No evidence of trade-offs in the evolution of sperm numbers and sperm size in mammals

Journal of Evolutionary Biology

Volumn 28, Issue 10, 2015, Pages 1816-1827

  Tourmente, M ^a   Delbarco Trillo, J ^b   Roldan, E R S ^a  

^a MUSEO NACIONAL DE CIENCIAS NATURALES   (Spain)

^b LIVERPOOL JOHN MOORES UNIVERSITY   (United Kingdom)

Author keywords

Energetic constraints; Metabolic rate; Sexual selection; Sperm competition; Sperm numbers; Sperm size

Indexed keywords

BIOENERGETICS; EVOLUTIONARY BIOLOGY; FITNESS; MAMMAL; METABOLISM; REPRODUCTIVE BIOLOGY; REPRODUCTIVE COST; SEXUAL SELECTION; SIZE; SPERM; SPERM COMPETITION; TRADE-OFF;

ANIMALIA; EUTHERIA; MAMMALIA; METATHERIA;

CYTOLOGY; HUMAN; MALE; ORGAN SIZE; SPERMATOZOON; SPERMATOZOON COUNT; TESTIS;

HUMANS; MALE; ORGAN SIZE; SPERM COUNT; SPERMATOZOA; TESTIS;

EID: 84943665892     PISSN: 1010061X     EISSN: 14209101     Source Type: Journal    
DOI: 10.1111/jeb.12698     Document Type: Article

References (98)

