Sexual selection and senescence: Male size-dimorphic ungulates evolved relatively smaller molars than females

American Naturalist

Volumn 170, Issue 3, 2007, Pages 370-380

  Carranza, Juan ^a   Pérez Barbería, F Javier ^b  

^a UNIVERSITY OF EXTREMADURA   (Spain)

^b SCOTTISH CROP RESEARCH INSTITUTE   (United Kingdom)

Author keywords

Mammalian herbivores; Mating systems; Senescence; Sexual dimorphism; Sexual selection; Tooth wear

Indexed keywords

BODY MASS; BODY SIZE; DEER; EVOLUTIONARY THEORY; INTRASEXUAL INTERACTION; POLYGYNY; REPRODUCTIVE STRATEGY; SENESCENCE; SEXUAL DIMORPHISM; SEXUAL SELECTION; TOOTH;

AGING; ANIMAL; ARTICLE; BODY SIZE; EVOLUTION; FEMALE; GENETIC SELECTION; HISTOLOGY; MALE; MAMMAL; MOLAR TOOTH; PHYLOGENY; PHYSIOLOGY; SEXUAL DEVELOPMENT;

AGING; ANIMALS; BODY SIZE; EVOLUTION; FEMALE; MALE; MAMMALS; MOLAR; PHYLOGENY; SELECTION (GENETICS); SEX CHARACTERISTICS;

CERVUS ELAPHUS; MAMMALIA; UNGULATA;

EID: 34548175447     PISSN: 00030147     EISSN: None     Source Type: Journal    
DOI: 10.1086/519852     Document Type: Article

References (82)

