The good-genes and compatible-genes benefits of mate choice

American Naturalist

Volumn 174, Issue 5, 2009, Pages 741-752

  Puurtinen, Mikael ^a   Ketola, Tarmo ^a   Kotiaho, J S ^a  

^a UNIVERSITY OF JYVÄSKYLÄ   (Finland)

Author keywords

Female choice; Genetic compatibility; Indirect benefits; Sexual selection

Indexed keywords

ANIMAL; FITNESS; GENETIC VARIATION; GOOD GENES HYPOTHESIS; HERITABILITY; MATE CHOICE; SEXUAL SELECTION;

ANIMAL; ARTICLE; CROSS BREEDING; FEMALE; GENETIC VARIABILITY; GENETICS; MALE; MATE CHOICE; REPRODUCTION;

ANIMALS; CROSSES, GENETIC; FEMALE; GENETIC VARIATION; MALE; MATING PREFERENCE, ANIMAL; REPRODUCTION;

ANIMALIA;

EID: 72449139653     PISSN: 00030147     EISSN: None     Source Type: Journal    
DOI: 10.1086/606024     Document Type: Article

References (103)

1. Alatalo, R. V., J. Kotiaho, J. Mappes, and S. Parri. 1998. Mate choice for offspring performance: major benefits or minor costs? Proceedings of the Royal Society B: Biological Sciences 265:2297-2301.
2. Andersson, M. 1994. Sexual selection. Princeton University Press, Princeton, NJ.
3. Bang, A., P. Groønkjœr, C. Clemmesen, and H. Hoøie. 2006. Parental effects on early life history traits of Atlantic herring (Clupea harengus L.) larvae. Journal of Experimental Marine Biology and Ecology 334:51-63.
4. Bilde, T., U. Friberg, A. A. Maklakov, J. D. Fry, and G. Arnqvist. 2008. The genetic architecture of fitness in a seed beetle: assessing the potential for indirect genetic benefits of female choice. BMC Evolutionary Biology 8:295. (Pubitemid 352784095)
5. Birkhead, T. R., and A. P. Moøller. 1998. Sperm competition, sexual selection and different, routes to fitness. Pages 757-781 in T. R. Birkhead and A. P. Moøller, eds. Sperm competition and sexual selection. Academic Press, San Diego, CA.
6. Birkhead, T. R., and T. Pizzari. 2002. Postcopulatory sexual selection. Nature Reviews Genetics 3:262-273.
7. Blouin, M. S. 1992. Genetic correlations among morphometric traits and rates of growth and differentiation in the green tree frog, Hyla cinerea. Evolution 46:735-744.
8. Boake, C. R. B. 1985. Genetic consequences of mate choice: a quantitative genetic method for testing sexual selection theory. Science 227:1061-1063.
9. Casalini, M., M. Agbali, M. Reichard, M. Konecna, A. Bryjova, and C. Smith. 2009. Male dominance, female mate choice, and intersexual conflict in the rose bitterling (Rhodeus ocellatus). Evolution 63:366-376.
10. Charlesworth, B. 1987. The heritability of fitness. Pages 21-40 in J. W. Bradbury and M. B. Andersson, eds. Sexual selection: testing the alternatives. Wiley, Chichester.
11. Charlesworth, B., and D. Charlesworth. 1999. The genetic basis of inbreeding depression. Genetical Research 74:329-340.
12. Colegrave, N., J. Kotiaho, and J. L. Tomkins. 2002. Mate choice or polyandry: reconciling genetic compatibility and good genes sexual selection. Evolutionary Ecology Research 4:911-917. (Pubitemid 135695636)
13. Comstock, R. E., and H. F. Robinson. 1948. The components of genetic variance in populations of biparental progenies and their use in estimating the average degree of dominance. Biometrics 4:254-266.
14. Crnokrak, P., and D. A. Roff. 1995. Dominance variance: associations with selection and fitness. Heredity 75:530-540. (Pubitemid 26470298)
15. Darwin, C. 1871. The descent, of man and selection in relation to sex. J. Murray, London.
16. Dawson, P. S. 1965. Estimation of components of phenotypic variance for development rate in Tribolium. Heredity 20:417.
17. Dowling, D. K., U. Friberg, F. Hailer, and G. Arnqvist. 2007. Intergenomic epistasis for fitness: within-population interactions between cytoplasmic and nuclear genes in Drosophila melanogaster. Genetics 175:235-244.
