Patterns of sperm use in two populations of Red-sided Garter Snake (Thamnophis sirtalis parietalis) with long-term female sperm storage

Canadian Journal of Zoology

Volumn 92, Issue 1, 2014, Pages 33-40

  Friesen, Christopher R ^a,b   Mason, Robert T ^a   Arnold, Stevan J ^a   Estes, Suzanne ^c  

^a OREGON STATE UNIVERSITY   (United States)

^b UNIVERSITY OF SYDNEY   (Australia)

^c PORTLAND STATE UNIVERSITY   (United States)

Author keywords

Mating system; Parentage; Postcopulatory sexual selection; Red sided Garter Snake; Sperm competition; Sperm storage; Squamate; Thamnophis sirtalis parietalis

Indexed keywords

FEMALE; PARENTAGE; PATERNITY; REPRODUCTIVE STRATEGY; SEXUAL SELECTION; SNAKE; SPERM; SPERM COMPETITION;

EID: 84891708649     PISSN: 00084301     EISSN: 14803283     Source Type: Journal    
DOI: 10.1139/cjz-2013-0195     Document Type: Article

References (91)

1. Adams, E.M., Jones, A.G., and Arnold, S.J. 2005. Multiple paternity in a natural population of a salamander with long-term sperm storage. Mol. Ecol. 14(6): 1803-1810. doi:10.1111/j.1365-294X.2005.02539.x. PMID:15836651.
2. Aleksiuk, M., and Gregory, P.T. 1974. Regulation of seasonal mating behavior in Thamnophis sirtalis parietalis. Copeia, 1974(3): 681-689. doi:10.2307/1442681.
3. Alonzo, S.H., and Pizzari, T. 2013. Selection on female remating interval is influenced by male sperm competition strategies and ejaculate characteristics. Philos. Trans. R. Soc. B Biol. Sci. 368(1613). doi:10.1098/rstb.2012.0044. PMID: 23339235.
4. Arnqvist, G., and Rowe, L. 2005. Sexual conflict. Princeton University Press Princeton, N.J.
5. Birkhead, T.R., and Brillard, J.-P. 2007. Reproductive isolation in birds: postcopulatory prezygotic barriers. Trends Ecol. Evol. 22(5): 266-272. doi:10.1016/ j.tree.2007.02.004. PMID:17306413.
6. Birkhead, T.R., and 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(4): 295-311. doi:10.1111/j.1095-8312.1993.tb0 0933.x.
7. Birkhead, T.R., and Møller, A.P. 1998. Sperm competition and sexual selection. Academic Press, San Diego, Calif.
8. Birkhead, T.R., Martinez, J.G., Burke, T., and Froman, D.P. 1999. Sperm mobility determines the outcome of sperm competition in the domestic fowl. Proc. R. Soc. B Biol. Sci. 266(1430): 1759-1764. doi:10.1098/rspb.1999.0843.
9. Bittner, T.D., and King, R.B. 2003. Gene flow and melanism in garter snakes revisited: a comparison of molecular markers and island vs. coalescent models. Biol. J. Linn. Soc. 79(3): 389-399. doi:10.1046/j.1095-8312.2003.00199.x.
10. Blanchard, F.C. 1943. A test of fecundity of the garter snake Thamnophis sirtalis sirtalis (Linnaeus) in the year following the year of insemination. Mich. Acad. Sci. Arts Lett. 28: 313-316.
11. Blanchard, F.N., and Blanchard, F.C. 1941. The inheritance of melanism in the garter snake Thamnophis sirtalis sirtalis (Linnaeus), and some evidence of effective autumn mating. Mich. Acad. Sci. Arts Lett. 26: 177-193.
12. Blanchard, F.N., and Finster, E.B. 1933. A method of marking living snakes for future recognition, with a discussion of some problems and results. Ecology, 14(4): 334-347. doi:10.2307/1932657.
