genet. 3, 262-273.
6. Birkhead, T.R., Veiga, J.P. & Moller, A.P. (1994). Male sperm reserves and copulation behaviour in the House Sparrow, Passer domesticus. Proc. R. Soc. London B Biol. Sci. 256, 247.
7. Bissoondath, C. & Wiklund, C. (1996). Effect of male mating history and body size on ejaculate size and quality in two polyandrous butterflies, Pieris napi and Pieris rapae (Lepidoptera: Pieridae). Funct. Ecol. 10, 457-464.
8. Blanchard, F.N. & Blanchard, F. (1941). Mating of the garter snake Thamnophis sirtalis. Mich. Acad. Sci. Arts Lett. 27, 215-234.
9. Boschetto, C., Gasparini, C. & Pilastro, A. (2011). Sperm number and velocity affect sperm competition success in the guppy (Poecilia reticulata). Behav. Ecol. Sociobiol. 65, 813-821.
10. Bradshaw, S.D. (1986). Ecophysiology of desert reptiles. Sydney, Australia: Academic Press.
11. Casselman, S.J., Schulte-Hostedde, A.I. & Montgomerie, R. (2006). Sperm quality influences male fertilization success in walleye (Sander vitreus). Can. J. Fish. Aquat. Sci. 63, 2119-2125.
12. Cooper, T.G., Noonan, E., von Eckardstein, S., Auger, J., Baker, H.G., Behre, H.M., Haugen, T.B., Kruger, T., Wang, C. & Mbizvo, M.T. (2010). World Health Organization reference values for human semen characteristics. Hum. Reprod. Update 16, 231-245.
13. Crews, D., Camazine, B., Diamond, M., Mason, R., Tokarz, R.R. & Garstka, W.R. (1984). Hormonal independence of courtship behavior in the male garter snake. Horm. Behav. 18, 29-41.
14. Delbarco-Trillo, J. (2011). Adjustment of sperm allocation under high risk of sperm competition across taxa: a meta-analysis. J. Evol. Biol. 24, 1706-1714.
15. Dewsbury, D.A. (1982). Ejaculate cost and male choice. Am. Nat. 119, 601-610.
16. Duvall, D., Schuett, G.W. & Arnold, S.J. (1993). Ecology and evolution of snake mating systems, In Snakes: ecology and behavior: 165-200. Seigel, R.A. & Collins, J.T. (Eds). New York: McGraw-Hill.
17. Dziminski, M.A., Roberts, J.D., Beveridge, M. & Simmons, L.W. (2009). Sperm competitiveness in frogs: slow and steady wins the race. Proc. R. Soc. London B Biol. Sci. 276, 3955-3961.
18. Emlen, S.T. & Oring, L.W. (1977). Ecology, sexual selection, and the evolution of mating systems. Science 197, 215-223.
19. Fahrig, B.M., Mitchell, M.A., Eilts, B.E. & Paccamonti, D.L. (2007). Characterization and cooled storage of semen from corn snakes (Elaphe guttata). J. Zoo Wildl. Med. 38, 7-12.
20. Figenschou, L., Folstad, I., Rudolfsen, G., Hanssen, S., Kortet, R., Skau, P., Killie, J., Oskam, I. & Strand, H. (2013). The relative effect of parasites and social status on sperm traits in Arctic charr. Behav. Ecol. 24, 497-504.
21. Fitch, H.S. (1965). An ecological study of the garter snake, Thamnophis sirtalis. Univ. Kans. Publ. Mus. Nat. Hist. 15, 493-564.
22. Friesen, C.R., Shine, R., Krohmer, R.W. & Mason, R.T. (2013). Not just a chastity belt: the functional significance of mating plugs in garter snakes, revisited. Biol. J. Linn. Soc. 109, 893-907. (Online DOI: 10.1111/bij.12089).
23. Friesen, C.R., Mason, R.T., Arnold, S.J. & Estes, S. (2014). Patterns of sperm use in two populations of Red-sided Garter Snake (Thamnophis sirtalis parietalis) with long-term female sperm storage. Can. J. Zool. 92, 33-40.
