Sperm competition selects for sperm quantity and quality in the Australian Maluridae

PLoS ONE

Volumn 6, Issue 1, 2011, Pages

  Rowe, Melissah ^a,b   Pruett Jones, Stephen ^a  

^a UNIVERSITY OF CHICAGO   (United States)

^b UNIVERSITY OF OSLO   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL TISSUE; ARTICLE; AUSTRALIA; BIRD; COMPARATIVE STUDY; CONTROLLED STUDY; MALE; MALURIDAE; NONHUMAN; SEMINIFEROUS TUBULE; SEXUAL SELECTION; SPERM COMPETITION; SPERMATOGENESIS; SPERMATOZOON COUNT; SPERMATOZOON MOTILITY; TESTIS SIZE; ANIMAL; COMPETITIVE BEHAVIOR; CYTOLOGY; FERTILIZATION; PHYSIOLOGY; REPRODUCTION; SONGBIRD; SPERMATOZOON; TESTIS;

MALURIDAE; TROGLODYTINAE;

ANIMALS; COMPETITIVE BEHAVIOR; FERTILIZATION; MALE; PASSERIFORMES; REPRODUCTION; SONGBIRDS; SPERM COUNT; SPERMATOZOA; TESTIS;

EID: 79551514296     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0015720     Document Type: Article

References (106)

