No association between sperm competition and sperm length variation across dung flies (Scathophagidae)

Journal of Evolutionary Biology

Volumn 26, Issue 11, 2013, Pages 2341-2349

  Sharma, M D ^a   Minder, A M ^b   Hosken, D J ^a  

^a UNIVERSITY OF EXETER   (United Kingdom)

^b ETH ZURICH   (Switzerland)

Author keywords

Comparative study; Diptera; Scathophaga; Scatophaga; Sperm; Sperm competition

Indexed keywords

BIRD; COMPARATIVE STUDY; FLY; INTRASPECIFIC VARIATION; MORPHOLOGY; REPRODUCTIVE BIOLOGY; SIZE DISTRIBUTION; SOCIAL INSECT; SPERM; SPERM COMPETITION;

AVES; DIPTERA; HEXAPODA; SCATHOPHAGA; SCATHOPHAGIDAE;

ANIMAL; ARTICLE; CELL SIZE; COMPARATIVE STUDY; CYTOLOGY; DIPTERA; FEMALE; MALE; PHYSIOLOGY; REGRESSION ANALYSIS; SCATHOPHAGA; SCATOPHAGA; SEXUAL BEHAVIOR; SPERM; SPERM COMPETITION; SPERMATOZOON;

COMPARATIVE STUDY; DIPTERA; SCATHOPHAGA; SCATOPHAGA; SPERM; SPERM COMPETITION;

ANIMALS; CELL SIZE; DIPTERA; FEMALE; MALE; REGRESSION ANALYSIS; SEXUAL BEHAVIOR, ANIMAL; SPERMATOZOA;

EID: 84885864580     PISSN: 1010061X     EISSN: 14209101     Source Type: Journal    
DOI: 10.1111/jeb.12232     Document Type: Article

References (72)

