Ejaculate quality in spotted hyenas: Intraspecific variation in relation to life-history traits

Journal of Mammalogy

Volumn 94, Issue 1, 2013, Pages 90-99

  Curren, Leslie J ^a   Weldele, Mary L ^b   Holekamp, Kay E ^a  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Crocuta crocuta; dispersal status; ejaculate quality; individual repeatability; intraspecific variation; sperm competition; spotted hyena

Indexed keywords

CARNIVORE; DISPERSAL; HYPOTHESIS TESTING; INDIVIDUAL VARIATION; INTRASEXUAL INTERACTION; INTRASPECIFIC COMPETITION; LIFE HISTORY TRAIT; MALE; MAMMAL; REPRODUCTIVE BIOLOGY; SEX ROLE; SEXUAL SELECTION; SPERM COMPETITION; WILD POPULATION;

EID: 84874092155     PISSN: 00222372     EISSN: 15451542     Source Type: Journal    
DOI: 10.1644/12-MAMM-A-057.1     Document Type: Article

References (103)

1. ANDERSSON, M. 1994. Sexual selection. Princeton University Press, Princeton, New Jersey.
2. BERGER, D., L. FRANK, AND S. E. GLICKMAN. 1992. Unraveling ancient mysteries: biology, behavior, and captive management of the spotted hyena, Crocuta crocuta. Pp. 139-148 in Proceedings of the Joint Conference of American Association of Zoo Veterinarians and American Association of Wildlife Veterinarians, Oakland, California.
3. BIRKHEAD, T. R., D. J. HOSKEN, AND S. S. PITNICK. 2008. Sperm biology: an evolutionary perspective. Academic Press, London, United Kingdom.
4. BIRKHEAD, T. R., J. G. MART́INEZ, T. BURKE, AND D. P. FROMAN. 1999. Sperm mobility determines the outcome of sperm competition in the domestic fowl. Proceedings of the Royal Society of London, B. Biological Sciences 266:1759-1764.
5. BIRKHEAD, T. R., E. J. PELLATT, P. BREKKE, R. YEATES, AND H. CASTILLO-JUAREZ. 2005. Genetic effects on sperm design in the zebra finch. Nature 434:383-387.
6. BIRKHEAD, T. R., AND T. PIZZARI. 2002. Postcopulatory sexual selection. Nature Reviews Genetics 3:262-273.
7. BONANNO, V. L., AND A. I. SCHULTE-HOSTEDDE. 2009. Sperm competition and ejaculate investment in red squirrels (Tamiasciurus hudsonicus). Behavioral Ecology and Sociobiology 63:835-846.
8. BOYDSTON, E., K. KAPHEIM, R. VAN HORN, AND L. SMALE. 2005. Sexually dimorphic patterns of space use throughout ontogeny in the spotted hyena (Crocuta crocuta). Journal of Zoology (London) 267:271-281.
9. BROWN, J. L., ET AL. 1991. Developmental changes in pituitary-gonadal function in free-ranging lions (Panthera leo leo) of the Serengeti Plains and Ngorongoro Crater. Journal of Reproduction and Fertility 91:29-40.
10. CORNWALLIS, C. K., AND T. R. BIRKHEAD. 2006. Social status and availability of females determine patterns of sperm allocation in the fowl. Evolution 60:1486-1493.
11. CROSIER, A. E., L. MARKER, J. HOWARD, B. S. PUKAZHENTHI, J. N. HENGHALI, AND D. E. WILDT. 2007. Ejaculate traits in the Namibian cheetah (Acinonyx jubatus): influence of age, season and captivity. Reproduction, Fertility and Development 19:370-382.
12. CUNHA, G., Y. WANG, N. PLACE, W. LIU, AND L. BASKIN. 2003. Urogenital system of the spotted hyena (Crocuta crocuta Erxleben): a functional histological study. Journal of Morphology 256:205-218.
13. DARWIN, C. 1871. The descent of man. Murray, London, United Kingdom.
14. DEAN, M., K. ARDLIE, AND M. NACHMAN. 2006. The frequency of multiple paternity suggests that sperm competition is common in house mice (Mus domesticus). Molecular Ecology 15:4141-4151.
15. DENK, A. G. 2005. Paternity in mallards: effects of sperm quality and female sperm selection for inbreeding avoidance. Behavioral Ecology 16:825-833.
16. DIXSON, A., AND M. ANDERSON. 2004. Sexual behavior, reproductive physiology and sperm competition in male mammals. Physiology and Behavior 83:361-371.