1. Parker GA (1970) Sperm competition and its evolutionary consequences in the insects. Biol Rev 45: 525-567.
2. Møller AP (1991) Sperm competition, sperm depletion, paternal care, and relative testis size in birds. Am Nat 137: 882-906.
3. Harcourt AH, Purvis A, Liles L (1995) Sperm competition: mating system, not breeding season, affects testes size of primates. Funct Ecol 9: 468-476.
4. Hosken DJ (1997) Sperm competition in bats. Proc Roy Soc B 264: 385-392.
5. Stockley P, Gage MJG, Parker GA, Møller AP (1997) Sperm competition in fishes: the evolution of testis size and ejaculate characteristics. Am Nat 149: 933-954.
6. Hosken DJ, Ward PI (2001) Experimental evidence for testis size evolution via sperm competition. Ecol Lett 4: 10-13.
7. Byrne PG, Roberts JD, Simmons LW (2002) Sperm competition selects for increased testes mass in Australian frogs. J Evol Biol 15: 347-355.
8. Simmons LW, García-González F (2008) Evolutionary reduction in testes size and competitive fertilization success in response to the experimental removal of sexual selection in dung bettles. Evolution 62: 2580-2591.
9. Briskie JV, Montgomerie R (1992) Sperm size and sperm competition in birds. Proc Roy Soc B-Biol Sci 247: 89-95.
10. Dunn PO, Whittingham LA, Pitcher TE (2001) Mating systems, sperm competition, and the evolution of sexual dimorphism in birds. Evolution 55: 161-175.
11. Pitcher TE, Dunn PO, Whittingham LA (2005) Sperm competition and the evolution of testes size in birds. J Evol Biol 18: 557-567.
12. Immler S, Birkhead TR (2007) Sperm competition and sperm midpiece size: no consistent pattern in passerine birds. Proc Roy Soc B 274: 561-568.
13. Gage MJ (1991) Risk of sperm competition directly affects ejaculate size in the Mediterranean fruit fly. An Behav 42: 1036-1037.
14. Birkhead TR, Briskie JV, Møller AP (1993) Male sperm reserves and copulation frequency in birds. Behav Ecol Sociobiol 32: 85-93.
15. Firman RC, Simmons LW (2010) Experimental evolution of sperm quality via postcopulatory sexual selection in house mice. Evolution 64: 1245-1256.
16. Amann RP (1970) Sperm Production Rates. In: Johnson AD, Gomes WR, Vandemark NL, eds. The Testis Academic Press. pp 433-482.
17. de Reviers M, Williams JB (1984) Testis development and production of spermatozoa in the cockerel (Gallus domesticus). In Cunningham FJ, Lake PE, Hewitt D, eds. Reproductive Biology of Poultry Edited by British Poultry Science Ltd. pp 183-202.
18. Møller AP (1988) Testes size, ejaculate quality and sperm competition in birds. Biol J Linn Soc 33: 273-283.
19. Møller AP (1988) Ejaculate quality, testes size and sperm competition in primates. J Human Evol 17: 479-488.
20. Møller AP (1989) Ejaculate quality, testes size and sperm production in mammals. Funct Ecol 3: 91-96.
21. Schultz AH (1938) The relative weight of the testes in primates. Anat Rec 72: 387-394.
22. Lüpold S, Linz GM, Rivers JW, Westneat DF, Birkhead TR (2009) Sperm competition selects beyond relative testes size in birds. Evolution 63: 391-402.
23. Snook RR (2005) Sperm in competition: not playing by the numbers. Trends Ecol Evol 20: 46-53.
24. Pizzari T, Parker GA (2009) Sperm competition and sperm phenotype. In by Birkhead TR, Hosken DJ, Pitnick S, eds. Sperm Biology: An Evolutionary Perspective Academic Press. pp 205-244.
25. Birkhead TR, Martinez JG, Burke T, Froman DP (1999) Sperm mobility determines the outcome of sperm competition in the domestic fowl. Proc Roy Soc B-Biol Sci 266: 1759-1764.
26. Denk AG, Holzmann A, Peters A, Vermeirssen ELM, Kempenaers B (2005) Paternity in mallards: effects of sperm quality and female sperm selection for inbreeding avoidance. Behav Ecol 16: 825-833.
27. Pizzari T, Worley K, Burke T, Froman DP (2008) Sperm competition dynamics: ejaculate fertilising efficiency changes differentially with time. BMC Evol Biol 8: 332-338.
28. Gage MJG, Macfarlane CP, Yeates S, Ward RG, Searle JB, et al. (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, Simmons LW, Beveridge M, Evans JP (2010) Sperm swimming velocity predicts competitive fertilization success in the Green Swordtail Xiphophorus helleri. PLoSone 2010 5: e12146.