1. Bernasconi, M.V., Pawlowski, J., Valsangiacomo, C., Piffaretti, J.C. & Ward, P.I. 2000. Phylogeny of the Scathophagidae (Diptera, Calyptratae) based on mitochondrial DNA sequences. Mol. Phylogenet. Evol. 16: 308-315.
2. Birkhead, T.R., Hosken, D.J. & Pitnick, S. 2009 Sperm Biology: An Evolutionary Perspective. Academic Press, Oxford.
3. Blomberg, S.P., Lefevre, J.G., Wells, J.A. & Waterhouse, M. 2012. Independent contrasts and PGLS regression estimators are equivalent. Syst. Biol. 61: 382-391.
4. Briskie, J.V., Montgomerie, R. & Birkhead, T.R. 1997. The evolution of sperm size in birds. Evolution 51: 937-945.
5. Byrne, P.G., Roberts, J.D. & Simmons, L.W. 2002. Sperm competition selects for increased testes mass in Australian frogs. J. Evol. Biol. 15: 347-355.
6. Byrne, P.G., Simmons, L.W. & Roberts, J.D. 2003. Sperm competition and the evolution of gamete morphology in frogs. Proc. R. Soc. Lond. B 270: 2079-2086.
7. Calhim, S., Immler, S. & Birkhead, T.R. 2007. Postcopulatory sexual selection is associated with reduced variation in sperm morphology. PLoS ONE 2: e413.
8. Demont, M., Buser, C., Martin, O.Y. & Bussiere, L.F. 2011. Natural levels of polyandry: differential sperm storage and temporal changes in sperm competition intensity in yellow dung flies. Funct. Ecol. 25: 1079-1090.
9. Dobler, R. & Hosken, D.J. 2010. Response to selection and realized heritability of sperm length in the yellow dungfly (Scathophaga stercoraria). Heredity 104: 61-66.
10. Dybas, L.K. & Dybas, H.S. 1981. Coadaptation and taxonomic differentiation of sperm and spermathecae in featherwing beetles. Evolution 35: 168-174.
11. Erickson, R.P. 1990. Post-meiotic gene expression. Trends Genet. 6: 264-268.
12. Felsenstein, J. 1985. Phylogenies and the comparative method. Am. Nat. 125: 1-15.
13. Fitzpatrick, J.L. & Baer, B. 2011. Polyandry reduces sperm length variation in social insects. Evolution 65: 3006-3012.
14. 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.
15. Gage, M.J.G. 1994. Associations between body size, mating pattern, testis size and sperm lengths across butterflies. Proc. R. Soc. Lond. B 258: 247-254.
16. Gage, M.J.G. & Freckleton, R.P. 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: 625-632.
17. Gage, M.J.G. & Morrow, E.H. 2003. Experimental evidence for the evolution of numerous, tiny sperm via sperm competition. Curr. Biol. 13: 754-757.
18. García-Gonzáles, F. & Simmons, L.W. 2007. Shorter sperm confer higher competitive fertilization success. Evolution 61: 816-824.
19. Garland, T. & Ives, A.R. 2000. Using the past to predict the present: confidence intervals for regression equations in phylogenetic comparative methods. Am. Nat. 155: 346-364.
20. Garland, T., Midford, P.E. & Ives, A.R. 1999. An introduction to phylogenetically based statistical methods, with a new method for confidence intervals on ancestral values. Am. Zool. 39: 374-388.
21. Gavrilets, S. 2010. High dimensional fitness landscapes and speciation. In: Evolution: The Extended Synthesis (M. Pigliucci & G.B. Müller eds), pp. 45-79. MIT Press, London.
22. Gay, L., Hosken, D.J., Vasudev, R., Tregenza, T. & Eady, P.E. 2009. Sperm competition and maternal effects differentially influence testis and sperm size in Callosobruchus maculatus. J. Evol. Biol. 22: 1143-1150.
23. Grafen, A. 1989. The phylogenetic regression. Phil. Trans. R. Soc. B 326: 119-157.
24. Harcourt, A.H., Harvey, P.H., Larson, S.G. & Short, R.V. 1981. Testis weight, body-weight and breeding system in primates. Nature 293: 55-57.
25. Harvey, P.H. & Pagel, M.D. 1991. The Comparative Method in Evolutionary Biology. Oxford University Press, Oxford.
26. Helfenstein, F., Szep, T., Nagy, Z., Kempenaers, B. & Wagner, R.H. 2008. Between-male variation in sperm size, velocity and longevity in sand martins Riparia riparia. J. Avian Biol. 39: 647-652.
27. Higginson, D.M., Miller, K.B., Segraves, K.A. & Pitnick, S. 2012. Female reproductive tract form drives the evolution of complex sperm morphology. Proc. Natl. Acad. Sci. USA 109: 4538-4543.
28. Hosken, D.J. 1997. Sperm competition in bats. Proc. R. Soc. Lond. B 264: 385-392.
29. Hosken, D.J. 1998. Testes mass in megachiropteran bats varies in accordance with sperm competition theory. Behav. Ecol. Sociobiol. 44: 169-177.
30. Hosken, D.J. & Ward, P.I. 2001. Experimental evidence for testis size evolution via sperm competition. Ecol. Lett. 4: 10-13.
31. Hosken, D.J., Garner, T.W.J. & Ward, P.I. 2001. Sexual conflict selects for male and female reproductive characters. Curr. Biol. 11: 489-493.
32. Hosken, D.J., Garner, T.W.J. & Blanckenhorn, W.U. 2003. Asymmetry, testis and sperm size in yellow dung flies. Funct. Ecol. 17: 231-236.
33. Hunter, F.M. & Birkhead, T.R. 2002. Sperm viability and sperm competition in insects. Curr. Biol. 12: 121-123.
34. Immler, S., Calhim, S. & Birkhead, T.R. 2008. Increased postcopulatory sexual selection reduces the intramale variation in sperm design. Evolution 62: 1538-1543.
35. Jennions, M.D. & Passmore, N.I. 1993. Sperm competition in frogs: testis size and a 'sterile male' experiment on Chiromantis xerampelina (Rhacophoridae). Biol. J. Linn. Soc. 50: 211-220.
36. Kleven, O., Laskemoen, T., Fossoy, F., Robertson, R.J. & Lifjeld, J.T. 2008. Intraspecific variation in sperm length is negatively related to sperm competition in passerine birds. Evolution 62: 494-499.
37. LaMunyon, C.W. & Ward, S. 1998. Larger sperm outcompete smaller sperm in the nematode Caenorhabditis elegans. Proc. R. Soc. Lond. B 265: 1997-2002.
38. LaMunyon, C.W. & Ward, S. 1999. Evolution of sperm size in nematodes: sperm competition favours larger sperm. Proc. R. Soc. Lond. B 266: 263-267.
