Sneaker "jack" males outcompete dominant "hooknose" males under sperm competition in Chinook salmon (Oncorhynchus tshawytscha)

Ecology and Evolution

Volumn 3, Issue 15, 2013, Pages 4987-4997

  Young, Brent ^a   Conti, David V ^b   Dean, Matthew D ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

Hooknose; Jack; Salmon; Sexual selection; Sneaker male; Sperm competition

Indexed keywords

EID: 84889650604     PISSN: None     EISSN: 20457758     Source Type: Journal    
DOI: 10.1002/ece3.869     Document Type: Article

References (106)

1. Allen, C., H. Jr Rich, and T. Quinn. 2007. Condition-dependent reproductive tactics by large and small anadromous male sockeye salmon Oncorhynchus nerka. J. Fish Biol. 70:1302-1307.
2. Andersson, M. 1994. Sexual selection. Princeton Univ. Press, Princeton, NJ.
3. Appleby, A. E., J. M. Tipping, and P. R. Seidel. 2003. The effect of using two-year-old male coho salmon in hatchery broodstock on adult returns. N. Am. J. Aquac. 65:60-62.
4. Balshine, S., B. J. Leach, F. Neat, N. Y. Werner, and R. Montgomerie. 2001. Sperm size of African cichlids in relation to sperm competition. Behav. Ecol. 12:726-731.
5. Beausoleil, J.-M. J., S. M. Doucet, D. D. Heath, and T. E. Pitcher. 2012. Spawning coloration, female choice and sperm competition in the redside dace, Clinostomus elongatus. Anim. Behav. 83:969-977.
6. Berejikian, B. A., D. M. Van Doornik, R. C. Endicott, T. L. Hoffnagle, E. P. Tezak, M. E. Moore, et al. 2010. Mating success of alternative male phenotypes and evidence for frequency-dependent selection in Chinook salmon, Oncorhynchus tshawytscha. Can. J. Fish. Aquat. Sci. 67:1933-1941.
7. Berejikian, B. A., D. M. Van Doornik, and J. J. Atkins. 2011. Alternative male reproductive phenotypes affect offspring growth rates in Chinook salmon. Trans. Am. Fish. Soc. 140:1206-1212.
8. Bernasconi, G., T. L. Ashman, T. R. Birkhead, J. D. Bishop, U. Grossniklaus, E. Kubli, et al. 2004. Evolutionary ecology of the prezygotic stage. Science 303:971-975.
9. Boschetto, C., C. Gasparini, and A. Pilastro. 2011. Sperm number and velocity affect sperm competition success in the guppy (Poecilia reticulata). Behav. Ecol. Sociobiol. 65:813-821.
10. Bouck, G. R., and J. Jacobson. 1976. Estimation of salmonid sperm concentration by microhematocrit technique. Trans. Am. Fish. Soc. 105:534-535.
11. Boudry, P., B. Collet, F. Cornette, V. Hervouet, and F. Bonhomme. 2002. High variance in reproductive success of the Pacific oyster (Crassostrea gigas, Thunberg) revealed by microsatellite-based parentage analysis of multifactorial crosses. Aquaculture 204:283-296.
12. Burness, G., S. J. Casselman, A. I. Schulte-Hostedde, C. D. Moyes, and R. Montgomerie. 2004. Sperm swimming speed and energetics vary with sperm competition risk in bluegill (Lepomis macrochirus). Behav. Ecol. Sociobiol. 56:65-70.
13. Carlson, S. M., H. B. Jr Rich, and T. P. Quinn. 2004. Reproductive life-span and sources of mortality for alternative male life-history strategies in sockeye salmon, Oncorhynchus nerka. Can. J. Zool. 82:1878-1885.
14. Comstock, R. E., and H. F. Robinson. 1948. The components of genetic variance in populations of biparental progenies and their use in estimating the average degree of dominance. Biometrics 4:254-266.