30. Malo AF, Garde JJ, Soler AJ, García AJ, Gomendio M, et al. (2005) Male fertility in natural populations of red deer is determined by sperm velocity and the proportion of normal spermatozoa. Biol Reprod 72: 822-829.
31. Kleven O, Fossøy F, Laskemoen T, Robertson RJ, Rudolfsen G, et al. (2009) Comparative evidence for the evolution of sperm swimming speed by sperm competition and female sperm storage duration in passerine birds. Evolution 63: 2466-2473.
32. Lüpold S, Calhim S, Immler S, Birkhead TR (2009) Sperm morphology and sperm velocity in passerine birds. Proc Roy Soc B 276: 1175-1181.
33. Fitzpatrick JL, Montgomerie R, Desjardins JK, Stiver KA, Kolm N, et al. (2009) Female promiscuity promotes the evolution of faster sperm in cichlid fishes. PNAS 106: 1128-1132.
34. Anderson MJ, Dixson AF (2002) Motility and the midpiece in primates. Nature 416: 496.
35. Gomendio M, Roldan ERS (1991) Sperm competition influences sperm size in mammals. Proc Biol Sci 243: 181-185.
36. Anderson MJ, Chapman SJ, Videan EN, Evans E, Fritz J, et al. (2007) Functional evidence for differences in sperm competition in humans and chimpanzees. Am J Phys Anth 134: 274-280.
37. Balshine S, Leach BJ, Neat F, Werner NY, Montgomerie R (2001) Sperm size of African cichlids in relation to sperm competition. Behav Ecol 12: 726-731.
38. Lüpold S, Linz GM, Birkhead TR (2009) Sperm design and variation in the New World blackbirds (Icteridae). Behav Ecol Sociobiol 63: 899-909.
39. Gage MJ, Freckleton RP (2003) Relative testis size and sperm morphometry across mammals: no evidence for an association between sperm competition and sperm length. Proc Roy Soc B 270: 625-632.
40. García-González F, Simmons LW (2005) Sperm viability matters in insect sperm competition. Curr Biol 15: 271-275.
41. Hunter FM, Birkhead TR (2002) Sperm viability and sperm competition in insects. Curr Biol 12: 121-123.
42. Rowley I, Russell E (1997) Fairy-wrens and grasswrens: Maluridae. Oxford University Press, Oxford.
43. Christidis L (1999) Evolution and biogeography of the Australian grasswrens, Amytornis (Aves: Maluridae): Biochemical perspectives. Aust J Zool 47: 113-124.
44. Harrison CJO (1969) The affinities of the blue wren genus Malurus and related genera with special reference to the grass wren genus Amytornis. Emu 69: 1-8.
45. Maguire GS, Mulder RA (2004) Breeding biology and demography of the southern emu-wren (Stipiturus malachurus). Aust J Zool 52: 583-604.
46. Kingma SA, Hall ML, Segelbacher G, Peters A (2009) Radical loss of an extreme extra-pair mating system. BMC Ecol 9: 15-25.
47. Mulder RA, Dunn PO, Cockburn A, Lazenby-Cohen KA, Howell MJ (1994) Helpers liberate female fairy-wrens from constraints on extra-pair mate choice. Proc Roy Soc London B- Biol Sci 255: 223-229.
48. Brooker MG, Rowley I, Adams M, Baverstock PR (1990) Promiscuity an inbreeding avoidance mechanism in a socially monogamous species. Behav Ecol Sociobiol 26: 191-200.
49. Karubian J (2002) Costs and benefits of variable breeding plumage in the redbacked fairy-wren. Evolution 56: 1673-1682.
50. Webster MS, Tarvin KA, Tuttle EM, Pruett-Jones S (2004) Reproductive promiscuity in the splendid fairy-wren: effects of group size and auxiliary reproduction. Behav Ecol 15: 907-915.
51. Maguire GS, Mulder RA (2008) Low levels of extra-pair paternity in southern emu-wrens (Aves: Maluridae). Aust J Zool 56: 79-84.
52. Webster MS, Varian CW, Karubian J (2008) Plumage color and reproduction in the red-backed fairy-wren: Why be a dull breeder? Behav Ecol 19: 517-524.
53. Rowe M, Pruett-Jones S (2006) Reproductive biology and sperm competition in Australian fairy-wrens. Avian Poultry Biol Rev 17: 21-37.
54. Møller AP, Briskie JV (1995) Extra-pair paternity, sperm competition and the evolution of testis size in birds. Behavioral Ecology and Sociobiology 36: 357-365.
55. Griffith SC, Owens IPF, Thuman KA (2002) Extra pair paternity in birds: a review of interspecific variation and adaptive function. Mol Ecol 11: 2195-2212.
