Mitochondrial haplotype does not affect sperm velocity in the zebra finch Taeniopygia guttata

Journal of Evolutionary Biology

Volumn 23, Issue 2, 2010, Pages 422-432

  Mossman, J A ^a   Slate, J ^a   Birkhead, T R ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

Author keywords

Computer assisted sperm analysis; Haplotype; Maternal inheritance; Mitochondrial DNA; MtDNA; Sperm velocity; Taeniopygia guttata; Zebra finch

Indexed keywords

MITOCHONDRIAL DNA;

EVOLUTIONARY BIOLOGY; FERTILITY; FITNESS; MATERNAL EFFECT; MITOCHONDRIAL DNA; MUTATION; PASSERINE; PHENOTYPE;

ANIMAL; ARTICLE; FEMALE; FINCH; GENETIC FITNESS; GENETICS; HAPLOTYPE; MALE; PHYSIOLOGY; SPERMATOZOON; SPERMATOZOON MOTILITY;

ANIMALS; DNA, MITOCHONDRIAL; FEMALE; FINCHES; GENETIC FITNESS; HAPLOTYPES; MALE; SPERM MOTILITY; SPERMATOZOA;

ANIMALIA; TAENIOPYGIA GUTTATA;

EID: 74349102141     PISSN: 1010061X     EISSN: 14209101     Source Type: Journal    
DOI: 10.1111/j.1420-9101.2009.01913.x     Document Type: Article

References (77)