18. Dowling, D. K., U. Friberg, and J. Lindell. 2008. Evolutionary implications of non-neutral mitochondrial genetic variation. Trends in Ecology & Evolution 23:546-554.
19. Dziminski, M. A., J. D. Roberts, and L. W. Simmons. 2008. Fitness consequences of parental compatibility in the frog Crinia georgiana. Evolution 62:879-886.
20. Evans, J. R., and D. J. Marshall. 2005. Male-by-female interactions influence fertilization success and mediate the benefits of polyandry in the sea urchin Heliocidaris erythrogramma. Evolution 59:106-112.
21. Evans, J. P., F. Garcia-Gonzalez, and D. J. Marshall. 2007. Sources of genetic and phenotypic variance in fertilization rates and larval traits in a sea urchin. Evolution 61:2832-2838.
22. Falconer, D. S., and T. F. C. Mackay. 1996. Introduction to quantitative genetics. Pearson, Harlow.
23. Fedorka, K. M., and T. A. Mousseau. 2004. Female mating bias results in conflicting sex-specific offspring fitness. Nature 429:65-67.
24. Firman, R. C., and L. W. Simmons. 2008. Polyandry fadlitates postcopulatory inbreeding avoidance in house mice. Evolution 62:603-611.
25. Fossoy, F., A. Johnsen, and J. T. Lifjeld. 2008. Multiple genetic benefits of" female promiscuity in a socially monogamous passerine. Evolution 62:145-156.
26. Fromhage, L., H. Kokko, and J. M. Reid. 2009. Evolution of mate choice for genome-wide heterozygosity. Evolution 63:684-694.
27. Gillingham, M. A. F., D. S. Richardson, H. Loøvlie, A. Moynihan, K. Worley, and T. Pizzari. 2009. Cryptic preference for MHC-dissimilar females in male red junglefowl, Gallus gallus. Proceedings of the Royal Society B: Biological Sciences 276:1083-1092.
28. Greeff, J. M., G. J. J. van Vuuren, P. Kryger, and J. C. Moore. 2009. Outbreeding and possibly inbreeding depression in a pollinating fig wasp with a mixed mating system. Heredity 102:349-356.
29. Gustafsson, L. 1986. Lifetime reproductive success and heritabilities: empirical support for Fisher's fundamental theorem. American Naturalist 128:761-764.
30. Head, M. L., J. Hunt, M. D. Jennions, and R. Brooks. 2005. The indirect benefits of mating with attractive males outweigh the direct costs. PLoS Biology 3:e33.
31. Helgason, A., S. Palsson, D. F. Guthbjartsson, T. Kristjansson, and K. Stefansson. 2008. An association between the kinship and fertility of human couples. Science 319:813-816. (Pubitemid 351225871)
32. Hill, W. G., M. E. Goddard, and P. M. Visscher. 2008. Data and theory point to mainly additive genetic variance for complex traits. PLoS Genetics 4:el000008.
33. Hunt, J., and L. W. Simmons. 2002. The genetics of maternal care: direct and indirect genetic effects on phenotype in the dung beetle Onthophagus taurus. Proceedings of the National Academy of Sciences of the USA 99:6828-6832. (Pubitemid 34526217)
34. Hunt, J., L. Bussière, M. D. Jennions, and R. Brooks. 2004. What is genetic quality? Trends in Ecology & Evolution 19:329-333.
35. Huuskonen, H., O.-P. Penttinen, and J. Piironen. 2003. Effects of temperature and parental background on the embryonic survival and metabolic rate of newly hatched Arctic charr. Pages 35-44 in H. I. Browman and A. B. Skiftesvik, eds. The big fish bang. Proceedings of the 26th Annual Larval Fish Conference. Institute of Marine Research, Bergen.
36. Ivy, T. M. 2007. Good genes, genetic compatibility and the evolution of polyandry: use of the diallel cross to address competing hypotheses. Journal of Evolutionary Biology 20:479-487.
37. Jacob, A., S. Nussle, A. Britschgi, G. Evanno, R. Muller, and C. Wedekind. 2007. Male dominance linked to size and age, but not to "good genes" in brown trout (Salmo trutta). BMC Evolutionary Biology 7:207.