56. Tuttle EM, Pruett-Jones S, Webster MS (1996) Cloacal protuberances and extreme sperm production in Australian fairy-wrens. Proc Roy Soc B 263: 1359-1364.
57. Taborsky M (1998) Sperm competition in fish: 'bourgeois' males and parasitic spawning. Trends Ecol Evol 13: 222-227.
58. Wolfson A (1952) The cloacal protuberance - a means for determining breeding condition in live male passerines. Bird-Banding 23: 159-165.
59. Gee GF, Bertschinger H, Donoghue AM, Blanco J, Soley J (2004) Reproduction in nondomestic birds: Physiology, semen collection, artificial insemination and cryopreservation. Avian Poult Biol Rev 15: 47-101.
60. Rowe M, Swaddle JP, Pruett-Jones S, Webster MS (2010) Plumage coloration, ejaculate quality and reproductive phenotype in the red-backed fairy-wren. An Behav 79: 1239-1246.
61. Lessells CM, Boag PT (1987) Unrepeatable repeatabilities: a common mistake. Auk 104: 116-121.
62. Laskemoen T, Kleven O, Fossøy F, Robertson RJ, Rudolfsen G, et al. (2010) Sperm quantity and quality effects on fertilization success in a highly promiscuous passerine, the tree swallow Tachycineta bicolor. Behav Ecol Sociobiol 64: 1473-1484.
63. Wishart GJ, Wilson YI (1997) Sperm motility and metabolism I. Visual scoring of motility using the hanging drop method. In Bakst MR, Cecil HC, eds. Techniques for Semen Evaluation, Semen Storage, and Fertility Determination The Poultry Science Association.
64. Penfold LM, Wildt DE, Herzog TL, Lynch W, Ware L, et al. (2000) Seasonal patterns of LH, testosterone and semem quality in the Northern pintail duck (Anas acuta). Reprod Fert Devel 12: 229-235.
65. Cooper DM, Rowell JG (1958) Relations between fertility, embryonic survival and some semen characteristics in the chicken. Poultry Science 37: 699-707.
66. Bakst MR, Cecil HC (1997) Sperm viability I. Nigrosin/eosin stain for determining live/dead and abnormal sperm counts. In Bakst MR, Cecil HC, eds. Techniques for Semen Evaluation, Semen Storage, and Fertility Determination The Poultry Science Association. pp 29-34.
67. Tuttle EM, Pruett-Jones SG (2004) Estimates of extreme sperm production: morphological and experimental evidence from reproductively promiscuous fairy-wrens (Malurus). An Behav 68: 541-550.
68. Birkhead TR, Petrie M (1995) Ejaculate features and sperm utilization in peafowl Pavo cristatus. Proc Roy Soc Lond B-Biol Sci 261: 153-158.
69. Wishart GJ, Lindsay C, Staines HJ, McCormick P (2002) Semen quality in captive Houbara bustard, Chlamydotis undulata undulata. Reprod Fert Devel 14: 401-405.
70. Ciereszko A, Rybnik PK, Horbańczuk JO, Dietrich GJ, Deas A, et al. (2010) Biochemical characterization and sperm motility parameters of ostrich (Stuthio camelus) semen. An Reprod Sci 122: 222-228.
71. Sontakke SD, Umapathy G, Sivaram V, Kholkute SD, Shivaji S (2004) Semen characteristics, cryopreservation, and successful artificial insemination in the Blue rock pigeon (Columba livia). Theriogenology 62: 139-153.
72. R Development Core Team (2010) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0. Available: http://www.R-project.org.
73. Felsenstein J (1985) Phylogenies and the comparative method. Am Nat 125: 1-15.
74. Pagel M (1999) Inferring the historical patterns of biological evolution. Nature 401: 877-884.
75. Freckleton RP, Harvey PH, Pagel M (2002) Phylogenetic analysis and comparative data: a test and review of evidence. Am Nat 160: 712-726.
76. Paradis E, Claude J, Strimmer K (2004) APE: analysis of phylogenetics and evolution in R language. Bioinformatics 20: 289-290.
77. Christidis L, Schodde R (1997) Relationships within the Australo-Papuan fairywrens (Aves: Malurinae): An evaluation of the utility of allozyme data. Aust J Zool 45: 113-129.
78. Driskell AC, Norman JA, Pruett-Jones S, Mangall E, Sonsthagen S, et al. (2011) A multigene phylogeny examining evolutionary and ecological relationships in the Australo Papuan wrens of the subfamily Malurinae (Aves). Mol Phylo Evol, in press.
79. Martin PA, Reimers TJ, Lodge JR, Dziuk PJ (1974) The effect of ratios and numbers of spermatozoa mixed from two males on proportions of offspring. J Reprod Fert 39: 251-258.