13. Blouin-Demers, G., Gibbs, H.L., and Weatherhead, P. 2005. Genetic evidence for sexual selection in black ratsnakes, Elaphe obsoleta. Anim. Behav. 69(1): 225-234. doi:10.1016/j.anbehav.2004.03.012.
14. Boomsma, J.J., Baer, B., and Heinze, J. 2005. The evolution of male traits in social insects. Annu. Rev. Entomol. 50: 395-420. doi:10.1146/annurev.ento.50.07 1803.130416. PMID:15822204.
15. Booth, W., Smith, C.F., Eskridge, P.H., Hoss, S.K., Mendelson, J.R., III, and Schuett, G.W. 2012. Facultative parthenogenesis discovered in wild vertebrates. Biol. Lett. 8(6): 983-985. doi:10.1098/rsbl.2012.0666. PMID:22977071.
16. Collins, J.T., and Taggart, T.W. 2002. Standard common and current scientific names for North American amphibians, turtles, reptiles and crocodilians. Center for North American Herpetology, Lawrence, Kans.
17. Crews, D., and Moore, M.C. 1986. Evolution of mechanisms controlling mating behavior. Science, 231(4734): 121-125. doi:10.1126/science.3941893. PMID: 3941893.
18. Devine, M.C. 1984. Potential for sperm competition in reptiles: behavioral and physiological consequences. In Sperm competition and the evolution of animal mating systems. Edited by R.L. Smith. Academic Press, Orlando, Fla. pp. 509-521.
19. DeWoody, J., Nason, J.D., and Hipkins, V.D. 2006. Mitigating scoring errors in microsatellite data from wild populations. Mol. Ecol. Notes, 6(4): 951-957. doi:10.1111/j.1471-8286.2006.01449.x.
20. DiLeo, M.F., Row, J.R., and Lougheed, S.C. 2010. Discordant patterns of population structure for two co-distributed snake species across a fragmented Ontario landscape. Divers. Distrib. 16(4): 571-581. doi:10.1111/j.1472-4642.2010. 00667.x.
21. Duvall, D., Schuett, G.W., and Arnold, S.J. 1993. Ecology and evolution of snake mating systems. In Snakes: ecology and behavior. Edited by R.A. Seigel and J.T. Collins. McGraw-Hill, New York. pp. 165-200.
22. Dyke, A. 2004. An outline of North American deglaciation with emphasis on central and northern Canada. Dev. Quat. Sci. 2: 373-424. doi:10.1016/S1571-0866(04)80209-4.
23. Eberhard, W.G. 1996. Female control: sexual selection by cryptic female choice. Princeton University Press, Princeton, N.J.
24. Eberhard, W.G., Birkhead, T.R., and Møller, A.P. 1998. Female roles in sperm competition. In Sperm competition and sexual selection. Edited by T.R. Birkhead and A.P. Møller. Academic Press, San Diego, Calif. pp. 91-116.
25. Emlen, S.T., and Oring, L.W. 1977. Ecology, sexual selection, and the evolution of mating systems. Science, 197(4300): 215-223. doi:10.1126/science.327542. PMID:327542.
26. Evans, J.P., Zane, L., Francescato, S., and Pilastro, A. 2003. Directional postcopulatory sexual selection revealed by artificial insemination. Nature, 421(6921): 360-363. doi:10.1038/nature01367. PMID:12540898.
27. Fox, W. 1956. Seminal receptacles of snakes. Anat. Rec. 124(3): 519-539. doi:10. 1002/ar.1091240303. PMID:13314111.
28. Friesen, C.R., Shine, R., Krohmer, R.W., and Mason, R.T. 2013. Not just a chastity belt: the functional significance of mating plugs in garter snakes, revisited. Biol. J. Linn. Soc. 109(4): 893-907. doi:10.1111/bij.12089.
