Effects of cytoplasmic genes on sperm viability and sperm morphology in a seed beetle: Implications for sperm competition theory?

Journal of Evolutionary Biology

Volumn 20, Issue 1, 2007, Pages 358-368

  Dowling, D K ^a   Nowostawski, A Larkeson ^a   Arnqvist, G ^a  

^a UPPSALA UNIVERSITY   (Sweden)

Author keywords

Adaptive evolution; Cytoplasmic; Maternal age; Maternal effects; Maternal inheritance; Mitochondrial DNA; Nuclear; Sperm quality

Indexed keywords

MITOCHONDRIAL DNA;

BEETLE; CYTOPLASM; FERTILIZATION (REPRODUCTION); GENETIC VARIATION; INTROGRESSION; MATERNAL EFFECT; MITOCHONDRIAL DNA; MORPHOLOGY; SPERM COMPETITION; VIABILITY;

ADAPTATION; ANIMAL; ARTICLE; BEETLE; COMPARATIVE STUDY; CROSS BREEDING; CYTOLOGY; GENETIC VARIABILITY; GENETICS; INHERITANCE; MALE; PHYSIOLOGY; SPERMATOZOON;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; BEETLES; CROSSES, GENETIC; DNA, MITOCHONDRIAL; INHERITANCE PATTERNS; MALE; SPERMATOZOA; VARIATION (GENETICS);

BRUCHINAE; CALLOSOBRUCHUS MACULATUS; COLEOPTERA;

EID: 33845716161     PISSN: 1010061X     EISSN: 14209101     Source Type: Journal    
DOI: 10.1111/j.1420-9101.2006.01189.x     Document Type: Article

References (75)

