Evolutionary Ecology

, Volume 21, Issue 3, pp 295–306 | Cite as

Phenotypic plasticity in sperm production rate: there’s more to it than testis size

Original Paper

Abstract

Evolutionary theory predicts that males should produce more sperm when sperm competition is high. Because sperm production rate is difficult to measure in most organisms, comparative and experimental studies have typically used testis size instead, while assuming a good correspondence between testis size and sperm production rate. Here we evaluate this common assumption using the marine flatworm Macrostomum lignano, in which we can estimate sperm production rate because the accumulation of produced sperm can be observed in vivo. In earlier studies we have shown that testis size is phenotypically plastic in M. lignano: worms can be induced to make larger testes by raising them in groups instead of pairs, and these larger testes have a higher cell proliferation activity (i.e. they are more energetically costly). Here we demonstrate that worms with such experimentally enlarged testes have a higher sperm production rate. Moreover, although testis size and sperm production rate were related linearly, worms with experimentally enlarged testes had a higher sperm production rate per unit testis size (i.e. a higher spermatogenic efficiency). We thus show that phenotypically plastic adjustment of sperm production rate includes a component that is independent of testis size. We discuss possible reasons for this novel finding, and suggest that the relationship between testis size and sperm production needs to be evaluated in other species as well.

Keywords

Cell cycle Male allocation Phenotypic plasticity Platyhelminthes Sperm competition Testis size 