29. García-González, F., and Simmons, L.W. 2005. Sperm viability matters in insect sperm competition. Curr. Biol. 15(3): 271-275. doi:10.1016/j.cub.2005.01.032. PMID:15694313.
30. Garner, T.W.J., and Larsen, K.W. 2005. Multiple paternity in the western terrestrial garter snake, Thamnophis elegans. Can. J. Zool. 83(5): 656-663. doi:10.1139/ z05-057.
31. Garner, T.W.J., Gregory, P.T., McCracken, G.F., Burghardt, G.M., Koop, B.F., McLain, S.E., and Nelson, R.J. 2002. Geographic variation of multiple paternity in the common garter snake (Thamnophis sirtalis). Copeia, 2002(1): 15-23. doi:10.1643/0045-8511(2002)002[0015:GVOMPI]2.0.CO;2.
32. Garner, T.W.J., Pearman, P.B., Gregory, P.T., Tomio, G., Wischniowski, S.G., and Hosken, D.J. 2004. Microsatellite markers developed from Thamnophis elegans and Thamnophis sirtalis and their utility in three species of garter snakes. Mol. Ecol. Notes, 4(3): 369-371. doi:10.1111/j.1471-8286.2004.00656.x.
33. Gavrilets, S. 2000. Rapid evolution of reproductive barriers driven by sexual conflict. Nature, 403(6772): 886-889. doi:10.1038/35002564. PMID:10706284.
34. Gay, L., Hosken, D.J., Eady, P., Vasudev, R., and Tregenza, T. 2010. The evolution of harm-effect of sexual conflicts and population size. Evolution, 65(3): 725-737. doi:10.1111/j.1558-5646.2010.01181.x.
35. Gibbs, H.L., and Weatherhead, P.J. 2001. Insights into population ecology and sexual selection in snakes through the application of DNA-based genetic markers. J. Hered. 92(2): 173-179. doi:10.1093/jhered/92.2.173. PMID:11396576.
36. Gilchrist, A.S., and Partridge, L. 1997. Heritability of pre-adult viability differences can explain apparent heritability of sperm displacement ability in Drosophila melanogaster. Proc. R. Soc. B Biol. Sci. 264(1386): 1271-1275. doi:10. 1098/rspb.1997.0175. PMID:9332012.
37. 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(8): 1063-1069. doi:10.1139/z74-141.
38. Gregory, P.T. 2006. Influence of income and capital on reproduction in a viviparous snake: direct and indirect effects. J. Zool. (Lond.), 270(3): 414-419. doi:10.1111/j.1469-7998.2006.00149.x.
39. Gregory, P.T., and Larsen, K.W. 1993. Geographic variation in reproductive characteristics among Canadian populations of the common garter snake (Thamnophis sirtalis). Copeia, 1993: 946-958. doi:10.2307/1447072.
40. Gregory, P.T., and Stewart, K.W. 1975. Long-distance dispersal and feeding strategy of the red-sided garter snake (Thamnophis sirtalis parietalis) in the Interlake of Manitoba. Can. J. Zool. 53(3): 238-245. doi:10.1139/z75-030.
41. Halpert, A.P., Garstka, W.R., and 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. J. Morphol. 174(2): 149-159. doi:10.1002/ jmor.1051740204.
42. Hoffman, L.H., and Wimsatt, W.A. 1972. Histochemical and electron microscopic observations on the sperm receptacles in the garter snake oviduct. Am. J. Anat. 134(1): 71-95. doi:10.1002/aja.1001340107. PMID:4260659.
43. Hölldobler, B., and Wilson, E.O. 1990. The ants. Belknap Press of Harvard University Press, Cambridge, Mass.
44. Kalinowski, S.T., Taper, M.L., and Marshall, T.C. 2007. Revising how the computer program Cervus accommodates genotyping error increases success in paternity assignment. Mol. Ecol. 16(5): 1099-1106. doi:10.1111/j.1365-294X.2007. 03089.x. PMID:17305863.