17. EAST, M., T. BURKE, K. WILHELM, C. GREIG, AND H. HOFER. 2003. Sexual conflicts in spotted hyenas: male and female mating tactics and their reproductive outcome with respect to age, social status and tenure. Proceedings of the Royal Society of London, B. Biological Sciences 270:1247-1254.
18. EAST, M., AND H. HOFER. 2001. Male spotted hyenas (Crocuta crocuta) queue for status in social groups dominated by females. Behavioral Ecology 12:558-568.
19. EBERHARD, W. G. 1996. Female control: sexual selection by cryptic female choice. Princeton University Press, Princeton. New Jersey.
20. ENGH, A., ET AL. 2002. Reproductive skew among males in a female-dominated mammalian society. Behavioral Ecology 13:193-200.
21. ENSLEY, P., A. WING, B. GOSINK, B. LASLEY, AND B. DURRANT. 1982. Application of noninvasive techniques to monitor reproductive function in a brown hyena (Hyaena brunnea). Zoo Biology 1:333-343.
22. FAULKES, C., S. TROWELL, J. JARVIS, AND N. BENNETT. 1994. Investigation of numbers and motility of spermatozoa in reproduc-tively active and socially suppressed males of two eusocial African mole-rats, the naked mole-rat (Heterocephalus glaber) and the Damaraland mole-rat (Cryptomys damarensis). Reproduction 100:411-416.
23. FIRMAN, R. C., AND L. W. SIMMONS. 2010. Experimental evolution of sperm quality via postcopulatory sexual selection in house mice. Evolution 64:1245-1256.
24. FIRMAN, R. C., AND L. W. SIMMONS. 2011. Experimental evolution of sperm competitiveness in a mammal. BMC Evolutionary Biology 11:19.
25. FITZPATRICK, J., J. DESJARDINS, K. STIVER, R. MONTGOMERIE, AND S. BALSHINE. 2005. Male reproductive suppression in the cooperatively breeding fish Neolamprologus pulcher. Behavioral Ecology 17:25-33.
26. FITZPATRICK, J. L., R. MONTGOMERIE, J. K. DESJARDINS, K. A. STIVER, N. KOLM, AND S. BALSHINE. 2009. Female promiscuity promotes the evolution of faster sperm in cichlid fishes. Proceedings of the National Academy of Sciences 106:1128-1132.
27. FRANK, L. G. 1986. Social organization of the spotted hyaena Crocuta crocuta. II. Dominance and reproduction. Animal Behaviour 34:1510-1527.
28. FRANK, L. G., S. E. GLICKMAN, AND I. POWCH. 1990. Sexual dimorphism in the spotted hyaena (Crocuta crocuta). Journal of Zoology (London) 221:308-313.
29. GAGE, M. J. G. 1994. Associations between body size, mating pattern, testis size and sperm lengths across butterflies. Proceedings of the Royal Society of London, B. Biological Sciences 258:247-254.
30. GAGE, M. J. G., AND R. P. FRECKLETON. 2003. Relative testis size and sperm morphometry across mammals: no evidence for an association between sperm competition and sperm length. Proceedings of the Royal Society of London, B. Biological Sciences 270:625-632.
31. GAÑÁN, N., ET AL. 2010. Reproductive traits in captive and free-ranging males of the critically endangered Iberian lynx (Lynx pardinus). Reproduction 139:275-285.
32. GARBER, P., L. MOYA, J. PRUETZ, AND C. IQUE. 1996. Social and seasonal influences on reproductive biology in male moustached tamarins (Saguinus mystax). American Journal of Primatology 38:29-46.
33. GLICKMAN, S. E., L. G. FRANK, S. PAVGI, AND P. LICHT. 1992. Hormonal correlates of 'masculinization' in female spotted hyaenas (Crocuta crocuta). 1. Infancy to sexual maturity. Journal of Reproduction and Fertility 95:451-462.
34. GOMENDIO, M., A. H. HARCOURT, AND E. R. S. ROLDÁN. 1998. Sperm competition in mammals. Pp. 667-751 in Sperm competition and sexual selection (T. Birkhead and A. Mller, eds.). Academic Press, London, United Kingdom.
35. GOMENDIO, M., A. F. MALO, J. GARDE, AND E. R. S. ROLDAN. 2007. Sperm traits and male fertility in natural populations. Reproduction 134:19-29.
36. GOMENDIO, M., J. MARTIN-COELLO, C. CRESPO, C. MAGAÑA, AND E. R. S. ROLDAN. 2006. Sperm competition enhances functional capacity of mammalian spermatozoa. Proceedings of the National Academy of Sciences 103:15113-15117.