1. Albon, S. D., B. Mitchell, and B. W. Staines. 1983. Fertility and body weight in female red deer: a density-dependent relationship. Journal of Animal Ecology 52:969-980.
2. Andersson, M. 1994. Sexual selection. Princeton University Press, Princeton, NJ.
3. Badyaev, A. V. 2002. Growing apart: an ontogenetic perspective on the evolution of sexual size dimorphism. Trends in Ecology & Evolution 17:369-378.
4. Bérubé, C. H., M. Festa-Bianchet, and J. T. Jorgenson. 1999. Individual differences, longevity and reproductive senescence in bighorn ewes. Ecology 80:2555-2565.
5. Blomberg, S. P., T. Garland Jr., and A. R. Ives. 2003. Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57:717-745.
6. Carranza, J., S. Alarcos, C. Sánchez-Prieto, J. Valencia, and C. Mateos. 2004. Disposable-soma senescence mediated by sexual selection in an ungulate. Nature 432:215-218.
7. Carranza, J., C. Mateos, S. Alarcos, C. Sánchez-Preito, and J. Valencia. Forthcoming. Sex-specific strategies of dentine depletion in red deer. Biological Journal of the Linnean Society.
8. Catchpole, E. A., B. J. T. Morgan, T. N. Coulson, S. N. Freeman, and S. D. Albon. 2000. Factors influencing Soay sheep survival. Journal of the Royal Statistical Society C 49:453-472.
9. Clutton-Brock, T. H., ed. 1988. Reproductive success: studies of individual variation in contrasting breeding systems. University of Chicago Press, Chicago.
10. Clutton-Brock, T. H., F. E. Guinness, and S. D. Albon. 1982. Red deer: behaviour and ecology of two sexes. Edinburgh University Press, Edinburgh.
11. Clutton-Brock, T. H., S. D. Albon, and F. E. Guinness. 1988. Reproductive success in male and female red deer. Pages 325-343 in T. H. Clutton-Brock, ed. Reproductive success: studies of individual variation in contrasting breeding systems. University of Chicago Press, Chicago.
12. Corbet, G. B., and J. E. Hill. 1986. A world list of mammalian species. British Museum (Natural History), London.
13. Darwin, C. 1871. The descent of man, and selection in relation to sex. Appleton, New York.
14. Ericsson, G., and K. Wallin. 2001. Age-specific moose (Alces alces) mortality in a predator-free environment: evidence for senescence in females. Ecoscience 8:157-163.
15. Ericsson, G., K. Wallin, J. P. Ball, and M. Broberg. 2001. Age-related reproductive effort and senescence in free-ranging moose Alces alces. Ecology 82:1613-1620.
16. Festa-Bianchet, M., M. Apollonio, F. Mari, and G. Rasola. 1990. Aggression among lekking male fallow deer (Dama dama): territory effects and relationship with copulatory success. Ethology 85:236-246.
17. Fortelius, M. 1985. Ungulate cheek teeth: developmental, functional, and evolutionary interrelations. Annales Zoologici Fennici 180:1-76.
18. Gaillard, J.-M., and N. G. Yoccoz. 2003. Temporal variation in survival of mammals: a case of environmental canalization? Ecology 84:3294-3306.
19. Gaillard, J.-M., D. Delorme, J.-M. Boutin, G. Van Laere, and R. Pradel. 1993. Roe deer survival patterns: a comparative analysis of contrasting populations. Journal of Animal Ecology 62:778-791.
20. Garland, T., Jr., and C. M. Janis. 1993. Does metatarsal femur ratio predict maximal running speed in cursorial mammals? Journal of Zoology (London) 229:133-151.
21. Garland, T., Jr., P. H. Harvey, and A. R. Ives. 1992. Procedures for the analysis of comparative data using phylogenetically independent contrasts. Systematic Biology 41:18-32.
22. Gatesy, J., G. Amato, E. Vrba, G. Schaller, and R. DeSalle. 1997. A cladistic analysis of mitochondrial ribosomal DNA from the Bovidae. Molecular Phylogenetics and Evolution 7:303-319.
23. Geist, V., and M. Bayer. 1988. Sexual dimorphism in the Cervidae and its relation to habitat. Journal of Zoology (London) 214:45-53.
24. GenStat. 2002. GenStat 6.1 reference manual. VSN International, Oxford.
25. Gentry, A. W. 1992. The subfamilies and tribes of the family Bovidae. Mammal Review 22:1-32.
26. Gentry, A. W., and J. J. Hooker. 1988. The phylogeny of the Artiodactyla. Pages 235-272 in M. J. Benton, ed. The phylogeny and classification of the tetrapods. Vol. 2. Mammals. Clarendon, Oxford.
27. Gosling, L. M., M. Petrie, and M. E. Rainy. 1987. Lekking in topi: a high-cost, specialist strategy. Animal Behaviour 35:616-618.