45. King, R.B., Milstead, W.B., Gibbs, H.L., Prosser, M.R., Burghardt, G.M., and McCracken, G.F. 2001. Application of microsatellite DNA markers to discriminate between maternal and genetic effects on scalation and behavior in multiply-sired garter snake litters. Can. J. Zool. 79(1): 121-128. doi:10.1139/z00-183.
46. Kissner, K.J., Weatherhead, P.J., and Gibbs, H.L. 2005. Experimental assessment of ecological and phenotypic factors affecting male mating success and polyandry in northern watersnakes, Nerodia sipedon. Behav. Ecol. Sociobiol. 59(2): 207-214. doi:10.1007/s00265-005-0026-7.
47. Lande, R. 1981. Models of speciation by sexual selection on polygenic traits. Proc. Natl. Acad. Sci. U.S.A. 78(6): 3721-3725. doi:10.1073/pnas.78.6.3721.
48. Lande, R. 1992. Neutral theory of quantitative genetic variance in an island model with local extinction and colonization. Evolution, 46(2): 381-389. doi: 10.2307/2409859.
49. LeMaster, M.P., and Mason, R.T. 2002. Variation in a female sexual attractiveness pheromone controls male mate choice in garter snakes. J. Chem. Ecol. 28(6): 1269-1285. doi:10.1023/A:1016294003641. PMID:12184402.
50. LeMaster, M.P., and Mason, R.T. 2003. Pheromonally mediated sexual isolation among denning populations of red-sided garter snakes, Thamnophis sirtalis parietalis. J. Chem. Ecol. 29(4): 1027-1043. PMID:12775159.
51. Lougheed, S.C., Gibbs, H.L., Prior, K.A., and Weatherhead, P.J. 1999. Hierarchical patterns of genetic population structure in black rat snakes (Elaphe obsoleta obsoleta) as revealed by microsatellite DNA analysis. Evolution, 53(6): 1995-2001. doi:10.2307/2640459.
52. Lutterschmidt, D.I., LeMaster, M.P., and Mason, R.T. 2006. Minimal overwintering temperatures of red-sided garter snakes (Thamnophis sirtalis parietalis): a possible cue for emergence? Can. J. Zool. 84(5): 771-777. doi:10.1139/z06-043.
53. Macmillan, S. 1995. Restoration of an extirpated red-sided garter snake Thamnophis sirtalis parietalis population in the Interlake region of Manitoba, Canada. Biol. Conserv. 72(1): 13-16. doi:10.1016/0006-3207(94)00054-T.
54. Martin, O.Y., and Hosken, D.J. 2003. The evolution of reproductive isolation through sexual conflict. Nature, 423(6943): 979-982. doi:10.1038/nature 01752.
55. Mason, R., MacMillan, S., Whittier, J., Krohmer, R., and Koonz, W. 1991. Thamnophis sirtalis parietalis (red-sided garter snake) population morph variation. Herpetol. Rev. 22: 61.
56. McCracken, G.F., Burghardt, G.M., and Houts, S.E. 1999. Microsatellite markers and multiple paternity in the garter snake Thamnophis sirtalis. Mol. Ecol. 8(9): 1475-1479. doi:10.1046/j.1365-294x.1999.00720.x. PMID:10564453.
57. Miller, G.T., and Pitnick, S. 2002. Sperm-female coevolution in Drosophila. Science, 298(5596): 1230-1233. doi:10.1126/science.1076968. PMID:12424377.
58. Mooi, R.D., Wiens, J.P., and Casper, G.S. 2011. Extreme color variation within populations of the Common Gartersnake, Thamnophis sirtalis, in central North America, with implications for subspecies status. Copeia, 2011(2): 187-200. doi:10.1643/CH-10-067.