38. Jones, T. M., R. J. Quinnell, and A. Balmford. 1998. Fisherian flies: benefits of female choice in a lekking sandfly. Proceedings of the Royal Sodety B: Biological Sciences 265:1651-1657.
39. Kempenaers, B. 2007. Mate choice and genetic quality: a review of the heterozygosity theory. Advances in the Study of Behavior 37:189-278.
40. Kokko, H., R. Brooks, M. D. Jennions, and J. Morley. 2003. The evolution of mate choice and mating biases. Proceedings of the Royal Society B: Biological Sciences 270:653-664. (Pubitemid 36359742)
41. Kokko, H., M. D. Jennions, and R. Brooks. 2006. Unifying and testing models of sexual selection. Annual Review of Ecology, Evolution, and Systematics 37:43-66. (Pubitemid 44907612)
42. Kotiaho, J. S., and M. Puurtinen. 2007. Mate choice for indirect genetic benefits: scrutiny of the current, paradigm. Functional Ecology 21:638-644. (Pubitemid 47052341)
43. Kotiaho, J. S., L. W. Simmons, J. Hunt, and J. L. Tomkins. 2003. Males influence maternal effects that promote sexual selection: a quantitative genetic experiment with dung beetles Onthophagus taurus. American Naturalist 161:852-859.
44. Kotiaho, J. S., N. R. LeBas, M. Puurtinen, and J. L. Tomkins. 2008. On the resolution of the lek paradox. Trends in Ecology & Evolution 23:1-3.
45. Kruuk, L. E. B., T. H. Clutton-Brock, J. Slate, J. M. Pemberton, S. Brotherstone, and F. E. Guinness. 2000. Heritability of fitness in a wild mammal population. Proceedings of the National Academy of Sciences of the USA 97:698-703.
46. Laurila, A., S. Karttunen, and J. Merilä. 2002. Adaptive phenotypic plasticity and genetics of larval life histories in two Rana temporaria populations. Evolution 56:617-627.
47. Lehmann, L., L. F. Keller, and H. Kokko. 2006. Mate choice evolution, dominance effects, and the maintenance of genetic variation. Journal of Theoretical Biology 244:282-295.
48. Lynch, M., and B. Walsh. 1998. Genetics and analysis of quantitative traits. Sinauer, Sunderland, MA.
49. Maklakov, A. A., U. Friberg, D. K. Dowling, G. Arnqvist, and D. Promislow. 2006. Within-population variation in cytoplasmic genes affects female life span and aging in Drosophila melanogaster. Evolution 60:2081-2086.
50. Marshall, D. J., and J. P. Evans. 2005. The benefits of polyandry in the free-spawning polychaete Galeolaria caespitosa. Journal of Evolutionary Biology 18:735-741.
51. -. 2007. Context-dependent genetic benefits of polyandry in a marine hermaphrodite. Biology Letters 3:685-688.
52. Mays, H. L., Jr., and G. E. Hill. 2004. Choosing mates: good genes versus genes that are a good fit. Trends in Ecology & Evolution 19:554-559.
53. Mead, L. S., and S. J. Arnold. 2004. Quantitative genetic models of sexual selection. Trends in Ecology & Evolution 19:264-271.
54. Merilä, J., and B. C. Sheldon. 1999. Genetic architecture of fitness and nonfitness traits: empirical patterns and development, of ideas. Heredity 83:103-109. (Pubitemid 29452118)
55. Merilä, J., F. Söderman, R. O'Hara, K. Räsänen, and A. Laurila. 2004. Local adaptation and genetics of add-stress tolerance in the moor frog, Rana arvalis. Conservation Genetics 5:513-527. (Pubitemid 39225126)
56. Miller, R. H., J. E. Legates, and C. C. Cockerham. 1963. Estimation of nonadditive hereditary variance in traits of mice. Genetics 48:177-188.
57. Moøller, A. P., and R. V. Alatalo. 1999. Good-genes effects in sexual selection. Proceedings of the Royal Society B: Biological Sciences 266:85-91.
58. Mousseau, T. A., and D. A. Roff. 1987. Natural selection and the heritability of fitness components. Heredity 59:181-198.
59. Neff, B. D. 2004. Stabilizing selection on genomic divergence in a wild fish population. Proceedings of the National Academy of Sciences of the USA 101:2381-2385.