28. Grafen, A. 1989. The phylogenetic regression. Philosophical Transactions of the Royal Society B: Biological Sciences 326:119-157.
29. Hamilton, W. D. 1966. The moulding of senescence by natural selection. Journal of Theoretical Biology 12:12-45.
30. Harvey, P. H., and M. D. Pagel. 1991. The comparative method in evolutionary biology. Oxford University Press, Oxford.
31. Hillson, S. 1986. Teeth. Cambridge Manuals in Archaeology. Cambridge University Press, Cambridge.
32. Isaac, J. L. 2005. Potential causes and life-history consequences of sexual size dimorphism in mammals. Mammal Review 35:101-115.
33. Janis, C. M. 1982. Evolution of horns in ungulates: ecology and paleoecology. Biological Reviews 57:261-318.
34. Janis, C. M., and K. M. Scott. 1988. The phylogeny of the Ruminantia (Artiodactyla, Mammalia). Pages 273-282 in M. J. Benton, ed. The phylogeny and classification of the tetrapods. Vol. 2. Mammals. Clarendon, Oxford.
35. Jarman, P. J. 1974. The social organisation of antelope in relation to their ecology. Behaviour 48:215-267.
36. Jorgenson, J. T., M. Festa-Bjanchet, J.-M. Gaillard, and W. D. Wishart. 1997. Effects of age, sex, disease and density on survival of bighorn sheep. Ecology 78:1019-1032.
37. Kingdon, J. 1982. East African mammals: an atlas of evolution in Africa. Bovids. Academic Press, London.
38. Kirkwood, T. B. L. 1985. Comparative and evolutionary aspects of longevity. Pages 27-44 in C. E. Finch and E. L. Schneider, eds. Handbook of the biology of ageing. Van Nostrand Reinhold, New York.
39. Kirkwood, T. B. L., and S. N. Austad. 2000. Why do we age? Nature 408:233-238.
40. Kirkwood, T. B. L., and M. R. Rose. 1991. Evolution of senescence: late survival sacrificed for reproduction. Philosophical Transactions of the Royal Society B: Biological Sciences 332:5-24.
41. Komers, P. E., F. Messier, and C. C. Gates. 1994. Plasticity of reproductive behaviour in wood bison bulls: on risks and opportunities. Ethology Ecology and Evolution 6:485-495.
42. Lande, R. 1980. Sexual dimorphism, sexual selection, and adaptation in polygenic characters. Evolution 34:292-305.
43. Lande, R., and S. J. Arnold. 1985. Evolution of mating preference and sexual dimorphism. Journal of Theoretical Biology 117:651-664.
44. Loe, L. E., A. Mysterud, R. Langvatn, and N. C. Stenseth. 2003. Decelerating and sex-dependent tooth wear in Norwegian red deer. Oecologia (Berlin) 135:346-353.
45. Loison, A., M. Festa-Bianchet, J.-M. Gaillard, J. T. Jorgenson, and J. M. Jullien. 1999a. Age-specific survival in five populations of ungulates: evidence of senescence. Ecology 80:2539-2554.
46. Loison, A., J.-M. Gaillard, C. Pèlabon, and N. G. Yoccoz. 1999b. What factors shape sexual size dimorphism in ungulates? Evolutionary Ecology Research 1:611-633.
47. Lucas, P. W. 2004. Dental functional morphology. Cambridge University Press, Cambridge.
48. McArthur, C., and G. D. Sanson. 1988. Tooth wear in eastern grey kangaroos (Macropus giganteus) and western grey kangaroos (Macropus fuliginosus), and its potential influence on diet selection, digestion and population parameters. Journal of Zoology (London) 215:491-504.
49. McElligott, A. G., R. Altwegg, and T. J. Hayden. 2002. Age-specific survival and reproductive probabilities: evidence for senescence in male fallow deer (Dama dama). Proceedings of the Royal Society B: Biological Sciences 269:1129-1137.
50. Moore, S. L., and K. Wilson. 2002. Parasites as a viability cost of sexual selection in natural populations of mammals. Science 297:2015-2018.
51. Nowak, R. M. 1999. Walker's mammals of the world. Johns Hopkins University Press, Baltimore.
52. Owens, I. P. F. 2002. Sex differences in mortality rate. Science 297:2008-2009.
53. Owen-Smith, N. 1993. Comparative mortality rates of male and female kudus: the costs of sexual size dimorphism. Journal of Animal Ecology 6:428-440.
54. Pagel, M. D. 1992. A method for the analysis of comparative data. Journal of Theoretical Biology 156:431-442.
55. _. 1997. Inferring evolutionary processes from phylogenies. Zoologica Scripta 26:331-348.
56. _. 1999. Inferring the historical patterns of biological evolution. Nature 401:877-884.
57. Patterson, H. D., and R. Thompson. 1971. Recovery of interblock information when block sizes are unequal. Biometrika 58:545-554.