59. Olsson, M., and Madsen, T. 1998. Sexual selection and sperm competition in reptiles. In Sperm competition and sexual selection. Edited by T.R. Birkhead and A.P. Møller. Academic Press, San Diego, Calif. pp. 503-578.
60. Orr, T.J., and Zuk, M. 2013. Does delayed fertilization facilitate sperm competition in bats? Behav. Ecol. Sociobiol. 67(12): 1903-1913. doi:10.1007/s00265-013-1598-2.
61. Parker, G.A. 1998. Sperm competition and the evolution of ejaculates: towards a theory base. In Sperm competition and sexual selection. Edited by T.R. Birkhead and A.P. Møller. Academic Press, San Diego, Calif. pp. 3-49.
62. Parker, G.A., and Birkhead, T.R. 2013. Polyandry: the history of a revolution. Philos. Trans. R. Soc. B Biol. Sci. 368(1613): 1-8. doi:10.1098/rstb.2012.0335.
63. Pitnick, S., Wolfner, M.F., and Suarez, S.S. 2009. Ejaculate-female and spermfemale interactions. In Sperm biology: an evolutionary perspective. Edited by T.R. Birkhead, D.J. Hosken, and S. Pitnick. Elsevier/Academic Press, London. pp. 247-304.
64. Placyk, J.S., Burghardt, G.M., Small, R.L., King, R.B., Casper, G.S., and Robinson, J.W. 2007. Post-glacial recolonization of the Great Lakes region by the common gartersnake (Thamnophis sirtalis) inferred from mtDNA sequences. Mol. Phylogenet. Evol. 43(2): 452-467. doi:10.1016/j.ympev.2006.10. 023.
65. Prosser, M.R., Gibbs, H.L., and Weatherhead, P.J. 1999. Microgeographic population genetic structure in the northern water snake, Nerodia sipedon sipedon detected using microsatellite DNA loci. Mol. Ecol. 8(2): 329-333. doi:10.1046/ j.1365-294X.1999.00530.x. PMID:10065548.
66. Rye, L.A. 2000. Analysis of areas of intergradation between described subspecies of the common garter snake, Thamnophis sirtalis, in Canada. Ph.D. thesis, The University of Guelph, Guelph, Ont.
67. Seigel, R.A. 1987. Snakes-ecology and evolutionary biology. Macmillan, New York.
68. Sever, D.M., and Hamlett, W.C. 2002. Female sperm storage in reptiles. J. Exp. Zool. 292(2): 187-199. doi:10.1002/jez.1154. PMID:11754034.
69. Shine, R. 2004. Mechanisms and consequences of sexual conflict in garter snakes (Thamnophis sirtalis, Colubridae). Behav. Ecol. 15(4): 654-660. doi: 10.1093/beheco/arh058.
70. Shine, R., O'Connor, D., and Mason, R.T. 2000a. Sexual conflict in the snake den. Behav. Ecol. Sociobiol. 48(5): 392-401. doi:10.1007/s002650000255.
71. Shine, R., Olsson, M.M., Moore, I.T., LeMaster, M.P., Greene, M., and Mason, R.T. 2000b. Body size enhances mating success in male garter snakes. Anim. Behav. 59(3): F4-F11. doi:10.1006/anbe.1999.1338. PMID:10715190.
72. Shine, R., Elphick, M.J., Harlow, P.S., Moore, I.T., LeMaster, M.P., and Mason, R.T. 2001. Movements, mating, and dispersal of red-sided gartersnakes (Thamnophis sirtalis parietalis) from a communal den in Manitoba. Copeia, 2001(1): 82-91. doi:10.1643/0045-8511(2001)001[0082:MMADOR]2.0.CO;2.
73. Shine, R., Langkilde, T., Wall, M., and Mason, R.T. 2006. Temporal dynamics of emergence and dispersal of garter snakes from a communal den in Manitoba. Wildl. Res. 33(2): 103-111. doi:10.1071/WR05030.
74. Shuster, S.M., and Wade, M.J. 2003. Mating systems and strategies. Princeton University Press, Princeton, N.J.