1. Agnarsson, I. & May-Collado, L.J. 2008. The phylogeny of Cetartiodactyla: the importance of dense taxon sampling, missing data, and the remarkable promise of cytochrome b to provide reliable species-level phylogenies. Mol. Phylogenet. Evol. 48: 964-985.
2. Ambriz, D., Rosales, A.M., Sotelo, R., Mora, J.A., Rosado, A. & García, A.R. 2002. Changes in the quality of rabbit semen in 14 consecutive ejaculates obtained every 15 Minutes. Syst. Biol. Reprod. Med. 48: 389-395.
3. Anderson, M.J., Dixson, A.S. & Dixson, A.F. 2006. Mammalian sperm and oviducts are sexually selected: evidence for co-evolution. J. Zool. 270: 682-686.
4. Aulerich, R.J., Ringer, R.K. & Sloan, C.S. 1972. Electro ejaculation of mink (Mustela vison). J. Anim. Sci. 34: 230-233.
5. Austin, C.R. & Short, R.V. 1985. Reproduction in Mammals: Volume 4, Reproductive Fitness. Cambridge University Press, Cambridge, UK.
6. delBarco-Trillo, J. 2011. Adjustment of sperm allocation under high risk of sperm competition across taxa: a meta-analysis. J. Evol. Biol. 24: 1706-1714.
7. delBarco-Trillo, J., Tourmente, M. & Roldan, E.R.S. 2013. Metabolic rate limits the effect of sperm competition on mammalian spermatogenesis. PLoS ONE 8: e76510.
8. Bedford, J.M., Rodger, J.C. & Breed, W.G. 1984. Why so many mammalian spermatozoa - a clue from marsupials? Proc. R. Soc. Lond. B Biol. Sci. 221: 221-233.
9. Bininda-Emonds, O.R.P., Cardillo, M., Jones, K.E., MacPhee, R.D., Beck, R.M., Grenyer, R. et al. 2007. The delayed rise of present-day mammals. Nature 446: 507-512.
10. Birkhead, T.R. 1992. Sperm storage and the fertile period in the Bengalese finch. Auk 109: 620-625.
11. Birkhead, T.R. & Møller, A.P. 1998. Sperm Competition and Sexual Selection. Academic Press, San Diego, CA, USA.
12. Birkhead, T.R., Sheldon, B.C. & Fletcher, F. 1994. A comparative study of sperm-egg interactions in birds. J. Reprod. Fertil. 101: 353-361.
13. Birkhead, T.R., G ., M.J., Burke, T. & Froman, D.P. 1999. Sperm mobility determines the outcome of sperm competition in the domestic fowl. Proc. R. Soc. Lond. B Biol. Sci. 266: 1759-1764.
14. Birkhead, T.R., Hosken, D.J. & Pitnick, S.S. 2009. Sperm Biology: An Evolutionary Perspective. Academic Press, Burlington, MA, USA.
15. Brillard, J.P. & Bakst, M.R. 1990. Quantification of spermatozoa in the sperm storage tubules of turkey hens and the relation to sperm numbers in the perivitelline layer of eggs. Biol. Reprod. 43: 271-275.
16. Briskie, J.V., Montgomerie, R. & Birkhead, T.R. 1997. The evolution of sperm size in birds. Evolution 51: 937-945.
17. Burkitt, M., Walker, D., Romano, D.M. & Fazeli, A. 2012. Using computational modeling to investigate sperm navigation and behavior in the female reproductive tract. Theriogenology 77: 703-716.
18. Coy, P. & Aviles, M. 2010. What controls polyspermy in mammals, the oviduct or the oocyte? Biol. Rev. Camb. Philos. Soc. 85: 593-605.
19. Coy, P., Garcia-Vazquez, F.A., Visconti, P.E. & Aviles, M. 2012. Roles of the oviduct in mammalian fertilization. Reproduction 144: 649-660.
20. Dewsbury, D.A. 1982. Ejaculate cost and male choice. Am Nat 119: 601-610.
21. Dubey, S., Salamin, N., Ohdachi, S.D., Barriere, P. & Vogel, P. 2007. Molecular phylogenetics of shrews (Mammalia: Soricidae) reveal timing of transcontinental colonizations. Mol. Phylogenet. Evol. 44: 126-137.
22. Eisenbach, M. & Giojalas, L.C. 2006. Sperm guidance in mammals - an unpaved road to the egg. Nat. Rev. Mol. Cell Biol. 7: 276-285.
23. Fabre, P., Hautier, L., Dimitrov, D. & Douzery, E.J. 2012. A glimpse on the pattern of rodent diversification: a phylogenetic approach. BMC Evol. Biol. 12: 88.
24. Felsenstein, J. 1985. Phylogenies and the comparative method. Am Nat 125: 1-15.
25. Fitzpatrick, J.L., Montgomerie, R., Desjardins, J.K., Stiver, K.A., Kolm, N. & Balshine, S. 2009. Female promiscuity promotes the evolution of faster sperm in cichlid fishes. Proc. Natl Acad. Sci. USA 106: 1128-1132.
26. Flynn, J.J., Finarelli, J.A., Zehr, S., Hsu, J. & Nedbal, M.A. 2005. Molecular phylogeny of the carnivora (mammalia): assessing the impact of increased sampling on resolving enigmatic relationships. Syst. Biol. 54: 317-337.