15. Cosson, J. 2010. Frenetic activation of fish spermatozoa flagella entails short-term motility, portending their precocious decadence. J. Fish Biol. 76:240-279.
16. Devlin, R. H., B. K. McNeil, I. I. Solar, and E. M. Donaldson. 1994. A rapid PCR-based test for Y-chromosomal DNA allows simple production of all-female strains of Chinook salmon. Aquaculture 128:211-220.
17. Evans, J. P., and D. J. Marshall. 2005. Male-by-female interactions influence fertilization success and mediate the benefits of polyandry in the sea urchin Heliocidaris erythrogramma. Evolution 59:106-112.
18. Evans, J. P., P. Rosengrave, C. Gasparini, and N. J. Gemmell, 2013. Delineating the roles of males and females in sperm competition. Proc. R. Soc. B 280:20132047.
19. Evans, J. P., L. Zane, S. Francescato, and A. Pilastro. 2003. Directional postcopulatory sexual selection revealed by artificial insemination. Nature 421:360-363.
20. Fitzpatrick, J. L., J. K. Desjardins, N. Milligan, R. Montgomerie, and S. Balshine. 2007. Reproductive-tactic-specific variation in sperm swimming speeds in a shell-brooding cichlid. Biol. Reprod. 77:280-284.
21. Fitzpatrick, J. L., M. Almbro, A. Gonzalez-Voyer, N. Kolm, and L. W. Simmons. 2012. Male contest competition and the coevolution of weaponry and testes in pinnipeds. Evolution 66:3595-3604.
22. Flannery, E. W. 2011. Sperm competition and the alternative reproductive tactics of Chinook salmon. Pp. 106. Biology. Univ. of Windsor, Canada.
23. Flannery, E. W., I. A. Butts, M. Slowinska, A. Ciereszko, and T. E. Pitcher. 2013. Reproductive investment patterns, sperm characteristics, and seminal plasma physiology in alternative reproductive tactics of Chinook salmon (Oncorhynchus tshawytscha). Biol. J. Linn. Soc. 108:99-108.
24. Fleming, I. and J. Reynolds. 2004. Salmonid breeding systems. Pp. 264-294 in A. P. Hendry and S. C. Stearns, eds. Evolution illuminated: salmon and their relatives. Oxford Univ. Press, Oxford, U.K.
25. Fu, P., B. D. Neff, and M. R. Gross. 2001. Tactic-specific success in sperm competition. Proc. R. Soc. Lond. B Biol. Sci. 268:1105-1112.
26. Gaffney, P. M., C. M. Bernat, and S. K. Jr Allen. 1993. Gametic incompatibility in wild and cultured populations of the eastern oyster, Crassostrea virginica (Gmelin). Aquaculture 115:273-284.
27. Gage, M. J. G., P. Stockley, and G. A. Parker. 1995. Effects of alternative male mating strategies on characteristics of sperm production in the atlantic salmon (Salmo salar): theoretical and empirical investigations. Philos. Trans. R. Soc. B Biol. Sci. 350:391-399.
28. Gage, M., C. Macfarlane, S. Yeates, R. Ward, J. Searle, and G. Parker. 2004. Spermatozoal traits and sperm competition in Atlantic salmon: relative sperm velocity is the primary determinant of fertilization success. Curr. Biol. 14:44-47.
29. Gasparini, C., and A. Pilastro. 2011. Cryptic female preference for genetically unrelated males is mediated by ovarian fluid in the guppy. Proc. R. Soc. Lond. B Biol. Sci. 278:2495-2501.
30. Gasparini, C., G. Andreatta, and A. Pilastro. 2012. Ovarian fluid of receptive females enhances sperm velocity. Naturwissenschaften 99:417-420.
31. Geyer, L. B., and S. R. Palumbi. 2005. Conspecific sperm precedence in two species of tropical sea urchins. Evolution 59:97-105.
