Mass-specific metabolic rate and sperm competition determine sperm size in marsupial mammals

PLoS ONE

Volumn 6, Issue 6, 2011, Pages

  Tourmente, Maximiliano ^a   Gomendio, Montserrat ^a   Roldan, Eduardo R S ^a  

^a MUSEO NACIONAL DE CIENCIAS NATURALES   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ARTICLE; BODY MASS; BODY SIZE; CELL SIZE; MALE; MALE GENITAL TRACT PARAMETERS; MARSUPIAL; METABOLIC RATE; NONHUMAN; SPECIES DIFFERENCE; SPERM COMPETITION; SPERM SIZE; ANIMAL; BASAL METABOLIC RATE; BODY WEIGHT; CYTOLOGY; FEMALE; HISTOLOGY; ORGAN SIZE; PHYSIOLOGY; SPERMATOZOON; TESTIS;

ANIMALIA; EUTHERIA; MAMMALIA; METATHERIA;

ANIMALS; BASAL METABOLISM; BODY WEIGHT; CELL SIZE; FEMALE; MALE; MARSUPIALIA; ORGAN SIZE; SPERMATOZOA; TESTIS;

EID: 79959483231     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0021244     Document Type: Article

References (67)

1. Cummins JM, Woodall PF, (1985) On mammalian sperm dimensions. J Reprod Fert 75: 153-175.
2. Pitnick S, Markow TA, Spicer GS, (1995) Delayed male maturity is a cost of producing large sperm in Drosophila. Proc Natl Acad Sci USA 92: 10614-10618.
3. Gomendio M, Roldan ERS, (1991) Sperm competition influences sperm size in mammals. Proc R Soc B 243: 181-185.
4. Gomendio M, Roldan ERS, (2008) Implications of diversity in sperm size and function for sperm competition and fertility. Int J Dev Biol 52: 439-447.
5. Fitzpatrick JL, Montgomerie R, Desjardins JK, Stiver KA, Kolm N, Balshine S, (2009) Female promiscuity promotes the evolution of faster sperm in cichlid fishes. Proc Natl Acad Sci USA 106: 1128-1132.
6. Lüpold S, Calhim S, Immler S, Birkhead TR, (2009) Sperm morphology and sperm velocity in passerine birds. Proc R Soc B 276: 1175-1181.
7. Tourmente M, Gomendio M, Roldan ERS, Giojalas L, Chiaraviglio M, (2009) Sperm competition and reproductive mode influence sperm dimensions and structure among snakes. Evolution 63: 2513-2524.
8. Tourmente M, Gomendio M, Roldan ERS, (2011) Sperm competition and the evolution of sperm design in mammals. BMC Evol Biol 11: 12.
9. Hosken DJ, (1997) Sperm competition in bats. Proc R Soc B 264: 385-392.
10. Gage MJG, Freckleton R, (2003) Relative testis size and sperm morphometry across mammals: no evidence for an association between sperm competition and sperm length. Proc R Soc B 270: 625-632.
11. Anderson M J, Dixson AF, (2002) Sperm competition: motility and the midpiece in primates. Nature 416: 496.
12. Anderson MJ, Nyholt J, Dixson AF, (2005) Sperm competition and the evolution of sperm midpiece volume in mammals. J Zool 267: 135-145.
13. Malo AF, Gomendio M, Garde J, Lang-Lenton B, Soler AJ, Roldan ERS, (2006) Sperm design and sperm function. Biol Lett 2: 246-249.
14. Gomendio M, Tourmente M, Roldan ERS, (2011) Why mammalian lineages respond differently to sexual selection: metabolic rate constrains the evolution of sperm size. Proc R Soc B in press (doi: 10.1098/rspb.2011.0275).
15. Sibly RM, Brown JH, (2007) Effects of body size and lifestyle on evolution of mammal life histories. Proc Natl Acad Sci USA 104: 17707-17712.
16. Savage VM, Allen AP, Brown JH, Gillooly JF, Herman AB, et al. (2007) Scaling of number, size, and metabolic rate of cells with body size in mammals. Proc Natl Acad Sci USA 104: 4718-4723.
17. Rose RW, Nevison CM, Dixson AF, (1997) Testes weight, body weight and mating system in marsupials and monotremes. J Zool Lond 243: 523-531.
18. Taggart DA, Breed WG, Temple-Smith PD, Purvis A, Shimmin G, (1998) Reproduction, mating strategies and sperm competition in marsupials and monotremes. In: Birkhead TR, Møller AP, editors. Sperm competition and sexual selection San Diego Academic Press pp. 623-666.