80. Parker GA (1982) Why are there so many tiny sperm? Sperm competition and the maintenance of two sexes. J Theor Biol 96: 281-294.
81. Birkhead TR, Pizzari T (2002) Postcopulatory sexual selection. Nat Rev Gene 3: 262-273.
82. Briskie JV (1993) Anatomical adaptations to sperm competition in Smith's Longspurs and other polygynandrous passerines. Auk 110: 875-888.
83. Mulder RA, Cockburn A (1993) Sperm competition and the reproductive anatomy of male superb fairy-wrens. Auk 110: 588-593.
84. Double M, Cockburn A (2000) Pre-dawn infidelity: Females control extra-pair mating in superb fairy-wrens. Proc Roy Soc Lond B-Biol Sci 267: 465-470.
85. Birkhead TR, Fletcher F, Pellatt EJ, Staples A (1995) Ejaculate quality and the success of extra-pair copulation in the zebra finch. Nature 377: 422-424.
86. Clulow J, Jones RC (1982) Production, transport, maturation, storage and survival of spermatozoa in the male Japanese quail, Coturnix coturnix. J Reprod Fert 64: 259-266.
87. Westneat DF, McGraw LA, Fraterrigo JM, Birkhead TR, Fletcher F (1998) Patterns of courtship behavior and ejaculate characteristics in male red-winged blackbirds. Behav Ecol Sociobiol 43: 161-171.
88. Amann RP (1981) A critical review of methods for evaluation of spermatogenesis from seminal characteristics. J Andrology 2: 37-58.
89. Lin M, Jones RC, Blackshaw AW (1990) The cycle of the seminiferous epithelium in the Japanes quail (Coturnix coturnix japonica) and estimation of its duration. J Reprod Fert 88: 481-490.
90. Noirault J, Brillard J-P, Bakst MR (2006) Spermatogenesis in the turkey (Meleagris gallopavo): Quantitative approach in immature and adult males subjected to various photoperiods. Theriogenology 65: 845-859.
91. Peirce EJ, Breed WG (2001) A comparative study of sperm production in two species of Australian arid zone rodents (Pseudomys australis, Notomys alexis) with marked differences in testis size. Reproduction 121: 239-247.
92. Parapanov R, NussléS, Hausser J, Vogel P (2008) Relationships of basal metabolic rate, relative testis size and cycle length of spermatogenesis in shrews (Mammalia, Soricidae). Reprod Fert Devel 20: 431-439.
93. Ramm SA, Stockley P (2010) Sperm competition and sperm length influence the rate of mammalian spermatogenesis. Biol Lett 6: 219-221.
94. Froman DP, Wardell JC, Feltmann AJ (2006) Sperm mobility: deduction of a model explaining phenotypic variation in roosters (Gallus domesticus). Biol Reprod 74: 487-491.
95. Allen TE, Grigg GW (1958) Sperm transport in the fowl. Aust J Ag Res 8: 788-799.
96. Lake P (1975) Gamete production and the fertile period with particular reference to domesticated birds. Symp Zool Soc Lond 35: 225-244.
97. Cohen J (1967) Correlation between sperm ''redundancy'' and chiasma frequency. Nature 215: 862-863.
98. Cohen J (1973) Cross-overs, sperm redundancy and their close association. Heredity 31: 408-413.
99. Blumenstiel JP (2010) Sperm competition can drive a male-biased mutation rate. J Theo Biol 249: 624-632.
100. Aitken RJ, Roman SD (2008) Antioxidant systems and oxidative stress in the testes. Oxidative Medicine and Cellular Longevity 1: 15-24.
101. Fujihara N, Howarth B (1978) Lipid peroxidation in fowl spermatozoa. Poult Sci 57: 1766-1768.
102. Wishart GJ (1984) Effects of lipid peroxide formation in fowl semen on sperm motility, ATP content and fertilizing ability. J Reprod Fert 71: 113-118.
103. Costantini D, Rowe M, Butler MW, McGraw KJ (2010) From molecules to living systems: historical and contemporary issues in oxidative stress and antioxidant ecology. Funct Ecol 24: 950-959.
104. Froman DP, Pizzari T, Feltman AJ, Castillo-Juarez H, Birkhead TR (2002) Sperm mobility: mechanisms of fertilizing efficiency, genetic variation and phenotypic relationship with male status in the domestic fowl, Gallus gallus domesticus. Proc Roy Soc B 269: 607-612.
105. Rowe M, McGraw KJ (2008) Carotenoids in the seminal fluid of wild birds: interspecific variation in fairy-wrens. Condor 110: 694-700.
106. Chapman T (2001) Seminal fluid-mediated fitness traits in Drosophila. Heredity 87: 511-521.