32. Gharrett, A., and S. Shirley. 1985. A genetic examination of spawning methodology in a salmon hatchery. Aquaculture 47:245-256.
33. Gile, S. R., and M. M. Ferguson. 1995. Factors affecting male potency in pooled gamete crosses of rainbow trout, Oncorhynchus mykiss. Environ. Biol. Fishes 42:267-275.
34. Ginzburg, A. S. 1972. Fertilization in fishes and the problem of polyspermy. Pp. 366 in Z. Blake, B. Golek, eds. Israel Program for Scientific Translations, Jerusalem, Israel.
35. Gómez Montoto, L., C. Magana, M. Tourmente, J. Martin-Coello, C. Crespo, J. J. Luque-Larena, et al. 2011. Sperm competition, sperm numbers and sperm quality in muroid rodents. PLoS ONE 6:e18173.
36. Greig, C., D. P. Jacobson, and M. A. Banks. 2003. New tetranucleotide microsatellites for fine-scale discrimination among endangered chinook salmon (Oncorhynchus tshawytscha). Mol. Ecol. Notes 3:376-379.
37. Gross, M. R. 1985. Disruptive selection for alternative life histories in salmon. Nature 313:47-48.
38. Gross, M. R. 1991. Evolution of alternative reproductive strategies: frequency-dependent sexual selection in male bluegill sunfish. Philos. Trans. R. Soc. B Biol. Sci. 332:59-66.
39. Gross, M. R. 1996. Alternative reproductive strategies and tactics: diversity within sexes. Trends Ecol. Evol. 11:92-98.
40. Healey, M. C. 1991. Life history of chinook salmon (Oncorhynchus tshawytscha). pp. 311-393 in C. Groot and L. Margolis, eds. Pacific salmon life histories. University of Washington Press, Seattle, Washington.
41. Heath, D. D., R. H. Devlin, J. W. Heath, and G. K. Iwama. 1994. Genetic, environmental and interaction effects on the incidence of jacking in Oncorhynchus tshawytscha (Chinook salmon). Heredity 72:146-154.
42. Heath, D., L. Rankin, C. Bryden, J. Heath, and J. Shrimpton. 2002. Heritability and Y-chromosome influence in the jack male life history of chinook salmon (Oncorhynchus tshawytscha). Heredity 89:311-317.
43. Hoysak, D., and N. Liley. 2001. Fertilization dynamics in sockeye salmon and a comparison of sperm from alternative male phenotypes. J. Fish Biol. 58:1286-1300.
44. Hoysak, D. J., N. R. Liley, and E. B. Taylor. 2004. Raffles, roles, and the outcome of sperm competition in sockeye salmon. Can. J. Zool. 82:1017-1026.
45. Hutchings, J. and R. Myers. 1988. Mating success of alternative maturation phenotypes in male Atlantic salmon, Salmo salar. Oecologia 75:169-174.
46. Iwamatsu, T., N. Yoshizaki, and Y. Shibata. 1997. Changes in the chorion and sperm entry into the micropyle during fertilization in the teleostean fish, Oryzias latipes. Dev. Growth Differ. 39:33-41.
47. Jordan, W., and A. Youngson. 1992. The use of genetic marking to assess the reproductive success of mature male Atlantic salmon parr (Salmo salar, L.) under natural spawning conditions. J. Fish Biol. 41:613-618.
48. Kime, D., K. Van Look, B. McAllister, G. Huyskens, E. Rurangwa, and F. Ollevier. 2001. Computer-assisted sperm analysis (CASA) as a tool for monitoring sperm quality in fish. Comp. Biochem. Physiol. C: Toxicol. Pharmacol. 130:425-433.
49. Kupriyanova, E., and J. N. Havenh2002. Variation in sperm swimming behaviour and its effect on fertilization success in the serpulid polychaete Galeolaria caespitosa. Invertebr. Reprod. Dev. 41:21-26.
50. Levitan, D. R. 1993. The importance of sperm limitation to the evolution of egg size in marine invertebrates. Am. Nat. 141:517-536.