24. Froman, D. & Feltmann, A. (2000). Sperm mobility: phenotype in roosters (Gallus domesticus) determined by concentration of motile sperm and straight line velocity. Biol. Reprod. 62, 303-309.
25. Froman, D.P. (2007). Sperm motility in birds: insights from fowl sperm. Soc. Reprod. Fertil. Suppl. 65, 293-308.
26. Froman, D.P. & Kirby, J.D. (2005). Sperm mobility: phenotype in roosters (Gallus domesticus) determined by mitochondrial function. Biol. Reprod. 72, 562-567.
27. Froman, D.P. & McLean, D.J. (1996). Objective measurement of sperm motility based upon sperm penetration of Accudenz®. Poult. Sci. 75, 776-784.
28. Froman, D.P., Feltmann, A.J., Rhoads, M.L. & Kirby, J.D. (1999). Sperm mobility: a primary determinant of fertility in the domestic fowl (Gallus domesticus). Biol. Reprod. 61, 400-405.
29. Gage, M.J.G., Macfarlane, C.P., Yeates, S., Ward, R.G., Searle, J.B. & Parker, G.A. (2004). Spermatozoal traits and sperm competition in Atlantic salmon: relative sperm velocity is the primary determinant of fertilization success. Curr. Biol. 14, 44-47.
30. Gibson, J.B. & Rabalais, F.C. (1973). Helminth parasites of Natrix sipedon sipedon and Thamnophis sirtalis sirtalis from the Ottawa National Wildlife Refuge, Ohio. Am. Midl. Nat. 89, 239-241.
31. Gregory, P.G. (1984). Communal denning in snakes, In Vertebrate ecology and systematics: a tribute to Henry S. Fitch: 57-76. Fitch, H.S. & Seigel, R.A. (Eds). Lawrence: University of Kansas.
32. Gregory, P.T. (1974). Patterns of spring emergence of the red-sided garter snake (Thamnophis sirtalis parietalis) in the Interlake region of Manitoba. Can. J. Zool. 52, 1063-1069.
33. Hawley, A.W.L. & Aleksiuk, M. (1975). Thermal regulation of spring mating behavior in the red-sided garter snake (Thamnophis sirtalis parietalis). Can. J. Zool. 53, 768-776.
34. Hines, A.H., Jivoff, P.R., Bushmann, P.J., van Montfrans, J., Reed, S.A., Wolcott, D.L. & Wolcott, T.G. (2003). Evidence for sperm limitation in the blue crab, Callinectes sapidus. Bull. Mar. Sci. 72, 287-310.
35. Hoskins, M.A. & Aleksiuk, M. (1973). Effects of temperature on the kinetics of malate dehydrogenase from a cold climate reptile, Thamnophis sirtalis parietalis. Comp. Biochem. Physiol. B. 45, 343-353.
36. Joy, J.E. & Crews, D. (1985). Social dynamics of group courtship behavior in male red-sided garter snakes (Thamnophis sirtalis parietalis). J. Comp. Psychol. 99, 145-149.
37. Kelly, C.D. & Jennions, M.D. (2011). Sexual selection and sperm quantity: meta-analyses of strategic ejaculation. Biol. Rev. 86, 863-884.
38. Kitchell, J.F. (1969). Thermophilic and thermophobic responses of snakes in a thermal gradient. Copeia 1969, 189-191.
39. Krohmer, R.W., Grassman, M. & Crews, D. (1987). Annual reproductive cycle in the male red-sided garter snake, Thamnophis sirtalis parietalis: field and laboratory studies. Gen. Comp. Endocrinol. 68, 64-75.
40. Kvarnemo, C. & Simmons, L.W. (2013). Polyandry as a mediator of sexual selection before and after mating. Philos. Trans. R. Soc. Lond. B. Biol Sci. 368, 1471-2970.
41. Lafferty, K.D. & Kuris, A.M. (2009). Parasitic castration: the evolution and ecology of body snatchers. Trends Parasitol. 25, 564-572.
