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Mass-Specific Metabolic Rate and Sperm Competition Determine Sperm Size in Marsupial Mammals

By Maximiliano Tourmente, Montserrat Gomendio and Eduardo R. S. Roldan

Abstract

Two complementary hypotheses have been proposed to explain variation in sperm size. The first proposes that post-copulatory sexual selection favors an increase in sperm size because it enhances sperm swimming speed, which is an important determinant of fertilization success in competitive contexts. The second hypothesis proposes that mass-specific metabolic rate acts as a constraint, because large animals with low mass-specific metabolic rates will not be able to process resources at the rates needed to produce large sperm. This constraint is expected to be particularly pronounced among mammals, given that this group contains some of the largest species on Earth. We tested these hypotheses among marsupials, a group in which mass-specific metabolic rates are roughly 30% lower than those of eutherian mammals of similar size, leading to the expectation that metabolic rate should be a major constraint. Our findings support both hypotheses because levels of sperm competition are associated with increases in sperm size, but low mass-specific metabolic rate constrains sperm size among large species. We also found that the relationship between sperm size and mass-specific metabolic rate is steeper among marsupials and shallower among eutherian mammals. This finding has two implications: marsupials respond to changes in mass-specific metabolic rate by modifying sperm length to a greater extent, suggesting that they are more constrained by metabolic rate. In addition, for any given mass-specific metabolic rate, marsupials produce longer sperm. We suggest that this is the consequence of marsupials diverting resources away from sperm numbers and into sperm size, due to their efficient sperm transport along the female tract and the existence of mechanisms to protect sperm

Topics: Research Article
Publisher: Public Library of Science
OAI identifier: oai:pubmedcentral.nih.gov:3120838
Provided by: PubMed Central

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Citations

  1. (2008). A dated phylogeny of marsupials using a molecular supermatrix and multiple fossil constraints.
  2. (2004). A farewell to Bonferroni: the problems of low statistical power and publication bias.
  3. (2008). A phylogeny and timescale for marsupial evolution based on sequences for five nuclear genes.
  4. (2008). A phylogeny and timescale for the living genera of kangaroos and kin (Macropodiformes: Marsupialia) based on nuclear DNA sequences.
  5. (2009). A phylogeny of Diprotodontia (Marsupialia) based on sequences for five nuclear genes.
  6. (2003). Confidence intervals.
  7. (1995). Delayed male maturity is a cost of producing large sperm in Drosophila.
  8. (2003). Effect sizes for experimenting psychologists.
  9. (2007). Effects of body size and lifestyle on evolution of mammal life histories.
  10. (1982). Ejaculate cost and male choice.
  11. (1988). Ejaculate quality, testes size and sperm competition in primates.
  12. (1989). Ejaculate quality, testes size and sperm production in mammals.
  13. (2008). Family-level relationships among the Australasian marsupial ‘‘herbivores’’ (Diprotodontia: koala, wombats, kangaroos and possums).
  14. (2009). Female promiscuity promotes the evolution of faster sperm in cichlid fishes.
  15. (2003). Fibrous sheath of mammalian spermatozoa.
  16. (2010). Genetic patterns of paternity and testes size in mammals.
  17. (2004). Glyceraldehyde 3-phosphate dehydrogenase-S, a sperm-specific glycolytic enzyme, is required for sperm motility and male fertility.
  18. (2010). Goswami A
  19. (2008). Implications of diversity in sperm size and function for sperm competition and fertility.
  20. (1982). Is sperm cheap? Limited male fertility and female choice in the lemon tetra (Pisces,
  21. (1997). Is sperm really so cheap? Costs of reproduction in male adders, Vipera berus.
  22. (2005). Life of marsupials.
  23. (2010). Linking sperm length and velocity: the importance of intramale variation.
  24. (2005). Male fertility in natural populations of red deer is determined by sperm velocity and the proportion of normal spermatozoa.
  25. (2002). Measuring relative investment: a case study of testes investment in species with alternative male reproductive tactics.
  26. (1991). Meta-analytic procedures for social research. Newbury Park:
  27. (2008). Molecular relationships of species of Pseudantechinus,
  28. (2006). Moving to the beat: a review of mammalian sperm motility regulation.
  29. (1985). On mammalian sperm dimensions.
  30. (2009). PanTheria: a species-level database of life history, ecology, and geography of extant and recently extinct mammals.
  31. (1994). Parametric measures of effect size. In: The handbook of research synthesis
  32. (2002). Phylogenetic analysis and comparative data: a test and review of evidence.
  33. (1985). Phylogenies and the comparative method.
  34. (2003). Relative testis size and sperm morphometry across mammals: no evidence for an association between sperm competition and sperm length.
  35. (1998). Reproduction, mating strategies and sperm competition in marsupials and monotremes.
  36. (2003). Reproductive biology of carnivorous marsupials: Clues to the likelihood of sperm competition.
  37. (2007). Scaling of number, size, and metabolic rate of cells with body size in mammals.
  38. (2009). Sperm competition and reproductive mode influence sperm dimensions and structure among snakes.
  39. (2009). Sperm competition and sperm phenotype.
  40. (1984). Sperm competition and the evolution of animal mating strategies. In: Sperm competition and the evolution of animal mating systems.
  41. (1998). Sperm competition and the evolution of ejaculates: towards a theory base. In: Spermcompetition and sexual selection
  42. (2011). Sperm competition and the evolution of sperm design in mammals.
  43. (2005). Sperm competition and the evolution of sperm midpiece volume in mammals.
  44. (2010). Sperm competition games: sperm size (mass) and number under raffle and displacement, and the evolution of P2.
  45. (1997). Sperm competition in bats.
  46. (1998). Sperm competition in mammals. In: Sperm competition and sexual selection
  47. (2010). Sperm competition in the Macropodoidea: a review of evidence.
  48. (1991). Sperm competition influences sperm size in mammals.
  49. (2011). Sperm competition selects for sperm quantity and quality in the Australian Maluridae.
  50. (2002). Sperm competition: motility and the midpiece in primates.
  51. (2006). Sperm design and sperm function.
  52. (1999). Sperm mobility determines the outcome of sperm competition in the domestic fowl.
  53. (1999). Sperm mobility: A primary determinant of fertility in the domestic fowl (Gallus domesticus).
  54. (2009). Sperm morphology and sperm velocity in passerine birds.
  55. (2000). Sperm velocity and longevity trade-off and influence fertilization in the sea urchin Lytechinus variegatus.
  56. (2004). Spermatozoal traits and sperm competition in Atlantic salmon: relative sperm velocity is the primary determinant of fertilization success.
  57. (1988). Statistical power analysis for the behavioral sciences.
  58. (2002). Targeted disruption of the AKAP4 gene causes defects in sperm flagellum and motility.
  59. (1997). Testes weight, body weight and mating system in marsupials and monotremes.
  60. (2002). Testis-specific cytochrome c-null mice produce functional sperm but undergo early testicular atrophy.
  61. (1991). The comparative method in evolutionary biology.
  62. (2007). The scaffold role of the fibrous sheath.
  63. (1986). Trombulak SC
  64. (1982). Why are there so many tiny sperm? Sperm competition and the maintenance of two sexes.
  65. (2011). Why mammalian lineages respond differently to sexual selection: metabolic rate constrains the evolution of sperm size. Proc R Soc B,
  66. (1984). Why so many mammalian spermatozoa - a clue from marsupials?