51. Levitan, D. R. 1996. Effects of gamete traits on fertilization in the sea and the evolution of sexual dimorphism. Nature 382:153-155.
52. Levitan, D. R. 2000. Sperm velocity and longevity trade off each other and influence fertilization in the sea urchin Lytechinus variegatus. Proc. R. Soc. Lond. B Biol. Sci. 267:531-534.
53. Levitan, D. R. 2012. Contemporary evolution of sea urchin gamete-recognition proteins: experimental evidence of density-dependent gamete performance predicts shifts in allele frequencies over time. Evolution 66:1722-1736.
54. Levitan, D. R., and D. L. Ferrell. 2006. Selection on gamete recognition proteins depends on sex, density, and genotype frequency. Science 312:267-269.
55. Levitan, D. R., and A. P. Stapper. 2010. Simultaneous positive and negative frequency-dependent selection on sperm bindin, a gamete recognition protein in the sea urchin Strongylocentrotus purpuratus. Evolution 64:785-797.
56. Liljedal, S., G. Rudolfsen, and I. Folstad. 2008. Factors predicting male fertilization success in an external fertilizer. Behav. Ecol. Sociobiol. 62:1805-1811.
57. Locatello, L., A. Pilastro, R. Deana, A. Zarpellon, and M. B. Rasotto. 2007. Variation pattern of sperm quality traits in two gobies with alternative mating tactics. Funct. Ecol. 21:975-981.
58. Marshall, D. J., and J. P. Evans. 2005. The benefits of polyandry in the free-spawning polychaete Galeolaria caespitosa. J. Evol. Biol. 18:735-741.
59. Marshall, D. J., C. A. Styan, and M. J. Keough. 2002. Sperm environment affects offspring quality in broadcast spawning marine invertebrates. Ecol. Lett. 5:173-176.
60. Maynard Smith, J. 1982. Evolution and the theory of games. Cambridge Univ. Press, Cambridge, U.K.
61. Mengerink, K. J. and V. D. Vacquier. 2001. Glycobiology of sperm-egg interactions in deuterostomes. Glycobiology 11:37R-43R.
62. Montgomerie, R. and J. Fitzpatrick. 2009. Testis size, sperm size, and sperm competition. Pp. 1-53 in B. G. M. Jamieson, ed. Reproductive biology and phylogeny of fishes. Science Publishers Inc., Enfield, NH.
63. Myers, J. M., R. G. Kope, G. J. Bryant, D. Teel, L. J. Lierheimer, T. C. Wainwright, et al. 1998. Status review of Chinook salmon from Washington, Idaho, Oregon, and California. US Dept. Comm., NOAA Tech. Memo. NMFS-NWFSC-35, 443 pp.
64. Neff, B. D. and L. M. Wahl. 2004. Mechanisms of sperm competition: testing the fair raffle. Evolution 58:1846-1851.
65. Neff, B. D., P. Fu, and M. R. Gross. 2003. Sperm investment and alternative mating tactics in bluegill sunfish (Lepomis macrochirus). Behav. Ecol. 14:634-641.
66. Nelson, R. J. and T. D. Beacham. 1999. Isolation and cross species amplification of microsatellite loci useful for study of Pacific salmon. Anim. Genet. 30:228-229.
67. Pakkasmaa, S., N. Peuhkuri, A. Laurila, H. Hirvonen, and E. Ranta. 2001. Female and male contribution to egg size in salmonids. Evol. Ecol. 15:143-153.
68. Pakkasmaa, S., O.-P. Penttinen, and J. Piironen. 2006. Metabolic rate of Arctic charr eggs depends on their parentage. J. Comp. Physiol. B. 176:387-391.
69. Palumbi, S. R. 1999. All males are not created equal: fertility differences depend on gamete recognition polymorphisms in sea urchins. Proc. Natl Acad. Sci. USA 96:12632-12637.