42. Larsen, K.W., Gregory, P.T. & Antoniak, R. (1993). Reproductive ecology of the common garter snake, Thamnophis sirtalis, at the northern limit of its range. Am. Midl. Nat. 129, 336-345.
43. Liljedal, S., Folstad, I. & Skarstein, F. (1999). Secondary sex traits, parasites, immunity and ejaculate quality in the Arctic charr. Proc. R. Soc. London B Biol. Sci. 266, 1893-1898.
44. Lutterschmidt, D.I., LeMaster, M.P. & Mason, R.T. (2006). Minimal overwintering temperatures of red-sided garter snakes (Thamnophis sirtalis parietalis): a possible cue for emergence? Can. J. Zool. 84, 771-777.
45. Mattson, K.J., Vries, A.D., McGuire, S.M., Krebs, J., Louis, E.E. & Loskutoff, N.M. (2007). Successful artificial insemination in the corn snake, Elaphe gutatta, using fresh and cooled semen. Zoo Biol. 26, 363-369.
46. Måsvaer, M., Liljedal, S. & Folstad, I. (2004). Are secondary sex traits, parasites and immunity related to variation in primary sex traits in the Arctic charr? Proc. R. Soc. London B Biol. Sci. 271, 40-42.
47. Miller, G.T. & Pitnick, S. (2002). Sperm-female coevolution in Drosophila. Science 298, 1230-1233.
48. Moore, I.T., Lerner, J.P., Lerner, D.T. & Mason, R.T. (2000). Relationships between annual cycles of testosterone, corticosterone, and body condition in male red-spotted garter snakes, Thamnophis sirtalis concinnus. Physiol. Biochem. Zool. 73, 307-312.
49. Nakatsuru, K. & Kramer, D.L. (1982). Is sperm cheap? Limited male fertility and female choice in the lemon tetra (Pisces, Characidae). Science 216, 753-755.
50. Olsson, M. (2001). 'Voyeurism' prolongs copulation in the dragon lizard Ctenophorus fordi. Behav. Ecol. Sociobiol. 50, 378-381.
51. Olsson, M. & Madsen, T. (1998). Sexual selection and sperm competition in reptiles, In Sperm competition and sexual selection: 503-578. Birkhead, T.R. & Møller, A.P. (Eds). San Diego, CA: Academic Press.
52. Olsson, M., Madsen, T. & Shine, R. (1997). Is sperm really so cheap? Costs of reproduction in male adders, Vipera berus. Proc. R. Soc. London B Biol. Sci. 264, 455-459.
53. Parker, G.A. (1970). Sperm competition and its evolutionary consequences in the insects. Biol. Rev. 45, 525-567.
54. Parker, G.A. (1971). The reproductive behaviour and the nature of sexual selection in Scatophaga stercoraria L. (Diptera:Scatophagidae). J. Anim. Ecol. 40, 215-233.
55. Parker, G.A. (1982). Why are there so many tiny sperm? Sperm competition and the maintenance of two sexes. J. Theor. Biol. 96, 281-294.
56. Parker, G.A. (1990). Sperm competition games: raffles and roles. Proc. R. Soc. London B Biol. Sci. 242, 120-126.
57. Parker, G.A. & Birkhead, T.R. (2013). Polyandry: the history of a revolution. Philos. Trans. R. Soc. Lond., B, Biol. Sci. 368, 1-8.
58. Parker, G.A. & Pizzari, T. (2010). Sperm competition and ejaculate economics. Biol. Rev. 85, 897-934.
59. Pizzari, T., Froman, D.P. & Birkhead, T.R. (2002). Pre- and post-insemination episodes of sexual selection in the fowl, Gallus g. domesticus. Heredity 88, 112-116.
60. Pizzari, T., Cornwallis, C.K. & Froman, D.P. (2007). Social competitiveness associated with rapid fluctuations in sperm quality in male fowl. Proc. R. Soc. London B Biol. Sci. 274, 853-860.
61. Pizzari, T., Dean, R., Pacey, A., Moore, H. & Bonsall, M.B. (2008a). The evolutionary ecology of pre- and post-meiotic sperm senescence. Trends Ecol. Evol. 23, 131-140.