1. Amo, T., Yadava, N., Oh, R., Nicholls, D.G. Brand, M.D. 2008. Experimental assessment of bioenergetic differences caused by the common European mitochondrial DNA haplogroups H and T. Gene 411 : 69 76.
2. Anderson, S., Bankier, A.T., Barrell, B.G., Debruijn, M.H.L., Coulson, A.R., Drouin, J., Eperon, I.C., Nierlich, D.P., Roe, B.A., Sanger, F., Schreier, P.H., Smith, A.J.H., Staden, R. Young, I.G. 1981. Sequence and organization of the human mitochondrial genome. Nature 290 : 457 465.
3. Aziz, N., Saleh, R.A., Sharma, R.K., Lewis-Jones, I., Esfandiari, N., Thomas, A.J. Jr. Agarwal, A. 2004. Novel association between sperm reactive oxygen species production, sperm morphological defects, and the sperm deformity index. Fertil. Steril. 81 : 349 354.
4. Bedford, J.M. 1990. Sperm dynamics in the epididymis. In : Gamete Physiology (A.H. Asch, J.P. Bamaceda I. Johnson, eds pp. 53 67. Norwell, MA.
5. Birkhead, T.R. 1998. Sperm competition in birds: mechanisms and function. In : Sperm Competition and Sexual Selection (T.R. Birkhead A.P. Møller, eds pp. 579 622. Academic Press, London, UK.
6. Birkhead, T.R. Fletcher, F. 1995. Male phenotype and ejaculate quality in the zebra finch Taeniopygia guttata. Proc. R. Soc. B 262 : 329 334. (Pubitemid 26023713)
7. Birkhead, T.R. Møller, A.P. 1998. Sperm Competition and Sexual Selection. Academic Press, London, UK.
8. Birkhead, T.R. Pizzari, T. 2002. Postcopulatory sexual selection. Nat. Rev. Genet. 3 : 262 273.
9. Birkhead, T.R., Fletcher, F., Pellatt, E.J. Staples, A. 1995. Ejaculate quality and the success of extra-pair copulations in the zebra finch. Nature 377 : 422 423. (Pubitemid 26449349)
10. Birkhead, T.R., Martinez, J.G., Burke, T. Froman, D.P. 1999. Sperm mobility determines the outcome of sperm competition in the domestic fowl. Proc. R. Soc. B 266 : 1759 1764.
11. Birkhead, T.R., Pellatt, E.J., Brekke, P., Yeates, R. Castillo-Juarez, H. 2005. Genetic effects on sperm design in the zebra finch. Nature 434 : 383 387.
12. Birkhead, T.R., Pellatt, E.J., Matthews, I.M., Roddis, N.J., Hunter, F.M., McPhie, F. Castillo-Juarez, H. 2006. Genic capture and the genetic basis of sexually selected traits in the zebra finch. Evolution 60 : 2389 2398.
13. Blount, J.D., Moller, A.P. Houston, D.C. 2001. Antioxidants, showy males and sperm quality. Ecol. Lett. 4 : 393 396.
14. Bruford, M.W., Hanotte, O., Brookfield, J.F.Y. Burke, T. 1998. Multilocus and single-locus DNA fingerprinting. In : Molecular Genetic Analysis of Populations: A Practical Approach, 2nd edn (A.R. Hoelzel, ed pp. 287 336. IRL Press, Oxford.
15. Cardullo, R.A. Baltz, J.M. 1991. Metabolic regulation in mammalian sperm-mitochondrial volume determines sperm length and flagellar beat frequency. Cell. Motil. Cytoskel. 19 : 180 188.
16. Cavallo, A. Martin, A.C.R. 2005. Mapping SNPs to protein sequence and structure data. Bioinformatics 21 : 1443 1450.
17. Crochet, P.-A. Desmarais, E. 2000. Slow rate of evolution in the mitochondrial control region of gulls (Aves: Laridae). Mol. Biol. Evol. 17 : 1797 1806.
18. Cummins, J. 1998. Mitochondrial DNA in mammalian reproduction. Rev. Reprod. 3 : 172 182.
19. DiMauro, S. Davidzon, G. 2005. Mitochondrial DNA and disease. Ann. Med. 37 : 222 232.
20. DiMauro, S. Schon, E.A. 2003. Mechanisms of disease: mitochondrial respiratory-chain diseases. N. Eng. J. Med. 348 : 2656 2668.
21. Dowling, D.K., Nowostawski, A.L. Arnqvist, G. 2007. Effects of cytoplasmic genes on sperm viability and sperm morphology in a seed beetle: implications for sperm competition theory? J. Evol. Biol. 20 : 358 368.
22. Dowling, D.K., Friberg, U. Lindell, J. 2008. Evolutionary implications of non-neutral mitochondrial genetic variation. Trends Ecol. Evol. 23 : 546 554.
23. Folgerø, T., Bertheussen, K., Lindal, S., Torbergsen, T. Oian, P. 1993. Mitochondrial disease and reduced sperm motility. Hum. Reprod. 8 : 1863 1868.
24. Ford, W.C.L. 2006. Glycolysis and sperm motility: does a spoonful of sugar help the flagellum go round? Hum. Reprod. Update 12 : 269 274.
25. Frank, S.A. Hurst, L.D. 1996. Mitochondria and male disease. Nature 383 : 224.
26. Friberg, U. Dowling, D.K. 2008. No evidence of mitochondrial genetic variation for sperm competition within a population of Drosophila melanogaster. J. Evol. Biol. 21 : 1798 1807.