70. Parker, G. 1990a. Sperm competition games: raffles and roles. Proc. R. Soc. Lond. B Biol. Sci. 242:120-126.
71. Parker, G. 1990b. Sperm competition games: sneaks and extra-pair copulations. Proc. R. Soc. Lond. B Biol. Sci. 242:127-133.
72. Perchec, G., M. Cosson, J. Cosson, C. Jeulin, and R. Billard. 1998. Morphological and kinetic changes of carp (Cyprinus carpio) spermatozoa after initiation of motility in distilled water. Cell Motil. Cytoskelet. 35:113-120.
73. Pitcher, T. E., S. M. Doucet, J. M. J. Beausoleil, and D. Hanley. 2009. Secondary sexual characters and sperm traits in coho salmon Oncorhynchus kisutch. J. Fish Biol. 74:1450-1461.
74. Quinn, T. P., and C. J. Foote. 1994. The effects of body size and sexual dimorphism on the reproductive behaviour of sockeye salmon, Oncorhynchus nerka. Anim. Behav. 48:751-761.
75. Rasotto, M. B., and C. Mazzoldi. 2002. Male traits associated with alternative reproductive tactics in Gobius niger. J. Fish Biol. 61:173-184.
76. Reichard, M., S. C. Le Comber, and C. Smith. 2007. Sneaking from a female perspective. Anim. Behav. 74:679-688.
77. Rosengrave, P., N. J. Gemmell, V. Metcalf, K. McBride, and R. Montgomerie. 2008. A mechanism for cryptic female choice in chinook salmon. Behav. Ecol. 19:1179-1185.
78. Rudolfsen, G., L. Figenschou, I. Folstad, H. Tveiten, and M. Figenschou. 2006. Rapid adjustments of sperm characteristics in relation to social status. Proc. R. Soc. Lond. B Biol. Sci. 273:325-332.
79. Rudolfsen, G., L. Figenschou, I. Folstad, and O. Kleven. 2008. Sperm velocity influence paternity in the Atlantic cod (Gadus morhua L.). Aquac. Res. 39:212-216.
80. Rutter, C. 1903. Natural history of the quinnat salmon. A report of investigations in the Sacramento River, 1896-1901. Bull. U.S. Fish Comm. for 1902 22:65-141.
81. Schulte-Hostedde, A. I., J. S. Millar, and G. J. Hickling. 2005. Condition dependence of testis size in small mammals. Evol. Ecol. Res. 7:143-149.
82. Simmons, L. W., and J. L. Fitzpatrick. 2012. Sperm wars and the evolution of male fertility. Reproduction 144:519-534.
83. Simmons, L., J. Tomkins, and J. Hunt. 1999. Sperm competition games played by dimorphic male beetles. Proc. R. Soc. Lond. B Biol. Sci. 266:145-150.
84. Skarstein, F., I. Folstad, S. Liljedal, and M. Grahn. 2005. MHC and fertilization success in the Arctic charr (Salvelinus alpinus). Behav. Ecol. Sociobiol. 57:374-380.
85. Smith, C. C., and M. J. Ryan. 2010. Evolution of sperm quality but not quantity in the internally fertilized fish Xiphophorus nigrensis. J. Evol. Biol. 23:1759-1771.
86. Snook, R. 2005. Sperm in competition: not playing by the numbers. Trends Ecol. Evol. 20:46-53.
87. Sørum, V., L. Figenschou, G. Rudolfsen, and I. Folstad. 2011. Spawning behaviour of Arctic charr (Salvelinus alpinus): risk of sperm competition and timing of milt release for sneaker and dominant males. Behaviour 148:1157-1172.
88. Spies, I. B., D. J. Brasier, P. T. L. O'Reilly, T. R. Seamons, and P. Bentzen. 2005. Development and characterization of novel tetra-, tri-, and dinucleotide microsatellite markers in rainbow trout (Oncorhynchus mykiss). Mol. Ecol. Notes 5:278-281.