27. Freckleton, R.P., Harvey, P.H. & Pagel, M. 2002. Phylogenetic analysis and comparative data: A test and review of evidence. Am Nat 160: 712-726.
28. Froman, D.P. & Kirby, J.D. 2005. Sperm mobility: phenotype in roosters (Gallus domesticus) determined by mitochondrial function. Biol. Reprod. 72: 562-567.
29. Gage, M.J.G. 1994. Associations between body size, mating pattern, testis size and sperm lengths across butterflies. Proc. R. Soc. Lond. B Biol. Sci. 258: 247-254.
30. Gage, M.J.G., Macfarlane, C.P., Yeates, S., Ward, R.G., Searle, J.B. & Parker, G.A. 2004. Spermatozoal Traits and Sperm Competition in Atlantic Salmon. Curr. Biol. 14: 44-47.
31. Gasparini, C., Simmons, L.W., Beveridge, M. & Evans, J.P. 2010. Sperm swimming velocity predicts competitive fertilization success in the green swordtail Xiphophorus helleri. PLoS ONE 5: e12146.
32. Gomendio, M. & Roldan, E.R.S. 1991. Sperm competition influences sperm size in mammals. Proc. R. Soc. Lond. B Biol. Sci. 243: 191-185.
33. Gomendio, M. & Roldan, E.R.S. 1993. Coevolution between male ejaculates and females reproductive biology in eutherian mammals. Proc. R. Soc. Lond. B Biol. Sci. 252: 7-12.
34. Gomendio, M. & Roldan, E.R.S. 2008. Implications of diversity in sperm size and function for sperm competition and fertility. Int. J. Dev. Biol. 52: 439-447.
35. Gomendio, M., Harcourt, A.H. & Roldan, E.R.S. 1998. Sperm competition in mammals. In: Sperm Competition and Sexual Selection (T.R. Birkhead & A.P. Møller, eds), pp. 667-755. Academic Press, San Diego, CA, USA.
36. Gomendio, M., Tourmente, M. & Roldan, E.R.S. 2011. Why mammalian lineages respond differently to sexual selection: metabolic rate constrains the evolution of sperm size. Proc. R. Soc. Lond. B Biol. Sci. 278: 3135-3141.
37. Gomez Montoto, L., Magana, C., Tourmente, M., Martin-Coello, J., Crespo, C., Luque-Larena, J.J. et al. 2011a. Sperm competition, sperm numbers and sperm quality in muroid rodents. PLoS ONE 6: e18173.
38. Gomez Montoto, L., Varea Sanchez, M., Tourmente, M., Martin-Coello, J., Luque-Larena, J.J., Gomendio, M. et al. 2011b. Sperm competition differentially affects swimming velocity and size of spermatozoa from closely related muroid rodents: head first. Reproduction 142: 819-830.
39. Guidobaldi, H.A., Teves, M.E., Unates, D.R. & Giojalas, L.C. 2012. Sperm transport and retention at the fertilization site is orchestrated by a chemical guidance and oviduct movement. Reproduction 143: 587-596.
40. Harcourt, A.H., Harvey, P.H., Larson, S.G. & Short, R.V. 1981. Testis weight, body wheight and breeding system in primates. Nature 293: 55-57.
41. Harper, M.J.K. 1982. Sperm egg and transport. In: Germ Cells and Fertilization, vol. 1 (C.R. Austin & R.V. Short, eds), pp. 102-127. Cambridge University Press, Cambridge, UK.
42. Harvey, P.H. & Pagel, J.E. 1991. The Comparative Method in Evolutionary Biology. Oxford University Press, Oxford, UK.
43. Hess, R.A. & Franca, L.R. 2008. Spermatogenesis and cycle of the seminiferous epithelium. In: Molecular Mechanisms in Spermatogenesis (C.Y. Cheng, ed.), pp. 1-15. Landes Bioscience, Austin, TX, USA.
44. Hosken, D.J. & Ward, P.I. 2001. Experimental evidence for testis size evolution via sperm competition. Ecol. Lett. 4: 10-13.
45. Hunter, R.H.F. 1993. Sperm:egg ratios and putative molecular signals to modulate gamete interactions in oolytocous mammals. Mol. Reprod. Dev. 35: 324-327.
46. Hunter, R.H. 1996. Ovarian control of very low sperm egg ratios at the commencement of mammalian fertilization to avoid polyspermy. Mol. Reprod. Dev. 44: 417-422.
47. Hunter, R.H. 2012. Components of oviduct physiology in eutherian mammals. Biol. Rev. Camb. Philos. Soc. 87: 244-255.
48. Immler, S., Pitnick, S., Parker, G.A., Durrant, K.L., Lüpold, S., Calhim, S. et al. 2011. Resolving variation in the reproductive tradeoff between sperm size and number. Proc. Natl Acad. Sci. USA 108: 5325-5330.
