Males influence maternal effects that promote sexual selection: A quantitative genetic experiment with dung beetles Onthophagus taurus

American Naturalist

Volumn 161, Issue 6, 2003, Pages 852-859

  Kotiaho, Janne S ^a,b   Simmons, Leigh W ^a   Hunt, John ^a,c   Tomkins, Joseph L ^a,d  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^b UNIVERSITY OF JYVÄSKYLÄ   (Finland)

^c UNIVERSITY OF NEW SOUTH WALES   (Australia)

^d UNIVERSITY OF ST ANDREWS   (United Kingdom)

Author keywords

Coefficient of additive genetic variance; Differential allocation; Heritability; Indirect genetic effects; Maternal effects

Indexed keywords

BEETLE; GENETIC DIFFERENTIATION; HERITABILITY; MATERNAL EFFECT; SEXUAL SELECTION;

ANIMAL; ARTICLE; BEETLE; BODY CONSTITUTION; EVOLUTION; FEMALE; GENETIC SELECTION; GENETIC VARIABILITY; GENETICS; HISTOLOGY; MALE; PHYSIOLOGY; SEX RATIO;

ANIMALS; BEETLES; BODY CONSTITUTION; EVOLUTION; FEMALE; MALE; SELECTION (GENETICS); SEX RATIO; VARIATION (GENETICS);

ANIMALIA; COLEOPTERA; INSECTA; ONTHOPHAGUS; ONTHOPHAGUS TAURUS;

EID: 0038302128     PISSN: 00030147     EISSN: None     Source Type: Journal    
DOI: 10.1086/375173     Document Type: Article

References (55)