89. Stockley, P., and A. Purvis. 1993. Sperm competition in mammals: a comparative study of male roles and relative investment in sperm production. Funct. Ecol. 7:560-570.
90. Stockley, P., M. J. G. Gage, G. A. Parker, and A. P. Moller. 1997. Sperm competition in fishes: the evolution of testis size and ejaculate characteristics. Am. Nat. 149:933-954.
91. Stoltz, J. A., and B. D. Neff. 2006. Sperm competition in a fish with external fertilization: the contribution of sperm number, speed and length. J. Evol. Biol. 19:1873-1881.
92. Swanson, W. J., and V. D. Vacquier. 2002. The rapid evolution of reproductive proteins. Nat. Rev. Genet. 3:137-144.
93. Taborsky, M. 1998. Sperm competition in fish:bourgeois' males and parasitic spawning. Trends Ecol. Evol. 13:222-227.
94. Tanaka, Y., T. Hayashi, D. G. III Miller, K. Tainaka, and J. Yoshimura. 2009. Breeding games and dimorphism in male salmon. Anim. Behav. 77:1409-1413.
95. Tazzyman, S. J., T. Pizzari, R. M. Seymour, and A. Pomiankowski. 2009. The evolution of continuous variation in ejaculate expenditure strategy. Am. Nat. 174:E71-E82.
96. Tourmente, M., M. Gomendio, and E. Roldan. 2011. Sperm competition and the evolution of sperm design in mammals. BMC Evol. Biol. 11:12.
97. Tourmente, M., M. Rowe, M. M. González-Barroso, E. Rial, M. Gomendio, and E. R. S. Roldan. 2013. Postcopulatory sexual selection increases ATP content in rodent spermatozoa. Evolution. 67:1838-1846.
98. Uglem, I., T. F. Galloway, G. Rosenqvist, and I. Folstad. 2001. Male dimorphism, sperm traits and immunology in the corkwing wrasse (Symphodus melops L.). Behav. Ecol. Sociobiol. 50:511-518.
99. Vacquier, V. D. 1998. Evolution of gamete recognition proteins. Science 281:1995-1998.
100. Vladić, T. V., and T. Järvi. 2001. Sperm quality in the alternative reproductive tactics of Atlantic salmon: the importance of the loaded raffle mechanism. Proc. R. Soc. Lond. B Biol. Sci. 268:2375-2381.
101. Vladić, T. V., L. A. Forsberg, and T. Järvi. 2010. Sperm competition between alternative reproductive tactics of the Atlantic salmon in vitro. Aquaculture 302:265-269.
102. Williamson, K. S., A. R. Murdoch, T. N. Pearsons, E. J. Ward, and M. J. Ford. 2010. Factors influencing the relative fitness of hatchery and wild spring Chinook salmon (Oncorhynchus tshawytscha) in the Wenatchee River, Washington, USA. Can. J. Fish. Aquat. Sci. 67:1840-1851.
103. Withler, R. 1988. Genetic consequences of fertilizing chinook salmon (Oncorhynchus tshawytscha) eggs with pooled milt. Aquaculture 68:15-25.
104. Yanagimachi, R., G. N. Cherr, M. C. Pillai, and J. D. Baldwin. 1992. Factors controlling sperm entry into the micropyles of salmonid and herring eggs. Dev. Growth Differ. 34:447-461.
105. Yeates, S. E., S. Einum, I. A. Fleming, H.-J. Megens, R. J. M. Stet, K. Hindar, et al. 2009. Atlantic salmon eggs favour sperm in competition that have similar major histocompatibility alleles. Proc. R. Soc. Lond. B Biol. Sci. 276:559-566.
106. Yeates, S. E., S. E. Diamond, S. Einum, B. C. Emerson, W. V. Holt, and M. J. G. Gage. in press. Cryptic choice of conspecific sperm controlled by the impact of ovarian fluid on sperm swimming behaviour. Evolution.