62. Pizzari, T., Worley, K., Burke, T. & Froman, D.P. (2008b). Sperm competition dynamics: ejaculate fertilising efficiency changes differentially with time. BMC Evol. Biol. 8, 332-339.
63. Preston, B.T. I., Stevenson, R., Pemberton, J.M. & Wilson, K. (2001). Dominant rams lose out by sperm depletion. Nature 409, 681-682.
64. Rau, M. & Gordon, D. (1978). Overwintering of helminths in the garter snake (Thamnophis sirtalis sirtalis). Can. J. Zool. 56, 1765-1767.
65. Schulte-Hostedde, A. & Montgomerie, R. (2006). Intraspecific variation in ejaculate traits of the northern watersnake (Nerodia sipedon). J. Zool. 270, 147-152.
66. Shine, R., Olsson, M.M. & Mason, R.T. (2000). Chastity belts in gartersnakes: the functional significance of mating plugs. Biol. J. Linnean Soc. 70, 377-390.
67. Shine, R., Elphick, M.J., Harlow, P.S., Moore, I.T., LeMaster, M.P. & Mason, R.T. (2001). Movements, mating, and dispersal of red-sided gartersnakes (Thamnophis sirtalis parietalis) from a communal den in Manitoba. Copeia 2001, 82-91.
68. Shine, R., Langkilde, T., Wall, M. & Mason, R.T. (2006). Temporal dynamics of emergence and dispersal of garter snakes from a communal den in Manitoba. Wildl. Res. 33, 103-111.
69. Simmons, L. & Parker, G. (1992). Individual variation in sperm competition success of yellow dung flies, Scatophaga stercoraria. Evolution 46, 366-375.
70. Simmons, L.W. (2005). The evolution of polyandry: sperm competition, sperm selection, and offspring viability. Annu. Rev. Ecol. Evolut. Syst. 36, 125-146.
71. Smith, C. & Ryan, M. (2010). Evolution of sperm quality but not quantity in the internally fertilized fish Xiphophorus nigrensis. J. Evol. Biol. 23, 1759-1771.
72. Tokarz, R.R. (1999). Relationship between copulation duration and sperm transfer in the lizard Anolis sagrei. Herpetologica 55, 234-241.
73. Tokarz, R.R. & Slowinski, J.B. (1990). Alternation of hemipenis use as a behavioural means of increasing sperm transfer in the lizard Anolis sagrei. Anim. Behav. 40, 374-379.
74. Tourmente, M., Cardozo, G., Bertona, M., Guidobaldi, A., Giojalas, L. & Chiaraviglio, M. (2006). The ultrastructure of the spermatozoa of Boa constrictor occidentalis, with considerations on its mating system and sperm competition theories. Acta Zool. 87, 25-32.
75. Tourmente, M., Cardozo, G.A., Guidobaldi, H.A., Giojalas, L.C., Bertona, M. & Chiaraviglio, M. (2007). Sperm motility parameters to evaluate the seminal quality of Boa constrictor occidentalis, a threatened snake species. Res. Vet. Sci. 82, 93-98.
76. Tourmente, M., Gomendio, M., Roldan, E.R.S., Giojalas, L.C. & Chiaraviglio, M. (2009). Sperm competition and reproductive mode influence sperm dimensions and structure among snakes. Evolution 63, 2513-2524.
77. Tourmente, M., Giojalas, L.C. & Chiaraviglio, M. (2011). Sperm parameters associated with reproductive ecology in two snake species. Herpetologica 67, 58-70.
78. Uller, T. & Olsson, M. (2008). Multiple paternity in reptiles: patterns and processes. Mol. Ecol. 17, 2566-2580.
79. Uller, T., Stuart-Fox, D. & Olsson, M. (2010). Evolution of primary sexual characters in reptiles, In Evolution of primary sexual characters in animals: 425-452. Leonard, J.L. & Córdoba-Aguilar, A. (Eds). Oxford: Oxford University Press.
80. Wedell, N., Gage, M.J.G. & Parker, G.A. (2002). Sperm competition, male prudence and sperm-limited females. Trends Ecol. Evol. 17, 313-320.