37. GOYMANN, W., M. EAST, B. WACHTER, O. HÖNER, E. MÖSTL, AND H. HOFER. 2003. Social status does not predict corticosteroid levels in postdispersal male spotted hyenas. Hormones and Behavior 43:474-479.
38. HARCOURT, A., P. HARVEY, S. LARSON, AND R. SHORT. 1981. Testis weight, body weight and breeding system in primates. Nature 293:55-57.
39. HOLEKAMP, K. E., AND C. L. SISK. 2003. Effects of dispersal status on pituitary and gonadal function in the male spotted hyena. Hormones and Behavior 44:385-394.
40. HOLEKAMP, K. E., AND L. SMALE. 1993. Ontogeny of dominance in free-living spotted hyaenas: juvenile rank relations with other immature individuals. Animal Behaviour 46:451-466.
41. HOLEKAMP, K. E., AND L. SMALE. 1998. Dispersal status influences hormones and behavior in the male spotted hyena. Hormones and Behavior 33:205-216.
42. HOLEKAMP, K. E., L. SMALE, AND M. SZYKMAN. 1996. Rank and reproduction in the female spotted hyaena. Journal of Reproduction and Fertility 108:229-237.
43. HOLEKAMP, K. E., J. E. SMITH, C. C. STRELIOFF, R. C. VAN HORN, AND H. E. WATTS. 2012. Society, demography and genetic structure in the spotted hyena. Molecular Ecology 21:613-632.
44. HOLEKAMP, K. E., M. SZYKMAN, E. E. BOYDSTON, AND L. SMALE. 1999. Association of seasonal reproductive patterns with changing food availability in an equatorial carnivore, the spotted hyaena (Crocuta crocuta). Journal of Reproduction and Fertility 116:87-93.
45. HOLT, C., W. V. HOLT, H. D. MOORE, H. C. REED, AND R. M. CURNOCK. 1997. Objectively measured boar sperm motility parameters correlate with the outcomes of on-farm inseminations: results of two fertility trials. Journal of Andrology 18:312-323.
46. HOSKEN, D. J., T. W. GARNER, AND P. I. WARD. 2001. Sexual conflict selects for male and female reproductive characters. Current Biology 11:489-493.
47. HOSKEN, D. J., AND P. I. WARD. 2001. Experimental evidence for testis size evolution via sperm competition. Ecology Letters 4:10-13.
48. IOSSA, G., C. D. SOULSBURY, P. J. BAKER, AND S. HARRIS. 2008. Sperm competition and the evolution of testes size in terrestrial mammalian carnivores. Functional Ecology 22:655-662.
49. JOHNSTON, L., D. ARMSTRONG, AND J. BROWN. 1994. Seasonal effects on seminal and endocrine traits in the captive snow leopard (Panthera uncia). Reproduction 102:229-236.
50. KENAGY, G., AND S. TROMBULAK. 1986. Size and function of mammalian testes in relation to body size. Journal of Mammalogy 67:1-22.
51. KIDD, S. A., B. ESKENAZI, AND A. J. WYROBEK. 2001. Effects of male age on semen quality and fertility: a review of the literature. Fertility and Sterility 75:237-248.
52. KISHK, W. 2008. Interrelationship between ram plasma testosterone level and some semen characteristics. Slovak Journal of Animal Science 41:67-71.
53. KRUUK, H. 1972. The spotted hyaena: a study of predation and social behavior. University of Chicago Press, Chicago, Illinois.
54. MALO, A., J. GARDE, A. SOLER, A. GARĆIA, M. GOMENDIO, AND E. ROLDAN. 2005. Male fertility in natural populations of red deer is determined by sperm velocity and the proportion of normal spermatozoa. Biology of Reproduction 72:822.
55. MALO, A., M. GOMENDIO, J. GARDE, B. LANG-LENTON, A. SOLER, AND E. ROLDAN. 2006. Sperm design and sperm function. Biology Letters 2:246.
56. MARDIA, K. V., J. T. KENT, AND J. M. BIBBY. 1979. Multivariate analysis. Academic Press, London, United Kingdom.
57. MATTHEWS, L. 1939. Reproduction in the spotted hyaena, Crocuta crocuta (Erxleben). Philosophical Transactions of the Royal Society of London, B. Biological Sciences 230:1-78.
58. MEASEY, G., J. SILVA, AND M. DI-BERNARDO. 2003. Testing for repeatability in measurements of length and mass in Chthonerpeton indistinctum (Amphibia: Gymnophiona), including a novel method of calculating total length of live caecilians. Herpetological Review 34:35-38.