60. Neff, B. D., and T. E. Pitcher. 2005. Genetic quality and sexual selection: an integrated framework for good genes and compatible genes. Molecular Ecology 14:19-38.
61. -. 2008. Mate choice for non-additive genetic benefits: a resolution to the lek paradox Journal of Theoretical Biology 254:147-155.
62. -. 2009. Mate choice for nonadditive genetic benefits and the maintenance of genetic diversity in song sparrows. Journal of Evolutionary Biology 22:424-429.
63. Newman, R. A. 1988. Genetic variation for larval anuran (Scaphiopus couchii) development, time in an uncertain environment. Evolution 42:763-773.
64. Nilsson, J. 1992. Genetic parameters of growth and sexual maturity in Arctic char (Salvelinus alpinus). Aquaculture 106:9-19.
65. Norris, K. 1993. Heritable variation in a plumage indicator of viability in male great tits Parus major. Nature 362:537-539. (Pubitemid 23113026)
66. Pakkasmaa, S., and M. Jones. 2002. Individual-level analysis of early life history traits in hatchery-reared lake trout. Journal of Fish Biology 60:218-225.
67. Peer, K., and M. Taborsky. 2005. Outbreeding depression, but no inbreeding depression in haplodiploid ambrosia beetles with regular sibling mating. Evolution 59:317-323. (Pubitemid 40356046)
68. Penn, D. J. 2002. The scent of genetic compatibility: sexual selection and the major histocompatibility complex. Ethology 108:1-21. (Pubitemid 34134669)
69. Pétrie, M. 1994. Improved growth and survival of offspring of peacocks with more elaborate trains. Nature 371:598-599. (Pubitemid 24315738)
70. Pitcher, T. E., and B. D. Neff. 2006. MHC class IIB alleles contribute to both additive and nonadditive genetic effects on survival in chinook salmon. Molecular Ecology 15:2357-2365.
71. -. 2007. Genetic quality and offspring performance in chinook salmon: implications for supportive breeding. Conservation Genetics 8:607-616.
72. Pusey, A., and M. Wolf. 1996. Inbreeding avoidance in animals. Trends in Ecology & Evolution 11:201-206.
73. Puurtinen, M., T. Ketola, and J. S. Kotiaho. 2005. Genetic compatibility and sexual selection. Trends in Ecology & Evolution 20:157-158.
74. Queller, D., and K. F. Goodnight. 1989. Estimating relatedness using genetic markers. Evolution 43:258-275.
75. Qvarnström, A., J. E. Brommer, and L. Gustafsson. 2006. Testing the genetics underlying the co-evolution of mate choice and ornament in the wild. Nature 441:84-86. (Pubitemid 43827955)
76. Rand, D. M., A. G. Clark, and L. M. Kann. 2001. Sexually antagonistic cytonuclear fitness interactions in Drosophila melanogaster. Genetics 159:173-187.
77. Reid, J. M. 2007. Secondary sexual ornamentation and non-additive genetic benefits of female mate choice. Proceedings of the Royal Society B: Biological Sciences 274:1395-1402.
78. Reinhold, K. 2004. Modeling a version of the good-genes hypothesis: female choice of locally adapted males. Organisms, Diversity and Evolution 4:157-163. (Pubitemid 39098743)
79. Reynolds, J. D., and M. R. Gross. 1992. Female mate preference enhances offspring growth and reproduction in a fish, Poecilia reticulata. Proceedings of the Royal Society B: Biological Sciences 250:57-62.
80. Richard, M., S. Losdat, J. Lecomte, M. de Fraipont, and J. Clobert. 2009. Optimal level of inbreeding in the common lizard. Proceedings of the Royal Society B: Biological Sciences 276:2779-2786.
81. Roberts, S. C., and L. M. Gosling. 2003. Genetic similarity and quality interact in mate choice decisions by female mice. Nature Genetics 35:103-106.
82. Roberts, S. C., M. L. Hale, and M. Petrie. 2006. Correlations between heterozygosity and measures of genetic similarity: implications for understanding mate choice. Journal of Evolutionary Biology 19:558-569.