19. Taggart DA, Shimmin GA, Dickman CR, Breed WG, (2003) Reproductive biology of carnivorous marsupials: Clues to the likelihood of sperm competition. In: Jones M, Dickman CR, Archer M, editors. Predators with pouches: the biology of carnivorous marsupials Collingwood CSIRO pp. 358-375.
20. Paplinska JZ, Bencini R, Fisher DO, Newell GR, Goldizen AW, et al. (2010) Sperm competition in the Macropodoidea: a review of evidence. In: Coulson G, Eldridge M, editors. Macropods: The biology of kangaroos, wallabies and rat-kangaroos Collingwood CSIRO pp. 66-76.
21. Tyndale-Biscoe H, (2005) Life of marsupials. Collingwood CSIRO.
22. Weisbecker V, Goswami A, (2010) Brain size, life history and metabolism at the marsupial/placental dichotomy. Proc Natl Acad Sci USA 107: 16216-16221.
23. Fitzpatrick JL, Garcia-Gonzalez F, Evans JP, (2010) Linking sperm length and velocity: the importance of intramale variation. Biol Lett 6: 797-799.
24. Froman DP, Feltmann AJ, Rhoads ML, Kirby JD, (1999) Sperm mobility: A primary determinant of fertility in the domestic fowl (Gallus domesticus). Biol Reprod 61: 400-405.
25. Levitan DR, (2000) Sperm velocity and longevity trade-off and influence fertilization in the sea urchin Lytechinus variegatus. Proc R Soc B 267: 531-534.
26. Malo AF, Garde J, Soler AJ, García AJ, Gomendio M, Roldan ERS, (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.
27. Birkhead TR, Martinez JG, Burke T, Froman DP, (1999) Sperm mobility determines the outcome of sperm competition in the domestic fowl. Proc R Soc B 266: 1759-1764.
28. Gage MJG, Macfarlane CP, Yeates S, Ward RG, Searle JB, Parker GA, (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. Turner RM, (2006) Moving to the beat: a review of mammalian sperm motility regulation. Reprod Fertil Dev 18: 25-38.
30. Narisawa S, Hecht NB, Goldberg E, Boatright KM, Reed JC, Millan JL, (2002) Testis-specific cytochrome c-null mice produce functional sperm but undergo early testicular atrophy. Mol Cell Biol 22: 5554-5562.
31. Miki K, Qu W, Goulding EH, Willis WD, Bunch DO, et al. (2004) Glyceraldehyde 3-phosphate dehydrogenase-S, a sperm-specific glycolytic enzyme, is required for sperm motility and male fertility. Proc Natl Acad Sci USA 101: 16501-16506.
32. Eddy EM, Toshimori K, O'Brien DA, (2003) Fibrous sheath of mammalian spermatozoa. Microsc Res Tech 61: 103-115.
33. Eddy EM, (2007) The scaffold role of the fibrous sheath. In: Roldan ERS, Gomendio M, editors. Spermatology Nottingham Nottingham University Press pp. 45-62.
34. Miki K, Willis W, Brown P, Goulding E, Fulcher K, Eddy EM, (2002) Targeted disruption of the AKAP4 gene causes defects in sperm flagellum and motility. Dev Biol 248: 331-342.
35. Parker GA, (1998) Sperm competition and the evolution of ejaculates: towards a theory base. In: Birkhead TR, Møller AP, editors. In: Spermcompetition and sexual selection San Diego Academic Press pp. 3-54.
36. Jones KE, Bielby J, Cardillo M, Fritz SA, O'Dell J, et al. (2009) PanTheria: a species-level database of life history, ecology, and geography of extant and recently extinct mammals. Ecology 90: 2648.
37. Møller AP, (1988) Ejaculate quality, testes size and sperm competition in primates. J Hum Evol 17: 479-488.
38. Møller AP, (1989) Ejaculate quality, testes size and sperm production in mammals. Funct Ecol 3: 91-96.
39. Rowe M, Pruett-Jones S, (2011) Sperm competition selects for sperm quantity and quality in the Australian Maluridae. PLoS One 6: e15720.
40. Parker GA, (1982) Why are there so many tiny sperm? Sperm competition and the maintenance of two sexes. J Theor Biol 96: 281-294.
41. Parker GA, (1984) Sperm competition and the evolution of animal mating strategies. In: Sperm competition and the evolution of animal mating systems. Smith RL, editor. London: Academic Press. pp 1-60.
42. Dewsbury DA, (1982) Ejaculate cost and male choice. Am Nat 279: 601-610.