1. Andersson, M. 1986. Evolution of condition-dependent sex ornaments and mating preferences: sexual selection based on viability differences. Evolution 40:804-816.
2. Arnqvist, G., and T. Nilsson. 2000. The evolution of polyandry: multiple mating and female fitness in insects. Animal Behaviour 60:145-164.
3. Boucher, L., and J. Huignard. 1987. Transfer of male secretions from the spermatophore to the female insect in Caryedon serratus (Ol.): analysis of the possible trophic role of these secretions. Journal of Insect Physiology 33:949-957.
4. Burley, N. 1985. Leg band color and mortality patterns in captive breeding populations of zebra finches. Auk 102: 647-651.
5. _. 1986. Sexual selection for aesthetic traits in species with biparental care. American Naturalist 127:415-445.
6. _. 1988. The differential allocation hypothesis: an experimental test. American Naturalist 132:611-628.
7. 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.
8. Cook, D. 1988. Sexual selection in dung beetles. II. Female fecundity as an estimate of male reproductive success in relation to horn size, and alternative behavioural strategies in Onthophagus binodis Thunberg (Scarabaeidae: Onthophagini). Australian Journal of Zoology 36:521-532.
9. Cunningham, E. J., and A. F. Russell. 2000. Egg investment is influenced by male attractiveness in the mallard. Nature 404:74-77.
10. Drnevich, J. M., R. S. Papke, C. L. Rauser, and R. L. Rutowski. 2001. Material benefits from multiple mating in female mealworm beetles (Tenebrio molitor L.). Journal of Insect Behavior 14:215-231.
11. Eady, P. E., N. Wilson, and M. Jackson. 2000. Copulating with multiple mates enhances female fecundity but not egg-to-adult survival in the bruchid beetle Callosobruchus maculatus. Evolution 54:2161-2165.
12. Emlen, D. J. 1994. Environmental control of horn length dimorphism in the beetle Onthophagus acuminatus (Coleoptera: Scarabaeidae). Proceedings of the Royal Society of London B, Biological Sciences 256:131-136.
13. _. 1997a. Alternative reproductive tactics and male dimorphism in the horned beetle Onthophagus acuminatus (Coleoptera: Scarabaeidae). Behavioral Ecology and Sociobiology 41:335-341.
14. _. 1997b. Diet alters male horn allometry in the beetle Onthophagus acuminatus (Coleoptera: Scarabidae). Proceedings of the Royal Society of London B, Biological Sciences 264:567-574.
15. Falconer, D. S., and T. F. C. Mackay. 1996. Introduction to quantitative genetics. Longman, Essex.
16. Fox, C. W. 1993a. The influence of maternal age and mating frequency on egg size and offspring performance in Callosobruchus maculatus (Coleoptera: Bruchidae). Oecologia (Berlin) 96:139-146.
17. _. 1993b. Multiple mating, lifetime fecundity and female mortality of the bruchid beetle, Callosobruchus maculatus (Coleoptera: Bruchidae). Functional Ecology 7:203-208.
18. Fox, C. W., L. A. McLennan, and T. A. Mousseau. 1995. Male body size affects female lifetime reproductive success in a seed beetle. Animal Behaviour 50:281-284.
19. Gil, D., J. Graves, N. Hazon, and A. Wells. 1999. Male attractiveness and differential testosterone investment in zebra finch eggs. Science (Washington, D.C.) 286: 126-128.
20. Hendrix, L. J., M. W. Carter, and D. T. Scott. 1982. Covariance analysis with heterogeneity of slopes in fixed models. Biometrics 38:641-650.
21. Houle, D. 1992. Comparing evolvability and variability of quantitative traits. Genetics 130:195-204.
22. Hunt, J., and L. W. Simmons. 1997. Patterns of fluctuating asymmetry in beetle horns: an experimental examination of the honest signalling hypothesis. Behavioral Ecology and Sociobiology 41:109-114.
23. _. 1998a. Patterns of fluctuating asymmetry in beetle horns: no evidence for reliable signalling. Behavioral Ecology 9:465-470.
24. _. 1998b. Patterns of parental provisioning covary with male morphologyin a horned beetle (Onthophagus taurus) (Coleoptera: Scarabidae). Behavioral Ecology and Sociobiology 42:447-451.
25. _. 2000. Maternal and paternal effects on offspring phenotype in the dung beetle Onthophagus taurus. Evolution 54:936-941.
26. _. 2001. Status-dependent selection in the dimorphic beetle Onthophagus taurus. Proceedings of the Royal Society of London B, Biological Sciences 268:2409-2414.
27. _. 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.
28. Hunt, J., L. W. Simmons, and J. S. Kotiaho. 2002. A cost of maternal care in the dung beetle Onthophagus taurus? Journal of Evolutionary Biology 15:57-64.
29. Kolm, N. 2001. Females produce larger eggs for large males in a paternal mouthbrooding fish. Proceedings of the Royal Society of London B, Biological Sciences 268: 2229-2234.
30. Kotiaho, J. S. 2000. Testing the assumptions of conditional handicap theory: costs and condition dependence of a sexually selected trait. Behavioral Ecology and Sociobiology 48:188-194.
31. Kotiaho, J. S., L. W. Simmons, and J. L. Tomkins. 2001. Towards a resolution of the lek paradox. Nature 410: 684-686.
32. Lynch, M., and B. Walsh. 1998. Genetics and analysis of quantitative traits. Sinauer, Sunderland, Mass.
33. Moczek, A. P., and D. J. Emlen. 2000. Male horn dimorphism in the scarab beetle Onthophagus taurus: do alternative reproductive tactics favor alternative phenotypes? Animal Behaviour 59:459-466.
34. Mousseau, T. A., and C. W. Fox. 1998. Maternal effects as adaptations. Oxford University Press, Oxford.
35. Nilsson, T., C. Fricke, and G. Arnqvist. 2002. Patterns of divergence in the effects of mating on female reproductive performance in flour beetles. Evolution 56: 111-120.
36. Nur, N., and O. Hasson. 1984. Phenotypic plasticity and the handicap principle. Journal of Theoretical Biology 110:275-297.
37. Petrie, M., and A. Williams. 1993. Peahens lay more eggs for peacocks with larger trains. Proceedings of the Royal Society of London B, Biological Sciences 251:127-131.
38. Pomiankowski, A., and A. P. Møller. 1995. A resolution of the lek paradox. Proceedings of the Royal Society of London B, Biological Sciences 260:21-29.
39. Qvarnström, A., and T. D. Price. 2001. Maternal effects, paternal effects and sexual selection. Trends in Ecology & Evolution 16:95-100.
40. Rauter, C. M., and A. J. Moore. 2002. Evolutionary importance of parental care performance, food resources and direct and indirect genetic effects in a burying beetle. Journal of Evolutionary Biology 15:407-417.
41. Reyer, H.-U., G. Frei, and C. Som. 1999. Cryptic female choice: frogs reduce clutch size when amplexed by undesired males. Proceedings of the Royal Society of London B, Biological Sciences 266:2101-2107.
42. Reznick, D. 1985. Cost of reproduction: an evaluation of the empirical evidence. Oikos 44:257-267.
43. Roff, D. 1997. Evolutionary quantitative genetics. Chapman & Hall, New York.
44. Rooney, J., and S. M. Lewis. 1999. Differential allocation of male-derived nutrients in two lampyrid beetles with contrasting life-history characteristics. Behavioral Ecology 10:97-104.
45. _. 2002. Fitness advantage from nuptial gifts in female fireflies. Ecological Entomology 27:373-377.
46. Rowe, L., and D. Houle. 1996. The lek paradox and the capture of genetic variance by condition dependent traits. Proceedings of the Royal Society of London B, Biological Sciences 263:1415-1421.
47. Sheldon, B. 2000. Differential allocation: tests, mechanisms and implications. Trends in Ecology & Evolution 15: 397-402.
48. Simmons, L. W. 2001. Sperm competition and its evolutionary consequences in the insects. Princeton University Press, Princeton, N.J.
49. Simmons, L. W., and J. S. Kotiaho. 2002. Evolution of ejaculates: patterns of phenotypic and genotypic variation and condition dependence in sperm competition traits. Evolution 56:1622-1631.
50. Simmons, L. W., J. L. Tomkins, and J. Hunt. 1999. Sperm competition games played by dimorphic male beetles. Proceedings of the Royal Society of London B, Biological Sciences 266:145-150.
51. Sowig, P. 1996. Duration and benefits of biparental brood care in the dung beetle Onthophagus vacca (Coleoptera: Scarabaeidae). Ecological Entomology 21:81-86.
52. Trivers, R. L. 1972. Parental investment and sexual selection. Pages 136-172 in B. Campbell, ed. Parental investment and sexual selection. Aldine-Atherton, Chicago.
53. Wedell, N. 1996. Mate quality affects reproductive effort in a paternally investing species. American Naturalist 148:1075-1088.
54. Williams, G. C. 1966. Natural selection, the costs of reproduction, and a refinement of Lack's principle. American Naturalist 100:687-690.
55. Wolf, J. B., E. D. Brodie III, J. M. Cheverud, A. J. Moore, and M. J. Wade. 1998. Evolutionary consequences of indirect genetic effects. Trends in Ecology & Evolution 13:64-69.