27. Froman, D.P. Feltmann, A.J. 1998. Sperm mobility: a quantitative trait of the domestic fowl (Gallus domesticus). Biol. Reprod. 58 : 379 384.
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. Froman, D.P., Feltmann, A.J., Rhoads, M.L. Kirby, J.D. 1999. Sperm mobility: a primary determinant of fertility in the domestic fowl (Gallus domesticus). Biol. Reprod. 61 : 400 405.
30. Froman, D.P., Pizzari, T., Feltmann, A.J., Castillo-Juarez, H. Birkhead, T.R. 2002. Sperm mobility: mechanisms of fertilizing efficiency, genetic variation and phenotypic relationship with male status in the domestic fowl, Gallus gallus domesticus. Proc. R. Soc. B 269 : 607 612.
31. Gemmell, N.J., Metcalf, V.J. Allendorf, F.W. 2004. Mother's curse: the effect of mtDNA on individual fitness and population viability. Trends Ecol. Evol. 19 : 238 244.
32. Harvey, P.H. May, R.M. 1989. Copulation dynamics - out for the sperm count. Nature 337 : 508 509.
33. Hinten, G.N., Hale, M.C., Gratten, J., Mossman, J.A., Lowder, B.V., Mann, M.K. Slate, J. 2007. SNP-SCALE: SNP scoring by colour and length exclusion. Mol. Ecol. Resour. 7 : 377 388.
34. Holyoake, A.J., Sin, I.L., Benny, P.S. Sin, F.Y.T. 1999. Association of a novel human mtDNA ATPase6 mutation with immature sperm cells. Andrologia 31 : 339 345.
35. Holyoake, A.J., McHugh, P., Wu, M., O'Carroll, S., Benny, P., Lin, I.L. Sin, F.Y.T. 2001. High incidence of single nucleotide substitutions in the mitochondrial genome is associated with poor semen parameters in men. Int. J. Androl. 24 : 175 182.
36. Hurst, L.D. 1992. Intragenomic conflict as an evolutionary force. Proc. R. Soc. B 248 : 135 140.
37. Johns, D.R. 1995. Seminars in medicine of the Beth Israel Hospital, Boston: mitochondrial DNA and disease. N. Eng. J. Med. 333 : 638 644.
38. Kao, S.H., Chao, H.T. Wei, Y.H. 1995. Mitochondrial deoxyribonucleic acid 4977 bp deletion is associated with diminished fertility and motility of human sperm. Biol. Reprod. 52 : 729 736.
39. Kao, S.H., Chao, H.T. Wei, Y.H. 1998. Multiple deletions of mitochondrial DNA are associated with the decline of motility and fertility of human spermatozoa. Mol. Hum. Reprod. 4 : 657 666.
40. Keller, L. Reeve, H.K. 1995. Why do females mate with multiple males - the sexually selected sperm hypothesis. Adv. Study Behav. 24 : 291 315.
41. Kruuk, L.E.B. 2004. Estimating genetic parameters in natural populations using the 'animal model'. Philos. Trans. R. Soc. Lond. B Biol. Sci. 359 : 873 890.
42. Kvist, L., Martens, J., Nazarenko, A.A. Orell, M. 2003. Paternal leakage of mitochondrial DNA in the great tit (Parus major). Mol. Biol. Evol. 20 : 243 247. (Pubitemid 36237382)
43. Lloyd, D.R., Phillips, D.H. Carmichael, P.L. 1997. Generation of putative intrastrand cross-links and strand breaks in DNA by transition metal ion-mediated oxygen radical attack. Chem. Res. Toxicol. 10 : 393 400.
44. Miki, K., Qu, W.D., Goulding, E.H., Willis, W.D., Bunch, D.O., Strader, L.F., Perreault, S.D., Eddy, E.M. O'Brien, D.A. 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.
45. Mishmar, D., Ruiz-Pesini, E., Golik, P., Macaulay, V., Clark, A.G., Hosseini, S., Brandon, M., Easley, K., Chen, E., Brown, M.D., Sukernik, R.I., Olckers, A. Wallace, D.C. 2003. Natural selection shaped regional mtDNA variation in humans. Proc. Natl Acad. Sci. USA 100 : 171 176.
46. Montiel-Sosa, F., Ruiz-Pesini, E., Enriquez, J.A., Marcuello, A., Diez-Sanchez, C., Montoya, J., Wallace, D.C. Lopez-Perez, M.J. 2006. Differences of sperm motility in mitochondrial DNA haplogroup U sublineages. Gene 368 : 21 27.
47. Moore, F.L. Reijo-Pera, R.A. 2000. Male sperm motility dictated by mother's mtDNA. Am. J. Hum. Genet. 67 : 543 548.
48. Morrow, E.H. Gage, M.J. 2001. Artificial selection and heritability of sperm length in Gryllus bimaculatus. Heredity 87 : 356 362.
49. Mossman, J.A., Birkhead, T.R. Slate, J. 2006. The whole mitochondrial genome sequence of the zebra finch (Taeniopygia guttata). Mol. Ecol. Resour. 6 : 1222 1227.
50. Mossman, J.A., Slate, J., Humphries, S. Birkhead, T.R. 2009. Sperm morphology and velocity are genetically co-determined in the zebra finch. Evolution 63 : 2730 2737.
51. Parker, G.A. 1970. Sperm competition and its evolutionary consequences in insects. Biol. Rev. Camb. Philos. Soc. 45 : 525 567.