39. Lifjeld, J.T., Laskemoen, T., Kleven, O., Albrecht, T. & Robertson, R.J. 2010. Sperm length variation as a predictor of extrapair paternity in passerine birds. PLoS ONE 5: e13456.
40. Martin, O.Y., Hosken, D.J. & Ward, P.I. 2004. Post-copulatory sexual selection and female fitness in Scathophaga stercoraria. Proc. R. Soc. Lond. B 271: 353-359.
41. Martins, E.P. 1999. Estimation of ancestral states of continuous characters: a computer simulation study. Syst. Biol. 48: 642-650.
42. Martins, E.P. & Hansen, T.F. 1997. Phylogenies and the comparative method: a general approach to incorporating phylogenetic information into the analysis of interspecific data. Am. Nat. 149: 646-667.
43. Miller, G.T. & Pitnick, S. 2002. Sperm-female coevolution in Drosophila. Science 298: 1230-1233.
44. Minder, A.M., Hosken, D.J. & Ward, P.I. 2005. Co-evolution of male and female reproductive characters across the Scathophagidae (Diptera). J. Evol. Biol. 18: 60-69.
45. Moore, H.D.M., Martin, M. & Birkhead, T.R. 1999. No evidence for killer sperm or other selective interactions between human spermatozoa in ejaculates of different males in vitro. Proc. R. Soc. Lond. B 266: 2343-2350.
46. Morrow, E.H. & Gage, M.J.G. 2000. The evolution of sperm length in moths. Proc. R. Soc. Lond. B 267: 307-313.
47. Oppliger, A., Naciri-Graven, Y., Ribi, G. & Hosken, D.J. 2003. Sperm length influences fertilization success during sperm competition in the snail Viviparus ater. Mol. Ecol. 12: 485-492.
48. Orme, D., Freckleton, R., Thomas, G., Petzoldt, T., Fritz, S., Isaac, N. et al. 2012. Caper: Comparative Analyses of Phylogenetics and Evolution in R. URL http://cran.r-project.org/package=caper
49. Pagel, M. 1997. Inferring evolutionary processes from phylogenies. Zool. Scr. 26: 331-348.
50. Pagel, M. 1999. The maximum likelihood approach to reconstructing ancestral character states of discrete characters on phylogenies. Syst. Biol. 48: 612-622.
51. Parker, G.A. 1970a. Sperm competition and its evolutionary effect on copula duration in the fly Scatophaga stercoraria. J. Insect Physiol. 16: 1301-1328.
52. Parker, G.A. 1970b. Sperm competition and its evolutionary consequences in the insects. Biol. Rev. 45: 525-567.
53. Parker, G. 1998. Sperm competition and the evolution of ejaculates: towards a theory base. In: Sperm Competition and Sexual Selection (T.R. Birkhead, A.P. Møller, eds), pp. 3-54. Academic Press, London.
54. Parker, G.A. & Begon, M.E. 1993. Sperm competition games - sperm size and number under gametic control. Proc. R. Soc. Lond. B 253: 255-262.
55. Parker, G.A., Ball, M.A., Stockley, P. & Gage, M.J.G. 1997. Sperm competition games: a prospective analysis of risk assessment. Proc. R. Soc. Lond. B 264: 1793-1802.
56. Pitnick, S., Miller, G.T., Reagan, J. & Holland, B. 2001. Males' evolutionary responses to experimental removal of sexual selection. Proc. R. Soc. Lond. B 268: 1071-1080.
57. Pitnick, S., Miller, G.T., Schneider, K. & Markow, T.A. 2003. Ejaculate-female coevolution in Drosophila mojavensis. Proc. R. Soc. Lond. B 270: 1507-1512.
58. Pitnick, S., Dobler, R. & Hosken, D.J. 2009a. Sperm length is not influenced by haploid gene expression in the flies Drosophila melanogaster and Scathophaga stercoraria. Proc. R. Soc. Lond. B 276: 4029-4034.
59. Pitnick, S., Hosken, D.J. & Birkhead, T.R. 2009b Sperm morphological diversity. In: Sperm Biology: An Evolutionary Perspective (T.R. Birkhead, D.J. Hosken, S. Pitnick, eds), pp. 69-149. Academic Press, London.
60. Presgraves, D.C., Baker, R.H. & Wilkinson, G.S. 1999. Coevolution of sperm and female reproductive tract morphology in stalk-eyed flies. Proc. R. Soc. Lond. B 266: 1041-1047.
61. R Development Core Team 2011. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing. Vienna, Austria. URL http://www.R-project.org
62. Radwan, J. 1996. Intraspecific variation in sperm competition success in the bulb mite: a role for sperm size. Proc. R. Soc. Lond. B 263: 855-859.
63. Rohlf, F.J. 2001. Comparative methods for the analysis of continuous variables: geometric interpretations. Evolution 55: 2143-2160.
64. Simmons, L.W. 2001. Sperm Competition and its Evolutionary Consequences in the Insects. Princeton University Press, Princeton.
65. Simmons, L.W. & Garcia-Gonzalez, F. 2008. Evolutionary reduction in testes size and competitive fertilization success in response to the experimental removal of sexual selection in dung beetles. Evolution 62: 2580-2591.
66. Simmons, L.W., Stockley, P., Jackson, R.L. & Parker, G.A. 1996. Sperm competition or sperm selection: no evidence for female influence over paternity in yellow dung flies Scatophaga stercoraria. Behav. Ecol. Sociobiol. 38: 199-206.
67. Simmons, L.W., Tomkins, J.L. & Hunt, J. 1999. Sperm competition games played by dimorphic male beetles. Proc. R. Soc. Lond. B 266: 145-150.
68. 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.
69. Van Valen, L. 2005. The statistics of variation. In: Variation (H. Benedikt, K.H. Brian, eds), pp. 29-47. Academic Press, Burlington.
70. Vibranovski, M.D.M., Chalopin, D.S., Lopes, H.F., Long, M. & Karr, T.L. 2010. Direct evidence for postmeiotic transcription during Drosophila melanogaster spermatogenesis. Genetics 186: 431-433.
71. Ward, P.I. & Hauschteck-Jungen, E. 1993. Variation in sperm length in the yellow dung fly Scathophaga stercoraria (L). J. Insect Physiol. 39: 545-547.
72. Ward, P.I. & Simmons, L.W. 1991. Copula duration and testes size in the yellow dung fly, Scathophaga stercoraria (L.) - the effects of diet, body size, and mating history. Behav. Ecol. Sociobiol. 29: 77-85.