References

  1. Amann RP (1970) Sperm production rates. In: Johnson AD, Gomes WR, Vandermark NL (eds) The testis. Academic Press, New York, pp 433–482Google Scholar
  2. Andersen RA, Berges JA, Harrison PJ, Watanabe MM (2005) Recipes for freshwater and seawater media. In: Andersen RA (ed) Algal culturing techniques. Elsevier, Amsterdam, pp 429–538Google Scholar
  3. Aspbury AS, Gabor CR (2004a) Differential sperm priming by male sailfin mollies (Poecilia latipinna): effects of female and male size. Ethology 110:193–202CrossRefGoogle Scholar
  4. Aspbury AS, Gabor CR (2004b) Discriminating males alter sperm production between species. Proc Natl Acad Sci USA 101:15970–15973CrossRefGoogle Scholar
  5. Bozynski CC, Liley NR (2003) The effect of female presence on spermiation, and of male sexual activity on ‘ready’ sperm in the male guppy. Anim Behav 65:53–58CrossRefGoogle Scholar
  6. Brauer VS, Schärer L, Michiels NK (in press) Phenotypically flexible sex allocation in a simultaneous hermaphrodite. Evolution Google Scholar
  7. Byrne PG, Roberts JD, Simmons LW (2002) Sperm competition selects for increased testes mass in Australian frogs. J Evol Biol 15:347–355CrossRefGoogle Scholar
  8. Cooke PS, Porcelli J, Hess RA (1992) Induction of increased testis growth and sperm production in adult rats by neonatal administration of the goitrogen propylthiouracil (PTU): the critical period. Biol Reprod 46:146–154PubMedCrossRefGoogle Scholar
  9. Cooke PS, Zhao YD, Hansen LG (1996) Neonatal polychlorinated biphenyl treatment increases adult testis size and sperm production in the rat. Toxicol Appl Pharmacol 136:112–117PubMedCrossRefGoogle Scholar
  10. de Reviers M, Williams JB (eds) (1984) Testis development and production of spermatozoa in the cockerel (Gallus domesticus). British Poultry Science, HarlowGoogle Scholar
  11. Evans JP, Magurran AE (1999) Geographic variation in sperm production by Trinidadian guppies. Proc R Soc Lond B 266:2083–2087CrossRefGoogle Scholar
  12. Gage MJG (1994) Associations between body size, mating pattern, testis size and sperm lengths across butterflies. Proc R Soc Lond B 258:247–254CrossRefGoogle Scholar
  13. Gage MJG, Freckleton RP (2003) Relative testis size and sperm morphometry across mammals: no evidence for an association between sperm competition and sperm length. Proc R Soc Lond B 270:625–632CrossRefGoogle Scholar
  14. Gage MJG, Stockley P, Parker GA (1995) Effects of alternative male strategies on characteristics of sperm production in the Atlantic salmon (Salmo salar): theoretical and empirical investigations. Phil Trans R Soc Lond B 350:391–399CrossRefGoogle Scholar
  15. Gupta G, Maikhuri JP, Dwivedi AK, Dhar JD, Setty BS (1999) Changes in daily sperm production rate in rats under the influence of a potent antispermatogenic agent, CDRI 84/35. Contraception 59:401–404PubMedCrossRefGoogle Scholar
  16. Hellriegel B, Blanckenhorn WU (2002) Environmental influences on the gametic investment of yellow dung fly males. Evol Ecol 16:505–522CrossRefGoogle Scholar
  17. Hosken DJ (1997) Sperm competition in bats. Proc R Soc Lond B 264:385–392CrossRefGoogle Scholar
  18. Johnson RK, Eckardt GR, Rathje TA, Drudik DK (1994) 10 generations of selection for predicted weight of testes in swine – direct response and correlated response in body-weight, backfat, age at puberty, and ovulation rate. J Anim Sci 72:1978–1988PubMedGoogle Scholar
  19. Ladurner P, Rieger RM, Baguña J (2000) Spatial distribution and differentiation potential of stem cells in hatchlings and adults in the marine platyhelminth Macrostomum sp.: a bromodeoxyuridine analysis. Dev Biol 226:231–241PubMedCrossRefGoogle Scholar
  20. Ladurner P, Schärer L, Salvenmoser W, Rieger RM (2005) A new model organism among the lower Bilateria and the use of digital microscopy in taxonomy of meiobenthic Platyhelminthes: Macrostomum lignano, n. sp (Rhabditophora, Macrostomorpha) J Zool Syst Evol Res 43:114–126CrossRefGoogle Scholar
  21. LaMunyon CW, Ward S (1998) Larger sperm outcompete smaller sperm in the nematode Caenorhabditis elegans. Proc R Soc Lond B 265:1997–2002CrossRefGoogle Scholar
  22. LaMunyon CW, Ward S (1999) Evolution of sperm size in nematodes: sperm competition favours larger sperm. Proc R Soc Lond B 266:263–267CrossRefGoogle Scholar
  23. LaMunyon CW, Ward S (2002) Evolution of larger sperm in response to experimentally increased sperm competition in Caenorhabditis elegans. Proc R Soc Lond B 269:1125–1128CrossRefGoogle Scholar
  24. Malo AF, Roldan ER S, Garde J, Soler AJ, Gomendio M (2005) Antlers honestly advertise sperm production and quality. Proc R Soc Lond B 272:149–157CrossRefGoogle Scholar
  25. Minder AM, Hosken DJ, Ward PI (2005) Co-evolution of male and female reproductive characters across the Scathophagidae (Diptera). J Evol Biol 18:60–69PubMedCrossRefGoogle Scholar