49. Ishijima, S. 2012. Comparative analysis of movement characteristics of lancelet and fish spermatozoa having different morphologies. Biol. Bull. 222: 214-221.
50. Johnson, L. & Thompson, D.L. 1983. Age-related and seasonal variation in the Sertoli cell population, daily sperm production and serum concentrations of Follicle-stimulating hormone, Luteinizing hormone and Testosterone in stallions. Biol. Reprod. 29: 777-789.
51. Kelly, C.D. & Jennions, M.D. 2011. Sexual selection and sperm quantity: meta-analyses of strategic ejaculation. Biol. Rev. 86: 863-884.
52. Kleven, O., Føssoy, F., Laskemoen, T., Robertson, R.J., Rudolfsen, G. & Lifjeld, J.T. 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.
53. Kunhbar, H.K., Samo, M.U., Memon, A. & Solangi, A.A. 2003. Biometrical studies of reproductive organs of Thari cows. Pak. J. Biol. Sci. 6: 322-324.
54. Lüpold, S. 2013. Ejaculate quality and constraints in relation to sperm competition levels among eutherian mammals. Evolution 67: 3052-3060.
55. Lüpold, S., Calhim, S., Immler, S. & Birkhead, T.R. 2009. Sperm morphology and sperm velocity in passerine birds. Proc. R. Soc. Lond. B Biol. Sci. 276: 1175-1181.
56. Malo, A.F., Garde, J.J., Soler, A.J., Garcia, A.J., Gomendio, M. & Roldan, E.R.S. 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.
57. Mattner, P.E. & Voglmayr, J.K. 1962. A comparison of ram semen collected by the artificial vagina and by electro-ejaculation. Aust. J. Exp. Agric. 2: 78-81.
58. Meredith, R.W., Westerman, M. & Springer, M.S. 2008. A phylogeny and timescale for the living genera of kangaroos and kin (Macropodiformes: Marsupialia) based on nuclear DNA sequences. Aust. J. Zool. 26: 395-410.
59. Meredith, R.W., Westerman, M. & Springer, M.S. 2009. A phylogeny of Diprotodontia (Marsupialia) based on sequences for five nuclear genes. Mol. Phylogenet. Evol. 51: 554-571.
60. Møller, A.P. 1989. Ejaculate quality, testes size and sperm production in mammals. Funct. Ecol. 3: 91-96.
61. Nakagawa, S. & Cuthill, I.C. 2007. Effect size, confidence interval and statistical significance: a practical guide for biologists. Biol. Rev. 82: 591-605.
62. Orme, D. 2013. The caper package: comparative analysis of phylogenetics and evolution in R. https://cran.r-project.org/web/packages/caper/vignettes/caper.pdf
63. Pages, M., Chaval, Y., Herbreteau, V., Waengsothorn, S., Cosson, J.F., Hugot, J.P. et al. 2010. Revisiting the taxonomy of the Rattini tribe: a phylogeny-based delimitation of species boundaries. BMC Evol. Biol. 10: 184.
64. Parker, G.A. 1970. Sperm competition and its evolutionary consequences in insects. Biol. Rev. 45: 525-567.
65. Parker, G.A. 1982. Why are there so many tiny sperm? Sperm competition and the maintenance of two sexes. J. Theor. Biol. 96: 281-294.
66. Parker, G.A. 1990. Sperm competition games: raffles and roles. Proc. R. Soc. Lond. B Biol. Sci. 242: 120-126.
67. Parker, G.A. 1993. Sperm competition games: sperm size and sperm number under adult control. Proc. R. Soc. Lond. B Biol. Sci. 253: 245-254.
68. Parker, G.A. & Pizzari, T. 2010. Sperm competition and ejaculate economics. Biol. Rev. Camb. Philos. Soc. 85: 897-934.
69. Parker, G.A. & Simmons, L.W. 1991. A model of constant random sperm displacement during mating: evidence from Scatophaga. Proc. R. Soc. Lond. B Biol. Sci. 246: 107-115.
70. Parker, G.A., Immler, S., Pitnick, S. & Birkhead, T.R. 2010. Sperm competition games: sperm size (mass) and number under raffle and displacement, and the evolution of P2. J. Theor. Biol. 264: 1003-1023.
71. Perry, M.M. 1987. Nuclear events from fertilization to the early cleavage stages in de domestic fowl (Gallus domesticus). J. Anat. 150: 99-109.
72. Peters, A.R. & Ball, P.J.H. 1987. Reproduction in Cattle. Butterworths, London, UK.
73. Pierce, J.D., Ferguson, B., Salo, A., Sawrey, D.K., Shapiro, L.E., Taylor, S.A. et al. 1990. Patterns of sperm allocation across successive ejaculates in four species of voles (Microtus). J. Reprod. Fertil. 88: 141-149.
74. Pitnick, S. & Markow, T.A. 1994. Sperm size, testes size, and the allocation of ejaculate among successive mates by the sperm limited fly Drosophila pachea and its relatives. Am Nat 143: 785-819.