58. Pelletier, F., and M. Festa-Bianchet. 2004. Effects of body mass, age, dominance and parasite load on foraging time of bighorn rams, Ovis canadensis. Behavioral Ecology and Sociobiology 56:546-551.
59. Pemberton, J. M., S. D. Albon, F. E. Guinness, T. H. Clutton-Brock, and G. A. Dover. 1992. Behavioral estimates of male mating success tested by DNA fingerprinting in a polygynous mammal. Behavioral Ecology and Sociobiology 3:66-75.
60. Pemberton, J. M., D. W. Coltman, J. A. Smith, and D. R. Bancroft. 2004. Mating patterns and male breeding success. Pages 166-189 in T. H. Clutton-Brock and J. Pemberton, eds. Soay sheep dynamics and selection in an island population. Cambridge University Press, Cambridge.
61. Pérez-Barbería, F. J., and I. J. Gordon. 1998. Factors affecting food comminution during chewing in ruminants: a review. Biological Journal of the Linnean Society 63:233-256.
62. _. 2000. Differences in body mass and oral morphology between the sexes in the Artiodactyla: evolutionary relationships with sexual segregation. Evolutionary Ecology Research 2:667-684.
63. _. 2001. Relationships between oral morphology and feeding style in the Ungulata: a phylogenetically controlled evaluation. Proceedings of the Royal Society B: Biological Sciences 268:1023-1032.
64. _. 2005. Gregariousness increases brain size in ungulates. Oecologia (Berlin) 145:41-52.
65. Pérez-Barbería, F. J., I. J. Gordon, and M. Pagel. 2002. The origins of sexual dimorphism in body size in ungulates. Evolution 56:1276-1285.
66. Pérez-Barbería, F. J., D. A. Elston, I. J. Gordon, and A. W. Illius. 2004. The evolution of phylogenetic differences in the efficiency of digestion in ruminants. Proceedings of the Royal Society B: Biological Sciences 271:1081-1090.
67. Pond, K. R., W. C. Ellis, and D. E. Akin. 1984. Ingestive mastication and fragmentation of forages. Journal of Agricultural Science 58:1567-1574.
68. Poppi, D. P., B. W. Norton, D. J. Minson, and R. E. Hendricksen. 1980. The validity of the critical size theory for particles leaving the rumen. Journal of Agricultural Science 94:275-280.
69. Promislow, D. E. L. 1992. Costs of sexual selection in natural population of mammals. Proceedings of the Royal Society B: Biological Sciences 247:203-210.
70. Promislow, D. E. L., and P. H. Harvey. 1990. Living fast and dying young: a comparative analysis of life history variation among mammals. Journal of Zoology (London) 220:417-437.
71. Randi, E., N. Mucci, F. Claro-Hergueta, A. Bonnet, and E. J. P. Douzery. 2001. A mitochondrial DNA control region phylogeny of the Cervinae: speciation in Cervus and implications for conservation. Animal Conservation 4:1-11.
72. Reeve, J. P., and D. J. Fairbairn. 2001. Predicting the evolution of sexual size dimorphism. Journal of Evolutionary Biology 14:244-254.
73. Reiss, M. J. 1989. The allometry of growth and reproduction. Cambridge University Press, Cambridge.
74. Rose, M. R. 1984. Laboratory evolution of postponed senescence in Drosophila melanogaster. Evolution 38:1004-1010.
75. _. 1991. Evolutionary biology of aging. Oxford University Press, New York.
76. Skogland, T. 1988. Tooth wear by food limitation and its life history consequences in wild reindeer. Oikos 51:238-242.
77. Tyler, N. J. C. 1987. Natural limitation of the abundance of the high arctic Svalbard reindeer. PhD thesis. University of Cambridge.
78. Weladji, R. B., A. Mysterud, Ø. Holand, and D. Lenvik. 2002. Age-related reproductive effort in reindeer (Rangifer tarandus): evidence of senescence. Oecologia (Berlin) 131:79-82.
79. Williams, G. C. 1957. Pleiotropy, natural selection and the evolution of senescence. Evolution 11:398-411.
80. Wilson, K., B. T. Grenfell, J. G. Pilkington, H. E. G. Boyd, and F. M. D. Gulland. 2004. Parasites and their impact. Pages 113-165 in T. H. Clutton-Brock and J. Pemberton, eds. Soay sheep dynamics and selection in an island population. Cambridge University Press, Cambridge.
81. Yoccoz, N. G., A. Mysterud, R. Langvatn, and N. C. Stenseth. 2002. Age- and density-dependent reproductive effort in male red deer. Proceedings of the Royal Society B: Biological Sciences 269:1523-1528.
82. Zuk, M., and K. A. McKean. 1996. Sex differences in parasite infections: patterns and processes. International Journal for Parasitology 26:1009-1024.