43. Nakatsuru K, Kramer DL, (1982) Is sperm cheap? Limited male fertility and female choice in the lemon tetra (Pisces, Characidae). Science 216: 753-755.
44. Olsson M, Madsen T, Shine R, (1997) Is sperm really so cheap? Costs of reproduction in male adders, Vipera berus. Proc R Soc B 264: 455-459.
45. Pitnick S, Wolfner MF, Suarez SS, (2009) Ejaculate-female and sperm-female interactions. In: Birkhead TR, Hosken DJ, Pitnick S, editors. Sperm biology: An evolutionary perspective Burlington Academic Press pp. 247-304.
46. Pizzari T, Parker GA, (2009) Sperm competition and sperm phenotype. In: Birkhead TR, Hosken DJ, Pitnick S, editors. Sperm biology: An evolutionary perspective Burlington Academic Press pp. 207-245.
47. Parker GA, Immler S, Pitnick S, Birkhead TR, (2010) Sperm competition games: sperm size (mass) and number under raffle and displacement, and the evolution of P2. J Theor Biol 264: 1003-1023.
48. Bedford JM, Rodger JC, Breed WG, (1984) Why so many mammalian spermatozoa- a clue from marsupials? Proc R Soc B 221: 221-233.
49. Gomendio M, Harcourt AH, Roldan ERS, (1998) Sperm competition in mammals. In: Birkhead TR, Møller AP, editors. In: Sperm competition and sexual selection San Diego Academic Press pp. 667-756.
50. Soulsbury CD, (2010) Genetic patterns of paternity and testes size in mammals. PLoS One 5: e9581.
51. Felsenstein J, (1985) Phylogenies and the comparative method. Am Nat 125: 1-15.
52. Harvey PH, Pagel MD, (1991) The comparative method in evolutionary biology. Oxford Oxford University Press.
53. Freckleton R, Harvey PH, Pagel MD, (2002) Phylogenetic analysis and comparative data: a test and review of evidence. Am Nat 160: 712-726.
54. Meredith RW, Westerman M, Case JA, Springer MS, (2008) A phylogeny and timescale for marsupial evolution based on sequences for five nuclear genes. J Mammal Evol 15: 1-36.
55. Beck RMD, (2008) A dated phylogeny of marsupials using a molecular supermatrix and multiple fossil constraints. J Mammal 89: 175-189.
56. Westerman M, Young J, Krajewski C, (2008) Molecular relationships of species of Pseudantechinus, Parantechinus and Dasykaluta (Marsupialia: Dasyuridae). Aus Mammal 29: 201-212.
57. Meredith RW, Westerman M, Springer MS, (2008) A phylogeny and timescale for the living genera of kangaroos and kin (Macropodiformes: Marsupialia) based on nuclear DNA sequences. Aus J Zool 56: 395-410.
58. Meredith RW, Westerman M, Springer MS, (2009) A phylogeny of Diprotodontia (Marsupialia) based on sequences for five nuclear genes. Mol Phylogenet Evol 51: 554-571.
59. Phillips MJ, Pratt RC, (2008) Family-level relationships among the Australasian marsupial ''herbivores'' (Diprotodontia: koala, wombats, kangaroos and possums). Mol Phylogenet Evol 46: 594-605.
60. Nagakawa S, (2004) A farewell to Bonferroni: the problems of low statistical power and publication bias. Behav Ecol 15: 1044-1045.
61. Rosenthal R, (1991) Meta-analytic procedures for social research. Newbury Park SAGE Publications.
62. Rosenthal R, (1994) Parametric measures of effect size. In: Cooper H, Hedges L, editors. New York SAGE Publications pp. 231-244 In: The handbook of research synthesis.
63. Rosnow R, Rosenthal R, (2003) Effect sizes for experimenting psychologists. Can J Exp Psychol 57: 221-237.
64. Cohen J, (1988) Statistical power analysis for the behavioral sciences. New Jersey Erlbaum Hillsdale.
65. Smithson M, (2003) Confidence intervals. London SAGE Publications.
66. Kenagy GJ, Trombulak SC, (1986) Size and function of mammalian testes in relation to body size. J Mammal 67: 1-22.
67. Tomkins JL, Simmons LW, (2002) Measuring relative investment: a case study of testes investment in species with alternative male reproductive tactics. Anim Behav 63: 1009-1016.