83. Rodríguez-Muñoz, R., and T. Tregenza. 2008. Genetic compatibility and hatching success in the sea lamprey (Petromyzon marinus). Biology Letters 5:286-288.
84. Roff, D. A., and K. Emerson. 2006. Epistasis and dominance: evidence for differential effects in life-history versus morphological traits. Evolution 60:1981-1990.
85. Roffi D. A., and T. A. Mousseau. 1987. Quantitative genetics and fitness: lessons from Drosophila. Heredity 58:103-118.
86. Rowe, L., and D. Houle. 1996. The lek paradox and the capture of genetic variance by condition dependent traits. Proceedings of the Royal Society B: Biological Sciences 263:1415-1421. (Pubitemid 27178059)
87. Rudolfsen, G., L. Figenschou, I. Folstad, J. T. Noedeide, and E. Soøreng. 2005. Potential fitness benefits from mate selection in the Atlantic cod (Gadus morhua). Journal of Evolutionary Biology 18:172-179.
88. Rülicke, T. R., M. Chapuisat, F. R. Hornberger, E. Macas, and C. Wedekind. 1998. MHC-genotype of progeny influenced by parental infection. Proceedings of the Royal Society B: Biological Sciences 265:711-716.
89. Rundle, H. D., A. Ödeen, and A. OØ. Mooers. 2007. An experimental test for indirect benefits in Drosophila melanogaster. BMC Evolutionary Biology 8:36.
90. Semlitsch, R. D. 1993. Adaptive genetic variation in growth and development of tadpoles of the hybridogenetic Rana esculenta complex. Evolution 47:1805-1818.
91. Sherman, C. D. H., E. Wapstra, T. Uller, and M. Olsson. 2008. Males with high genetic similarity to females sire more offspring in sperm competition in Peron's tree frog Litoria peronii. Proceedings of the Royal Society B: Biological Sciences 275:971-978.
92. Simmons, L. W. 2005. The evolution of polyandry: sperm competition, sperm selection, and offspring viability. Annual Review of Ecology, Evolution, and Systematics 36:125-146.
93. Sommer, S., and P. B. Pearman. 2003. Quantitative genetic analysis of larval life history traits in two alpine populations of Rana temporaria. Genetica 118:1-10. (Pubitemid 36463366)
94. Teplitsky, C., J. A. Mills, J. W. Yarrall, and J. Merilä. 2009. Heritability of fitness componente in a wild bird population. Evolution 63:716-726.
95. Tomkins, J. L., J. Radwan, J. S. Kotiaho, and T. Tregenza. 2004. Genic capture and resolving the lek paradox. Trends in Ecology & Evolution 19:323-328.
96. Travis, J., S. B. Emerson, and M. Blouin. 1987. A quantitative-genetic analysis of larval life-history traits in Hyla crucifier. Evolution 41: 145-156.
97. Tregenza, T., and N. Wedell. 2000. Genetic compatibility, mate choice and patterns of parentage: invited review. Molecular Ecology 9: 1013-1027. (Pubitemid 30613148)
98. Wedekind, C., M. Chapuisat, E. Macas, and T. Rulicke. 1996. Nonrandom fertilization in mice correlates with the MHC and something else. Heredity 77:400-409. (Pubitemid 26380815)
99. Wedekind, C., R. Müller, and H. Spicher. 2001. Potential genetic benefits of mate selection in whitefish. Journal of Evolutionary Biology 14:980-986. (Pubitemid 34029806)
100. Wedekind, C., G. Evanno, D. Urbach, A. Jacob, and R. Müller. 2008. "Good-genes" and "compatible-genes" effects in an alpine whitefish and the information content of breeding tubercles over the course of the spawning season. Genetica 134:21-30.
101. Wedell, N., and T. Tregenza. 1999. Successful fathers sire successful sons. Evolution 53:620-625.
102. Zeh, J. A., and D. W. Zeh. 1996. The evolution of polyandry. I. Intragenomic conflict and genetic incompatibility. Proceedings of the Royal Society B: Biological Sciences 263:1711-1717.
103. -. 1997. The evolution of polyandry. II. Post-copulatory defences against, genetic incompatibility. Proceedings of the Royal Society B: Biological Sciences 264:69-75.