59. MEEKER, J. D., L. GODFREY-BAILEY, AND R. HAUSER. 2006. Relationships between serum hormone levels and semen quality among men from an infertility clinic. Journal of Andrology 28:397-406.
60. MINTER, L. J., AND T. J. DELIBERTO. 2008. Seasonal variation in serum testosterone, testicular volume, and semen characteristics in the coyote (Canis latrans). Theriogenology 69:946-952.
61. MONTOTO, L., ET AL. 2011. Sperm competition, sperm numbers and sperm quality in muroid rodents. PLoS ONE 6:e18173.
62. MORATO, R., ET AL. 2001. Comparative analyses of semen and endocrine characteristics of free-living versus captive jaguars (Panthera onca). Reproduction 122:745-751.
63. MORROW, E., AND M. GAGE. 2001. Consistent significant variation between individual males in spermatozoal morphometry. Journal of Zoology (London) 254:147-153.
64. PARKER, G. 1990. Sperm competition games: sneaks and extra-pair copulations. Proceedings of the Royal Society of London, B. Biological Sciences 242:127-133.
65. PARKER, G. A. 1970. Sperm competition and its evolutionary consequences in the insects. Biological Reviews 45:525-567.
66. PARKER, G. A., AND T. PIZZARI. 2010. Sperm competition and ejaculate economics. Biological Reviews 85:897-934.
67. PITNICK, S., AND D. J. HOSKEN. 2010. Postcopulatory sexual selection. Pp. 379-399 in Evolutionary behavioral ecology (D. F. Wesneat and C. W. Fox, eds.). Oxford University Press, Oxford, United Kingdom.
68. PITNICK, S., G. T. MILLER, J. REAGAN, AND B. HOLLAND. 2001. Males' evolutionary responses to experimental removal of sexual selection. Proceedings of the Royal Society of London, B. Biological Sciences 268:1071-1080.
69. POWELL, D., P. TYLER, AND L. PECK. 2001. Effect of sperm concentration and sperm ageing on fertilisation success in the Antarctic soft-shelled clam Laternula elliptica and the Antarctic limpet Nacella concinna. Marine Ecology Progress Series 215:191-200.
70. PRESTON, B. T., I. R. STEVENSON, J. M. PEMBERTON, D. W. COLTMAN, AND K. WILSON. 2003. Overt and covert competition in a promiscuous mammal: the importance of weaponry and testes size to male reproductive success. Proceedings of the Royal Society of London, B. Biological Sciences 270:633-640.
71. QUINN, G. P., AND M. J. KEOUGH. 2002. Experimental design and data analysis for biologists. Cambridge University Press, Cambridge, United Kingdom.
72. RAMM, S. A., G. A. PARKER, AND P. STOCKLEY. 2005. Sperm competition and the evolution of male reproductive anatomy in rodents. Proceedings of the Royal Society of London, B. Biological Sciences 272:949-955.
73. RAMM, S. A., AND P. STOCKLEY. 2008. Adaptive plasticity of mammalian sperm production in response to social experience. Proceedings of the Royal Society of London, B. Biological Sciences 276:745-751.
74. R DEVELOPMENT CORE TEAM. 2007. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
75. REVELLE, W. 2010. psych: procedures for personality and psychological research. Northwestern University, Evanston, Illinois.
76. REYNOLDS, J., S. ROMMEL, AND M. PITCHFORD. 2004. The likelihood of sperm competition in manatees-explaining an apparent paradox. Marine Mammal Science 20:464-476.
77. ROBERTS, D. W. 2010. labdsv: ordination and multivariate analysis for ecology. R package version 1.4-1. http://CRAN.R-project.org/ package¼labdsv. Accessed 6 July 2011.
78. SARKAR, D. 2008. Lattice: multivariate data visualization with R. Springer, New York.
79. SCHULTE-HOSTEDDE, A. I., AND J. S. MILLAR. 2004. Intraspecific variation of testis size and sperm length in the yellow-pine chipmunk (Tamias amoenus): implications for sperm competition and reproductive success. Behavioral Ecology and Sociobiology 55:272-277.
80. SERRANO, J., I. FOLSTAD, G. RUDOLFSEN, AND L. FIGENSCHOU. 2006. Do the fastest sperm within an ejaculate swim faster in subordinate than in dominant males of arctic char? Canadian Journal of Zoology 84:1019-1024.
81. SHROUT, P. E., AND J. L. FLEISS. 1979. Intraclass correlations: uses in assessing rater reliability. Psychological Bulletin 86:420-428.