75. Pitnick, S., Miller, G.T., Reagan, J. & Holland, B. 2001. Males' evolutionary responses to experimental removal of sexual selection. Proc. R. Soc. Lond. B Biol. Sci. 268: 1071-1080.
76. Preston, B.T., Stevenson, I.R., Pemberton, J.M. & Wilson, K. 2001. Dominant rams lose out by sperm depletion. Nature 409: 681-682.
77. Prothero, D.R. & Foss, S.E. 2007. The Evolution of Artiodactyls. JHU Press, Baltimore, MD, USA.
78. R Development Core Team. 2011. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/
79. Ramm, S.A. & Stockley, P. 2009. Adaptive plasticity of mammalian sperm production in response to social experience. Proc. R. Soc. Lond. B Biol. Sci. 276: 745-751.
80. Ramm, S.A. & Stockley, P. 2010. Sperm competition and sperm length influence the rate of mammalian spermatogenesis. Biol. Lett. 6: 219-221.
81. Robinson, T.J. & Matthee, C.A. 2005. Phylogeny and evolutionary origins of the Leporidae: a review of cytogenetics, molecular analyses and a supermatrix analysis. Mammal Rev. 35: 231-247.
82. Schneiders, A., Sonsken, J. & Hodges, J.K. 2004. Penile vibratory stimulation in the marmoset monkey: a practical alternative to electro-ejaculation, yielding ejaculates of enhanced quality. J. Med. Primatol. 33: 98-104.
83. Sheldon, B.C. 2000. Differential allocation: tests, mechanisms and implications. Trends Ecol. Evol. 15: 397-402.
84. Simmons, L.W. 2001. Sperm Competition and its Evolutionary Consequences in Insects. Princeton University Press, Princeton, NJ, USA.
85. Smithson, M. 2002. Confidence Intervals. SAGE Publications, London, UK.
86. Snook, R.R., Hosken, D.J. & Karr, T.L. 2011. The biology and evolution of polyspermy: insights from cellular and functional studies of sperm and centrosomal behavior in the fertilized egg. Reproduction 142: 779-792.
87. Soulsbury, C.D. 2010. Genetic patterns of paternity and testes size in mammals. PLoS ONE 5: e9581.
88. Suarez, S.S. 2008. Regulation of sperm storage and movement in the mammalian oviduct. Int. J. Dev. Biol. 52: 455-462.
89. Suarez, S.S. & Pacey, A.A. 2006. Sperm transport in the female reproductive tract. Hum. Reprod. Update 12: 23-37.
90. Taggart, D.A., Breed, W.G., Temple-Smith, P.D., Purvis, A. & Shimmin, G. 1998. Reproduction, mating strategies and sperm competition in marsupials and monotremes. In: Sperm Competition and Sexual Selection (T.R. Birkhead & A.P. Møller, eds), pp. 623-666. Academic Press, London, UK.
91. Taggart, D.A., Shimmin, G., Dickman, C.R. & Breed, W.G. 2003. Reproductive biology of carnivorous marsupials: clues to the likelihood of sperm competition. In: Predators With Pouches: The Biology of Carnivorous Marsupials (M. Jones, C.R. Dickman & M. Archer, eds), pp. 358-375. CSIRO, Collingwood, Vic., Australia.
92. Takei, G.L., Miyashiro, D., Mukai, C. & Okuno, M. 2014. Glycolysis plays an important role in energy transfer from the base to the distal end of the flagellum in mouse sperm. J. Exp. Biol. 217: 1876-1886.
93. Tomkins, J.L. & Simmons, L.W. 2002. Measuring relative investment: a case study of testes investment in species with alternative male reproductive tactics. Anim. Behav. 63: 1009-1016.
94. Tourmente, M., Gomendio, M., Roldan, E.R.S., Giojalas, L.C. & Chiaraviglio, M. 2009. Sperm competition and reproductive mode influence sperm dimensions and structure among snakes. Evolution 63: 2513-2524.
95. Tourmente, M., Gomendio, M. & Roldan, E.R.S. 2011a. Mass-specific metabolic rate and sperm competition determine sperm size in marsupial mammals. PLoS ONE 6: e21244.
96. Tourmente, M., Gomendio, M. & Roldan, E.R.S. 2011b. Sperm competition and the evolution of sperm design in mammals. BMC Evol. Biol. 11: 12.
97. Tourmente, M., Rowe, M., González-Barroso, M.M., Rial, E., Gomendio, M. & Roldan, E.R.S. 2013. Postcopulatory sexual selection increases ATP content in rodent spermatozoa. Evolution 67: 1838-1846.
98. Wedell, N., Gage, M.J.G. & Parker, G.A. 2002. Sperm competition, male prudence and sperm-limited females. Trends Ecol. Evol. 17: 313-320.