1. Arnqvist, G. & Rowe, L. 2002. Antagonistic coevolution in a group of insects. Nature 415: 787-789.
2. Arnqvist, G. & Rowe, L. 2005. Sexual Conflict. Princeton University Press, Princeton, NJ.
3. Baccetti, B., Burrini, A.G., Dallai, R., Giusti, F., Mazzini, M., Renieri, T., Rosati, F. & Selmi, G. 1973. Structure and function of the spermatozoon of Tenebrio molitor (The spermatozoon of Arthropoda. XX). J. Mechanochem. Cell Motil. 2: 149-161.
4. Ballard, J.W.O. & Rand, D.M. 2005. The population biology of mitochondrial DNA and its phylogenetic implications. Annu. Rev. Ecol. Evol. Syst. 36: 621-642.
5. Ballard, J.W.O. & Whitlock, M.C. 2004. The incomplete natural history of mitochondria. Mol. Ecol. 13: 729-744.
6. Báo, S., Lins, U., Farina, M. & De Souza, W. 1992. Mitochondrial derivatives of Culex quinquefasciatus (Culicidae) spermatozoon: some new aspects evidenced by cytochemistry and image processing. J. Ultrastruct. Mol. Struct. Res. 109: 46-51.
7. Bernasconi, G., Hellriegel, B., Heyland, A. & Ward, P.I. 2002. Sperm survival in the female reproductive tract in the fly Scathophaga stercoraria (L). J. Insect Physiol. 48: 197-203.
8. Bigliardi, E., Baccetti, B., Burrini, G. & Pallini, V. 1970. The spermatozoon of Arthropoda. XII. The distribution of some enzymes in the insect sperm tail. In: Comparative Spermatology (B. Baccetti, ed.), pp. 451-464. Academic Press, New York.
9. Birkhead, T.R., Martinéz, 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.
10. 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.
11. ter Braak, C.J.F. 1987. Permutation versus bootstrap significance tests in multiple regression and ANOVA ANOVA. Aust. J. Stat. 29: 91-100.
12. Byrne, P.G., Simmons, L.W. & Roberts, J.D. 2003. Sperm competition and the evolution of gamete morphology in frogs. Proc. R. Soc. B 270: 2079-2086.
13. Champion de Crespigny, F.E. & Wedell, N. 2006. Wolbachia infection reduces sperm competitive ability in an insect. Proc. R. Soc. B 273: 1455-1458.
14. Chippindale, A.K., Gibson, J.R. & Rice, W.R. 2001. Negative genetic correlation for adult fitness between sexes reveals ontogenetic conflict in Drosophila. Proc. Natl Acad. Sci. USA 98: 1671-1675.
15. Collins, A.M. & Donoghue, A.M. 1999. Viability assessment of honeybee sperm, Apis mellifera, sperm using dual fluorescent staining. Theriogenology 51: 1513-1523.
16. Credland, P.F. & Wright, A.W. 1989. Factors affecting female fecundity in the cowpea seed beetle, Callosobruchus maculatus (Coleoptera: Bruchidae). J. Stored Prod. Res. 25: 125-136.
17. Cummins, J.M., Jequier, A.M., Martin, R., Mehmet, D. & Goldblatt, J. 1998. Semen levels of mitochondrial DNA deletions in men attending an infertility clinic do not correlate with phenotype. J. Androl. 21: 47-52.
18. Dewsbury, D.A. 1982. Ejaculate cost and male choice. Am. Nat. 119: 601-610.
19. Dick, K.M. & Credland, P.F. 1984. Egg production and development of three strains of Callosobruchus maculatus (F.) (Coleoptera: Bruchidae). J. Stored Prod. Res. 20: 221-227.
20. Eady, P. 1994. Sperm transfer and storage in relation to sperm competition in Callosobruchus maculatus. Behav. Ecol. Sociobiol. 35: 123-129.
21. Fox, C.W. & Dingle, H. 1994. Dietary mediation of maternal age effects on offspring performance in a seed beetle (Coleoptera: Bruchidae). Funct. Ecol. 8: 600-606.
22. Fox, C.W., Bush, M.L. & Wallin, W.G. 2003. Maternal age affects offspring lifespan of the seed beetle, Callosobruchus maculatus. Funct. Ecol. 17: 811-820.
23. Frank, S.A. & Hurst, L.D. 1996. Mitochondria and male disease. Nature 383: 224.
24. 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.
25. Gage, M.J.G. 1994. Associations between body size, mating pattern, testis size and sperm lengths across butterflies. Proc. R. Soc. B 258: 247-254.
26. Gage, M.J.G. 1995. Continuous variation in reproductive strategy as an adaptive response to population density in the moth Plodia interpunctella. Proc. R. Soc. B 261: 25-30.
27. 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.
28. 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: relative sperm velocity is the primary determinant of fertilization success. Curr. Biol. 14: 44-47.
29. García-González, F. & Simmons, L.W. 2005. Sperm viability matters in insect sperm competition. Curr. Biol. 15: 271-275.
30. Gemmell, N.J. & Allendorf, F.W. 2001. Mitochondrial mutations may decrease population viability. Trends Ecol. Evol. 16: 115-117.
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. Green, K. 2003. Age-related variation in mean sperm length, in the rove beetle Aleochara bilineata. J. Insect Physiol. 49: 993-998.
33. Harvey, P.H. & May, R.M. 1989. Copulation dynamics - out for the sperm count. Nature 337: 508-509.
34. 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.
35. Hosken, D.J. 2003. Sperm biology: size indeed matters. Curr. Biol. 13: R355-R356.
36. Hunter, F.M. & Birkhead, T.R. 2002. Sperm viability and sperm competition in insects. Curr. Biol. 12: 121-123.
37. James, A.C. & Ballard, J.W.O. 2003. Mitochondrial genotype affects fitness in Drosophila simulans. Genetics 164: 187-194.
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 in 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. Stud. Behav. 24: 291-315.
41. Kondo, N., Shimada, M. & Fukatsu, T. 1999. High prevalence of Wolbachia in the azuki bean beetle Callosobruchus chinensis (Coleoptera, Bruchidae). Zool. Sci. 16: 955-962.
42. Kondo, N., Nikoh, N., Ijichi, N., Shimada, M. & Fukatsu, T. 2002. Genome fragment of Wolbachia endosymbiont transferred to X chromosome of host insect. Proc. Natl Acad. Sci. USA 99: 14280-14285.