82. SIKES, R. S., W. L. GANNON, AND THE ANIMAL CARE AND USE COMMITTEE OF THE AMERICAN SOCIETY OF MAMMALOGISTS. 2011. Guidelines of the American Society of Mammalogists for the use of wild mammals in research. Journal of Mammalogy 92:235-253.
83. SMALE, L., L. G. FRANK, AND K. E. HOLEKAMP. 1993. Ontogeny of dominance in free-living spotted hyaenas: juvenile rank relations with adult females and immigrant males. Animal Behaviour 46:467-477.
84. SMALE, L., S. NUNES, AND K. E. HOLEKAMP. 1997. Sexually dimorphic dispersal in mammals: patterns, causes, and consequences. Advances in the Study of Behavior 26:181-250.
85. SOULSBURY, C. D. 2010. Genetic patterns of paternity and testes size in mammals. PLoS ONE 5:e9581.
86. STENE, J., G. FISCHER, E. STENE, M. MIKKELSEN, AND E. PETERSEN. 1977. Paternal age effect in Down's syndrome. Annals of Human Genetics 40:299-306.
87. STOCKLEY, P. 2004. Sperm competition in mammals. Human Fertility 7:91-97.
88. STOCKLEY, P., AND A. PURVIS. 1993. Sperm competition in mammals: a comparative study of male roles and relative investment in sperm production. Functional Ecology 7:560-570.
89. SWANSON, E. M., I. DWORKIN, AND K. E. HOLEKAMP. 2011. Lifetime selection on a hypoallometric size trait in the spotted hyena. Proceedings of the Royal Society of London, B. Biological Sciences 278:3277-3285.
90. SZYKMAN, M., R. VAN HORN, A. ENGH, AND E. BOYDSTON. 2007. Courtship and mating in free-living spotted hyenas. Behaviour 144:815-846.
91. THONGTIP, N., ET AL. 2008. Potential factors affecting semen quality in the Asian elephant (Elephas maximus). Reproductive Biology and Endocrinology 6:1-9.
92. TOURMENTE, M., M. GOMENDIO, AND E. ROLDAN. 2011. Sperm competition and the evolution of sperm design in mammals. BMC Evolutionary Biology 11:12.
93. TREGENZA, T., F. ATTIA, AND S. S. BUSHAIBA. 2009. Repeatability and heritability of sperm competition outcomes in males and females of Tribolium castaneum. Behavioral Ecology and Sociobiology 63:817-823.
94. VAN HORN, R. C., A. L. ENGH, K. T. SCRIBNER, S. M. FUNK, AND K. E. HOLEKAMP. 2004. Behavioural structuring of relatedness in the spotted hyena (Crocuta crocuta) suggests direct fitness benefits of clan-level cooperation. Molecular Ecology 13:449-458.
95. VAN HORN, R. C., T. L. MCELHINNY, AND K. E. HOLEKAMP. 2003. Age estimation and dispersal in the spotted hyena (Crocuta crocuta). Journal of Mammalogy 84:1019-1030.
96. VAN HORN, R. C., H. E. WATTS, AND K. E. HOLEKAMP. 2008. Do female hyaenas choose mates based on tenure? Nature 454:E1.
97. VLADIC, T., AND T. JARVI. 2001. Sperm quality in the alternative reproductive tactics of Atlantic salmon: the importance of the loaded raffle mechanism. Proceedings of the Royal Society of London, B. Biological Sciences 268:2375-2381.
98. WANG, C., A. LEUNG, AND A. SINHA-HIKIM. 1993. Reproductive aging in the male brown-Norway rat: a model for the human. Endocrinology 133:2773.
99. WARD, P. I. 1998. Intraspecific variation in sperm size characters. Heredity 80:655-659.
100. WERDELIN, L., AND M. E. LEWIS. 2000. Carnivora from the South Turkwel hominid site, northern Kenya. Journal of Paleontology 74:1173-1180.
101. WILDT, D. E., ET AL. 1983. Unique seminal quality in the South African cheetah and a comparative evaluation in the domestic cat. Biology of Reproduction 29:1019-1025.
102. WILDT, D. E., ET AL. 1987. Similarity in ejaculate-endocrine characteristics in captive versus free-ranging cheetahs of two subspecies. Biology of Reproduction 36:351-360.
103. WOLF, K. N., ET AL. 2000. Age-dependent changes in sperm production, semen quality, and testicular volume in the black-footed ferret (Mustela nigripes). Biology of Reproduction 63:179-187.