Cytonuclear interactions and the economics of mating in seed beetles

American Naturalist

Volumn 176, Issue 2, 2010, Pages 131-140

  Dowling, Damian K ^a   Meerupati, Tejashwari ^b   Arnqvist, Göran ^c  

^a MONASH UNIVERSITY   (Australia)

^b LUND UNIVERSITY   (Sweden)

^c UPPSALA UNIVERSITY   (Sweden)

Author keywords

Cost of mating; Cytonuclear; Cytoplasm; Evolution; Mitochondrial DNA; Sexual conflict

Indexed keywords

MITOCHONDRIAL DNA;

ARMS RACE; BEETLE; CYTOLOGY; CYTOPLASM; FEMALE; GENE EXPRESSION; GENETIC VARIATION; GENOME; HERITABILITY; HYPOTHESIS TESTING; MITOCHONDRIAL DNA; MUTATION; REPRODUCTIVE COST; SEXUAL CONFLICT;

ANIMAL; ARTICLE; BEETLE; CYTOLOGY; EVOLUTION; FEMALE; GENE; GENETIC SELECTION; GENETIC VARIABILITY; GENETICS; GENOME; LONGEVITY; MALE; METABOLISM; PHYSIOLOGY; SEX DIFFERENCE; SEXUAL BEHAVIOR; INSECT GENOME;

ANIMALS; BEETLES; DNA, MITOCHONDRIAL; EVOLUTION; FEMALE; GENES; GENETIC VARIATION; GENOME, INSECT; LONGEVITY; MALE; SELECTION, GENETIC; SEX FACTORS; SEXUAL BEHAVIOR, ANIMAL; BIOLOGICAL EVOLUTION;

BRUCHINAE; CALLOSOBRUCHUS MACULATUS;

EID: 77955625543     PISSN: 00030147     EISSN: None     Source Type: Journal    
DOI: 10.1086/653671     Document Type: Article

References (69)