75. Shuster, S.M., Briggs, W.R., and Dennis, P.A. 2013. How multiple mating by females affects sexual selection. Philos. Trans. R. Soc. B Biol. Sci. 368(1613). doi:10.1098/rstb.2012.0046.
76. Simmons, L.W. 2001. Sperm competition and its evolutionary consequences in the insects. Princeton University Press, Princeton, N.J.
77. Simmons, L.W., and Siva-Jothy, M.T. 1998. Sperm competition in insects: mechanisms and the potential for selection. In Sperm competition and sexual selection. Edited by T.R. Birkhead and A.P. Møller Academic Press, San Diego, Calif.
78. Spitze, K. 1993. Population structure in Daphnia obtusa: quantitative genetic and allozymic variation. Genetics, 135(2): 367-374.
79. Stewart, G.R. 1972. An unusual record of sperm storage in a female garter snake (genus Thamnophis). Herpetologica, 28(4): 346-347.
80. Stockley, P. 1999. Sperm selection and genetic incompatibility: does relatedness of mates affect male success in sperm competition? Proc. R. Soc. B Biol. Sci. 266(1429): 1663-1669. doi:10.1098/rspb.1999.0829.
81. Thornhill, R. 1983. Cryptic female choice and its implications in the scorpionfly Harpobittacus nigriceps. Am. Nat. 122(6): 765-788. doi:10.1086/284170.
82. Thornhill, R., and Alcock, J. 1983. The evolution of insect mating systems. Harvard University Press, Cambridge, Mass.
83. Tregenza, T., and Wedell, N. 2000. Genetic compatibility, mate choice and patterns of parentage. Mol. Ecol. 9(8): 1013-1027. doi:10.1046/j.1365-294x.2000. 00964.x. PMID:10964221.
84. Uller, T., and Olsson, M. 2008. Multiple paternity in reptiles: patterns and processes. Mol. Ecol. 17(11): 2566-2580. doi:10.1111/j.1365-294X.2008.03772.x. PMID:18452517.
85. Uller, T., Stuart-Fox, D., and Olsson, M. 2010. Evolution of primary sexual characters in reptiles. In Evolution of primary sexual characters in animals. Edited by J.L. Leonard and A. Córdoba-Aguilar. Oxford University Press, Oxford. pp. 425-452.
86. Ursenbacher, S., Erny, C., and Fumagalli, L. 2009. Male reproductive success and multiple paternity in wild, low-density populations of the adder (Vipera berus). J. Hered. 100(3): 365-370. doi:10.1093/jhered/esn104. PMID:19074755.
87. Uyeda, J.C., Arnold, S.J., Hohenlohe, P.A., and Mead, L.S. 2009. Drift promotes speciation by sexual selection. Evolution, 63(3): 583-594. doi:10.1111/j.1558-5646.2008.00589.x.
88. Westphal, M.F. 2007. On the evolution of correlated color traits in garter snakes. Ph.D. thesis, Department of Zoology, Oregon State University, Corvallis.
89. Whittier, J.M., Mason, R.T., and Crews, D. 1985. Mating in the red-sided garter snake, Thamnophis sirtalis parietalis: differential effects on male and female sexual behavior. Behav. Ecol. Sociobiol. 16(3): 257-261. doi:10.1007/BF 00310989.
90. Wusterbarth, T., King, R.B., Duvall, M.R., Grayburn, W.S., and Burghardt, G.M. 2010. Phylogenetically widespread multiple paternity in New World natricine snakes. Herpetol. Conserv. Biol. 2010(5): 86-93.
91. Zeh, J.A., and Zeh, D.W. 1997. The evolution of polyandry II: Post-copulatory defences against genetic incompatibility. Proc. R. Soc. B Biol. Sci. 264(1378): 69-75. doi:10.1098/rspb.1997.0010.