43. Kujoth, G.C., Hiona, A., Pugh, T.D., Someya, S., Panzer, K., Wohlgemuth, S.E., Hofer, T., Seo, A.Y., Sullivan, R., Jobling, W.A., Morrow, J.D., Van Remmen, H., Sedivy, J.M., Yamasoba, T., Tanokura, M., Weindruch, R., Leeuwenburgh, C. & Prolla, T.A. 2005. Mitochondrial DNA mutations, oxidative stress, and apoptosis in mammalian aging. Science 309: 481-484.
44. Manly, B.F.J. 1997. Randomization, Bootstrap and Monte Carlo Methods in Biology, 2nd edn. Chapman and Hall, London.
45. Mitchell, J.A., Nelson, L. & Hafez, E. 1976. Motility of spermatozoa. In: Human Semen and Fertility Regulation in Men (E.S.E. Hafez, ed.), pp. 83-106. C. V. Mosby, St Louis, MO.
46. Moore, F.L. & Reijo-Pera, R.A. 2000. Male sperm motility dictated by mother's mtDNA. Am. J. Hum. Genet. 67: 542-548.
47. Moore, P.J., Harris, W.E., Montrose, V.T., Levin, D. & Moore, A. 2004. Constraints on evolution and postcopulatory sexual selection: trade-offs among ejaculate characteristics. Evolution 58: 1773-1780.
48. Morrow, E.H. & Gage, M.J.G. 2001. Artificial selection and heritability of sperm length in Gryllus bimaculatus. Heredity 87: 356-362.
49. Olsson, M., Madsen, T. & Shine, R. 1997. Is sperm really so cheap? Costs of reproduction in male adders, Vipera berus. Proc. R. Soc. B 264: 455-459.
50. Ouedraogo, A.P. & Huignard, J. 1981. Polymorphism and ecological reactions in Callosobruchus maculatus F. (Coleoptera, Bruchidae) in Upper Volta. In: The Ecology of Bruchids Attacking Legumes (Pulses). Series Entomologica, Vol. 19 (V. Labeyrie, ed.), pp. 175-184. Dr W. Junk Publishers, The Hague.
51. Perotti, M.E. 1973. The mitochondrial derivative of the spermatozoon of Drosophila before and after fertilization. J. Ultrastruct. Res. 44: 181-198.
52. Pitnick, S. 1996. Investment in testes and the cost of making long sperm in Drosophila. Am. Nat. 148: 57-80.
53. Pitnick, S. & Markow, T.A. 1994. Large-male advantages associated with costs of sperm production in Drosophila hydei, a species with giant sperm. Proc. Natl Acad. Sci. USA 91: 9277-9281.
54. Pizzari, T. & Birkhead, T.R. 2002. The sexually-selected sperm hypothesis: sex-biased inheritance and sexual antagonism. Biol. Rev. 77: 183-209.
55. Rand, D.M. 2001. The units of selection on mitochondrial DNA. Annu. Rev. Ecol. Syst. 32: 415-448.
56. Rand, D.M., Clark, A.G. & Kann, L.M. 2001. Sexually antagonistic cytonuclear fitness interactions in Drosophila melanogaster. Genetics 159: 173-187.
57. Ruiz-Pesini, E., Lapeña, A.-C., Díez-Sánchez, C., Péres-Martos, A., Montoya, J., Alvarez, E., Díaz, M., Urriés, A., Montoro, L., López-Péres, M.J. & Enríquez, J.A. 2000. Human mtDNA haplotypes associated with high or reduced spermatozoa motility. Am. J. Hum. Genet. 67: 682-696.
58. Samuels, D.C. 2004. Mitochondrial DNA repeats constrain the life span of mammals. Trends Genet. 20: 226-229.
59. Savalli, U.M. & Fox, C.W. 1998. Genetic variation in paternal investment in a seed beetle. Anim. Behav. 56: 953-961.
60. Simmons, L.W. & Kotiaho, J.S. 2002. Evolution of ejaculates: patterns of phenotypic and genotypic variation and condition dependence in sperm competition traits. Evolution 56: 1622-1631.
61. Simmons, L.W. & Roberts, B. 2005. Bacterial immunity traded for sperm viability in male crickets. Science 309: 2031.
62. Simmons, L.W., Wernham, J., Garcia-Gonzalez, F. & Kamien, D. 2003. Variation in paternity in the field cricket Teleogryllus oceanicus: no detectable influence of sperm numbers or sperm length. Behav. Ecol. 14, 539-545.
63. Sivinski, J. 1984. Sperm competition. In: Sperm Competition and the Evolution of Animal Mating Systems (R.L. Smith, ed.), pp. 85-115. Academic Press, London.
64. Snook, R.R. 2005. Sperm in competition: not playing by the numbers. Trends Ecol. Evol. 20: 46-53.
65. Snook, R.R. & Hosken, D.J. 2004. Sperm death and dumping in Drosophila. Nature 428: 939-941.
66. St John, J.C., Jokhi, R.P. & Barratt, C.L.R. 2001. Men with oligoasthenoteratozoospermia harbour higher numbers of multiple DNA deletions in their spermatozoa, but individual deletions are not indicative of overall aetiology. Mol. Hum. Reprod. 7: 103-111.
67. St John, J.C., Jokhi, R.P. & Barratt, C.L.R. 2005. The impact of mitochondrial genetics on male infertility. Int. J. Androl. 28: 65-73.
68. Trifunovic, A., Wredenberg, A., Falkenberg, M., Spelbrink, J.N., Rovio, A.T., Bruder, C.E., Bohlooly, Y.M., Gidlof, S., Oldfors, A., Wibom, R., Tornell, J., Jacobs, H.T. & Larsson, N.G. 2005. Premature ageing in mice expressing defective mitochondrial DNA polymerase. Nature 429: 417-423.
69. Tuda, M., Rönn, J., Buranapanichpan, S., Wasano, N. & Arnqvist, G. 2006. Evolutionary diversification of the bean beetle genus Callosobruchus (Coleoptera: Bruchidae): traits associated with stored-product pest status. Mol. Ecol., in press.
70. Van Voorhies, W.A. 1992. Production of sperm reduces nematode life-span. Nature 360: 456-458.
71. Wade, M.J. & Chang, N.W. 1995. Increased male-fertility in Tribolium confusum beetles after infection with the intracellular parasite Wolbachia. Nature 373: 72-74.
72. Ward, P.I. 2000. Sperm length is heritable and sex-linked in the yellow dung fly Scathophaga stercoraria. Journal of Zoology 251: 349-353.
73. Werner, M., Zissler, D. & Peschke, K. 1999. Structure and energy pathways of spermatozoa of the rove beetle Aleochara bilineata (Coleoptera, Staphylinidae). Tissue Cell 31: 413-420.
74. Zeh, J.A. 2004. Sexy sons: a dead end for cytoplasmic genes. Proc. R. Soc. B 271 (Suppl.): S306-S309.
75. Zeyl, C., Andreson, B. & Weninck, E. 2005. Nuclear-mitochondrial epistasis for fitness in Saccharomyces cerevisiae. Evolution 59: 910-914.