1. Arnqvist, G., and L. Rowe. 1995. Sexual conflict and arms races between the sexes: a morphological adaptation for control of mating in a female insect. Proceedings of the Royal Society B: Biological Sciences 261:123-127.
2. -. 2005. Sexual conflict. Princeton University Press, Princeton, NJ.
3. Arnqvist, G., T. Nilsson, and M. Katvala. 2005. Mating rate and fitness in female bean weevils. Behavioral Ecology 16:123-127.
4. Ayroles, J. F., M. A. Carbone, E. A. Stone, K. W. Jordan, R. F. Lyman, M. M. Magwire, S. M. Rollmann, et al. 2009. Systems genetics of complex traits in Drosophila melanogaster. Nature Genetics 41:299-307.
5. Ballard, J. W. O., and M. Kreitman. 1995. Is mitochondrial DNA a strictly neutral marker? Trends in Ecology & Evolution 10:485-488.
6. Ballard, J. W. O., and D. M. Rand. 2005. The population biology of mitochondrial DNA and its phylogenetic implications. Annual Review of Ecology, Evolution, and Systematics 36:621-642.
7. Ballard, J. W. O., and M. C. Whitlock. 2004. The incomplete natural history of mitochondria. Molecular Ecology 13:729-744.
8. Blier, P. U., F. Dufresne, and R. S. Burton. 2001. Natural selection and the evolution of mtDNA-encoded peptides: evidence for intergenomic co-adaptation. Trends in Genetics 17:400-406.
9. Cerenius, L., and K. Söderhäll. 2004. The prophenoloxidase- activating system in invertebrates. Immunological Reviews 198:116-126.
10. Chapman, T., L. F. Liddle, J. M. Kalb, M. F. Wolfner, and L. Partridge. 1995. Cost of mating in Drosophila melanogaster females is mediated by male accessory gland products. Nature 373:241-244.
11. Charlat, S., G. D. D. Hurst, and H. Mercot. 2003. Evolutionary consequences of Wolbachia infections. Trends in Genetics 19:217-223.
12. Clancy, D. J. 2008. Variation in mitochondrial genotype has substantial lifespan effects which may be modulated by nuclear background. Aging Cell 7:795-804.
13. Clark, A. G. 1984. Natural selection with nuclear and cytoplasmic transmission. I. A deterministic model. Genetics 107:679-701.
14. -. 1985. Natural selection with nuclear and cytoplasmic transmission. II. Tests with Drosophila from diverse populations. Genetics 111:97-112.
15. Clark, A. G., and E. M. S. Lyckegaard. 1988. Natural selection with nuclear and cytoplasmic transmission. III. Joint analysis of segregation and mtDNA in Drosophila melanogaster. Genetics 118:471-481.
16. Crudgington, H. S., and M. T. Siva-Jothy. 2000. Genital damage, kicking and early death: the battle of the sexes takes a sinister turn in the bean weevil. Nature 407:855-856.
17. Dowling, D. K., and L. W. Simmons. 2009. ROS as universal constraints in life-history evolution. Proceedings of the Royal Society B: Biological Sciences 276:1737-1745.
18. Dowling, D. K., U. Friberg, and G. Arnqvist. 2007a. A comparison of nuclear and cytoplasmic genetic effects on sperm competitiveness and female remating in a seed beetle. Journal of Evolutionary Biology 20:2113-2125.
19. Dowling, D. K., A. L. Nowostawski, and G. Arnqvist. 2007b. Effects of cytoplasmic genes on sperm viability and sperm morphology in a seed beetle: implications for sperm competition theory? Journal of Evolutionary Biology 20:358-368.
20. Dowling, D. K., U. Friberg, F. Hailer, and G. Arnqvist. 2007c. Intergenomic epistasis for fitness: within-population interactions between cytoplasmic and nuclear genes in Drosophila melanogaster. Genetics 175:235-244.
21. Dowling, D. K., K. C. Abiega, and G. Arnqvist. 2007d. Temperaturespecific outcomes of cytoplasmic-nuclear interactions on egg-toadult development time in seed beetles. Evolution 61:194-201.
22. Dowling, D. K., U. Friberg, and J. Lindell. 2008. Evolutionary implications of non-neutral mitochondrial genetic variation. Trends in Ecology & Evolution 23:546-554.
23. Dowling, D. K., A. A. Maklakov, U. Friberg, and F. Hailer. 2009. Applying the genetic theories of ageing to the cytoplasm: cytoplasmic genetic covariation for fitness and lifespan. Journal of Evolutionary Biology 22:818-827.
24. Ellegren, H., and J. Parsch. 2007. The evolution of sex-biased genes and sex-biased gene expression. Nature Reviews Genetics 8:689-698.
25. Ferber, M. L., A. F. Rios, G. Kuhl, M. A. Comendador, and C. Louis. 1997. Infection of the gonads of the SimES strain of Drosophila simulans by the hereditary reovirus DSV. Journal of Invertebrate Pathology 70:143-149.
26. Fiumera, A. C., B. L. Dumont, and A. G. Clark. 2006. Natural variation in male-induced "cost-of-mating" and allele-specific association with male reproductive genes in Drosophila melanogaster. Philosophical Transactions of the Royal Society B: Biological Sciences 361:355-361.
27. Fowler, K., and L. Partridge. 1989. A cost of mating in female fruit flies. Nature 338:760-761.
28. Frank, S. A., and L. D. Hurst. 1996. Mitochondria and male disease. Nature 383:224.
29. Fricke, C., and G. Arnqvist. 2004. Divergence in replicated phylogenies: the evolution of partial post-mating prezygotic isolation in bean weevils. Journal of Evolutionary Biology 17:1345-1354.
30. Fricke, C., G. Arnqvist, and N. Amaro. 2006. Female modulation of reproductive rate and its role in postmating prezygotic isolation in Callosobruchus maculatus. Functional Ecology 20:360-368.
31. Gay, L., P. E. Eady, R. Vasudev, D. J. Hosken, and T. Tregenza. 2009. Costly sexual harassment in a beetle. Physiological Entomology 34:86-92.
32. Gregorius, H. R., and M. D. Ross. 1984. Selection with gene-cytoplasm interaction. I. Maintenance of cytoplasm polymorphisms. Genetics 107:165-178.
33. Harano, T., and T. Miyatake. 2007. Interpopulation variation in female remating is attributable to female and male effects in Callosobruchus chinensis. Journal of Ethology 25:49-55.
34. Harman, D. 1956. Aging: a theory on free radical radiation chemistry. Journal of Gerontology 11:298-300.
35. -. 1972. The biologic clock: the mitochondria? Journal of the American Geriatrics Society 20:145-147.