  26. Møller AP (1989) Ejaculate quality, testes size and sperm production in mammals. Funct Ecol 3:91–96CrossRefGoogle Scholar
  27. Moreira JR, Macdonald DW, Clarke JR (1997) Correlations of testis mass in capybaras (Hydrochaeris hydrochaeris): dominance assurance of sperm competition. J Zool 241:457–463CrossRefGoogle Scholar
  28. Morrow EH, Gage MJG (2000) The evolution of sperm length in moths. Proc R Soc Lond B 267:307–313CrossRefGoogle Scholar
  29. Nakatsuru K, Kramer DL (1982) Is sperm cheap? Limited male fertility and female choice in the lemon tetra (Pisces, Characidae). Science 216:753–755CrossRefPubMedGoogle Scholar
  30. Newlon AW, Yund PO, Stewart-Savage J (2003) Phenotypic plasticity of reproductive effort in a colonial ascidian, Botryllus schlosseri. J Exp Zool A 297A:180–188CrossRefGoogle Scholar
  31. Parker GA (1998) Sperm competition and the evolution of ejaculates: towards a theory base. In: Birkhead TR, Møller AP (eds) Sperm competition and sexual selection. Academic Press, London, England, pp 3–54Google Scholar
  32. 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 121:239–247PubMedCrossRefGoogle Scholar
  33. Pilastro A, Scaggiante M, Rasotto MB (2002) Individual adjustment of sperm expenditure accords with sperm competition theory. Proc Natl Acad Sci USA 99:9913–9915PubMedCrossRefGoogle Scholar
  34. Pitnick S, Markow TA (1994a) Large-male advantages associated with costs of sperm production in Drosophila hydei, a species with giant sperm. Proc Natl Acad Sci USA 91:9277–9281CrossRefGoogle Scholar
  35. Pitnick S, Markow TA (1994b) Male gametic strategies: sperm size, testes size, and the allocation of ejaculate among successive mates by the sperm-limited fly Drosophila pachea and its relatives. Am Nat 143:785–819CrossRefGoogle Scholar
  36. Pitnick S, Miller GT, Reagan J, Holland B (2001) Males’ evolutionary responses to experimental removal of sexual selection. Proc R Soc Lond B 268:1071–1080CrossRefGoogle Scholar
  37. Radwan J (1996) Intraspecific variation in sperm competition success in the bulb mite: a role for sperm size. Proc R Soc Lond B 263:855–859CrossRefGoogle Scholar
  38. Rathje TA, Johnson RK, Lunstra DD (1995) Sperm production in boars after 9 generations of selection for increased weight of testis. J Anim Sci 73:2177–2185PubMedGoogle Scholar
  39. Rieger RM, Gehlen M, Haszprunar G, Holmlund M, Legniti A, Salvenmoser W, Tyler S (1988) Laboratory cultures of marine Macrostomida (Turbellaria). Fortschr Zool 36:523Google Scholar
  40. Sall J, Lehman A (1996) JMP start statistics: A guide to statistical and data analysis using JMP, JMPIN software. Duxbury Press, Belmont, USAGoogle Scholar
  41. Schärer L, Joss G, Sandner P (2004a) Mating behaviour of the marine turbellarian Macrostomum sp.: these worms suck. Mar Biol 145:373–380CrossRefGoogle Scholar
  42. Schärer L, Ladurner P (2003) Phenotypically plastic adjustment of sex allocation in a simultaneous hermaphrodite. Proc R Soc Lond B 270:935–941CrossRefGoogle Scholar
  43. Schärer L, Ladurner P, Rieger RM (2004b) Bigger testes do work more: experimental evidence that testis size reflects testicular cell proliferation activity in the marine invertebrate, the free-living flatworm Macrostomum sp. Behav Ecol Sociobiol 56:420–425CrossRefGoogle Scholar
  44. Schärer L, Sandner P, Michiels NK (2005) Trade-off between male and female allocation in the simultaneously hermaphroditic flatworm Macrostomum sp. J Evol Biol 18:396–404PubMedCrossRefGoogle Scholar
  45. Schärer L, Zaubzer J, Salvenmoser W, Seifarth C, Ladurner P (in press) Tracking sperm of a donor in a recipient: an immunocytochemical approach. Animal Biol Google Scholar
  46. Tuttle EM, Pruett-Jones S (2004) Estimates of extreme sperm production: morphological and experimental evidence from reproductively promiscuous fairy-wrens (Malurus). Anim Behav 68:541–550CrossRefGoogle Scholar
  47. Tuttle EM, Pruett-Jones S, Webster MS (1996) Cloacal protuberances and extreme sperm production in Australian fairy-wrens. Proc R Soc Lond B 263:1359–1364CrossRefGoogle Scholar
  48. Tyler S (1981) Development of cilia in embryos of the turbellarian Macrostomum. Hydrobiologia 84:231–239CrossRefGoogle Scholar
  49. Wedell N, Gage MJG, Parker GA (2002) Sperm competition, male prudence and sperm-limited females. Trends Ecol Evol 17:313–320CrossRefGoogle Scholar
  50. Wistuba J, Schrod A, Greve B, Hodges JK, Aslam H, Weinbauer GF, Luetjens CM (2003) Organization of seminiferous epithelium in primates: relationship to spermatogenic efficiency, phylogeny, and mating system. Biol Reprod 69:582–591PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2006

Authors and Affiliations

  1. 1.Division of Ultrastructural Research and Evolutionary BiologyInstitute of Zoology, University of InnsbruckInnsbruckAustria

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