52. Parker, G.A. 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, UK.
53. Pereira, L., Goncalves, J., Franco-Duarte, R., Silva, J., Rocha, T., Arnold, C., Richards, M. Macaulay, V. 2007. No evidence for an mtDNA role in sperm motility: data from complete sequencing of asthenozoospermic males. Mol. Biol. Evol. 24 : 868 874.
54. Pesole, G., Gissi, C., De Chirico, A. Saccone, C. 1999. Nucleotide substitution rate of mammalian mitochondrial genomes. J. Mol. Evol. 48 : 427 434.
55. Pizzari, T. Birkhead, T.R. 2002. The sexually-selected sperm hypothesis: sex-biased inheritance and sexual antagonism. Biol. Rev. Camb. Philos. Soc. 77 : 183 209.
56. R Development Core Team. 2008. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org.
57. Rand, D.M. 2001. The units of selection on mitochondrial DNA. Annu. Rev. Ecol. Syst. 32 : 415 448.
58. Robin, E.D. Wong, R. 1988. Mitochondrial DNA molecules and virtual number of mitochondria per cell in mammalian cells. J. Cell. Physiol. 136 : 507 513.
59. Ruiz-Pesini, E., Diez, C., Lapena, A.C., Perez-Martos, A., Montoya, J., Alvarez, E., Arenas, J. Lopez-Perez, M.J. 1998. Correlation of sperm motility with mitochondrial enzymatic activities. Clin. Chem. 44 : 1616 1620.
60. Ruiz-Pesini, E., Lapena, A.C., Diez-Sanchez, C., Perez-Martos, A., Montoya, J., Alvarez, E., Diaz, M., Urrieis, A., Montoro, L., Lopez-Perez, M.J. Enriquez, J.A. 2000a. Human mtDNA haplogroups associated with high or reduced spermatozoa motility. Am. J. Hum. Genet. 67 : 682 696.
61. Ruiz-Pesini, E., Lapena, A.C., Diez, C., Alvarez, E., Enriquez, J.A. Lopez-Perez, M.J. 2000b. Seminal quality correlates with mitochondrial functionality. Clin. Chim. Acta 300 : 97 105.
62. Ruiz-Pesini, E., Diez-Sanchez, C., Lopez-Perez, M.J. Enriquez, J.A. 2007. The role of the mitochondrion in sperm function: is there a place for oxidative phosphorylation or is this a purely glycolytic process? Curr. Top. Dev. Biol. 77 : 3 19.
63. Shen, Y.-Y., Shi, P., Sun, Y.-B. Zhang, Y.-P. 2009. Relaxation of selective constraints on avian mitochondrial DNA following the degeneration of flight ability. Genome Res. 19 : 1760 1765.
64. Simmons, L.W. 2003. The evolution of polyandry: patterns of genotypic variation in female mating frequency, male fertilization success and a test of the sexy-sperm hypothesis. J. Evol. Biol. 16 : 624 634.
65. Slate, J., Hale, M.C. Birkhead, T.R. 2007. Simple sequence repeats in zebra finch (Taeniopygia guttata) expressed sequence tags: a new resource for evolutionary genetic studies of passerines. BMC Genomics 8 : 52.
66. Sorenson, M.D. Quinn, T.W. 1998. Numts: a challenge for avian systematics and population biology. Auk 115 : 214 221.
67. Spiropoulos, J., Turnbull, D.M. Chinnery, P.F. 2002. Can mitochondrial DNA mutations cause sperm dysfunction? Mol. Hum. Reprod. 8 : 719 721.
68. Thorburn, D.R. 2004. Mitochondrial disorders: prevalence, myths and advances. J. Inherit. Metab. Dis. 27 : 349 362.
69. Torroni, A., Huoponen, K., Francalacci, P., Petrozzi, M., Morelli, L., Scozzari, R., Obinu, D., Savontaus, M.L. Wallace, D.C. 1996. Classification of European mtDNAs from an analysis three European populations. Genetics 144 : 1835 1850.
70. Trounce, I., Neill, S. Wallace, D.C. 1994. Cytoplasmic transfer of the MtDNA nt T8993G (ATP6) point mutation associated with Leigh-Syndrome into mtDNA-less cells demonstrates co-segregation with a decrease in state III respiration and ADP/O ratio. Proc. Natl Acad. Sci. USA 91 : 8334 8338.
71. Wallace, D.C. 1992. Diseases of the mitochondrial DNA. Ann. Rev. Biochem. 61 : 1175 1212.
72. Wallace, D.C. 1999. Mitochondrial diseases in man and mouse. Science 283 : 1482 1488.
73. Wallace, D.C. 2005. A mitochondrial paradigm of metabolic and degenerative diseases, aging, and cancer: a dawn for evolutionary medicine. Annu. Rev. Genet. 39 : 359 407.
74. Ward, P.I. 2000. Sperm length is heritable and sex-linked in the yellow dung fly (Scathophaga stercoraria). J. Zool. Lond. 251 : 349 353.
75. Wolfson, A. 1954. Sperm storage at lower than body temperature outside the body cavity in some passerine birds. Science 120 : 68 71.
76. Zeh, J.A. Zeh, D.W. 2005. Maternal inheritance, sexual conflict and the maladapted male. Trends Genet. 21 : 281 286.
77. Zeviani, M. Antozzi, C. 1997. Mitochondrial disorders. Mol. Hum. Reprod. 3 : 133 148.