36. Hotzy, C., and G. Arnqvist. 2009. Sperm competition favors harmful males in seed beetles. Current Biology 19:404-407.
37. Innocenti, P., and E. H. Morrow. 2009. Immunogenic males: a genome-wide analysis of reproduction and the cost of mating in Drosophila melanogaster females. Journal of Evolutionary Biology 22:964-973.
38. James, A. C., and J. W. O. Ballard. 2003. Mitochondrial genotype affects fitness in Drosophila simulans. Genetics 164:187-194.
39. Juchault, P., C. Louis, G. Martin, and G. Noulin. 1991. Masculinization of female isopods (Crustacea) correlated with non-Mendelian inheritance of cytoplasmic viruses. Proceedings of the National Academy of Sciences of the USA 88:10460-10464. (Pubitemid 21915855)
40. Kemp, D. J., and R. L. Rutowski. 2004. A survival cost to mating in a polyandrous butterfly, Colias eurytheme. Oikos 105:65-70.
41. Kondo, R., Y. Satta, E. T. Matsuura, H. Ishiwa, N. Takahata, and S. I. Chigusa. 1990. Incomplete maternal transmission of mitochondrial DNA in Drosophila. Genetics 126:657-663.
42. Lansman, R. A., J. C. Avise, and M. D. Huettel. 1983. Critical experimental test of the possibility of paternal leakage of mitochondrial DNA. Proceedings of the National Academy of Sciences of the USA 80:1969-1971.
43. López-Ferber, M., J. C. Veyrunes, and L. Croizier. 1989. Drosophila S virus is a member of the Reoviridae family. Journal of Virology 63:1007-1009.
44. Lynch, M. 1997. Mutation accumulation in nuclear, organelle, and prokaryotic transfer RNA genes. Molecular Biology and Evolution 14:914-925.
45. Maklakov, A. A., U. Friberg, D. K. Dowling, and G. Arnqvist. 2006. Within-population variation in cytoplasmic genes affects female life span and aging in Drosophila melanogaster. Evolution 60:2081-2086.
46. Matsuura, E. T., Y. T. Tanaka, and N. Yamamoto. 1997. Effects of the nuclear genome on the selective transmission of mitochondrial DNA in Drosophila. Genes and Genetic Systems 72:119-123.
47. Rand, D. M. 2001. The units of selection on mitochondrial DNA. Annual Review of Ecology and Systematics 32:415-448.
48. Rand, D. M., A. G. Clark, and L. M. Kann. 2001. Sexually antagonistic cytonuclear fitness interactions in Drosophila melanogaster. Genetics 159:173-187.
49. Rand, D. M., R. A. Haney, and A. J. Fry. 2004. Cytonuclear coevolution: the genomics of cooperation. Trends in Ecology & Evolution 19:645-653.
50. Rand, D. M., A. Fry, and L. Sheldahl. 2006. Nuclear-mitochondrial epistasis and Drosophila aging: introgression of Drosophila simulans mtDNA modifies longevity in D melanogaster nuclear backgrounds. Genetics 172:329-341.
51. Rawson, P. D., and R. S. Burton. 2002. Functional coadaptation between cytochrome c and cytochrome c oxidase within allopatric populations of a marine copepod. Proceedings of the National Academy of Sciences of the USA 99:12955-12958.
52. Reznick, D. 1985. Costs of reproduction: evaluation of the empirical evidence. Oikos 44:257-267.
53. Rolff, J., and G. Joop. 2002. Estimating condition: pitfalls of using weight as a fitness correlate. Evolutionary Ecology Research 4:931-935.
54. Rönn, J., M. Katvala, and G. Arnqvist. 2006. The costs of mating and egg production in Callosobruchus seed beetles. Animal Behaviour 72:335-342.
55. -. 2007. Coevolution between harmful male genitalia and female resistance in seed beetles. Proceedings of the National Academy of Sciences of the USA 104:10921-10925.
56. Rowe, L., E. Cameron, and T. Day. 2003. Detecting sexually antagonistic coevolution with population crosses. Proceedings of the Royal Society B: Biological Sciences 270:2009-2016.
57. Sakurai, G., and E. Kasuya. 2008. The costs of harassment in the adzuki bean beetle. Animal Behaviour 75:1367-1373.
58. Savalli, U. M., and C. W. Fox. 1998. Genetic variation in paternal investment in a seed beetle. Animal Behaviour 56:953-961.
59. Shabalina, S. A., L. Y. Yampolsky, and A. S. Kondrashov. 1997. Rapid decline of fitness in panmictic populations of Drosophila melanogaster maintained under relaxed natural selection. Proceedings of the National Academy of Sciences of the USA 94:13034-13039.
60. Tatar, M., J. R. Carey, and J. W. Vaupel. 1993. Long-term cost of reproduction with and without accelerated senescence in Callosobruchus maculatus: analysis of age-specific mortality. Evolution 47:1302-1312.
61. Tsai, C. W., E. A. McGraw, E. D. Ammar, R. G. Dietzgen, and S. A. Hogenhout. 2008. Drosophila melanogaster mounts a unique immune response to the rhabdovirus Sigma virus. Applied and Environmental Microbiology 74:3251-3256.
62. Tuda, M., J. Ronn, S. Buranapanichpan, N. Wasano, and G. Arnqvist. 2006. Evolutionary diversification of the bean beetle genus Callosobruchus (Coleoptera: Bruchidae): traits associated with storedproduct pest status. Molecular Ecology 15:3541-3551.
63. Wade, M. J., and Y. Brandvain. 2009. Reversing mother's curse: selection on male mitochondrial fitness effects. Evolution 63:1084-1089.
64. Werren, J. H., L. Baldo, and M. E. Clark. 2008. Wolbachia: master manipulators of invertebrate biology. Nature Reviews Microbiology 6:741-751.
65. Willett, C. S., and R. S. Burton. 2003. Environmental influences on epistatic interactions: viabilities of cytochrome c genotypes in interpopulation crosses. Evolution 57:2286-2292.
66. Yanagi, S., and T. Miyatake. 2003. Costs of mating and egg production in female Callosobruchus chinensis. Journal of Insect Physiology 49:823-827.
67. Zeh, J. A. 2004. Sexy sons: a dead end for cytoplasmic genes. Proceedings of the Royal Society B: Biological Sciences 271 (suppl.): S306-S309.
68. Zeh, J. A., and D. W. Zeh. 2005. Maternal inheritance, sexual conflict and the maladapted male. Trends in Genetics 21:281-286.
69. Zeyl, C., B. Andreson, and E. Weninck. 2005. Nuclear-mitochondrial epistasis for fitness in Saccharomyces cerevisiae. Evolution 59:910-914.